Skip to main content
SpringerLink
Log in

Genome analysis provides insight about pathogenesis of Indian strains of Rhizoctonia solani in rice

  • Original Article
  • Published:
Functional & Integrative Genomics Aims and scope Submit manuscript

Abstract

The Rhizoctonia solani species complex is comprised of strains belonging to different anastomosis groups and causes diseases in several economically important crops, including rice. However, individuals within same anastomosis group exhibit distinct morphological and pathological differences on the same host. In this study, we have sequenced the genome of two aggressive Indian strains (BRS11 and BRS13) belonging to AG1-IA anastomosis group and compared them with the available genome of R. solani AG1-IA. We identified several SNPs and Indels in both of these genomes, in comparison to the AG1-IA genome. Furthermore, we observed expansion and emergence of orthogroups in these Indian strains and identified those potentially associated with pathogenesis. Amongst them, transposable elements, cell wall degrading enzymes, transcription factors, and oxalate decarboxylase were noteworthy. The current study unravels genetic variations and identifies genes that might account for pathogenicity variations amongst R. solani strains.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Ahvenniemi P, Wolf M, Lehtonen MJ, Wilson P, German-Kinnari M, Valkonen JPT (2009) Evolutionary diversification indicated by compensatory base changes in ITS2 secondary structures in a complex fungal species, Rhizoctonia solani. J Mol Evol 69:150–163

    Article  CAS  PubMed  Google Scholar 

  • Ajayi-Oyetunde OO, Bradley CA (2018) Rhizoctonia solani: taxonomy, population biology and management of rhizoctonia seedling disease of soybean. Plant Pathol 67:3–17

    Article  CAS  Google Scholar 

  • Anderson JP, Sperschneider J, Win J, Kidd B, Yoshida K, Hane J, Saunders DGO, Singh KB (2017) Comparative secretome analysis of Rhizoctonia solani isolates with different host ranges reveals unique secretomes and cell death inducing effectors. Sci Rep 7:10410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Banniza S, Rutherford MA (2001) Diversity of isolates of Rhizoctonia solani AG-1 1A and their relationship to other anastomosis groups based on pectic zymograms and molecular analysis. Mycol Res 105:33–40

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carling DE, Leine RH, Kebler KM (1987) Characterization of a new anastomosis group (AG-9) of Rhizoctonia solani. Phytopathology 77:1609–1612

    Article  Google Scholar 

  • Carling DE, Kuninaga S, Brainard KA (2002) Hyphal anastomosis reactions, rDNA-internal transcribed spacer sequences, and virulence levels among subsets of Rhizoctonia solani anastomosis group-2 (AG-2) and AG-BI. Phytopathology 92:43–50

    Article  CAS  PubMed  Google Scholar 

  • Chibucos MC, Soliman S, Gebremariam T, Lee H, Daugherty S, Orvis J, Shetty AC, Crabtree J, Hazen TH, Etienne KA, Kumari P, O’Connor TD, Rasko DA, Filler SG, Fraser CM, Lockhart SR, Skory CD, Ibrahim AS, Bruno VM (2016) An integrated genomic and transcriptomic survey of mucormycosis-causing fungi. Nat Commun 7:12218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cingolani P, Platts A, Wang LL, Coon M, Nguyen T, Wang L, Land SJ, Lu X, Ruden DM (2012) A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly (Austin) 6:80–92

    Article  CAS  Google Scholar 

  • Črešnar B, Petrič Š (2011) Cytochrome P450 enzymes in the fungal kingdom. Biochim Biophys Acta Proteins Proteomics 1814:29–35

    Article  CAS  Google Scholar 

  • Cubeta MA, Thomas E, Dean RA et al (2014) Draft genome sequence of the plant-pathogenic soil fungus Rhizoctonia solani anastomosis group 3 strain Rhs1AP. Genome Announc 2:e01072–e01014

    Article  PubMed  PubMed Central  Google Scholar 

  • Doyle JJ, Doyle JL (1990) A rapid total DNA preparation procedure for fresh plant tissue. Focus (Madison) 12:13–15

    Google Scholar 

  • Emms DM, Kelly S (2015) OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol 16:157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghosh S, Gupta SK, Jha G (2014) Identification and functional analysis of AG1-IA specific genes of Rhizoctonia solani. Curr Genet 60:327–341

    Article  CAS  PubMed  Google Scholar 

  • Ghosh S, Kanwar P, Jha G (2018) Identification of candidate pathogenicity determinants of Rhizoctonia solani AG1-IA, which causes sheath blight disease in rice. Curr Genet 64:729–740

    Article  CAS  PubMed  Google Scholar 

  • González García V, Portal Onco MA, Rubio Susan V (2006) Review. Biology and systematics of the form genus Rhizoctonia. Spanish J Agric Res 4:55–79

