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Links Between Morphology and Function of the Pollen Wall: an Experimental Approach

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Links Between Morphology and Function of the Pollen Wall: an Experimental Approach See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/291420840 Links between morphology and function of the pollen wall: An experimental approach Article in Botanical Journal of the Linnean Society · April 2016 Impact Factor: 2.53 · DOI: 10.1111/boj.12378 READS 58 7 authors, including: Christian Raquin François Brisset French National Centre for Scientific Resea… Université Paris-Saclay 42 PUBLICATIONS 507 CITATIONS 112 PUBLICATIONS 1,123 CITATIONS SEE PROFILE SEE PROFILE Beatrice Albert Pierre-Henri Gouyon Université Paris-Sud 11 Muséum National d'Histoire Naturelle 23 PUBLICATIONS 364 CITATIONS 156 PUBLICATIONS 4,557 CITATIONS SEE PROFILE SEE PROFILE All in-text references underlined in blue are linked to publications on ResearchGate, Available from: Alexis Matamoro-Vidal letting you access and read them immediately. Retrieved on: 20 April 2016 Botanical Journal of the Linnean Society, 2016, 180, 478–490. With 6 figures Links between morphology and function of the pollen wall: an experimental approach ALEXIS MATAMORO-VIDAL1,2,*, CHRISTIAN RAQUIN2, FRANCß OIS BRISSET3,HEL ENE COLAS1, BENJAMIN IZAC2,BEATRICE ALBERT2† and PIERRE-HENRI GOUYON1† 1Departement Systematique et Evolution, Museum national d’Histoire naturelle, UMR 7205 MNHN- CNRS, Paris, 75005, France 2Universite Paris Sud-11. Ecologie, Systematique et Evolution, UMR 8079 CNRS-AgroParisTech, Orsay, 91405, France 3Universite Paris Sud-11. ICMMO, UMR 8182 CNRS, Orsay, 91405, France Received 17 April 2015; revised 3 December 2015; accepted for publication 18 December 2015 The wall of pollen grains exhibits morphological variation in many features including apertures, ornamentation and thickness, but the function of these characters remains to be clarified. It has been suggested that they are involved in the accommodation of volume changes (harmomegathy). To investigate this further, we developed a protocol that induces a controlled hydration of the pollen without affecting its metabolism and we applied it to six species differing in their pollen wall morphology. The entry of water caused pollen swelling and volume increase leading to breakage of the wall and/or of the plasma membrane, such that the per cent of intact grains was negatively correlated with the level of hydration. Qualitative and quantitative differences were observed between the species. Breakage of the exine was observed only in pollen lacking apertures and with thin exine. Variation in the exine ornamentation and thickness could explain the interspecific differences observed for the rates of breakage of the plasma membrane. Our results suggest that pollen wall morphology matters for survival and maintenance of pollen integrity further to volume increase due to hydration. We propose a rationale for future studies that should allow disentangling the contribution of different pollen morphological and physiological features to harmomegathy. © 2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016, 180, 478–490. ADDITIONAL KEYWORDS: aperture pattern – exine ornamentation – harmomegathy – natural selection. INTRODUCTION drates and eventually germinates (Edlund, Swanson & Preuss, 2004). Additional hydration–dehydration Plant male success depends largely on the viability phases can occur before or during the dispersal of of pollen until the pollen tube reaches and fertilizes the grain, depending on the relative humidity of the ovules. This makes the understanding of how pollen environment and of the time of dispersal (Lisci, grains adapt to environmental fluctuations an Tanda & Pacini, 1994; Pacini, 2000; Franchi et al., important issue for plant evolution. During its life 2011). cycle, a pollen grain can go through several hydra- Many structural, physiological and molecular tion and dehydration phases. When pollen reaches mechanisms are used by pollen grains to adjust to maturity in the anther, it is transferred from a liq- changes in water content and to maintain internal uid environment to an atmospheric environment. In stability (Firon, Nepi & Pacini, 2012). The external most angiosperm species, pollen dehydrates and wall of the pollen (the exine) is made of a highly remains in this state until it lands on a compatible resistant polymer called sporopollenin. Mechanisms stigma. Once it is on the stigma, the pollen rehy- allowing changes in the shape and in the volume of the wall in order to accommodate the variation in *Corresponding author. E-mail: [email protected] the volume of the cytoplasm caused by changing †These authors contributed equally. hydration are thus necessary to avoid pollen 478 © 2016 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016, 