The genetic dissection of floral pollination syndromes

A major factor in the evolution of the angiosperms is the adaptation of plants to animal pollinators. The specific morphology of a flower, its color, nectar composition and scent production can all contribute to reproductive success by attracting pollinators and by limiting out-crossing with other species. It has now become feasible to dissect the genetic basis of plant adaptation to different pollinators.     

Genetics of flower size and nectar volume in Petunia pollination syndromes

The two related Petunia species, P. axillaris and P. integrifolia, are sympatric at various locations in South America but do not hybridise. Divergent pollinator preferences are believed to be in part responsible for their reproductive isolation. The volume of nectar produced and several components of flower morphology might contribute to pollinator-dependant reproductive isolation. In this study, we aimed to identify the genetic changes underlying the quantitative differences observed between these two Petunia species in flower size and nectar volume. We mapped quantitative trait loci (QTL) responsible for the different phenotypes of P. axillaris and P. integrifolia in an inter-specific backcross population. QTL of small to moderate effect control the differences in flower size and volume of nectar. In addition, we observed strong suppression of meiotic recombination in Petunia, even between closely related species, which precluded a fine resolution of QTL mapping. Thus, our data suggest that flower size and nectar volume are highly polygenic. They are likely to have evolved gradually through pollinator-mediated adaptation or reinforcement, and are not likely to have been primary factors in early steps of pollinator isolation of P. axillaris and P. integrifolia.     

Trends in floral scent chemistry in pollination syndromes: floral scent composition in hummingbird-pollinated taxa

We studied an assemblage of 17 species of bird-pollinated Ecuadorian plants (from 14 angiosperm families), including taxa pollinated by short-billed (trochiline) and sickle-billed (hermit) hummingbirds. Hummingbirds are widely supposed to ignore fragrance while visiting flowers. We collected floral headspace odours in order to test the general prediction that specialist hummingbird-pollinated flowers are scentless. In nine out of 17 of these species we failed to detect any odours using gas chromatography-mass spectrometry (GC-MS), whereas the remaining eight species produced trace levels of volatile compounds. Most of these odour compounds were of terpenoid or lipoxygenase derivation and are commonly emitted by vegetative as well as floral plant tissues. Further studies will be required to determine whether these weak odours attract alternative pollinators, repel enemies or represent vestiges of a scented ancestry.  © 2004 The Linnean Society of London, Botanical Journal of the Linnean Society , 2004, 146 , 191–199.     

Trends in floral scent chemistry in pollination syndromes: floral scent composition in moth-pollinated taxa

KNUDSEN, J. T. & TOLLSTEN, L., Trends in floral scent chemistry in pollination syndromes: floral scent composition in moth-pollinated taxa. Floral scent from 15 moth-pollinated species in nine families was collected by head-space adsorption. The chemical composition was determined by coupled gas chromatography-mass spectrometry (GC-MS). The typical floral scent of moth-pollinated flowers contains some acyclic terpene alcohols, their corresponding hydrocarbons, benzenoid alcohols and esters and small amounts of some nitrogen compounds. The floral scent composition of sphingophilous flowers can be distinguished from that of phalaenophilous flowers by the presence of oxygenated sesquiterpenes. The flowers of three of the studied species had the general appearance and floral scent composition of moth-pollinated flowers, but contained no nectar reward. These species probably rely on deceptive pollination by naive visitors, which are deceived by the similarity of the flowers' morphological and scent chemistry to that of rewarding moth flowers. The finding of similar or structurally closely related floral scent compounds in both temperate and tropical species from both the Old and New worlds suggests that floral scent composition has been selected by a specific group of pollinators, moths that have similar sensory preferences. The functions of floral scent in moth-pollinated flowers are discussed in relation to an often observed over-representation of male moth visitors.     

Pollen morphology in relation to floral types and pollination syndromes in Pedicularis (Orobanchaceae)

Floral diversification in the genus Pedicularis (Orobanchaceae) is remarkable among flowering plants. In this genus, floral morphology and pollinator behavior are closely co-adaptive. In the current paper, pollen grains of 23 representative species of Pedicularis mainly from North America, with two species from Japan and two species from China, whose pollination ecology was previously studied, were examined using light microscopy and scanning electron microscopy. Two pollen aperture types and three kinds of exine ornamentation were recognized among these species. In addition, pollen data from previous and the current studies of Pedicularis were integrated and analyzed, together with some pollination characters. There was a significant association between pollen aperture types and corolla types, as well as between pollination syndromes and corolla types. However, there was no association of exine ornamentations with corolla types. The relationships and evolution of this genus were discussed with regards to pollen morphology, corolla types and pollination syndromes.     

