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Rice CaM-binding transcription factor (OsCBT) mediates defense signaling via transcriptional reprogramming

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Abstract

The mutant allele of rice calmodulin-binding transcription activator OsCBT, oscbt-1, exhibits broad-spectrum resistance against rice pathogens. Previously, we reported that the strong resistance of the oscbt-1 mutant to pathogens was conferred by a constitutive upregulation of defense-related genes even under pathogen-free conditions. We also found strong induction of the hypersensitive response as a reaction to pathogen invasion. The results suggest that OsCBT acts as a negative regulator of basal resistance to pathogen attack. To identify the transcriptional network regulated by OsCBT, we compared global gene expression profiles between wild-type (WT) and oscbt-1 rice plants grown under pathogen-free conditions. The results of a 3′ tiling microarray revealed that in oscbt-1 plants, 81 genes are upregulated and 200 genes are downregulated when compared with the WT. A gene ontology analysis showed that differentially regulated genes in oscbt-1 were very closely associated with “death” GO term in a biological process category, and “catalytic activity” and “binding” GO terms in a molecular function category. A MapMan analysis indicated that the functions of these genes were associated with plant responses to biotic stress. Moreover, the results from quantitative real-time PCR in the oscbt-1 mutant showed a significant effect on the gene expression patterns of the fungal pathogen response. Our results suggested that the OsCBT regulates a rice defense response by modulating the expressions of various defense-related genes.

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References

  • Berridge MJ, Lipp P, Bootman MD (2000) The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1(1):11–21

    CAS  PubMed  Google Scholar 

  • Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379–406

    CAS  PubMed  Google Scholar 

  • Bouché N, Scharlat A, Snedden W, Bouchez D, Fromm H (2002) A novel family of calmodulin-binding transcription activators in multicellular organisms. J Biol Chem. 277(24):21851–21861

    PubMed  Google Scholar 

  • Cheng X, Wu Y, Guo J, Du B, Chen R, Zhu L, He G (2013) A rice lectin receptor-like kinase that is involved in innate immune responses also contributes to seed germination. Plant J 76(4):687–698

    CAS  PubMed  PubMed Central  Google Scholar 

  • Choi MS, Kim MC, Yoo JH, Moon BC, Koo SC, Park BO, Lee JH, Koo YD, Han HJ, Lee SY, Chung WS, Lim CO, Cho MJ (2005) Isolation of a calmodulin-binding transcription factor from rice (Oryza sativa L.). J Biol Chem 280(49):40820–40831

    CAS  PubMed  Google Scholar 

  • Doherty CJ, Van Buskirk HA, Myers SJ, Thomashow MF (2009) Roles for Arabidopsis CAMTA transcription factors in cold-regulated gene expression and freezing tolerance. Plant Cell 21(3):972–984

    CAS  PubMed  PubMed Central  Google Scholar 

  • Du L, Ali GS, Simons KA, Hou J, Yang T, Reddy ASN, Poovaiah BW (2009) Ca(2+)/calmodulin regulates salicylic-acid-mediated plant immunity. Nature 457(7233):1154–1158

    CAS  PubMed  Google Scholar 

  • Elmore JM, Lin ZJ, Coaker G (2011) Plant NB-LRR signaling: upstreams and downstreams. Curr Opin Plant Biol 14(4):365–371

    CAS  PubMed  PubMed Central  Google Scholar 

  • Finkler A, Padan RA, Fromm H (2007) CAMTAs: calmodulin-binding transcription activators from plants to human. FEBS Lett 581(21):3893–3898

    CAS  PubMed  Google Scholar 

  • Galon Y, Nave R, Boyce JM, Nachmias D, Knight MR, Fromm H (2008) Calmodulin-binding transcription activator (CAMTA) 3 mediates biotic defense responses in Arabidopsis. FEBS Lett 582(6):943–948

    CAS  PubMed  Google Scholar 

  • Galon Y, Aloni R, Nachmias D, Snir O, Feldmesser E, Scrase-Field S, Boyce JM, Bouche N, Knight MR, Fromm H (2010a) Calmodulin-binding transcription activator 1 mediates auxin signaling and responds to stresses in Arabidopsis. Planta 232(1):165–178

