7/27/2019 Root Nodules(Rhizobium Legumes).pdf

1/2

Root Nodules (Rhizobium,Legumes)Nicholas J Brewin,John Innes Centre, Norwich, UK

Legume root nodules provide a built-in supply of nitrogen fertilizer. Nodules arise from a

symbiotic association with soil bacteria termed rhizobia that have the capacity to convert

atmospheric nitrogen into a form that is available for plant growth.

Introduction

Nitrogen is an essential nutrient because it is a majorcomponent of proteins and nucleic acids. Although 80% ofthe planets atmosphere is nitrogen, dinitrogen gas ischemically inert and unavailable to higher plants andanimals. The global nitrogen cycle depends on the capacityof certain bacteria and cyanobacteria to reduce atmo-

spheric nitrogen into ammonia, a nitrogenous form thatcan be assimilated by all other organisms.

During the course of human evolution, it is curious thatprimitive agriculturalists selected and cultivated a largenumber of plants belonging to the family Leguminosae(Fabaceae). Examples of grain legumes include beans, peasand lentils, all of which are particularly nutritious becauseof the high protein content of their seed. Examples offodder legumes include clover, alfalfa and vetch, whichcontribute to the fertility of pasture and hence to thenourishment of ruminant animals. Some woody legumesare important sources of timber (e.g. Acacia and Leucae-na), while others (e.g. gorse and broom) are colonizers of

poor and sandy soils where nitrogen (nitrate) is at apremium. In all of these situations, legumes have acompetitive advantage because they are able to establisha root nodulesymbiosis that allows them to be independentof the nitrogen status of the soil.

Legumes have root nodules that harbour soil bacteriacollectivelytermed rhizobia. These symbiotic bacteria havethe capacity to establish a new organ (the root nodule); tocolonize host cells; and to develop the capacity for nitrogenfixation inside plant tissues. The legume root nodule is afully differentiated tissue with many distinct cell typesshowing morphological and functional specialization. Itsphysiology is fully integrated into the growth anddevelopment of the whole plant.

Biochemistry and Physiology

Nitrogen fixation depends on a complex of bacterialenzymes termed nitrogenase. At the heart of the catalyticprocess is a highly complex cofactor comprising iron,molybdenum and sulfur. The conversion of dinitrogen to

ammonia requires large amounts of energy and reductanAt least 16 molecules of energy-carrying ATP (adenosintriphosphate) are consumed during the reduction of eacmolecule of nitrogen. Hydrogen is always evolved as a byproduct (eqn [I]).

N2+8H++8e 2NH3+H2 [ I]

The nitrogenase enzymes are highly sensitive to oxygedamage, yet rhizobia require oxygen for growth anrespiration. In general, rhizobia do not fix nitrogen in thsoil but only within root nodules where the internal oxygeconcentration is regulated to be about 1000 times belowambient (330 nmol L1). Despite the low oxygen concentration, the intracellular rhizobia sustain a vigorous level ooxidative respiration. Oxygen diffusion is facilitatethrough intercellular air spaces and through an oxygescavenging haemoprotein (leghaemoglobin) that represents a major component of the cytoplasm in nodule cells

The differentiated nitrogen-fixing forms of rhizobia artermed bacteroids. Bacteroids are enclosed within a hosderived membrane (the peribacteroid membrane) tharegulates metabolic exchanges between the bacterium anits intracellular environment. Organic acids (e.g. malateare apparently the principal carbon source transported tbacteroids. Ammonia, the primary product of nitrogefixation, is exported to the host cell cytoplasm and isubsequently assimilated by the action of glutaminsynthase. In effect, the peribacteroid unit operates like prokaryote organelle concerned with nitrogen fixation: itoften referred to as a symbiosome.

Symbiosis is based on metabolic exchange for mutuabenefit. The plant supplies carbon from photosynthesand the root nodule provides a low-oxygen niche forhizobium. In exchange, rhizobium provides the plant witits own source of fixed nitrogen.