    Article  Google Scholar 

  • Guermache F, Rodier-Goud M, Caesar A, Héraud C, Bon MC (2012) Bi-fluorescence imaging for estimating accurately the nuclear condition of Rhizoctonia spp. Lett Appl Microbiol 54:568–571

    Article  CAS  PubMed  Google Scholar 

  • Gupta A, Chattoo BB (2008) Functional analysis of a novel ABC transporter ABC4 from Magnaporthe grisea. FEMS Microbiol Lett 278:22–28

    Article  CAS  PubMed  Google Scholar 

  • Hane JK, Anderson JP, Williams AH, Sperschneider J, Singh KB (2014) Genome sequencing and comparative genomics of the broad host-range pathogen Rhizoctonia solani AG8. PLoS Genet 10(5):e1004281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuninaga S, Yokosawa R (1985) DNA Base sequence homology in Rhizoctonia solani Kühn. Jpn J Phytopathol 51:127–132

    Article  Google Scholar 

  • Kuninaga S, Natsuaki T, Takeuchi T, Yokosawa R (1997) Sequence variation of the rDNA ITS regions within and between anastomosis groups in Rhizoctonia solani. Curr Genet 32:237–243

    Article  CAS  PubMed  Google Scholar 

  • Kuninaga S, Carling DE, Takeuchi T, Yokosawa R (2006) Comparison of rDNA-ITS sequences between potato and tobacco strains in Rhizoctonia solani AG-3. J Gen Plant Pathol 66:2–11

    Article  Google Scholar 

  • Langmead B, Salzberg SL (2012) Fast gapped-read alignment with bowtie 2. Nat Methods 9:357–359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liang X, Moomaw EW, Rollins JA (2015) Fungal oxalate decarboxylase activity contributes to Sclerotinia sclerotiorum early infection by affecting both compound appressoria development and function. Mol Plant Pathol 16:825–836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma L, Chen Z, Huang DW, Kutty G, Ishihara M, Wang H, Abouelleil A, Bishop L, Davey E, Deng R, Deng X, Fan L, Fantoni G, Fitzgerald M, Gogineni E, Goldberg JM, Handley G, Hu X, Huber C, Jiao X, Jones K, Levin JZ, Liu Y, Macdonald P, Melnikov A, Raley C, Sassi M, Sherman BT, Song X, Sykes S, Tran B, Walsh L, Xia Y, Yang J, Young S, Zeng Q, Zheng X, Stephens R, Nusbaum C, Birren BW, Azadi P, Lempicki RA, Cuomo CA, Kovacs JA (2016) Genome analysis of three Pneumocystis species reveals adaptation mechanisms to life exclusively in mammalian hosts. Nat Commun 7:10740

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • MacPherson S, Larochelle M, Turcotte B (2006) A fungal family of transcriptional regulators: the zinc cluster proteins. Microbiol Mol Biol Rev 70:583–604

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murzin AG, Brenner SE, Hubbard T, Chothia C (1995) SCOP: a structural classification of proteins database for the investigation of sequences and structures. J Mol Biol 247:536–540

    CAS  PubMed  Google Scholar 

  • Narasimhan V, Danecek P, Scally A, Xue Y, Tyler-Smith C, Durbin R (2016) BCFtools/RoH: a hidden Markov model approach for detecting autozygosity from next-generation sequencing data. Bioinformatics 32:1749–1751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Newman D (1939) The distribution of range in samples from a normal population, expressed in terms of an independent estimate of standard deviation. Biometrika 31:20–30

    Article  Google Scholar 

  • Ospina-Giraldo MD, Griffith JG, Laird EW, Mingora C (2010) The CAZyome of Phytophthora spp.: a comprehensive analysis of the gene complement coding for carbohydrate-active enzymes in species of the genus Phytophthora. BMC Genomics 11:525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pascual CB, Toda T, Raymondo AD, Hyakumachi M (2000) Characterization by conventional techniques and PCR of Rhizoctonia solani isolates causing banded leaf sheath blight in maize. Plant Pathol 49:108–118

    Article  CAS  Google Scholar 

  • Ponting CP, Schultz J, Milpetz F, Bork P (1999) SMART: identification and annotation of domains from signalling and extracellular protein sequences. Nucleic Acids Res 27:229–232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raffaele S, Kamoun S (2012) Genome evolution in filamentous plant pathogens: why bigger can be better. Nat Rev Microbiol 10:417–430