Emission mechanism of floral scent in Petunia axillaris

The mechanism of floral scent emission was studied in Petunia axillaris, a plant with a diurnal rhythm of scent output. The emission rate of each volatile compound oscillated in synchrony with its endogenous concentration, so that the intensity of the floral scent appeared to be determined by the endogenous concentrations. The composition of major volatiles in the flower tissue and the flower headspace showed characteristic differences. A negative correlation was found between the boiling points of the volatile compounds and the ratio of their emitted and endogenous concentrations, indicating that the composition of the floral scent depends directly on the endogenous composition of the volatile compounds. We conclude that in P. axillaris, the physiological regulation of floral scent emission operates not in the vaporization process but in the control of the endogenous concentrations of volatiles through biosynthesis and metabolic conversion.     

Active pollination favours sexual dimorphism in floral scent

Zoophilous flowers often transmit olfactory signals to attract pollinators. In plants with unisexual flowers, such signals are usually similar between the sexes because attraction of the same animal to both male and female flowers is essential for conspecific pollen transfer. Here, we present a remarkable example of sexual dimorphism in floral signal observed in reproductively highly specialized clades of the tribe Phyllantheae (Phyllanthaceae). These plants are pollinated by species-specific, seed-parasitic Epicephala moths (Gracillariidae) that actively collect pollen from male flowers and pollinate the female flowers in which they oviposit; by doing so, they ensure seeds for their offspring. We found that Epicephala-pollinated Phyllanthaceae plants consistently exhibit major qualitative differences in scent between male and female flowers, often involving compounds derived from different biosynthetic pathways. In a choice test, mated female Epicephala moths preferred the scent of male flowers over that of female flowers, suggesting that male floral scent elicits pollen-collecting behaviour. Epicephala pollination evolved multiple times in Phyllantheae, at least thrice accompanied by transition from sexual monomorphism to dimorphism in floral scent. This is the first example in which sexually dimorphic floral scent has evolved to signal an alternative reward provided by each sex, provoking the pollinator''s legitimate altruistic behaviour.     

Effects of pollination on floral attraction and longevity

The end of a flower's attraction to pollinators may be due toa range of visible cues such as permanent flower closure, acolour change, and withering or abscission of the petals. Floralattraction may be reduced by pollination. Pollination-inducedconclusion of floral attraction is often due to a colour changeor to flower closure. This may or may not be followed by a reductionin floral longevity, defined as the time to petal withering,wilting or shattering. In a few species floral longevity isincreased following pollination-induced flower closure or apollination-induced change in colour. Floral attraction, therefore,has to be disting uished from floral longevity. A literature survey shows that pollination rapidly reduces floralattraction in numerous orchids, but among other plant familiesonly about 60 genera have been found to show pollination-inducedshortening of floral attraction. Although only a few specieshave been investigated, it was invariably established that theeffect of pollination is blocked by inhibitors of ethylene synthesisor ethylene perception, hence is mediated by ethylene. The flowersthat cease to be attractive to pollinators, shortly followingpollination, tend to be from families that are known mainlyto comprise species in which flower longevity, petal colour,or flower closure, is sensitive to exogenous ethylene. Thisindicates that the effect of pollination on floral attractionis generally mediated by endogenous ethylene. Numerous species reportedly show a decrease in the period offloral attraction after exposure to ethylene, whereas only fora small number of species a decrease in the period of floralattraction induced by pollination has been observed. This discrepancymay be due to the greater attention that has been paid to theeffects of ethylene. Nonetheless, the possibility remains thatendogenous ethylene has a role in changing perianth form andcolour in addition to signalling the occurrence of pollination. Key words: Ethylene sensitivity, flower closure, flower longevity, pollination, petal colour, petal wilting, petal withering, petal abscission     

Angiosperm phylogeny,floral morphology and pollination ecology

Summary The different aspects of floral evolution—Angiosperm descent, floral morphology and pollination ecology—are discussed on the basis of the anthocorm theory of the angiospermous flower. Opposed ideas are critically compared and rejected mainly on account of several inconsistencies and flaws in old floral concepts. Floral evolution passed from a very early phase of dicliny, anemophily and aphananthy of the anthocorm to a phase of incipient entomophily soon associated with a partial sex reversal within the anthocorm. This second phase culminated in the monoclinous and primarily zoophilous flower types, whereas other floral types, more particularly the primarily anemophilous, diclinous flowers, are the direct descendants of the anthocorms of the initial phase. The second phase (to be differentiated in phase II and phase IIA) gave rise to at least two morphologically different flower types and two separate semophyletic lines of floral evolution (phase III and III A), in each of which the primary zoophily is almost always associated with the development of intrafloral semaphylls (petals) usually (at least in dicotyledonous groups) of androecial derivation. Early flower types were aphananthous and clearly anthocormoid (a condition still approximately represented by the so-called inflorescences of theSaururaceae) and assumed the morphology and other characteristics of a true flower by contractions, condensations, readjustments, oligomerisations, reductions and modifications (semaphylls!) leading to the great variety of adaptive floral patterns.

