Biogeography of nodulated legumes and their nitrogen-fixing symbionts
TL;DR: This review highlights both longitudinal and latitudinal trends and considers these in relation to the location of major land masses over geological time and Australia is identified as being a special case and latitudes north of the equator as being pivotal in the evolution of highly specialized systems in which the differentiated rhizobia effectively become ammonia factories.
Abstract: Contents 40 I. 40 II. 41 III. 44 IV. 48 V. 49 VI. 49 VII. 52 VIII. 53 53 References 53 SUMMARY: In the last decade, analyses of both molecular and morphological characters, including nodulation, have led to major changes in our understanding of legume taxonomy. In parallel there has been an explosion in the number of genera and species of rhizobia known to nodulate legumes. No attempt has been made to link these two sets of data or to consider them in a biogeographical context. This review aims to do this by relating the data to the evolution of the two partners: it highlights both longitudinal and latitudinal trends and considers these in relation to the location of major land masses over geological time. Australia is identified as being a special case and latitudes north of the equator as being pivotal in the evolution of highly specialized systems in which the differentiated rhizobia effectively become ammonia factories. However, there are still many gaps to be filled before legume nodulation is sufficiently understood to be managed for the benefit of a world in which climate change is rife.
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TL;DR: Rhizobia are some of the best-studied plant microbiota, which must exist in soil and compete with other members of the microbiota before infecting legumes and forming N2-fixing bacteroids.
Abstract: Rhizobia are some of the best-studied plant microbiota These oligotrophic Alphaproteobacteria or Betaproteobacteria form symbioses with their legume hosts Rhizobia must exist in soil and compete with other members of the microbiota before infecting legumes and forming N2-fixing bacteroids These dramatic lifestyle and developmental changes are underpinned by large genomes and even more complex pan-genomes, which encompass the whole population and are subject to rapid genetic exchange The ability to respond to plant signals and chemoattractants and to colonize nutrient-rich roots are crucial for the competitive success of these bacteria The availability of a large body of genomic, physiological, biochemical and ecological studies makes rhizobia unique models for investigating community interactions and plant colonization
329 citations
Ludwig Maximilian University of Munich1, Weber State University2, University of Toulouse3, National University of Quilmes4, Wageningen University and Research Centre5, University of Lyon6, University of California, Davis7, Stockholm University8, University of Montpellier9, Cornell University10, Beijing Genomics Institute11, University of Wisconsin-Madison12, Technische Universität München13, University of Alberta14
TL;DR: Molecular evidence is used to ask how the current pattern of plant species with NFN symbiosis evolved and to suggest that this symbiosis is subject to an underestimated adverse selection pressure.
Abstract: The root nodule symbiosis of plants with nitrogen-fixing bacteria impacts global nitrogen cycles and food production but is restricted to a subset of genera within a single clade of flowering plants. To explore the genetic basis for this scattered occurrence, we sequenced the genomes of ten plant species covering the diversity of nodule morphotypes, bacterial symbionts and infection strategies. In a genome-wide comparative analysis of a total of 37 plant species, we discovered signatures of multiple independent loss-of-function events in the indispensable symbiotic regulator NODULE INCEPTION (NIN) in ten out of 13 genomes of non-nodulating species within this clade. The discovery that multiple independent losses shaped the present day distribution of nitrogen-fixing root nodule symbiosis in plants reveals a phylogenetically wider distribution in evolutionary history and a so far underestimated selection pressure against this symbiosis.
267 citations
Cites background from "Biogeography of nodulated legumes a..."
...An alternative model proposes two independent gains within the legumes: the first at the most recent common ancestor of the papilionoids and the clade to which Castanospermum australe belongs (21-291 enriched-expanded clusters), or at the base of the papilionoids (4-32), and the second gain at the base of the caesalpinioid andmimosoid clade (7-92)....
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...In addition to this scattered distribution, a further unsolved mystery that surrounds the evolution of NFN symbiosis is its diversity at multiple levels: Legumes (Fabales) and the nonlegume Parasponia (Rosales) (8) form nodules with rhizobia, whereas species of the actinobacterial genus Frankia infect actinorhizal plants from eight plant families of the orders Fagales, Cucurbitales, and Rosales (9)....
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TL;DR: Strain-specific legume rhizobia symbioses can develop in particular habitats and are likely to be at least in part related to the relative occurrence of the potential symbionts in soils of the different regions.
