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Floral monosymmetry, which is conspicuous and prominent

in many angiosperms, has attracted much attention fromboth developmental geneticists and pollination biologists.

A combined evolutionary biological approach to studying floral

monosymmetry in the Lamiales, the order that contains the

model plant Antirrhinum, is just beginning to take shape. In

contrast, floral leftright asymmetry has largely been neglected,

although it is much in discussion in animal biology, probably

because in flowers (unlike in animals) leftright asymmetry is

not predominant. Nevertheless, there are patterns in the

evolution of floral leftright asymmetry that are interesting

enough to be addressed by developmental genetics. These are

the direction of contortion in flowers with contort petal

aestivation, and the direction of deflection of pollination organs

in groups with enantiostylous flowers or in some groups with

enclosed pollination organs, such as beans (Phaseolinae,

Fabaceae) or louseworts (Pedicularis, Orobanchaceae).

AddressesInstitute of Systematic Botany, University of Zurich, Zollikerstrasse 107,8008 Zurich, Switzerland; e-mail: [email protected]

Current Opinion in Plant Biology 2001, 4 :8691

1369-5266/01/$ see front matter 2001 Elsevier Science Ltd. All rights reserved.

IntroductionFloral symmetry is not only aesthetically attractive but is ofeminent biological significance. Research into symmetry in

plants has attracted much attention over the past few years

and is being approached from different directions [1,2,3].

In this review, I distinguish three kinds of symmetry: poly-

symmetry (i.e. actinomorphy, with several symmetry

planes), monosymmetry (i.e. zygomorphy, with one sym-

metry plane), and asymmetry (i.e. without any symmetry

plane) (Figure 1). In most of the recent publications, only

polysymmetry and monosymmetry are discussed, and are

referred to as symmetry and asymmetry, respectively [4,5].

Thus, the term asymmetry has not always been used in the

same sense. The development of monosymmetry is beinginvestigated using molecular developmental genetics, start-

ing with the model plant Antirrhinum [1,68]. The

significance of monosymmetric flowers is also being stud-

ied from the point of view of pollination biology

[911,12,13]. Another kind of symmetry in flowers is

leftright asymmetry (i.e. enantiomorphy: with left and

right morphs). The developmental biology of leftright

asymmetry is being intensively studied in animals [14] but,

as yet, has attracted little attention in plants apart from

some studies on pollination biology. Some evolutionary

aspects of floral leftright asymmetry were, however, dis-

cussed recently [15,16]. InArabidopsis, tortifolia mutants

produce leftright asymmetry in petioles by twisted growth

[17]. This seems to be the only example in which leftright

asymmetry in plants has been addressed from a molecular

developmental point of view.

Evolution of floral monosymmetryFrom our knowledge of angiosperm fossil history and phy-

logeny, we know that polysymmetric flowers predated

monosymmetric flowers; the first clearly monosymmetric

flowers are known from the Upper Cretaceous (Turonian)

period, that is 3040 million years after the first known

floral fossils, which were polysymmetric [1820]. Floral

monosymmetry has originated many times frompolysymmetry and several large, successful clades with

predominantly or entirely monosymmetric flowers have

evolved, such as orchids, legumes, Dipsacales, Lamiales,

and Asteraceae. Monosymmetric flowers are commonly

presented to the side in such a way that they have an upper

(i.e. adaxial) and a lower (i.e. abaxial) half that are different

in shape. Floral monosymmetry is a successful system

because of its potential for efficient precision mechanisms

in pollination biology. It has also been shown that bees

have a preference for symmetrical (i.e. monosymmetric

and polysymmetric) patterns, which is either innate or

learned [11,12,13]. It has been argued that the evolution

of monosymmetry in the mentioned clades was mediatedby bee pollination, at least in the initial stages.

The molecular developmental genetics of monosymmetry

was first elucidated in the model speciesAntirrhinum majus,

that is snapdragon (Antirrhinaceae). Antirrhinum flowers

consist of three five-merous whorls of sepals, petals and sta-

mens, and a two-merous whorl of carpels. Monosymmetry

is expressed by the weaker early development of the upper

half of the flower relative to the lower half, which results in

the suppression of the upper (odd) stamen; in the mature

flower it is only present as a tiny staminode. It was found

that two genes, cycloidea and dichotoma, play a major role in

this monosymmetry: if both of these genes fail to function,

the flowers become polysymmetric [1,4,8,21,22]. Such

Evolution of floral symmetryPeter K Endress

Figure 1

The three forms of floral symmetry addressed in this review. Planes ofsymmetry are indicated by broken lines.

