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TRANSCRIPT
REP O RT DN UAL CP T IF VEO BYT IOE LI
C O
O GIS S TEH ST
The International Journal of Plant Reproductive Biology 6(1) pp. 45-53, 2014
ABSTRACT
Abnormal variants in reproductive structures of Geum rivale L. (Rosaceae) are described. Structures were identified as cases of complete or partial homeosis forms on flowers and flower-bearing stems. A monopodial-rosette model of shoot formation and the existence of gynophores in the flowers facilitate their appearance. The diversity of homeosis structures was analyzed and an approach to their classification is suggested.
Keywords: Teratology, proliferation, classification, monopodial rosette-forming plants.
Homeosis Variants of Reproductive Structure Anomalies of Geum rivale L. (Rosaceae)
А.А. Notov* & E.A. Andreeva
Faculty of Biology, Department of Botany, Tver State University, 170100 Tver, Zhelyabova St. 33, 170100, RUSSIA
*e-mail: [email protected]
Received: 25.09. 2013; Accepted: 16.10.2013; Published on line: 07.12.2013
INTRODUCTION transformations may be connected with adaptation to
autogamy and indicate an expansion of adaptive
capacity (Maltsev 1905). The prevalence of
Many specimens of herbaceous Rosaceae have proliferations in Geum rivale was particularly
proven to be interesting objects for studying anomalies interesting (Krechetovich 1926, 1950, Konovalov
of reproductive structures. Widespread occurence of 1948). In case of proliferation the development of the
anomalies is conditioned by sufficient plasticity of flower-bearing stem doesn't end with the formation of a
generative organ morphogenesis in some taxa normal flower. The axis of the flower continues to grow
(Andreeva 2010, Notov & Andreeva 2011, 2013) and and forms another flower or inflorescence.
Geum rivale L. is among them. Proliferations are usually connected with morphological
Anomalous flowers and flower-bearing stems of this transformations of different elements of the flower
species were described in XIX c. (Beketov 1882). He (Krechetovich 1950). Examples of “sectorial
discovered flowers with proliferations and a double chimaeras” were also described. They combine certain
perianth (Beketov 1882). Maltsev (1905) noted the elements of calyx lobes and petals (Krechetovich 1950).
transformation of calyx lobes into leaflike structures and The cases of vegetative buds forming in axils of calyx
the elongation of the gynophores. Variations with lobes were recorded. I.N. Konovalov (1948) attempted
reduced stamens and carpels, as well as variations with to understand the mechanisms of proliferation and the
normally developed generative structures were factors that facilitate their development. The process of
identif ied. The author believes that these flower axis branching is compared with the process of
46 January, 6 (1)The International Journal of Plant Reproductive Biology 6(1) pp.45-53, 2014
of the array of developing anomalous variants may accessory bud formation. It is assumed that the increase contribute considerably to our understanding of normal in the frequency of proliferations may be connected with morphogenesis and the mechanisms of its regulation.environmental effects (mechanical impact, lack of
nutritional elements, effects of phytopathological MATERIALS & METHODSviruses). The author believes that these Geum rivale
anomalies form as a results of damage by insects and Exceptionally interesting material on the phytopathological processes.
reproductive structure anomalies of Geum rivale was Some studies mention cases of mass appearances of collected at the end of June-beginning of July of 1995. Geum rivale anomalous flowers (Gureeva & Kartashov We studied a population of Geum rivale in the area of 1982). They were recorded in the Kemerov Region in Feryazkino village, located in the Kalinisky District of habitats under high voltage power lines. Studies describe Tver Region. Totally 207 specimens from a damp cases of mass appearance of double flowers (with lowland meadow filled with wild and graminaceous number of petals up to 25), phylloid calyxes and grasses were analyzed. Ten samples had damaged apical epicalyxes, proliferate flowers and “sectorial buds. These damages were connected to nibbling by chimaeras” (Gureeva & Kartashov 1982). It has been
identified that the duration of the anomalies mouse-like rodents. This leads to an unfolding of development increases by 10-15 days. The frequency of atypical off-shoots. Buds located between the vegetative anomalies in various habitats was also revealed. The and reproductive zones started to grow, that facilitated maximum frequency is observed in marsh habitats widespread appearance of anomalies. Many located directly beneath high-voltage power lines. With proliferations were noted in the flowers, as well as the increase in distance from high-voltage power lines various chimerical structures comprised of different the frequency of terates decreased (Gureeva & flower parts (Andreeva & Notov 2008). Additional Kartashov 1982). materials on Geum rivale were collected by the authors
At the present time all necessary prerequisites for in the Tver Region in 2008-2009.the analysis of patterns in the formation of anomalous The authors attempted to systematize the identified structures have been created. The morphological basis anomalies relying on the notions of homeosis and for studying the anomaly diversity in Geum rivale has homeotic structures (Sattler 1988, 1994).been prepared by biomorphological, rhythmological and teratological studies of some herbaceous Rosaceae
RESULTS & DISCUSSION(Petukhova 1980, 2000, Chernobrova & Petukhova 1991, Notov & Glazunova 1994, Tikhomirov et al. 1995,
Organization of typical structures—It is Andreeva & Notov 2008, Andreeva 2010). The place of
impossible to correctly characterize anomalies without anomalous structures in the shoot system of plant can be analyzing biomorphology, seasonal development better identified using the concept of architectural rhythms and organization of normal structures. Geum models (Serebryakova 1977, 1983, 1987). Also, general rivale is a monopodial rosette-forming short-rhizomed studies of theoretic morphologies and development polycarpic organism (Petukhova 2000). A monopodial-genetics have appeared. They aid in identifying of rosette architectural model is typical for it morphogenetic mechanisms of anomaly formation (Serebryakova 1977, Petukhova 1980, 2000). The (Fedorov 1958, Lodkina 1977, Sattler 1988, 1994, shoots are clearly differentiated into two types: Lutova et al. 2000, 2010, Ezhova & Sklyarova 2001).vegetative and reproductive. Vegetative shoots form an However, up to the present moment there were epigeogenic rhizome that has a skeletal function and is considerable difficulties in morphological interpretation the basis for the perennial plant body. They are of many types of anomalous reproductive organs of perennial, rosette and have leaves of a medial formation. Geum rivale. The morphogenetic mechanisms of their Reproductive shoots are ephemerous and specialized. appearance are unclear. It is especially hard to classify They are represented by elongated axil flower stalks. numerous proliferation types (prolifications) that are After blooming and fructification the flower stalks die often seen in this species. Thus, additional
comprehensive studies are necessary. A detailed analysis away completely.
