murdoch research repository · 10.1016/j.meatsci.2010.04.042 this is a pdf file of an unedited...
TRANSCRIPT
MURDOCH RESEARCH REPOSITORY
This is the author’s final version of the work, as accepted for publication following peer review but without the publisher’s layout or pagination.
The definitive version is available at http://dx.doi.org/10.1016/j.meatsci.2010.04.042
Warner, R.D., Greenwood, P.L., Pethick, D.W. and Ferguson,
D.M. (2010) Genetic and environmental effects on meat quality. Meat Science, 86 (1). pp. 171-183.
http://researchrepository.murdoch.edu.au/3161/
Copyright: © 2010 The American Meat Science Association.
It is posted here for your personal use. No further distribution is permitted.
�������� ����� ��
Genetic and environmental effects on meat quality
R.D. Warner, P.L. Greenwood, D.W. Pethick, D.M. Ferguson
PII: S0309-1740(10)00177-4DOI: doi: 10.1016/j.meatsci.2010.04.042Reference: MESC 5083
To appear in: Meat Science
Received date: 24 February 2010Revised date: 28 April 2010Accepted date: 30 April 2010
Please cite this article as: Warner, R.D., Greenwood, P.L., Pethick, D.W. & Ferguson,D.M., Genetic and environmental effects on meat quality, Meat Science (2010), doi:10.1016/j.meatsci.2010.04.042
This is a PDF file of an unedited manuscript that has been accepted for publication.As a service to our customers we are providing this early version of the manuscript.The manuscript will undergo copyediting, typesetting, and review of the resulting proofbefore it is published in its final form. Please note that during the production processerrors may be discovered which could affect the content, and all legal disclaimers thatapply to the journal pertain.
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
1
Genetic and environmental effects on meat quality
R. D. Warner1*, P.L. Greenwood2, D.W. Pethick3 and D.M. Ferguson4
1 Department of Primary Industries, 600 Sneydes Rd, Werribee, 3030, Australia
2 Industry & Investment NSW, Beef Industry Centre of Excellence, University of
New England, Armidale NSW 2351, Australia
3 Department of Veterinary and Biomedical Sciences, Murdoch University, WA,
Australia
4 CSIRO Livestock Industries, FD McMaster Laboratory, Chiswick, Locked Bag 1
Armidale NSW 2350, Australia.
* Corresponding author. Telephone +61 3 97420477. Email address
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
2
ABSTRACT
In order for livestock industries to consistently produce high quality meat, there must
be an understanding of the factors that cause quality to vary, as well as the
contribution of genetics. A brief overview of meat tenderness is presented to
understand how genotype and environment may interact to influence this trait.
Essentially, meat tenderness is determined from the contribution of connective tissue,
sarcomere length determined pre-rigor and rate of proteolysis during ageing, as well
as contributions from intramuscular fat and post-mortem energy metabolism. The
influence of mutations in myostatin, the callipyge gene, the Carwell or ribe eye
muscle gene as well as the calpain system on meat tenderness is presented. Specific
examples of interactions between the production or processing environment and
genetics are presented for both sheep and cattle. The day-to-day variation in
tenderness is evident across experiments and this variation needs to be controlled in
order to consistently produce tender meat.
Keywords – genetics, environment, G×E, meat quality, stress, tenderness, consumer,
heritability, cattle, sheep
CONTENTS
1 Introduction ............................................................................................................ 3 2 Meat quality defined .............................................................................................. 6 3 A brief overview of meat tenderness ..................................................................... 7
3.1 Effects of sarcomere length ........................................................................... 8
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
3
3.2 Effects of proteolysis post-slaughter .............................................................. 9 3.3 Effects of connective tissue ......................................................................... 10 3.4 Effects of intramuscular fat (IMF) ............................................................... 11 3.5 Effects of glycogen metabolism ................................................................... 13 3.6 Interactions between factors ........................................................................ 14
4 Standardising pre- and post-slaughter conditions ................................................ 15 5 Specific gene or gene marker effects on beef and sheepmeat quality ................. 17
5.1 Calpain system gene markers for tenderness in cattle ................................. 18 5.2 Callipyge sheep ............................................................................................ 19 5.3 Carwell or Rib Eye Muscling (REM) gene in sheep ................................... 20 5.4 Mutations resulting in non-functional myostatin in cattle and sheep .......... 21
6 Partitioning of genetics and environmental effects on beef quality ..................... 24 6.1 Heritability estimates and genetic correlations for beef quality traits ......... 24 6.2 Production environment ............................................................................... 26 6.3 Post-slaughter environment ......................................................................... 29
7 Partitioning of genetics and environmental effects on sheepmeat quality ........... 31 7.1 Genetic effects ............................................................................................. 31 7.2 Production Environment .............................................................................. 34 7.3 Post-slaughter environment ......................................................................... 37
8 Summary and conclusions ................................................................................... 38
1 Introduction
The supply of meat which is wholesome, safe, nutritious, and of high quality to the
consumer will ensure continued consumption of meat. In affluent countries,
consumers are increasingly demanding meat products which are of high quality 100%
of the time. In order for livestock industries to consistently produce high quality meat,
there must be an understanding of the factors that cause quality to vary, and
implementation of management systems to minimise quality variation.
Beef and sheep meat quality are the primary subjects of this review, though reference
is made to evidence from pigs, where the results are considered applicable. There
have previously been reviews on the effect of genetics on meat quality of cattle
(Burrow, Moore, Johnston, Barendse & Bindon, 2001; Hocquette, Lehnert, Barendse,
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
4
Cassar-Malek & Picard, 2007; Lehnert, Wang, Tan & Reverter, 2006; Mullen,
Pannier & Hamill, 2009) and sheep (Bishop & Karamichou, 2009; Safari, Fogarty &
Gilmour, 2005; Warner, Pethick, Greenwood, Ponnampalam, Banks & Hopkins,
2007b). Obviously there are also reviews on the multitude of effects of environment
on meat quality. This review focuses on the relative contribution of genetics and
environment, and any interactions, in determining meat quality. Recent research is
discussed as well as specific genes known to influence meat quality in cattle and
sheep.
The environmental effects on meat quality are best defined as those not attributable to
genetics, and include on-farm, pre-slaughter, and post-slaughter processing factors.
Genetics is defined as heredity and a unit of heredity that occupies a specific locus on
a chromosome is defined as a gene; a sequence of bases on a DNA molecule (Stenesh,
1989). While there are many examples of single-gene-locus traits, current thinking in
biology discredits the notion that a small number of genes, and that genes alone, can
determine most complex traits. At the molecular level, DNA interacts with signals
from other genes and from the environment. At the level of individuals, particular
genes influence the development of a trait in the context of a particular environment.
Thus, measurements of the degree to which a trait is influenced by genes versus
environment will depend on the particular environment and genes examined.
It is recognised that environmental influences, eg. in utero nutrition, can have effects
beyond a single generation (Gluckman, Hanson & Beedle, 2007), which is the study
of epigenetics. In addition, mitochondrial DNA is transmitted exclusively through
dam lines and a mitochondrial maternal effect has been described (Burrow, 2001).
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
5
The effect has been defined as an effect of dam on offspring performance, additional
to the direct additive, maternal and permanent environmental contributions and may
have both a genetic and environmental origin (Burrow, 2001). Epigenetics and
maternal effects through mitochondrial DNA are potentially exciting new areas of
research but are beyond the scope of this review.
Intra- and inter-muscle variation in a trait also occurs thus the effect of genes on a trait
will depend on the muscle, and the location within a muscle, and should be defined as
such. Generally, muscles respond to their environment as they grow and develop, eg.
tension on a muscle, nerve supply, blood supply carrying nutrients and oxygen,
frequency of nerve stimulation, hormonal messages, etc. Thus a muscle develops
partly in response to its environment, as well as in response to its genes.
A phenotype can be simply described as the sum of the genetic and environmental
variation in a measured outcome (trait) such as tenderness or intramuscular fat.
Phenotype can also be described as a result of the interaction between genotype and
environment, in addition to variation not readily attributable to either (Peaston and
Whitelaw, 2006) Heritability is the proportion of phenotypic variation in a population
that is attributable to genetic variation among individuals.
Variation in a trait of interest can also be influenced by genetic-environment (G x E)
interactions where the expression of a genetic trait, or genotype, changes in response
to the environment. In our review of the literature, we found seven studies where
there was some evidence of a G x E interaction for meat quality traits and these are
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
6
presented in the relevant sections. This evidence indicates that G x E interactions may
be a relatively important contributor to the phenotypic variance in meat quality traits.
2 Meat quality defined
Meat quality is defined by those traits the consumer perceives as desirable which
includes both visual and sensory traits and credence traits of safety, health and more
intangible traits such as ‘clean’and green’ or welfare status of the production system
(Becker, 2000). Important visual traits include; colour and texture of the meat, fat
colour, amount and distribution of fat as well as the absence of excess water (purge)
in the tray (Glitsch, 2000). Once cooked, consumer satisfaction is largely determined
by how tender the meat is as well as its flavour/odour and juiciness (Glitsch, 2000).
Consumers of lamb in Australia usually place the highest weighting on flavour/odour,
followed by tenderness and lastly juiciness (Pethick, Pleasants, Gee, Hopkins & Ross,
2006). This is in contrast to consumers of beef who generally rate tenderness as the
most important palatability trait (Huffman, Miller, Hoover, Wu, Brittin & Ramsey,
1996; Robinson, Ferguson, Oddy, Perry & Thompson, 2001; Watson, Gee,
Polkinghorne & Porter, 2008) although this can vary with country (Glitsch, 2000).
Recent consumer data from Meat Standards Australia indicate that flavour has
increased in importance to beef consumers, most likely as a result of reducing the
variation in tenderness (Rod Polkinghorne, pers. comm.).
Over the last two decades in Australia, the genetic and environmental contributions to
the variation in beef and sheepmeat quality traits, particularly tenderness, have been
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
7
characterised and these will be discussed further within this review. The results from
large scale beef and lamb progeny evaluation programs in Australia show that despite
our knowledge, there is still considerable variation in meat tenderness which remains
unexplained. This review will focus primarily on meat tenderness simply because
quantification of the genetic and non-genetic variation in beef tenderness, and to a
limited extent sheep tenderness, has received more attention compared with the other
quality traits such as colour, flavour and water-holding capacity.
3 A brief overview of meat tenderness
A brief overview of meat tenderness is presented in order to understand how genotype
and environment may interact to influence this trait. Tenderness is an important meat
quality trait and the biological, structural and physiological mechanisms underlying
meat tenderness have been extensively investigated (Dransfield & Jones, 1980;
Harper, 1999; Koohmaraie, 1988; Tornberg, 1996). Essentially, meat tenderness is
determined by the amount and solubility of connective tissue, sarcomere shortening
during rigor development, and postmortem proteolysis of myofibrillar and
myofibrillar-associated proteins (Koohmaraie & Geesink, 2006). Intramuscular fat
also indirectly influences meat tenderness (Harper, 1999; Hocquette, Gondret, Baéza,
Médale, Jurie & Pethick, 2010; Nishimura, Hattori & Takahashi, 1999; Tornberg,
1996) as does the rate and extent of post-mortem energy metabolism (Thompson,
Perry, Daly, Gardner, Johnston and Pethick, 2006. These are discussed below.
Interactions occur between these factors which can be difficult to separate (Harper,
1999) and each of these is influenced to a greater or lesser degree by genotype and the
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
8
pre- or post-slaughter environment. Furthermore, each of these factors are generally
non-linear in their effect on meat tenderness, with continuing debate over the
importance of each factor, depending on the muscle, the species, the age of the animal
and the data available.
3.1 Effects of sarcomere length
Early work showed the pivotal effect of muscle sarcomere length on meat tenderness
(Marsh & Leet, 1966) and the phenomenon of cold-shortening has been extensively
discussed (Hwang, Devine & Hopkins, 2003). The effect of sarcomere length on
meat toughness was traditionally thought to be mediated through the increased
overlap of myofilaments (Dransfield & Rhodes, 1976) and that the toughness comes
from the myofibrillar structure (see Lepetit, Grajales & Favier, 2000). Rowe (1974)
observed that the angle that perimysium collagen fibres make with muscle fibres is
dependent on post-rigor sarcomere length. More recently, Lepetit et al. (2000)
showed that the amplitude of cold-shortening, and thus toughening, is dependent on
the muscle collagen content and the toughening is strongly influenced by the cooking
temperature.
Any one muscle will of course not have uniform sarcomere lengths throughout as
each muscle fibre goes into rigor at different times. At intermediate rates of
temperature decline, minimal shortening of sarcomeres occurs at rigor (Marsh,
Ringkob, Russell, Swartz & Pagel, 1987b; Pike, Ringkob, Beekman, Koh &
Gerthoffer, 1993). If the temperature decline is too rapid and glycolysis is slow, cold-
shortening occurs resulting in a profound increase in toughness (Marsh et al., 1987b;
Pike et al., 1993). If the temperature fall is too slow, and glycolysis is fast, rigor-
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
9
toughening can occur with associated tougher meat, due to a failure of the tenderising
processing during ageing (Dransfield, 1994; Marsh, Ringkob, Russell, Swartz &
Pagel, 1987a; Pike et al., 1993). Once rigor occurs, sarcomere length does not
generally change with ageing (Koohmaraie, Doumit & Wheeler, 1996). Thus the
normal pre-rigor restraint on muscles through tendons and attachments, which can be
increased through the post-slaughter application of tenderstretch (hanging by the aitch
bone), can minimise the degree of sarcomere shortening and associated toughening.
