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Identification of a small set of genes commonly regulated in rice roots in response to beneficial rhizobacteria

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Abstract

Rhizosphere bacteria, whether phytopathogenic or phytobeneficial, are thought to be perceived by the plant as a threat. Plant Growth-Promoting Rhizobacteria (PGPR), such as many strains of the Azospirillum genus known as the main phytostimulator of cereals, cooperate with host plants and favorably affect their growth and health. An earlier study of rice root transcriptome, undertaken with two rice cultivars and two Azospirillum strains, revealed a strain-dependent response during the rice-Azospirillum association and showed that only a few genes, including some implicated in plant defense, were commonly regulated in all tested conditions. Here, a set of genes was selected from previous studies and their expression was monitored by qRT-PCR in rice roots inoculated with ten PGPR strains isolated from various plants and belonging to various genera (Azospirillum, Herbaspirillum, Paraburkholderia). A common expression pattern was highlighted for four genes that are proposed to be markers of the rice-PGPR interaction: two genes involved in diterpenoid phytoalexin biosynthesis (OsDXS3 and OsDTC2) and one coding for an uncharacterized protein (Os02g0582900) were significantly induced by PGPR whereas one defense-related gene encoding a pathogenesis-related protein (PR1b, Os01g0382000) was significantly repressed. Interestingly, exposure to a rice bacterial pathogen also triggered the expression of OsDXS3 while the expression of Os02g0582900 and PR1b was down-regulated, suggesting that these genes might play a key role in rice-bacteria interactions. Integration of these results with previous data led us to propose that the jasmonic acid signaling pathway might be triggered in rice roots upon inoculation with PGPR.

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Abbreviations

IAA:

Indole acetic acid

ISR:

Induced systemic resistance

JA:

Jasmonic acid

MAMP:

Microbe-associated molecular patterns

PGPR:

Plant Growth-Promoting Rhizobacteria

References

  • Ait Barka E, Gognies S, Nowak J, Audran J-C, Belarbi A (2002) Inhibitory effect of endophyte bacteria on Botrytis cinerea and its influence to promote the grapevine growth. Biol Control 24:135–142

    Article  Google Scholar 

  • Akatsuka T, Sekido H, Takeuchi S, Kono Y, Kodama O (1985) Novel phytoalexins (oryzalexins a, b and c) isolated from rice blast leaves infected with Pyricularia oryzae. Agric Biol Chem 49:1689–1701

    CAS  Google Scholar 

  • Baldani VLD, de Alvarez MAB, Baldani JI, Döbereiner J (1986a) Establishment of inoculated Azospirillum spp. in the rhizosphere and in roots of field grown wheat and sorghum. Plant Soil 90:37–40

    Article  Google Scholar 

  • Baldani JI, Baldani VLD, Seldin L, Dobereiner J (1986b) Characterization of Herbaspirillurn seropedicae gen. nov. sp. nov. a root-associated nitrogen-fixing bacterium. Int J Syst Bacteriol 36:86–93

    Article  CAS  Google Scholar 

  • Blanvillain-Baufumé S, Reschke M, Solé M, Auguy F, Doucoure H, Szurek B, Meynard D, Portefaix M, Cunnac S, Guiderdoni E, Boch J, Koebnik R (2017) Targeted promoter editing for rice resistance to Xanthomonas oryzae pv. oryzae reveals differential activities for SWEET14-inducing TAL effectors. Plant Biotechnol J 15:306–317

    Article  PubMed  CAS  Google Scholar 

  • Breitler J, Campa C, Georget F, Bertrand B, Etienne H (2016) A single-step method for RNA isolation from tropical crops in the field. Sci Rep 6:38368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buscaill P, Rivas S (2014) Transcriptional control of plant defence responses. Curr Opin Plant Biol 20:35–46

