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Pollination Drop Proteome and Reproductive Organ Transcriptome Comparison in Gnetum Reveals Entomophilous Adaptation

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G C A T T A C G G C A T genes Article Pollination Drop Proteome and Reproductive Organ Transcriptome Comparison in Gnetum Reveals Entomophilous Adaptation Chen Hou 1 , Richard M. K. Saunders 2 , Nan Deng 3,4 , Tao Wan 5,6 and Yingjuan Su 1,* 1 School of Life Sciences, Sun Yat-Sen University, Xingangxi Road No. 135, Guangzhou 510275, China; [email protected] 2 Division of Ecology & Biodiversity, School of Biological Sciences, The University of Hong Kong, Pokfulam Road, Hong Kong, China; [email protected] 3 Institute of Ecology, Hunan Academy of Forestry, Shaoshannan Road, No. 6581, Changsha 410004, China; [email protected] 4 Hunan Cili Forest Ecosystem State Research Station, Cili 427200, China 5 Key Laboratory of Southern Subtropical Plant Diversity, Fairy Lake Botanical Garden, Shenzhen & Chinese Academy of Science, Liantangxianhu Road, No. 160, Shenzhen 518004, China; [email protected] 6 Sino-Africa Joint Research Centre, Chinese Academy of Science, Moshan, Wuhan 430074, China * Correspondence: [email protected] Received: 30 August 2019; Accepted: 11 October 2019; Published: 12 October 2019 Abstract: Gnetum possesses morphologically bisexual but functionally unisexual reproductive structures that exude sugary pollination drops to attract insects. Previous studies have revealed that the arborescent species (G. gnemon L.) and the lianoid species (G. luofuense C.Y.Cheng) possess different pollination syndromes. This study compared the proteome in the pollination drops of these two species using label-free quantitative techniques. The transcriptomes of fertile reproductive units (FRUs) and sterile reproductive units (SRUs) for each species were furthermore compared using Illumina Hiseq sequencing, and integrated proteomic and transcriptomic analyses were subsequently performed. Our results show that the differentially expressed proteins between FRUs and SRUs were involved in carbohydrate metabolism, the biosynthesis of amino acids and ovule defense. In addition, the differentially expressed genes between the FRUs and SRUs (e.g., MADS-box genes) were engaged in reproductive development and the formation of pollination drops. The integrated protein-transcript analyses revealed that FRUs and their exudates were relatively conservative while the SRUs and their exudates were more diverse, probably functioning as pollinator attractants. The evolution of reproductive organs appears to be synchronized with changes in the pollination drop proteome of Gnetum, suggesting that insect-pollinated adaptations are not restricted to angiosperms but also occur in gymnosperms. Keywords: insect pollination; label-free quantitative sequencing; pollination drops; proteome; transcriptome; Gnetales 1. Introduction Animal pollination (and entomophily in particular) has a profound impact on species diversity and the geographical distribution of extant seed plants [1–3]. In marked contrast to angiosperms, however, entomophily has rarely been reported in gymnosperms, and is restricted to cycads [4–6] and Gnetales [7,8]. The reports of insect pollination in Gnetales (comprising three genera, Ephedra L., Welwitschia Hook.f. and Gnetum L.) include E. foeminea Forssk. [9–11], W. mirabilis Hook.f. [12] and several Gnetum species [13–17] (Figure1). In contrast, the majority of Ephedra species are wind Genes 2019, 10, 800; doi:10.3390/genes10100800 www.mdpi.com/journal/genes Genes 2019, 10, 800 2 of 21 Genes 2019, 10, x FOR PEER REVIEW 2 of 22 pollinated [9,10,18] and African Gnetum species are likely to be predominantly anemophilous [19,20] or withwith windwind pollination pollination as as a supplementa supplement to entomophilyto entomophily (e.g., (e.g.,G. parvifolium G. parvifolium(Warb.)(Warb.)W.C.Cheng W.C.Cheng [21]). Insect[21]). Insect pollination pollination has been has inferred been inferred to be the to plesiomorphic be the plesiomorphic condition condition within the within Gnetales, thewith Gnetales, wind pollinationwith wind pollination derived [9, 11derived,19]. [9,11,19]. Figure 1.1.ReproductiveReproductive evolution evolution and and morphology morphology of of GnetumGnetum..( (AA)) A A schematic schematic phylogeny illustrating the pollinationpollination biology biology and and inferred inferred reproductive reproductive evolution evolution of the Gnetalesof the Gnetales (modified (modified from Jörgensen from andJörgensen Rydin, and 2015). Rydin, Yellow 2015) arrows. Yellow denote arrows the denote phylogenetic the phylogenetic placement placement of the two of theGnetum two Gnetumspecies investigatedspecies investigated in the present in the present study. ( Bstudy–E) Reproductive. (B–E) Reproductive structures structures and pollination and pollination drops of dropsG. gnemon of G. andgnemonG. luofuenseand G. luofuense.