3.2 Effects of proteolysis post-slaughter
The proteolysis contribution to meat tenderness is predominantly regulated by the
protease levels in the muscle at slaughter, duration of post-rigor ageing and protease
activity during ageing (Koohmaraie et al., 2006). Sarcomere length at rigor also has
been shown to contribute to proteolysis post-slaughter through its effect on limiting
access of proteases to myofibrillar protein substrate in cold-shortened beef
semitendinosus (Weaver, Bowker & Gerrard, 2008).
The mechanism of post-mortem tenderisation has been described in detail by
Koohmaraie (1994), Taylor, Geesink, Thompson, Koohmaraie and Goll (1995) and
Tornberg (1996). The rate and extent of post mortem proteolysis by the calpain
system explains the majority of the observed improvement in tenderness with ageing
of meat (Koohmaraie, 1994; Taylor et al., 1995). The activity of these proteolytic
enzymes is also regulated by the rate of pH and temperature decline during rigor
development (Dransfield, 1994), ionic strength (Ouali, 1984), oxidation of calpain
post-slaughter (Rowe, Maddock, Lonergan & Huff-Lonergan, 2004) and possibly
other factors.
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
10
The effect of the calpain system on tenderisation post-slaughter relies on a balance
between the rate of activation and activity, and the rate of inactivation or denaturation
of the proteolytic enzymes (Dransfield, 1992; Dransfield, 1993; Dransfield, 1994;
Dransfield, Etherington & Taylor, 1992; Dransfield, Wakefield & Parkman, 1992).
The rate of activation and activity is reliant on the concentrations of calpain 1, calpain
II and their inhibitor, calpastatin at slaughter and the conditions at slaughter
(Koohmaraie, 1994). The inactivation of the calpain system through denaturation
occurs more rapidly when the pH-temperature conditions associated with rigor-
toughening occur (Dransfield, 1994).
3.3 Effects of connective tissue
The connective tissue contribution to meat tenderness is predominantly determined by
the development of heat-stable cross-links as well as the total collagen content, and
are predominantly established in the animal pre-slaughter (Harper, 1999) although
there is some influence post-slaughter through sarcomere length (Lepetit et al., 2000).
Connective tissue is an integral component of muscle that transmits contractive forces
from the myofibrils in the postnatal animal (McCormick, 1994). Connective tissue
consists primarily of an extracellular matrix and is the predominant component of
endomysium, perimysium and epimysium (Harper, 1999). Collagens are the major
protein constituents of perimysial connective tissue (Dransfield, 1977), and as an
animal matures, covalent cross-links between collagen fibrils become heat-stable and
these links significantly increase meat toughness (McCormick, 1994).
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
11
Simplistically, the cross-links determine the extent of tension generated during
heating and the residual adhesion between muscle fibers and hence, the greater the
number of cross-links, the tougher the meat (Bailey, 1985; Light, Champion, Voyle &
Bailey, 1985). It is therefore not the amount of collagen present, rather the degree of
structural linkage in collagen that determines its contribution to meat tenderness
(Bailey, 1985; Light et al., 1985). However as with all biology and meat science, there
are always cases that do not fit our understanding. In Japanese black cattle, Nishimura
et al. (1999) found that age-related increases in semitendinosus toughness were
unrelated to collagen solubility or total collagen.
Connective tissue that is present within the muscle is macroscopically unaffected by
slaughter per se, or by rigor mortis (Harper, 1999). It is generally considered that
connective tissue does not change or degrade post-slaughter although small post-
slaughter changes during tenderstretch hanging may contribute to increased
tenderness (Harper, 1999). As discussed above, sarcomere shortening influences the
perimysial collagen fibrils and Lepetit et al. (2000) has shown that at cooking
temperatures above 60oC, the increased toughness of cold-shortened meat is derived
from the myofibrillar as well as from the collagen components. The contribution of
perimysial collagen in shortened muscles to the measured toughness, depends on the
total collagen, the collagen thermal stability and on the cooking temperature.
3.4 Effects of intramuscular fat (IMF)
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
12
Marbling is defined as the intramuscular fat (IMF), or adipose tissue, deposited
between perimysium surrounding muscle bundles, and is visible to the human eye as
‘flecks’ or spots of fat. Marbling is a visual score given to a piece of meat whereas
IMF is the chemically measured fat content (includes membrane lipids) although the
terms are often used interchangeably. Early work from the USA showed that higher
levels of marbling were associated with improved palatability in cooked beef (McBee,
Jr. & Wiles, 1967; Smith, Savell, Cross, Carpenter, Murphey & Aalhus, 1987)
although generally marbling degree accounts for only 3-10% of the variation in
sensory tenderness of beef (Nishimura et al., 1999). There has been extensive debate
about the contribution that intramuscular fat makes to the sensory attributes of meat
(Hocquette et al., 2010; Oddy et al., 2001).
Hocquette et al. (2010) stated that IMF directly affects juiciness and flavour, but
tenderness was influenced indirectly. IMF appears to separate and dilute perimysial
collagen fibres and disorganize the structure of intramuscular connective tissue that
contributes to increased meat toughness (Hocquette et al., 2010). Nishimura et al.
(1999) found that in heavily marbled (>8% IMF) Japanese black cattle, the
perimysium is separated into thinner collagen fibrils.
In general, some IMF is important to palatability and at low IMF levels (<8%), this is
most likely primarily through improved juiciness and flavour. At high IMF levels
(>8%), disruption in the connective tissue in the perimysium appears to occur, which
influences the toughness deriving from the structure of the muscle.
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
13
3.5 Effects of glycogen metabolism
Post-mortem energy metabolism in muscle and in particular, glycolysis and rigor
onset, are important for determining sarcomere length (Thompson et al, 2006). The
pre-rigor metabolism and availability of substrate, combined with muscle temperature,
in any muscle in a carcass will determine the shortening occurring at rigor and thus
the post-rigor sarcomere length (Koohmaraie & Geesink, 2006). As discussed above,
cold-shortening and heat-toughening in muscles will influence the myofibrillar, the
connective tissue and also the proteolytic contributions to meat tenderness. Thus it is
evident that control of energy metabolism post-mortem is important for producing
tender meat.
Muscle metabolism pre-rigor in any muscle of a carcass can vary significantly with (i)
nutrition of the animal influencing pre-slaughter muscle glycogen levels (Knee,
Cummins, Walker, Kearney & Warner, 2007), (ii) pre-slaughter stress influencing
muscle metabolism at slaughter (Channon, Payne & Warner, 2000), (iii) muscle fibre
type (Thompson et al., 2006), (iii) post-slaughter electrical stimulation of the carcass
(Simmons, Daly, Mudford, Richards, Jarvis & Pleiter, 2006), (iv) genetics (Warner et
al., 2006; Martin, Gardner, Thompson & Hopkins, 2006; Gardner, Kennedy, Milton &
Pethick, 1998) as well as through unidentified causes. In theory, effective control of
post-mortem pH and temperature decline can provide precise management of meat
quality outcomes (Simmons et al., 2006) as well as allowing more precise
measurement of heritability of traits of interest and variation between genotypes and
breeds. In practice, this can be difficult to achieve under commercial conditions and
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
14
variable responses are usually due to animal history rather than processing conditions
(Simmons et al., 2006).
Meat tenderness varies not only with the rate of glycolysis and rigor onset post-
slaughter, but also with the extent of glycolysis, classically identified through the
ultimate pH (pHu) achieved in a muscle. The relationship between meat pHu and
tenderness is quadratic, with a peak in toughness at pHu 6.1 (Purchas &
Aungsupakorn, 1993). The improved tenderness as ultimate pH increases above 6.1
appears to be largely attributable to improvements in water-holding capacity and
consequent decreases in cooking losses, and to the greater activity of proteases at pH
values close to neutrality (Yu & Lee, 1986). The reasons for beef becoming tougher
with intermediate elevations in pH to around 6.1 appear to be due to reduced
sarcomere length (Purchas et al., 1993).
3.6 Interactions between factors
As previously stated, the extent of myofibrillar shortening has a profound effect on
initial tenderness. However, shortening can also influence aged meat tenderness as
proteolysis will occur more slowly in meat with shortened sarcomeres for two
reasons. Firstly, because rigor onset occurs at a later stage, ageing occurs more slowly
due to the low initial temperatures in the muscle delaying activation of the calpains
(Dransfield, 1994). The second reason is because of limited access of the proteases to
the protein substrate within the sarcomeric structure, as shown by Weaver et al.
(2008).
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
15
In muscles which have undergone some shortening due to high rigor temperatures,
there is both rapid activation and inactivation of the proteases with a net reduction in
tenderisation (Dransfield, 1994). Structure and function of muscle determine
phenotype and therefore influence gene expression and metabolic profile.
Interrelationships between structure and function make it difficult to establish cause
and effect between any particular structural feature and a gross phenotype such as
meat toughness (Harper, 1999).
4 Standardising pre- and post-slaughter conditions
Even under controlled pre- and post-slaughter management protocols there is still
unexplained variation in traits like tenderness associated with the day, abattoir and
year the animals were slaughtered, as shown in pigs (Purslow et al., 2008), cattle
(Johnston, Reverter, Robinson & Ferguson, 2001) and sheep (Purchas, Sobrinho,
Garrick & Lowe, 2002).
Robinson et al. (2001) showed that strict protocols should be used to control pre- and
post-slaughter management in order to reduce the variation in tenderness
measurements of the longissimus and semintendinosus muscles from 3,440 Bos
indicus beef carcasses. Subsequent to the work by Robinson et al. (2001), Burrow et
al. (2001) suggested that alternative methods of hanging of carcasses, such as
tenderstretch, may reduce the amount of variation in shear force values observed.
Wolcott, Johnston, Barwick, Iker, Thompson & Burrow (2009) compared
tenderstretch and achilles hanging, within a beef carcasses, using 290 temperate and
290 tropical composite breeds to test the change in variation. The longissimus shear
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
16
force of tropical composite cattle was on average 7.4 Newtons tougher then the
longissimus of temperate breeds with a similar reduction in shear force due to
tenderstretch (8.2 N), for both breeds (Wolcott et al., 2009),.
Despite efforts to standardise the effects of electrical stimulation and chilling rate on
the temperature and pH fall post-slaughter, wide variation is often found between
animals, abattoirs and also slaughter dates within abattoirs (Thompson, Hopkins,
D'Souza, Walker, Baud & Pethick, 2005). This can be due to variation in electrode
contact with the carcass, electrical resistance within the carcass and variation in wave
form, current and frequency. But even with these standardised, the muscle metabolic
response to electrical stimulation, as measured by muscle pH, can vary widely,
depending on the metabolic state of the animal at slaughter. For example, Warner,
Bond & Kerr (2000) reported that the muscle pH of lambs undergoing exercise pre-
slaughter shows no response to post-slaughter electrical stimulation whereas the
muscle pH of lambs un-exercised pre-slaughter drops by 0.5 pH units. Similarly in a
mob of 70 cattle, the range in muscle pH drop in response to electrical stimulation
was 0 (no change) to 0.8 pH units (drop from 6.6 to 5.8) (R. Warner, unpublished
results). In addition, other electrical inputs such as at the immobiliser and hide puller,
can contribute significant variation in muscle pH fall between beef carcasses.
Features of the animal’s pre-slaughter experience, including acute stress and physical
activity, have been shown to influence markedly the toughness of beef (Warner,
Ferguson, Cottrell & Knee, 2007a; Gruber, Tatum, Engle, Chapman, Belk & Smith,
2009) and lamb (Warner, Ferguson, McDonagh, Channon, Cottrell & Dunshea,
2005a) through mechanisms that are not well-understood. A farm animal which has
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
17
had a poor handling experience on the farm, may respond adversely to handling
experiences between farm and slaughter, resulting in inferior meat quality (eg. in pigs;
D'Souza, Warner, Dunshea & Leury, 1998). Warner, Dunshea, Ponnampalam &
Cottrell (2005b) hypothesised that the release of nitric oxide during stress activates
the calpain system and causes the increased toughness.
The origins for a day of slaughter, abattoir and animal effect on meat tenderness are
not fully understood. Some factors that may contribute include variation; between
animals in stress susceptibility and temperament, in handling and handlers at the
abattoir, in stress during transport and loading/unloading, in inclement weather
influencing the animals’ behaviour and variation in application of electrical
stimulation as well as the carcass response to stimulation.
5 Specific gene or gene marker effects on beef and
sheepmeat quality
Although many meat quality traits have generally been assumed to be under the
control of multiple genes, there is considerable evidence that single genes account for
a relatively large amount of variation for some traits (Burrow et al., 2001).
Gene markers for tenderness targeting expression of the calpain proteolytic system
have been developed (Barendse, 2002; Barendse, Harrison, Bunch & Thomas, 2008;
Page et al., 2002; White et al., 2005). The Carwell gene is another that has been
characterised for its effects on tenderness and rib eye (loin) muscling in sheep (Nicoll
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
18
et al., 1998; Jopson et al., 2001). The callipyge gene in sheep (Cockett et al., 1993)
and the double muscling gene in cattle (Arthur, 1995) have very large affects on
carcass attributes but the specific causes of altered expression of carcass traits,
chromsomal sites of mutations, and effects on meat tenderness differ substantially.
This is discussed below.