    Article  CAS  PubMed  Google Scholar 

  • Cartieaux F, Thibaud MC, Zimmerli L, Lessard P, Sarrobert C, David P, Gerbaud A, Robaglia C, Somerville S, Nussaume L (2003) Transcriptome analysis of Arabidopsis colonized by a plant-growth promoting rhizobacterium reveals a general effect on disease resistance. Plant J 36:177–188

    Article  CAS  PubMed  Google Scholar 

  • Chamam A, Sanguin H, Bellvert F, Meiffren G, Comte G, Wisniewski-Dyé F, Bertrand C, Prigent-Combaret C (2013) Plant secondary metabolite profiling evidences strain-dependent effect in the Azospirillum-Oryza sativa association. Phytochemistry 87:65–77

    Article  CAS  PubMed  Google Scholar 

  • Chen C, Ané JM, Zhu H (2008) OsIPD3, an ortholog of the Medicago truncatula DMI3 interacting protein IPD3, is required for mycorrhizal symbiosis in rice. New Phytol 180:311–315

    Article  CAS  PubMed  Google Scholar 

  • Chen X, Miché L, Sachs S, Wang Q, Buschart A, Yang H, Vera Cruz CM, Hurek T, Reinhold-Hurek B (2015) Rice responds to endophytic colonization which is independent of the common symbiotic signaling pathway. New Phytol 208:531–543

    Article  CAS  PubMed  Google Scholar 

  • Compant S, Reiter B, Sessitsch A, Nowak J, Clément C, Barka EA (2005) Endophytic colonization of Vitis vinifera L. by plant growth-promoting bacterium Burkholderia sp. strain PsJN. Appl Environ Microbiol 71:1685–1693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Devescovi G, Bigirimana J, Degrassi G, Cabrio L, LiPuma JJ, Kim J, Hwang I, Venturi V (2007) Involvement of a quorum-sensing-regulated lipase secreted by a clinical isolate of Burkholderia glumae in severe disease symptoms in rice. Appl Environ Microbiol 73:4950–4958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Drogue B, Sanguin H, Chamam A, Mozar M, Llauro C, Panaud O, Prigent-Combaret C, Picault N, Wisniewski-Dyé F (2014) Plant root transcriptome profiling reveals a strain-dependent response during Azospirillum-rice cooperation. Front Plant Sci 5:1–14

    Article  Google Scholar 

  • Egamberdieva D, Wirth SJ, Alqarawi AA, Abd-Allah EF, Hashem A (2017) Phytohormones and beneficial microbes: essential components for plants to balance stress and fitness. Front Microbiol 8:2104

    Article  PubMed  PubMed Central  Google Scholar 

  • Elbeltagy A, Nishioka K, Sato T, Suzuki H, Ye B, Hamada T, Isawa T, Mitsui H, Minamisawa K (2001) Endophytic colonization and in planta nitrogen fixation by a Herbaspirillum sp. Isolated from wild rice species. Appl Environ Microbiol 67:5285–5293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gutjahr C, Banba M, Croset V, An K, Miyao A, An G, Hirochika H, Imaizumi-Anraku H, Paszkowski U (2008) Arbuscular mycorrhiza-specific signaling in rice transcends the common symbiosis signaling pathway. Plant Cell 20:2989–3005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ito Y, Kurata N (2006) Identification and characterization of cytokinin-signalling gene families in rice. Gene 382:57–65

    Article  CAS  PubMed  Google Scholar 

  • Kang Y, Kim J, Kim S, Kim H, Lim JY, Kim M, Kwak J, Moon JS, Hwang I (2008) Proteomic analysis of the proteins regulated by HrpB from the plant pathogenic bacterium Burkholderia glumae. Proteomics 8:106–121

    Article  CAS  PubMed  Google Scholar 

  • King E, Wallner A, Rimbault I, Barrachina A, Klonowska A, Moulin L, Czernic P (2019) Monitoring of rice transcriptional responses to contrasted colonizing patterns of phytobeneficial Burkholderia s.l. reveals a temporal shift in JA systemic response. Front Plant Sci 10:1141