In the reproductive period the root system is leaves are vegetative, they don't begin to grow
represented only with adventitious roots. They form (suppression zone). Auxiliary branching of the rhizome
in nodes on the entire length of the internode at the provides for buds in the axils of “hibernating” leaves
lower side of the rhizome. Visually the root system (renewal zone). Parts of a vegetative stem which include
is fibrous and evenly fimbriate. both vegetative and generative buds comprise an
The rhizome grows monopodially. It is horizontal, elementary shoot (Petukhova 1980, 2000). Two zones
close to the surface of the ground at a depth of 0, 5–1, 5 can be identified on it: a vegetative and a generative one.
cm. Borders of yearly shoots can be found on it based on Flower stalks have 3-5 nodes, leaves and don't take
typical bends and different lengths of internodes. On root. Their internodes are elongated. Leaves on flower
each augmentation a vegetative and reproductive zone stalks are considerably smaller than rosette leaves. They
can be identified. Lateral buds within these zones give are more often whole, round and bud-like and have small
rise to vegetative shoots and flower stalks accordingly. and sharp stipule. Sometimes auxiliary locules form on
The lifetime of yearly augmentations is 4-5 years. lamina. As a rule they are smaller than the top one. The
Beginning with the basal parts the rhizome gradually leaves at the top are almost sessile and oblongish-
dies. The length of the remaining part is up to 25 cm. Due rhombic in shape. Buds do not form in the axils of most
to new unfolding shoots the rhizome branches out. An flower stalk leaves. Only in the axils of one (rarely two)
adult Geum rivale plant has a patulous system of top leaves one or two auxiliary axes ending with a flower
rhizomes. develop. The inflorescence of Geum rivale is
Leaves of a medial formation (rosette leaves) form monothelial. It can be considered an oliganthous
only on vegetative stems which become the rhizome as a cymoid.
result of the contractile function of forming adventitious The flowers are actinomorphic. The calyx is dark
roots. Leaves of vegetative stems are intermittently red; the calyx lobes are almost erect. Epicalyx lobes are
lyrate-pinnate-partite or dissected with 1-3 pairs of narrow and a lot shorter than the calyx. The petals are
auxiliaries and a large end segment. They are long light pink with dark-red veins. They are inversely egg-
petiolate and have a widened base. Leaf form and size shaped, erose at the top of the limb and narrow into an
differs within the yearly augmentation. “spring” leaves unguis at the base. The androecium consists of a lot of
are smaller than others (their length is 5 to 15 cm.), the stamens that are located at the edge of the hypanthium.
first ones have a pair of large rounded auxiliary segments The gynoecium is apocarpous and consists of a large
and a number of smaller pairs. The teeth on the edges are amount of pistils. The fruit is multiachenes. A gynophore
low and shallow. The size grows gradually and the top germinates during fruit bearing.
segment becomes singly-laminated. “summer” leaves Anomalous variants—The high frequency of
reach maximum size (20 to 40 cm in length), their edges significantly transformed flower stalks as compared to
are double or triple toothed, the teeth are large and sharp. normal ones in Geum rivale makes a separate discussion
The top segment is dissected, the auxiliary ones are of approaches to classification of anomalous structures
large, oblique, and in addition to paired ones there are necessary. The analysis of their diversity should be based
also small individual segments. The degree of partition on the understanding of the typical morphogenesis
gradually decreases. The last leaves of this series have a characteristics of the stem system and its elements.
large whole or weakly-laminated bud-like top segment Some characteristics of stem formation and flower
(sometimes also wide and inversely egg-shaped), a pair development result in a high frequency of homeotic
of auxiliary and a few mostly individual small segments. transformations.
“Hibernating” leaves have a bud-like top segment and The first unique feature is connected with the
small auxiliary segments. The first “hibernating” leaves architectural model characteristic of Geum rivale. As a
are large (20-30 cm long), but the following grow result of clear differentiation of shoots based on their
smaller. functions, lifetime and structure, the shoot system
Reproductive buds of Geum rivale form in axils of morphogenesis occurs due to the association of two
“spring” leaves (enrichment zone). Buds of “summer” different morphogenetic programs. The first ones
2014 47Anomalies Reproductive Structure of Geum rivale L.
46 January, 6 (1)The International Journal of Plant Reproductive Biology 6(1) pp.45-53, 2014
of the array of developing anomalous variants may accessory bud formation. It is assumed that the increase contribute considerably to our understanding of normal in the frequency of proliferations may be connected with morphogenesis and the mechanisms of its regulation.environmental effects (mechanical impact, lack of
nutritional elements, effects of phytopathological MATERIALS & METHODSviruses). The author believes that these Geum rivale
anomalies form as a results of damage by insects and Exceptionally interesting material on the phytopathological processes.
reproductive structure anomalies of Geum rivale was Some studies mention cases of mass appearances of collected at the end of June-beginning of July of 1995. Geum rivale anomalous flowers (Gureeva & Kartashov We studied a population of Geum rivale in the area of 1982). They were recorded in the Kemerov Region in Feryazkino village, located in the Kalinisky District of habitats under high voltage power lines. Studies describe Tver Region. Totally 207 specimens from a damp cases of mass appearance of double flowers (with lowland meadow filled with wild and graminaceous number of petals up to 25), phylloid calyxes and grasses were analyzed. Ten samples had damaged apical epicalyxes, proliferate flowers and “sectorial buds. These damages were connected to nibbling by chimaeras” (Gureeva & Kartashov 1982). It has been
identified that the duration of the anomalies mouse-like rodents. This leads to an unfolding of development increases by 10-15 days. The frequency of atypical off-shoots. Buds located between the vegetative anomalies in various habitats was also revealed. The and reproductive zones started to grow, that facilitated maximum frequency is observed in marsh habitats widespread appearance of anomalies. Many located directly beneath high-voltage power lines. With proliferations were noted in the flowers, as well as the increase in distance from high-voltage power lines various chimerical structures comprised of different the frequency of terates decreased (Gureeva & flower parts (Andreeva & Notov 2008). Additional Kartashov 1982). materials on Geum rivale were collected by the authors
At the present time all necessary prerequisites for in the Tver Region in 2008-2009.the analysis of patterns in the formation of anomalous The authors attempted to systematize the identified structures have been created. The morphological basis anomalies relying on the notions of homeosis and for studying the anomaly diversity in Geum rivale has homeotic structures (Sattler 1988, 1994).been prepared by biomorphological, rhythmological and teratological studies of some herbaceous Rosaceae
RESULTS & DISCUSSION(Petukhova 1980, 2000, Chernobrova & Petukhova 1991, Notov & Glazunova 1994, Tikhomirov et al. 1995,
Organization of typical structures—It is Andreeva & Notov 2008, Andreeva 2010). The place of
impossible to correctly characterize anomalies without anomalous structures in the shoot system of plant can be analyzing biomorphology, seasonal development better identified using the concept of architectural rhythms and organization of normal structures. Geum models (Serebryakova 1977, 1983, 1987). Also, general rivale is a monopodial rosette-forming short-rhizomed studies of theoretic morphologies and development polycarpic organism (Petukhova 2000). A monopodial-genetics have appeared. They aid in identifying of rosette architectural model is typical for it morphogenetic mechanisms of anomaly formation (Serebryakova 1977, Petukhova 1980, 2000). The (Fedorov 1958, Lodkina 1977, Sattler 1988, 1994, shoots are clearly differentiated into two types: Lutova et al. 2000, 2010, Ezhova & Sklyarova 2001).vegetative and reproductive. Vegetative shoots form an However, up to the present moment there were epigeogenic rhizome that has a skeletal function and is considerable difficulties in morphological interpretation the basis for the perennial plant body. They are of many types of anomalous reproductive organs of perennial, rosette and have leaves of a medial formation. Geum rivale. The morphogenetic mechanisms of their Reproductive shoots are ephemerous and specialized. appearance are unclear. It is especially hard to classify They are represented by elongated axil flower stalks. numerous proliferation types (prolifications) that are After blooming and fructification the flower stalks die often seen in this species. Thus, additional
comprehensive studies are necessary. A detailed analysis away completely.