5.1 Calpain system gene markers for tenderness in cattle
Gene markers have been used to identify cattle with better performance for
commercial traits including meat tenderness (Barendse, 2002; Barendse et al., 2008;
Page et al., 2002; White et al., 2005). Markers for tenderness have been identified and
these markers are known to influence the expression of the calpain-calpastatin enzyme
complex that regulates the rate of protein degradation in the live animal and post-
mortem muscle (Koohmaraie, Kent, Shackelford, Veiseth & Wheeler, 2002).
The associations between these tenderness markers and meat quality traits were
quantified within two concurrent experiments using 377 Brahman (Bos indicus) cattle
at two different locations (Cafe, McIntyre, Robinson, Geesink, Barendse &
Greenwood, 2010a; Cafe et al., 2010b). Cattle were selected for the study from
industry and research herds at weaning based on their genotype for Calpastatin
(CAST, CAST:c.2832A>G: Barendse, 2002) and Calpain 3 (CAPN3,
APN3:c.1538+225G>T: Barendse et al., 2008) gene markers and the gene marker
status for µ-calpain (CAPN1-316, CAPN1:c.947C>G: Page et al., 2002) was also
identified. Each marker is for a single nucleotide polymorphisms (SNP) within genes
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
19
controlling the calpain proteolytic system. The alleles differ in their effects on meat
tenderness, with the favorable allele being associated with more tender meat.
In these studies, the gene markers had significant effects on shear force in the
longissimus of Brahman cattle, but few effects on other meat quality traits (Cafe et al.,
2010b, Table 1). Cattle with the favorable genotype for the three markers had reduced
shear force compared to those with the unfavorable genotypes. The combined effects
of the favorable marker alleles resulted in a 15.8 N reduction in shear force following
7 d aging (Table 1). Although the size of the effect of individual markers varied with
experimental site, muscle, method of carcass suspension and aging period, there were
no interactions (Cafe et al., 2010a,b). The results of Cafe et al. (2010a,b) are
important as they provide evidence of few adverse effects due to the calpain system
gene markers on production, carcass and beef quality related characteristics.
5.2 Callipyge sheep
The Callipyge sheep phenotype results from a mutation on chromosome 18 when
present in heterozygous offspring that inherit the mutation from their sire (Cockett et
al., 1994, 1996; Jackson, Green & Miller, 1997a; Freking et al., 1998a). They have
extreme muscling, particularly in the hindquarters, reduced fatness and improved feed
efficiency, but have extremely tough meat (Freking, Keele, Nielson & Leymaster,
1998b; Freking, Smith & Leymaster, 2004; Jackson et al., 1997a; Jackson, Miller and
Green, 1997b,c; Koohmaraie, Shackelford, Wheeler, Lonergan & Doumit, 1995). In
Callipyge sheep, increased myofibre size is due to a greater proportion and size of
type 2X/2B (fast glycolytic) muscle fibres and a reduction in the percentages of type
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
20
2A (fast oxidative-glycolytic) and 1 (slow oxidative) myofibres present (Koohmaraie
et al., 1995; Carpenter, Owen, Cockett & Snowder, 1996; Lorenzen et al., 2000). The
muscle of Callipyge sheep has increased calpastatin (Geesink & Koohmaraie, 1999;
Duckett, Snowder & Cockett, 2000), reduced breaks in the I-band region during post
mortem aging (Taylor & Koohmaraie, 1998) and no change in collagen cross-linking
(Field, McCormick, Brown, Hinds & Snowder, 1996) compared to normal sheep,
hence the myofibrillar rather than the connective tissue component is primarily
responsible for the markedly increased toughness. Efforts to improve the tenderness
and consumer acceptability of meat from Callipyge lambs have included electrical
stimulation, prolonged aging, freezing prior to aging, injection of calcium chloride,
the Hydrodyne® process, and different cooking methods, with variable degrees of
success (Carpenter & Solomon, 1995; Solomon, Long, Eastridge & Carpenter, 1995;
Clare, Jackson, Miller, Elliot & Ramsey, 1997; Shackelford, Wheeler & Koohmaraie,
1997, 1998; Duckett, Klein, Dodson & Snowder, 1998).
5.3 Carwell or Rib Eye Muscling (REM) gene in sheep
It has emerged that certain Australian Poll Dorset sires produce offspring with
increased longissimus cross-sectional area and mass at equivalent live or carcass
weights (Barendse, 1995; Banks, 1997; Nicoll et al., 1998; Greenwood, Davis, Gaunt
& Ferrier, 2006a). This is apparently due to segregation at a locus on chromosome 18
known as the rib-eye muscling (REM) or Carwell locus (Nicoll et al., 1998; Jopson et
al., 2001). This locus maps in close proximity to the Callipyge locus (see Section on
Callipyge), however no published data is available concerning the precise
chromosomal position of the sequence variant responsible. Association analysis has
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
21
been performed in half-sib progeny derived from Poll Dorset and White Faced
Suffolk sires which demonstrated heterozygosity for DNA markers linked to the
Carwell mutation (Kijas et al., data unpublished). Significant effects were detected for
increased loin weight, as well as for muscling and leanness (CT scan measurements),
however the magnitude of the effects were generally small (Kijas, personal
communication). The Carwell phenotype may have inferior eating quality due to
increased toughness (Cummins, 1997; Davis, Ferrier & Gaunt, 1999; Jopson et al.,
2001; Hopkins & Fogarty, 1998), although this effect appears to be small and variable
compared to that in Callipyge lambs.
Clearly, the development and application of markers for this and other alleles
associated with increased muscling within the Australian sheep population will need
to ensure that the increase in sheep meat yield does not come at the expense of
sheepmeat quality characteristics including tenderness.
5.4 Mutations resulting in non-functional myostatin in cattle and sheep
The most extreme effects of specific genes on muscle characteristics are those
associated with double muscled cattle and the Callipyge sheep phenotypes. Although
mutations for these genes result in increased muscularity, their chromosomal sites,
specific causes and effects differ substantially, as summarised in Table 2.
The high degree of muscling that is evident in some European breeds of cattle (eg.
Belgian Blue and Piedmontese) is in some cases associated with mutations in the gene
regulating myostatin (Bellinge, Liberles, Iaschi, O’Brien & Kay, 2004). Mutations in
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
22
the myostatin gene (MSTN, also known as growth differentiation factor 8, GDF8)
have been documented to alter muscling and muscle structure in cattle (Lines,
Pitchford, Kruk & Bottema, 2009). If the gene is inactivated through the mutations,
the protein is non-functional, causing the ‘double muscled’ phenomenon (Joulia-
Ekaza & Cabello, 2006). The most common mutation is caused by an 11 base pair
deletion (del 11) at base 821, evident within the Belgian Blue breed (Switonski,
2002). Animals can be homozygous positive for the mutation, and exhibit extreme
muscling, or heterozygote for the mutation, expressing muscling intermediate between
the homozygous positive and the wild-type. In Belgian Blue, the mutation has been
associated with significant reductions in the shear force and a decrease in total
collagen content (Ngapo, Berge, Culioli, Dransfield, De Smet & Claeys, 2002).
Within the Limousin cattle population, a gene variant of myostatin, F94L, which
increases muscle mass also results in meat which is more tender, through a reduction
in the collagen/elastin content of muscle (Lines et al., 2009). The mechanism for this
gene variant is not known.
A study investigating the benefits of incorporating single MSTN loss-of-function
alleles into breeding programmes to improve muscularity was conducted in two
Australian beef cattle herds of Angus origin (O’Rourke et al., 2009). Both the
research and commercial herds had Low and High muscling lines which were
homozygous for ‘normal’ (also called wild-type) myostatin and a High muscling line
which was heterozygous for the 821 del11 myostatin allele that results in non-
functional myostatin. There were no differences due to genotype for shear force or
compression in longissimus samples from both herds (O’Rourke et al., 2009) (Table
3). A reduction in shear force for the m. semitendinosus samples was evident due to
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
23
genotype in the commercial herd, but not in the research herd. Tatum, Gronewald,
Seideman & Lamm (1990) and Wheeler, Shackelford, Casas, Cundiff and
Koohmaraie (2001) found increased tenderness in Piedmontese which were
heterozygous for the 821 del11 myostatin allele and similar findings were found in
Charolais heterozygotes (Levéziel et al., 2006; Casas et al., 1998). However, Gill,
Bishop, McCorquodale, Williams and Wiener (2009) did not find significant effects
of heterozygosity on tenderness.
A mutation (g+6723G>A) in the myostatin gene (GDF8) that causes translational
inhibition has been shown to result in increased muscling in Texel and other sheep
(Laville et al., 2004; Clop et al., 2006; Kijas, McColloch, Hocking Edwards, Oddy,
Lee & van de Werf, 2007), and other mutations in the sheep myostatin gene have also
been identified that influence muscling and fatness (Kijas et al., 2007). The
g+6723G>A mutation increased the percentage of fast glycolytic myofibres (Laville
et al., 2004), but did not affect shear force (Kijas et al., 2007). However, it did reduce
intramuscular fat and reduce sensory scores for eating quality including tenderness
(Kijas et al., 2007). In another study, objective meat quality traits including
longissimus and semimembranosus shear force were not affected by a QTL
encompassing GDF8, which influences carcass composition in Texel sheep (Johnson,
McEwan, Dodds, Purchas & Blair, 2005).
In general, mutations in the myostatin gene in cattle often, but not always, result in
improved tenderness which has been attributed to a decrease in the amount of
collagen in muscle relative to myofibres (Boccard, 1982; Uytterhaegen et al. 1994)
and in the amount of stable non-reducible cross links (Bailey, Enser, Dransfield,
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
24
Restall, and Avery, 1982). Mutations in the myostatin gene in sheep appear to have
no influence on shear force, although there may be a reduction in consumer
perception of tenderness, perhaps due to intramuscular fat-related effects.
6 Partitioning of genetics and environmental effects on beef
quality
6.1 Heritability estimates and genetic correlations for beef quality traits
In their extensive reviews of genetic parameters for beef quality traits, Marshall
(1999) and Burrow et al. (2001) reported that objective tenderness measures (shear
force) and intramuscular fat percentage were moderately heritable (h2 0.2 - 0.3) whilst
objective (reflectance; L, a* and b* values) and subjective assessments of meat colour
and water holding traits (drip loss, cooking loss percentage) were less heritable (h2 0.1
- 0.25). For consumer panel scores of tenderness, juiciness and flavour, the average
heritability was also low ranging from 0.05 – 0.2 with panel tenderness score being
the highest at 0.22 (Marshall, 1999; Burrow et al., 2001). From this we can conclude
that of the total phenotypic variance in beef quality traits, genetics accounts for 5 –
30%, depending on the trait. Secondly, given the low to moderate heritability for the
traits, the opportunity for genetic improvement is somewhat limited but would appear
best for traits such as tenderness and intramuscular fat percentage. With respect to
tenderness, this opportunity is greater however for Bos indicus or tropically adapted
breeds given the higher heritability (longissimus shear force h2 = 0.30; consumer
panel tenderness score h2 = 0.31) and phenotypic variance compared to Bos taurus
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
25
breeds (shear force h2 = 0.09; consumer panel tenderness score h2 = 0.1) (Johnston,
Reverter, Ferguson, Thompson & Burrow, 2003).
There is a genetic correlation between IMF and tenderness in beef carcasses. For
temperate breeds of cattle, the genetic correlation between IMF and consumer panel
tenderness or shear force is 0.61 and -0.38 respectively (Reverter et al., 2003a). As the
genetic correlation between consumer tenderness and consumer flavour or juiciness is
high (0.93 and 1.0 respectively) (Johnston et al., 2003a), this suggests the correlation
between IMF and consumer panel tenderness is most likely driven by palatability
traits other then tenderness. IMF can be measured on the live animal thus selection for
IMF in vivo will also result in some genetic improvement in shear force. Preliminary
data from the meat of lambs in the sheep Co-operative Research Centre (CRC) in
Australia suggest that the genetic correlation between shear force and IMF is also high
(Sue Mortimer, pers. comm.).
Whilst the phenotypic relationship between temperament and tenderness is low
(Burrow, Seifert & Corbet, 1988; Colditz, Ferguson, Greenwood, Doogan, Petherick
& Kilgour, 2007; Kadel, Johnston, Burrow, Graser & Ferguson, 2006; King et al.,
2006), the same cannot be said for the genetic correlation (rg = 0.3–0.4) between
these two traits in cattle (Kadel et al., 2006; Reverter, Johnston, Perry, Goddard &
Burrow, 2003b). The mechanism is not clear but certainly this data together with data
from Warner et al. (2007a), Gruber et al. (2009) and Voisinet, Grandin, O'Connor,
Tatum and Deesing (1997) suggests that stress has a significant and negative effect on
meat tenderness, when measured by shear force or consume panel. The most likely
causative mechanism is through effects on the proteolytic system, as proposed by
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
26
Warner et al. (2005b), but it is also possible that another unknown mechanism is
involved.
6.2 Production environment
Cattle are grown and finished in a range of different production environments. Under
extensive pasture-based environments, diet composition and feed availability can vary
considerably resulting in variable rates and patterns of growth and changes in energy
metabolism and body composition which in turn, can directly and indirectly affect
beef quality. The impact of nutrition on muscle properties and product quality has
been extensively reviewed by Oddy et al. (2001) and Hocquette et al. (2007). The
focus of the following section is to examine the interaction between animal genetics
and the production environment.
