The beneficial plant growth-promoting association of Rhizobium leguminosarum bv. trifolii with rice roots
Authors: Yanni Youssef G. , Rizk Rizk Y. , El-Fattah Faiza K. Abd , Squartini Andrea , Corich Viviana , Giacomini Alessio , de Bruijn Frans , Rademaker Jan , Maya-Flores Jaime , Ostrom Peggy , Vega-Hernandez Maria , Hollingsworth Rawle I. , Martinez-Molina Eustoquio , Mateos Pedro , Velazquez Encarna , Wopereis Judith , Triplett Eric , Umali-Garcia Mercedes , Anarna Juliet A. , Rolfe Barry G. , Ladha Jadish K. , Hill James , Mujoo Rajni , Ng Perry K. , Dazzo Frank B. 
Published: September 2002

This paper originates from an address at the 8th International Symposium on Nitrogen Fixation with Non-Legumes, Sydney, NSW, December 2000
This paper summarizes a multinational collaborative project to search for
natural, intimate associations between rhizobia and rice
(Oryza sativa L.), assess their impact on plant growth,
and exploit those combinations that can enhance grain yield with less
dependence on inputs of nitrogen (N) fertilizer. Diverse, indigenous
populations of Rhizobium leguminosarum bv. trifolii (the
clover root-nodule endosymbiont) intimately colonize rice roots in the
Egyptian Nile delta where this cereal has been rotated successfully with
berseem clover (Trifolium alexandrinum L.) since
antiquity. Laboratory and greenhouse studies have shown with certain rhizobial
strain–rice variety combinations that the association promotes root and
shoot growth thereby significantly improving seedling vigour that carries over
to significant increases in grain yield at maturity. Three field inoculation
trials in the Nile delta indicated that a few strain–variety
combinations significantly increased rice grain yield, agronomic fertilizer
N-use efficiency and harvest index. The benefits of this association leading
to greater production of vegetative and reproductive biomass more likely
involve rhizobial modulation of the plant’s root architecture for more
efficient acquisition of certain soil nutrients [e.g. N, phosphorus (P),
potassium (K), magnesium (Mg), calcium (Ca), zinc (Zn), sodium (Na) and
molybdenum (Mo)] rather than biological N2 fixation. Inoculation
increased total protein quantity per hectare in field-grown grain, thereby
increasing its nutritional value without altering 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 )]
phytohormones representing two major classes of plant growth regulators. Axenically collected rice root exudate significantly enhanced E11’s production of this auxin. This strain extensively colonized the rice root surface under gnotobiotic culture conditions, producing distributions of spatial patchiness that would favour their localized erosion of the epidermal surface, colonization of small crevices at epidermal junctions as a possible portal to enter into the root, and quorum sensing of diffusible signal molecules indicating that their nearest bacterial neighbours are in close proximity in situ. Studies of selected rhizobial endophytes of rice indicated that they produced cell-bound cellulase and polygalacturonase enzymes that can hydrolyze glycosidic bonds in plant cell walls, and non-trifolitoxin bacteriocin(s) that can inhibit other strains of clover rhizobia. Strain E11 was able to endophytically 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 indicate 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 N2-fixing endosymbiont phase within legume root nodules, and a beneficial growth-promoting endocolonizer phase within cereal roots in the same crop rotation. Our results further indicate the potential opportunity to exploit this newly described, plant�rhizobia association by developing biofertilizer inoculants that may assist low-income farmers in increasing cereal production (especially rice) with less fertilizer N inputs, fully consistent with both sustainable agriculture and environmental safety.