(B) A female. (B) A strobilusfemale strobilus of G. gnemon of G. .(gnemonC) A. male (C) A strobilus male strobilus of G. gnemon of G. gnemonwith sterile with reproductivesterile reproductive units (SRUs) units (SRUs producing) producing pollination pollination drops. drops. (D) A ( femaleD) A female strobilus strobilus of G. luofuenseof G. luofuensewith awith moth a moth sucking sucking pollination pollination drops drops from from a fertile a fertile reproductive reproductive units units (FRU). (FRU) (.E (E)) A A male male strobilusstrobilus of G. luofuense with SRUs producing pollinationpollination drops.drops. Photographs by C. Hou. Pollination drops are essential in gymnosperm reproduction, providing a site for pollen attachment and a medium for germination [[2222–26].]. Gymnosperm pollination drops are composed of carbohydrates, minerals,minerals, lipids, lipids, amino amino acids acids and and proteins proteins [25 –[2528].–28 Among]. Among these these chemicals, chemicals, sugars sugars such assuch sucrose as sucrose are the are main the rewardmain reward for insect forpollinators, insect pollinators, and are and therefore are therefore comparable comparable to floral nectarto floral in angiospermsnectar in angiosperms [25–27,29]. [25 The–27,29 proteins]. The in p theroteins pollination in the dropspollination of gymnosperms drops of gymnosperms are furthermore are involvedfurthermore in involved varied physiological in varied physiological and ecological and ecological processes, processes, such as pollensuch as tube pollen growth tube growth [30,31], carbohydrate[30,31], carbohydrate metabolism metabolism [30] and [30] ovule and protection ovule protection against against fungi and fungi pathogens and pathogens [31–33]. [3 These1–33]. proteins,These prot foundeins, infound the apoplast,in the apoplast, are secreted are secreted by the nucellusby the nucellus and are referredand are referred to as secretome to as secretome proteins. Inproteins. contrast, In thecontrast, proteins the that proteins are not detectedthat are innot the detected apoplast in are the derived apoplast from are the derived breakdown from of the nucellusbreakdown during of the the nucellus formation during of a the pollen formation chamber, of anda pollen are known chamber, as degradomeand are known proteins as degradome [28,34,35]. Degradomeproteins [28,34,35] proteins. D inegradome the pollination proteins drops in of the gymnosperms pollination are drops probably of gymnosperms associated with are degenerated probably megasporesassociated with [36] anddegenerated the nucellus megaspores degeneration [36] mediated and the by programmednucellus degeneration cell death (PCD)mediated [37]. Forby anprogrammed example, acid cell phosphatase death (PCD) activity [37]. For was an found example, in the nucellusacid phosphat of the femalease activity reproductive was found units in of the an Ephedranucellusspecies of the [female38], and reproductive degradome units proteins of an have Ephedra been shownspecies to[38] be, moreand degradome abundant than proteins secretome have proteinsbeen shown in the to pollination be more dropsabundant of several than Ephedrasecretomespecies proteins [34]. in the pollination drops of several Ephedra species [34]. Pollination drops in the Gnetales have a typical function, with fertile reproductive units (FRUs) and sterile reproductive units (SRUs) producing sugar-rich drops as a reward for insect pollinators [7–9,11,19]. A recent study [35] has shown that protein numbers in the pollination drops of FRUs Genes 2019, 10, 800 3 of 21 Pollination drops in the Gnetales have a typical function, with fertile reproductive units (FRUs) and sterile reproductive units (SRUs) producing sugar-rich drops as a reward for insect pollinators [7–9,11,19]. A recent study [35] has shown that protein numbers in the pollination drops of FRUs (henceforth female drops) in G. gnemon L. and W. mirabilis (17 and one, respectively) are considerably fewer than in those of SRUs (male drops, 25 and 138 in the two species, respectively). The reasons why the protein numbers in female and male drops differ so markedly and their association with insect pollination have yet to be convincingly explained. This might be associated with the fact that the total sugar concentration (TSC) in the male drops of G. gnemon was significantly lower than the female drops, although the relative proportion of different sugar types was identical between the female and male drops [27]. In addition, many degradome proteins were reported in the female drops of seven Ephedra species, as well as male drops of G. gnemon and W. mirabilis [34,35]. The degradome proteins are the consequence of cell apoptosis during the formation of the pollen chamber, as reported in
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