SpringerLink
Log in

Oschib1 gene encoding a GH18 chitinase confers resistance against sheath blight disease of rice caused by Rhizoctonia solani AG1-IA

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Sheath blight disease of rice caused by Rhizoctonia solani AG1-IA, is a major fungal disease responsible for huge loss to grain yield and quality. The major limitation of achieving persistent and reliable resistance against R. solani is the governance of disease resistance trait by many genes. Therefore, functional characterization of new genes involved in sheath blight resistance is necessary to understand the mechanism of resistance as well as evolving effective strategies to manage the disease through host-plant resistance. In this study, we performed RNA sequencing of six diverse rice genotypes (TN1, BPT5204, Vandana, N22, Tetep, and Pankaj) from sheath and leaf tissue of control and fungal infected samples. The approach for identification of candidate resistant genes led to identification of 352 differentially expressed genes commonly present in all the six genotypes. 23 genes were analyzed for RT-qPCR expression which helped identification of Oschib1 showing differences in expression level in a time-course manner between susceptible and resistant genotypes. The Oschib1 encoding classIII chitinase was cloned from resistant variety Tetep and over-expressed in susceptible variety Taipei 309. The over-expression lines showed resistance against R. solani, as analyzed by detached leaf and whole plant assays. Interestingly, the resistance response was correlated with the level of transgene expression suggesting that the enzyme functions in a dose dependent manner. We report here the classIIIb chitinase from chromosome10 of rice showing anti-R. solani activity to combat the dreaded sheath blight disease.

Key message

The comprehensive transcriptome analysis of diverse rice cultivars led to identification of Oschib1 gene encoding a novel chitinase that contributes sheath blight disease resistance in a dose dependent manner.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Canada)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability

The data generated in this study will be made available on request.

References

  • AICRIP (2021) - Progress Report, Crop Protection (Entomology, Plant Pathology), All India Coordinated Rice Improvement Project, ICAR-Indian Institute of Rice Research, Rajendranagar, Hyderabad– 500 030, Telangana State, India. Vol.2, pp 1-317

  • Bandopadhyay R, Haque I, Singh D, Mukhopadhyay K (2010) Levels and stability of expression of transgenes. Transgenic crop plants: principles and development. Pp.145– 86

  • BhaskarRao T, Chopperla R, Prathi NB, Balakrishnan M, Prakasam V, Laha GS, Balachandran SM, Mangrauthia SK (2020) A comprehensive gene expression profile of pectin degradation enzymes reveals the molecular events during cell wall degradation and pathogenesis of rice sheath blight pathogen Rhizoctonia Solani AG1-IA. J Fungi 6(2):71

    Article  Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30(15):2114–2120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brooks SA (2007) Sensitivity to a phytotoxin from Rhizoctonia solani correlates with sheath blight susceptibility in rice. Phytopathology 97(10):1207–1212

    Article  CAS  PubMed  Google Scholar 

  • Cao H, Yang Z, Song S, Xue M, Liang G, Li N (2022) Transcriptome analysis reveals genes potentially related to maize resistance to Rhizoctonia solani. Plant Physiol Biochem 193:78–89

    Article  CAS  PubMed  Google Scholar 

  • Datta K, Tu J, Oliva N, Ona I, Velazhahan R, Mew TW, Muthukrishnan S, Datta SK (2001) Enhanced resistance to sheath blight by constitutive expression of infection-related rice chitinase in transgenic elite indica rice cultivars. Plant Sci 160(3):405–414

    Article  CAS  PubMed  Google Scholar 

  • Dobon A, Bunting DC, Cabrera-Quio LE, Uauy C, Saunders DG (2016) The host-pathogen interaction between wheat and yellow rust induces temporally coordinated waves of gene expression. BMC Genomics 17(1):1–4

    Article  Google Scholar 

  • FAO, Food and Agriculture Organization of the United Nations (2020) FAOSTAT Database

