The Legume-Rhizobium Symbiosis

by

Joel L. Sachs, Kelsey Gano-Cohen, Amanda C. Hollowell, John U. Regus

• LAST REVIEWED: 24 July 2013
• LAST MODIFIED: 24 July 2013
• DOI: 10.1093/obo/9780199830060-0095

Introduction

Most plants on earth do not have sufficient soil nitrogen. Yet legumes (plants in the family Fabaceae), unlike most plants, have access to nitrogen from both mineral sources and symbiotic sources. Legumes can become infected with nitrogen-fixing bacteria known as rhizobia. These bacteria live in the soil, and when a legume grows nearby a molecular communication ensues that enables the legume roots to become infected. In a process guided by both the bacteria and the plant, the rhizobia invade plant tissue and ultimately inhabit individual plant cells within the host’s roots. Once inside the plant, the rhizobia can become efficient symbionts, breaking down dinitrogen from air pockets in the soil into forms that are useful for the plant, in exchange for sugars from the plant. This legume-rhizobium interaction has become a key model for dissecting the molecular basis for communication among species and represents one of the best-understood mutualistic symbioses. Nonetheless, much remains to be understood about this system. Although the host plant appears to have control over key aspects of rhizobial infection and growth within host tissues, the mechanistic basis of this control is poorly understood, and it is unknown how such control evolved. Also, rhizobia could represent a massive boon to agriculture, since they might allow us to avoid the costly process of industrial nitrogen fixation. But the use of rhizobia in agricultural systems has been relatively unsuccessful, and research has made only modest progress in solving this critical problem. While researchers have characterized hundreds of rhizobial strains that fix nitrogen very effectively under greenhouse conditions, these strains are often unsuccessful at competing against indigenous soil rhizobia under real field conditions. Although some biologists hold great hopes for the use of rhizobia to enhance legume production, this promise still remains mostly unrealized. Understanding this symbiosis is a problem that relates to many fields including biology, biochemistry, ecology, evolution, genetics, physiology, and agronomic sciences. An integrative ecological and evolutionary perspective is useful in the study of the legume-rhizobium symbiosis. This emerging perspective takes into account the immense diversity of the legumes and rhizobia that take part in the symbiosis as well as the diverse ecological conditions under which rhizobia and legumes interact. Moreover, this perspective seeks to understand how natural selection shapes each partner and how the interaction can vary depending on extrinsic conditions. This broad view might ultimately enable us to better manipulate the interaction to optimize agricultural productivity. Here, we begin by inferring the evolutionary history of legume and rhizobial lineages to better understand the diversity of both partners. We then describe the molecular and cellular mechanisms of infection and how the mechanistic basis of the symbiosis can vary among host and symbiont lineages. Finally, we turn to evolutionary and ecological aspects of the interaction. We review the selective forces that maintain cooperation between symbionts and hosts and explore the utility of evolutionary theory for optimizing agricultural productivity.

Introductory Works

Sprent 2001 documents the many species in the legume family that have the ability to form intimate, intracellular associations with diverse nitrogen-fixing bacteria, known as rhizobia. As Sprent, et al. 1987, a seminal review, explains, legumes begin life in a symbiont-free state and they acquire rhizobial symbionts in the soil each generation. Typically, rhizobia first infect legume seedlings soon after germination and form tumors (nodules) on the plant’s roots. For a successful infection, a compatible pairing of legume and rhizobial genotypes is required. However, as the key review Denison 2000 describes, the degree of specificity varies widely for both the bacteria and the plant partners. Once a symbiotic nodule is formed, the bacteria fix nitrogen for the plant in exchange for plant-derived photosynthates. Nodules eventually senesce, a process that Denison and Kiers 2004 argues is critical for rhizobia to escape back into the soil; the nodule tissue softens and breaks down, after which a subset of the rhizobia are released from the plant. An ecological meta-analysis, Cleveland, et al. 1999, showed how important legume-rhizobium symbioses are at a global scale, because symbiotic rhizobia convert atmospheric dinitrogen into compounds that are useable to legumes and ultimately to other plants. In terms of agriculture, only a handful of legume species are cultivated on a large scale, but Ferguson, et al. 2010 points out that these crops contribute more than 25 percent of global production, including food staples, fodder for livestock, cover crops, and emerging biofuels. There is a clear need to better understand the legume-rhizobium symbiosis both in the wild and in agriculture. Finally, it is important to note that the legume-rhizobium symbiosis is not unique. Other plants such as alders can also form nitrogen-fixing symbioses with bacteria; moreover, Sturz, et al. 2000 argues that a diversity of bacteria act as nitrogen-fixing bacterial endophytes and can provide growth benefits to many plants.

