prospects for using marker-assisted breeding to improve maize production in africa

Journal of the Science of Food and Agriculture J Sci Food Agric 88:745–755 (2008)

ReviewProspects for using marker-assistedbreeding to improve maize production in AfricaRobyn Stevens∗Donald Danforth Plant Science Center, 975 N Warson Rd, Saint Louis, MO 63132, USA

Abstract: Maize (Zea mays L.) production in sub-Saharan Africa has historically been constrained by a numberof biotic and abiotic factors, including drought, insects, disease, and weeds. New agricultural research involvinggenomics and molecular markers may assist plant breeders in developing new varieties that will benefit producersand consumers in this region. Over the past few decades, plant breeders have used molecular markers to identifynumerous genomic regions affecting maize production and nutritional value. Marker-assisted selection (MAS)presents the potential to improve the efficiency of plant breeding by allowing for the transfer of these specificgenomic regions of interest and accelerating the recovery of the elite parent background. However, to this point,few examples of successful MAS in breeding programs, particularly those with benefits in Africa, have been noted.This review discusses the use of molecular markers in the identification of quantitative trait loci (QTL) affectingthe production and nutritional quality of maize, as well as the potential to use the results from the vast number ofQTL studies that have been performed in MAS breeding programs. 2008 Society of Chemical Industry

Keywords: Zea mays L.; Africa; marker-assisted breeding; quantitative trait loci; micronutrients; drought

INTRODUCTIONMaize (Zea mays L.) is one of the oldest and mostimportant food grains in the world. It belongs tothe grass family Poaceae (Gramineae), tribe May-deae, and is the only cultivated species in this genus.Maize germplasm can be divided into temperate andtropical maize based on the latitude in which it isgrown; temperate maize is grown in cooler climatesbeyond 34 ◦N and 34 ◦S, while tropical maize is grownin warmer environments between the equator and30 ◦N and 30 ◦S. Tropical maize is further dividedinto subclasses based on the environment: lowland,mid-altitude, and highland.1 A variety of seed typesare planted in tropical regions, including landraces,open-pollinated varieties, and various types of hybrids.

Maize is of great economic importance around theworld, as human food, animal feed, and a source ofmany manufactured goods. While most maize grain isused for animal feed and manufacturing in the devel-oped world, in many developing countries 85% ormore is used for human consumption.2 While maizeis a New World crop, it has also become an importantsource of calories in many African countries. Through-out sub-Saharan Africa, maize accounts for an averageof 15% of daily caloric intake; however, this variesregionally, as some countries receive up to 50% oftheir daily calories from maize.3 However, agriculturethroughout the developing world suffers from a mul-titude of problems. Drought, nutrient-depleted soils,and disease create complex management issues for

farmers, while food insecurity and poor nutrition trou-ble urban consumers. A 1992 survey of maize scientistsfrom Africa, Asia, Latin America, and the Middle Eastidentified grain yield as the most important trait acrossall four continents.4 In Africa, tolerance to drought,weeds, streak virus, Striga, and other diseases werealso identified as important characteristics for maizeimprovement (Table 1).2,5

New agricultural research involving genomics andmolecular markers may assist plant breeders in devel-oping new technologies to help improve the problemsfacing producers and consumers in the developingworld. However, it is important that research aimedat assisting such regions also takes into account theproduction conditions and constraints faced by thesefarmers. Lack of credit and infrastructure mean thatinputs, including irrigation, fertilizers, and pesticides,may not be viable options for many small-scale farmersin sub-Saharan Africa. The development of varietiesthat are innately able to deal with biotic and abioticstresses appears to be the most beneficial for pro-ducers, while development of micronutrient-enrichedvarieties would be most helpful for consumers who suf-fer from deficiencies of particular nutrients, includingiron, zinc, and vitamin A.