  • Gao Y, Zhang C, Han X, Wang ZY, Ma L, Yuan P, Wu JN, Zhu XF, Liu JM, Li DP, Hu YB, Xuan YH (2018) Inhibition of OsSWEET11 function in mesophyll cells improves resistance of rice to sheath blight disease. Mol Plant Pathol Sep 19(9):2149–2161. https://doi.org/10.1111/mpp.12689Epub 2018 Jul 19. PMID: 29660235; PMCID: PMC6638089

    Article  CAS  Google Scholar 

  • Ghosh S, Kanwar P, Jha G (2017) Alterations in rice chloroplast integrity, photosynthesis and metabolome associated with pathogenesis of Rhizoctonia solani. Sci Rep 7(1):1–12

    Article  Google Scholar 

  • Hawkins LK, Mylroie JE, Oliveira DA, Smith JS, Ozkan S, Windham GL et al (2015) Characterization of the Maize Chitinase genes and their effect on aspergillus flavus and aflatoxin Accumulation Resistance. PLoS ONE 10(6):e0126185. https://doi.org/10.1371/journal.pone.0126185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Henrissat B (1991) A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J 280:309–316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res W 585–587. https://doi.org/10.1093/nar/gkm259

  • Kawahara Y, Oono Y, Kanamori H, Matsumoto T, Itoh T, Minami E (2012) Simultaneous RNA-Seq analysis of a mixed transcriptome of rice and blast fungus interaction. PLoS ONE 7(11):e49423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kawahara Y, de la Bastide M, Hamilton JP, Kanamori H, McCombie WR, Ouyang S, Schwartz DC, Tanaka T, Wu J, Zhou S, Childs KL, Davidson RM, Lin H, Quesada-Ocampo L, Vaillancourt B, Sakai H, Lee SS, Kim J, Numa H, Itoh T, Buell CR, Matsumoto T (2013) Improvement of the Oryza sativa nipponbare reference genome using next generation sequence and optical map data. Rice 6:4

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12(4):357–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar KK, Poovannan K, Nandakumar R, Thamilarasi K, Geetha C, Jayashree N, Kokiladevi E, Raja JA, Samiyappan R, Sudhakar D, Balasubramanian P (2003) A high throughput functional expression assay system for a defence gene conferring transgenic resistance on rice against the sheath blight pathogen, Rhizoctonia solani. Plant Sci 165(5):969–976

    Article  CAS  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25(16):2078–20791000 Genome Project Data Processing Subgroup

  • Li MY, Wang JN, Wang GD, Feng ZM, Ye YH, Jiang W, Zuo T, Zhang YF, Chen XJ, Pan XB, Ma YY, Chen ZX, Zuo SM (2019) Improvement of japonica rice resistance to sheath blight disease by incorporating quantative resistance genes qSB-11HJX and qSB-9TQ. J Yangzhou Univ 40:1–7

    Google Scholar 

  • Li D, Li S, Wei S, Sun W (2021) Strategies to manage rice sheath blight: lessons from interactions between Rice and Rhizoctonia solani. Rice 14(1):1–15

    Article  PubMed  PubMed Central  Google Scholar 

  • Liao Y, Smyth GK, Shi W (2014) Feature counts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30(7):923–930

    Article  CAS  PubMed  Google Scholar 

  • Love MI, Huber W, Anders S (2014) Moderated estimation of Fold change and dispersion for RNA-Seq data with DESeq2. Genome Biol 15(12):1–21

    Article  Google Scholar 

  • Mangrauthia SK, Bhogireddy S, Agarwal S, Prasanth VV, Voleti SR, Neelamraju S, Subrahmanyam D (2017) Genome-wide changes in microRNA expression during short and prolonged heat stress and recovery in contrasting rice cultivars. J Exp Bot 68(9):2399–2412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Margani R, Widadi S (2018) Utilizing Bacillus to inhibit the growth and infection by sheath blight pathogen, Rhizoctonia solani in rice. In IOP Conference Series: Earth and Environmental Science, IOP Publishing. 142(1): 012070

