Symbiotic Nitrogen Fixation in Legumes: Perspectives on the Diversity and Evolution of Nodulation by Rhizobium and Burkholderia Species
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Chapter 89 Symbiotic Nitrogen Fixation in Legumes: Perspectives on the Diversity and Evolution of Nodulation by Rhizobium and Burkholderia Species Robert Walker School of Biomedical Sciences, Faculty of Health Sciences, Curtin University, Bentley, WA, Australia Christina M. Agapakis Department of Molecular, Cell and Developmental Biology, University of California, Los Angeles, CA, USA Elizabeth Watkin School of Biomedical Sciences, Faculty of Health Sciences, Curtin University, Bentley, WA, Australia Ann M. Hirsch Department of Molecular, Cell and Developmental Biology, University of California, Los Angeles, CA, USA; Molecular Biology Institute, University of California, Los Angeles, CA, USA 89.1 INTRODUCTION Burkholderia,andtheirrelevancetothiswell-studied, benefcial interaction between bacterium and plant. More than a decade ago, we wrote an update on the In particular, we examine the concept of host range, Rhizobium–legume symbiosis asking the question “what biogeography, as well as evolutionary history with respect makes this symbiosis so special?” (Hirsch et al., 2001). to nodulation by Burkholderia and Rhizobium (see also Since that time, we have learned a great deal more about this Chapter 17). Phylogenetic analyses strongly indicate that important plant–microbe association. However, the story of both genera acquired the nodulation genes at approximately symbiotic nitrogen fxation in legumes has become more the same time as the legumes were evolving (Bontemps complicated due to the discovery of several Betaproteobac- et al., 2010). We elaborate on this evolutionary theme as we teria, namely species of Burkholderia and Cupriavidus, delve into the even earlier history of these two nodulating which also establish nitrogen-fxing nodules on legumes. and nitrogen-fxing bacterial families, with the goal of estab- In this chapter, we expand our analysis of the Rhizobium– lishing an evolutionary description of this still incompletely legume symbiosis to include the betarhizobia, specifcally understood symbiosis. Biological Nitrogen Fixation, Volume 2, First Edition. Edited by Frans J. de Bruijn. © 2015 John Wiley & Sons, Inc. Published 2015 by John Wiley & Sons, Inc. 913 914 Chapter 89 Symbiotic Nitrogen Fixation in Legumes: Perspectives on the Diversity and Evolution 89.2 THE LEGUMES into most of their major lineages within a relatively short period of time (ca. 55–50 Mya) (Herendeen et al., 1992; The legumes (Fabaceae or Leguminosae) are the third Doyle and Luckow, 2003; Lewis et al., 2005; Sprent, 2007, largest family of fowering plants (>19,000 species); only 2008). This is approximately the same time that the rest Asteraceae and Orchidaceae are larger (Lewis et al., 2005). of the angiosperm families were evolving (Lewis et al., The family is monophyletic, but comprises three subfamilies 2005). The boreotropical forest migration hypothesis has (36 tribes), namely Caesalpinioideae, Mimosoideae, and replaced the older Gondwanan theory in which legumes Papillionoideae, which represent 22%, 10%, and 67%, moved northward from their presumed sites of origin in respectively, of the family (Sprent, 2001). Of the three Africa to South America and then, before the land masses subfamilies, caesalpinioid legumes are less likely to be drifted apart 165–145 Mya, to North America. Nonetheless, nodulated, but this is not because they evolved frst (Sprent, the boreotropical hypothesis leaves much unexplained, 2007). Several caesalpinioid legumes considered to be especially with regard to the evolution of legume nodulation “basal” are not found in the fossil fora in the early history (Sprent, 2008; see Chapter 3). of the family (Herendeen et al., 1992). Although nodules have not been found in the fossil The structure of the fowers of the subfamily members record, it is extremely likely that many of the legumes were differs signifcantly (Fig. 89.1), but legumes are incredibly already developing root nodules inhabited by nitrogen-fxing diverse in many other features, including phytochemical rhizobia by the time that the major lineages were established. profles, nodulation status, and habitats. Legumes occupy The partnership between rhizobia and legumes is based on deserts and grass-poor, succulent-rich, dry environments apre-existingandancientrelationship,datingfromthe (S-biomes); tropical rain forests (R-biomes); grass-rich early Devonian (416–350 Mya) between arbuscular myc- prairies and savannahs (G-biomes); temperate ecosystems orrhizal fungi (AMF) and plants. The evolutionary origin (T-biomes); and agricultural systems derived from anthro- of the genes important for root nodulation that was derived pogenic input. Numerous books and