MARKER-ASSISTED BREEDINGConventional plant breeding has generally beenbased on measurable phenotypic characteristics. These

∗ Correspondence to: Robyn Stevens, Donald Danforth Plant Science Center, 975 N Warson Rd, Saint Louis, MO 63132, USAE-mail: [email protected](Received 23 March 2007; revised version received 18 August 2007; accepted 2 October 2007)Published online 9 January 2008; DOI: 10.1002/jsfa.3154

2008 Society of Chemical Industry. J Sci Food Agric 0022–5142/2008/$30.00

R Stevens

Table 1. Major constraints to maize production in sub-Saharan Africa

by region2

Mid-altitude/subtropical Tropical lowland

1. Low/declining soil fertility 1. Low/declining soil fertility2. Gray leaf spot 2. Drought/water stress3. Streak virus 3. Striga4. Weevils 4. Streak virus5. Borers (Chilo, Sesamia spp.) 5. Borers6. Drought

characteristics can be qualitative or quantitative.Qualitative traits are typically controlled by asingle, dominant gene, while quantitative traits arecontinuously distributed and affected by many genesand their interactions. Many traits may also be affectedby environmental conditions. In order to introduce anew trait, a cross-pollination is made, which introducesnew alleles for thousands of genes. Many progeny willnot possess ideal combinations of alleles, resultingin unfavorable characteristics. Multiple cycles ofevaluation in a variety of environments may berequired to identify the most favorable genotypes.Newer methods of plant breeding can significantlyreduce the time required for trait introgression.Marker-assisted selection (MAS) involves the selectionof plants carrying a particular region of DNA involvedin the expression of a trait of interest using molecularmarkers. The beauty of this technique is that markerphenotypes can be identified at the seedling stage,eliminating the time needed for plant maturationand reducing population sizes. In addition, screeningseedlings eliminates the potential for genotype-by-environment (G×E) interactions.

A number of molecular marker techniques havebeen developed for identifying polymorphisms inplants (Table 2). Restriction fragment length poly-morphisms (RFLPs) were the first widely used molec-ular markers. RFLPs are very effective at identifyingpolymorphisms; however, difficulty in automating theprocess and the large amounts of DNA required havereduced the use of this technique. Amplified frag-ment length polymorphisms (AFLPs) were developedas a polymerase chain reaction (PCR)-based methodfor detecting polymorphisms, but recently simplesequence repeats (SSRs) have been most frequentlyused, particularly in maize. SSRs have a number ofadvantages, including an easy automation process, alarge number of public SSR primers available, andcost-effectiveness once the primers are developed.With the recent availability of genome sequences, sin-gle nucleotide polymorphisms (SNPs) are becomingmore popular in both private and public breedingprograms.

MAS is possible for traits controlled by major genesand by quantitative trait loci (QTL). In order toidentify the regions affecting a trait, a breeder mustfirst identify parents that differ in the trait of interestand develop a population segregating for the trait.The parents are then screened for polymorphisms in

Table 2. Molecular marker techniques for plant breeding

RFLP AFLP SSR SNP

PCR-based No Yes Yes YesTechnical difficulty High Moderate Low LowEasily automated No No Yes YesDevelopment cost Low Moderate High HighCost per data point High Moderate Low Low

their genome using molecular markers. Polymorphicmarkers are applied to the entire population, and thedata are used to create a genetic linkage map. Thepopulation is screened for the phenotypic trait, andstatistical programs find molecular markers from thelinkage map associated with the trait. The markersclosely associated with the trait may be useful in MAS.6

However, for MAS to be successful, high-resolutionmaps are needed to identify markers that are closelylinked (<1 cM) to the genomic region controllingthe trait in order to ensure that recombination willnot occur between the gene and the marker. To getsuch high-resolution maps, population sizes are oftenover 1000 individuals.7–9 Markers also need to bevalidated by determining the reliability of the markerin predicting the phenotype in a variety of populationsand cultivars with different genetic backgrounds.10–15