In the reproductive period the root system is leaves are vegetative, they don't begin to grow
represented only with adventitious roots. They form (suppression zone). Auxiliary branching of the rhizome
in nodes on the entire length of the internode at the provides for buds in the axils of “hibernating” leaves
lower side of the rhizome. Visually the root system (renewal zone). Parts of a vegetative stem which include
is fibrous and evenly fimbriate. both vegetative and generative buds comprise an
The rhizome grows monopodially. It is horizontal, elementary shoot (Petukhova 1980, 2000). Two zones
close to the surface of the ground at a depth of 0, 5–1, 5 can be identified on it: a vegetative and a generative one.
cm. Borders of yearly shoots can be found on it based on Flower stalks have 3-5 nodes, leaves and don't take
typical bends and different lengths of internodes. On root. Their internodes are elongated. Leaves on flower
each augmentation a vegetative and reproductive zone stalks are considerably smaller than rosette leaves. They
can be identified. Lateral buds within these zones give are more often whole, round and bud-like and have small
rise to vegetative shoots and flower stalks accordingly. and sharp stipule. Sometimes auxiliary locules form on
The lifetime of yearly augmentations is 4-5 years. lamina. As a rule they are smaller than the top one. The
Beginning with the basal parts the rhizome gradually leaves at the top are almost sessile and oblongish-
dies. The length of the remaining part is up to 25 cm. Due rhombic in shape. Buds do not form in the axils of most
to new unfolding shoots the rhizome branches out. An flower stalk leaves. Only in the axils of one (rarely two)
adult Geum rivale plant has a patulous system of top leaves one or two auxiliary axes ending with a flower
rhizomes. develop. The inflorescence of Geum rivale is
Leaves of a medial formation (rosette leaves) form monothelial. It can be considered an oliganthous
only on vegetative stems which become the rhizome as a cymoid.
result of the contractile function of forming adventitious The flowers are actinomorphic. The calyx is dark
roots. Leaves of vegetative stems are intermittently red; the calyx lobes are almost erect. Epicalyx lobes are
lyrate-pinnate-partite or dissected with 1-3 pairs of narrow and a lot shorter than the calyx. The petals are
auxiliaries and a large end segment. They are long light pink with dark-red veins. They are inversely egg-
petiolate and have a widened base. Leaf form and size shaped, erose at the top of the limb and narrow into an
differs within the yearly augmentation. “spring” leaves unguis at the base. The androecium consists of a lot of
are smaller than others (their length is 5 to 15 cm.), the stamens that are located at the edge of the hypanthium.
first ones have a pair of large rounded auxiliary segments The gynoecium is apocarpous and consists of a large
and a number of smaller pairs. The teeth on the edges are amount of pistils. The fruit is multiachenes. A gynophore
low and shallow. The size grows gradually and the top germinates during fruit bearing.
segment becomes singly-laminated. “summer” leaves Anomalous variants—The high frequency of
reach maximum size (20 to 40 cm in length), their edges significantly transformed flower stalks as compared to
are double or triple toothed, the teeth are large and sharp. normal ones in Geum rivale makes a separate discussion
The top segment is dissected, the auxiliary ones are of approaches to classification of anomalous structures
large, oblique, and in addition to paired ones there are necessary. The analysis of their diversity should be based
also small individual segments. The degree of partition on the understanding of the typical morphogenesis
gradually decreases. The last leaves of this series have a characteristics of the stem system and its elements.
large whole or weakly-laminated bud-like top segment Some characteristics of stem formation and flower
(sometimes also wide and inversely egg-shaped), a pair development result in a high frequency of homeotic
of auxiliary and a few mostly individual small segments. transformations.
“Hibernating” leaves have a bud-like top segment and The first unique feature is connected with the
small auxiliary segments. The first “hibernating” leaves architectural model characteristic of Geum rivale. As a
are large (20-30 cm long), but the following grow result of clear differentiation of shoots based on their
smaller. functions, lifetime and structure, the shoot system
Reproductive buds of Geum rivale form in axils of morphogenesis occurs due to the association of two
“spring” leaves (enrichment zone). Buds of “summer” different morphogenetic programs. The first ones
2014 47Anomalies Reproductive Structure of Geum rivale L.
facilitates the formation of vegetative (skeletal) shoots, morphogenetic activity in the flower stalk axis. In
the second one facilitates the formation of flower stalks. connection with a low level of flower specialization this
Atypical auxiliary shoots can form in monopodial feature often provides for proliferations, which in turn is
rosette-forming plants as a result of “overlap” of these often connected with homeosis (Andreeva & Notov
programs or change in the place one of them “turns on”. 2008, 2009)
They combine the features of vegetative stems and The classification of anomalous structures of Geum
flower stalks to a various degree (Chernobrova & rivale can be simplified by the approach based on our
Petukhova 1991, Notov & Glazunova 1994, Tikhomirov understandings of homeosis and homeotic structures
& al. 1995, Andreeva & Notov 2008, 2009, Notov & (Sattler 1988,1994). In Geum rivale these structures may
Andreeva 2011, 2013). These shoots are sometimes be connected with different levels and elements of the
called “intermediate” (Chernobrova & Petukhova shoot system. The homeotic structures in the flower have
1991). Part of these shoots bears more resemblance to been studied in more detail. Special analyses of
flower stalks. However, leaves of a medial formation can transitional structure shoots that combine the features of
form on them, as well as sections with elongated vegetative and generative shoots are conducted very
internodal regions and axillary vegetative rosette shoots. rarely (Andreeva & Notov 2008). In these shoots the
In some cases ephemerous auxiliary roots form at the transformations may influence the elements of a lower
base of shoots. Other “intermediate” shoots bear more level (flowers, individual parts of flowers). Structures
resemblance to vegetative (skeletal) shoots. At the same that to a various extent combine elements of petals and
time their internodal regions can be elongated, leaves calyx lobes or petals and stamens are seen quite often in
may be smaller in size and less dissected as compared to the flower (Krechetovich 1926, 1950). In these cases,
typical rosette leaves. A higher frequency of these shoots researchers show incomplete homeosis (Sattler 1988,
in Geum rivale is a result of rather intense branching of 1994).
