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Nature’s Precision: The Intricate Pollen Dispersal Mechanisms of Papilionaceous Crops
Abstract
Pollination, a fascinating natural process, is crucial for the reproduction of flowering plants. It involves the transfer of pollen from the male reproductive part to the female reproductive part, enabling successful fertilization. Papilionaceous crops, belonging to the Fabaceae family, exhibit highly specialized pollen dispersal mechanisms that ensure effective pollination and genetic diversity. These mechanisms involve intricate interactions between floral structures and pollinators, primarily bees. By integrating findings from various studies, this review provides a comprehensive understanding of the intricate pollen dispersal mechanisms in papilionaceous crops such as piston/pump mechanism, explosive type mechanism, brush type mechanism and valvular mechanism. It also provides information about the role of different floral parts in pollen dispersal among the flowers. This review will be helpful in gaining insights about pollen dispersal mechanism and it contribution in improving crop yields and breeding programs.
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Sunnhemp (Crotalaria juncea L.) belonging to the family Fabaceae is having wide range of industrial utilization as fibre crop, fodder crop and green manure. Pollination is the key mutualism between two kingdoms of organisms. The ambiguity of whether sunnhemp is self-pollinated or cross-pollinated crop paved the way for our study. The simplest and most efficient approach to investigate the breeding system of C. juncea would be the combination of controlled hand pollination followed by pod set analysis. Floral biology study revealed the protandrous
characteristics of sunnhemp flowers. Flowers are zygomorphic and complete with dimorphic anthers. Breeding system study confirmed the prevalence of cross pollination in sunnhemp by higher per cent pod set in cross pollination in comparison with self-pollination.
This study aims to understand the role of floral traits in determining the pollination and reproduction of Desmodium grahamii (Fabaceae, Papilionoideae) with explosive floral mechanism in populations occurring in a natural reserve and botanical garden in southern Mexico City. We assessed the breeding system by quantifying floral and pollinator activity, compatibility, pollination, and reproductive success, assisted by field and laboratory analyses. Results showed that cross-pollination and self-pollination coexist, but bees are required for fruit and seed set. Flower colour is the primary attractant. Floral scent is also likely important because the petals were covered with papillae, although no scent was perceptible. Morphological and functional observations of D. grahamii exhibit simultaneous pollen release and stigma receptivity when the flower is activated by a pollinator and there is no secondary pollen presentation; this contrasts with what has been reported on other species of Desmodium. Pollen is the pollinators’ only reward, and its deposition and collection must be done synchronically, occurring when a bee lands and introduces its proboscis in the flower. In this study, we identified seven floral visitors: five bee pollinators and two syrphid flies as pollen thieves. On some occasions, Apis mellifera also behaves as a pollen thief. Fruit and seed set of flowers that were isolated from visitors may indicate a delayed pollination mechanism. Pollination results also suggest that Apis bees and syrphid flies may contribute to fruit and seed production when they forage on flowers at post-anthesis.
Biodiversity of insect pollinator’s species visiting sunnhemp crop was studied in TNAU Coimbatore, India. Fifteen insect
species belonging to four orders were recorded from sunnhemp flowers, of which nine belongs to order Hymenoptera, two to
Lepidoptera, two to Coleoptera and one to Diptera. Among the different insect pollinators Xylocopa latipes, Xylocopa
pubescens and Megachile lanata are the most frequent visitors. These are also capable of impeding pollination in sunnhemp
flowers. Among different bee species maximum mean population was observed in Megachile lanata-4.72 bees/M2/5 minutes
followed by Xylocopa latipes 3.65 bees/M2/5 minutes and lowest abundance was observed in case of Xylocopa pubescens
(3.215 bees/M2/5 minutes). The pollination index of Xylocopa latipes (7.05) was highestfollowed by Xylocopa pubescens
(6.85)and Megachile lanata (6.84). Hence it is concluded that Xylocopa latipes was the most efficient pollinator of
sunnhemp flower. The seed for this potentially valuable green manure crop is largely unavailable due to paucity of
pollinators and self-incompatible nature of the plant. These pollinators are able to overcome the floral barriers in sunnhemp
flowers. Compared to male bees, the females are more efficient in pollinating, the male bees collect only nectar while female
bees collect both nectar and pollen for the purpose of reproduction and feeding the offspring’-s.