    CAS  PubMed  Google Scholar 

  • Galon Y, Finkler A, Fromm H (2010b) Calcium-regulated transcription in plants. Mol Plant 3(4):653–669

    CAS  PubMed  Google Scholar 

  • Ho CL, Wu Y, Shen HB, Provart NJ, Geisler M (2012) A predicted protein interactome for rice. Rice (NY) 5(1):15

    Google Scholar 

  • Hong WJ, Chandran AKN, Jeon JS, Jung KH (2017) Construction and application of functional gene modules to regulatory pathways in rice. J Plant Biol 60(4):358–379

    CAS  Google Scholar 

  • Horie T, Costa A, Kim TH, Han MJ, Horie R, Leung HY, Miyao A, Hirochika H, An G, Schroeder JI (2007) Rice OsHKT2;1 transporter mediates large Na+ influx component into K+-starved roots for growth. EMBO J 26(12):3003–3014

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hou CX, Zhan YH, Jiang DA, Weng XY (2014) Functional characterization of a new pathogen induced xylanase inhibitor (RIXI) from rice. Eur J Plant Pathol 138(2):405–414

    CAS  Google Scholar 

  • Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP (2003) Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 31(4):e15

    PubMed  PubMed Central  Google Scholar 

  • Ishimaru Y, Masuda H, Suzuki M, Bashir K, Takahashi M, Nakanishi H, Mori S, Nishizawa NK (2007) Overexpression of the OsZIP4 zinc transporter confers disarrangement of zinc distribution in rice plants. J Exp Bot 58(11):2909–2915

    CAS  PubMed  Google Scholar 

  • Ishimaru Y, Masuda H, Bashir K, Inoue H, Tsukamoto T, Takahashi M, Nakanishi H, Aoki N, Hirose T, Ohsugi R, Nishizawa NK (2010) Rice metal-nicotianamine transporter, OsYSL2, is required for the long-distance transport of iron and manganese. Plant J 62(3):379–390

    CAS  PubMed  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444(7117):323–329

    CAS  PubMed  Google Scholar 

  • Joshi RK, Nayak S (2011) Functional characterization and signal transduction ability of nucleotide-binding site-leucine-rich repeat resistance genes in plants. Genet Mol Res 10(4):2637–2652

    CAS  PubMed  Google Scholar 

  • Jung KH, An G (2012) Application of MapMan and RiceNet drives systematic analyses of the early heat stress transcriptome in rice seedlings. J Plant Biol 55:436–449

    CAS  Google Scholar 

  • Kawakatsu T, Yamamoto MP, Touno SM, Yasuda H, Takaiwa F (2009) Compensation and interaction between RISBZ1 and RPBF during grain filling in rice. Plant J 59(6):908–920

    CAS  PubMed  Google Scholar 

  • Kim MC, Chung WS, Yun D-J, Cho MJ (2009) Calcium and calmodulin-mediated regulation of gene expression in plants. Mol Plant 2(1):13–21

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim Y, Park S, Gilmour SJ, Thomashow MF (2013) Roles of CAMTA transcription factors and salicylic acid in configuring the low-temperature transcriptome and freezing tolerance of Arabidopsis. Plant J 75(3):364–376

    CAS  PubMed  Google Scholar 

  • Koo SC, Choi MS, Chun HJ, Shin DB, Park BS, Kim YH, Park HM, Seo HS, Song JT, Kang KY, Yun DJ, Chung WS, Cho MJ, Kim MC (2009) The calmodulin-binding transcription factor OsCBT suppresses defense responses to pathogens in rice. Mol Cells 27(5):563–570

    CAS  PubMed  Google Scholar 

  • Kudla J, Batistic O, Hashimoto K (2010) Calcium signals: the lead currency of plant information processing. Plant Cell 22(3):541–563

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li W, Shao M, Yang J, Zhong W, Okada K, Yamane H, Qian G, Liu F (2013) Oscyp71Z2 involves diterpenoid phytoalexin biosynthesis that contributes to bacterial blight resistance in rice. Plant Sci 207:98–107