    Article  PubMed  PubMed Central  Google Scholar 

  • Kost T, Stopnisek N, Agnoli K, Eberl L, Weisskopf L (2013) Oxalotrophy, a widespread trait of plant-associated Burkholderia species, is involved in successful root colonization of lupin and maize by Burkholderia phytofirmans. Front Microbiol 4:421

    Google Scholar 

  • Kusajima M, Shima S, Fujita M, Minamisawa K, Che FS, Yamakawa H, Nakashita H (2020) Involvement of ethylene signaling in Azospirillum sp. B510-unduced disease resistance in rice. Biosci Biotechnol Biochem 82:1522–1526

    Article  CAS  Google Scholar 

  • Laborda P, Chen X, Wu GC, Wang SY, Lu XF, Ling J, Li KH, Liu FQ (2020) Lysobacter gummosus OH17 induces systemic resistance in Oryza sativa ‘Nipponbare’. Plant Pathol 69:838–848

    Article  CAS  Google Scholar 

  • Léon-Kloosterziel KM, Verhagen BWM, Keurentjes JJB, Vanpelt JA, Rep M, Vanloon LC, Pieterse CMJ (2005) Colonization of the Arabidopsis rhizosphere by fluorescent Pseudomonas spp. activates a root-specific, ethylene-responsive PR-5 gene in the vascular bundle. Plant Mol Biol 57:731–748

    Article  PubMed  CAS  Google Scholar 

  • Liang X, Chen X, Li C, Fan J, Guo Z (2017) Metabolic and transcriptional alternations for defense by interfering OsWRKY62 and OsWRKY76 transcriptions in rice. Sci Rep 7:1–15

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • MacDonald MJ, D’Cunha GB (2007) A modern view of phenylalanine ammonia lyase. Biochem Cell Biol 85:759

    Article  CAS  Google Scholar 

  • Marcel S, Sawers R, Oakeley E, Angliker H, Paszkowski U (2010) Tissue-adapted invasion strategies of the rice blast fungus Magnaporthe oryzae. Plant Cell 22:3177–3187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marone D, Russo MA, Laidò G, De Leonardis AM, Mastrangelo AM (2013) Plant nucleotide binding site-leucine-rich repeat (NBS-LRR) genes: active guardians in host defense responses. Int J Mol Sci 14:7302–7326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McGee JD, Hamer JE, Hodges TK (2001) Characterization of a PR-10 pathogenesis-related gene family induced in rice during infection with Magnaporthe grisea. Mol Plant-Microbe Interact 14:877–886

    Article  CAS  PubMed  Google Scholar 

  • Mehnaz S, Lazarovits G (2006) Inoculation effects of Pseudomonas putida, Gluconacetobacter azotocaptans, and Azospirillum lipoferum on corn plant growth under greenhouse conditions. Microb Ecol 51:326–335

    Article  PubMed  Google Scholar 

  • Mitsuhara I, Iwai T, Seo S, Yanagawa Y, Kawahigasi H, Hirose S, Ohkawa Y, Ohashi Y (2008) Characteristic expression of twelve rice PR1 family genes in response to pathogen infection, wounding, and defense-related signal compounds. Mol Genet Genom 279:415–427

    Article  CAS  Google Scholar 

  • Narsai R, Ivanova A, Ng S, Whelan J (2010) Defining reference genes in Oryza sativa using organ, development, biotic and abiotic transcriptome datasets. BMC Plant Biol 10:56

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nelson LM, Knowles R (1978) Effect of oxygen and nitrate on nitrogen fixation and denitrification by Azospirillum brasilensegrown in continuous culture. Can J Microbiol 24:1395–1403

