Skip to main content
Log in

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

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Armanhi JSL, De Souza RSC, De Araújo LM, Okura VK, Mieczkowski P, Imperial J et al (2016) Multiplex amplicon sequencing for microbe identification in community-based culture collections. Sci Rep 6:29543

    Article  CAS  Google Scholar 

  • Beemster GT, Fiorani F, Inzé D (2003) Cell cycle: The key to plant growth control? Trends Plant Sci 8:154–158

    Article  CAS  Google Scholar 

  • Biswas JC, Ladha JK, Dazzo FB, Yanni YG, Rolfe BG (2000a) Rhizobial inoculation influences seedling vigor and yield of rice. Agron J 92:880–886

    Article  Google Scholar 

  • Biswas JC, Ladha JK, Dazzo FB (2000b) Rhizibia inoculation improves nutrient uptake and growth of lowland rice. Soil Sci Soc Am J 64:1644–1650

    Article  CAS  Google Scholar 

  • Bottini R, Cassán F, Piccoli P (2004) Gibberellin production by bacteria and its involvement in plant growth promotion and yield increase. Appl Microbiol Biotechnol 65:497–503

    Article  CAS  Google Scholar 

  • Canellas LP, Balmori DM, Médici LO, Aguiar NO, Campostrini E, Rosa RCC et al (2013) A combination of humic substances and Herbaspirillum seropedicae inoculation enhances the growth of maize (Zea mays L.). Plant Soil 366:119–132

    Article  CAS  Google Scholar 

  • Chen X, Miché L, Sachs S, Wang Q, Buschart A, Yang HY et al (2015) Rice responds to endophytic colonization which is independent of the common symbiotic signaling pathway. New Phytol 208:531–543

    Article  CAS  Google Scholar 

  • Chi F, Shen SH, Cheng HP, Jing YX, Yanni YG, Dazzo FB (2005) Ascending migration of endophytic rhizobia, from roots to leaves, inside rice plants and assessment of benefits to rice growth physiology. Appl Environ Microbiol 71:7271–7278

    Article  CAS  Google Scholar 

  • Chi F, Yang PF, Han F, Jing YX, Shen SH (2010) Proteomic analysis of rice seedlings infected by Sinorhizobium meliloti 1021. Proteomics 10:1861–1874

    Article  CAS  Google Scholar 

  • Cho H-T, Cosgrove DJ (2000) Altered expression of expansin modulates leaf growth and pedicel abscission in Arabidopsis thaliana. Proc Natl Acad Sci USA 97:9783–9788

    Article  CAS  Google Scholar 

  • Cockcroft CE, den Boer BG, Healy JS, Murray JA (2000) Cyclin D control of growth rate in plants. Nature 405:575–579

    Article  CAS  Google Scholar 

  • Cosgrove DJ (2000) Loosening of plant cell walls by expansins. Nature 407:321–326

    Article  CAS  Google Scholar 

  • Cui K, Peng S, Xing Y, Xu C, Yu S, Zhang Q (2002) Molecular dissection of seedling-vigor and associated physiological traits in rice. Theor Appl Genet 105:745–753

    Article  CAS  Google Scholar 

  • Dazzo FB, Yanni YG, Jones A, Elsadany AY (2015) CMEIAS bioimage informatics that define the landscape ecology of immature microbial biofilms developed on plant rhizoplane surfaces. AIMS Bioeng 2:469–486

    Article  CAS  Google Scholar 

  • De Souza RSC, Okura VK, Armanhi JSL, Jorrín B, Lozano N, Da Silva MJ et al (2016) Unlocking the bacterial and fungal community assemblages of sugarcane microbiome. Sci Rep 6:28774

    Article  Google Scholar 

  • 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 11:121–135

    Article  CAS  Google Scholar 

  • Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth-promoting effects of diazotrophs in the rhizosphere. Crit Rev Plant Sci 22:107–149

    Article  CAS  Google Scholar 

  • Doerner P, Joergensen J, You R, Steppuhn J, Lamb C (1996) Control of root growth and development by cyclin expression. Nature 380:520–523

    Article  CAS  Google Scholar 

  • Frankenberger WT Jr, Arshad M (1995) Phytohormones in soil: microbial production and function. Marcel Dekker Inc, New York

    Google Scholar 

  • Galibert F, Finan TM, Long SR, Puhler A, Abola P, Ampe F, Barloy-Hubler F, Barnett MJ, Becker A, Boistard P et al (2001) The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293:668–672

    Article  CAS  Google Scholar 

  • Giordano W, Hirsch AM (2004) The expression of MaEXP1, a Melilotus alba expansin gene, is upregulated during the sweetclover-Sinorhizobium meliloti interaction. Mol Plant Microbe Interact 17:613–622