the rhizome. In Geum rivale, as opposed to other Some types of proliferations in Geum rivale are also
monopoid rosette-forming plants, the unfolding of new connected with the formation of transitionallly
vegetative shoots becomes regular. Various structured shoots (Chernobrova & Petukhova 1991,
“malfunctions” in the morphogenesis of shoots are also Notov & Glazunova 1994, Tikhomirov et al. 1995). As a
facilitated by a peculiar rhythm of seasonal rule they form at the border between vegetative and
development. A discrepancy between yearly and generative zones of the maternal skeletal axis. In this
elementary shoots has been identified in Geum rivale case, the probability of “overlap” of morphogenetic
(Petukhova 1980, 2000). The unfolding of flower stalks programs increases. The results of the malfunction in the
from generative buds that have formed in leaf axils of morphogenesis are transitional shoots that represent a
yearly augmentations occurs only in the spring of the type of incomplete homeosis. The frequency of these
following year. These features facilitate regular anomalies increases in case of damage to the apical buds
realization of morphogenetic processes connected with of vegetative shoots. The same effect occurs in cases of
both the formation of vegetative and generative shoots. phytopathogenic abnormalities (Maltsev 1905,
It increases the possibility of probable “overlap” of Konovalov 1948, Gureeva & Kartashov 1982).
morphogenetic programs. The “transitional” shoots that Structures that to a various extent combine elements of
develop at this point can be seen as structures with petals and calyx lobes or petals and stamens are seen
incomplete homeosis (Andreeva & Notov 2008, 2009). quite often in the flower (Krechetovich 1926, 1950). In
As a rule they appear from buds located at the boundary these cases researchers refer to incomplete homeosis
between the vegetative and generative zones. (Sattler 1988, 1994).
The second prerequisite for the formation of The diversity of homeotic structures is well
anomalies is the development of a gynophore in Geum illustrated by the material collected by the authors in
rivale. It forms at the fruiting stage and facilitates the 1995 near the Feryazkino village. As a result of damage
removal of fruits outside of the calyx. The functioning of to apical buds atypical auxiliary shoots formed on ten
the gynophores is connected with the prolongation of samples (Figs. 1 & 2). The wide distribution of
anomalies is a result of bud growth on the border formation (Fig. 1 A-D, Fig. 2). A number of flower stalks between the vegetative and the generative zones. with a rosette area at the base have been noted among
The authors identified types of generative shoots them. Leaves of medial formation, which in their with some features of skeletal shoots. Usually they are structure were identical to rosette leaves of a skeletal flower stalks with large petiolate leaves of a medial shoot formed in the rosette areas with short internodal
Fig. 1—The structure of the flower stalks of Geum rivale (samples 1, 2, 4, 7, vicinity of the village of Feryazkino, July 1995)
(A) (B)
(C) (D)
2014 49Anomalies Reproductive Structure of Geum rivale L. 48 January, 6 (1)The International Journal of Plant Reproductive Biology 6(1) pp.45-53, 2014
facilitates the formation of vegetative (skeletal) shoots, morphogenetic activity in the flower stalk axis. In
the second one facilitates the formation of flower stalks. connection with a low level of flower specialization this
Atypical auxiliary shoots can form in monopodial feature often provides for proliferations, which in turn is
rosette-forming plants as a result of “overlap” of these often connected with homeosis (Andreeva & Notov
programs or change in the place one of them “turns on”. 2008, 2009)
They combine the features of vegetative stems and The classification of anomalous structures of Geum
flower stalks to a various degree (Chernobrova & rivale can be simplified by the approach based on our
Petukhova 1991, Notov & Glazunova 1994, Tikhomirov understandings of homeosis and homeotic structures
& al. 1995, Andreeva & Notov 2008, 2009, Notov & (Sattler 1988,1994). In Geum rivale these structures may
Andreeva 2011, 2013). These shoots are sometimes be connected with different levels and elements of the
called “intermediate” (Chernobrova & Petukhova shoot system. The homeotic structures in the flower have
1991). Part of these shoots bears more resemblance to been studied in more detail. Special analyses of
flower stalks. However, leaves of a medial formation can transitional structure shoots that combine the features of
form on them, as well as sections with elongated vegetative and generative shoots are conducted very
internodal regions and axillary vegetative rosette shoots. rarely (Andreeva & Notov 2008). In these shoots the
In some cases ephemerous auxiliary roots form at the transformations may influence the elements of a lower
base of shoots. Other “intermediate” shoots bear more level (flowers, individual parts of flowers). Structures
resemblance to vegetative (skeletal) shoots. At the same that to a various extent combine elements of petals and
time their internodal regions can be elongated, leaves calyx lobes or petals and stamens are seen quite often in
may be smaller in size and less dissected as compared to the flower (Krechetovich 1926, 1950). In these cases,
typical rosette leaves. A higher frequency of these shoots researchers show incomplete homeosis (Sattler 1988,
in Geum rivale is a result of rather intense branching of 1994).
the rhizome. In Geum rivale, as opposed to other Some types of proliferations in Geum rivale are also
monopoid rosette-forming plants, the unfolding of new connected with the formation of transitionallly
vegetative shoots becomes regular. Various structured shoots (Chernobrova & Petukhova 1991,
“malfunctions” in the morphogenesis of shoots are also Notov & Glazunova 1994, Tikhomirov et al. 1995). As a
facilitated by a peculiar rhythm of seasonal rule they form at the border between vegetative and
development. A discrepancy between yearly and generative zones of the maternal skeletal axis. In this
elementary shoots has been identified in Geum rivale case, the probability of “overlap” of morphogenetic
(Petukhova 1980, 2000). The unfolding of flower stalks programs increases. The results of the malfunction in the
from generative buds that have formed in leaf axils of morphogenesis are transitional shoots that represent a
yearly augmentations occurs only in the spring of the type of incomplete homeosis. The frequency of these
following year. These features facilitate regular anomalies increases in case of damage to the apical buds
realization of morphogenetic processes connected with of vegetative shoots. The same effect occurs in cases of
both the formation of vegetative and generative shoots. phytopathogenic abnormalities (Maltsev 1905,
It increases the possibility of probable “overlap” of Konovalov 1948, Gureeva & Kartashov 1982).
morphogenetic programs. The “transitional” shoots that Structures that to a various extent combine elements of
develop at this point can be seen as structures with petals and calyx lobes or petals and stamens are seen
incomplete homeosis (Andreeva & Notov 2008, 2009). quite often in the flower (Krechetovich 1926, 1950). In
As a rule they appear from buds located at the boundary these cases researchers refer to incomplete homeosis
between the vegetative and generative zones. (Sattler 1988, 1994).