Polysymmetric Monosymmetric Asymmetric

Current Opinion in Plant Biology


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Evolution of floral symmetry Endress 87

secondarily polysymmetric flowers in Antirrhinaceae and

other families are called peloriae because Linnaeus, 250

years ago, created the generic namePeloria for a population

of Linaria vulgaris (also Antirrhinaceae) with monstrous,

polysymmetric flowers. The two genes, cycloidea and

dichotoma, differ slightly in the period during which they areactive and in the extent of the floral sector that they influ-

ence [21]. The two genes are similar in structure and,

together with some other genes, may have originated by

gene duplication [21,23,24].

Additional genes, radialis and divaricata, are also involved

in producing floral monosymmetry [25]. Studies on the

development of floral monosymmetry have been expanded

to other Antirrhinaceae, such asLinaria [26] andMisopates

[23], and to some Gesneriaceae [25,27,28,29]. Genes

of the cycloidea and dichotoma families also occur in these

closely related groups. In Linaria vulgaris, the mutation is

not based on a change in the nucleotide sequence but on

extensive methylation [26]. The evolution of the cycloidea

gene within a group of genera in Gesneriaceae was studied

in a combined phylogenetic and developmental study

[28], but its role in the formation of monosymmetric and

secondarily polysymmetric flowers in Gesneriaceae is not

yet clear [29]. As in the study on Linaria [26], the

nucleotide sequence of cycloidea was not altered in the poly-

symmetric forms of these Gesneriaceae. A variant of

monosymmetry that occurs repeatedly in various families of

Lamiales is reduction not only in the upper half of the

flower but also in the lower half. Such flowers may have

only two functional stamens, the upper pair, whereas theodd stamen and the lower pair are sterile or lacking. This

implies the action of at least one additional gene, which

affects the lower half of the flower. The divaricata gene is

known to affect the lower half of the flower; however, it

does not cause reduction of stamens [22]. In comparative

developmental studies, it appears that floral monosymme-

try is expressed at different stages depending on the

systematic group [30], and that even in polysymmetric

flowers there may be transient monosymmetric stages

[15,31]. It would be interesting to know whether this is a

genetic or epigenetic phenomenon.

Although monosymmetric flowers appeared later inangiosperm evolution than polysymmetric ones, it is clear

that in the Antirrhinaceae, polysymmetric flowers are

evolutionarily derived from monosymmetric flowers. This

can be deduced from two sources. First, phylogenetic

analyses show thatAntirrhinum andLinaria are nested in a

large group with monosymmetric flowers [32,33,34].

Second, the morphology of the Antirrhinaceae: polysym-

metric Linaria often have five nectar spurs, which

indicates that this is an unnatural form; flowers with nec-

tar spurs in monosymmetric clades always have a single

spur [35]. Within the Lamiales floral symmetry has also

changed by the loss of certain floral organs, for example in

Plantago, in which the odd sepal and the odd stamen have

been lost [15,36,37].

The phylogeny of Lamiales is relatively well resolved in

comparison with those of other angiosperm groups [33]

(Figure 2). The most highly nested families (i.e.

Acanthaceae, Lamiaceae, Orobanchaceae) have the most

extremely monosymmetric flowers with the odd stamin-

ode predominantly lacking and the two adaxial petalsclose together, sometimes even appearing as a single organ

[15,36]. It may be predicted that the genetic comple-

ment responsible for monosymmetry is more complex in

these most highly nested families than in the more basal

family Gesneriaceae. Antirrhinaceae (with Antirrhinum) is

in between these two groups on the phylogenetic grade of

the Lamiales. It may therefore have intermediate com-

plexity in its genetics of floral monosymmetry. The

relatively basal family Gesneriaceae has the most pro-

nounced incidence of polysymmetric flowers in Lamiales.

From their systematic distribution and structure, these

polysymmetric flowers were interpreted as reversals,

which were based on a relatively weakly rooted geneticconstitution for monosymmetry [36]. This evolutionary

direction was later supported by molecular studies [29].