  • Molla KA, Karmakar S, Chanda PK, Ghosh S, Sarkar SN, Datta SK, Datta K (2013) Rice oxalate oxidase gene driven by green tissue specific promoter increases tolerance to sheath blight pathogen (Rhizoctonia Solani) in transgenic rice. Mol Plant Pathol 14(9):910–922

  • Molla KA, Karmakar S, Molla J, Bajaj, Varshney RK, Datta SK, Datta K (2020) Understanding sheath blight resistance in rice: the road behind and the road ahead. Plant Biotechnol J 18(4):895–915

    Article  PubMed  PubMed Central  Google Scholar 

  • Naveenkumar R, Anandan A, Singh V, Prabhukarthikeyan SR, Parameswaran C, Sangeetha G, Mahender A, Keerthana U, Singh PK, Patra BC, Ali J Deciphering environmental factors and defense response of rice genotypes against sheath blight disease (2022). Physiol Mol Plant Pathol 122:101916. https://doi.org/10.1016/j.pmpp.2022.101916

  • Neuhaus JM, Fritig B, Linthorst HJ, Meins FJ, Mikkelsen JD, Ryals J (1996) A revised nomenclature for chitinase genes. Plant Mol Biology Report 14:102–104

    Article  CAS  Google Scholar 

  • Park CH, Kim S, Park JY, Ahn IP, Jwa NS, Im KH, Lee YH (2004) Molecular characterization of a pathogenesis-related protein 8 gene encoding a class III chitinase in rice. Mol Cells 17(1):144–150

    Article  CAS  PubMed  Google Scholar 

  • Prathi NB, Palit P, Madhu P, Ramesh M, Laha GS, Balachandran SM, Madhav MS, Sundaram RM, Mangrauthia SK (2018) Proteomic and transcriptomic approaches to identify resistance and susceptibility related proteins in contrasting rice genotypes infected with fungal pathogen Rhizoctonia Solani. Plant Physiol Biochem 130:258–266

    Article  CAS  PubMed  Google Scholar 

  • Prathi NB, Durga Rani CV, Balachandran SM, Prakasam V, Chandra Mohan Y, Nagalakshmi S, Srivastava SK, Sundaram RM, Mangrauthia SK (2021) Genome-wide expression profiling of small RNAs in Indian Strain of Rhizoctonia solani AG1-1A reveals differential regulation of milrnas during pathogenesis and crosstalk of gene regulation. Journal of Fungi, 7(7), p.561

  • Pusztahelyi T (2018) Chitin and chitin-related compounds in plant-fungal interactions. Mycology 9(3):189–201. https://doi.org/10.1080/21501203.2018.1473299PMID: 30181925; PMCID: PMC6115883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rao TB, Chopperla R, Methre R, Punniakotti E, Venkatesh V, Sailaja B, Reddy MR, Yugander A, Laha GS, Madhav MS, Sundaram RM, Ladhalakshmi D, Balachandran SM, Mangrauthia SK (2019) Pectin induced transcriptome of a Rhizoctonia solani strain causing sheath blight disease in rice reveals insights on key genes and RNAi machinery for development of pathogen derived resistance. Plant Mol Biol 100(1):59–71

    Article  CAS  PubMed  Google Scholar 

  • Reddy MR, Mangrauthia SK, Reddy SV, Manimaran P, Yugandhar P, Babu PN, Vishnukiran T, Subrahmanyam D, Sundaram RM, Balachandran SM (2021) PAP90, a novel rice protein plays a critical role in regulation of D1 protein stability of PSII. J Adv Res 30:197–211

    Article  CAS  PubMed  Google Scholar 

  • Richa K, Tiwari IM, Devanna BN, Botella JR, Sharma V, Sharma TR (2017) Novel chitinase gene LOC_Os11g47510 from indica rice tetep provides enhanced resistance against sheath blight pathogen Rhizoctonia Solani in rice. Front Plant Sci 8:596

