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Phylogeny and Phylogeography of Rhizobial Symbionts Nodulating Legumes of the Tribe Genisteae

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Phylogeny and Phylogeography of Rhizobial Symbionts Nodulating Legumes of the Tribe Genisteae View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Lincoln University Research Archive G C A T T A C G G C A T genes Review Phylogeny and Phylogeography of Rhizobial Symbionts Nodulating Legumes of the Tribe Genisteae Tomasz St˛epkowski 1,*, Joanna Banasiewicz 1, Camille E. Granada 2, Mitchell Andrews 3 and Luciane M. P. Passaglia 4 1 Autonomous Department of Microbial Biology, Faculty of Agriculture and Biology, Warsaw University of Life Sciences (SGGW), Nowoursynowska 159, 02-776 Warsaw, Poland; [email protected] 2 Universidade do Vale do Taquari—UNIVATES, Rua Avelino Tallini, 171, 95900-000 Lajeado, RS, Brazil; [email protected] 3 Faculty of Agriculture and Life Sciences, Lincoln University, P.O. Box 84, Lincoln 7647, New Zealand; [email protected] 4 Departamento de Genética, Instituto de Biociências, Universidade Federal do Rio Grande do Sul. Av. Bento Gonçalves, 9500, Caixa Postal 15.053, 91501-970 Porto Alegre, RS, Brazil; [email protected] * Correspondence: [email protected]; Tel.: +48-509-453-708 Received: 31 January 2018; Accepted: 5 March 2018; Published: 14 March 2018 Abstract: The legume tribe Genisteae comprises 618, predominantly temperate species, showing an amphi-Atlantic distribution that was caused by several long-distance dispersal events. Seven out of the 16 authenticated rhizobial genera can nodulate particular Genisteae species. Bradyrhizobium predominates among rhizobia nodulating Genisteae legumes. Bradyrhizobium strains that infect Genisteae species belong to both the Bradyrhizobium japonicum and Bradyrhizobium elkanii superclades. In symbiotic gene phylogenies, Genisteae bradyrhizobia are scattered among several distinct clades, comprising strains that originate from phylogenetically distant legumes. This indicates that the capacity for nodulation of Genisteae spp. has evolved independently in various symbiotic gene clades, and that it has not been a long-multi-step process. The exception is Bradyrhizobium Clade II, which unlike other clades comprises strains that are specialized in nodulation of Genisteae, but also Loteae spp. Presumably, Clade II represents an example of long-lasting co-evolution of bradyrhizobial symbionts with their legume hosts. Keywords: Bradyrhizobium; Genisteae; Microvirga; nifD; nodA; phylogeography 1. Introduction: Origin and Differentiation of the Tribe Genisteae The Genisteae is one of the largest tribes within the legume family (Fabaceae) with ca. 618 species within 25 genera [1]. Most genera within the Genisteae show a preference for a temperate climate although several lupin (Lupinus spp.) species inhabit tropical areas in eastern Brazil [2–4]. These predominantly woody legumes thrive in a wide range of habitats, including coastal dunes, scrubland, sagebrush steppes, grasslands, mountain woodlands, and meadows. Genisteae (especially lupins) inhabit areas across a wide altitudinal range, extending from sea level to the upper elevation limit for plant growth, i.e., ca. 5000 m [5]. Almost all of the Genisteae species tested can fix atmospheric nitrogen via symbiotic bacteria (general term ‘rhizobia’) in root nodules, and this gives them an advantage in low N soils if other factors are favourable for growth [6–8]. It has been estimated that the separation of the Genisteae and Crotalarieae took place in the Eocene ca. 41 million of years ago [9]. Evidence indicates that the formation of the two basal lineages, which later evolved into the extant genera Dichilus-Melolobium-Polhillia and Argyrolobium, occurred in southern Africa. Later, this tribe dispersed northward reaching the Mediterranean, Genes 2018, 9, 163; doi:10.3390/genes9030163 www.mdpi.com/journal/genes Genes 2018, 9, 163 2 of 25 where two other genera, Lupinus and Adenocarpus appeared. These events were followed by the emergenceGenes of2018 the, 9, x Cytisinae (nine genera) and Genistinae (eight genera) as predominant2 of Genisteae 25 groups in the Mediterranean [1,2,10]. Given that the time of separation of the genus Lupinus and the in southern Africa. Later, this tribe dispersed northward reaching the Mediterranean, where two Cytisinae-Genistinae genera has been estimated at ca. 16 million years ago, the process of differentiation other genera, Lupinus and Adenocarpus appeared. These events were followed by the emergence of into thethe extant Cytisinae Genisteae (nine genera) genera and may Genistinae have been (eight initiated genera) as in predominant the Oligocene, Genisteae albeit groups not laterin the than in the earlyMediterranean Miocene [11 [1,2,10].,12]. TheGiven environmental that the time of changes separation that of the are genus