In a large beef cattle genetic evaluation study, progeny (n = 7,781) from the same
sires from either temperate or tropically adapted breeds were grown to three slaughter
weights (220, 280 and 340 kg carcass weight) in both pasture and feedlot finishing
systems. The design and experimental protocols have been described in detail by
Upton, Burrow, Dundon, Robinson & Farrell (2001) and Perry, Shorthose, Ferguson
& Thompson (2001). Pasture finished cattle had significantly darker (lower L*
values) and tougher (higher shear force values and lower consumer tenderness scores)
meat and had less intramuscular fat than those finished in the feedlot (Reverter et al.,
2003a; Johnston et al., 2003). The effect of slaughter weight and hence slaughter age
on tenderness and meat colour measurements was less consistent and surprisingly
smaller in magnitude, compared to the effect of finishing system. Cattle finished at
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
27
heavier slaughter weights had higher intramuscular fat percentage and visual marbling
scores (Reverter et al., 2003a).
The genetic correlations between traits at different slaughter weights or between
pasture and feedlot finished cattle were generally high (>0.7) and close to unity for
most meat quality measures including longissimus shear force and intramuscular fat
%. These results do not lend support for G x E interactions as the ranking between
sires was not influenced by the weight at slaughter or whether progeny were finished
on pasture or in the feedlot.
Using a subset of this data, Johnston et al. (2001) published an earlier study
examining the sources of variation in longissimus shear force. After the additive
variance (genetic component), slaughter group was the second largest source of
explained variance in shear force accounting for 17.8% of the total phenotypic
variance (Table 4). Slaughter group was defined as all animals run together from
intake (year, season and sex), finishing system, slaughter weight and slaughter date.
Importantly, the partitioning of the slaughter group variance revealed that slaughter
weight and finishing system only accounted for the 1.4% of the total phenotypic
variance. This reinforces the point that when the post-slaughter conditions are
controlled, the contributions of these production factors to the variation in tenderness
are relatively low. Finally, slaughter date which also encapsulates differences between
abattoirs accounted for the majority (15.3%) of the slaughter group effect. This
highlights that there are other unidentified animal and/or environmental factors that
contribute to the variation in tenderness. Efforts to better understand, characterise and
control these may yield further improvements in this highly important consumer trait.
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
28
Effect of growth path on beef tenderness - The extent to which nutrition and growth
path affect beef tenderness and other production traits has been investigated in various
large-scale, long-term studies within the Beef CRC in Australia. In general, the closer
the nutritional perturbation to slaughter, the greater the potential to impact on beef
quality and in particular beef tenderness (Table 5). From this, it was concluded that
finishing systems can have significant effects on tenderness, whereas growth and
nutrition earlier in life have minimal or no impact. It is also notable that genotype ×
nutritional (environmental) interactions were not evident within the Beef CRC studies
(Table 5).
Rapid growth of cattle at pasture over the entire post-weaning period to the same
market weight or to feedlot entry may or may not improve beef tenderness (Perry &
Thompson, 2005; McKiernan & Wilkins, 2007; Table 5), and any improvements are
not consistent across breed types, geographic locations, and muscles (Perry et al.,
2005). In this regard, while beef eating quality characteristics decline with age (Perry
et al., 2005), serious adverse affects of backgrounding growth (also called ‘grow-out’
period, and corresponds to the post-weaning, pre-finishing period) on beef tenderness
are only likely to be evident if retarded growth results in animals being substantially
older when they reach the same market weight, by about 9 months, for example
Purchas, Burnham & Morris (2002).
More rapid growth of cattle during finishing or use of feedlot compared to pasture
finishing (Table 5) generally improves meat tenderness (Johnston et al., 2003; Perry et
al., 2005), although not always depending upon factors such as prior nutrition and the
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
29
duration of concentrate feeding (Troy, Murray, O’Sullivan, Mooney, Moloney &
Kerry, 2002).
6.3 Post-slaughter environment
A key point to highlight here is that unlike some beef quality traits such as
intramuscular fat percentage, the tenderness phenotype is not fixed at slaughter and
can be significantly affected by the post-slaughter processing conditions that prevail
during the first 24 h after slaughter and duration of ageing. Failure to control the post-
slaughter processing conditions may allow cold shortening or heat-toughening to
occur, particularly under rapid chilling regimens for the former. This of course can be
avoided through the application of effective electrical stimulation which accelerates
the rate of post-mortem glycolysis. As discussed above, cold shortening results in
profound changes to the phenotypic variance in tenderness. However it can also
influence the estimate of heritability for shear force as demonstrated by Johnston et al.
(2001). They showed that the exclusion of only three slaughter groups (n = 173)
where electrical stimulation was not applied, from the full dataset (n = 2661), resulted
in a 33% reduction in the phenotypic variance and an increase in the longissimus
shear force heritability from 0.19 to 0.31.
Another post-slaughter strategy to minimise cold shortening is tenderstretch. Wolcott
et al. (2009) conducted a study on 2180 Brahman and tropical composite feedlot
steers where one side was tenderstretched and the other hung normally via the
Achilles tendon. They showed that tenderstretch reduced the average shear force by
8.2 Newtons, for both breeds. The genetic and phenotypic variance for both breeds
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
30
was substantially reduced by tenderstretch, but importantly, the heritability was
essentially unchanged (h2= 0.32-0.33 for Achilles hung, h2 = 0.30 for tenderstretch
(standard errors were the same for Achilles hung and tenderstretch) (Wolcott et al.,
2009). Moreover, the genetic correlation between shear force measures in the
tenderstretched and Achilles hung sides was quite high (rg = 0.77 ± 0.11).
Collectively, these results indicate that the genetic or sire variance in shear force may
not be underpinned by differences in the mechanisms regulating post-mortem
myofibrillar contraction. Wolcott et al. (2009) also reported that the genetic
correlations between the difference in shear force (∆SF) due to hanging method (∆SF
= Achilles hung SF – tenderstretch SF) and Achilles hung SF and tenderstretch SF
were 0.92 ± 0.03 and 0.49 ± 0.19, respectively. This difference in the magnitude of
the rg is quite salient as it is suggestive of a small G x E interaction.
As discussed above, the rate and extent of post-mortem proteolysis also governs the
expression of tenderness. In two separate studies, the estimated heritability for beef
longissimus shear force varied with the duration of ageing (Figure 1) (O'Connor,
Tatum, Wulf, Green & Smith, 1997; Wulf, Tatum, Green, Morgan, Golden & Smith,
1996). Contrasting results between the studies were reported with respect to the
interaction between breed or sire within breed and ageing duration. Wulf et al. (1996)
found minimal re-ranking of sires for tenderness throughout the 1 – 35 days of ageing.
In contrast, O’Connor et al. (1997) found a significant breed x ageing interaction
where a more rapid rate of ageing (ie. tenderisation) was evident in Bos taurus
compared with Bos indicus composites. The reduced proteolytic potential and
therefore tougher meat in Bos indicus relative to Bos taurus cattle is reasonably well
documented (e.g Shackelford Koohmaraie, Miller, Crouse & Reagan, 1991; Wheeler,
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
31
Savell, Cross, Lunt & Smith, 1990) but the breed difference in tenderness can be
partially reduced through electrical stimulation (Ferguson, Jiang, Hearnshaw, Rymill
& Thompson, 2000).
In a study of 273 Limousin x Jersey steers and heifers where the post-mortem
conditions were very tightly controlled and rigor development and subsequent ageing
occurred at a constant temperature of 15oC, Daly (2000) reported a 17 kg (New
Zealand tenderometer measurements) difference in longissimus shear force between
animals at rigor and a 10 fold difference between animals in the rate of post-mortem
tenderisation. Notwithstanding the contributions to meat tenderness from other
structural variants (eg. myofibrillar shortening, connective tissue), the mechanisms
that underpin the variation in post-mortem proteolytic rate are probably the primary
contributors to the genetic variation in tenderness.
7 Partitioning of genetics and environmental effects on
sheepmeat quality
This subject has received much less research attention in sheep relative to cattle
although a large scale progeny evaluation project has recently commenced in
Australia.
7.1 Genetic effects
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
32
Most published information on genetic variation in sheep meat quality is from inter-
breed comparisons (Bishop et al., 2009) and there is a paucity of within breed genetic
estimates for sheep meat quality traits. For example, in the review by Safari et al.
(2005) of genetic parameter estimates for animal and quality traits in sheep, they only
found published estimates for the heritability of meat pH and colour (0.18 and 0.09,
respectively). However, new evidence is emerging as the heritabilities for tenderness
traits have been investigated in two recent studies. Karamichou, Richardson, Nute,
Wood and Bishop (2007) reported the heritability estimates of 0.15 for trained sensory
panel score and 0.39 for shear force in Scottish Blackface sheep (n=350). Preliminary
results of Mortimer et al. (2009) indicate a moderate heritability for shear force for
2,200 lambs with linked sires in seven flocks across Australia. More recent results
(Warner, unpublished results) indicate that the heritability of shear force after 5 days
ageing is 0.39, across 7 flocks, 90 sires and 2,500 progeny. This large study is
ongoing and it aims to generate phenotype data on at least 10,000 lamb progeny
across 7 flocks from four regions in Australia. This study will provide definitive
answers for the effect of genetic x environment interactions on meat quality traits
across the range of production systems for sheep in Australia.
Numerous studies have shown between breed, including sire differences, in lamb meat
tenderness (Young, Reid & Scales, 1993; Fisher et al., 2000; Purchas et al., 2002;
Hopkins et al., 1998; Marti'nez-Cerezo, Sanudo, Panea & Olleta, 2005; Martinez-
Moreno, Sanudo, Medel & Olleta, 2005). Comparing six lamb crossbreds including
Texels, Border Leicester, Poll Dorset and Merino crossed with Merinos, and second
crosses, Hopkins et al. (1998) found no differences in shear force between crossbreds
for either the longissimus or semimembranosus. In the same study, where the progeny
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
33
of the three Poll Dorset sires were evaluated, a significant sire difference of 11.7
Newtons was reported (Hopkins et al., 1998). The sire producing ‘tough’ meat in its
progeny appear to be a line that is genetically tough and is called a ‘Carwell’ sire (see
section above).
Selection for increased muscling in sheep can produce economic benefits through
increased carcass yield but are there any negative effects on meat quality? Consumers
have scored meat from lambs sired from high muscling rams as tougher, by ten units
(scale of 0-100) (derived from Hopkins, Stanley, Toohey, Gardner, Pethick & Van De
Ven, 2007b), relative to meat from lambs sired from low muscling rams, although no
difference was found in shear force (Hopkins et al., 2007b). In other studies, the
semimembranosus from lambs sired by high muscling rams had higher shear force
values then that from lambs sired by low muscling rams (66.5 vs 61.4 N, respectively)
(Hopkins, Stanley, Martin, Toohey & Gilmour, 2007a). The meat from progeny of
sires which are extreme in either muscling or fatness have been found to produce meat
which is unacceptable to the consumer via changes in tenderness (proteolysis,
connective tissue) or juiciness/flavour (IMF) and such sires should be avoided
(Warner et al., 2007b).
The role of intramuscular fat in the tenderness of meat from lamb carcasses has
received less research attention then beef. Variation in sire breeding values for
muscling and fatness affected consumer scores for tenderness of the longissimus
lumborum with scores declining as muscling increased and as fat decreased, which
appears to be driven by IMF (Thomson, 2009). Hopkins et al. (2007b) reported that
the meat from lambs sired by rams with a high breeding value for fatness had higher
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
34
sensory tenderness scores than that from rams with low breeding values for fatness.
Hopkins, Hegarty, Walker and Pethick (2006) used consumer panels to show that a
minimum of 5% IMF is required in order to achieve a failure rate of less than 10% for
tenderness.
The heritability of ultimate pH in lambs ranges from 0.18 to 0.27 (Safari et al. 2005;
Bishop et al., 2009; Fogarty, Safari, Taylor and Murray, 2003). There is evidence for
breed effects on the way muscle glycogen metabolism is regulated in lambs. For
example, there is clear evidence that Merino lambs are more susceptible to the high
pH or dark cutting syndrome (Warner et al. 2006). This appears to be due to greater
rates of glycogen loss between leaving the farm gate and slaughter (Gardner et al,
1998) suggesting Merino are more sensitive to stress than lambs sired by meat breeds.
Further work has shown that selection for increased muscularity can influence the
metabolism of glycogen in skeletal muscle. Thus lambs derived from sires with high
genetic merit for muscularity have higher muscle glycogen concentration at any given
level of nutrient intake (Martin, Gardner, Thompson and Hopkins, 2006). This
strongly suggests that lambs with higher muscularity will be less susceptible to the
high pH or dark cutting syndrome, which can impact on meat tenderness (Purchas et
al., 1993).
7.2 Production Environment
There is a paucity of research into sheep meat breeds that attempts to understand the
interactions of specific genetic selection indices on lamb performance, carcass
composition, and meat quality (Pethick, Warner & Banks, 2006). In Australia, sheep
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
35
can be slaughtered for meat at ages ranging from 4 months to 3-6 years and are grown
and finished under a range of environments and feeding systems, from green pasture
in spring to hay or grain feeding in autumn and winter. The major breeds that
contribute to the sheep meat industry are the Merino, Border Leicester and Poll
Dorset. Research to understand the influence of carcass breeding values, age, growth
path and nutritional supply on carcass and eating quality has been undertaken
(Pethick, Warner & Banks, 2007). This research, as well as research from around the
world, is reported below.
