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Poaceae) Laurent Hardion, Regine Verlaque, Gisele Haan-Archipoff, Daniel Cahen, Michel Hoff, Bruno Vila

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Poaceae) Laurent Hardion, Regine Verlaque, Gisele Haan-Archipoff, Daniel Cahen, Michel Hoff, Bruno Vila Cleaning up the grasses dustbin: systematics of the Arundinoideae subfamily (Poaceae) Laurent Hardion, Regine Verlaque, Gisele Haan-Archipoff, Daniel Cahen, Michel Hoff, Bruno Vila To cite this version: Laurent Hardion, Regine Verlaque, Gisele Haan-Archipoff, Daniel Cahen, Michel Hoff, et al.. Cleaning up the grasses dustbin: systematics of the Arundinoideae subfamily (Poaceae). Plant Systematics and Evolution, Springer Verlag (Germany), 2017, 303 (10), pp.1331-1339. 10.1007/s00606-017-1451-6. hal-01681605 HAL Id: hal-01681605 https://hal.archives-ouvertes.fr/hal-01681605 Submitted on 7 May 2018 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. Cleaning up the grasses dustbin: systematics of the Arundinoideae subfamily (Poaceae) Laurent Hardion 1, Régine Verlaque 2, Gisèle Haan-Archipoff 3, Daniel Cahen 4,·Michel Hoff 3,·Bruno Vila 2 1Laboratoire Image Ville Environnement (LIVE), University of Strasbourg, CNRS, Institut de Botanique, 28 rue Goethe, 67000 Strasbourg, France 2Institut Méditerranéen de Biodiversité et d’Écologie (IMBE), UMR CNRS, IRD, Aix-Marseille University, Avignon University, Marseille, France 3Herbarium of the University of Strasbourg (STR), Faculty of Life Sciences, Strasbourg, France 4Herbarium, Royal Botanic Gardens, Kew, Richmond, UK Corresponding author: Laurent Hardion, [email protected] Abstract Among the 12 subfamilies currently considered in the systematics of Poaceae, the Arundinoideae have long been considered as a dustbin group, with a diversity of forms putatively hiding incertae sedis . Because this subfamily has been poorly investigated using molecular markers for the last two decades, the present study provides the first complete phylogeny of the Arundinoideae based on five plastid DNA loci sequenced for 12 genera, and analysed with and without plastome data from previous studies. The refined Arundinoideae appear to be a robust evolutionary lineage of Poaceae, divided into three tribes with some biogeographical patterns: (1) tribe Arundineae, the most heterogeneous tribe, including Eurasian Arundo , Australian Amphipogon and Monachather , and South African Dregeochloa ; (2) tribe Crinipedeae (described here), including Crinipes , Elytrophorus , Styppeiochloa and Pratochloa (described here), with a South and East African distribution; and (3) tribe Molinieae, including Hakonechloa , Molinia and Phragmites , with a Eurasian distribution. Despite reduction in size, this small subfamily conserves a high diversity of morphological forms, with several small but highly differentiated genera. Finally, the molecular dating approach provides an evolutionary framework to understand the diversification of Arundinoideae, refuting Gondwanan vicariance between genera and suggesting capability for long distance dispersal. Keywords Arundo , Crinipedeae, Phragmites, Phylogeny, Pratochloa, Taxonomy 1 Introduction Poaceae Barnhart is one of the most fascinating plant families by its usefulness for humans and its ecological and taxonomic diversification. Although several angiosperm families possess higher species richness, grasses exceed all others by their ecological significance (Kellogg 2000 ). Thanks to numerous adaptive strategies such as C- 4 metabolism (GPWG II 2012 ), Poaceae occur in almost all terrestrial ecosystems and dominate grassland biomes covering a quarter of land surfaces (Shantz 1954 ). In addition, about half of the annual production of global agriculture is due to the domestication of four of the c. 12,000 grass species (http://faostat.fao. org/ ). In this context, the understanding of grass evolutionary history represents a major scientific challenge. Since the groundwork studies by Brown ( 1810 , 1814 ), Poaceae have been periodically revised in several subfamilies and tribes (a synthesis in Prat 1960 ; Clayton and Renvoize 1986 ). For the last two decades, molecular studies have accelerated this systematics resolution (Clark et al. 1995 ; Duvall and Morton 1996 ; Hilu et al. 1999 ; Hsiao et al. 1999 ; GPWG 2001 ), with the current consideration of 12 subfamilies, 51 tribes and 771 genera (Soreng et al. 2015 ), structured in two main lineages, the BOP and PACMAD clades (Fig. 1). Arundinoideae Kunth ex Beilschm. were dissociated from these two historical lineages early on, due to apically reduced florets and laterally compressed spikelets—specific to the ‘festucoid’ type—versus subtropical distribution