In addition, for MAS to be a useful technology, thegenotyping technique must be highly reproducible,economical, and user-friendly. The cost of usingMAS compared to conventional plant breeding variesconsiderably between studies, and must take intoconsideration a number of factors including traitinheritance, phenotypic evaluation method, and thecosts of field/greenhouse space, labor, and resources.6

In some cases, phenotypic screening is cheaper orthe trait of interest is not suitable for MAS.16,17

However, in many cases, phenotypic screening is time-consuming and/or difficult, so markers may be cheaperand preferable.17–19 Molecular markers can be usedin early generations to identify only plants containingmarkers linked to the desired trait, reducing the size offurther field trials by eliminating unwanted genotypes.In backcrossing programs, selection to identifymarkers linked with the desired trait from the donorparent occurs while also selecting for markers to speedrecovery of the recurrent parent’s genetic background.Table 3 presents the theoretical proportion of therecurrent parent genome after each generation ofbackcrossing. This proportion is calculated as follows:(2n+1 − 1)/2n+1, where n is the number of backcrosses.

Table 3. Percentage of recurrent parent genome after backcrossing

Generation Recurrent parent genome (%)

BC1 75.0BC2 87.5BC3 93.8BC4 96.9BC5 98.4BC6 99.2

746 J Sci Food Agric 88:745–755 (2008)DOI: 10.1002/jsfa

Marker-assisted breeding to improve maize production

However, these percentages are only realized whenpopulation size is very large – some progeny willrecover a greater proportion of the recurrent parentgenome, while others will recover a smaller proportion.In a traditional backcrossing program, at least sixbackcross generations would be needed to recover99% of the recurrent parent. MAS allows for theidentification of progeny with the largest proportion ofthe recurrent parent genome in the first generation. Sowhile the cost of marker-assisted backcrossing may behigher than traditional breeding methods in the shortrun, time savings in cultivar development and releasemay lead to economic benefits in the long-term.6,20

BREEDING FOR DROUGHT RESISTANCELow water availability is a major cause of cropyield reduction around the world.21 Maize yields aredecreased by 15% annually in the lowland tropicsand subtropics, but in some regions and years thelosses are much greater.22 Maize generally is notirrigated in the tropics, so the natural variability inrainfall timing and amount can result in droughtat any point in the development of the maize crop.Losses due to drought are particularly high when thestress occurs just before or during flowering. Whilesilk growth is very sensitive to changes in water status,tassel development and pollen shed (anthesis) are farless affected. Drought conditions around floweringtime can cause the interval between anthesis andsilk emergence (i.e., anthesis–silking interval, ASI)to be lengthened, so the late emerging silks are notpollinated, leading to lower yield.23–29 In addition,photosynthesis is severely affected, and accumulationof carbohydrates is reduced. This leads to a shortageof assimilates in the developing ear.21,30–33

The International Maize and Wheat ImprovementCenter (CIMMYT) has engaged in selection fordrought-resistant maize varieties over the past threedecades. Selections were made based on grain yield,ASI, and level of leaf senescence under severe andintermediate drought stress. Improvements in yieldunder drought conditions averaged 126 kg ha−1 percycle. These sources were introgressed into localAfrican germplasm, resulting in hybrids with stable,superior performance in southern and eastern Africa,and an open-pollinated variety superior to commercialhybrids under moderate-to-severe water stress.34 Inaddition, the gains from selection showed littleinteraction with the environment.29,35–38

MAS could also be a useful tool in the developmentof germplasm with increased stress tolerance. Anumber of QTL involved in yield components ofmaize have already been identified. In fact, QTLfor grain yield have been identified on all tenchromosomes of maize, some accounting for a highpercentage of phenotypic variance.39–44 However,these major QTL each mapped at different locations,highlighting inconsistency in yield QTL acrossdifferent genetic materials. In addition, selection based

solely on grain yield is often considered inefficientdue to the reduced variance and heritability ofyield components under environmental stress.45,46