associated Lupinus with and the the Cytisinae- global climate coolingGenistinae and growing genera aridification has been estimated from at the ca. 16 end million of the years Eocene ago, the may process have of playeddifferentiation pivotal into roles the in the Genisteaeextant speciation Genisteae process genera [may13,14 have]. Similarly, been initiated the mountainin the Oligocene, uplifts albeit in the not western later than parts in the of early North and South AmericaMiocene [11,12]. triggered The replicateenvironmental radiations changes in that the ar genuse associatedLupinus with, the resulting global climate in the cooling appearance and of ca. growing aridification from the end of the Eocene may have played pivotal roles in the Genisteae 200 species with a great variety of morphological forms [12,15]. speciation process [13,14]. Similarly, the mountain uplifts in the western parts of North and South TheAmerica amphi-Atlantic triggered replicate distribution radiations of Genisteae in the genus species Lupinus points, resulting to dispersal in the appearance events having of ca. 200 occurred across thespecies Atlantic with aOcean great variety into theof morphological areas nowcomprising forms [12,15]. a distinct Fabaceae flora. The thesis of this review is thatThe the amphi-Atlantic complex evolutionary distribution of history Genisteae of spec theies Genisteae points to dispersal tribe is reflectedevents having by theoccurred diversity of rhizobiumacross symbionts, the Atlantic with Ocean which into the it areas interacts. now comprisi Indeed,ng sevena distinct out Fabaceae of the flora. 16 authenticated The thesis of this rhizobial review is that the complex evolutionary history of the Genisteae tribe is reflected by the diversity of genera can nodulate particular Genisteae species (Figure1). Thus, the objective of this work is to rhizobium symbionts, with which it interacts. Thus, the objective of this work is to present present a comprehensive phylogenetic phylogenetic and andphylogeographic phylogeographic data concerning data concerning the rhizobia the that rhizobia nodulate that this nodulate this legumelegume tribe. tribe. Figure 1. A Bayesian posterior probability consensus tree based on 1408 bps of 16S rRNA derived Figure 1.fromA 16 Bayesian rhizobialposterior and 4 related probability genera (the consensusgenera nodulating tree based Genisteae on are 1408 in bold bps case-underlined). of 16S rRNA derived from 16The rhizobial strains used and for 4 related this construction genera (the and generathe 16S rRNA nodulating Genbank Genisteae accession numbers are in bold were: case-underlined). Rhizobium The strainsleguminosarum used for thisATCC construction 10004 (U29386), and theSinorhizobium 16S rRNA fredii Genbank ATCC accession 35423 (X67231), numbers Allorhizobium were: Rhizobium leguminosarumundicola ATCC 700741 10004 (Y17047), (U29386), PararhizobiumSinorhizobium capsulatum fredii ATCC 43294 35423 (X73042), (X67231), NeorhizobiumAllorhizobium galegae undicola ATCC 43677 (D11343), Shinella zoogloeoides ATCC 19623 (AB238789), Ciceribacter lividus MSSRFBL1 ATCC 700741 (Y17047), Pararhizobium capsulatum ATCC 43294 (X73042), Neorhizobium galegae ATCC (NR 135717), Mesorhizobium loti ATCC 700743 (X67229), Aminobacter anthyllidis STM 4645(FR869633), Shinella zoogloeoides Ciceribacter lividus 43677 (D11343),Phyllobacterium brassicacearum LMGATCC 22836 19623 (AY785319), (AB238789), Ochrobactrum lupini LMG MSSRFBL122726 (AY457038), (NR 135717), MesorhizobiumMethylobacterium loti ATCC marchantiae 700743 (X67229), DSM 21328Aminobacter (FJ157976), Bradyrhizobium anthyllidis STM lupini 4645(FR869633), USDA 3051 (KM114861),Phyllobacterium brassicacearumBosea lupiniLMG LMG 22836 26383 (AY785319), (FR774992),Ochrobactrum Azorhizobium lupinioxalatiphilumLMG 22726DSM 18749 (AY457038), (FR799325),Methylobacterium Labrys marchantiaeokinawensisDSM 21328DSM 18385 (FJ157976), (AB236169),Bradyrhizobium Devosia honganensis lupini ACCCUSDA 19737 3051 (KP339871), (KM114861), ParaburkholderiaBosea lupini LMG 26383 (FR774992),caribensis CCUGAzorhizobium 42847 (Y17009), oxalatiphilum Cupriavidus alkaliphilusDSM 18749 LMG (FR799325), 26294 (HQ438078),Labrys and okinawensis Microvirga lupiniDSM 18385 LMG 26460 (EF191408). The 16S rRNA sequences were aligned in MUSCLE [16] and implemented in (AB236169), Devosia honganensis ACCC 19737 (KP339871), Paraburkholderia caribensis CCUG 42847 MEGA 6.0 [17]. The Bayesian analyses were performed using BEAST 1.7 software [18]. The model of (Y17009), Cupriavidus alkaliphilus LMG 26294 (HQ438078), and Microvirga lupini LMG 26460 (EF191408). nucleotide evolution used in all of the analyses was GTR + I + G, as selected by the jModel Test software The 16S[19]. rRNA The Yule sequences process was were selected aligned as a tree in MUSCLEprior to Bayesian [16] andanalysis,
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