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Plant Molecular Biology

, Volume 97, Issue 6, pp 507–523 | Cite as

Rhizobia promote the growth of rice shoots by targeting cell signaling, division and expansion

  • Qingqing Wu
  • Xianjun Peng
  • Mingfeng Yang
  • Wenpeng Zhang
  • Frank B. Dazzo
  • Norman Uphoff
  • Yuxiang Jing
  • Shihua Shen
Article

Abstract

Key message

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.

Abstract

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.

Keywords

Endophytic rhizobia Growth-promotion Computer-assisted microscopy Plant–microbe interaction Rice 

Notes

Acknowledgements

We are grateful to Weiwei Zhang for his expertise in microarray data analysis.

Author contributions

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.

Funding

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.

Supplementary material

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Supplementary Figure 6 Classification and distribution of differentially expressed TFs and PKs in rice seedlings responding to S. meliloti 1021 LC inoculation at the 4 time points. The vertical axis represents the number of upregulated TFs/PKs genes at the 4 different time points distinguished by their colors. TFs: transcript factors, PKs: protein kinases (TIF 1208 KB)
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Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Qingqing Wu
    • 1
  • Xianjun Peng
    • 1
  • Mingfeng Yang
    • 1
    • 2
  • Wenpeng Zhang
    • 1
  • Frank B. Dazzo
    • 3
  • Norman Uphoff
    • 4
  • Yuxiang Jing
    • 1
  • Shihua Shen
    • 1
  1. 1.Institute of BotanyThe Chinese Academy of SciencesBeijingChina
  2. 2.College of BiotechnologyBeijing University of AgricultureBeijingChina
  3. 3.Department of Microbiology and Molecular GeneticsMichigan State UniversityEast LansingUSA
  4. 4.SRI International Network and Resources Center (SRI-Rice)Cornell UniversityIthacaUSA

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