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True Nectar Or Stigmatic Secretion? True nectar or stigmatic secretion? Structural evidence elucidates an old controversy regarding nectaries in Anthurium Élder Antônio Sousa Paiva, Igor Ballego-campos, Marc Gibernau To cite this version: Élder Antônio Sousa Paiva, Igor Ballego-campos, Marc Gibernau. True nectar or stigmatic secretion? Structural evidence elucidates an old controversy regarding nectaries in Anthurium. American Journal of Botany, Botanical Society of America, 2021, 108 (1), pp.37-50. 10.1002/ajb2.1595. hal-03113084 HAL Id: hal-03113084 https://hal.archives-ouvertes.fr/hal-03113084 Submitted on 18 Jan 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. 1 American Journal of Botany 108(1) : 1-14. doi:10.1002/ajb2.1595 2 3 Research article 4 True nectar or stigmatic secretion? Structural evidence elucidates an old 5 controversy regarding nectaries in Anthurium 6 7 Élder Antônio Sousa Paiva1*, Igor Ballego-Campos1 and Marc Gibernau2 8 9 1Departamento de Botânica, Instituto de Ciências Biológicas, Universidade Federal de 10 Minas Gerais, Belo Horizonte, 31270-901, MG, Brazil. 11 2CNRS-University of Corsica Pascal Paoli, UMR 6134 SPE, Equipe Chimie et 12 Biomasse, Route des Sanguinaires - Vignola, 20000 Ajaccio, France 13 *Corresponding author. Email: [email protected] 14 15 Manuscript received _______; revision accepted _______. 16 17 18 Nectar and stigmatic secretion in Anthurium 19 20 21 22 23 24 25 26 27 28 29 1 30 31 32 ABSTRACT 33 PREMISE: Floral rewards are essential in the understanding of floral function and 34 evolution of the relationships between flowers and pollinators. Due to the scarcity of 35 structural studies, the presence of sugars in stigmatic exudates, as well as the presence 36 of floral nectaries in Anthurium, is quite controversial. To solve this, we investigated the 37 floral anatomy of A. andraeanum to elucidate whether (i) tepals are secretory organs, 38 (ii) tepals possess a structurally recognizable nectary, and (iii) tepalar secretion differs 39 from stigmatic secretion. 40 METHODS: Floral structure was assessed through light and electron microscopy on 41 samples of immature, pistillate, and staminate flowers. The dynamic of the starch 42 reserve was investigated, and the sugar content in the floral exudates was assessed using 43 thin-layer chromatography. 44 RESULTS: Sugar analysis did not detect sucrose, glucose, or fructose in the stigmatic 45 secretions, but confirmed their presence in the tepalar ones. Stigmatic secretion was 46 produced by secretory stigmatic papillae, while tepalar exudates were produced by non- 47 vascularized nectaries located in the apex of tepals. These nectaries were characterized 48 by cells with cytoplasm rich in organelles, as well as a high content of calcium oxalate 49 crystals and the presence of modified stomata. 50 CONCLUSIONS: Our results showed for the first time a nectary presence on tepals 51 and true nectar secretion for A. andraeanum. Stigmatic secretion appears to be a distinct 52 substance, and its often-reported sugar content seems to be a result of sample 53 contamination. Nectar and stigmatic secretion have been often mistaken in other 54 Anthurium species, and deserve a revision for this genus. 55 56 KEY WORDS: Araceae; floral ultrastructure; floral nectary; floral rewards; nectar 57 secretion; stigmatic papillae; sugary secretions 58 59 60 61 2 62 63 INTRODUCTION 64 Floral rewards are essential in the understanding of floral function and evolution 65 of plant-pollinator interactions (Baker and Baker, 1975; Cruden et al. 1983; 66 Abrahamczyk et al., 2017). By exuding nectar, oils, scents or resins, floral glands are 67 key features in plant reproductive success and in the development of the diverse 68 relationships between flower and pollinators (Tölke et al., 2020). 69 Araceae, one of the most diverse monocot families, is mainly insect-pollinated 70 (Gibernau 2011, 2016; Díaz-Jiménez et al., 2019), but surprisingly they are traditionally 71 considered to be nectarless (Schwerdtfeger et al., 2002). Interestingly, sugars have been 72 reported from secretions produced by the stigma in Anthurium (Bleiweiss et al., 2019), 73 resulting in a significant controversy regarding floral exudates in the genus, especially 74 concerning the occurrence of true nectar in its flowers. Quite straightforward terms, 75 such as “nectaries”, “nectar”, and “pollination drops” have been indifferently used for 76 Anthurium floral secretions leading to confusion not only of words, but also of the floral 77 physiological processes. In fact, despite the presence of sugary secretion in the flowers 78 of this diverse neotropical genus, nectary could not accurately point out. Indeed, we 79 even surely answer whether or not such a nectary exists. Here, we have studied in detail 80 the floral anatomy of Anthurium, and the chemical nature of its secretions to clarify 81 these issues. This is a crucial point that may help to understand the floral biology and 82 evolution of plant-insect interaction in aroids. On the other hand, there are gaps 83 regarding the prospection of floral secretory structures in Anthurium, which precludes 84 analyses concerning the homology of floral glands. 