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The Morphophysiological Dormancy in Amborella Trichopoda Seeds Is a Pleisiomorphic Trait in Angiosperms

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The Morphophysiological Dormancy in Amborella Trichopoda Seeds Is a Pleisiomorphic Trait in Angiosperms Annals of Botany Page 1 of 10 doi:10.1093/aob/mcw244, available online at www.aob.oxfordjournals.org The morphophysiological dormancy in Amborella trichopoda seeds is a pleisiomorphic trait in angiosperms Bruno Fogliani1,2,*, Gildas Gateble^ ´1, Matthieu Villegente2, Isabelle Fabre1, Nicolas Klein1,2, Nicolas Anger1, Carol C. Baskin3,4 and Charlie P. Scutt5 1Institut Agronomique ne´o-Cale´donien (IAC), BP 73 Port Laguerre, 98890 Paı¨ta, New Caledonia, 2Laboratoire Insulaire du Vivant et de l’Environnement (LIVE)–EA 4243, University of New Caledonia (UNC), BP R4, 98851 Noumea, New Caledonia, 3Department of Biology, University of Kentucky, Lexington, KY 40506, USA, 4Department of Plant and Soil Sciences, University of Kentucky, Lexington, KY 40546, USA and 5Reproduction et De´veloppement des Plantes (RDP; UMR5667, CNRS- INRA-Universite´ de Lyon), Ecole Normale Supe´rieure de Lyon, 46 alle´e d’Italie, 69364 Lyon Cedex 07, France *For correspondence. E-mail [email protected] Received: 14 July 2016 Returned for revision: 5 September 2016 Editorial decision: 5 October 2016 Background and Aims Recent parsimony-based reconstructions suggest that seeds of early angiosperms had ei- ther morphophysiological or physiological dormancy, with the former considered as more probable. The aim of this study was to determine the class of seed dormancy present in Amborella trichopoda, the sole living representative of the most basal angiosperm lineage Amborellales, with a view to resolving fully the class of dormancy present at the base of the angiosperm clade. Methods Drupes of A. trichopoda without fleshy parts were germinated and dissected to observe their structure and embryo growth. Pre-treatments including acid scarification, gibberellin treatment and seed excision were tested to determine their influence on dormancy breakage and germination. Character-state mapping by maximum parsi- mony, incorporating data from the present work and published sources, was then used to determine the likely class of dormancy present in early angiosperms. Key Results Germination in A. trichopoda requires a warm stratification period of at least approx. 90 d, which is followed by endosperm swelling, causing the water-permeable pericarp–mesocarp envelope to split open. The em- bryo then grows rapidly within the seed, to radicle emergence some 17 d later and cotyledon emergence after an ad- ditional 24 d. Gibberellin treatment, acid scarification and excision of seeds from the surrounding drupe tissues all promoted germination by shortening the initial phase of dormancy, prior to embryo growth. Conclusions Seeds of A. trichopoda have non-deep simple morphophysiological dormancy, in which mechanical resis- tance of the pericarp–mesocarp envelope plays a key role in the initial physiological phase. Maximum parsimony analy- ses, including data obtained in the present work, indicate that morphophysiological dormancy is likely to be a pleisiomor- phic trait in flowering plants. The significance of this conclusion for studies of early angiosperm evolution is discussed. Key words: Amborellaceae, Amborella trichopoda, evolution of seed dormancy, ANA-grade angiosperm, seed germination, morphophysiological dormancy, rudimentary embryo. INTRODUCTION As dormancy is a key trait for survival and fitness (Linkies et al.,2010), the reconstruction of the evolution of dormancy Seed dormancy can be defined as the retardation of radicle emer- mechanisms is of particular interest. In the angiosperms, such gence (germination) under otherwise favourable conditions for reconstruction work is now possible as studies performed germination (Bewley et al., 2015). There are five major classes over the last approx. 15 years (summarized at http://www. of seed dormancy: morphological, physiological, morphophysio- mobot.org/MOBOT/research/APweb/; Byng et al.,2016) have logical, physical and combinational, within each of which further provided a solid phylogenetic framework. According to the sub-classes may be recognized (Baskin and Baskin, 2004). majority of phylogenetic studies, the orders Amborellales, Among the five major classes of dormancy, physiological dor- Nymphaeales and Austrobaileyales, collectively termed the mancy (PD) is characterized by the presence in the mature seed ANA grade, diverged sequentially from a remaining lineage of a fully developed embryo, which takes >30 d following imbi- from which all other living angiosperms, the euangiosperms, bition before the radicle emerges. In contrast, morphological dor- are descended. A slightly different evolutionary hypothesis, mancy (MD) is characterized by thepresenceinthematureseed which has emerged from a few analyses (Qiu et al.,2001, of an incompletely developed embryo that, under appropriate 2010; Xi et al., 2014), places Amborellales and Nymphaeales conditions, begins to grow immediately following imbibition, together in a first-diverging angiosperm clade, with but takes <30 d to complete development before the radicle Austrobaileyales as a second-diverging lineage, sister to euan- emerges. In morphophysiological dormancy (MPD), a combina- giosperms. The euangiosperms are composed of the major tionofPDandMDispresent,delayinggerminationfor>30 d. groups of eudicots and monocots, in addition to the moderately VC The Author 2017. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: [email protected] Page 2 of 10 Fogliani et al. — Seed dormancy in the first flowering plants sized magnoliid clade and the two smaller taxa of MATERIALS AND METHODS Chloranthaceae and Ceratophyllum. Fruit collection As a result of the largely successful resolution of angiosperm phylogeny, analyses of the basally diverging ANA-grade line- Mature fruits of Amborella trichopoda were harvested during the ages have been particularly informative for the reconstruction season of natural dispersal from plants growing at an altitude of of character states at the base of the flowering plants. The likely around 600 m on the Plateau de Dogny in the central part of earliest diverging ANA-grade order, Amborellales, contains Grande Terre (S2137021Á600, E16552006Á300), New Caledonia. Amborella trichopoda Baill. as its only living representative. One batch, collected on 8 July 2008 and sown7dlater,wasused This species is a dioecious shrub, endemic to the understorey of for dissection and observations on embryo development, while a humid tropical forests on the southern Pacific island of New second batch was harvested on 23 December 2008 and used for Caledonia. The mature A. trichopoda embryo is short and broad germination experiments, starting on 15 January 2009. Empty (Bailey and Swamy, 1948; Tobe et al., 2000), suggesting the drupes were removed under vacuum, and fleshy parts of the re- possible presence of MD. Fourcade et al. (2015) refer to unpub- maining drupes were removed by gently rubbing fruits on a sieve lished studies of germination and dormancy in this species, under running water prior to further studies. Drupes without fle- though no detailed work has previously been undertaken. shy parts (DWFP) were stored prior to use in plastic zip-lock The likely second-earliest diverging ANA-grade order, bags at room temperature (25 6 2 C). Nymphaeales, contains three aquatic families, Nymphaeceae, Cabombaceae and Hydatellaceae, of which the latter is indi- cated by molecular phylogeny to be basally diverging (Saarela Physical characteristics of mature DWFP and seeds et al.,2007). Physiological dormancy has been reported in the To assess A. trichopoda for the possible presence of dor- Nymphaeaceae genera Nymphaea (six species studied) and mancy, we first studied the physical characteristics of its mature Nuphar (one species studied) and in the Cabombaceae genus DWFP and seed sensu stricto. Immediately after harvesting Cabomba (one species studies), as summarized by Willis et al. four replicates of 100 DWFP and of 100 seeds sensu stricto ex- (2014). In contrast, seeds of Trithuria (three species studied), tracted from the DWFP were weighed. Also, three replicates of the only genus of Hydatellaceae, have MPD (Tuckett et al., 20 DWFP and 20 seeds sensu stricto were measured, and aver- 2010). Interestingly, MPD in Trithuria contains an extreme age dimensions were determined. The length and width of en- morphological component as embryos in mature Trithuria tire DWFP, as well as those that had been cut transversally or seeds show very limited differentiation and consist of only longitudinally, were measured using a dissecting microscope about 18–23 cells, depending on the species (Tuckett et al., equipped with a micrometer. DWFP were mounted on scanning 2010; Friedman et al., 2012). electron microscope specimen holders using double-sided car- The third-diverging ANA-grade order, Austrobaileyales, bon adhesive tape and carbon-metalized (10–15 nm), as de- contains three families of woody species, Austrobaileyaceae, scribed by Rabier et al. (2008). Observations and size Trimeniaceae and Schisandraceae. The Schisandraceae genera measurements were made using a Philips XL 30 environmental Schisandra (three species studied) and Illicium (five species scanning electron microscope. Moisture content of four repli- studied) both have MPD (summarized by Willis et al., 2014), cates of 25 DWFP was determined gravimetrically (103 6 2 C while dormancy in the remaining genera of Austrobaileyales for 17 6 1 h), by the protocol of MacKay et al. (2002),observ- has yet to be assessed. ing standard procedures
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