• Cleveland, C. C., A. R. Townsend, D. S. Schimel, et al. 1999. Global patterns of terrestrial biological nitrogen (N₂) fixation in natural ecosystems. Global Biogeochemical Cycles 13:623–645.

  DOI: 10.1029/1999GB900014

  This expansive meta-analysis of biological nitrogen fixation discusses the global importance and biome specificity of natural sources of nitrogen fixation.

• Denison, R. F. 2000. Legume sanctions and the evolution of symbiotic cooperation by rhizobia. American Naturalist 156:567–576.

  DOI: 10.1086/316994

  This seminal paper was the first to broadly review the evolution and ecology of cooperation in the legume-rhizobium symbiosis. Denison offered the first general description of host sanctions in this system and provides key information about the symbiosis in the language of evolutionary biologists and ecologists.

• Denison, R. F., and E. T. Kiers. 2004. Lifestyle alternatives for rhizobia: Mutualism, parasitism, and forgoing symbiosis. FEMS Microbiology Letters 237:187–193.

  DOI: 10.1111/j.1574-6968.2004.tb09695.x

  This conceptual paper explores rhizobial lifestyles that extend beyond beneficial symbiosis, including exploitation of the legume host (parasitism) and growth in the soil without host infection. Unlike previous work on this topic, this paper explores the different outcomes of symbiosis from the point of view of the bacterium and highlights the diverse ecological contexts that challenge rhizobial bacteria.

• Ferguson, B. J., A. Indrasumunar, S. Hayashi, et al. 2010. Molecular analysis of legume nodule development and autoregulation. Journal of Integrative Plant Biology 52:61–76.

  DOI: 10.1111/j.1744-7909.2010.00899.x

  This paper provides an extremely broad and detailed review of what is known about the molecular bases of host mechanisms that control nodule development. This is one of the key works that attempt to make clear connections with the phenotypes of how hosts control rhizobial infections and the molecular bases of these plant traits. Moreover, the authors offer an excellent description of the global importance of nitrogen fixation in legume nodules.

• Sprent, J. I. 2001. Nodulation in legumes. Kew, UK: Royal Botanic Gardens.

  This book explores the biology and diversity of rhizobial nodulation in legumes.

• Sprent, J. I., J. M. Sutherland, and S. M. de Faria. 1987. Some aspects of the biology of nitrogen-fixing organisms. Philosophical Transactions of the Royal Society of London, B: Biological Sciences 317:111–129.

  DOI: 10.1098/rstb.1987.0051

  This excellent review offers one of the very early introductions to the basic biology of the legume-rhizobium symbiosis. If one wants to learn about this symbiosis in general, this is a great place to start.

• Sturz, A. V., B. R. Christie, and J. Nowak. 2000. Bacterial endophytes: Potential role in developing sustainable systems of crop production. Critical Reviews in Plant Sciences 19:1–30.

  DOI: 10.1016/S0735-2689(01)80001-0

  This review explores the diverse types of beneficial interactions that soil bacteria can have when residing within nonlegume plant roots. It explores multiple mechanisms by which these bacterial lineages can enhance plant growth, especially in agricultural systems.