Rhizobia promote the growth of rice shoots by targeting cell signaling, division and expansion
The growth-promotion of rice seedling following inoculation with Sinorhizobium meliloti 1021 was a cumulative outcome of elevated expression of genes that function in accelerating cell division and enhancing cell expansion.
Various endophytic rhizobacteria promote the growth of cereal crops. To achieve a better understanding of the cellular and molecular bases of beneficial cereal-rhizobia interactions, we performed computer-assisted microscopy and transcriptomic analyses of rice seedling shoots (Oryza sativa) during early stages of endophytic colonization by the plant growth-promoting Sinorhizobium meliloti 1021. Phenotypic analyses revealed that plants inoculated with live rhizobia had increased shoot height and dry weight compared to control plants inoculated with heat-killed cells of the same microbe. At 6 days after inoculation (DAI) with live cells, the fourth-leaf sheaths showed significant cytological differences including their enlargement of parenchyma cells and reduction in shape complexity. Transcriptomic analysis of shoots identified 2,414 differentially-expressed genes (DEGs) at 1, 2, 5 and 8 DAI: 195, 1390, 1025 and 533, respectively. Among these, 46 DEGs encoding cell-cycle functions were up-regulated at least 3 days before the rhizobia ascended from the roots to the shoots, suggesting that rhizobia are engaged in long-distance signaling events during early stages of this plant-microbe interaction. DEGs involved in phytohormone production, photosynthetic efficiency, carbohydrate metabolism, cell division and wall expansion were significantly elevated at 5 and 8 DAI, consistent with the observed phenotypic changes in rice cell morphology and shoot growth-promotion. Correlation analysis identified 104 height-related DEGs and 120 dry-weight-related DEGs that represent known quantitative-trait loci for seedling vigor and increased plant height. These findings provide multiple evidences of plant–microbe interplay that give insight into the growth-promotion processes associated with this rhizobia-rice beneficial association.
KeywordsEndophytic rhizobia Growth-promotion Computer-assisted microscopy Plant–microbe interaction Rice
We are grateful to Weiwei Zhang for his expertise in microarray data analysis.
WQQ did portions of the experiments and data analysis, and wrote initial drafts of the manuscript. PXJ performed parts of the data re-analysis, re-organization and rewrote major portions of the manuscript. YMF and ZWP performed the cultivation of rice seedlings, their inoculation with S. meliloti 1021, measurement of rice seedling growth, and collection of samples for the microarray experiments. FBD and NTU made valuable suggestions on this work and manuscript revisions based on their research participation in this field. FBD also contributed some of the quantitative image analyses of cell populations within tissue samples. SSH and YXJ were responsible for originating the overall concept and the successive experimental designs, evaluating the scientific implications of the data obtained, and participated in preparation of the manuscript. All authors approved the final manuscript.
This work was supported by the State Key Basic Research and Development Plan of China (2010CB126503).
Compliance with ethical standards
Conflict of interest
The authors have no conflicts of interest to declare.
- Dermatsev V, Weingarten-Baror C, Resnick N, Gadkar V, Wininger S, Kolotilin I et al (2010) Microarray analysis and functional tests suggest the involvement of expansins in the early stages of symbiosis of the arbuscular mycorrhizal fungus Glomus intraradices on tomato (Solanum lycopersicum). Mol Plant Pathol 11:121–135CrossRefGoogle Scholar
- Frankenberger WT Jr, Arshad M (1995) Phytohormones in soil: microbial production and function. Marcel Dekker Inc, New YorkGoogle Scholar
- Machado RG, de Sá ELS, Bruxel M, Giongo A, Santos NDS, Nunes AS (2013) Indoleacetic acid producing rhizobia promote growth of tanzania grass (Panicudm maximum) and pensacola grass (Paspalum saurae). Int J Agric Biol 15:827–834Google Scholar
- Perrine FM, Prayitno J, Weinman JJ, Dazzo FB, Rolfe BG (2001) Rhizobium plasmids are involved in the inhibition or stimulation of rice growth and development. Austr J Plant Physiol 28:923–937Google Scholar
- Reddy PM, Ladha JK, So RB, Hernandez RJ, Ramos MC, Angeles OR et al (1997) Rhizobial communication with rice roots: Induction of phenotypic changes, mode of invasion and extent of colonization. In: Ladha JK, de Bruijn FJ, Malik KA (eds) Opportunities for biological nitrogen fixation in rice and other non-legumes. Kluwer, Dordrecht, pp 81–98CrossRefGoogle Scholar
- Yanni YG, Rizk RR, El-Fattah FKA, Squartini A, Corich V et al (2001) The beneficial plant growth-promoting association of Rhizobium leguminosarum bv. trifolii with rice roots. Austr J Plant Physiol 28:845–870Google Scholar
- Yoshida S, Forno DA, Cock J, Gomez KA (1972) Laboratory manual for physiological studies of rice. Int Rice Res Inst, ManilaGoogle Scholar