The two basal-most families in Lamiales [33] have

unusual flowers with four sepals and petals, and two sta-

mens and carpels. These flowers are disymmetric in the

Oleaceae and monosymmetric in the small and poorly

studied family Calceolariaceae, which presents a difficulty

to the interpretation of the early evolution of floral form in

the Lamiales [15]. Extensive studies on the rate of evo-

lutionary directions from polysymmetry to monosymmetry

and vice versa show that changes take place frequently in

both directions. The change from polysymmetry to mono-

symmetry seems to be easier extrinsically (i.e. ecologically)

but more difficult intrinsically (i.e. developmentally) than

Figure 2

Cladogram of Lamiales, simplified after Olmstead et al . [33](only the larger families are included), and trend of expression offloral monosymmetry.

Orobanchaceae

Lamiaceae

Acanthaceae

Bignoniaceae

Verbenaceae

Scrophulariaceae

Antirrhinaceae

Gesneriaceae

Calceolariaceae

Oleaceae

Highly monosymmetriclip flowers, odd staminodemostly lacking

Floral monosymmetryexpressed to variousdegrees, odd staminodepresent or lacking

Floral monosymmetryrelatively weakly expressed,odd staminode present

(Flowers tetramerous)



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88 Growth and development

change in the opposite direction [34,38]. In Gesneriaceae,

an instance of reversion back to monosymmetry from a

clade with secondarily polysymmetric flowers has been

identified [28]; thereby suggesting that evolution back

and forth occurs more often than previously believed [35].

Evolution of floral leftright asymmetryLeftright asymmetry is prominent in animals, and thedevelopment of leftright asymmetry from a bilateral

(monosymmetric) stage is under discussion. Interest in

leftright asymmetry was initiated because of the medical

importance of disturbed leftright asymmetry in humans;

it then expanded to vertebrates and animals in general. In

the past three years the molecular developmental genetic

literature on leftright asymmetry in animals has exploded

[14]. Leftright asymmetry may occur in two morphs (i.e.

left and right), also called enantiomorphy. In animals,

species and larger taxa are commonly characterised by the

presence of only a single morph. In contrast, in plants,

leftright asymmetry is much less prominent and hasscarcely been tackled, neither from an evolutionary nor

from a developmental genetic point of view. Two kinds of

leftright asymmetry affect flower structure.

Flowers with an asymmetric shape at anthesis

This type of asymmetry has evident repercussions for polli-

nation and has been discussed mainly by floral biologists.

The occurrence of this asymmetry is scattered in several

families in which otherwise monosymmetric flowers are pre-

dominant. In one asymmetrical form, that is enantiostyly,

the style and stigma are not in the middle of the flowers but

curved to one side (Figure 3). Enantiostyly is known to

occur in at least 14 genera from 10 or more families [16,39].

In another asymmetrical form, the flowers have only one

stamen, such as in the Cannaceae, the Marantaceae, some

Zingiberaceae, a few orchids, some Vochysiaceae, and

Centranthus of Valerianaceae. The most complicated asym-

metric flowers are those in which the pollination organs are

enclosed in a keel or the upper lip; the first condition is pre-

sent in several genera of beans (Phaseolinae of legumes),the second inPedicularis (Orobanchaceae) [15].

Enantiostyly occurs mainly in pollen flowers that are buzz-

pollinated (i.e. pollinated by vibration) [40]. It has been

hypothesised that an advantage of enantiostyly is the

removal of the style from the median plane, which avoids

damage to the style and stigma from large buzzing bees

[41,42]. In most cases of enantiostyly, both floral morphs are

known to occur on the same individual (monomorphic

enantiostyly). Only in a few species of three monocot fam-

ilies are they separated on different individuals (dimorphic

enantiostyly) [16]. Because the families in which enan-

tiostyly is present are only distantly related, it can be

concluded that enantiostyly has evolved convergently many

times. In theStreptocarpus/Saintpaulia clade (Gesneriaceae),

enantiostyly had one or two origins [27]. Because dimor-

phic enantiostyly is much rarer than monomorphic

enantiostyly, and because species with dimorphic enan-

tiostyly always have close relatives with monomorphic

enantiostyly, it can be concluded that dimorphic enan-

tiostyly has evolved from monomorphic enantiostyly [16].

