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Nectar biosynthesis is conserved among floral and extrafloral nectaries.

ABSTRACT: Nectar is a primary reward mediating plant-animal mutualisms to improve plant fitness and reproductive success. Four distinct trichomatic nectaries develop in cotton (Gossypium hirsutum), one floral and three extrafloral, and the nectars they secrete serve different purposes. Floral nectar attracts bees for promoting pollination, while extrafloral nectar attracts predatory insects as a means of indirect protection from herbivores. Cotton therefore provides an ideal system for contrasting mechanisms of nectar production and nectar composition between different nectary types. Here, we report the transcriptome and ultrastructure of the four cotton nectary types throughout development and compare these with the metabolomes of secreted nectars. Integration of these datasets supports specialization among nectary types to fulfill their ecological niche, while conserving parallel coordination of the merocrine-based and eccrine-based models of nectar biosynthesis. Nectary ultrastructures indicate an abundance of rough endoplasmic reticulum positioned parallel to the cell walls and a profusion of vesicles fusing to the plasma membranes, supporting the merocrine model of nectar biosynthesis. The eccrine-based model of nectar biosynthesis is supported by global transcriptomics data, which indicate a progression from starch biosynthesis to starch degradation and sucrose biosynthesis and secretion. Moreover, our nectary global transcriptomics data provide evidence for novel metabolic processes supporting de novo biosynthesis of amino acids secreted in trace quantities in nectars. Collectively, these data demonstrate the conservation of nectar-producing models among trichomatic and extrafloral nectaries.

SUBMITTER: Chatt EC

PROVIDER: S-EPMC8133665 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Ant guards protect plants from herbivores, but can also hinder pollination by damaging reproductive structures and/or repelling pollinators. Natural selection should favour the evolution of plant traits that deter ants from visiting flowers during anthesis, without waiving their defensive services. The Distraction Hypothesis posits that rewarding ants with extrafloral nectar could reduce their visitation of flowers, reducing ant-pollinator conflict while retaining protection of other structures.We characterised the proportion of flowers occupied by ants and the number of ants per flower in a Mexican ant-plant, Turnera velutina. We clogged extrafloral nectaries on field plants and observed the effects on patrolling ants, pollinators and ants inside flowers, and quantified the effects on plant fitness. Based on the Distraction Hypothesis, we predicted that preventing extrafloral nectar secretion should result in fewer ants active at extrafloral nectaries, more ants inside flowers and a higher proportion of flowers occupied by ants, leading to ant-pollinator conflict, with reduced pollinator visitation and reduced plant fitness.Overall ant activity inside flowers was low. Preventing extrafloral nectar secretion through clogging reduced the number of ants patrolling extrafloral nectaries, significantly increased the proportion of flowers occupied by ants from 6.1% to 9.7%, and reduced plant reproductive output through a 12% increase in the probability of fruit abortion. No change in the numbers of ants or pollinators inside flowers was observed. This is the first support for the Distraction Hypothesis obtained under field conditions, showing ecological and plant fitness benefits of the distracting function of extrafloral nectar during anthesis. Synthesis. Our study provides the first field experimental support for the Distraction Hypothesis, suggesting that extrafloral nectaries located close to flowers may bribe ants away from reproductive structures during the crucial pollination period, reducing the probability of ant occupation of flowers, reducing ant-pollinator conflict and increasing plant reproductive success.

Project description:To our knowledge, there are no studies about the structure and ecological function of extrafloral nectaries (EFNs) in Opuntia robusta. This is the first description of EFNs in O. robusta, where young spines have an interesting structure and a secreting function, which are different from EFNs described in other Cactaceae species. We used light, scanning-electron, and transmission-electron microscopy to examine morphology, anatomy, and ultrastructure of the secretory spines in areoles in female and hermaphrodite individuals of O. robusta. Young cladodes develop areoles with modified and secretory spines as EFNs only active during the early growth phase. EFNs are non-vascularized structures, with no stomata, that consist of a basal meristematic tissue, a middle elongation region, and an apical secretory cone formed by large globular epidermal cells, containing nectar and medullar elongated cells. We observed the presence of Golgi apparatus, vesicles and plastids in the medullar and sup-epidermal cells of the spine. We propose that the nectar is stored in the globular cells at the apex of the spine and secreted by breaking through the globular cells or by pores. We recorded a more frequent presence of ants on younger cladode sprouts producing young secreting spines: this result is parallel with the predictions of Optimal Defense Hypothesis, which states that younger plant organs should be better defended than older ones because their loss produces a higher fitness impairment. Although Diaz-Castelazo's hypothesis states that a more complex structure of EFNs correlates with their lower among-organs dispersion, comparing to less complex EFNs, non-vascularized structure of EFNs in O. robusta is not associated with their higher among-organs dispersion likened to O. stricta, which produces vascularized EFNs. We provide evidence that this characteristic is not a good taxonomic feature of Opuntia genus. Moreover, the comparison of EFNs of O. robusta and O. stricta suggests that the hypothesis of Diaz-Castelazo should be revised: it is rather a rule but not a law.

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Nectar biosynthesis is conserved among floral and extrafloral nectaries.

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