and epidermal features—specific to the ‘panicoid’ type (Avdulov 1931 ; Jacques-Félix 1958 ; Stebbins and Crampton 1959 ; Prat 1960 ; Fig. 1a). Arundinoideae included incertae sedis taxa, which sometimes led to consider it to be a basal clade of Poaceae, or even a taxonomic ‘dustbin group’ (Prat 1960 ; Auquier 1963 ; Clayton and Renvoize 1986 ). Consequently, Arundinoideae have included up to 736 species and 72 genera (Conert 1961 , 1966 ; Renvoize 1981 ; Soreng et al. 2015 ), but its molecular polyphyly (Barker et al. 1995 , 1998 ; Hsiao et al. 1998 ) led to its drastic reduction by the description of Danthonioideae H.P.Linder & N.P.Barker (GPWG 2001 ) and the reinstatement of Micrairoideae Pilg. (Sánchez-Ken et al. 2007 ). Following these treatments, Arundinoideae have become one of the smallest grass subfamilies, with 15 genera and about 42 species (Table 1). But these taxa show a surprising ecological and morphological heterogeneity, from helophyte reeds such as Phragmites australis (Cav.) Trin. ex Steud., one of the most cosmopolitan plant species, to dwarf xerophytes such as Dregeochloa pumila (Nees) Conert, the only succulent grass living in Southern African sandy deserts. Repeated morphological analyses of Arundinoideae provided some interesting insights but failed to clearly resolve their classification. This is partly due to the diversity of forms and few evident synapomorphies in such a small subfamily (Renvoize 1981 ; Linder et al. 1997 ). In addition, several taxa currently in the Arundinoideae may be erroneously included. In return, some apparent Arundinoideae may be misplaced in other subfamilies, such as ‘ Eragrostis walteri Pilg.’ previously considered as the only non-C4 Chloridoideae, but recently placed in the Arundinoideae based on molecular 2 data (Ingram et al. 2011 ). Finally, several species and genera ( Dichaetaria Nees ex Steud., Leptagrostis C.E.Hubb., Nematopoa C.E.Hubb. Piptophyllum C.E.Hubb., Zenkeria Trin.) of Arundinoideae have never been studied in a molecular phylogeny, due to their rarity and restricted distributions, some of them being represented only by a few herbarium specimens (Linder et al. 1997 ). Fig. 1 Places of the Arundinoideae subfamily (in red ) in the historical representation of grass systematics, from an old literature synthesis of morphological and anatomical studies (modified from Prat 1936 ; a) to a recent molecular phylogeny (modified from GPWG II 2012 ; b). Clade sizes are proportional to their species richness (also indicated between brackets ). BOP clade, Bambusoideae–Oryzoideae– Pooideae (in grey ); PACMAD clade, Panicoideae– Aristidoideae– Chloridoideae–Micrairoideae–Arundinoideae–Danthonioideae (in white ) Table 1 Genera, species richness (S) and geographical distribution of the subfamily Arundinoideae Genus S Distribution Amphipogon R.Br. (= Diplopogon R.Br.) 9 Australia Arundo L. 5 Tropical Eurasia Crinipes Hochst. 2 East Africa Dichaetaria Nees ex Steud. 1 India Dregeochloa Conert 2 South Africa Elytrophorus P.Beauv. 2 Africa–Asia–Australia Hakonechloa Makino ex Honda 1 Japan Leptagrostis C.E.Hubb. 1 East Africa Molinia Schrank (= Moliniopsis Hayata) 3 Eurasia Monachather Steud. 1 Australia Nematopoa C.E.Hubb. 1 South Africa Phragmites Adans. 5 Cosmopolitan Piptophyllum C.E.Hubb. 1 South Africa Styppeiochloa De Winter 3 South Africa *Zenkeria Trin. 5 India Total 42 Old World + Australia * Genus removed from the subfamily based on the present study 3 The present study attempts to provide the first complete phylogeny of the Arundinoideae subfamily. The main challenges are (1) to test the monophyly of taxa currently included in Arundinoideae, (2) to resolve the phylogenetic relationships within this subfamily in order to identify putative tribes and (3) to initiate the understanding of the evolutionary history of this small but heterogeneous sub-family. To address this, we used five plastid DNA loci previously investigated to resolve the systematics of Poaceae. We also added previously published plastomes (complete plastid genomes) of several species, in order to increase the resolution of phylogenetic reconstructions and improve the calibration of molecular dating. Finally, we provide a taxonomic treatment to improve the classification of Arundinoideae. Materials and methods DNA extraction and plastid DNA sequencing Sampling includes samples from BM, CANB, ETH, K, MARS, P, PRE and STR Herbaria (Online Resource 1). For each sample, about 1 cm 2 of leaf material was crushed by two metallic marbles in 2-mL tubes treated with liquid nitrogen and placed in a ball mill. Total DNA was extracted following Doyle and Doyle ( 1987 ) with a modification
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