In the papilionaceous flowers with explosive pollination mechanism, the androecium and the gynoecium are subjected to great pressure in the keel. It has been suggested that at the first visit nearly all pollen grains are released and that the floral parts do not return to their original positions; this would be a cue for pollinators to avoid activated flowers. The dependence on the pollinators suggests that explosive flowers will not produce fruits if the mechanism is not activated. In this paper, we have tested these ideas studying the reproductive biology of three Desmodium species, D. incanum, D. subsericium and D. uncinatum. Specifically, we studied the floral traits, reproductive system, pollination mechanism and floral visitors, for the three species. The results indicated that the keel and the wings play a key role in the activation of the explosive mechanism. The three species have a secondary pollen presentation, diurnal flowers, and a short floral cycle. According to the results, all the species studied were self-compatible, with two species producing fruits by autonomous self-pollination. Desmodium flowers were visited and activated by native and exotic bee species. During the first visit nearly all the pollen was released; after that, new visits were low or null. Our results indicated that the activation of the mechanism is not essential for the production of fruits, that explosive flowers are visited only once and that the changes in the positions of the floral parts are the cues that keep pollinators away from the flowers with activated mechanism.
On average, nectar-collecting bumble bees Bombus deposited 0.6% of the pollen removed from the flowers of Erythronium grandiflorum (Liliaceae) onto the stigmas of subsequently visited flowers. Because the proportion deposited declined as the amount removed increased, an individual plant would maximise its total pollen dispersal by relying on many pollen-removing visits while limiting the pollen removed by each pollinator. This restriction of pollen removal could be achieved by a plant presenting only a small portion of its pollen at one time (packaging) and/or by limiting the amount of presented pollen that a pollinator removes during a single visit (dispensing). The restriction of pollen removal required to maximize the expected total deposition on stigmas depends on the number of pollinator visits a plant receives, variation in the frequency of visits, and the pattern of pollen removal during a series of visits. Many aspects of floral biology contribute to a plant's ability to restrict pollen removal, including inflorescence size, flower morphology, anthesis patterns, nectar production, and dichogamy. Selection increasing paternal fitness of animal-pollinated plants could therefore elicit one of a variety of evolutionary responses; the specific response will depend on characteristics of both the plant and the pollinator. -Authors
We studied the biology and floral rewards of 34 taxa ofGenisteae from the SW of Europe. Most of the floral attributes show a statistically significant direct relationship. Anther biomass of the lower whorl (lW) is significantly lower than that of the upper whorl (uW), and the ratio of the two (Rv) differs among the taxa. All taxa are polliniferous, and Retama sphaerocarpa also secretes nectar. They can be considered xenogamous or facultative xenogams on the basis of their high pollen/ovule (P/O) ratios. Three principal mechanisms of pollen releasing are identified in this tribe: valvular, pump and explosive; the latter comprises specialized and nonspecialized subtypes. Pollination is sternotribic except in the specialized explosive mechanism, in which it is noto-sternotribic. Thus some pollen serves as food (pollen from the uW, which adheres to the ventral surface of the insect) and part of the pollen fulfils a polliniferous function (pollen from the lW, which adheres to the dorsal surface). Species that use a pump mechanism have very low Rv values (Rv=0.08–0.26); species with valvular or nonspecialized explosive mechanisms have Rv values between 0.24 and 0.58; those with a specialized mechanism of pollen presentation have high Rv values (0.6–0.76). In contrast to expectations, the highest P/O ratios appear in the specialized explosive system, which allows a single visit from the insect.
We studied the allocation of reproductive resources in 32 Mediterranean legume species. Correlations between main parameters
were analysed at interspecific level. For each species we described the type of pollen presentation and examined its systematic
significance. The high P/O values observed reflect low pollen transfer efficiency, typical of xenogamous species. Lowest P/Os
were found in species with brush or explosive tripping mechanism, while highest ones were associated to primary pollen presentation.
No trade-off was observed between P/O and the volume of a single pollen grain, nor between pollen number and pollen grain
volume. Perennials showed higher P/Os compared to annuals, in accordance with the assumption that annual species are often
self-compatible while most perennials are outcrossers. Fruit and seed set, evaluated in eight species under different experimental
conditions, showed a close dependence on insects, and the existence of self-compatibility in three species (Colutea arborescens, Coronilla emerus, Hedysarum coronarium). In Colutea arborescens and Coronilla emerus pollen-pistil interaction and pre-zygotic barriers to selfing were investigated through stigma receptivity tests and in-vivo
pollen germination trials. Results demonstrated the importance of the stigmatic cuticle in reducing levels of autogamy. Productivity
tests confirmed the utility of P/O ratio as indirect measure of species' breeding system.
