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Advances in Rhizobium Research Critical Reviews in Plant Sciences, 21(4):323–378 (2002) Advances in Rhizobium Research A. Sessitsch,1* J.G. Howieson,2 X. Perret,3 H. Antoun,4 and E. Martínez- Romero5 1ARC Seibersdorf research GmbH, Division of Environmental and Life Sciences, A-2444 Seibersdorf, Austria; 2Centre for Rhizobium Studies, Murdoch University, Murdoch 6150, Western Australia; 3Laboratoire de Biologie Moléculaire des Plantes Supérieures, Université de Genève, 1292 Chambésy, Geneva, Switzerland; 4Recherche en Sciences de la Vie et de la Santé, Université Laval, Quebec, Canada; 5Centro de Investigacion Sobre Fijacion de Nitrogeno, UNAM, Cuernavaca, Morelos, Mexico Referee: Prof. Dr. Dietrich Werner, FG Zellbiologie und Angewandte Botanik, Fachbereich Biologie, Philipps-Universität Marburg, Karl-von-Frisch-Strasse, D-35032 Marburg, Germany * Author for correspondence. (Tel: +43 50550 3509; fax: +43 50550 3444; e-mail: [email protected]) ABSTRACT: Rhizobia are well known for their capacity to establish a symbiosis with legumes. They inhabit root nodules, where they reduce atmospheric nitrogen and make it available to the plant. Biological nitrogen fixation is an important component of sustainable agriculture, and rhizobial inoculants have been applied frequently as biofertilizers. In this review we present recently developed technologies and strategies for selecting quality inoculant strains by taking into consideration the complex interaction between the edaphic environment with the genotypes of both the legume and its microsymbiont. Enhanced competitive ability in an inoculant strain is a key requirement for successful colonization of plant roots, nodule formation, and subsequent N2-fixation. We discuss several avenues for the management and manipulation of rhizobial competition as well as genes that influence competition in the rhizosphere. The use of molecular techniques has greatly contributed to our knowledge of nodule-bacterial diversity and phylogeny. Approaches to the study of rhizobial diversity as well as mechanisms for the evolutionary diversification of nodulating bacteria are presented. Rhizobium genomes ranging from 5.5 to 9 Mb have been sequenced recently and deposited in public databases. A comparison of sequence data has led to a better understanding of genes involved in the symbiotic process as well as possible mechanisms responsible for horizontal transfer of genetic elements and symbiosis genes among rhizobia. Furthermore, rhizobia are frequent rhizosphere colonizers of a wide range of plants and may also inhabit nonleguminous plants endophytically. In these rhizospheric and endophytic habitats they may exhibit several plant growth-promoting effects, such as hormone production, phosphate solubilization, and the suppression of pathogens. KEY WORDS: biological nitrogen fixation, rhizobial competition, diversity, genome structure, plant growth promotion. I. INTRODUCTION gume crops and pasture species often fix as much as 200 to 300 kg nitrogen per hectare (Peoples Rhizobia encompass a range of bacterial gen- et al., 1995). Globally, symbiotic nitrogen fixa- era, including Rhizobium, Bradyrhizobium, tion has been estimated to amount to at least 70 Sinorhizobium, Mesorhizobium, Allorhizobium, million metric tons of nitrogen per year (Brockwell and Azorhizobium, which are able to establish a et al., 1995). In 1999, world consumption of fer- symbiosis with leguminous plants. They elicit the tilizer nitrogen was 88 million tons and apart formation of specialized organs, called nodules, from the consumption of nonrenewable energy on roots or stems of their hosts, in which they sources, environmental pollution from fertilizer reduce atmospheric nitrogen and make it avail- nitrogen escaping the root zone is high because in able to the plant. Symbiotic nitrogen fixation is an many cases nitrogen fertilizers are not used effi- important source of nitrogen, and the various le- ciently by crops (Peoples et al., 1994). Therefore, 0735-2689/02/$.50 © 2002 by CRC Press LLC 323 biological nitrogen fixation is an important and Perception and transduction of these key signal integral component of sustainable agricultural molecules for nodule organogenesis has been re- systems. Furthermore, biological nitrogen fixa- viewed recently (Broughton et al., 2000; tion from legumes offers more flexible manage- Miklashevichs et al., 2001). Genes involved in ment than fertilizer nitrogen because the pool of the nodulation process or in determining competi- organic nitrogen becomes slowly available to tive ability have also been identified recently and nonlegume species (Peoples et al., 1995). Con- are addressed in this review (see Section III), as comitant with N2-fixation, the use of legumes in are several attempts to improve