    Article  CAS  PubMed  Google Scholar 

  • Okada A, Shimizu T, Okada K, Kuzuyama T, Koga J, Shibuya N, Nojiri H, Yamane H (2007) Elicitor induced activation of the methylerythritol phosphate pathway toward phytoalexins biosynthesis in rice. Plant Mol Biol 65:177–187

    Article  CAS  PubMed  Google Scholar 

  • Olivares FL, James EK, Baldani JI, Döbereiner J (1997) Infection of mottled stripe disease-susceptible and resistant sugar cane varieties by the endophytic diazotroph Herbaspirillum. New Phytol 135:723–727

    Article  Google Scholar 

  • Ona O, Van Impe J, Prinsen E, Vanderleyden J (2005) Growth and indole-3-acetic acid biosynthesis of Azospirillum brasilense Sp245 is environmentally controlled. FEMS Microbiol Lett 246:125–132

    Article  CAS  PubMed  Google Scholar 

  • Pankievicz VCS, Camilios-Neto D, Bonato P, Balsanelli E, Tadra-Sfeir MZ, Faoro H, Chubatsu LS, Donatti L, Wajnberg G, Passetti F, Monteiro RA, Pedrosa FO, Souza EM (2016) RNA-seq transcriptional profiling of Herbaspirillum seropedicae colonizing wheat (Triticum aestivum) roots. Plant Mol Biol 90:589–603

    Article  CAS  PubMed  Google Scholar 

  • Paxton JD (1981) Phytoalexins—a working redefinition. J Phytopathol 101:106–109

    Article  Google Scholar 

  • Pedrosa FO, Monteiro RA, Wassem R, Cruz LM, Ayub RA, Colauto NB, Fernandez MA et al (2011) Genome of Herbaspirillum seropedicae strain SmR1, a specialized diazotrophic endophyte of tropical grasses. PLoS Genet 7:e1002064

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng Y, Bartley LE, Chen X, Dardick C, Chern M, Ruan R (2008) OSWRKY62 is a negative regulator of basal and XA21 -mediated defense against Xanthomonas oryzae pv. oryzae in rice. Mol Plant 1:446–458

    Article  CAS  PubMed  Google Scholar 

  • Pereg L, de-Bashan LE, Bashan Y (2016) Assessment of affinity and specificity of Azospirillum for plants. Plant Soil 399:389–414

    Article  CAS  Google Scholar 

  • Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Van Wees SCM, Bakker PAHM (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375

    Article  CAS  PubMed  Google Scholar 

  • Rekha K, Kumar RM, Ilango K, Rex A, Usha B (2018) Transcriptome profiling of rice roots in early response to Bacillus subtilis (RR4) colonization. Botany 96:749–765

    Article  CAS  Google Scholar 

  • Rondeau M, Esmaeel Q, Crouzet J, Blin P, Gosselin I, Sarazin C, Pernes M, Beaugrand J, Wisniewski-Dyé F, Vial L, Faure D, Clément C, Ait Barka E, Jacquard C, Sanchez L (2019) Biofilm constructing variants of Paraburkholderia phytofirmans PsJN outcompete the wild-type form in free-living and static conditions but not in planta. Appl Environ Microbiol 85:e02670-18

    Article  PubMed  PubMed Central  Google Scholar 

  • Schloter M, Hartmann A (1998) Endophytic and surface colonization of wheat roots (Triticum aestivum) by different Azospirillum brasilense strains studied with strain-specific monoclonal antibodies. Symbiosis 25:159–179

    Google Scholar 

  • Sekido H, Akatsuka T (1987) Mode of action of oryzalexin D against Pyricularia oryzae. Agric Biol Chem 51:1967–1971

    CAS  Google Scholar 

  • Sessitsch A, Coenye T, Sturz AV, Vandamme P, Barka EA, Salles JF, Van Elsas JD, Faure D, Reiter B, Glick BR, Wang-Pruski G, Nowak J (2005) Burkholderia phytofirmans sp. nov., a novel plant-associated bacterium with plant-beneficial properties. Int J Syst Evol Microbiol 55:1187–1192