    Article  CAS  Google Scholar 

  • Gonzalez N, Vanhaeren H, Inzé D (2012) Leaf size control: complex coordination of cell division and expansion. Trends Plant Sci 17:332–340

    Article  CAS  Google Scholar 

  • Gutiérrez-Zamora ML, Martínez-Romero E (2001) Natural endophytic association between Rhizobium etli and maize (Zea mays L.). J Biotechnol 91:117–126

    Article  Google Scholar 

  • He JX, Gendron JM, Sun Y, Gampala SS, Gendron N, Sun CQ et al (2005) BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses. Science 307:1634–1638

    Article  CAS  Google Scholar 

  • Hilali A, Prevost D, Broughton WJ, Antoun H (2001) Effects de I’inoculation avec des souches de Rhizobium leguminosarum biovar trifolii sur la croissance du blé dans deux sols du Marco. Can J Microbiol 47:590–593

    Article  CAS  Google Scholar 

  • Jha B, Thakur MC, Gontia I, Albrecht V, Stoffels M, Schmid M et al (2009) Isolation, partial identification and application of diazotrophic rhizobacteria from traditional Indian rice cultivars. Eur J Soil Biol 45:62–72

    Article  CAS  Google Scholar 

  • Lee J, Das A, Yamaguchi M, Hashimoto J, Tsutsumi N, Uchimiya H et al (2003) Cell cycle function of a rice B2-type cyclin interacting with a B-type cyclin-dependent kinase. Plant J 34:417–425

    Article  CAS  Google Scholar 

  • Li C, Wong WH (2001) Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc Natl Acad Sci USA 98:31–36

    Article  CAS  Google Scholar 

  • Li XJ, Guo X, Zhou YH, Shi K, Zhou J, Yu JQ et al (2016) Overexpression of a brassinosteroid biosynthetic gene Dwarf enhances photosynthetic capacity through activation of Calvin cycle enzymes in tomato. BMC Plant Biol 16:33

    Article  Google Scholar 

  • Liang Y, Cao YG, Tanaka K, Thibivilliers S, Wan JR, Choi J et al (2013) Non-legumes respond to rhizobial Nod factors by suppressing the innate immune response. Science 341:1384–1387

    Article  CAS  Google Scholar 

  • Lupwayi NZ, Clayton GW, Hanson KG, Rice WA, Biederbeck VO (2004) Endophytic rhizobia in barley, wheat and canola roots. Can J Plant Sci 84:37–45

    Article  Google 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 15:827–834

    CAS  Google Scholar 

  • Magyar Z, De Veylder L, Atanassova A, Bakó L, Inzé D, Bögre L (2005) The role of the Arabidopsis E2FB transcription factor in regulating auxin-dependent cell division. Plant Cell 17:2527–2541

    Article  CAS  Google Scholar 

  • Marshall WF, Young KD, Swaffer M, Wood E, Nurse P, Kimura A et al (2012) What determines cell size? BMC Biol 10:101

    Article  Google Scholar 

  • Mishra RP, Singh RK, Jaiswal HK, Kumar V, Maurya S (2006) Rhizobium-mediated induction of phenolics and plant growth-promotion in rice (Oryza sativa L.). Curr Microbiol 52:383–389

    Article  CAS  Google Scholar 

  • Miyata K, Hayafune M, Kobae Y, Kaku H, Nishizawa Y, Masuda Y et al (2016) Evaluation of the role of the LysM receptor-like kinase, OsNFR5/OsRLK2 for AM symbiosis in rice. Plant Cell Physiol 57:2283–2290

    Article  CAS  Google Scholar 

  • Ozturk A, Caglar O, Sahin F (2003) Yield response of wheat and barley to inoculation of plant growth-promoting rhizobacteria at various levels of nitrogen fertilization. J Plant Nutr Soil Sci 166:262–266

    Article  CAS  Google 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 28:923–937

    CAS  Google 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 81–98

    Chapter  Google Scholar 

  • Schloter M, Wiehe W, Assmus B, Steindi H, Becke H, Höflich G et al (1997) Root colonization of different plants by plant growth-promoting Rhizobium leguminosarum bv. trifolii R39 studied with monospecific polyclonal antisera. Appl Environ Microbiol 63:2038–2046

    CAS  PubMed  PubMed Central  Google Scholar 

  • Senthilkumar M, Madhaiyan M, Sundaram S, Kannaiyan S (2009) Intercellular colonization and growth promoting effects of Methylobacterium sp. with plant-growth regulators on rice (Oryza sativa L. Cv CO-43). Microbiol Res 164:92–104

    Article  CAS  Google Scholar 

  • Sessitsch A, Hardoim P, Döring J, Weilharter A, Krause A, Woyke T et al (2012) Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol Plant Microbe Interact 25:28–36