    Article  PubMed  PubMed Central  Google Scholar 

  • Sailaja B, Anjum N, Vishnu Prasanth V, Sarla N, Subrahmanyam D, Voleti SR, Viraktamath BC, Mangrauthia SK (2014) Comparative study of susceptible and tolerant genotype reveals efficient recovery and root system contributes to heat stress tolerance in rice. Plant Mol Biology Report 32:1228–1240

    Article  CAS  Google Scholar 

  • Samal P, Molla KA, Bal A, Ray S, Swain H, Khandual A, Sahoo P, Behera M, Jaiswal S, Iquebal A, Chakraborti M (2022) Comparative transcriptome profiling reveals the basis of differential sheath blight disease response in tolerant and susceptible rice genotypes. Protoplasma 1:1–3

    Google Scholar 

  • Senapati M, Tiwari A, Sharma N, Chandra P, Bashyal BM, Ellur RK, Bhowmick PK, Bollinedi H, Vinod KK, Singh AK, Krishnan SG (2022) Rhizoctonia solani Kühn pathophysiology: status and prospects of sheath blight disease management in rice. Front Plant Sci 13:881116. https://doi.org/10.3389/fpls.2022.881116

  • Shah JM, Singh R, Veluthambi K (2013) Transgenic rice lines constitutively co-expressing tlp-D34 and chi11 display enhancement of sheath blight resistance. Biol Plant 57(2):351–358

    Article  CAS  Google Scholar 

  • Shi W, Zhao SL, Liu K, Sun YB, Ni ZB, Zhang GY, Tang HS, Zhu JW, Wan BJ, Sun HQ, Dai JY (2020) Comparison of leaf transcriptome in response to Rhizoctonia solani infection between resistant and susceptible rice cultivars. BMC Genomics 21:1–6

    Article  Google Scholar 

  • Shobha Rani N, Srikanth S, Bhadana VP, Badri J, Sundaram RM, Senguttuvel P, Prasad GSV, Shah T, Prasad PVNS, Hari Prasad AS, Subba Rao LB, Agarwal SK, Viraktamath BC (2014) Genetic Diversity and Genealogy of Rice Varieties in India. Directorate of Rice Research (Indian Council of Agricultural Research), Rajendranagar, Hyderabad-500030, India. Technical Book No. 83/2014,368 pp

  • Sneh B, Burpee L, Ogoshi A (1991) Identification of Rhizoctonia Species. APS

  • Taheri P, Tarighi S (2011) Cytomolecular aspects of rice sheath blight caused by Rhizoctonia solani. Eur J Plant Pathol 129(4):511–528

    Article  Google Scholar 

  • Tanaka J, Takashima T, Abe N, Fukamizo T, Numata T, Ohnuma T (2023) Characterization of two rice GH18 chitinases belonging to family 8 of plant pathogenesis-related proteins. Plant Sci 326:111524

    Article  CAS  PubMed  Google Scholar 

  • Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, Van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28(5):511–515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Venu RC, Jia Y, Gowda M, Jia MH, Jantasuriyarat C, Stahlberg E, Li H, Rhineheart A, Boddhireddy P, Singh P, Rutger N (2017) RL-SAGE and microarray analysis of the rice transcriptome after Rhizoctonia solani infection. Mol Genet Genomics 278:421–431

    Article  Google Scholar 

  • Wang J, Qi M, Liu J, Zhang Y (2015) CARMO: a comprehensive annotation platform for functional exploration of rice multi-omics data. Plant J 83(2):359–374

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Luo H, Wang H, **ang Z, Wei S, Zheng W (2022) Comparative transcriptome analysis of rice cultivars resistant and susceptible to Rhizoctonia Solani AG1-IA. BMC Genomics 23(1):1–4

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang X, Yan S, Li Y, Li G, Sun S, Li J, Cui Z, Huo J, Sun Y, Wang X et al (2023) Comparison of transcriptome between tolerant and susceptible Rice Cultivar reveals positive and negative regulators of response to Rhizoctonia solani in Rice. Int J Mol Sci 24:14310. https://doi.org/10.3390/ijms241814310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Chen L, Fu C, Wang L, Liu H, Cheng Y, Li S, Deng Q, Wang S, Zhu J, Liang Y (2017) Comparative transcriptome analyses of gene expression changes triggered by Rhizoctonia Solani AG1 IA infection in resistant and susceptible rice varieties. Front Plant Sci 8:1422