This evolutionary direction can also be derived from phylo-

genetic analyses of the families with dimorphic enantiostyly

[16]. For the same reasons, it can be stated that enan-

tiostylous flowers have evolved from monosymmetricflowers. The reproductive biological reasons that explain

why dimorphic enantiostyly is so rare have also been

discussed [16]. Studies so far indicate that in the unista-

minate asymmetric flowers mentioned, both floral morphs

are present in the same inflorescence [15,43].

In contrast, in both (phylogenetically unrelated) forms of

flowers with enclosed pollination organs, as found in the

Phaseolinae (Fabaceae) and Pedicularis (Orobanchaceae),

only one morph of asymmetry has been identified in pre-

liminary observations [15]. Moreover, a single morph is

found not only within individual plants, but also within

species and at higher levels. In the Phaseolinae, the keel iscurved anticlockwise (if viewed from the front). In

Pedicularis, the flowers (especially the upper lip) are distorted

clockwise. Why this contrast? It may be that flowers with

enclosed pollination organs are ergonomically more difficult

to work by pollinators than those with unenclosed pollina-

tion organs. If flowers with enclosed pollination organs can

be consistently worked from the same side, however, their

ergonomic disadvantage may be reduced pollination takes

less time. Therefore, it could be expected that there is

selective pressure for plants to produce only one floral

morph, not only at the level of an individual but at the pop-

ulation level. During speciation, this single morph may have

been retained so that it is now uniform in a genus or larger

group. In contrast, in more open and simpler flowers, the

Figure 3

The two forms of leftright asymmetry in flowers addressed in this review.

Left Right

(a)Enantiostyly

Left Right

(b)Contort petal aestivation

Current opinion in Plant Biology


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presence of two morphs in an individual has no effect or

only a minor effect on pollinator visiting time per flower.

Flowers with a contort petal aestivation

This kind of asymmetry is most pronounced in floral buds,

whereas in open flowers it may be less prominent. In suchflowers two morphs are possible: sinistrorse (i.e. contorted

to the left) and dextrorse (i.e. contorted to the right)

(Figure 3). It has long been known that some plant fami-

lies show unfixed (flexible) behaviour in which both

morphs occur in the same species and individual (enan-

tiomorphy); whereas others show fixed behaviour in which

only one morph occurs within a species, genus or even

family [44]. Spiral phyllotaxis, such as that present in flow-

ers of many basal angiosperms and in the calyx of many

eudicots, is also leftright asymmetric. As far as is known,

both morphs may always occur in one individual [15,44].

The distribution of the two petal contortion behaviours is

also significant at higher systematic levels ([15];

Figure 4). First, within the eudicots, the largest group of

the angiosperms, contort flowers are represented mainly in

the rosids and asterids; in other angiosperms contort aesti-

vation is infrequent or lacking. Second, most rosids with

contort aestivation (except some Myrtales and a few

Brassicales and Malpighiales) show the unfixed pattern.

Third, in contrast, all asterids with contort aestivation have

a fixed behaviour. In groups with a fixed behaviour, the

morph can change within the phylogeny of a family. In the

Apocynaceae, it has long been known that some genera are

consistently sinistrose, whereas others are consistentlydextrorse. Phylogenetic studies show that the switch from

one to the other morph has occurred only once or a few

times within the family [15,45,46].

In the unfixed pattern, the expression of the two morphs is

dependent on chance or is governed by the symmetry of

the entire inflorescence. Thus, the expression of the two

morphs seems to be epigenetic. In monochasial partial

inflorescences (e.g. in Oxalis), dextrorse and sinistrorse

morphs regularly alternate in the manner of pendulum

symmetry. In a racemose inflorescence (e.g. inAbutilon), the

distribution (i.e. the sequence of sinistrorse and dextrorse

morphs) is irregular. In contrast, in the fixed pattern, it hasto be assumed that the morph is genetically determined, as

it is in the body plan of animals. The developmental mech-

anism that determines the morph is, however, unknown in

flowers. It would also be interesting to know why the fixed

pattern is found so consistently in contort flowers of aster-

ids but is uncommon in rosids. Is it a mere coincidence that

the fixed pattern evolved in asterids or did the ancestral

asterids have flowers of a degree of complexity that caused

selective pressure towards the maintenance of a single

morph for pollination biological reasons?