It is accepted that the papilionaceous corolla of the Fabaceae evolved under the selective pressure of bee pollinators. Morphology and function of different parts of Coronilla emerus L. flowers were related to their role in the pollination mechanism. The corolla has a vexillum with red nectar lines, a keel hiding stamens and pistil, and two wing petals fasten to the keel with two notched folds. Pollinators land on the complex of keel and wings, trigger the protrusion of pollen and finally of the stigma from the keel tip. Data on pollen viability and stigma receptivity prove that flowers are proterandrous. The results of hand-pollination experiments confirmed that insects are fundamental to set seed. Interaction with pollinators allows not only the transport of pollen but also the rupture of the stigmatic cuticle, necessary to achieve both allogamy and autogamy. Field observations showed that Hymenoptera, Lepidoptera, and Diptera visited the flowers. Only some of the Hymenoptera landed on the flowers from the front and elicited pollination mechanisms. Most of the insects sucked the nectar from the back without any pollen transfer. Finally, morphological and functional characteristics of C. emerus flowers are discussed in terms of floral larceny and reduction in pollination efficiency.
Rhynchosia beddomei flowers during December-March with peak flowering during January. The flowers are hermaphroditic, nectariferous, self-compatible and have explosive pollination mechanism adapted for pollination by bees, especially carpenter bees. The flowers not visited by bees fall off while those visited and pollinated by them set fruit. Therefore, R. beddomei is obligately dependent on pollinating bees for pollination which occurs due to tripping of the explosive mechanism.
The pollen brush commonly is referred to as a “bearded” or “pubescent” style in taxonomic literature and traditionally is taken to be an aggregation of trichomes on the distal end of the style, and occasionally including the stigma. We present data that support the taxonomic utility of the pollen brush but define it more specifically as a dense aggregation of erect trichomes emanating from the style (not stigma or ovary) and functioning in secondary pollen presentation. We recommend avoiding such vague terminology as bearded or pubescent styles as these refer not only to the pollen brush but also to ciliate and penicillate stigmas and ciliate styles. The latter three conditions have some taxonomic use, and since their occurrence is not necessarily correlated with the presence of a pollen brush, they should be distinguished from it. We estimate that the pollen brush has arisen independently in the following eight taxa: 1) Crotalaria and Bolusia (Crotalaraieae), 2) subtribe Coluteinae (Galegeae), 3) Tephrosia subgenus Barbistyla (Millettieae), 4) Adenodolichos (Phaseoleae subtribe Cajaninae), 5) Clitoria (Phaseoleae subtribe Clitoriinae), 6) the subtribe Phaseolinae (Phaseoleae), 7) the Robinia group (Robinieae), and 8) the tribe Vicieae. Its hypothesized homology within each of these groups is supported by a cooccurrence with other taxonomic characters, both morphological and molecular.
Flowers from diverse angiosperm families conceal their pollen within a keel. Visitors in search of nectar enter the narrow entrance between the movable keel and the opposed immovable flag. Thus, they secondarily release (doses of) pollen from its cover. As bees are the only visitors able to handle these flowers and thus their essential pollinators on one hand and the only pollen foragers on the other hand, keel blossoms are best understood as an adaptive response of plants to the dilemma of strong competition for pollen between flowers and bees.
Delayed autonomous self-pollination allows outcrossing to occur while also ensuring that seeds are produced in the absence of pollen vectors. We investigated variation in the efficacy of this pollination mechanism in populations of Hibiscus laevis. Recurvature of stylar branches occurred after 1 d of anthesis, and in plants from Ohio, Illinois, Arkansas, and Oklahoma this behavior resulted in autonomous selfing (surprisingly, stylar movement was facultative in that it did not take place when the stigmas were already pollinated). In contrast to these more northern populations, the distance between anthers and stigmas was too great to allow autonomous selfing in plants from Texas, Mississippi, and Louisiana. Greenhouse studies of plants from Ohio demonstrated that autonomous selfing resulted in an average of 29.5 seeds per flower, as compared to 59.9 seeds per flower from hand-pollination of stigmas with self pollen. In an assessment of the possible significance of this selfing mode, emasculated flowers did not set significantly fewer seeds in a natural stand in Ohio, suggesting that few seeds resulted from autonomous selfing al that site. Modest inbreeding depression was detected at this population. Our results suggest that delayed autonomous selfing is more common in northern populations, where it may facilitate population establishment and persistence at times when pollinators are scarce.