Bacterial and Plant Genetics

A number of rhizobium genes are critical for host-specifinodulation on legumes, but are not necessary for survivaas free-living soil bacteria. The products of these nodgene

Article Contents

Introductory article

. Introduction

. Biochemistry and Physiology

. Bacterial and Plant Genetics

. Taxonomy and Evolution

ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net

7/27/2019 Root Nodules(Rhizobium Legumes).pdf

2/2

are involved in a molecular dialogue that results in theinitiation of nodule development on the appropriate hostlegume.

Each legume host exudes a characteristic set of organiccompounds (flavonoids) that are sensed specifically by thenodD gene product(s) of an infective rhizobium strain.Following this recognition event, transcription of a further

set of rhizobium nodgenes takes place. This culminates inthe synthesis and secretion of specific signal molecules,termed Nod factors that specifically activate host cells ofthe appropriate legume. Structurally, Nod factors arechemically decorated oligomers of N-acetylglucosamine(the constituent of chitin) and, characteristically, they eachcarry an unsaturated acyl chain on the nonreducing sugar.By a process that is still not understood at the molecularlevel, Nod factors initiate nodule initiation by inducingcortical cell divisions. Nod factors also promote host cellcolonization by provoking a reorganization of cell wallgrowth in epidermal cells and root hairs.

Taxonomy and Evolution

When rhizobial strains are analysed by standard taxo-nomic criteria based on gene sequence comparisons, it isclear that these bacteria do not form part of a homo-geneous taxonomic group. The Rhizobiaceae as a distinctbacterial family does not exist. The clear implication is thatnod genes, nitrogenase genes and other genes concernedwith intracellular symbiosis have been transferred hor-izontally by gene exchange between various groups of soilbacteria to create new genetic combinations that areoptimally adapted both for survival in the soil and for thenodulation of some particular legume host.

On the plant side, the Leguminosae constitute a verylarge family (18 000 species), within which the capacity todevelop root nodules appears to have evolved several times

independently. However, the predisposition to form roonodules is not restricted to the Leguminosae but rather tthe Rosid clade I, which includes the Leguminosae as jusone of its families. Unlike all other groups of higher plantthis clade contains several instances of the evolution onon-legume root nodule symbioses. In these cases thnodule endophyte is not a rhizobial strain (as currentl

defined) but is instead an actinomycete, Frankia, filamentous Gram-positive bacterium. Examples of actnorhizal plants include Alnus, Caeanothus and CasuarinaThere is one example of a non-legume root nodulsymbiosis in which the endophyte is unquestionably rhizobium strain: this involves the ulmaceous shruParasponia, which also belongs to Rosid clade I.

Further Reading

Brewin NJ (1991) Development of the legume root nodule. Annu

Review of Cell Biology 7: 191226.Cook DR (1999) Medicago truncatula a model in the making! Curre

Opinion in Plant Biology 2: 301304.

Crespi M and Galvez S (2000) Molecular mechanisms in root nodu

development. Journal of Plant Growth Regulation 19: 155166.

Downie JA and Brewin NJ (1999) Plantmicroorganism symbiosis. I

Russo VEA et al. (eds) Development Genetics, Epigenetics an

Environmental Regulation, pp. 211232. Berlin: Springer-Verlag.

Gualtieri G and Bisseling T (2000) The evolution of nodulation. Pla

Molecular Biology 42: 181194.

ParniskeM (2000) Intracellularaccommodation of microbes by plants

common developmental program for symbiosis and disease?Curre

Opinion in Plant Biology 3: 320328.

Schultze M and Kondorosi A (1998) Regulation of symbiotic ro

nodule development. Annual Review of Genetics 32: 3357.

Spaink HP (2000) Root nodulation and infection factors produced rhizobial bacteria. Annual Review of Microbiology 54: 257288.

Sprent JI (2001) Nodulation in Legumes. London: Cromwell Press.

Stougaard J (2000) Regulators and regulation of legume root nodu

development. Plant Physiology 124: 531540.

Root Nodules (Rhizobium, Legumes)

2 ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net