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Zusammenfassung Die drei Aspekte der Evolution der Blüte — die Abstammungsgeschichte der Angiospermen, Blütenmorphologie und Bestäubungsökologie — werden, ausgehend von der Anthokormtheorie der Angiospermenblüte, eingehend besprochen. Entgegengesetzte Meinungen werden kritisch verglichen und hauptsächlich auf Grund mehrerer Strittigkeiten und Fehler der älteren blütenmorphologischen Axiomen abgelehnt. Die Evolution der Blüte fing an mit einer frühen Phase mit Diklinie, Anemophilie und Aphananthie des Anthokorms und schritt allmählich weiter in die Richtung von beginnender Entomophilie, bald mit einer partiellen Geschlechtsinversion innerhalb des Anthokorms zusammengehend. Diese zweite Phase kulminierte in den monoklinen und primär zoophilen Blütentypen, während andere Blütengestalten, besonders die primär anemophilen und diklinen Angiospermenblüten, die unmittelbaren Abkömmlinge der Initialphase des Anthokorms sind. Aus der zweiten Phase (in den Phasen II und II A unterzuteilen) entwickelten sich wenigstens zwei morphologisch differenzierte Blütenformen und auch zwei geschiedene Blütensemophylesen (die Phasen III und III A), in jeder die primäre Zoophilie fast immer verbunden ist mit der Entwicklung von intrafloralen und (wenigstens bei Dikotylen) meistens von Staubblättern angeleiteten Semaphyllen (Kronblätter). Die frühen Blütentypen waren aphanantisch und anfänglich noch deutlich anthokormoid (ein Zustand der heutzutage noch von der sogenannten Infloreszenz der Saururaceen annähernd vertreten wird) und nahmen allmählich die entgültige Gestalt von einer der vielen adaptiven Blütentypen an durch eine Verkürzung der Blütenachse, und durch ein Zusammendrängen, Oligomerisation und (Semaphylle!) Abänderung der Blütenteile.

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Résumé Divers aspects de l'évolution de la fleur — à savoir la descendance des Angiospermes, la morphologie de la fleur, et l'écologie de la pollination — sont discutés à partir de l'hypothèse florale de l'anthocorme. Les opinions opposées, après d'être comparées et critisées, sont rejetées principalement à cause des inconséquences et inconsistances des anciens théorèmes morphologiques concernant l'origine de la fleur. L'évolution de la fleur commençait avec une phase d'antan de diclinie, anémophilie et aphananthie, et s'avançait graduellement dans la direction d'une phase entomophilique initiale, bientôt accompagnée d'un renversement de sexe partiel à l'intérieur de l'anthocorm. La deuxième phase culminait vers les types florals monoclines avec zoophilie primaire pendant que des autres types florals, particulièrement les fleurs diclines avec anémophilie primaire, sont les descendants directs du stade initiale de l'anthocorme. A partir de la phase II (se divisant aux stades II et II A), au moins deux types florals différents et aussi deux sémophylèses florals séparés (les phases III et III A) se développaient. Dans chacun de ses phases III et III A la zoophilie primaire est presque toujours accouplée avec l'origine des sémaphylles intrafloraux (pétales) le plus souvent (du moins chez les dicotylédones) dérivés des étamines. Les anciens types des fleurs ayant été aphanantique et au début encore nettement anthocormoïdes (quelle condition est maintenant toujours représentée par la soi-disante inflorescence des Saururacées), graduellement prenaient la forme d'une des plusieurs types floraux adaptifs par une contraction de l'axe florale et par l'entassement, l'oligomérisation et (sémaphylles!) la modification des pièces de la fleur.