85 Most of the pollination interactions in Araceae are mutualisms (Chartier et al., 86 2014). Three types of rewarding mutualisms have evolved in this plant group; the 3 87 inflorescences “offering” a food reward, such as stigmatic exudates, nectar and/or 88 pollen (Diaz and Kite, 2006; Gibernau, 2011); a sexual reward such as a liquid floral 89 perfume for male euglossine bees (Hentrich et al., 2007, 2010; Etl et al., 2017); a 90 mating site with food rewards (Maia et al., 2013) or a mating and oviposition site 91 (Franz, 2007). 92 Anthurium is the largest aroid genus comprising 950 described and more than 93 2,000 estimated Neotropical species (Boyce and Croat, 2018). This taxonomically 94 complex megagenus is one of the most morphologically and ecologically diverse aroid 95 genera (Carlsen and Croat, 2019). Historically considered to be pollinated primarily by 96 euglossine bees (Croat, 1980), Anthurium species also exhibit highly diverse pollination 97 interactions, which include different kinds of bees (Apini, Augochlorini, Euglossini, 98 Halictini, Meliponini, Tapinotaspidini), beetles (Curculionidae), and flies 99 (Cecidomyiidae, Drosophilidae); but also lepidopterans (Lepidotera), thrips 100 (Thysanoptera) and even hummingbirds (see reviews Hartley and Gibernau, 2019; and 101 Díaz-Jiménez et al., 2019). However, A. andraeanum has been reported to be visited by 102 fragrance collecting male euglossine bees of Eulaema seabrai in wild Brazilian 103 populations (Rocha-Filho et al., 2012). 104 All Araceae have a protogynous flowering sequence (Díaz-Jiménez et al., 2019), 105 but its duration in Anthurium is quite variable, ranging from one week to over 30 days 106 (Croat, 1980; Hentrich et al., 2010). Flowering starts with the female phase, with the 107 production of drops of stigmatic secretion in some species, while in others, stigmas just 108 have a moist appearance indicating their receptivity (Croat, 1980; Etl et al., 2017). 109 Subsequently, the inflorescence enters a male phase, with the stamens emerging from 110 several flowers in a progressive sequence (Croat, 1980; Hentrich et al., 2010). 4 111 It is well established that during the pistillate phase, the flowers exude a 112 secretion through the stigma that is the so-called pollination drop. Pollination drops are 113 better known as fluid secretions produced by the ovules of gymnosperms, which are 114 involved in reproduction (Coulter et al., 2012). However, stigmatic exudates are 115 reported in flowers of several angiosperm species, sometimes considered similar to 116 pollination drops of gymnosperms, in which they are related to male gamete transport 117 towards the megagametophyte (see Nepi et al., 2009 and references therein). From now 118 on, we will adopt the term stigmatic secretion, even though pollination drop is usually 119 used for stigmatic exudates in Araceae. In Anthurium species, the stigmatic secretion 120 can form conspicuous drops on the stigma surface of each flower and may contain 121 soluble sugars, being considered analogous to nectar (Bleiweiss et al., 2019) or even 122 considered nectar by some authors (Croat, 1980; Kraemer and Schmitt, 1999; Franz, 123 2007). However, not one of these studies interprets the stigma as a nectary. 124 In Araceae, the presence of sugars in the stigmatic secretion is reported for 125 genera other than Anthurium, as in Monstera (Ramirez and Gomez, 1978) and Arum 126 (Diaz and Kite, 2006), although in the latter the authors highlight the small proportion 127 of sugars, present at a lower concentration than observed in the nectar. The stigmatic 128 secretion is consistently sweet, and in the case of A. seibertii Croat & R.A.Baker, it was 129 reported to contain 8% sugar comprised of a combination of sucrose, glucose, and 130 fructose (in Croat, 1980). In Arum maculatum L., a terrestrial species widespread across 131 most of Europe and the Caucasus, the concentration of sucrose equivalent ranged 132 between 9–12.5% in the stigmatic secretions tested. This sugar concentration was only 133 slightly higher than that of the phloem in the same species (8% sucrose equivalent) 134 (Lack and Diaz, 1991). In Arum hygrophilum Boiss. of Israel, the stigmatic secretions 135 contained above 5% sugar (Koach, 1985). 5 136 The presence of true floral nectaries in Anthurium is quite controversial (see 137 Hartley et al., 2017 and references therein). Aroids and the genus Anthurium, in 138 particular, are supposed to be nectarless (Schwerdtfeger et al., 2002).
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