    Article  CAS  PubMed  Google Scholar 

  • Soto MJ, Domínguez-Ferreras A, Pérez-Mendoza D, Sanjuán J, Olivares J (2009) Mutualism versus pathogenesis: the give-and-take in plant-bacteria interactions. Cell Microbiol 11:381–388

    Article  CAS  PubMed  Google Scholar 

  • Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31:425–448

    Article  CAS  PubMed  Google Scholar 

  • Spaepen S, Vanderleyden J, Okon Y (2009) Plant growth-promoting actions of rhizobacteria. In: Van Loon LC (ed) Plant innate immunity, vol 51. Elsevier, Amsterdam, pp 283–320

    Google Scholar 

  • Spaepen S, Bossuyt S, Engelen K, Marchal K, Vanderleyden J (2014) Phenotypical and molecular responses of Arabidopsis thaliana roots as a result of inoculation with the auxin-producing bacterium Azospirillum brasilense. New Phytol 201:850–861

    Article  CAS  PubMed  Google Scholar 

  • Stringlis IA, Proietti S, Hickman R, Van Verk M, Zamioudis C, Pieterse CMJ (2018) Root transcriptional dynamics induced by beneficial rhizobacteria and microbial immune elicitors reveal signatures of adaptation to mutualists. Plant J 93:166–180

    Article  CAS  PubMed  Google Scholar 

  • Tarrand JJ, Krieg NR, Döbereiner J (1978) A taxonomic study of the Spirillum lipoferum group, with descriptions of a new genus, Azospirillum gen. nov. and two species, Azospirillum lipoferum (Beijerinck) comb. nov. and Azospirillum brasilense sp. nov. Can J Microbiol 24:967–980

    Article  CAS  PubMed  Google Scholar 

  • Thomas-Bauzon D, Weinhard P, Villecourt P, Balandreau J (1982) The spermosphere model. I. Its use in growing, counting, and isolating N 2 -fixing bacteria from the rhizosphere of rice. Can J Microbiol 28:922–928

    Article  Google Scholar 

  • Toyomasu T, Kagahara T, Okada K, Koga J, Hasegawa M, Mitsuhashi W, Sassa T, Yamane H (2008) Diterpene phytoalexins are biosynthesized in and exuded from the roots of rice seedlings. Biosci Biotechnol Biochem 72:562–567

    Article  CAS  PubMed  Google Scholar 

  • Trân Vân V, Ngôkê S, Berge O, Hebbar P, Heulin T, Faure D, Bally R (1997) Isolation of Azospirillum lipoferum from the rhizosphere of rice by a new, simple method. Can J Microbiol 43:486–490

    Article  Google Scholar 

  • Vacheron J, Moënne-Loccoz Y, Dubost A, Gonçalves-Martins M, Muller D, Prigent-Combaret C (2016) Fluorescent Pseudomonas strains with only few plant-beneficial properties are favored in the maize rhizosphere. Front Plant Sci 7:1–13

    Article  Google Scholar 

  • Valette M, Rey M, Gerin F, Comte G, Wisniewski-Dyé F (2020) A common metabolomic signature is observed upon inoculation of rice roots with various rhizobacteria. J Integr Plant Biol 62:228–246

    Article  CAS  PubMed  Google Scholar 

  • van de Mortel JE, de Vos RCH, Dekkers E, Pineda A, Guillod L, Bouwmeester K, van Loon JJA, Dicke M, Raaijmakers JM (2012) Metabolic and transcriptomic changes induced in Arabidopsis by the rhizobacterium Pseudomonas fluorescens SS101. Plant Physiol 160:2173–2188

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Verhagen BWM, Glazebrook J, Zhu T, Chang H-S, van Loon LC, Pieterse CMJ (2004) The transcriptome of rhizobacteria-induced systemic resistance in Arabidopsis. Mol Plant-Microbe Interact 17:895–908