The age of the animal appears to be the largest environmental effect in sheep meat
tenderness (Warner et al., 2007b). Meat from lambs is given a higher tenderness score
by consumers, then meat from older sheep, for both the loin and leg muscles (Pethick,
Hopkins, D'Souza, Thompson & Walker, 2005a). Surprisingly, the difference in
consumer score between an 8-month old lamb and a 6 year old sheep is only 10
consumer points, for both the longissimus thoracis and the biceps femoris (Pethick et
al., 2005a). This is also reflected in an increase in shear force with age of the sheep
(Hopkins et al., 2007a) and is attributed to a reduction in collagen solubility (Young et
al., 1993).
Nutrition in the six weeks pre-slaughter (ME from 6.2 to 11.0 MJ/kg) and the plane of
the nutrition from birth to weaning, appear to have no effect on consumer scores for
tenderness (Pethick et al., 2005b; Hopkins et al., 2005b, respectively). Faster growth
in lambs has been shown to result in thinner connective tissue, but there were no
effects on objective or consumer measures of meat tenderness (Allingham, Barris,
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
36
Reverter, Hilsenstein, Van De Ven & Hopkins, 2009) and there was no interaction
with genotype or sire.
There is little data on the effect of genetic-environmental interactions on lamb meat
quality or tenderness. In a study by Hopkins et al. (2005) utilising 140 crossbred
lambs, there was no interaction between growth rate from birth to slaughter and sire
Estimated Breeding Value (EBV) for muscling for either eating quality or shear force.
Subsequently, Hopkins et al. (2007b) found in 627 cross-bred lambs that for lambs
which were weaned early and fed a ‘restricted’ diet, the lambs sired by fast growth
sires had tougher longissimus, although this was not the case in early-weaned full-fed
or late-weaned lambs. (Hopkins et al., 2007b) found subtle interactions between
selection for growth or muscling or fatness traits and growth path and suggested that
the impact of a period of restriction and refeeding on meat and eating quality will be
meditated by the sire genetics.
Arsenos et al. (2002) showed an interaction between breed and slaughter weight for
tenderness of the leg muscles of lamb carcasses. For the Boutsko breed, lambs
slaughtered at 48% of their mature weight were significantly tougher then lambs
slaughtered at 55% mature weight, whereas for the Serres and Karagouniko breeds,
the tenderness of the meat was similar between slaughter groups.
Purchas et al. (2002) showed a genotype x year interaction with Romney sires
producing significantly lower shear force values in the semimembranosus than Finn x
Poll Dorset sires (8.40 vs 10.21 kg, respectively) in one year but not in the preceding
two years.
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
37
7.3 Post-slaughter environment
Effective electrical simulation used on lamb and sheep carcases results in meat which
is generally more acceptable to the consumer in terms of tenderness (Shaw, Baud,
Richards, Pethick, Walker & Thompson, 2005) and as discussed above tenderstretch
can be used to overcome the toughening effects of both cold-shortening and heat-
toughening (Thompson et al., 2005).
Martinez-Moreno et al. (2005) showed an interaction between genotype, live weight
and ageing time post-slaughter for consumer tenderness scores(Figure 2). At the start
of the ageing period, there were no differences in trained taste panel scores for
tenderness between meat and dairy breeds or between lambs slaughtered at 11 or 31
kg liveweight. With ageing for 4 or 8 days, marked tenderisation occurred in the meat
breed slaughtered at 31 kg but not for meat lambs slaughtered at 11 kg. For the dairy
breed, tenderisation occurred at a similar rate for both live weights.
Thompson, Gardiner, Thomson and Allingham (2007) showed that although the
progeny of sires with high breeding values for muscling or growth had tougher meat,
there was no interaction with hanging method (ie. Achilles v. tenderstretch) or
electrical stimulation.
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
38
8 Summary and conclusions
Tenderness is an important quality trait to the consumer. It is vital to control the pre-
and post-slaughter environment when attempting to determine the contributions of
genetic and production factors to meat tenderness. Genetic improvement in meat
tenderness is possible, via traditional quantitative and more recently by genomic
approaches (eg calpain markers). The greatest gains in tenderness in beef cattle appear
to be in breeds like Bos Indicus where the phenotypic variation is larger. Variation in
proteolysis appears to be the dominant contributor to genetic variation in tenderness,
certainly in cattle. Increasing muscle mass is achievable by targeted selection for
specific mutations in the myostatin gene, but if the increase comes at the expense of
tenderness, then we question if real gains have been made.
The progressive improvement in meat tenderness through selection of cattle and sheep
known to have ‘tender’ genetics, will be agonising slow unless strict attention is paid
to processing procedures. Interactions between genotype and environment contribute
to the phenotypic variation in meat tenderness. There are certainly other factors that
contribute to the variation in tenderness, including variation between slaughter dates
and abattoirs. This highlights that there are unidentified animal and/or environmental
factors that contribute to the variation in tenderness. Efforts to better understand,
characterise and control these may yield further improvements in this highly
important consumer trait.
Acknowledgements
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
39
Comments on the manuscript from James Kijas (CSIRO) are gratefully
acknowledged, as well as biometrical advice from Kym Butler (DPI, Werribee). The
assistance of Owen Young (New Zealand) and Roger Purchas (New Zealand) in
finding references is also acknowledged and the helpful comments from the
anonymous reviewers.
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
40
References
Allingham, P. G., Barris, W., Reverter, A., Hilsenstein, V., Van De Ven, R. &
Hopkins, D. L. (2009). Sire and growth-path effects on sheep meat production.
3. Fascicular structure of lamb loin muscle (m. longissimus lumborum) and the
impact on eating quality. Animal Production Science, 49, 239-247.
Arsenos, G., Banos, G., Fortomaris, P., Katsaounis, N., Stamataris, C., Tsaras, L. &
Zygoyiannis, D. (2002). Eating quality of lamb meat: effects of breed, sex,
degree of maturity and nutritional management. Meat Science, 60, 379-387.
Arthur, P. F. (1995). Double muscling in cattle: a review. Journal of Agricultural
Science, 46, 1493-1515.
Bailey, A. J. (1985). The role of collagen in the developement of muscle and its
relationship to eating quality. Journal of Animal Science, 60(6), 1580-1580.
Banks, R. (1997). The Meat Elite Project: Establishment and achievements of an elite
meat sheep nucleus. In Proceedings of the Association for the Advancement of
Animal Breeding and Genetics, 12 (pp. 598-601).
Barendse, W. (1995). Muscular hypertrophy gene in Poll Dorset Sheep. Final Report
Project M.677. Sydney: Meat Research Corporation.
Barendse, W. J. (2002). DNA markers for meat tenderness. International patent
publication W0 02/064820.
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
41
Barendse, W., Harrison, B. E., Bunch, R. J. & Thomas, M. B. (2008). Variation at the
Calpain 3 gene is associated with meat tenderness in zebu and composite breeds
of cattle. BMC Genetics, 9, 41.
Becker, T. (2000). Consumer perception of fresh meat quality: a framework for
analysis. British Food Journal, 102, 158-176.
Bellinge, R. H. S., Liberles, D. A., Iaschi, S. P. A., O’Brien, P. A. & Kay, G. K.
(2004). Myostatin and its implications on animal breeding: a review. Animal
Genetics, 36, 1-6.
Bishop, S. C. & Karamichou, E. (2009). Genetic and genomic approaches to
improving sheep meat quality. In: J. P. Kerry & D. A. Ledward (eds) Improving
the Sensory and Nutritional Quality of Fresh Meat. Cambridge, UK: Woodhead
Publishing.
Burrow, H. M., Moore, S. S., Johnston, D. J., Barendse, W. & Bindon, B. M. (2001).
Quantitative and molecular genetic influences on properties of beef: a review.
Australian Journal of Experimental Agriculture, 41, 893-919.
Burrow, H. M., Seifert, G. W. & Corbet, N. J. (1988). A new technique for measuring
temperament in cattle. Proceedings of Australian Society of Animal Production,
17, 154-157.
Cafe, L. M., McIntyre, B. M., Robinson, D. L., Geesink, G. H., Barendse, W. &
Greenwood, P. L. (2010a). Production and processing studies on calpain-system
gene markers for tenderness in cattle: 1. Growth, efficiency, temperament and
carcass characteristics. Journal of Animal Science (submitted - revised
manuscript sent back Mar 2010).
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
42
Cafe, L.M., McIntyre, B. M., Robinson, D. L., Geesink, G. H., Barendse, W.,
Thompson, J. M., Pethick, D. W. & Greenwood, P. L. (2010b). Production and
processing studies on calpain-system gene markers for tenderness in cattle: 2.
Objective meat quality. Journal of Animal Science (submitted-revised
manuscript sent back Mar 2010).
Carpenter, C. E., Owen, D. R., Cockett, N. E. & Snowder, G. D. (1996). Histology
and composition of muscles from normal and Callipyge lambs. Journal of
Animal Science, 74, 388-393.
Carpenter, C. E. & Solomon, M. (1995). Post-mortem processing procedures to
tenderise callipyge lamb. In Proceedings of the International Congress of Meat
Science and Technology, 41, 620-621.
Casas, E., Keele, J. W., Shackelford, S. D., Koohmaraie, M., Sonstegard, T. S., Smith,
T. P., Kappes, S. M. & Stone, R. T. (1998). Association of the muscle
hypertrophy locus with carcass traits in beef cattle. Journal of Animal Science,
76, 468-473.
Channon, H. A., Payne, A. & Warner, R. D. (2000). Halothane genotype, pre-
slaughter handling and stunning method all influence pork quality. Meat
Science, 56, 291-299.
Clare, T. L., Jackson, S. P., Miller, M. F., Elliott, C. T. & Ramsey, C. B. (1997).
Improving tenderness of normal and callipyge lambs with calcium chloride.
Journal of Animal Science, 75, 377-385.
Clop, A., Marcq, F., Takeda, H., Pirrottin, D., Toroir, X., Bibe, B., Bouix, J., Caiment,
F., Elsen, J-M., Eychenne, F., Larzul, C., Laville, E., Meisch, F., Milenkovic,
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
43
D., Tobin, J., Charlier, C. & Georges, M. (2006). A mutation creating a
potential illegitimate microRNA target site in the myostatin gene affects
muscularity in sheep. Nature Genetics, 38, 813-818.
Cockett, N. E., Jackson, S. P., Shay, T. L., Nielsen, D., Moore, S. S., Steele, M. R.,
Barendse, W., Greene, R. D. & Georges, M. (1993). Chromosomal localization
of the callipyge gene in sheep (Ovis aries) using bovine DNA markers.
Proceedings of the National Academy of Sciences USA, 91, 3019-3023.
Cockett, N. E., Jackson, S. P., Shay, T. L., Famir, F., Bergmans, S., Snowder, G. D.,
Nielson, D. M. & Georges, M. (1996). Polar overdominance at the ovine
Callipyge locus. Science, 273, 236-238.
Colditz, I. G., Ferguson, D. M., Greenwood, P. L., Doogan, V. J., Petherick, J. C. &
Kilgour, R. J. (2007). Regrouping unfamiliar animals in the weeks prior to
slaughter has few effects on physiology and meat quality in Bos taurus feedlot
steers. Australian Journal of Experimental Agriculture, 47, 763-769.
Cummins, L. (1997). Muscle genes and lamb tenderness. Is there a muscular
hypertrophy gene in Australia and does it cause tough meat? A PIRD funded
investigation by the Heywood Advanced Breeders Group and Agriculture
Victoria using terminal lamb sire genetics from Mr P. Rose’s Carwell Stud.
Hamilton: Pastoral and Veterinary Institute, Agricultural Victoria.
Daly, C.C. (2000). Live animal contribution to beef tenderness. Proceedings of the
New Zealand Society of Animal Production, 60, 103–106.
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
44
Davis, J., Ferrier, G. & Gaunt, G. (1999). The assessment of genetic expression and
nutritional effects on lamb eating quality. Final Report LAMB.326 for Meat &
Livestock Australia. Rutherglen: Agriculture Victoria.
D'Souza, D. N., Warner, R. D., Dunshea, F. R. & Leury, B. J. (1998). Effect of on-
farm and pre-slaughter handling of pigs on meat quality. Australian Journal of
Agricultural Research, 49, 1021-1025.
Dransfield, E. (1977). Intramuscular composition and texture of beef muscles. Journal
of Science in Food and Agriculture, 28, 844-842.
Dransfield, E. (1992). Modelling post-mortem tenderisation--III: Role of calpain I in
conditioning. Meat Science, 31, 85-94.
Dransfield, E. (1993). Modelling Post-mortem tenderisation-IV: Role of calpains and
calpastatin in conditioning. Meat Science, 34, 217-234.
Dransfield, E. (1994). Modelling post mortem tenderisation - V: Inactivation of
calpains. Meat Science, 37, 391-409.
Dransfield, E., Etherington, D. J. & Taylor, M. A. J. (1992). Modelling post-mortem
tenderisation--II: Enzyme changes during storage of electrically stimulated and
non-stimulated beef. Meat Science, 31, 75-84.
Dransfield, E. & Jones, R. C. D. (1980). Tenderising in m longissimus dorsi of beef
veal rabbit lamb and pork. Meat Science, 5, 139-147.
Dransfield, E., Wakefield, D. K. & Parkman, I. D. (1992). Modelling post-mortem
tenderisation--I: Texture of electrically stimulated and non-stimulated beef.
Meat Science, 31, 57-73.
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
45
Dransfield, E. & Rhodes, D. N. (1976). Effect of post-rigor muscle length on the
texture of meat. Journal of Science in Food and Agriculture, 27(5), 483-486.
Duckett, S. K., Klein, T. A., Dodson, M. V. & Snowder, G. D. (1998). Tenderness of
normal and callipyge lamb aged fresh or after freezing. Meat Science, 49, 19-26.