papers have described from the arbuscular-mycorrhizal (AM) symbiosis has been the biology, nodulation, and evolution of the legumes, so we extensively studied and reviewed (Hirsch et al., 2001; Szcz- describe only a few salient features in this chapter (Sprent, glowsky and Amyot, 2003; Streng et al., 2011; and others; 2001; Doyle and Luckow, 2003; Lewis et al., 2005). see also Chapters 42, 54, 55, 108, 110). The legumes are believed to have evolved ca. 65–50 million years ago (Mya) in the late Cretaceous/early Tertiary after the K/T extinction (Lavin et al., 2005). This 89.3 THE RHIZOBIA hypothesis is in part based on the discovery of legume fossils dating from the Paleocene (ca. 66–56 Mya; Herendeen et al., “Rhizobia” is the collective term given to bacteria capa- 1992) and also on molecular analysis developed from matK ble of inducing the development of and then populating and rbcL phylogenies (Lavin et al., 2005). The evolutionary nitrogen-fxing nodules (Sprent, 2001). A long-standing migration of legumes southward is postulated to have started debate exists over whether legumes and rhizobia coevolved north of the Tethys Sea, under warmer climate conditions, or whether the plants selected for symbiotic bacteria, but after the continents drifted apart (see Doyle and Luckow, the presence of horizontal gene transfer and the lack of par- 2003; Sprent, 2007). This boreotropical origin, deduced allel speciation between legumes and rhizobia might argue in part from the current habitats of legumes, is consistent against a coevolutionary trajectory (Martínez-Romero, with the migration of legumes from an S-biome to the R-, 2009; Young and Johnston, 1989). G-, and T-biomes (Lewis et al., 2005). Both molecular Up to 2001, only the Alphaproteobacteria in the family and fossil data suggest that legumes rapidly diversifed Rhizobiaceae had been classifed as rhizobia. These bacteria (a) (b) (c) Figure 89.1 Examples of fowers from the three legume subfamilies. (a) Caesalpinoideae: Chamaecrista fasciculata (N.A. Fujishige). (b) Mimosoideae: Caliandra hematocephala (A.M. Hirsch). (c) Papillionoideae: Swainsona formosa (W. Deng). 89.5 The Root-Nodulating Burkholderia Species 915 were frst isolated from root nodules by Beijerinck (1890), 89.4 THE BETARHIZOBIA and the name Rhizobium was suggested shortly afterwards by Frank (1889) (see additional references in Gyaneshwar In 2001, two genera of the family Burkholderiaceae, et al., 2011; see Chapter 88). Until the 1980s, all the legume Burkholderia and Cupriavidus,werereportedtonodu- root-nodulating bacteria (RNB) were classifed in the genus late legumes, but at that time were not shown to induce Rhizobium,whichhadbeendividedintofastandslow effective, that is, nitrogen-fxing nodules on their hosts growers. After it became apparent that signifcantly greater (Moulin et al., 2001; see Chapter 17). Much of the original differences than just growth rate existed, Bradyrhizobium work on the Burkholderia symbiotic species focused on (Bradyrhizobiaceae)wasproposedbyJordan(1982)to B. tuberum and B. phymatum,butitwasquicklyshownthat encompass the slow-growing species whereas the name Rhi- neither species re-infected the hosts from which they were zobium was retained for the fast growers. Using a molecular originally isolated (Aspalathus carnosa and Machaerium clock approach, the split between Rhizobium and Bradyrhi- lunatum,respectively).Laterstudiesshowedthatbothgen- zobium is estimated to have taken place 800–300 Mya era established nitrogen-fxing nodules with a number of depending on the gene analyzed (Turner and Young, 2000). legume hosts. The majority of Burkholderia species have Rhizobium has also been subdivided into a number been isolated from nodules of Mimosoideae, especially the of distinct genera. Chen et al. (1988) isolated fast- and genus Mimosa. Mimosa spp. are native to the Neotropics slow-growing rhizobia from nodules of soybean (Glycine although a few endemics live in the Paleotropics, mainly in soja)andfromsoil,andafteranalyzingcellularcomposition Madagascar, and also extend into southeast tropical Africa and by using methods such as DNA–DNA hybridization, and India (Lewis et al., 2005; see Chapter 17). serology, and phage typing, proposed a new genus, Sinorhi- Some Burkholderia species are free-living and function zobium. Thus, the fast-growing isolate Rhizobium fredii as soil-dwelling microbes in bioremediation or act as plant was renamed Sinorhizobium fredii.In2008,however,tax- growth-promoting bacteria (PGPB) living as epiphytes on plants (de Bruijn, 2013). Still others appear to be endophytes onomists questioned whether Sinorhizobium was distinct based on their isolation from both legume and nonlegume from the genus Ensifer,andtheJudicialCommissionof hosts following surface sterilization of plant tissues the International Committee on Systematics of Prokaryotes