The second prerequisite for the formation of The diversity of homeotic structures is well
anomalies is the development of a gynophore in Geum illustrated by the material collected by the authors in
rivale. It forms at the fruiting stage and facilitates the 1995 near the Feryazkino village. As a result of damage
removal of fruits outside of the calyx. The functioning of to apical buds atypical auxiliary shoots formed on ten
the gynophores is connected with the prolongation of samples (Figs. 1 & 2). The wide distribution of
anomalies is a result of bud growth on the border formation (Fig. 1 A-D, Fig. 2). A number of flower stalks between the vegetative and the generative zones. with a rosette area at the base have been noted among
The authors identified types of generative shoots them. Leaves of medial formation, which in their with some features of skeletal shoots. Usually they are structure were identical to rosette leaves of a skeletal flower stalks with large petiolate leaves of a medial shoot formed in the rosette areas with short internodal
Fig. 1—The structure of the flower stalks of Geum rivale (samples 1, 2, 4, 7, vicinity of the village of Feryazkino, July 1995)
(A) (B)
(C) (D)
2014 49Anomalies Reproductive Structure of Geum rivale L. 48 January, 6 (1)The International Journal of Plant Reproductive Biology 6(1) pp.45-53, 2014
The spectrum of morphological types turned out to regions (Fig. 1A, 2). In one case ephemerous auxiliary be very broad, that complicates the developing of roots were found on these rosette regions (Fig. 2). In a anomalies classification. Due to the fact that in many number of cases vegetative buds have formed and started cases different examples of homeosis were found, the to unfold on flower stalks. Rosette shoots with long classification was based on the homeosis concept. petiolate leaves started to form from these buds (Fig. 1A, Diversity of homeotic structures should be systematized B, Fig. 2). As a result, some elements characteristic of based on our understanding of the replacement structure skeletal shoots were noted on the studied anomalous type and the degree of its concordance with the normal flower stalks. Among them are adventitious roots, structure of this type (Notov 1996, Andreeva & Notov rosette areas, axillary shoots, and long petiolate leaves 2008, Notov & Andreeva 2011, 2013). The last feature is with a large lamina (Fig. 2).connected with identifying of complete and partial In many cases proliferations were found on homeosis types. This approach was used during the
anomalous generative shoots (Figs. 1 & 2) (Andreeva & design of Table 1. In this diagram we also tried to take
Notov 2008). As a rule they were connected with the into account the theoretically possible types and identify
formation of various chimerical structures. These the main logical restrictions.
structures included elements of various flower parts In addition to various cases of complete homeosis
(Figs. 1 & 2). Different types of petals with fragments of (carpels, petals and stamens on the axis of a proliferating
calyx lobes and calyx lobes with petal-like appendixes flower stalk, carpels in the corolla area) different types of
(Fig. 1A,B,D), petals with anthers (Fig. 1B), and partial homeosis are also mentioned (structures that to stamens with fragments of petals (Fig. 1C) have been some degree combined features of leaves of medial identified. Such structures represent cases of incomplete formation, leaflets of the epicalyx, calyx lobes, petals homeosis. Examples of partial homeosis are carpels, and calyx lobes, stamens and petals) (Table 1). petals and stamens on the axis of a proliferating flower Characteristics of the flower stalk elements and skeletal stalk; carpels in the corolla area; calyx lobes in the form shoots may be combined at various levels of auxiliary of leaves of medial formation; leaf-like pistils (Fig. 1 B, shoots. This diagram can also be useful when searching C, D, Fig.2). for currently unidentified anomalies.
Fig. 2—Some types of anomalies of the reproductive structures of Geum rivale: А – flower-bearing stem of a normal
structure; * – proliferate flowers; ▼ – homeotic structures that combine different flower elements (B); the flower-bearing stem of a normal structure is in the box.
(A)
(B)
Tab
le 1
– T
he
div
ersi
ty o
f h
om
eoti
c st
ruct
ure
s of
Geu
m r
ival
e:
– l
ogi
call
y i
mp
oss
ible
ty
pes
; ?
– p
oss
ible
ty
pes
th
at
ha
ven
't y
et b
een
iden
tifi
ed;
SH
– s
hoo
t; [
] –
exa
mp
les
if i
nco
mp
lete
ho
meo
sis
A r
epla
cem
ent
stru
ctu
re o
r it
s el
emen
ts t
hat
dev
elop
s w
ith
in a
typ
ical
pat
tern
Typ
ical
stru
ctu
re(s
kele
tal)
sho
ots
×
vege
tati
ve
flo
wer
sta
lk
flow
erre
cept
acle
epic
alyx
lob
eca
lyx
lobe
pe
tal
st
amen
c
arpe
l
Veg
etat
ive
(ske
leta
l) s
hoo
ts
(VS
)
Flo
wer
sta
lk(I
nflo
resc
ence
)(F
S)
Flo
wer
(F
)
Rec
epta
cle
(R)
Epi
caly
x lo
be
(EL
)
Cal
yx l
obe
(CL
)
Pet
al(P
C)
Sta
men
(S
)
Car
pel
(C)
skel
etal
SH
in
the
vege
tati
ve
zone
[gen
erat
ive
SH
of
int
erm
edia
te
stru
ctur
e]
× × [EL
in
the
form
of
a l
eaf
of
med
ial
form
atio
n]
[CL
in
the
form
of
a l
eaf
of
med
ial
form
atio
n]
× × [lea
flik
e C
]
FS
in
vege
tati
ve
zone
[on
the
bord
e r o
f tw
o zo
nes]
[VS
int
erm
edia
te
stru
ctur
e]
FS
on
the
site
of
F[F
wit
h el
emen
ts F
S
FS
on
the
site
of
R [
F w
ith
elem
ents
F
S]
[EL
in
the
form
of
a le
af o
f to
p fo
rmat
ion]
[CL
in
the
form
of
a le
af o
f to
p fo
rmat
ion]
? ? . [lea
flik
e C
]
× × [R w
ith
flow
er]
× × × × ?
