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Biological Nitrogen Fixation

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Biological Nitrogen Fixation See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/318670413 Biological nitrogen fixation Article · January 2015 CITATIONS READS 4 4,620 9 authors, including: Sergio Svistoonoff Alexandre Tromas Institute of Research for Development CCG, UNAM, Cuernavaca, Mexico 102 PUBLICATIONS 1,783 CITATIONS 33 PUBLICATIONS 410 CITATIONS SEE PROFILE SEE PROFILE Nathalie Diagne Laurent Laplaze Institut Sénégalais de Recherches Agricoles Institute of Research for Development 49 PUBLICATIONS 331 CITATIONS 179 PUBLICATIONS 6,298 CITATIONS SEE PROFILE SEE PROFILE Some of the authors of this publication are also working on these related projects: pgpr wheat and phaseolus v View project Root biology and adaptation to abiotic stresses in pearl millet View project All content following this page was uploaded by Didier Bogusz on 04 August 2017. The user has requested enhancement of the downloaded file. Annals of Botany 111: 743–767, 2013 doi:10.1093/aob/mct048, available online at www.aob.oxfordjournals.org INVITED REVIEW Biological nitrogen fixation in non-legume plants Carole Santi1, Didier Bogusz2 and Claudine Franche2,* 1Universite´ de Perpignan, Via Domitia, Avenue Paul Alduy, 66100 Perpignan, France and 2Equipe Rhizogene`se, UMR DIADE (IRD/UM2), Institut de Recherche pour le De´veloppement, 911 Avenue Agropolis, BP64501, 34394 Montpellier Cedex 5, France * For correspondence. E-mail [email protected] Received: 4 October 2012 Revision requested: 28 November 2012 Accepted: 23 January 2013 Published electronically: 10 March 2013 † Background Nitrogen is an essential nutrient in plant growth. The ability of a plant to supply all or part of its requirements from biological nitrogen fixation (BNF) thanks to interactions with endosymbiotic, associative and endophytic symbionts, confers a great competitive advantage over non-nitrogen-fixing plants. † Scope Because BNF in legumes is well documented, this review focuses on BNF in non-legume plants. Despite the phylogenic and ecological diversity among diazotrophic bacteria and their hosts, tightly regulated communi- cation is always necessary between the microorganisms and the host plant to achieve a successful interaction. Ongoing research efforts to improve knowledge of the molecular mechanisms underlying these original relation- ships and some common strategies leading to a successful relationship between the nitrogen-fixing microorgan- isms and their hosts are presented. † Conclusions Understanding the molecular mechanism of BNF outside the legume–rhizobium symbiosis could have important agronomic implications and enable the use of N-fertilizers to be reduced or even avoided. Indeed, in the short term, improved understanding could lead to more sustainable exploitation of the biodiversity of ni- trogen-fixing organisms and, in the longer term, to the transfer of endosymbiotic nitrogen-fixation capacities to major non-legume crops. Key words: Nitrogen fixation, non-legume, symbiosis, nodulation, actinorhizal plant, Frankia, cyanobacteria, Parasponia, plant growth-promoting rhizobacteria, PGPR. INTRODUCTION diazotrophs. Various types of associations/interactions occur between diazotrophs and their host plants. The highly specific Nitrogen is an essential element in plant development and a and most efficient processes for nitrogen fixation involve the limiting factor in plant growth. It represents about 2 % of the formation of root nodules on legumes and non-legumes. The total plant dry matter that enters the food chain. diazotrophic bacteria involved in these endosymbiotic interac- Nevertheless, plants cannot directly access dinitrogen gas, tions include rhizobia (Gram negative) members of the alpha- which makes up about 80 % of the atmosphere. Plants subgroup of the phylum proteobacteria that associate with absorb the available nitrogen in the soil through their roots legumes (family Fabaceae) (not included in this review; see in the form of ammonium and nitrates. The limited bio- Schultze and Kondorosi, 1998; Oldroyd and Downie, 2008; availability of nitrogen and the dependence of crop growth Desbrosses and Stougaard, 2011) and the non-legume on this element have spawned a massive N-based fertilizer in- Parasponia species (family Cannabaceae), and Frankia sp. dustry worldwide (Dobermann, 2007; Westhoff, 2009). About (Gram positive) members of the actinomycete family that as- 60 % of synthetic nitrogen fertilizers are presently used for sociate with a broad spectrum of plants belonging to eight cereals, with irrigated rice production accounting for approx. families collectively called actinorhizal plants. In addition, 10 % of the use. Since .50 % of the fertilizer applied