Selection for secondary traits, in combination withgrain yield, may allow for the most improvementin drought stress tolerance. Suitable secondary traitsshould be genetically associated with grain yield underdrought, highly heritable, stable, easy to measure, andnot associated with yield loss under ideal growingconditions.47 Based upon work at CIMMYT andPioneer Hi-Bred, key secondary traits under droughtinclude reduced barrenness, ASI, and staygreen, thetendency for plants to retain green leaves oftenresulting from delayed senescence.48

ASI may be an ideal secondary trait for droughtresistance selection. Short ASI is indicative of rapidearly ear growth, while a long ASI is associated withdrought susceptibility, low harvest index, slow eargrowth, and barrenness.36,49 DuPlessis and Dijkhuisreported an 82% reduction in grain yield as ASIincreased from 0 to 28 days.50 A similar observationwas made by Bolanos and Edmeades, who observeda 90% reduction in yield as ASI increased from −0.4to 10 days.29 Experiments at CIMMYT have shownthat heritability of ASI was similar to or higher thanheritability of grain yield under drought conditions,and ASI shows a high negative correlation with grainyield, particularly kernel number and ear number perplant.50–54 A number of QTL have been identifiedthat are involved in the expression of ASI underwater-stressed conditions.26,39,44,55,56 The results ofRibault et al. indicate the presence of QTL with fairlystable effects on ASI under two different drought stressconditions.39,56 Of the seven QTL observed for ASI,five were common under both intermediate and severewater stress, and three of these were also observedunder well-watered conditions (bins 1.08, 2.07/2.08,and 6.05). Sari-Gorla et al. also identified a QTL forASI in bin 1.08 in a different genetic background.26 Inaddition to the consistency of QTL over different waterlevels and genetic backgrounds, the heritability of ASIis high under drought and the measurement is notsubjective, making this a potentially useful secondarytrait for MAS.26,56

In 1994, CIMMYT began a backcross MASprogram to improve the drought tolerance ofCML247, an elite tropical inbred line with a longASI. The donor line was Ac7643, a drought-tolerantline with a short ASI in water-limited conditions.Five genomic regions involved in the expression ofa short ASI under severe stress were transferredfrom Ac7643 to CML247. MAS was used at twobackcross and two self-pollination cycles to identifythe desired donor alleles and to recover as much of therecurrent parent background as possible. The 70 bestlines were selected to be crossed with two CIMMYTtesters. The resulting test-crosses performed betterunder severe stress than the control, and the bestgenotype among the 70 performed two to four timesbetter than the control. However, the advantage

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decreased as the intensity of stress decreased, anddisappeared when stress reduced yield by less than40%. No yield reduction was seen under well-wateredconditions.57,58

Chlorophyll content of the leaf also decreases asa function of the severity of water stress, lead-ing to senescence.59–61 Drought promotes increasedethylene production in plants by increasing 1-aminocyclopropane-2-carboxylate (ACC) synthesisand its conversion to ethylene.62–64 Inhibition of ethy-lene synthesis reduces drought-induced loss of chloro-phyll and prevents drought-induced senescence.65,66

Examples of functional and cosmetic staygreen havebeen described.67,68 Functional staygreen is due toextended photosynthesis, while cosmetic staygreen isdue to retention of chlorophyll after photosynthesishas ceased.67 Functional staygreen may be affectedby the expression of ACC synthase (ACS), which isinvolved in the first steps of ethylene biosynthesis.Young et al. found that loss of ZmACS6 expression inmaize resulted in delayed leaf senescence under nor-mal growth conditions and inhibited drought-inducedleaf senescence. Zmacs6 leaves exhibited a delayin drought-induced senescence, retained near-normallevels of chlorophyll and protein, and maintained phys-iological and biochemical function.69