Abstract: Most species in the Leguminosae (legume family) can fix atmospheric nitrogen (N₂) via symbiotic bacteria (rhizobia) in root nodules. Here, the literature on legume-rhizobia symbioses in field soils was reviewed and genotypically characterised rhizobia related to the taxonomy of the legumes from which they were isolated. The Leguminosae was divided into three sub-families, the Caesalpinioideae, Mimosoideae and Papilionoideae. Bradyrhizobium spp. were the exclusive rhizobial symbionts of species in the Caesalpinioideae, but data are limited. Generally, a range of rhizobia genera nodulated legume species across the two Mimosoideae tribes Ingeae and Mimoseae, but Mimosa spp. show specificity towards Burkholderia in central and southern Brazil, Rhizobium/Ensifer in central Mexico and Cupriavidus in southern Uruguay. These specific symbioses are likely to be at least in part related to the relative occurrence of the potential symbionts in soils of the different regions. Generally, Papilionoideae species were promiscuous in relation to rhizobial symbionts, but specificity for rhizobial genus appears to hold at the tribe level for the Fabeae (Rhizobium), the genus level for Cytisus (Bradyrhizobium), Lupinus (Bradyrhizobium) and the New Zealand native Sophora spp. (Mesorhizobium) and species level for Cicer arietinum (Mesorhizobium), Listia bainesii (Methylobacterium) and Listia angolensis (Microvirga). Specificity for rhizobial species/symbiovar appears to hold for Galega officinalis (Neorhizobium galegeae sv. officinalis), Galega orientalis (Neorhizobium galegeae sv. orientalis), Hedysarum coronarium (Rhizobium sullae), Medicago laciniata (Ensifer meliloti sv. medicaginis), Medicago rigiduloides (Ensifer meliloti sv. rigiduloides) and Trifolium ambiguum (Rhizobium leguminosarum sv. trifolii). Lateral gene transfer of specific symbiosis genes within rhizobial genera is an important mechanism allowing legumes to form symbioses with rhizobia adapted to particular soils. Strain-specific legume rhizobia symbioses can develop in particular habitats.
223 citations
TL;DR: This review addresses recent findings in nodulation control, presents detailed models of the molecular mechanisms driving these processes, and identifies gaps in these processes that are not yet fully explained.
Abstract: Global demand to increase food production and simultaneously reduce synthetic nitrogen fertilizer inputs in agriculture are underpinning the need to intensify the use of legume crops. The symbiotic relationship that legume plants establish with nitrogen-fixing rhizobia bacteria is central to their advantage. This plant-microbe interaction results in newly developed root organs, called nodules, where the rhizobia convert atmospheric nitrogen gas into forms of nitrogen the plant can use. However, the process of developing and maintaining nodules is resource intensive; hence, the plant tightly controls the number of nodules forming. A variety of molecular mechanisms are used to regulate nodule numbers under both favourable and stressful growing conditions, enabling the plant to conserve resources and optimize development in response to a range of circumstances. Using genetic and genomic approaches, many components acting in the regulation of nodulation have now been identified. Discovering and functionally characterizing these components can provide genetic targets and polymorphic markers that aid in the selection of superior legume cultivars and rhizobia strains that benefit agricultural sustainability and food security. This review addresses recent findings in nodulation control, presents detailed models of the molecular mechanisms driving these processes, and identifies gaps in these processes that are not yet fully explained.
199 citations
TL;DR: The study of hopanoids offers rich opportunities for discovery regarding how hopanoid production is regulated, howHopanoids act biophysically and biochemically, and how their production affects bacterial interactions with other organisms, such as plants.
Abstract: Lipid research represents a frontier for microbiology, as showcased by hopanoid lipids. Hopanoids, which resemble sterols and are found in the membranes of diverse bacteria, have left an extensive molecular fossil record. They were first discovered by petroleum geologists. Today, hopanoid-producing bacteria remain abundant in various ecosystems, such as the rhizosphere. Recently, great progress has been made in our understanding of hopanoid biosynthesis, facilitated in part by technical advances in lipid identification and quantification. A variety of genetically tractable, hopanoid-producing bacteria have been cultured, and tools to manipulate hopanoid biosynthesis and detect hopanoids are improving. However, we still have much to learn regarding how hopanoid production is regulated, how hopanoids act biophysically and biochemically, and how their production affects bacterial interactions with other organisms, such as plants. The study of hopanoids thus offers rich opportunities for discovery.
127 citations
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TL;DR: An advanced version of the Molecular Evolutionary Genetics Analysis software, which currently contains facilities for building sequence alignments, inferring phylogenetic histories, and conducting molecular evolutionary analysis, is released, which enables the inference of timetrees, as it implements the RelTime method for estimating divergence times for all branching points in a phylogeny.
Abstract: We announce the release of an advanced version of the Molecular Evolutionary Genetics Analysis (MEGA) software, which currently contains facilities for building sequence alignments, inferring phylogenetic histories, and conducting molecular evolutionary analysis. In version 6.0, MEGA now enables the inference of timetrees, as it implements the RelTime method for estimating divergence times for all branching points in a phylogeny. A new Timetree Wizard in MEGA6 facilitates this timetree inference by providing a graphical user interface (GUI) to specify the phylogeny and calibration constraints step-by-step. This version also contains enhanced algorithms to search for the optimal trees under evolutionary criteria and implements a more advanced memory management that can double the size of sequence data sets to which MEGA can be applied. Both GUI and command-line versions of MEGA6 can be downloaded from www.megasoftware.net free of charge.
