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.
Floral nectar is a rich secretion produced by the nectary gland and is offered as reward to attract pollinators leading to improved seed set. Nectars are composed of a complex mixture of sugars, amino acids, proteins, vitamins, lipids, organic and inorganic acids. This composition is influenced by several factors, including floral morphology, mechanism of nectar secretion, time of flowering, and visitation by pollinators. The objective of this study was to determine the contributions of flowering time, plant phylogeny, and pollinator selection on nectar composition in Nicotiana. The main classes of nectar metabolites (sugars and amino acids) were quantified using gas chromatography/mass spectrometric analytical platforms to identify differences among fifteen Nicotiana species representing day- and night-flowering plants from ten sections of the genus that are visited by five different primary pollinators. The nectar metabolomes of different Nicotiana species can predict the feeding preferences of the target pollinator(s) of each species, and the nectar sugars (i.e., glucose, fructose, and sucrose) are a distinguishing feature of Nicotiana species phylogeny. Moreover, comparative statistical analysis indicate that pollinators are a stronger determinant of nectar composition than plant phylogeny.
23United States 24 25 Author contributions 26 ECC, CJC, and BJN conceived and planned the study. Sample collection, microscopy, and 27 metabolomic analyses were conducted by ECC, SNM, and NAMF. Additional contributions 28 for microscopic analyses were provided by HTH. RNA preparation was completed by PMK, 29 RR, and CJC. MH processed all RNAseq data and conducted informatics analyses in 30 conjunction with ECC. ECC and BJN wrote the manuscript with feedback from all 31 coauthors. 33One sentence summary 34 The eccrine-based model of nectar synthesis and secretion is conserved in both trichomatic 35 and extrafloral nectaries determined by a system-based comparison of cotton (Gossypium 36 hirsutum) nectaries. 37 Abstract 47 Nectar is a primary reward mediating plant-animal mutualisms to improve plant fitness and 48 reproductive success. In Gossypium hirsutum (cotton), four distinct trichomatic nectaries 49 develop, one floral and three extrafloral. The secreted floral and extrafloral nectars serve 50 different purposes, with the floral nectar attracting bees to promote pollination and the 51 extrafloral nectar attracting predatory insects as a means of indirect resistance from herbivores. 52 Cotton therefore provides an ideal system to contrast mechanisms of nectar production and 53 nectar composition between floral and extrafloral nectaries. Here, we report the transcriptome, 54 ultrastructure, and metabolite spatial distribution using mass spectrometric imaging of the four 55 cotton nectary types throughout development. Additionally, the secreted nectar metabolomes 56 were defined and were jointly composed of 197 analytes, 60 of which were identified. 57 Integration of theses datasets support the coordination of merocrine-based and eccrine-based 58 models of nectar synthesis. The nectary ultrastructure supports the merocrine-based model due 59 to the abundance of rough endoplasmic reticulum positioned parallel to the cell walls and 60 profusion of vesicles fusing to the plasma membranes. The eccrine-based model which consist 61 of a progression from starch synthesis to starch degradation and to sucrose biosynthesis was 62 supported by gene expression data. This demonstrates conservation of the eccrine-based model 63 for the first time in both trichomatic and extrafloral nectaries. Lastly, nectary gene expression 64 data provided evidence to support de novo synthesis of amino acids detected in the secreted 65 nectars.66 67 68 69 130 synthesis to assess for the first time whether this model is conserved among trichomatic and 131 extrafloral nectaries. 132 Results 133 Domesticated Upland cotton, G. hirsutum (TM-1), develops four types of nectaries, 134 three are extrafloral and one is floral, and all consist of multicellular glandular trichomes, 135 specifically called papillae. The three extrafloral nectary types, foliar, bracteal, and 136 circumbracteal, are subcategorized as vegetative or reproductive. The vegetative foliar nectary 137is located on the abaxial surface of the leaf midrib ( Fig. 1A; Fig...
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