Micro-array data comparing gene expression understressed and unstressed conditions have also exposedregions of the genome that may be useful in furtherbreeding efforts. Research on dehydration tolerance inArabidopsis has identified at least four signal transduc-tion pathways that function during abiotic stress andhas identified numerous genes and binding elementsthat respond to dehydration stress.70–73 In maize,Andjelkovic and Thompson compared gene expres-sion of 2500 cDNA clones in maize kernels underwater-stressed and unstressed conditions. Twenty-sixgenes were identified as dehydration-induced, includ-ing a maize DRE (dehydration-responsive element) and anumber of ABA-inducible proteins, which are knownto have protective functions under drought stress.Most of the genes identified have previously beencharacterized in Arabidopsis, rice, or barley.74

BREEDING FOR RESISTANCE TO BIOTICSTRESSESTropical maize is plagued by a variety of biotic stresses,including diseases, insects, and parasitic weeds. Over60% of the maize area in eastern and southern Africasuffers from insect and disease infestations each year.75

Sugarcane mosaic virus (SCMV) is a majorpathogen of maize throughout sub-Saharan Africa.The disease causes chlorosis, stunting, and severeyield loss in maize.76–79 SCMV is a maize pathogenicpotyvirus and is transmitted by aphids.80 Two genes,Scm1 and Scm2, conferring resistance to SCMV havebeen identified and mapped to chromosomes 6S and 3,respectively.76,81 A number of genes conferring resis-tance to variety of pathogens have also been identifiedin these genomic regions.82–85

Maize streak virus (MSV) is also an important dis-ease of maize occurring in most sub-Saharan Africancountries. MSV is a geminivirus that is transmittedby Cicadulina spp. leafhoppers. The yield loss dueto this disease can range from close to zero to near100%.86–90 Collaborative efforts between CIMMYTand the International Institute of Tropical Agriculture(IITA) have produced a large collection of germplasmwith improved MSV resistance for the tropics; how-ever, the method of resistance is still unclear.91 Anumber of studies presenting conflicting hypothesesfor the genetic control of MSV resistance in maize havebeen published.92–98 Recently, using controlled inocu-lation procedures and population structure that couldbe replicated over time and locations, Kyetere et al.identified a single, partially dominant gene (Msv1)on chromosome 1, which confers resistance to MSVin inbred Tzi4 and a set of recombinant inbredlines (RILs) derived from Tzi4 (resistant) and Hi34(susceptible).99,100 Welz et al. identified a major QTLat the same location on chromosome 1 in CIMMYTinbred line CML202, likely allelic or identical to Msv1.Three minor QTL were also identified in the earlystage of infection, but these became non-significant atthe later stage. This may be due to declined effective-ness at later infection stages, or due to a masking effectof the major gene.101

Gray leaf spot (GLS) is a serious leaf blight problemin tropical maize. This disease is caused by the fungusCercospora zeae-maydis and is usually most severe infields with reduced or no tillage. Yield losses of over30% often occur due to the loss of leaf tissue and subse-quent lodging problems.2,102 QTL for GLS resistancehave been identified in multiple studies. However,these QTL have varied considerably between stud-ies and environments. Bubeck et al. identified QTLspanning all ten maize chromosomes.103 Both SaghiMaroof et al. and Lehmensiek et al. identified QTLat the same location on chromosomes 1 and 5. Addi-tional QTL were identified on chromosomes 2, 4, and8 by Saghi Maroof et al. and on chromosome 3 byLehmensiek et al.104,105

A number of stem borers also attack maize in Africa,including the spotted stem borer (Chilo partellus),African maize stem borer (Busseola fusca), Africanpink stem borer (Sesamia calamistis), and African sug-arcane borer (Eldana saccharina). CIMMYT has usedconventional breeding methods, recombination andrecurrent selection, to develop germplasm that is resis-tant to seven borer species.106,107 A number of studieshave mapped QTL for resistance to southwestern cornborer (SWCB).108–110 While SWCB is not a problemin Africa, SWCB resistance has been correlated withresistance to other maize borers.107,111