    Article  CAS  PubMed  Google Scholar 

  • Vial L, Lavire C, Mavingui P, Blaha D, Haurat J, Moënne-Loccoz Y, Bally R, Wisniewski-Dyé F (2006) Phase variation and genomic architecture changes in Azospirillum. J Bacteriol 188:5364–5373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann Bot 111:1021–1058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wisniewski-Dyé F, Herrera AM, Drogue B, Acosta-Cruz E, Prigent-Combaret C, Lozano L, González V, Barbe V, Rouy Z, Mavingui P, Borland S (2012) Genome sequence of Azospirillum brasilense CBG497 and comparative analyses of Azospirillum core and accessory genomes provide insight into niche adaptation. Genes 3:576–602

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yamane H (2013) Biosynthesis of phytoalexins and regulatory mechanisms of it in rice. Biosci Biotechnol Biochem 77:1141–1148

    Article  CAS  PubMed  Google Scholar 

  • Yang DL, Yang Y, He Z (2013) Roles of plant hormones and their interplay in rice immunity. Mol Plant 6:675–685

    Article  CAS  PubMed  Google Scholar 

  • Yang J, Duan GH, Li CQ, Liu L, Han GY, Zhang YL, Wang CM (2020) The crosstalks between jasmonic acid and other plant hormone signaling highlight the Involvement of jasmonic acid as a core component in plant response to biotic and abiotic stresses. Front Plant Sci 10:1349

    Article  Google Scholar 

  • Yano K, Satoko Y, Muller J, Singh S, Banba M, Vickers K, Markmann K, White C, Schuller B, Sato S, Asamizu E, Tabata S, Murooka Y, Perry J, Wang TL, Kawaguchi M, Imaizumi-Anraku H, Hayashi M, Parniske M (2008) CYCLOPS, a mediator of symbiotic intracellular accommodation. Proc Natl Acad Sci 105:20540–20545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zaplin ES, Liu Q, Li Z, Butardo VM, Blanchard CL, Rahman S (2013) Production of high oleic rice grains by suppressing the expression of the OsFAD2-1 gene. Funct Plant Biol 40:996–1004

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Bao Y, Shan D, Wang Z, Song X, Wang Z, Wang J, He L, Wu L, Zhang Z, Niu D, Jin H, Zhao H (2018) Magnaporthe oryzae induces the expression of a microRNA to suppress the immune response in rice. Plant Physiol 177:352–368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We wish to thank Emmanuel Guiderdoni (AGAP laboratory, CIRAD Montpellier) for gift of Nipponbare seeds and Lisa Sanchez for providing the GFP-tagged P. phytofirmans PsJN strain. We are grateful to Jonathan Gervaix (AME platform of UMR CNRS-5557) for his invaluable help in acetylene reduction assay, to Danis Abrouk (iBio platform of UMR CNRS-5557) and Samuel Barreto for their great help in statistical analyses. The platform “Serre” of FR41 (University Lyon 1) was used to carry out this work. MV receives a fellowship from «Ministère de l’enseignement supérieur et de la recherche».

Funding

This study was supported by reccurent funding from CNRS and University Lyon 1. MV receives a fellowship from « Ministère de l’enseignement supérieur et de la recherche » .

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M.V. conducted experiments and wrote the paper; M.R., J.D. and F.G. conducted experiments; F.W.D. designed experiments and wrote the paper; all authors discussed the data, and read and approved the contents of this manuscript.

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Correspondence to Florence Wisniewski-Dyé.

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Valette, M., Rey, M., Doré, J. et al. Identification of a small set of genes commonly regulated in rice roots in response to beneficial rhizobacteria. Physiol Mol Biol Plants 26, 2537–2551 (2020). https://doi.org/10.1007/s12298-020-00911-1

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