nitrogen fixation rotations offers control of crop diseases and pests by genetic engineering. Furthermore, the sequence (Robson, 1990; Graham and Vance, 2000). information of whole rhizobial genomes (Kaneko Inoculation of legumes with rhizobial strains et al., 2000; Galibert et al., 2001) or symbiotic selected for high N2-fixing capacity can improve islands (Freiberg et al., 1997; Göttfert et al., 2001) nitrogen fixation in agriculture, particularly when has become available, providing a more complete local rhizobial strains are absent from soils or picture of rhizobial genomes, which is discussed ineffective. However, newly introduced strains in Section V. often fail to compete with well-adapted indig- The objective of this review is to synthesize enous populations. Substantial efforts have been fundamental results from very early research re- undertaken to improve nodulation by trying to ports with modern outputs. We hope the outcome understand the factors that affect the interactions of our efforts is to stimulate research at many between rhizobia and soil fauna, between macro- levels, from the field to the laboratory, in this vital and microsymbionts, as well as between these process of symbiotic N2-fixation. components and the edaphic environment. Strat- egies to facilitate decision making regarding the choice of legume and — if required — the choice II. ADVANCES IN TECHNOLOGIES AND of an appropriate inoculant strain of rhizobia are STRATEGIES FOR SELECTING addressed in Section II of this review. INOCULANT QUALITY RHIZOBIAL Our understanding of the vast diversity of STRAINS nodulating bacteria has increased extraordinarily due to the application of molecular markers in In this section, we review advances in tech- bacterial taxonomy. The search for novel rhizobia nologies and strategies for selecting inoculant has not only expanded our knowledge on the quality strains of root-nodule bacteria for the pur- evolution of nodule bacteria, but also provided pose of maximizing legume derived N2-fixation very valuable information on strains with varying in agriculture. This objective has been a pursuit of nodulating and N2 fixation capabilities as well as scientists for over 100 years, but it is especially different physiological properties. These aspects relevant in today’s world because biological N2- are discussed in section IV. Furthermore, consid- fixation is considered an essential element of ag- erable knowledge has been obtained on the diver- ricultural sustainability. The Bellagio conference sity and beneficial effects of rhizobia living in on N2-fixation (Kennedy and Cocking, 1997) ac- association with nonleguminous plants. The plant knowledged that with the decline in the price of growth-promoting effects of free-living rhizo- manufactured fertilizer in the 1990s, biological sphere rhizobia as well as of endophytic strains N2-fixation with legumes and rhizobia, was most are reviewed in Section VI. likely to remain in extensive, rather than inten- The interaction between legume and rhizobia sive, agricultural systems. However, Graham and has been studied intensively at a molecular level. Vance (2000) warned that a world decline in ag- This interaction starts with a signal exchange ricultural dependence on biological nitrogen fixa- between both partners. Plant roots secrete spe- tion was incompatible with the need to increase cific flavonoids that interact with the bacterial world protein production from a notably deterio- NodD protein, resulting in the activation of rating area of global arable land. The urgency for rhizobial nod genes and synthesis of Nod factors. advancement in the quality and utilization of 324 rhizobial inoculants (and legumes) in both inten- A. Decision Making Relative to the sive and extensive forms of world agriculture was Adoption of Legumes and in promulgated with some force and clarity. The Assessment of the Requirement to potential economic benefits of improving global Inoculate N2-fixation in agriculture by 10% have been esti- mated at close to US$ 1 billion annually (Herridge The integration of legumes into farming sys- and Rose, 2000). tems is acknowledged to have wide-ranging ben- Relative to the almost weekly advances made efits, the most important being N2-fixation and in our understanding of the genetics of the root the control of cereal crop diseases and pests nodule bacteria, which are covered in later sec- (Robson, 1990; Graham and Vance, 2000). Eight tions of this review, advances made in rhizobial other ancillary benefits to legume cultivation have ecology appear pedestrian. This is not an indict- been listed by Howieson et al. (2000a). Although ment of the outputs from rhizobial ecologists, but legumes have been used since antiquity in human more an affirmation of the complexities
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