Duckett, S. K., Snowder, G. D. & Cockett, N. E. (2000). Effect of the callipyge gene
on muscle growth, calpastatin activity, and the tenderness of three muscles
across the growth curve. Journal of Animal Science, 78, 2836-2841.
Ferguson, D.M., Jiang, S., Hearnshaw, H., Rymill, S.M. & Thompson, J.M. (2000).
Effect of electrical stimulation on protease activity and tenderness of
M.longissimus from cattle with different proportions of Bos indicus content.
Meat Science, 55, 265-272.
Field, R. A., McCormick, R. J., Brown, D. R., Hinds, F. C. & Snowder, G. D. (1996).
Collagen crosslinks in longissimus muscle grom lambs expressing the callipyge
gene. Journal of Animal Science, 74, 2943-2947.
Fisher, A. V., Enser, M., Richardson, R. I., Wood, J. D., Nute, G. R., Kurt, E.,
Sinclair, L. A. & Wilkinson, R. G. (2000). Fatty acid composition and eating
quality of lamb types derived from four diverse breed Î production systems.
Meat Science, 55, 141-147.
Fogarty, N. M., Safari, E., Taylor, P. J., & Murray, W. (2003). Genetic parameters for
meat quality and carcass traits and their correlation with wool traits in Australian
Merino sheep. Australian Journal of Agricultural Research, 54, 715-722.
Freking, B. A., Keele, J. W., Beattie, C. W., Kappes, S. M., Smith, T. P. L.,
Sonstegard, T. S., Nielson, M. K. & Leymaster, K.A. (1998a). Evaluation of the
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
46
ovine Callipyge locus: I. Relative chromosomal position and gene action.
Journal of Animal Science, 76, 2062-2071.
Freking, B. A., Keele, J. W., Nielson, M. K. & Leymaster, K. A. (1998b). Evaluation
of the ovine Callipyge locus: II. Genotypic effects on growth, slaughter and
carcass traits. Journal of Animal Science, 76, 2549-2559.
Freking, B. A., Smith, T. P. L. & Leymaster, K. A. (2004). The Callipyge mutation
for sheep muscular hypertrophy – genetics, physiology and meat quality. In M.
F. W. te Pas, M. E. Everts & H. P. Haagsman, Muscle development in livestock
animals (pp. 317-342). Wallingford: CAB International.
Gardner, G. E., Kennedy, L., Milton, J. T. B., & Pethick, D. W. (1999). Glycogen
metabolism and ultimate pH of muscle in Merino, first-cross, and second-cross
wether lambs as affected by stress before slaughter. Australian Journal of
Agricultural Research, 50, 175-181.
Geesink, G. H. & Koohmaraie, M. (1999). Postmortem proteolysis and
calpain/calpastatin activity in callipyge and normal lamb biceps femoris during
extended post-mortem storage. Journal of Animal Science, 77, 1490-1501.
Gill, J. L., Bishop, S. C., McCorquodale, C., Williams, J. L. & Wiener, P. (2009).
Associations between the 11-bp deletion in the myostatin gene and carcass
quality in Angus-sired cattle. Animal Genetics, 40, 97-100.
Glitsch, K. (2000). Consumer perceptions of fresh meat quality: cross-national
comparison. British Food Journal, 102, 177-194-
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
47
Gluckman, P. D., Hanson, M. A. & Beedle, A. S. (2007). Non-genomic
transgenerational inheritance of disease risk. BioEssays, 29(2), 145-154.
Greenwood, P. L. & Cafe, L. M. (2007). Prenatal and pre-weaning growth and
nutrition of cattle: Long-term consequences for beef production. Animal, 1,
1297-1313.
Greenwood, P. L., Cafe, L. M., Hearnshaw, H., Hennessy, D. W., Thompson, J. M. &
Morris, S. G. (2006b). Long-term consequences of birth weight and growth to
weaning for carcass, yield and beef quality characteristics of Piedmontese- and
Wagyu-sired cattle. Australian Journal of Experimental Agriculture, 46, 257-
269.
Greenwood, P. L., Davis, J., Gaunt, G. M. & Ferrier, G. R. (2006a). Influences on the
loin and cellular characteristics of the m. longissimus lumborum of Australian
Poll Dorset-sired lambs. Australian Journal of Agricultural Research, 57, 1-12.
Greenwood, P. L. & Dunshea, F. R. (2009). Biology and regulation of carcass
composition. In J. P. Kerry & D. Ledward (eds), Improving the sensory and
nutritional quality of fresh meat (pp. 19-60). Cambridge: Woodhead Publishing.
Gruber, S. L., Tatum, J. D., Engle, T. E., Chapman, P. L., Belk, K. E. & Smith, G. C.
(2009). Relationships of behavioral and physiological symptoms of pre-
slaughter stress to beef LM tenderness. Journal of Animal Science, In press,
Harper, G. S. (1999). Trends in skeletal muscle biology and the understanding of
toughness in beef. Australian Journal of Agricultural Research, 50, 1105-1129.
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
48
Hocquette, J. F., Gondret, F., Baéza, E., Médale, F., Jurie, C. & Pethick, D. W.
(2010). Intramuscular fat content in meat-producing animals: development
genetic and nutritional control and identification of putative markers. Animal, 4
(2), 303-319.
Hocquette, J. F., Lehnert, S., Barendse, W., Cassar-Malek, I. & Picard, B. (2007).
Recent advances in cattle functional genomics and their application to beef
quality. Animal, 1, 159-173.
Hopkins, D. L. & Fogarty, N. M. (1998). Diverse lamb genotypes--2. Meat pH, colour
and tenderness. Meat Science, 49, 477-488.
Hopkins, D. L., Hegarty, R. S. & Farrell, T. C. (2005). Relationship between sire
estimated breeding values and the meat and eating quality of meat from their
progeny grown on two planes of nutrition. Australian Journal of Experimental
Agriculture, 45, 525-533.
Hopkins, D. L., Hegarty, R. S., Walker, P. J. & Pethick, D. W. (2006). Relationship
between animal age, intramuscular fat, cooking loss, pH, shear force and eating
quality of aged meat from sheep. Australian Journal of Experimental
Agriculture, 46, 879-884.
Hopkins, D. L., Stanley, D. F., Martin, L. C., Toohey, E. S. & Gilmour, A. R.
(2007a). Genotype and age effects on sheep meat production. 3. Meat quality.
Australian Journal of Experimental Agriculture, 47, 1151-1164.
Hopkins, D. L., Stanley, D. F., Toohey, E. S., Gardner, G. E., Pethick, D. W. & Van
De Ven, R. (2007b). Sire and growth path effects on sheep meat production. 2.
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
49
Meat and eating quality. Australian Journal of Experimental Agriculture, 47,
1219-1228.
Huffman, K. L., Miller, M. F., Hoover, L. C., Wu, C. K., Brittin, H. C. & Ramsey, C.
B. (1996). Effect of beef tenderness on consumer satisfaction with steaks
consumed in the home and restaurant. Journal of Animal Science, 74, 91-97.
Hwang, I. H., Devine, C. E. & Hopkins, D. L. (2003). The biochemical and physical
effects of electrical stimulation on beef and sheep meat tenderness. Meat
Science, 65, 677-691.
Jackson, S. P., Green, R. D. & Miller, M. F. (1997a). Phenotypic characterization of
Rambouillet sheep expressing the Callipyge gene: I. Inheritance of the condition
and production characteristics. Journal of Animal Science, 75, 14-18.
Jackson, S. P., Miller, M. F. & Green, R. D. (1997b). Phenotypic characterization of
Rambouillet sheep expressing the Callipyge gene: II. Carcass characteristics and
retail yield. Journal of Animal Science, 75, 125-132.
Jackson, S. P., Miller, M. F. & Green, R. D. (1997c). Phenotypic characterization of
Rambouillet sheep expressing the Callipyge gene: III. Muscle weights and
muscle weight distribution. Journal of Animal Science, 75, 133-138.
Johnson, P. L., McEwan, J.C., Dodds, K. G., Purchas, R. W. & Blair, H. T. (2005).
Meat quality traits were unaffected by a quantitative trait locus affecting leg
composition traits in Texel sheep. Journal of Animal Science, 83, 2729-2735.
Johnston, D. J., Reverter, A., Ferguson, D. M., Thompson, J. M. & Burrow, H. M.
(2003). Genetic and phenotypic characterisation of animal, carcass, and meat
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
50
quality traits from temperate and tropically adapted beef breeds. 3. Meat quality
traits. Australian Journal of Agricultural Research, 54, 135-147.
Johnston, D. J., Reverter, A., Robinson, D. L. & Ferguson, D. M. (2001). Sources of
variation in mechanical shear force measures of tenderness in beef from
tropically adapted genotypes, effects of data editing and their implications for
genetic parameter estimation. Australian Journal of Experimental Agriculture,
41, 991-996.
Jopson, N. B., Nicoll, G. B., Stevenson-Barry, J. M., Duncan, S., Greer, G. J., Bain,
W. E., Gerard, E. M., Glass, B. C., Broad, T. E. & McEwan, J. C. (2001). Mode
of inheritance and effects on meat quality of the rib-eye muscling (REM) QTL
in sheep. In Proceedings of the Australian Association of Animal Breeding and
Geneticis, 14, 111-114.
Joulia-Ekaza, D. & Cabello, G. (2006). Myostatin regulation of muscle development:
Molecular basis, natural mutations, physiopathological aspects. Experimental
Cell Research, 312, 2401-2414.
Kadel, M. J., Johnston, D. J., Burrow, H. M., Graser, H. & Ferguson, D. M. (2006).
Genetics of flight time and other measures of temperament and their value as
selection criteria for improving meat quality traits in tropically adapted breeds
of beef cattle. Australian Journal of Agricultural Research, 57, 1029-1035.
Karamichou, E., Richardson, R. I., Nute, G. R., Wood, J. D. & Bishop, S. C. (2007).
Genetic analyses of sensory characteristics and relationships with fatty acid
composition in the meat from Scottish Blackface lambs. Animal, 1, 1524-1531.
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
51
Kijas, J. W., McCulloch, R., Hocking Edwards, J. E., Oddy, V. H., Lee, S. H. & van
der Werf, J. (2007). Evidence for multiple alleles effecting muscling and fatness
in the Ovine GDF8 locus. BMC Genetics, 8, 80.
King, D. A., Schuehle Pfeiffer, C. E., Randel, R. D., Welsh, J., Oliphint, R. A., Baird,
B. E., Curley, J. & Vann, R. C. (2006). Influence of animal temperament and
stress responsiveness on the carcass quality and beef tenderness of feedlot cattle.
Meat Science, 74, 546-556.
Knee, B. W., Cummins, L. J., Walker, P. J., Kearney, G. A. & Warner, R. D. (2007).
Reducing dark-cutting in pasture-fed beef steers by high-energy
supplementation. Australian Journal of Experimental Agriculture, 47, 1277-
1283.
Koohmaraie, M. (1988). The role of Endogenous proteases in meat tenderness.
Reciprocal Meat Conference Proceedings, 41, 89-100.
Koohmaraie, M. (1994). Muscle proteinases and meat ageing. Meat Science, 36, 93-
104.
Koohmaraie, M., Doumit, M. E. & Wheeler, T. L. (1996). Meat toughening does not
occur when rigor shortening is prevented. Journal of Animal Science, 74, 2935-
2942.
Koohmaraie, M. & Geesink, G. H. (2006). Contribution of postmortem muscle
biochemistry to the delivery of consistent meat quality with particular focus on
the calpain system. Meat Science, 74, 34-43.
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
52
Koohmaraie, M., Kent, M. P., Shackelford, S. D., Veiseth, E. & Wheeler, T. L.
(2002). Meat tenderness and muscle growth: Is there any relationship? Meat
Science, 62, Special Issue S1, 345-352.
Koohmaraie, M., Shackelford, S. D., Wheeler, T. L., Lonergan, S. M. & Doumit, M.
E. (1995). A muscle hypertrophy condition in lamb (Callipyge):
Characterization of effects on muscle growth and meat quality traits. Journal of
Animal Science, 73, 3596-3607.
Laville, E., Bouix, J., Sayd, T., Bibé, B., Elsen, J. M., Larzul, C., Eychenne, F.,
Marcq, F. & Georges, M. (2004). Effects of a quantitative trait locus for muscle
hypertrophy from Belgian Texel sheep on carcass conformation and
muscularity. Journal of Animal Science, 82, 3128-3137.
Lepetit, J., Grajales, A. & Favier, R. (2000). Modelling the effect of sarcomere length
on collagen thermal shortening in cooked meat: consequence on meat
toughness. Meat Science, 54, 239-250.
Lehnert, S. A., Wang, Y. H., Tan, S. H. & Reverter, A. (2006). Gene expression-
based approaches to beef quality research. Australian Journal of Experimental
Agriculture, 46, 165-172.
Levéziel, H., Hocquette, J. F., Lepetit, J., Denoyelle, C., Dodelin, V., Payet, N.,
Malafosse, A. & Renand, G. (2006). Q204X myostatin mutation effects on
carcass and meat quality traits in heterozygous Charolais young bulls. In 52nd
International Congress of Meat Science and Technology (pp. 65-66), Dublin,
Ireland.
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
53
Light, N., Champion, A. E., Voyle, C. & Bailey, A. J. (1985). The rοle of epimysial,
perimysial and endomysial collagen in determining texture in six bovine
muscles. Meat Science, 13, 137-149.
