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Effect of Aperture Number on Pollen Germination, Survival and Reproductive Success in Arabidopsis Thaliana

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Effect of Aperture Number on Pollen Germination, Survival and Reproductive Success in Arabidopsis Thaliana Annals of Botany 121: 733–740, 2018 doi:10.1093/aob/mcx206, available online at www.academic.oup.com/aob Effect of aperture number on pollen germination, survival and reproductive success in Arabidopsis thaliana Downloaded from https://academic.oup.com/aob/article-abstract/121/4/733/4816140 by Valparaiso University user on 05 February 2019 Béatrice Albert1,*, Adrienne Ressayre2, Christine Dillmann2, Ann L. Carlson3, Robert J. Swanson3, Pierre-Henri Gouyon4 and Anna A. Dobritsa5 1Ecologie Systématique Evolution, Univ. Paris-Sud, CNRS, AgroParisTech, Université Paris-Saclay, 91405 Orsay cedex, France, 2UMR de Génétique Végétale, Univ. Paris-Sud, INRA, CNRS, Université Paris-Saclay, Gif sur Yvette, F-91190, France, 3Biology Department, Valparaiso University, Valparaiso, IN 46383, USA, 4Institut de Systématique, Évolution, Biodiversité, ISYEB-UMR 7205-CNRS, MNHN, UPMC, EPHE, Muséum National d’Histoire Naturelle, Sorbonne Universités, 57 rue Cuvier, CP39, F-75005, Paris, France and 5Department of Molecular Genetics and Center for Applied Plant Sciences, The Ohio State University, 015 Rightmire Hall, 1060 Carmack Road, Columbus, OH 43210, USA *For correspondence. E-mail [email protected] Received: 3 April 2017 Returned for revision: 27 September 2017 Editorial decision: 16 November 2017 Accepted: 15 December 2017 Published electronically 18 January 2018 • Background and Aims Pollen grains of flowering plants display a fascinating diversity of forms, including diverse patterns of apertures, the specialized areas on the pollen surface that commonly serve as the sites of pollen tube initiation and, therefore, might play a key role in reproduction. Although many aperture patterns exist in angiosperms, pollen with three apertures (triaperturate) constitutes the predominant pollen type found in eudicot species. The aim of this study was to explore whether having three apertures provides selective advantages over other aperture patterns in terms of pollen survival, germination and reproductive success, which could potentially explain the prevalence of triaperturate pollen among eudicots. • Methods The in vivo pollen germination, pollen tube growth, longevity and competitive ability to sire seeds were compared among pollen grains of Arabidopsis thaliana with different aperture numbers. For this, an arabidopsis pollen aperture series was used, which included the triaperturate wild type, as well as mutants without an aperture (inaperturate) and with more than three apertures. • Key Results Aperture number appears to influence pollen grain performance. In most germination and longevity experiments, the triaperturate and inaperturate pollen grains performed better than pollen with higher aperture numbers. In mixed pollinations, in which triaperturate and inaperturate pollen were forced to compete with each other, the triaperturate pollen outperformed the inaperturate pollen. • Conclusions Triaperturate pollen grains might provide the best trade-off among various pollen performance traits, thus explaining the prevalence of this morphological trait in the eudicot clade. Key words: Pollen aperture, Arabidopsis thaliana, pollen germination, longevity, pollen performance, competitive pollination, reproductive success INTRODUCTION performance, from survival to germination of pollen tubes (Wodehouse, 1935; Edlund et al., 2004; Halbritter and Hesse, Pollen grains, the male gametophytes of flowering plants, are 2004; Katifori et al., 2010; Vieira and Feijó, 2016). morphologically diverse across species, exhibiting differences Although a wide range of aperture patterns exists in angio- in size, shape, and macro- and ultrastructures of their pollen sperms (Erdtman, 1952; PalDat, http://www.paldat.org/), in walls (Erdtman, 1952; Heslop-Harrison, 1971; PalDat, http:// most species apertures exhibit one of the two predominant www.paldat.org/). One type of structure commonly present on patterns, considered to be two evolutionary stases (Bailey and the pollen surface are apertures, the areas characterized by a Nast, 1943; Matamoro-Vidal et al., 2016a). Basal angiosperms reduced deposition of the pollen wall exine (Hesse et al., 2009). and monocots mainly produce monosulcate pollen grains, char- Like other pollen features, aperture patterns are highly variable acterized by a single furrow-like aperture located at the distal among species: apertures can differ in morphology (pore, fur- pollen pole, while eudicots largely produce tricolpate pollen row or both), in number (from no apertures to >100) and in grains with three furrow-like, longitudinal apertures (Walker positions on the pollen surface (polar, equatorial or distributed and Doyle, 1975; Wortley et al., 2015), resulting in eudicots throughout the surface) (Erdtman, 1952). Apertures have been sometimes being referred to as the tricolpate clade (Donoghue proposed to play multiple roles: accommodate pollen deform- and Doyle, 1989; Judd and Olmstead, 2004). ation during changing hydration conditions; facilitate water The prevalence of the tricolpate, or more generally triapertu- and gas exchange; and participate in various aspects of pollen rate, pollen among eudicot species has long puzzled palynologists © The Author(s) 2018. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: [email protected]. 734 Albert et al. — Pollen aperture number influences pollen performance in Arabidopsis and evolutionary biologists (Walker and Doyle, 1975; Furness pollen grains (Prieu et al., 2016; Reeder et al., 2016) (pollen and Rudall, 2004). Previous studies have proposed that the triap- length = 24.25 ± 2.00 µm; n = 11). The mutation in the OSD1 erturate stasis in eudicots is more likely to be caused by selective gene leads to the production of functional diploid pollen grains pressures favouring this particular pollen type than by develop- due to the absence of the second meiotic division (d’Erfurth mental constraints limiting other pollen morphologies (Albert et al., 2009). Unlike in the triaperturate and four-aperturate pol- et al., 2009; Matamoro-Vidal et al., 2012; Matamoro-Vidal len grains, in the six- and eight-aperturate pollen, apertures were et al., 2016a). This idea is consistent with the general trend in no longer distributed around the pollen equator. Instead, they Downloaded from https://academic.oup.com/aob/article-abstract/121/4/733/4816140 by Valparaiso University user on 05 February 2019 angiosperms towards an increase in aperture number over evo- usually formed the edges of a tetrahedron or a square-based pyra- lutionary time, suggesting that aperture patterns might have an mid, respectively (Prieu et al., 2016; Reeder et al., 2016). influence on pollen reproductive performance (Walker, 1974; Walker and Doyle, 1975; Van Campo, 1976; Doyle and Hotton, 1991; Furness and Rudall, 2004). Growth conditions Although several studies have previously looked at various aspects of pollen performance (Williams and Mazer, 2016), the Plants were grown in a climatic chamber under the follow- question of whether it is indeed influenced by aperture patterns ing conditions: 16 h of light at 20 °C; 8 h of darkness at 16 °C. has remained largely unanswered (Dajoz et al., 1991, 1993; Experiments were carried out as soon as plants produced flow- Till-Bottraud et al., 2001; Edlund et al., 2004). ers (approx. 6 weeks after sowing). Here, we took advantage of recently characterized arabi- dopsis mutants which, together with a wild-type arabidopsis, constitute a pollen aperture series. They produce pollen with zero, three, four and a mix of four to eight apertures (d’Erfurth In vivo germination and pollen tube growth assays et al., 2009; Dobritsa et al., 2011; Dobritsa and Coerper, 2012; The in vivo germination experiments (Fig. 1) were per- Reeder et al., 2016), thereby covering most of the range of formed using nearly open flowers with non-dehisced stamens aperture numbers found in eudicots and allowing us to use pol- [stage 13 flowers (Alvarez-Buylla et al., 2010)] as the source len from a single species to assess the role of aperture patterns. of receptive pistils. Each receptive flower was removed from We used this series to test if differences in aperture numbers the plant and emasculated. Stigmas were then pollinated with affect four specific aspects of pollen performance – on-stigma pollen from the flowers that opened that day (young pollen pollen germination, growth of pollen tubes, pollen longevity grains), or from flowers that opened 3 d previously (old pollen and ability to sire seeds in competitive pollinations – and, if so, grains). Pollination was carried out on receptive flowers of the whether triaperturate pollen, the predominant class among the same genotype as pollen. Pollen grains were carefully depos- pollen of eudicots, performs better than the other pollen types ited on stigmas using tweezers under a dissecting microscope in these assays. to ensure that each pollen grain was in contact with the stigma surface. Care was taken to place enough pollen to provide suffi- cient statistical power for the germination percentage analysis, MATERIALS AND METHODS but not so much that it would make scoring germination events difficult. The average number of pollen grains per stigma was 55 ± 24. The pollinated flowers were incubated on a Petri dish Arabidopsis lines lined with filter paper dipped in water for either 30 min or 4 h, We used several Arabidopsis thaliana mutants that differ in after which their stigmas were
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