In addition to insects and disease, Africanagriculture also suffers greatly from the parasitic witch-weeds Striga hermonthica and S. asiatica. These weedsaffect maize, millet, and sorghum production in sub-Saharan Africa, causing over 100 million farmers tolose half of their production.112 Striga competes with



the host plant for carbon, nitrogen, and inorganicsolutes.113,114 Striga also has a phytotoxic effect onthe host within days of attachment to the roots.112–115

This lead to a reduction in height, biomass, and grainyield.114

Some tolerant varieties of maize that yield slightlybetter in the presence of Striga have been identified.These varieties produce less germination stimulantsin their root exudates, leading to fewer attachedparasites and/or later attachment of the parasites tothe root.116,117 However, parasite biomass and lossof crop yield are not linearly related, so breedingfor post-attachment resistance is likely to be amore effective form of control.114 Unfortunately, nopost-attachment resistance to Striga has been foundin cultivars of maize.117 However, post-attachmentresistance has been found in rice and sorghum,which share many syntenic genomic regions withmaize.

Haussmann et al. used two recombinant inbred line(RIL) populations for QTL mapping of regions affect-ing S. hermonthica resistance in sorghum (Sorghumbicolor (L.) Moench). The two RIL populations weredivided into two sets, and each set was grown infive environments in a single year. Five QTL werecommon across environments and years among bothsets of the two populations. One of these QTLcorresponds to the location of the low-germination-stimulant (lgs) locus, which causes low stimulationof Striga seed germination.118 In rice, a large num-ber of rice cultivars (Oryza sativa spp. japonica andindica, O. glaberrima, and wild relatives) were screenedfor post-attachment Striga resistance. A mappingpopulation of backcross inbred lines was developedusing the only strongly resistant cultivar, Nippon-bare (japonica spp.). Composite interval mappinganalysis of this population, followed by a subse-quent independent screen, revealed four confirmedQTL conferring post-attachment resistance in rice.119

These confirmed QTL in sorghum and rice maybe useful not only in marker-assisted breeding inthese crops, but also in maize and other importantgrains.120–125

BREEDING FOR ENHANCED MICRONUTRIENTCONTENTDespite the successes of the ‘Green Revolution’, bil-lions of people in the developing world still suffer

from food insecurity and malnutrition. In all devel-oping countries, 17% of people are undernourished.Sub-Saharan Africa is perhaps the worst region of theworld, with 33% of its population suffering – in centralAfrica alone, 55% of the population is undernourished(Table 4).126 Micronutrient deficiencies affect billionsof people in the developing world. Of all essentialmicronutrients, iron (Fe), zinc (Zn), iodine, and vita-min A (VA) are reported to be the most commonlydeficient micronutrients in humans.131 Micronutri-ent deficiencies severely affect one in three peopleworldwide, particularly women, children, and thepoor.132

Biofortification is the development of crops withenhanced micronutrient concentrations using eithertraditional plant breeding or biotechnology. Thisapproach is expected to have multiple benefits. First,low-income households will be implicitly targeted, asstaple crops are the most dominant part of the dietin these homes. Also, recurrent costs will be low, asthe one-time investment in research and developmentof these crops will provide nutritionally enhancedvarieties for production and consumption every year.In addition, farmers in remote areas who may havelimited access to other intervention methods can growthese crops themselves and store them for the dryseason.133,134

Micronutrient accumulation and uptake traits areinherited characteristics and should therefore beable to be improved through selective breeding,assuming that genetic variation exists.135,136 However,it is often difficult to select for micronutrientuptake characteristics due to environmental effectson plant growth and nutrient availability. Molecularmarkers are a consistent genetic property that canbe determined from analysis of plant material grownunder most conditions.135

VITAMIN AVitamin A deficiency (VAD) is one of the mostprevalent micronutrient deficiencies, particularly inAfrica, where approximately 49% of children underthe age of 5 are clinically or subclinically deficient.137

Severe VAD has a 60% fatality rate, and even sub-clinical deficiency increases preschooler mortality by23%.138 Micronutrient deficiencies also negativelyaffect aspects of human development that lower pro-ductive capacity by influencing life expectancy, cogni-tive development, work capacity, and infection rates.