Lines, D. S., Pitchford, W. S., Kruk, Z. A. & Bottema, C. D. K. (2009). Limousin
myostatin F94L variant affects semitendinosus tenderness. Meat Science, 81,
126-131.
Lorenzen, C.,L., Koohmaraie, M., Shackelford, S. D., Jahoor, F., Freetly, H. C.,
Wheeler, T. L., Savell, J. W., Fiorotto, M. L. (2000). Protein kinetics in
Callipyge lambs. Journal of Animal Science, 78, 78-87.
Marsh, B. B. & Leet, N. G. (1966). Studies on Meat Tenderness. III. The effects of
cold shortening on tenderness. Journal of Food Science, 31, 1122-1147.
Marsh, B. B., Ringkob, T. P., Russell, R. L., Swartz, D. R. & Pagel, L. A. (1987a).
Effects of early-postmortem glycolytic rate on beef tenderness. Meat Science,
21, 241-248.
Marsh, B. B., Ringkob, T. P., Russell, R. L., Swartz, D. R. & Pagel, L. A. (1987b).
Effects of early-postmortem glycolytic rate on beef tenderness. Meat Science,
21, 241-248.
Marshall, D.M. (1999). The genetics of meat quality. In R Fries & A. Ruvinsky (eds),
The Genetics of Cattle,pp. (pp. 605 – 636). Wallingford: CABI Publishing.
Martin, K.M., Garnder, G.E., Thompson, J.M. & Hopkins, D.L. (2006). Nutritional
impact on muscle glycogen metabolism in lambs selected for muscling.
International Journal of Sheep and Wool Science, 54(2), 233-234.
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
54
Marti'nez-Cerezo, S., Sanudo, C., Panea, B. & Olleta, J. L. (2005). Breed, slaughter
weight and ageing time effects on consumer appraisal of three muscles
of lamb. Meat Science, 69, 797-805.
Martinez-Moreno, M., Sanudo, C., Medel, I. & Olleta, J. L. (2005). Breed, slaughter
weight and ageing time effects on sensory characteristics of lamb. Meat Science,
69, 571-578.
McBee, J. L., Jr. & Wiles, J. A. (1967). Influence of Marbling and Carcass Grade on
the Physical and Chemical Characteristics of Beef. Journal of Animal Science,
26, 701-704.
McCormick, R. J. (1994). The flexibility of the collagen compartment of muscle.
Meat Science, 36, 79-91.
McKiernan, W. & Wilkins, J. (2007). The effect of genetic potential and pre feedlot
growth path on beef eating quality. In A. Jones (ed.), Agribusiness livestock
updates 2007 (pp. 124-125). Perth: Western Australian Department of
Agriculture.
Mortimer, S. I., Pearce, K. L., Jacob, R. H., Hopkins, D. L., Warner, R. D., Geesink,
G. H., Hocking-Edwards, J. E., Pethick, D. W., Van Der Werf, J. H. J. & Ball,
A. J. (2009). The information nucleus - genetically improving Australian lamb
production.
Mullen, A. M., Pannier, L. & Hamill, R. (2009). New insights into the biology of
meat quality from genomic and proteomic perspectives, with particular
emphasis on beef. In: J. P. Kerry & D. A. Ledward (eds) Improving the Sensory
and Nutritional Quality of Fresh Meat. Cambridge, UK: Woodhead Publishing.
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
55
Ngapo, T. M., Berge, P., Culioli, J., Dransfield, E., De Smet, S. & Claeys, E. (2002).
Perimysial collagen crosslinking and meat tenderness in Belgian Blue double-
muscled cattle. Meat Science, 61, 91-102.
Nicoll, G. B., Burkin, H. R., Broad, T. E., Jopson, N. B., Greer, G. J., Bain, W. E.,
Wright, C. S., Dodds, K. G., Fennessy, P. F. & McEwan, J. C. (1998). Genetic
linkage of microsatellite markers to the Carwell locus for rib-eye muscling in
sheep. In Proceedings of the 6th World Congress on Genetics Applied to
Livestock Production, 26, 529-532.
Nishimura, T., Hattori, A. & Takahashi, K. (1999). Structural changes in
intramuscular connective tissue during the fattening of Japanese black cattle:
effect of marbling on beef tenderization. Journal of Animal Science, 77, 93-
104.
O'Connor, S. F., Tatum, J. D., Wulf, D. M., Green, R. D. & Smith, G. C. (1997).
Genetic effects on beef tenderness in Bos indicus composite and Bos taurus
cattle. Journal of Animal Science, 75, 1822-1830.
Oddy, V. H., Harper, G. S., Greenwood, P. L. & McDonagh, M. B. (2001).
Nutritional and developmental effects on the intrinsic properties of muscles as
they relate to the eating quality of beef. Australian Journal of Experimental
Agriculture, 41, 921-942.
O’Rourke, B. A., Dennis, J. A., Healy, P. J., McKiernan, W. A., Greenwood, P. L.,
Cafe, L. M., Perry, D., Walker, K. H., Marsh, I., Parnell, P. F. & Arthur, P. F.
(2009). Quantitative analysis of performance, carcass and meat quality traits in
cattle from two Australian beef herds in which a null myostatin alleles is
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
56
segregating. Animal Production Science, 49, 297-305.
Ouali, A. (1984). Sensitivity to ionic strength of Mg---Ca-enhanced ATPase activity
as an index of myofibrillar ageing in beef. Meat Science, 11, 79-88.
Page, B. T., Casas, E., Heaton, M. P., Cullen, N. G., Hyndman, D. L., Morris, C. A.,
Crawford, A. M., Wheeler, T. L., Koohmaraie, M., Keele, J. W. & Smith, T. P.
L. (2002). Evaluation of single-nucleotide polymorphisms in CAPN1 for
association with meat tenderness in cattle. Journal of Animal Science, 80, 3077-
3085.
Peaston, A. & Whitelaw, E. (2006). Epigenetics and phenotypic variation in
mammals. Mammalian Genome, 17, 365-374.
Perry, D., Shorthose, W. R., Ferguson, D. M. & Thompson, J. M. (2001). Methods
used in the CRC program for the determination of carcass yield and beef quality.
Australian Journal of Experimental Agriculture, 41, 953-957.
Perry, D. & Thompson, J. M. (2005). The effect of growth rate during backgrounding
and finishing on meat quality traits in beef cattle. Meat Science, 69, 691-702.
Pethick, D. W., Davidson, R. H., Hopkins, D. L., Jacob, R. H., D'Souza, D. N.,
Thompson, J. M. & Walker, P. J. (2005b). The effect of dietary treatment on
meat quality and on consumer perception of sheep meat eating quality.
Australian Journal of Experimental Agriculture, 45, 517-524.
Pethick, D. W., Hopkins, D. L., D'Souza, D. N., Thompson, J. M. & Walker, P. J.
(2005a). Effects of animal age on the eating quality of sheep meat. Australian
Journal of Experimental Agriculture, 45, 491-498.
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
57
Pethick, D. W., Pleasants, A. B., Gee, A. M., Hopkins, D. L. & Ross, I. R. (2006).
Eating quality of commercal meat cuts from Australian lambs and sheep.
Proceedings of the New Zealand Society of Animal Production, 66, 363-367.
Pethick, D. W., Warner, R. D. & Banks, R. G. (2006). Genetic improvement of lamb -
industry issues and the need for integrated research. Australian Journal
of Agricultural Research, 57, 591-592.
Pethick, D. W., Warner, R. D. & Banks, R. G. (2007). The influence of genetics,
animal age and nutrition on lamb production ΓÇô an integrated research
program. Australian Journal of Experimental Agriculture, 47, 1117-1118.
Pike, M. M., Ringkob, T. P., Beekman, D. D., Koh, Y. O. & Gerthoffer, W. T. (1993).
Quadratic relationship between early-post-mortem glycolytic rate and beef
tenderness. Meat Science, 34, 13-26.
Purchas, R. W. & Aungsupakorn, R. (1993). Further investigations into the
relationship between ultimate pH and tenderness for beef samples from bulls
and steers. Meat Science, 34, 163-178.
Purchas, R. W., Burnham, D. L. & Morris, S. T. (2002). Effects of growth potential
and growth path on tenderness of beef longissimus muscle from bulls and steers.
Journal of Animal Science, 80, 3211-3221.
Purchas, R. W., Sobrinho, A. G. D., Garrick, D. J. & Lowe, K. I. (2002). Effects of
age at slaughter and sire genotype on fatness, muscularity, and the quality of
meat from ram lambs born to Romney ewes. New Zealand Journal of
Agricultural Research, 45, 77-86.
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
58
Purslow, P. P., Mandell, I. B., Widowski, T. M., Brown, J., deLange, C. F. M.,
Robinson, J. A. B., Squires, E. J., Cha, M. C. & VanderVoort, G. (2008).
Modelling quality variations in commercial Ontario pork production. Meat
Science, 80, 123-131.
Reverter, A., Johnston, D. J., Ferguson, D. M., Perry, D., Goddard, M. E., Burrow, H.
M., Oddy, V. H., Thompson, J. M. & Bindon, B. M. (2003a). Genetic and
phenotypic characterisation of animal, carcass, and meat quality traits from
temperate and tropically adapted beef breeds. 4. Correlations among animal,
carcass, and meat quality traits. Australian Journal of Agricultural Research,
54, 149-158.
Reverter, A., Johnston, D. J., Perry, D., Goddard, M. E. & Burrow, H. M. (2003b).
Genetic and phenotypic characterisation of animal, carcass, and meat quality
traits from temperate and tropically adapted beef breeds. 2. Abattoir carcass
traits. Australian Journal of Agricultural Research, 54, 119-134.
Robinson, D. L., Ferguson, D. M., Oddy, V. H., Perry, D. & Thompson, J. M. (2001).
Genetic and environmental influences on beef tenderness. Australian Journal of
Experimental Agriculture, 41, 997-1003.
Rowe, L. J., Maddock, K. R., Lonergan, S. M. & Huff-Lonergan, E. J. (2004).
Oxidative environments decrease tenderization of beef steaks through
inactivation of micro-calpain. Journal of Animal Science, 82, 3254-3266.
Rowe, R. W. D. (1974). Collagen Fibre arrangement in intramuscular connective
tissue. Changes associated with muscle shortening and their possible
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
59
relevance to raw meat toughness measurements. Journal of Food Technology,
9, 501-508.
Safari, E., Fogarty, N. M. & Gilmour, A. R. (2005). A review of genetic parameter
estimates for wool, growth, meat and reproduction traits in sheep. Livestock
Production Science, 92, 271-289.
Shackelford, S.D., Koohmaraie, M., Miller, M.F., Crouse, J.D. & Reagan, J.O. (1991).
An evaluation of tenderness of the longissimus muscle of Angus by Hereford
versus Brahman crossbred heifers. Journal Animal Science 69, 171-177.
Shackelford, S. D., Wheeler, T. M. & Koohmaraie, M. (1997). Effect of the callipyge
phenotype and cooking method on tenderness of several major lamb muscles.
Journal of Animal Science, 75, 2100-2105.
Shackelford, S. D., Wheeler, T. M. & Koohmaraie, M. (1998). Can the genetic
antagonisms of callipyge lamb be overcome? In Proceedings of the Reciprocal
Meat Conference, 51, 125-132.
Shaw, F. D., Baud, S. R., Richards, I., Pethick, D. W., Walker, P. J. & Thompson, J.
M. (2005). New electrical stimulation technologies for sheep carcasses.
Australian Journal of Experimental Agriculture, 45, 575-583.
Simmons, N. J., Daly, C. C., Mudford, C. R., Richards, I., Jarvis, G. & Pleiter, H.
(2006). Integrated technologies to enhance meat quality - An Australasian
perspective. Meat Science, 74, 172-179.
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
60
Smith, G. C., Savell, J. W., Cross, H. R., Carpenter, Z. L., Murphey, C. E. & Aalhus,
J. L. (1987). Relationship of usda quality grades to palatability of cooked beef.
Journal of Food Quality, 10, 269-286.
Solomon, M., Long, J. B., Eastridge, J. S. & Carpenter, C. E. (1995). Tenderising
callipyge lamb with the Hydrodyne® process. In Proceedings of the
International Congress of Meat Science and Technology, 41 (pp. 620-621).
Stenesh, J. (1989). Dictionary of biochemistry and molecular biology. J. Wiley and
Sons, Inc, New York, USA.
Switonski, M. (2002). Molecular genetics in beef cattle breeding - a review. Animal
Science Papers and Reports, 20 (Suppl. 1), 7-18.
Tatum, J. D., Gronewald, K. W., Seideman, S. C. & Lamm, W. D. (1990).
Composition and quality of beef from steers sired by piedmontese, gelbvieh
and red angus bulls. Journal of Animal Science, 68, 1049-1160.
Taylor, R. G., Geesink, G. H., Thompson, V. F., Koohmaraie, M. & Goll, D. E.
(1995). Is Z-disk degradation responsible for postmortem tenderization? Journal
of Animal Science, 73, 1351-1367.
Taylor, R. G. & Koohmaraie, M. (1998). Effects of postmortem storage on the
ultrastructure of the endomysium and myofibrils in normal and callipyge
longissimus. Journal of Animal Science, 76, 2811-2817.
Thompson, J. M., Gardner, G. E., Thomson, K. L. & Allingham, P. G. (2007). The
effect of muscling EBVs on sheep meat eating quality. Project SMEQ.045.