180, 478–490 POLLEN WALL MORPHOLOGY AND FUNCTION 479 breakage. The term harmomegathy was proposed by uniformly thin. In these pollen grains, the whole sur- Wodehouse (1935) to qualify such an accommodation face of the wall can be considered as an aperture. process, which is necessary to allow a retraction This type of pollen is thus referred to as omniapertu- (bending) of the wall during dehydration or an rate (Thanikaimoni et al., 1984). At the other extension (stretching) during hydration. Here, we extreme, there are pollen grains with a uniformly present an experimental approach aimed at thick exine. studying in a quantitative manner how pollen mor- The innermost layer of the pollen wall, the intine, phological and physiological characteristics may is beneath the exine and borders the surface of the help the grain to accommodate a volume increase cytoplasm. The intine is composed of pectin and cel- and avoid pollen breakage further to hydration. On lulose and it is much more capable of stretching the basis of the data obtained from this approach and contraction than the exine (Heslop-Harrison & and from published work, we propose a hypothetical Heslop-Harrison, 1982). Variability in the thickness model predicting response of the grain to hydration of the intine wall might affect the stretching pro- depending on its morphological and physiological cess and the efficiency of volume-change accommo- characteristics. dation. Two characteristics of the pollen wall, aperture Differences in aperture number, wall ornamenta- sites and exine ornamentation, have been suggested tion, and thickness, are likely to produce differences to be involved in volume-change accommodation on in harmomegathic efficiency. We studied whether the basis of comparative and theoretical approaches pollen morphology may affect the capacity of the (Wodehouse, 1935; Payne, 1972; Heslop-Harrison, grain to accommodate a volume-increase resulting 1979b; Muller, 1979; Blackmore & Barnes, 1986; from hydration. For this, we developed a protocol Thanikaimoni, 1986; Scotland, Barnes & Blackmore, that allows the hydration of the grains in a dose- 1990; Halbritter & Hesse, 2004; Chichiricco, 2007; dependent manner, without changing metabolism: Katifori et al., 2010; Volkova, Severova & Polevova, pollen grains were placed in solutions with different 2013). Apertures are sites on the wall where the concentrations of a non-metabolic sugar, which cre- exine is thin or absent (Fig. 1A–D). During dehydra- ates different levels of hydration without affecting tion of the grain, the membrane of the aperture sites the metabolism of the grains. We scored the rates folds inward, so that the edges of each aperture are of breakage in the exine and in the plasma mem- touching each other (Volkova et al., 2013), closing up brane of pollen grains exposed to four levels of the aperture site. It has been shown by mathemati- hydration. This was done for pollen grains of six cal modelling that the area and the shape of the species that differ in their aperture sites, wall orna- apertures contribute to harmomegathy by reducing mentation and thickness. The percentage of intact the necessity of the wall to stretch and bend in order pollen grains was found to be negatively correlated to accommodate volume-changes (Katifori et al., with the level of hydration. In addition, qualitative 2010). However, even if the apertural sites may and quantitative differences between the species accommodate a part of the volume-changes, some were observed. We summarize in a model how the flexibility of the wall is required: several species pro- morphological properties of the pollen wall could duce pollen with tiny apertures or totally lacking explain these differences. apertures (Fig. 1E, F), and they are still able to accommodate volume changes. This additional flexi- bility might be provided by other properties of the MATERIAL AND METHODS exine. Exine ornamentation is the pattern of the outer LIVING MATERIAL wall of the pollen (Fig. 1A0–F0) and is variable. For Pollen grains of six species were studied (Table 1). example, some species produce pollen with network- Plants were grown in the laboratory greenhouse like exine patterns made of wide spaces bordered by (Orsay, France) using material obtained from the ridges of exine narrower than these spaces (reticu- Parc Botanique de Launay (PBL) for the following late pattern, Fig. 1D0,E0). Other exine patterns are species: Carica papaya L. (voucher PBL-000536), Iris made of exine units (pilea) that have loose connec- germanica L. (voucher PBL-011139), Jatropha inte- tions with each other (crotonoid pattern, Fig. 1F0). gerrima Jacq. (voucher PBL-018013), Nicotiana syl- These exine units may move apart from each other vestris Speg. & Comes (voucher PBL-019066), and facilitate volume-changes
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