    Article  CAS  Google Scholar 

  • Singh RK, Mishra RP, Jaiswal HK, Kumar V, Pandey SP, Rao SB et al (2006) Isolation and identification of natural endophytic rhizobia from rice (Oryza sativa L.) through rDNA PCR-RFLP and sequence analysis. Curr Microbiol 52:345–349

    Article  CAS  Google Scholar 

  • Souleimanov A, Prithiviraj B, Smith DL (2002) The major Nod factor of Bradyrhizobium japonicum promotes early growth of soybean and corn. J Exp Bot 53:1929–1934

    Article  CAS  Google Scholar 

  • Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P et al (2004) Mapman: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37:914–939

    Article  CAS  Google Scholar 

  • Tkacz A, Poole P (2015) Role of root microbiota in plant productivity. J Exp Bot 66:2167–2175

    Article  CAS  Google Scholar 

  • Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98:5116–5121

    Article  CAS  Google Scholar 

  • Usadel B, Nagel A, Steinhauser D, Gibon Y, Bläsing OE, Redestig H et al (2006) PageMan: an interactive ontology tool to generate, display, and annotate overview graphs for profiling experiments. BMC Bioinform 7:535

    Article  Google Scholar 

  • Wang MJ, Yuan DJ, Gao WH, Li Y, Tan JF, Zhang XL (2013) A comparative genome analysis of PME and PMEI families reveals the evolution of pectin metabolism in plant cell walls. PLoS ONE 8:e72082

    Article  CAS  Google Scholar 

  • Wieczorek K, Golecki B, Gerdes L, Heinen P, Szakasits D, Durachko DM et al (2006) Expansins are involved in the formation of nematode-induced syncytia in roots of Arabidopsis thaliana. Plant J 48:98–112

    Article  CAS  Google Scholar 

  • Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59:225–251

    Article  CAS  Google Scholar 

  • Yanni YG, Dazzo FB (2010) Enhancement of rice production using endophytic strains of Rhizobium leguminosarum bv. trifolii in extensive field inoculation trials within the Egypt Nile delta. Plant Soil 336:129–142

    Article  CAS  Google Scholar 

  • Yanni YG, Rizk RR, Corich V, Squartini A, Ninke K et al (1997) Natural endophytic association between Rhizobium leguminosarum bv. trifolii and rice roots and assessment of its potential to promote rice growth. Plant Soil 194:99–114

    Article  CAS  Google 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 28:845–870

    CAS  Google Scholar 

  • Yanni YG, Zidan M, Dazzo F, Rizk R, Mehesen A, Abdelfattah F et al (2016a) Enhanced symbiotic performance and productivity of drought stressed common bean after inoculation with tolerant native rhizobia in extensive fields. Agric Ecosyst Environ 232:119–128

    Article  Google Scholar 

  • Yanni YG, Dazzo FB, Squartini A, Zanardo M, Zidan MI, Elsadany AEY (2016b) Assessment of the natural endophytic association between Rhizobium and wheat and its ability to increase wheat production in the Nile delta. Plant Soil 407:367–383

    Article  CAS  Google Scholar 

  • Yoshida S, Forno DA, Cock J, Gomez KA (1972) Laboratory manual for physiological studies of rice. Int Rice Res Inst, Manila

    Google Scholar 

Download references

Acknowledgements

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

Funding

This work was supported by the State Key Basic Research and Development Plan of China (2010CB126503).

Author information

Authors and Affiliations

Authors

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.

Corresponding authors

Correspondence to Yuxiang Jing or Shihua Shen.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest to declare.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Figure 1 (TIF 567 KB)

Supplementary Figure 2 (TIF 15313 KB)

Supplementary Figure 3 (TIF 1684 KB)

Supplementary Figure 4 (TIF 2909 KB)

Supplementary Figure 5 (TIF 258 KB)

11103_2018_756_MOESM6_ESM.tif

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)

Supplementary Figure 7 (TIF 483 KB)

Supplementary Figure 8 (TIF 485 KB)

Supplementary Table 1 (XLSX 11 KB)

Supplementary Table 2 (XLSX 254 KB)

Supplementary Table 3 (XLS 340 KB)

Supplementary Table 4 (XLSX 17 KB)

Supplementary Table 5 (XLSX 74 KB)

Supplementary Table 6 (XLSX 78 KB)

Supplementary Table 7 (XLSX 14 KB)

Supplementary Table 8 (XLSX 12 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wu, Q., Peng, X., Yang, M. et al. Rhizobia promote the growth of rice shoots by targeting cell signaling, division and expansion. Plant Mol Biol 97, 507–523 (2018). https://doi.org/10.1007/s11103-018-0756-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-018-0756-3

Keywords

Navigation