     

Quantifying hummingbird preference for floral trait combinations: The role of selection on trait interactions in the evolution of pollination syndromes

Darwin recognized the flower's importance for the study of adaptation and emphasized that the flower's functionality reflects the coordinated action of multiple traits. Here we use a multitrait manipulative approach to quantify the potential role of selection acting on floral trait combinations underlying the divergence and maintenance of three related North American species of Silene (Caryophyllaceae). We artificially generated 48 plant phenotypes corresponding to all combinations of key attractive traits differing among the three Silene species (color, height, inflorescence architecture, flower orientation, and corolla‐tube width). We quantified main and interaction effects of trait manipulation on hummingbird visitation preference using experimental arrays. The main effects of floral display height and floral orientation strongly influenced hummingbird visitation, with hummingbirds preferring flowers held high above the ground and vertically to the sky. Hummingbirds also prefer traits in a nonadditive manner as multiple two‐way and higher order interaction effects were important predictors of hummingbird visitation. Contemporary trait combinations found in hummingbird pollinated S. virginica are mostly preferred. Our study demonstrates the likelihood of pollination syndromes evolving due to selection on trait combinations and highlights the importance of trait interactions in understanding the evolution of complex adaptations.     

Differences in the floral anthocyanin content of red petunias and Petunia exserta

In order to resolve a conflict between previous papers regarding the floral anthocyanins of red flowers of Petunia exserta, a naturally occurring species, the HPLC profile of this species was compared with that of commercial red garden petunias. Both HPLC profiles extremely superficially resemble each other in terms of relative amounts and retention times of the major anthocyanins. However, co-elution on HPLC of the mixed sample resulted in clear separation of the components. Three major anthocyanins in red petunias were determined to be cyanidin 3-sophoroside, cyanidin 3-glucoside and peonidin 3-glucoside, which exhibited similar behaviors on HPLC to delphinidin 3-glucoside. delphinidin-3-rutinoside and petunidin 3-rutinoside, respectively, the major floral anthocyanins of P. exserta.     

Geographic variation of floral scent in a highly specialized pollination mutualism

Floral scents are important signals for communication between plants and pollinators. Several studies have focused on interspecific variation of these signals, but little is known about intraspecific variation in flower scent, particularly for species with wide geographic distributions. In the highly specific mutualism between Ficus species and their pollinating wasps, chemical mediation is crucial for partner encounter. Several studies show that scents, i.e. blends of volatiles, are species-specific, but no studies address interpopulation variation of scents in fig pollination mutualisms, which often have broad geographic distributions. In this study, using absorption/desorption headspace techniques, we analyzed variation in floral scent composition among three populations of each of two widely distributed Asian Ficus species. We identified more than 100 different volatile organic compounds, predominantly terpenes. In both species, significant differences were found between scent bouquets of East Asian and Indian populations. These differences are discussed in relation to geographical barriers that could disrupt gene exchange between these two areas, thereby isolating Indian populations from those of Eastern Asia.     

Integrating floral scent, pollination ecology and population genetics

1 . Floral scent is a key factor in the attraction of pollinators. Despite this, the role of floral scent in angiosperm speciation and evolution remains poorly understood. Modern population genetic approaches when combined with pollination ecology can open new opportunities for studying the evolutionary role of floral scent.
2 . A framework of six hypotheses for the application of population genetic tools to questions about the evolutionary role of floral scent is presented. When floral volatile chemistry is linked to pollinator attraction we can analyse questions such as: Does floral volatile composition reflect plant species boundaries? Can floral scent facilitate or suppress hybridization between taxa? Can the attraction of different pollinators influence plant mating systems and pollen-mediated gene flow? How is population genetic structure indirectly influenced by floral scent variation?
3 . The application of molecular tools in sexually deceptive orchids has confirmed that volatile composition reflects species boundaries, revealed the role of shared floral odour in enabling hybridization, confirmed that the sexual attraction mediated by floral odour has implications for pollen flow and population genetic structure and provided examples of pollinator-mediated selection on floral scent variation. Interdisciplinary studies to explore links between floral volatile variation, ecology and population genetics are rare in other plant groups.
4 . Ideal study systems for future floral scent research that incorporate population genetics will include closely related taxa that are morphologically similar, sympatric and co-flowering as well as groups that display wide variation in pollination mechanisms and floral volatiles.     

The diacylglycerol forming pathways differ among floral organs of Petunia hybrida

The origin of diacylglycerol, a substrate for membrane lipid biosynthesis, is not fully understood. Here, we report that Petunia hybrida floral organs contain large amounts of diacylglycerol. Our data suggest that in stamens and pistils diacylglycerol is supplied both from phosphatidylcholine by non-specific phospholipase C activity and de novo via the Kennedy pathway and phosphatidic acid phosphatase, whereas in petals the two-step pathway catalyzed by phospholipase D and phosphatidic acid phosphatase predominates. Therefore, the pathways that supply diacylglycerol differ among floral reproductive organs, although large amounts of diacylglycerol are commonly accumulated in these organs.