Table 4. Prevalence of undernourishment and micronutrient malnutrition126–130

% of population suffering from

Undernourishment Iron deficiency anaemia VA deficiency Iodine deficiencya Risk of zinc deficiency

Africab 31 46 32 43 68Developing world 17 37 25 35 61

a Based on urinary iodine less than 100 µg/L.b Region based on World Health Organization African region.


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These effects lead to an estimated 5–10% reduction ina country’s gross domestic product (GDP), resultingfrom increased strain on social services, includinghealth care, and decreased productivity.139

Humans are unable to synthesize VA or carotenoids,some of which are VA precursors. Therefore,consumption of an appropriate diet is crucial toreceiving adequate levels of VA. Pre-formed VA comesfrom animal products such as meat and eggs. In thedeveloping world, however, the majority of VA issynthesized from carotenoids, which can be foundin many fruits and vegetables. Unfortunately, dietsconsisting of mainly staples with little meat, fish, fruit,or vegetable products are often consumed in manyregions of developing countries, leaving people proneto VAD. USAID estimates that as many as 250 millionchildren worldwide under the age of 5 suffer from VADand an additional 20 million pregnant women are alsovitamin A deficient.128,140

Using molecular marker analysis, a number ofregions in the maize genome have been identifiedthat have an influence on the concentration of totalcarotenoids and individual carotenoid compounds.Wong et al. found regions on chromosomes 6 and7 that accounted for a large portion of variation intotal carotenoids, as well as variation in the individualcarotenoid compounds lutein, zeaxanthin, β-carotene,and β-cryptoxanthin. These regions contain the genesy1 (bin 6.01), which is associated with phytoenesynthase, and vp9 (bin 7.02), which is associated withζ -carotene desaturase, both of which are involved inthe carotenoid biosynthetic pathway (Fig. 1).141 Thesegenes have also been associated with quantitativevariation of carotenoids in the Solanaceae.142 Islamalso found QTL in bin 6.01 affecting individualand total carotenoids. In both studies, a regionon chromosome 8 was associated with variationfor individual carotenoid compounds but not totalcompounds.143 The lycopene epsilon cyclase gene hasrecently been placed to the region on chromosome8 where QTL affecting levels of specific carotenoidshave been detected.144 This enzyme influences fluxdown the α-carotene branch of the pathway versusthe β-carotene branch. Islam detected an additionalregion on chromosome 9 associated with totalcarotenoids and the individual compounds lutein andzeaxanthin.143

Two additional populations have been developedin order to identify QTL affecting flux into andwithin the carotenoid biosynthetic pathway: an A619× SC55 F2:3 mapping population derived fromparents with unique carotenoid profiles, and a DEexp× CI7 F2:3 population derived from parents withvery high levels of β-carotene. These populationswere created with the intention of providing resultscomplementary to the above cited studies. Theexpected results are designed to assist in breedingfor higher levels of the provitamin A carotenoidsβ-carotene and β-cryptoxanthin (Rocheford TR,personal communication).

Phytoene

Phytofluene

ζ-carotene

GGPP

Neurosporene

Lycopene

α-carotene β-carotene

β-cryptoxanthin

Lutein Zeaxanthin

PSYy1 β-LCY

ε-LCY β-LCY

PDSvp5

ZDSvp9

Figure 1. Carotenoid biosynthetic pathway (genes in italics). GGPP,geranylgeranyl diphosphate; PSY, phytoene synthase; PDS, phytoenedesaturase; ZDS, ζ -carotene desaturase; LCY, lycopene cyclase.