ConclusionsThe evolution of monosymmetry and secondary polysym-

metry in flowers of the Antirrhinaceae and Gesneriaceae is

being elucidated by molecular systematics and molecular

developmental genetics. Leftright asymmetry in flowers

has been much less studied. A particularly interesting exam-ple of leftright asymmetry is contort petal aestivation,

which shows both morphs in each individual plant in most

rosids but only one morph even at higher systematic levels

in asterids. The study of flower evolution and especially of

floral symmetry is a prominent example of a field in which

an integrative approach of different aspects, intrinsic (i.e.

developmental) and extrinsic (i.e. ecological) is necessary

[3,24,38,47]. Phylogenetics, fossil history, evaluation of

evolutionary changes in the diversity of floral forms, molec-

ular developmental genetics, and pollination biology from

the side of the plant and the pollinators, are all required to

develop an integrated view of flower evolution. It is impor-

tant to know how and when a new kind of symmetry arosefor the first time, but also how easily one kind can be

transformed into another kind, once they have evolved.

AcknowledgementsI thank Michael Donoghue, Rivka Dulberger, Valentin Grob, RichardOlmstead, Peter Rusert and Kay Schneitz for discussion and information. I amgrateful to Alex Bernhard for assistance with the illustrations.

References and recommended readingPapers of particular interest, published within the annual period of review,have been highlighted as:

of special interestof outstanding interest

1. Coen ES: Floral symmetry. EMBO J1996, 1 5 :6777-6788.2. Jean RV, D Barab(Eds): Symmetry in Plants. Singapore: World

Scientific, 1998.

Figure 4

Cladogram of angiosperms, simplified after Soltis et al. [20] (only the majorgroups are included), and evolution of patterns of contort petal aestivation.

Asterids

Rosids

Basal eudicots

Monocots

Basalangiosperms

Contort corollalacking

Contort corollararely present

Taxa with contort corolla always:

or RightLeftat highertaxonomic

levels!

Left Right

Taxa with contort corolla mostly:

in eachindividual!



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3. Diggle PK, Endress PK (Eds): Development, function and evolution of symmetry in plants. Int J Plant Sci1999, 1 6 0 :S1-S166.A special issue with articles that elucidate floral symmetry from differentview points: comparative developmental morphology, pollination biology,and perception of symmetry by bees.

4. Luo D, Carpenter R, Vincent C, Copsey L, Coen E: Origin of floralasymme try in Antirrhinum. Nature1996, 3 83 :794-799.

5. Hudson A: Developme nt of symme try in plants. Annu Rev Plant Physiol Plant Mol Biol2000, 5 1 :349-370.A review of symmetry studies in plants, mainly of the vegetative region.

6. Coen ES: The role of homeotic genes in flower de velopmentand evolut ion. Annu Rev Plant Physiol Plant Mol Biol1991,42 :241-280.

7. Coen ES, Nugent JM: Evolution of flowers and inflorescences.Development1994 (suppl):107-116.

8. Coen ES, Nugent JM, Luo D, Cubas P, Chadwick M, Copsey L,Carpenter R: Evolution of floral symm etry. Philos Trans R Soc LondBiol1995, 3 5 0 :35-38.

9. Dafni A, Kevan PG: Floral symm etry and nectar guides:ontogenetic constraints from floral development, colour patternrules, and functional significance. Bot J Linn Soc1996,120 :371-377.

10. Neal PR, Dafni A, Giurfa M: Floral symmetry and its role inplantpollinator system s: terminology, distribution, andhypotheses. Annu Rev Ecol Syst1998, 29 :345-373.

11. West EL, Laverty TM: Effect of floral symmetry on flower choiceand foraging behaviour of bumble bee s. Can J Zool1998,76 :730-739.

12. Lehrer M: Shape perception in the honeybee: symmetry as a global frame work. Int J Plant Sci1999, 1 6 0 :S51-S65.It is shown that in honeybees some types of response to visual stimuli arebased on innate behavioural programs. Polysymmetric and perpendicularmonosymmetric patterns (i.e. those most common in flowers) are preferredto other patterns.

13. Giurfa M, Dafni A, Neal PR: Floral symmetry and its role in plantpollinator systems. Int J Plant Sci1999, 1 6 0 :S41-S50.Floral symmetry is discussed from the perspective of insect pollinator per-

ception. The relationships between innate preferences of shapes andlearning are discussed.

14. Capdevila J, Vogan KJ, Tabin CJ, Izpisa Belmonte JC: Mechanismsof leftright determination in vertebrates. Cell2000, 1 0 1 :9-21.