× × × × × × × ×
× [lea
f of
top
fo
rmat
ion
in
the
form
of
EL
]
× × EL
ins
tead
of
CL
[CL
wit
h el
emen
ts o
f L
E]
[PT
wit
hfr
agm
ents
of
LE
]
× ×
× [lea
f of
top
fo
rmat
ion
in
the
form
of
EL
]
× ? CL
in
plac
e of
EL
[EL
wit
h fr
agm
ents
of
CL
]
[PT
wit
hfr
agm
ents
of
CL
]
CL
in
plac
e of
S
CL
-lik
e C
× PT
in
the
axil
of
a le
af o
f to
p fo
rmat
ion
[lea
f of
top
fo
rmat
ion
in t
he
form
of
PT
]× × P
T i
n pl
ace
of E
L
[EL
wit
h fr
agm
ents
of
PT
]
PT
in
plac
e of
CL
[C
L w
ith
frag
men
ts
of P
T)
[S w
ith
PT
-lik
e ou
tgro
wth
s]
PT
in
plac
e of
C
× S i
n th
e ax
il o
f a
lea
f
of
to
p
form
atio
n [S
on
FS
]
× × ? S i
n pl
ace
of C
L
[CL
wit
hfr
agm
ents
of S
]
S in
pla
ce o
f PT
[S
wit
h P
T-l
ike
outg
row
ths]
?
× × × × × ? ? ?
2014 51Anomalies Reproductive Structure of Geum rivale L. 50 January, 6 (1)The International Journal of Plant Reproductive Biology 6(1) pp.45-53, 2014
The spectrum of morphological types turned out to regions (Fig. 1A, 2). In one case ephemerous auxiliary be very broad, that complicates the developing of roots were found on these rosette regions (Fig. 2). In a anomalies classification. Due to the fact that in many number of cases vegetative buds have formed and started cases different examples of homeosis were found, the to unfold on flower stalks. Rosette shoots with long classification was based on the homeosis concept. petiolate leaves started to form from these buds (Fig. 1A, Diversity of homeotic structures should be systematized B, Fig. 2). As a result, some elements characteristic of based on our understanding of the replacement structure skeletal shoots were noted on the studied anomalous type and the degree of its concordance with the normal flower stalks. Among them are adventitious roots, structure of this type (Notov 1996, Andreeva & Notov rosette areas, axillary shoots, and long petiolate leaves 2008, Notov & Andreeva 2011, 2013). The last feature is with a large lamina (Fig. 2).connected with identifying of complete and partial In many cases proliferations were found on homeosis types. This approach was used during the
anomalous generative shoots (Figs. 1 & 2) (Andreeva & design of Table 1. In this diagram we also tried to take
Notov 2008). As a rule they were connected with the into account the theoretically possible types and identify
formation of various chimerical structures. These the main logical restrictions.
structures included elements of various flower parts In addition to various cases of complete homeosis
(Figs. 1 & 2). Different types of petals with fragments of (carpels, petals and stamens on the axis of a proliferating
calyx lobes and calyx lobes with petal-like appendixes flower stalk, carpels in the corolla area) different types of
(Fig. 1A,B,D), petals with anthers (Fig. 1B), and partial homeosis are also mentioned (structures that to stamens with fragments of petals (Fig. 1C) have been some degree combined features of leaves of medial identified. Such structures represent cases of incomplete formation, leaflets of the epicalyx, calyx lobes, petals homeosis. Examples of partial homeosis are carpels, and calyx lobes, stamens and petals) (Table 1). petals and stamens on the axis of a proliferating flower Characteristics of the flower stalk elements and skeletal stalk; carpels in the corolla area; calyx lobes in the form shoots may be combined at various levels of auxiliary of leaves of medial formation; leaf-like pistils (Fig. 1 B, shoots. This diagram can also be useful when searching C, D, Fig.2). for currently unidentified anomalies.
Fig. 2—Some types of anomalies of the reproductive structures of Geum rivale: А – flower-bearing stem of a normal
structure; * – proliferate flowers; ▼ – homeotic structures that combine different flower elements (B); the flower-bearing stem of a normal structure is in the box.
(A)
(B)
Tab
le 1
– T
he
div
ersi
ty o
f h
om
eoti
c st
ruct
ure
s of
Geu
m r
ival
e:
– l
ogi
call
y i
mp
oss
ible
ty
pes
; ?
– p
oss
ible
ty
pes
th
at
ha
ven
't y
et b
een
iden
tifi
ed;
SH
– s
hoo
t; [
] –
exa
mp
les
if i
nco
mp
lete
ho
meo
sis
A r
epla
cem
ent
stru
ctu
re o
r it
s el
emen
ts t
hat
dev
elop
s w
ith
in a
typ
ical
pat
tern
Typ
ical
stru
ctu
re(s
kele
tal)
sho
ots
×
vege
tati
ve
flo
wer
sta
lk
flow
erre
cept
acle
epic
alyx
lob
eca
lyx
lobe
pe
tal
st
amen
c
arpe
l
Veg
etat
ive
(ske
leta
l) s
hoo
ts
(VS
)
Flo
wer
sta
lk(I
nflo
resc
ence
)(F
S)
Flo
wer
(F
)
Rec
epta
cle
(R)
Epi
caly
x lo
be
(EL
)
Cal
yx l
obe
(CL
)
Pet
al(P
C)
Sta
men
(S
)
Car
pel
(C)
skel
etal
SH
in
the
vege
tati
ve
zone
[gen
erat
ive
SH
of
int
erm
edia
te
stru
ctur
e]
× × [EL
in
the
form
of
a l
eaf
of
med
ial
form
atio
n]
[CL
in
the
form
of
a l
eaf
of
med
ial
form
atio
n]
× × [lea
flik
e C
]
FS
in
vege
tati
ve
zone
[on
the
bord
e r o
f tw
o zo
nes]
[VS
int
erm
edia
te
stru
ctur
e]
FS
on
the
site
of
F[F
wit
h el
emen
ts F
S
FS
on
the
site
of
R [
F w
ith
elem
ents
F
S]
[EL
in
the
form
of
a le
af o
f to
p fo
rmat
ion]
[CL
in
the
form
of
a le
af o
f to
p fo
rmat
ion]
? ? . [lea
flik
e C
]
× × [R w
ith
flow
er]
× × × × ?
× × × × × × × ×
× [lea
f of
top
fo
rmat
ion
in
the
form
of
EL
]
× × EL
ins
tead
of
CL
[CL
wit
h el
emen
ts o
f L
E]
[PT
wit
hfr
agm
ents
of
LE
]
× ×
× [lea
f of
top
fo
rmat
ion
in
the
form
of
EL
]
× ? CL
in
plac
e of
EL
[EL
wit
h fr
agm
ents
of
CL
]
[PT
wit
hfr
agm
ents
of
CL
]
CL
in
plac
e of
S
CL
-lik
e C
× PT
in
the
axil
of
a le
af o
f to
p fo
rmat
ion
[lea
f of
top
fo
rmat
ion
in t
he
form
of
PT
]× × P
T i
n pl
ace
of E
L
[EL
wit
h fr
agm
ents
of
PT
]
PT
in
plac
e of
CL
[C
L w
ith
frag
men
ts
of P
T)
[S w
ith
PT
-lik
e ou
tgro
wth
s]
PT
in
plac
e of
C
× S i
n th
e ax
il o
f a
lea
f
of
to
p
form
atio
n [S
on
FS
]
× × ? S i
n pl
ace
of C
L
[CL
wit
hfr
agm
ents
of S
]
S in
pla
ce o
f PT
[S
wit
h P
T-l
ike
outg
row
ths]
?