Measured pollen removal from Aconitum delphinifolium, Aralia hispida, Lupinus sericeus, Mertensia paniculata, Pedicularis bracteosa and P. contorta. Much interspecific variation in pollen removal depends on the likelihood of contact between pollinator and anthers. Bumble bees Bombus spp. removed a median of 50-80% of the available pollen during 1st visits to species with exposed anthers. Only 19% was removed during initial manipulation of lupine flowers, which present pollen indirectly. Within species, removal increased with visit duration; it did not additionally depend on the number of visits involved. Removal typically changed in direct proportion to differences in pollen availability. Pollen size also affected removal, but it is unclear that this effect is direct. In most cases, removal was unaffected by species or caste of bee involved. Succeeding visits to a flower removed either a fixed or, more commonly, a declining proportion of the pollen remaining in a flower. A model of pollen dispersal indicates that a constant removal proportion would maximize dispersal when the number of visits a flower receives varies little. Diminishing proportional removal would allow plants to maintain pollen dispersal when the frequency of pollinator visits is uncertain. -from Author
Pollen presenters are specific floral structures, other than anthers, from which pollen is distributed for cross fertilization between flowers. They occur in only five families of monocotyledons and 20 families of the dicotyledons. Presenters in 15 families are described here. In the largest plant family (Asteraceae) all taxa have pollen presenters, while in others (e.g. Myrtaceae) they occur in only some species in a few genera. Most presenters are associated with the gynoecium and there is a wide range of forms involving hairs or outgrowths of the stylar tissue. Despite the placement of self pollen close to the stigma most taxa are outcrossing and avoid self fertilization by protandry, with the stigma being covered at anthesis, or by precise placement of pollen so that is does not contact the stigma. Likely selective advantages in the development of pollen presenters include greater accuracy in pollen transfer than in the normal anther to stigma movement and avoidance of interference between male and female organs in the flower. In some groups there is enhanced ability for female choice because effective pollen delivery enables a choice from among many pollen grains, while in others pollen presenters enhance male reproductive success. Study of the pollination biology of plants requires a knowledge of which plants have pollen presenters and a full understanding of the structures in the flower which are associated with the pollen presentation action.
Bumblebees foraging on vertical inflorescences start near the bottom and work upward, behavior commonly interpreted as a response to the greater amounts of nectar available in lower flowers. Lupinus polyphyllus, which produces no nectar, has more pollen available in upper flowers. Although bees are probably unable to detect this gradient, since pollen is hidden from their view, they still start low and forage upward. Therefore, we concluded that the bees' tendency to forage upward on vertical inflorescences is not tied to a reward gradient. In addition, bees use only about 15% of the flowers per inflorescence, although they could be much more efficient by visiting and revisiting every flower systematically. In general, revisits would not be penalized because most flowers contain enough pollen for several visits. Optimal foraging theory may not offer an adequate explanation for such gross inefficiency.
Vigna caracalla has the most complex flower among asymmetrical Papilionoideae. The objective of this study was to understand the relationships among floral characteristics, specialization, mating system and the role of floral visitors under different ecological contexts.
Five populations were studied in north-western Argentina, from 700 to 1570 m a.s.l. Anthesis, colour and odour patterns, stigmatic receptivity, visitors and pollination mechanism were examined and mating-system experiments were performed.
The petals are highly modified and the keel shows 3.75-5.25 revolutions. The sense of asymmetry was always left-handed. Hand-crosses showed that V. caracalla is self-compatible, but depends on pollinators to set seeds. Hand-crossed fruits were more successful than hand-selfed ones, with the exception of the site at the highest elevation. Bombus morio (queens and workers), Centris bicolor, Eufriesea mariana and Xylocopa eximia trigger the pollination mechanism (a 'brush type'). The greatest level of self-compatibility and autonomous self-pollination were found at the highest elevation, together with the lowest reproductive success and number of pollinators (B. morio workers only).
Self-fertilization may have evolved in the peripheral population at the highest site of V. caracalla because of the benefits of reproductive assurance under reduced pollinator diversity.
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