15. Endress PK: Symmetry in flowers: diversity and evolution. Int J Plant Sci1999, 1 6 0 :S3-S23.The biological and evolutionary significance of different kinds of floral sym-metry is discussed, especially from the point of view of comparative devel-opment and diversity of forms. The author discusses new insights intomonosymmetry in Lamiales, and especially into the evolution of leftrightasymmetry in contort flowers throughout the angiosperms.

16. Barrett SCH, Jesson LK, Baker AM: The evolution and function of stylar polymorphisms in flowering plants. Ann Botany2000,

85 (supp l A):253-265.This paper includes a discussion on the evolution of enantiostyly and on thequestion of why dimorphic enantiostyly is so rare in angiosperms.

17. Buschmann H, Fabri CO, Hauptmann M, Schaeffner AR: Tortifoliaslead the way to straight growth. Abstract 487 of the 11thInternational Conference on ArabidopsisResearch, 2000 June2428, Madison, USA.

18. Crane PR, Friis EM, Pedersen KR: The origin and earlydiversification of angiosperms. Nature1995, 37 4 :27-33.

19. Crepet WL: Timing in the evolution of derived floral characters.Upper Cretaceous (Turonian) taxa with tricolpate and tricolpate-derived pollen. Rev Palaeobot Palynol1996, 9 0 :339-359.

20. Soltis PS, Soltis DE, Chase MW: Angiosperm phylogeny inferredfrom multiple genes as a tool for comparative biology. Nature1999, 4 02:402-404.

21. Luo D, Carpenter R, Copsey L, Vincent C, Clark J, Coen E: Control of organ asymmetry in flowers of Antirrhinum. Cell1999,

9 9 :367-376.The authors show how dichotomaand cycloideaaffect the symmetry or

asymmetry of individual petals in Antirrhinumby their expression at differentsites of activity during development.

22. Almeida J, Rocheta M, Galego L: Genetic control of flower shape inAntirrhinum majus. Development1997, 124 :1387-1392.

23. Vieira CP, Vieira J, Charlesworth D: Evolution of the cycloidea gene fam ily in Antirrhinum and Misopates. Mol Biol Evol1999,

1 6:1474-1483.Studies of cycloideain seven Antirrhinum, two Misopates, one Linaria, oneCymbalaria, and one Digitalisspecies show that the cycloideagene familycomprises at least five apparently functional genes.

24. Theissen G: Evolutionary developmental genetics of floral symmetry: the revealing power of Linnaeus monstrous flower.

Bioessays2000, 22 :209-213.The plea of a molecular developmental geneticist for integrative studies inplant evolutionary biology.

25. Cronk Q, Mller M: Genetics of floral symme try revealed.Trends Ecol Evol1997, 12 :85-86.

26. Cubas P, Vincent C, Coen E: An epigene tic mutation responsible for natural variation in floral symm etry. Nature1999,

4 0 1 :157-161.A naturally occurring peloric mutant of Linaria vulgaris is characterised. Itscycloidea homologue gene does not show changes in the nucelotidesequence but it is extensively methylated and transcriptionally silent. Thismodification is heritable. Occasionally, the mutant reverts to normal bydemethylation of the cycloideahomologue and restoration of gene expres-

sion. This indicates that epigenetic mutations may play a more significantrole in plant evolution than previously assumed.

27. Harrison CJ, Mller M, Cronk QCB: Evolution and de velopment of floral diversity in Streptocarpusand Saintpaulia. Ann Botany1999,

8 4:49-60.A study of the diversity, development and evolution of floral form involvingvarious degrees of monosymmetry or polysymmetry in two genera ofGesneriaceae.

28. Mller M, Clokie M, Cubas P, Cronk QCB: Integrating molecular phylogenies and developmental genetics: a Gesneriaceae case

study. In Molecular Systematics and Plant Evolution. Edited byHollingsworth PM, Bateman RM, Gornall RJ. London: Taylor & Francis;1999:375-402.

A combination of a phylogenetic study of Gesneriaceae (based on the trnLintron and the spacer between trnL and trnF, and on ITS1 and ITS2) and ofthe cycloideagene in the same taxa. In three species that have reverted frommonosymmetry to polysymmetry, cycloideaappears to be intact. In one of

these clades, there has been a secondary reversion back to monosymmetryfrom secondary polysymmetry, which also implies that the gene is intact.