× × × × × ? ? ?
2014 51Anomalies Reproductive Structure of Geum rivale L. 50 January, 6 (1)The International Journal of Plant Reproductive Biology 6(1) pp.45-53, 2014
CONCLUSION Society of Naturalists 12(2). St. Petersburg Pp. 290-295.
[In Russian]To conclude, structures that can be identified as
cases of complete and partial homeosis are often formed Chernobrova OB & Petukhova LV 1991 Special cases of on the flower stalks of Geum rivale. Their emergence is lateral branching monopodial rosette-forming In: Flora facilitated by the monopodially-rosette model of shoot and vegetation of the southern taiga. Tver State formation and sufficient regularity in the unfolding of University, Tver Pp. 96-99. [In Russian]auxiliary vegetative (skeletal) shoots. The connection of two different morphogenetic programs during the
Ezhova TA & Sklyarova OA 2001 Genes controlling process of morphogenesis of the shoot system increases
inflorescence structure and their possible role in the possibility of possible “overlap” or alteration of the
evolution. Ontogenesis 32(6) 462-470. [In Russian]place one of them “turns on”. Proliferation is made easier by the existence of a gynophores and a rather low
Fedorov AA 1958 Teratology and morphogenesis in level of flower specialization. The possibility of plants. AN SSSR, Moscow, Leningrad. [In Russian]anomalies increases in case of forming of auxiliary
shoots from buds with initiation at the boundary between Gureeva II & Kartashov AG 1982 Cases of mass the vegetative and generative zones.teratology changes flowers of Geum rivale L. and Morphological types of homeotic anomalies of inflorescences of Inula salicina L. Ecology 6 64-68. Geum rivale are quite diverse. Their classification
should be based on the notions of replacement structure Konovalov IN 1948 Materials for the clarification of the type and the degree of its corresponding to the normal
structure of this type. The last feature is connected with morphological the essence of things prolification 1. On identifying of variant of complete and partial homeosis. the mechanism of prolification and conditions of its The suggested classification diagram may be useful for occurrence Bot. Zhurn 33(5) 496-509. [In Russian]searching for currently unidentified anomalies.
Acknowledgements — The authors are grateful to Mr. Krechetovich LM 1926 The teratology of the flowers of A.V. Serebryanaya for the translation of the text into Geum rivale In: Dnevnik Vsesoyuznogo sezda English. botanikov. Moscow Pp. 107-109.
LITERATURE CITED Krechetovich LM 1950 Flower of angiosperms Bjull.
Mosk. Obsch. Ispyt. Prir., otd. biol. 40(4) 28-40. [In Andreeva ЕА 2010 Anomalies of generative sphere
Russian]some monopodial rosette-forming herbaceous
Rosaceae. Ph.D. Thesis, Moscow. [In Russian] Kuznetsova TV, Pryakhina NI & Yakovlev GP 1992
Inflorescences: morphological classification. SPCPA Andreeva ЕА & Notov AA 2008 Homeosis varieties of
Press, St. Petersburg. [In Russian] anomalous generative structures of Geum rivale L.
Vestnik TGU. Ser. Biology & Ecology. 10(31/91) 143-Lodkina MM 1977 The teratology of a flower, the 146. [In Russian]morphological nature of its bodies and the problem of
the homology groups from the point of view of Andreeva ЕА & Notov AA 2009 Abnormal variants of developmental genetics. Bot. Zhurn. 62(12) 1731–1741. generative structures in monopodial rosette-forming [In Russian]Rosaceae. Vestnik TGU. Ser. Biology & Ecology. 15(34)
146-154. [In Russian]Lutova LA, Ezhova TA, Dodueva IE, Tikhanovich IA,
Khodaiova LT & Shishkova SO 2000 Genetics of plant Beketov A 1882 Ugly flowers of Geum intermedium and development. Nauka, St. Petersburg. [In Russian]Geum rivale In: Proceedings St. Petersburg of the
Lutova LA, Provorov NA, Tichodeev ON & Osipova the family Rosaceae. Ph.D. Thesis, Moscow. [In MA 2010 Genetics of plant development. N-L, St. Russian]Petersburg. [In Russian]
Petukhova LV 2000 Geum rivale. In: Biological flora Maltsev S 1905 Ugly flowers of Geum rivale In: Works of Moscow region. Vol. 14. Grif & К°, Moscow. Pp. of the Botanical garden of Yuriev University. Vol. 5. 128-142.Yuriev Pp. 162-164.
Sattler R 1988 Homeosis in plants. Am. J. Bot. 75 Notov AA & Andreeva EA 2011 On the approach to 1606–1617.classification of generative structures anomalies of
monopodial rosette-forming Rosaceae. Vestnik TGU. Sattler R. 1994 Homology, homeosis, and process Ser. Biology and Ecology. 24(32) 93–104. [In Russian] morphology in plants. In: Hall BK (ed.) Homology: the
hierarchical basis of comparative biology copyright. Notov AA & Andreeva EA 2013 Classification of Academic Press, New York Pp. 423–475.generative structure anomalies of monopodial rosette-
forming Rosaceae Int. J. Plant Rep. Bio. 5(2) 1-14. Serebryakova TI 1977 On the main «architectural
models» of herbaceous perennials and modi of their Notov AA & Glazunona KP 1994 A preliminary transformation. Bjull. Mosk. Obsch. Ispyt. Prir., otd. classification of abnormal flower and flower stalk Biol. 82(5) 112–128. [In Russian]structures in Alchemilla species of Middle Russia In:
Flora and vegetation of Tver region Tver. Univ. Press, Serebryakova TI 1983 On some modes of structural Tver Pp. 45–63. [In Russian] evolution in flowering plants. Zhurn. Obshchei Biol.
44(5) 579–593. [In Russian]Notov AA 1996. On the role of homeosis
transformations in the evolution of plants In:The Serebryakova TI 1987 The variants of models of shoot th9 Moscow meeting on the phylogeny of plants. formation in perennial herbs In: Morphogenesis and
Moskowskoe Obschestvo Ispytateley Prirody, rhythms of the development of higher plants. MPGU, Department of higher plants of the biological faculty of Moscow Pp. 3–19. [In Russian]Moscow State University, Moscow. Pp. 100-104. [In
Russian] Tikhomirov VN, Notov AA, Petukhova LV &
Glazunova KP 1995 Genus Aichemilla In: Biological Petukhova LV 1980 Comparative morphological study flora of Moscow region. Vol. 10. Argus, Moscow. Pp. of life forms some monopodial rosette-forming plants of 83-119.