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao H, Yao W, Ouyang Y, Yang W, Wang G, Lian X, **ng Y, Chen L, **e W (2015) RiceVarMap: a comprehensive database of rice genomic variations. Nucleic Acids Res 43(D1):D1018–D1022

    Article  CAS  PubMed  Google Scholar 

  • Zhou L, Cheung MY, Li MW, Fu Y, Sun Z, Sun SM, Lam HM (2010) Rice hypersensitive induced reaction protein 1 (OsHIR1) associates with plasma membrane and triggers hypersensitive cell death. BMC Plant Biol 10:1–10

    Article  Google Scholar 

Download references

Acknowledgements

Authors are thankful to the Director, ICAR-IIRR, for his kind support. Financial support received from DBT Grant (BT/PR6466/COE/34/16/2012) is acknowledged. NBP thanks PJTSAU, Hyderabad for providing fellowship. We are thankful to Nucleome Informatics Pvt. Ltd., Hyderabad, India for providing the commercial facility of RNA sequencing.

Funding

Financial support was received from Department of Biotechnology (DBT), Government of India (Grant No. BT/PR6466/COE/34/16/2012).

Author information

Authors and Affiliations

  1. Institute of Biotechnology, Professor Jayashankar Telangana State Agricultural University (PJTSAU), Rajendranagar, Hyderabad, 500030, India

    Naresh Babu Prathi & Chagamreddy Venkata Durga Rani

  2. ICAR-Indian Council of Agricultural Research (ICAR)- Indian Institute of Rice Research, Hyderabad, 500030, India

    Naresh Babu Prathi, Vellaisamy Prakasam, Gandikota Mahendranath, C. N. Neeraja, Raman Meenakshi Sundaram & Satendra K. Mangrauthia

  3. Institute of Rice Research, ARI, PJTSAU, Rajendranagar, Hyderabad, 500030, India

    Yeshala Chandra Mohan

  4. Department of Molecular Biology and Biotechnology, SV Agriculture College, Tirupati, 517502, India

    G. K. Sri Vidya

Authors
  1. Naresh Babu Prathi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chagamreddy Venkata Durga Rani
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vellaisamy Prakasam
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yeshala Chandra Mohan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gandikota Mahendranath
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. G. K. Sri Vidya
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. C. N. Neeraja
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Raman Meenakshi Sundaram
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Satendra K. Mangrauthia
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceived and designed the experiments: S.K.M, R.M.S, CVDR; Performed the experiments: N.B.P, S.K.M, V.P; Analysis of data: N.B.P, S.K.M, G.K.S.V. Wrote the article: N.B.P, S.K.M, R.M.S. Provided the resources: C.N.N, V.P., Y.C.M. and R.M.S. All authors have read and agreed to the published version of the manuscript.

Corresponding authors

Correspondence to Chagamreddy Venkata Durga Rani, Raman Meenakshi Sundaram or Satendra K. Mangrauthia.

Ethics declarations

Ethical Approval

The authors have no relevant financial or non-financial interests to disclose. The authors have no competing interests to declare that are relevant to the content of this article. All authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest or non-financial interest in the subject matter or materials discussed in this manuscript. The authors have no financial or proprietary interests in any material discussed in this article. This research does not involve human participants and/or animals. All the authors have read and approved the manuscript.

Competing Interests

The authors declare no competing interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Prathi, N.B., Durga Rani, C.V., Prakasam, V. et al. Oschib1 gene encoding a GH18 chitinase confers resistance against sheath blight disease of rice caused by Rhizoctonia solani AG1-IA. Plant Mol Biol 114, 41 (2024). https://doi.org/10.1007/s11103-024-01442-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11103-024-01442-z

Keywords

Search

Navigation