    CAS  PubMed  Google Scholar 

  • Mi H, Muruganujan A, Ebert D, Huang X, Thomas PD (2019) PANTHER version 14: more genomes, a new PANTHER GO-slim and improvements in enrichment analysis tools. Nucleic Acids Res 47(D1):D419–D426

    CAS  PubMed  Google Scholar 

  • Nakashima K, Tran LS, Van Nguyen D, Fujita M, Maruyama K, Todaka D, Ito Y, Hayashi N, Shinozaki K, Yamaguchi-Shinozaki K (2007) Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J 51(4):617–630

    CAS  PubMed  Google Scholar 

  • Nimchuk Z, Eulgem T, Holt BF 3rd, Dangl JL (2003) Recognition and response in the plant immune system. Annu Rev Genet 37(1):579–609

    CAS  PubMed  Google Scholar 

  • Pandey N, Ranjan A, Pant P, Tripathi RK, Ateek F, Pandey HP, Patre UV, Sawant SV (2013) CAMTA 1 regulates drought responses in Arabidopsis thaliana. BMC Genomics 14:216

    CAS  PubMed  PubMed Central  Google Scholar 

  • Reddy AS (2001) Calcium: silver bullet in signaling. Plant Sci 160(3):381–404

    CAS  PubMed  Google Scholar 

  • Reddy AS, Ali GS, Celesnik H, Day IS (2011) Coping with stresses: roles of calcium- and calcium/calmodulin-regulated gene expression. Plant Cell 23(6):2010–2032

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rotter A, Usadel B, Baebler S, Stitt M, Gruden K (2007) Adaptation of the MapMan ontology to biotic stress responses: application in solanaceous species. Plant Methods 3:10

    PubMed  PubMed Central  Google Scholar 

  • Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15(5):247–258

    CAS  PubMed  Google Scholar 

  • Sanders D, Pelloux J, Brownlee C, Harper JF (2002) Calcium at the crossroads of signaling. Plant Cell 14(Suppl):S401–S417

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schwessinger B, Ronald PC (2012) Plant innate immunity: perception of conserved microbial signatures. Annu Rev Plant Biol 63:451–482

    CAS  PubMed  Google Scholar 

  • Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13(11):2498–2504

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tian T, Liu Y, Yan H, You Q, Yi X, Du Z, Xu W, Su Z (2017) agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Res 45(W1):W122–W129

    CAS  PubMed  PubMed Central  Google Scholar 

  • Workman C, Jensen LJ, Jarmer H, Berka R, Gautier L, Saxild HH, Nielsen C, Brunak S, Knudsen S (2002) A new non-linear normalization method to reduce variability in DNA microarray experiments. Genome Biol. 3(9):research0048.1–research0048.16

    Google Scholar 

  • Yamamoto E, Yonemaru J, Yamamoto T, Yano M (2012) OGRO: The overview of functionally characterized genes in rice online database. Rice (NY) 5(1):26

    Google Scholar 

  • Yang T, Poovaiah BW (2002) A calmodulin-binding/CGCG box DNA-binding protein family involved in multiple signalling pathways in plants. J Biol Chem 277(47):45049–45058

    CAS  PubMed  Google Scholar 

  • Yuan B, Zhai C, Wang W, Zeng X, Xu X, Hu H, Lin F, Wang L, Pan Q (2011) The Pik-p resistance to Magnaporthe oryzae in rice is mediated by a pair of closely linked CC-NBS-LRR genes. Theor Appl Genet 122(5):1017–1028

    PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by Next Generation BioGreen21 Program (SSAC, Grant Number: PJ01318202), Rural Development Administration Republic of Korea and Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (2013R1A1A2062074 to M.C.K and 2016R1D1A1B01011803 to D.B.).

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Correspondence to Ki-Hong Jung or Min Chul Kim.

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Chung, JS., Koo, S.C., Jin, B.J. et al. Rice CaM-binding transcription factor (OsCBT) mediates defense signaling via transcriptional reprogramming. Plant Biotechnol Rep 14, 309–321 (2020). https://doi.org/10.1007/s11816-020-00603-y

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