52 January, 6 (1)The International Journal of Plant Reproductive Biology 6(1) pp.45-53, 2014 2014 53Anomalies Reproductive Structure of Geum rivale L.
CONCLUSION Society of Naturalists 12(2). St. Petersburg Pp. 290-295.
[In Russian]To conclude, structures that can be identified as
cases of complete and partial homeosis are often formed Chernobrova OB & Petukhova LV 1991 Special cases of on the flower stalks of Geum rivale. Their emergence is lateral branching monopodial rosette-forming In: Flora facilitated by the monopodially-rosette model of shoot and vegetation of the southern taiga. Tver State formation and sufficient regularity in the unfolding of University, Tver Pp. 96-99. [In Russian]auxiliary vegetative (skeletal) shoots. The connection of two different morphogenetic programs during the
Ezhova TA & Sklyarova OA 2001 Genes controlling process of morphogenesis of the shoot system increases
inflorescence structure and their possible role in the possibility of possible “overlap” or alteration of the
evolution. Ontogenesis 32(6) 462-470. [In Russian]place one of them “turns on”. Proliferation is made easier by the existence of a gynophores and a rather low
Fedorov AA 1958 Teratology and morphogenesis in level of flower specialization. The possibility of plants. AN SSSR, Moscow, Leningrad. [In Russian]anomalies increases in case of forming of auxiliary
shoots from buds with initiation at the boundary between Gureeva II & Kartashov AG 1982 Cases of mass the vegetative and generative zones.teratology changes flowers of Geum rivale L. and Morphological types of homeotic anomalies of inflorescences of Inula salicina L. Ecology 6 64-68. Geum rivale are quite diverse. Their classification
should be based on the notions of replacement structure Konovalov IN 1948 Materials for the clarification of the type and the degree of its corresponding to the normal
structure of this type. The last feature is connected with morphological the essence of things prolification 1. On identifying of variant of complete and partial homeosis. the mechanism of prolification and conditions of its The suggested classification diagram may be useful for occurrence Bot. Zhurn 33(5) 496-509. [In Russian]searching for currently unidentified anomalies.
Acknowledgements — The authors are grateful to Mr. Krechetovich LM 1926 The teratology of the flowers of A.V. Serebryanaya for the translation of the text into Geum rivale In: Dnevnik Vsesoyuznogo sezda English. botanikov. Moscow Pp. 107-109.
LITERATURE CITED Krechetovich LM 1950 Flower of angiosperms Bjull.
Mosk. Obsch. Ispyt. Prir., otd. biol. 40(4) 28-40. [In Andreeva ЕА 2010 Anomalies of generative sphere
Russian]some monopodial rosette-forming herbaceous
Rosaceae. Ph.D. Thesis, Moscow. [In Russian] Kuznetsova TV, Pryakhina NI & Yakovlev GP 1992
Inflorescences: morphological classification. SPCPA Andreeva ЕА & Notov AA 2008 Homeosis varieties of
Press, St. Petersburg. [In Russian] anomalous generative structures of Geum rivale L.
Vestnik TGU. Ser. Biology & Ecology. 10(31/91) 143-Lodkina MM 1977 The teratology of a flower, the 146. [In Russian]morphological nature of its bodies and the problem of
the homology groups from the point of view of Andreeva ЕА & Notov AA 2009 Abnormal variants of developmental genetics. Bot. Zhurn. 62(12) 1731–1741. generative structures in monopodial rosette-forming [In Russian]Rosaceae. Vestnik TGU. Ser. Biology & Ecology. 15(34)
146-154. [In Russian]Lutova LA, Ezhova TA, Dodueva IE, Tikhanovich IA,
Khodaiova LT & Shishkova SO 2000 Genetics of plant Beketov A 1882 Ugly flowers of Geum intermedium and development. Nauka, St. Petersburg. [In Russian]Geum rivale In: Proceedings St. Petersburg of the
Lutova LA, Provorov NA, Tichodeev ON & Osipova the family Rosaceae. Ph.D. Thesis, Moscow. [In MA 2010 Genetics of plant development. N-L, St. Russian]Petersburg. [In Russian]
Petukhova LV 2000 Geum rivale. In: Biological flora Maltsev S 1905 Ugly flowers of Geum rivale In: Works of Moscow region. Vol. 14. Grif & К°, Moscow. Pp. of the Botanical garden of Yuriev University. Vol. 5. 128-142.Yuriev Pp. 162-164.
Sattler R 1988 Homeosis in plants. Am. J. Bot. 75 Notov AA & Andreeva EA 2011 On the approach to 1606–1617.classification of generative structures anomalies of
monopodial rosette-forming Rosaceae. Vestnik TGU. Sattler R. 1994 Homology, homeosis, and process Ser. Biology and Ecology. 24(32) 93–104. [In Russian] morphology in plants. In: Hall BK (ed.) Homology: the
hierarchical basis of comparative biology copyright. Notov AA & Andreeva EA 2013 Classification of Academic Press, New York Pp. 423–475.generative structure anomalies of monopodial rosette-
forming Rosaceae Int. J. Plant Rep. Bio. 5(2) 1-14. Serebryakova TI 1977 On the main «architectural
models» of herbaceous perennials and modi of their Notov AA & Glazunona KP 1994 A preliminary transformation. Bjull. Mosk. Obsch. Ispyt. Prir., otd. classification of abnormal flower and flower stalk Biol. 82(5) 112–128. [In Russian]structures in Alchemilla species of Middle Russia In:
Flora and vegetation of Tver region Tver. Univ. Press, Serebryakova TI 1983 On some modes of structural Tver Pp. 45–63. [In Russian] evolution in flowering plants. Zhurn. Obshchei Biol.
44(5) 579–593. [In Russian]Notov AA 1996. On the role of homeosis
transformations in the evolution of plants In:The Serebryakova TI 1987 The variants of models of shoot th9 Moscow meeting on the phylogeny of plants. formation in perennial herbs In: Morphogenesis and
Moskowskoe Obschestvo Ispytateley Prirody, rhythms of the development of higher plants. MPGU, Department of higher plants of the biological faculty of Moscow Pp. 3–19. [In Russian]Moscow State University, Moscow. Pp. 100-104. [In
Russian] Tikhomirov VN, Notov AA, Petukhova LV &
Glazunova KP 1995 Genus Aichemilla In: Biological Petukhova LV 1980 Comparative morphological study flora of Moscow region. Vol. 10. Argus, Moscow. Pp. of life forms some monopodial rosette-forming plants of 83-119.
52 January, 6 (1)The International Journal of Plant Reproductive Biology 6(1) pp.45-53, 2014 2014 53Anomalies Reproductive Structure of Geum rivale L.