The beneficial plant growth-promoting association of Rhizobium leguminosarum bv. trifolii with rice roots

This paper summarizes a multinational collaborative project to search for n atural, intimate associations between rhizobia and rice (Oryza sativa L.), assess their impact on plant growth, and exploit those combinations that ca n enhance grain yield with less dependence on inputs of nitrogen (N) fertil izer. Diverse, indigenous populations of Rhizobium leguminosarum bv. trifol ii (the clover root-nodule endosymbiont) intimately colonize rice roots in the Egyptian Nile delta where this cereal has been rotated successfully wit h berseem clover (Trifolium alexandrinum L.) since antiquity. Laboratory an d greenhouse studies have shown with certain rhizobial strain-rice variety combinations that the association promotes root and shoot growth thereby si gnificantly improving seedling vigour that carries over to significant incr eases in grain yield at maturity. Three field inoculation trials in the Nil e delta indicated that a few strain-variety combinations significantly incr eased rice grain yield, agronomic fertilizer N-use efficiency and harvest i ndex. The benefits of this association leading to greater production of veg etative and reproductive biomass more likely involve rhizobial modulation o f the plant's root architecture for more efficient acquisition of certain s oil nutrients [e.g. N, phosphorus (P), potassium (K), magnesium (Mg), calci um (Ca), zinc (Zn), sodium (Na) and molybdenum (Mo)] rather than biological N-2 fixation. Inoculation increased total protein quantity per hectare in field-grown grain, thereby increasing its nutritional value without alterin g the ratios of nutritionally important proteins. Studies using a selected rhizobial strain (E11) indicated that it produced auxin (indoleacetic acid) and gibberellin [tentatively identified as gibberellin (GA(7))] phytohormo nes representing two major classes of plant growth regulators. Axenically c ollected rice root exudate significantly enhanced E11's production of this auxin. This strain extensively colonized the rice root surface under gnotob iotic culture conditions, producing distributions of spatial patchiness tha t would favour their localized erosion of the epidermal surface, colonizati on of small crevices at epidermal junctions as a possible portal to enter i nto the root, and quorum sensing of diffusible signal molecules indicating that their nearest bacterial neighbours are in close proximity in situ. Stu dies of selected rhizobial endophytes of rice indicated that they produced cell-bound cellulase and polygalacturonase enzymes that can hydrolyze glyco sidic bonds in plant cell walls, and non-trifolitoxin bacteriocin(s) that c an inhibit other strains of clover rhizobia. Strain E11 was able to endophy tically colonize rice roots of varieties commonly used by Filipino peasant farmers, and also to stimulate genotype-specific growth-promotion of corn ( Zea mays, maize) under field conditions. An amalgam of these results indica te some rhizobia have evolved an additional ecological niche enabling them to form a three-component life cycle including a free-living heterotrophic phase in soil, a N-2-fixing endosymbiont phase within legume root nodules, and a beneficial growth-promoting endocolonizer phase within cereal roots i n the same crop rotation. Our results further indicate the potential opport unity to exploit this newly described, plant-rhizobia association by develo ping biofertilizer inoculants that may assist low-income farmers in increas ing cereal production (especially rice) with less fertilizer N inputs, full y consistent with both sustainable agriculture and environmental safety.