However, the bioavailability of micronutrients fromVA-biofortified foods is still in question. Howeand Tanumihardjo recently conducted experimentsto determine the bioefficacy of β-carotene frombiofortified maize grain. In the first study, VA-depletedgerbils were fed diets of either 60% dark orange maizewith cottonseed oil, 60% white maize supplementedwith β-carotene in oil, 60% white maize supplementedwith VA in oil, or 60% white maize with cottonseedoil. The results of this study showed that dark orangemaize can contribute as much VA to the liver as β-carotene supplementation under depletion conditions,although both contributed less than supplemental VA.In their second study, VA-depleted gerbils were fedeither 30% or 60% maize diets of either yellow ororange grain. Resulting liver VA stores were higherin gerbils fed 60% orange maize diets than all othergroups, while gerbils fed 30% orange maize had higherhepatic VA stores than only the 30% yellow maizegroup.145 These results indicate that simply replacingwhite or yellow maize in the diet should have thedesired effect of increasing VA status in humans,although the exact benefits are still unknown.

Iron and zincIron deficiencies during childhood can impede mentaldevelopment, learning capacity, and physical growth.In adults, deficiencies reduce labor capacity.146 Insub-Saharan Africa, the incidence of iron deficiencyhas been increasing over the past 50 years.147 Zinc isessential for cellular machinery function and the healthof the whole organism. While it is difficult to diagnosezinc deficiency, it appears that deficiency reduces plantproductivity and negatively affects human health.148

Many barriers exist in breeding plants to accumulatemore micronutrient metals, such as Fe and Zn, in theiredible portions. Micronutrient uptake by the rootsmust be increased, and the micronutrients must thenbe efficiently translocated to the edible plant parts.The micronutrients must be able to accumulate andbe stored in a bioavailable form without causing harmto the plant.135,149 Kernel Fe and Zn concentrationshave been reported to be inversely correlated withgrain yield as the result of a dilution effect caused



by enhanced grain starch content. In addition, thereis some evidence of significant G×E interactions forFe and Zn concentrations in maize grain.150 Thesecharacteristics may create difficulty in breeding forenhanced levels in the grain.

Over 1800 maize samples from Mexico andZimbabwe exhibited a large degree of variation forkernel Fe and Zn concentrations, ranging from 9.6 to63.2 mg kg−1 and 12.9 to 57.6 mg kg−1, respectively.This variation was attributed to both genetic andenvironmental effects.150 In a study by Oikeh et al.,a significant component of variation in both Fe (11%)and Zn (34%) concentrations in maize grain was foundto be genetic, despite significant G×E interactions.151

Several candidate genes belonging to gene familiesof Fe and Zn transporters in maize have been identifiedusing rice genomic resources and characterized genesin other species. Molecular markers were identifiedwithin these gene sequences and may be useful infurther studies of Fe and Zn content traits.152

PERSPECTIVES FOR FUTUREMARKER-ASSISTED BREEDINGAlthough numerous QTL mapping studies haveidentified genomic regions influencing a variety oftraits of interest in maize breeding for tropicalregions, few marker-assisted breeding programs havemade use of these findings. The failure to utilizethe results of such studies is largely due to thevariable effectiveness of the markers in predictingthe desired phenotype, due to the low accuracy ofQTL studies, lack of transferability across diversegermplasm, or insufficient validation.6,15,18 However,improvements in statistical mapping software andinnovative strategies to incorporate MAS into breedingprograms may result in a larger role for MASin plant breeding.18,153–155 In addition, new high-density maps and improvement in marker technologieswill greatly increase the efficiency and effectivenessof MAS breeding programs.156–159 In combinationwith conventional breeding and continued efforts toprecisely map QTL and genes affecting importanttraits, MAS has the potential to be an effective tool infuture crop improvement for Africa and the world.

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