is actu- nitrogen-fixing cyanobacteria (mainly Nostoc sp.) have also ally used by plants, the inefficient use of nitrogen contributes been found to colonize different plant organs, either intracellu- to nitrate contamination of soils and ground water, leading to larly in the family Gunneraceae or extracellularly in liver- health hazards and compromising agricultural sustainability. worts, hornworts, Azolla and Cycadaceae. In contrast with Moreover, manufacturing N fertilizer requires six times more these symbioses, some diazotrophs, such as Azospirillum energy than that needed to produce either P or K fertilizers spp., Azoarcus spp. and Herbaspirillum, form associative (Da Silva et al., 1978). and/or endophytic relationships with a wide variety of plant Only some prokaryotes are able to use atmospheric nitrogen roots including those of cereals. In all these associations and through a process known as biological nitrogen fixation (BNF), symbioses, for the host plants the expected benefit of the inter- which is the conversion of atmospheric N2 to NH3, a form that action is the fixed nitrogen provided by the symbiotic partner, can be used by plants (Lam et al., 1996; Franche et al., 2009). which, in return, receives reduced carbon and possibly all the The bacteria responsible for nitrogen fixation are called diazo- other nutrients it requires. In addition, the symbiotic or endo- trophs; they encode nitrogenase, the enzyme complex that cat- phytic plant structure colonized by the nitrogen-fixing micro- alyses the conversion of N2 gas to ammonia. The nitrogenase organisms may provide the appropriate conditions for complex is highly conserved in free-living and symbiotic protecting the nitrogenase complex from oxygen exposure. # The Author 2013. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: [email protected] 744 Santi et al. — Biological nitrogen fixation in non-legume plants Rhizosphere associations between nitrogen-fixing microor- 1990). In addition, these perennial plants contribute to the N ganisms and plants have been a major driving force in allow- cycle through litter fall and soil decomposition. ing organisms to spread across the biosphere, occupy new niches, and adapt to a variety of environmental stresses. This Nitrogen-fixing actinobacteria Frankia review presents an overview and recent advances in the under- standing of the associations between a wide range of diazo- Frankia is a genus of soil actinomycetes in the family trophs and non-legumes. Discoveries and breakthroughs in Frankiaceae that fix nitrogen, both under symbiotic and free- legume and non-legume nitrogen fixation provide new living aerobic conditions, while most rhizobia do not insight into ways of manipulating key steps in this process. (Benson and Silvester, 1993). Phylogenetically, the filament- Finally, new perspectives to engineer nitrogen-fixing ability ous gram-positive Frankia sp. and the unicellular gram- in non-legume crops based on knowledge of endosymbiotic negative paraphyletic rhizobia are quite distant, suggesting processes in non-legumes are discussed. that these two major groups of nitrogen-fixing symbionts have acquired mechanisms for nitrogen fixation from different evolutionary origins (Normand et al., 1996). The first success- ful isolation of Frankia was reported relatively recently from ACTINORHIZAL SYMBIOSES Comptonia peregrina root nodules (Callaham et al., 1978). At present, over 200 strains of Frankia have been isolated Actinorhizal plants and their major ecological role from many, although not all, actinorhizal plant species. Actinorhizal plants have the ability to develop an endosymbi- Phylogenetic analyses revealed that Frankiae form a coherent osis with the nitrogen-fixing soil actinomycete Frankia. The clade within actinobacteria, and that strains generally fall into establishment of the symbiotic process results in the formation three major groups or clusters (Normand et al., 1996; Benson of root nodules in which Frankia provides fixed nitrogen to the and Clawson, 2000; Hahn, 2008). Cluster I consists of strains host plant in exchange for reduced carbon. Actinorhizal plants isolated from plants belonging to the order Fagales; they have represent a diverse group of about 220 species belonging to the most specific host range and are only able to interact with eight plant families distributed in the three orders, Fagales plants belonging to this clade. Strains belonging to cluster III (Betulaceae, Casuarinaceae and Myricaceae), Rosales have a wider host range and can interact with plants belonging (Rosaceae, Eleagnaceae and Rhamnaceae) and Cucurbitales to five families within the two distant plant orders Rosales and (Datiscaceae and Coriariaceae) (Wall, 2000; Pawlowski, Fagales. No strain belonging
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