29. Citerne HL, Mller M, Cronk QCB: Diversity of cycloidea-like ge nes in Gesneriaceae in relation to floral symmetry. Ann Botany2000,

8 6:167-176.Phylogenetic analysis of the cycloideagene in Gesneriaceae indicates thatindependent duplication and gene-loss events have occurred during the evo-lution of Gesneriaceae. Apparently, reversals to polysymmetry were notcaused by loss of function of cycloideagenes.

30. Tucker SC: Evolutionary lability of symm etry in early floral development. Int J Plant Sci1999, 1 6 0 :S25-S39.An extensive review of the early development of polysymmetric, monosym-metric and asymmetric flowers in angiosperms. The review shows that thetime of symmetry expression during development varies widely but is oftensimilar in larger groups.

31. Buzgo M, Endress PK: Floral structure and development ofAcoraceae and its systema tic relationships w ith basal

angiosperms. Int J Plant Sci2000, 1 6 1 :23-41.

32. Olmstead RG, Reeves PA: Evidence for the polyphyly of theScrophulariaceae based on chloroplast rbcL and ndhFsequences.Ann Missouri Bot G ard1995, 82 :176-193.

33. Olmstead RG, dePamphilis CW, Wolfe AD, Young ND, Elisens WJ, Reeves PA: Disintegration of the Scrophulariaceae. Am J B otany

2000, 87 :in press.An extensive phylogenetic study of the Scrophulariaceae and related fami-lies, which shows that the classical Scrophulariaceae are polyphyletic andtheir subgroups need to be considerably rearranged. This work is an impor-tant basis for evolutionary studies surrounding the model plant Antirrhinumand elsewhere.

34. Donoghue MJ, Ree RH, Baum DA: Phylogeny and the evolution offlower symme try in the Asteridae. Trends Plant S ci1998,3 :311-317.

35. Endress PK: Diversity and Evolutionary B iology of Tropical Flowers.Cambridge, UK: Cambridge University Press; 1994.

90 Growth and development


6/6

36. Endress PK: Antirrhinum and Asteridae - evolutionary changes offloral symmetry. Symp Ser Soc Exp Biol1998, 53 :133-140.

37. Reeves PA, Olmstead RG: Evolution of novel morphological,ecological, and reprodu ctive traits in a clade containingAntirrhinum. Am J Botany1998, 8 5 :1047-1056.

38. Ree RH, Donoghue MJ: Inferring rates of change in flower symme try in asterid angiosperms. Syst Biol1999, 4 8 :633-641.To date, this is the most detailed discussion on rates of evolutionary changesbetween polysymmetric and monosymmetric flowers in a large group ofangiosperms. Aspects of phylogenetics, developmental genetics and ecologyare discussed.

39. Wang G, Miura R, Kusanagi T: The enantiostyly and the pollinationbiology of M onochoria korsakowii(Pontederiaceae). Acta PhytotaxGeobot1995, 4 6:55-65.

40. Buchmann SL: Buzz pollination in angiosperms. In Handbook ofExperimental Pollination Biology. Edited by Jones CE, Little RJ.New York: Scientific and Academic Editions; 1983: 73-113.

41. Dulberger R: The floral biology of Cassia didymobotryaan dC. a uriculata (Caesalpiniaceae).Am J Botany1981, 6 8 :1350-1360.

42. Fenster CB: Mirror image flowers and their effect on outcrossingrate in Chamaecrista fasciculata (Leguminosae). Am J Bot1995,82 :46-50.

43. Stoutamire W: Pollination of Tipularia discolor, an orchid with

modified symm etry. Am Orchid Bull1978, 47 :413-415.

44. Schoute JC: On corolla ae stivation and p hyllotaxis of floralphyllomes. Verh K Akad Wet Amsterdam, Afd Natuurkunde, Sec 2,1935, 34(4):1-77.

45. Endress ME, Albert VA: A morphological cladistic study ofApocynaceae: trends in character evolution within a broadenedfamilial circumscription. Am J B otany1995, 82 (suppl):127.

46. Endress ME, Bruyns PV: A revised classification of theApocynaceae s.l. Bot Rev2000, 6 6:1-56.

47. Baum DA: The e volution of plant developme nt. Curr Opin PlantBiol1998, 1 :79-86.


1.2001.flowersymmetry

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