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
61
Final Report to MLA.1-63. Project SMEQ.045. Final Report to MLA. Meat and
Livestock Australia, Sydney. Australia.
Thompson, J. M., Hopkins, D. L., D'Souza, D. N., Walker, P. J., Baud, S. R. &
Pethick, D. W. (2005). The impact of processing on sensory and objective
measurements of sheep meat eating quality. Australian Journal of Experimental
Agriculture, 45, 561-573.
Thompson, J. M., Perry, D., Daly, B., Gardner, G. E., Johnston, D. J. & Pethick, D.
W. (2006). Genetic and environmental effects on the muscle structure response
post-mortem. Meat Science, 74, 59-65.
Thomson, K. L. (2009). Processing and genetic factors that affect post-mortem
tenderisation in beef and lamb carcasses. Ph.D. thesis. Murdoch University,
Perth, Australia.
Tomkins, N. W., Harper, G. S., Bruce, H. L. & Hunter, R. A. (2006). Effect of
different post-weaning growth paths on long-term weight gain, carcass
characteristics and eating quality of beef cattle. Australian Journal of
Experimental Agriculture, 46, 1571-1578.
Tornberg, E. (1996). Biophysical aspects of meat tenderness. Meat Science, 43, 175-
191.
Troy, D., Murray, B., O’Sullivan, A., Mooney, T., Moloney, A. & Kerry, J. (2002).
Influence of feeding systems on the eating quality of beef. Research Report No.
58. Dublin: Teagasc.
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
62
Tornberg, E. (1996). Biophysical aspects of meat tenderness. Meat Science, 43, 175-
191.
Upton, W., Burrow, H.M., Dundon, A., Robinson, D.L. & Farrell, E.B. (2001). CRC
breeding program design, measurements and database: methods that underpin
CRC research results. Australian Journal of Experimental Agriculture, 41, 943–
952.
Voisinet, B. D., Grandin, T., O'Connor, S. F., Tatum, J. D. & Deesing, M. J. (1997).
Bos indicus-cross feedlot cattle with excitable temperaments have tougher meat
and a higher incidence of borderline dark cutters. Meat Science, 46, 367-377.
Warner, R. D., Dunshea, F. R., Ponnampalam, E. N., Gardner, G. E., Martin, K. M.,
Salvatore, L., Hopkins, D. L., & Pethick, D. W. (2006). Quality Meat from
Merinos. International Journal of Sheep and Wool Science, 54(2), 48-53.
Warner, R. D., Bond, J. J. & Kerr, M. G. (2000). Meat Quality traits in lamb M.
longissimus thoracis et lumborum: The effect of pre-slaughter stress and
electrical stimulation. International Congress of Meat Science and Technology,
Buenos Aires, Argentina, 46, 154-155.
Warner, R. D., Dunshea, F. R., Ponnampalam, E. N. & Cottrell, J. J. (2005b). Effects
of nitric oxide and oxidation in vivo and postmortem on meat tenderness. Meat
Science, 71, 205-217.
Warner, R. D., Ferguson, D. M., Cottrell, J. J. & Knee, B. W. (2007a). Acute stress
induced by the preslaughter use of electric prodders causes tougher beef meat.
Australian Journal of Experimental Agriculture, 47, 782-788.
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
63
Warner, R. D., Ferguson, D. M., McDonagh, M. B., Channon, H. A., Cottrell, J. J. &
Dunshea, F. R. (2005a). Acute exercise stress and electrical stimulation
influence the consumer perception of sheep meat eating quality and objective
quality traits. Australian Journal of Experimental Agriculture, 45, 553-560.
Warner, R. D., Pethick, D. W., Greenwood, P. L., Ponnampalam, E. N., Banks, R. G.
& Hopkins, D. L. (2007b). Unravelling the complex interactions between
genetics, animal age and nutrition as they impact on tissue deposition, muscle
characteristics and quality of Australian sheep meat. Australian Journal of
Experimental Agriculture, 47, 1229-1238.
Watson, R., Gee, A., Polkinghorne, R. & Porter, M. (2008). Consumer assessment of
eating quality - Development of protocols for Meat Standards Australia (MSA)
testing. Australian Journal of Experimental Agriculture, 48 (11), 1360-1367.
Weaver, A. D., Bowker, B. C. & Gerrard, D. E. (2008). Sarcomere length influences
postmortem proteolysis of excised bovine semitendinosus muscle. Journal of
Animal Science, 86, 1925-1932.
Wheeler, T. L., Savell, J. W., Cross, H. R., Lunt, D. K. & Smith, S. B. (1990).
Mechanisms associated with the variation in tenderness of meat from Brahman
and Hereford cattle. Journal of Animal Science, 68, 4206-4220.
Wheeler, T. L., Shackelford, S. D., Casas, E., Cundiff, L. V. & Koohmaraie, M.
(2001). The effects of Piedmontese inheritance and myostatin genotype on the
palatability of longissimus thoracis, gluteus medius, semimembranosus, and
biceps femoris. Journal of Animal Science, 79, 3069-3074.
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
64
White, S. N., Casas, E., Wheeler, T. L., Shackelford, S. D., Koohmaraie, M., Riley, D.
G., Chase Jr, C. C., Johnson, D. D., Keele, J. W. & Smith, T. P. L. (2005). A
new single nucleotide polymorphism in CAPN1 extends the current tenderness
marker test to include cattle of Bos indicus, Bos taurus, and crossbred descent.
Journal of Animal Science, 83, 2001-2008.
Wolcott, M. L., Johnston, D. J., Barwick, S. A., Iker, C. L., Thompson, J. M. &
Burrow, H. M. (2009). Genetics of meat quality and carcass traits and the
impact of tenderstretching in two tropical beef genotypes. Animal Production
Science, 49, 383-398.
Wulf, D. M., Tatum, J. D., Green, R. D., Morgan, J. B., Golden, B. L. & Smith, G. C.
(1996). Genetic influences on beef longissimus palatability in charolais- and
limousin-sired steers and heifers. Journal of Animal Science, 74, 2394-2405.
Young, O. A., Reid, D. & Scales, G. (1993). Effect of breed and ultimate pH on the
odour and flavour of sheep meat. New Zealand Journal of Agricultural
Research, 36, 363-370.
Yu, L. P. & Lee, Y. B. (1986). Effects of postmortem pH and temperature on bovine
muscle structure and meat tenderness. Journal of Food Science ., 51, 774-780.
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
65
Table 1 Shear force (N) for Achilles (AT) and tenderstretch (TS) suspended longissimus and Achilles suspended semitendinosus aged for 1 or 7 d for Brahman cattle with a combination of favourable and unfavourable genotypes for tenderness across 3 markers in New South Wales (NSW) and Western Australian (WA) experiments (Cafe et al. 2010b).
AT longissimus TS longissimus AT semitendinosus 1 d 7 d 1 d 7 d 1 d 7 d NSW herd 0_0_0a 82.8 80.4 48.9 48.2 57.4 57.1 2_2_1 77.5 64.6 44.7 43.6 54.7 54.1 Difference 5.3 15.8 4.3 4.6 2.7 3.0 SED 4.53 4.04 1.29 1.35 1.65 1.61 P-value 0.243 <0.001 0.001 <0.001 0.106 0.062 WA herd 0_0_0 50.4 55.2 53.6 49.2 57.8 53.9 2_2_1 49.2 42.2 46.5 41.9 51.2 47.9 Difference 1.2 13.0 7.1 7.3 6.6 6.0 SED 4.21 3.47 4.34 3.48 3.04 2.61 P-value 0.784 <0.001 0.108 0.039 0.031 0.023 a: Marker combination of favorable alleles for CAST_CAPN3_CAPN1-4751. Note: 2_2_1 is a favourable combination and should result in more tender meat.
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
66
Table 2. Comparison of characteristics of double-muscled cattle and Callipyge sheep with normal cattle and sheep, respectively (derived from Greenwood and Dunshea, 2009) Double-muscled cattle Callipyge sheep Specific cause Myostatin (GDF8)
mutation (non-functional myostatin)
Uncertain (DLK-1 involved)
Location of single nucleotide polymorphisms(s)
Bovine chromosome 2 (Ovine chromosome 2)1
Ovine Chromosome 18
Genotype resulting in mutant phenotype
Homozygous for mutant allele (heterozygote has intermediate phenotype)
Heterozygote with mutant allele inherited from sire (polar overdominance)
Phenotypic expression Prenatal and postnatal Primarily postnatal Location of muscle
hypertrophy More generalised Hindquarter and loin
Myofibres of affected muscles
Hyperplasia More type 2X Less type 2A May have type 2
hypertrophy depending on mutation and genetic background of cattle
More glycolytic
No hyperplasia More type 2X Far less type 2A Type 2 hypertrophy More glycolytic
Predominant mechanism in enhanced muscle growth
Increased protein synthesis
Reduced protein degradation (more calpastatin)
Meat quality Similar or more tender, pale
Much tougher, pale
1 Mutation in sheep (especially Texel breed) which affects translation into myostatin protein
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
67
Table 3 Liveweight, carcass, yield and beef quality characteristics of steers in two beef cattle herds (A and B) containing animals varying in muscling selection line (Herd A only) and either homozygous normal for the myostatin gene (wt/wt) or heterozygous for the 821 del11 loss of function myostatin mutation (mh/wt) (derived from O’Rourke et al. 2009). Herd A1 Herd B1 Muscling Selection Line2
Low High High - -
Myostatin gene3 wt/wt wt/wt mh/wt s.e.d. wt/wt mh/wt s.e.d. n 19 14 11 - 12 12 - Carcass and yield characteristics Carcass weight (kg) 366 360 361 18.7 282 290 12.1 Rib fat depth (mm) 18.3 15.7 14.7 2.45 6.5 d 4.9 c 0.71 EMA (cm2) 70.4c 77.0d 85.0e 3.17 59.4 61.4 2.42 Retail yield (% CCW) 62.2c 63.5c 67.0d 0.72 68.6c 71.8d 0.43 Fat trim (% CCW) 18.5d 17.0d 14.5c 0.76 10.3d 8.4c 0.47 Bone (% CCW) 18.7d 18.9d 17.9c 0.26 21.1d 19.8c 0.36 Longissimus quality Shear force (kg) 4.6 5.1 4.1 0.43 4.1 4.1 0.20 Compression (kg) 1.6 1.8 1.6 0.10 1.9 1.9 0.10 IMF (%) 4.0 4.1 2.9 0.39 2.7 1.8 0.42
Semitendinosus quality Shear force (kg) 5.2 4.7 4.6 0.33 5.1b 4.4c 0.14 Compression (kg) 2.5 2.3 2.2 0.14 2.5 2.3 0.13 1Herd A established from Angus x Hereford cows, Herd B established from Angus and Charolais cows 2Muscling selection lines in Herd A steers; Low = low muscle selection line, High = high muscling selection line. Selection was based on muscle score as assessed at weaning. 3Myostatin gene; homozygous ‘normal’ (wild-type=wt) myostatin = wt/wt, heterozygous for the 821 del11 loss of function myostatin mutation = mh/wt Within herds, mean values followed by different letters are significantly different at P = 0.05
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
68
Table 4 Contributions to the total and slaughter group variance in longissimus shear force (from Johnston et al. 2001).
Overall variance components
Variance (kg2)
Slaughter group variance components
Variance (kg2)
Additive genetic 0.216 Slaughter weight and finishing system
0.010
Slaughter group 0.122 Electrical stimulation system*
0.008
Herd and sex 0.036 Slaughter date
0.109
Residual 0.330
Total 0.704 Total 0.127 *Low voltage versus high voltage electrical stimulation
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
69
Table 5 Effects of nutrition and growth during different stages of development for beef peak force (N) at heavier market weights of cattle, from Australian Beef Cooperative Research Centre studies demonstrating the relatively large effects due to nutrition during finishing compared to earlier in life.
Stage of growth and muscle
Breed type Comparison P-value Referencesa
Birth weight (Prenatal growth) Low High Longissimus Temperate 39.2 40.5 0.26 1,2 Semitendinosus Temperate 46.2 46.4 0.81 1,2 Pre-weaning growth (Weaning weight) Slow Rapid Longissimus Temperate 40.5 39.2 0.25 1,2 Semitendinosus Temperate 46.3 46.3 0.89 1,2 120 days post-weaning growth Weight
loss Rapid growth
Longissimus Tropically- adapted
76.5 73.5 >0.10 3
Semitendinosus Tropically- adapted
50.0 48.1 >0.10 3
Backgrounding growth Slow Rapid Longissimus Temperate 40.0 40.8 >0.10 4 Finishing system Pasture Feedlot Longissimus Temperate 42.7 38.6 <0.001 5 Semitendinosus Temperate 48.6 44.1 <0.001 5 Longissimus Tropically-
adapted 49.2 45.5 <0.001 5
Semitendinosus Tropically- adapted
49.3 45.0 <0.001 5
a: References: 1 Greenwood, Café, Hearnshaw, Hennessy, Thompson & Morris (2006); 2 Greenwood and Cafe (2007); 3 Tomkins, Harper, Bruce & Hunter. (2006); 4 McKiernan & Wilkins (2007); 5 Johnston, Reverter, Ferguson, Thompson & Burrow, (2003)
ACC
EPTE
D M
ANU
SCR
IPT
ACCEPTED MANUSCRIPT
70
Figure 1 Variation in within-breed heritability with days aged for longissimus shear force in beef for two studies. Each point is an estimate, with the standard error of the estimate indicated by a vertical line. The data is derived from O’Connor et al. (1997) and Wulf et al. (1996)