37,956 citations
01 Jan 2013
TL;DR: The Molecular Evolutionary Genetics Analysis (MEGA) software as discussed by the authors provides facilities for building sequence alignments, inferring phylogenetic histories, and conducting molecular evolutionary analysis, including the inference of timetrees.
Abstract: We announce the release of an advanced version of the Molecular Evolutionary Genetics Analysis (MEGA) software, which currently contains facilities for building sequence alignments, inferring phylogenetic histories, and conducting molecular evolutionary analysis. In version 6.0, MEGA now enables the inference of timetrees, as it implements the RelTime method for estimating divergence times for all branching points in a phylogeny. A new Timetree Wizard in MEGA6 facilitates this timetree inference by providing a graphical user interface (GUI) to specify the phylogeny and calibration constraints step-by-step. This version also contains enhanced algorithms to search for the optimal trees under evolutionary criteria and implements a more advanced memory management that can double the size of sequence data sets to which MEGA can be applied. Both GUI and command-line versions of MEGA6 can be downloaded from www. megasoftware.net free of charge.
30,478 citations
TL;DR: During evolution, the genetic programme for AM has been recruited for other plant root symbioses: functional adaptation of a plant receptor kinase that is essential for AM symbiosis paved the way for nitrogen-fixing bacteria to form intracellular symbiosis with plant cells.
Abstract: Arbuscular mycorrhiza (AM), a symbiosis between plants and members of an ancient phylum of fungi, the Glomeromycota, improves the supply of water and nutrients, such as phosphate and nitrogen, to the host plant. In return, up to 20% of plant-fixed carbon is transferred to the fungus. Nutrient transport occurs through symbiotic structures inside plant root cells known as arbuscules. AM development is accompanied by an exchange of signalling molecules between the symbionts. A novel class of plant hormones known as strigolactones are exuded by the plant roots. On the one hand, strigolactones stimulate fungal metabolism and branching. On the other hand, they also trigger seed germination of parasitic plants. Fungi release signalling molecules, in the form of 'Myc factors' that trigger symbiotic root responses. Plant genes required for AM development have been characterized. During evolution, the genetic programme for AM has been recruited for other plant root symbioses: functional adaptation of a plant receptor kinase that is essential for AM symbiosis paved the way for nitrogen-fixing bacteria to form intracellular symbioses with plant cells.
1,688 citations
University of Minnesota1, Institut national de la recherche agronomique2, Centre national de la recherche scientifique3, John Innes Centre4, Laboratory of Molecular Biology5, Agricultural Research Service6, Iowa State University7, West Virginia University8, University of Bonn9, Ghent University10, University of California, Davis11, Delaware Biotechnology Institute12, J. Craig Venter Institute13, University of Wisconsin-Madison14, National Center for Genome Resources15, King Saud University16, University of Oklahoma17, Cornell University18, Max Planck Society19, Wellcome Trust20, International Institute of Minnesota21, Rural Development Administration22, Carleton College23, Norwich Research Park24
TL;DR: The draft sequence of the M. truncatula genome sequence is described, a close relative of alfalfa (Medicago sativa), a widely cultivated crop with limited genomics tools and complex autotetraploid genetics, which provides significant opportunities to expand al falfa’s genomic toolbox.
Abstract: Legumes (Fabaceae or Leguminosae) are unique among cultivated plants for their ability to carry out endosymbiotic nitrogen fixation with rhizobial bacteria, a process that takes place in a specialized structure known as the nodule. Legumes belong to one of the two main groups of eurosids, the Fabidae, which includes most species capable of endosymbiotic nitrogen fixation. Legumes comprise several evolutionary lineages derived from a common ancestor 60 million years ago (Myr ago). Papilionoids are the largest clade, dating nearly to the origin of legumes and containing most cultivated species. Medicago truncatula is a long-established model for the study of legume biology. Here we describe the draft sequence of the M. truncatula euchromatin based on a recently completed BAC assembly supplemented with Illumina shotgun sequence, together capturing ∼94% of all M. truncatula genes. A whole-genome duplication (WGD) approximately 58 Myr ago had a major role in shaping the M. truncatula genome and thereby contributed to the evolution of endosymbiotic nitrogen fixation. Subsequent to the WGD, the M. truncatula genome experienced higher levels of rearrangement than two other sequenced legumes, Glycine max and Lotus japonicus. M. truncatula is a close relative of alfalfa (Medicago sativa), a widely cultivated crop with limited genomics tools and complex autotetraploid genetics. As such, the M. truncatula genome sequence provides significant opportunities to expand alfalfa's genomic toolbox.
1,153 citations
"Biogeography of nodulated legumes a..." refers background in this paper
...…herbaceous’ IRLC includes many economically important legumes such as common peas (Pisum sativum), lentils (Lens culinaris), chickpea, vetches (Vicia spp.), clover (Trifolium spp.) and lucerne (alfalfa) (Medicago sativa), as well as the model legumeMedicago truncatula (Young et al., 2011)....
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