    Article  CAS  PubMed  Google Scholar 

  • Rose PW, Prlić A, Altunkaya A, Bi C, Bradley AR, Christie CH, Costanzo LD, Duarte JM, Dutta S, Feng Z, Green RK, Goodsell DS, Hudson B, Kalro T, Lowe R, Peisach E, Randle C, Rose AS, Shao C, Tao YP, Valasatava Y, Voigt M, Westbrook JD, Woo J, Yang H, Young JY, Zardecki C, Berman HM, Burley SK (2017) The RCSB protein data bank: integrative view of protein, gene and 3D structural information. Nucleic Acids Res 45:D271–D281

    Article  CAS  PubMed  Google Scholar 

  • Sharon M, Kuninaga S, Hyakumachi M et al (2008) Classification of Rhizoctonia spp. using rDNA-ITS sequence analysis supports the genetic basis of the classical anastomosis grouping. Mycoscience 49:93–114

    Article  CAS  Google Scholar 

  • Sinclair JB (1970) Rhizoctonia solani: biology and pathology. In: Parmeter J. (ed) Rhizoctonia solani: biology and pathology. University of California Press, Berkeley, Los Angeles and London, pp 199–217

  • Singh A, Rohila R, Savary S et al (2003) Short communications infection process in sheath blight of rice caused by Rhizoctonia solani. Indian Phytopathol 56:434–438

    Google Scholar 

  • Sperschneider J, Dodds PN, Gardiner DM, Singh KB, Taylor JM (2018) Improved prediction of fungal effector proteins from secretomes with EffectorP 2.0. Mol Plant Pathol 19:2094–2110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stanke M, Waack S (2003) Gene prediction with a hidden Markov model and a new intron submodel. Bioinformatics 19:ii215–ii225

    Article  PubMed  Google Scholar 

  • Stanke M, Schöffmann O, Morgenstern B, Waack S (2006) Gene prediction in eukaryotes with a generalized hidden Markov model that uses hints from external sources. BMC Bioinformatics 7:62

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stanke M, Diekhans M, Baertsch R, Haussler D (2008) Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics 24:637–644

    Article  CAS  PubMed  Google Scholar 

  • States DJ, Gish W (1994) Combined use of sequence similarity and codon bias for coding region identification. J Comput Biol 1:39–50

    Article  CAS  PubMed  Google Scholar 

  • Stodart BJ, Harvey PR, Neate SM, Melanson DL, Scott ES (2007) Genetic variation and pathogenicity of anastomosis group 2 isolates of Rhizoctonia solani in Australia. Mycol Res 111:891–900

    Article  PubMed  Google Scholar 

  • Sumner DR (1996) Sclerotia formation by Rhizoctonia species and their survival. In: Rhizoctonia species: taxonomy, molecular biology, ecology, pathology and disease control, pp 207–215

    Google Scholar 

  • Taheri P, Gnanamanickam S, Höfte M (2007) Characterization, genetic structure, and pathogenicity of Rhizoctonia spp. associated with rice sheath diseases in India. Phytopathology 97:373–383

    Article  CAS  PubMed  Google Scholar 

  • Tarasov A, Vilella AJ, Cuppen E, Nijman IJ, Prins P (2015) Sambamba: fast processing of NGS alignment formats. Bioinformatics 31:2032–2034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) Clustal-W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thon MR, Pan H, Diener S, Papalas J, Taro A, Mitchell TK, Dean RA (2006) The role of transposable element clusters in genome evolution and loss of synteny in the rice blast fungus Magnaporthe oryzae. Genome Biol 7:R16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tiwari IM, Jesuraj A, Kamboj R, Devanna BN, Botella JR, Sharma TR (2017) Host delivered RNAi, an efficient approach to increase rice resistance to sheath blight pathogen (Rhizoctonia solani). Sci Rep 7:7521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Urban M, Cuzick A, Rutherford K, Irvine A, Pedro H, Pant R, Sadanadan V, Khamari L, Billal S, Mohanty S, Hammond-Kosack KE (2017) PHI-base: a new interface and further additions for the multi-species pathogen-host interactions database. Nucleic Acids Res 45:D604–D610

    Article  CAS  PubMed  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR protocols: a guide to methods and applications. Academic Press, Inc, pp 315–322

  • Wibberg D, Jelonek L, Rupp O, Hennig M, Eikmeyer F, Goesmann A, Hartmann A, Borriss R, Grosch R, Pühler A, Schlüter A (2013) Establishment and interpretation of the genome sequence of the phytopathogenic fungus Rhizoctonia solani AG1-IB isolate 7/3/14. J Biotechnol 167:142–155

    Article  CAS  PubMed  Google Scholar 

  • Wibberg D, Andersson L, Tzelepis G, Rupp O, Blom J, Jelonek L, Pühler A, Fogelqvist J, Varrelmann M, Schlüter A, Dixelius C (2016) Genome analysis of the sugar beet pathogen Rhizoctonia solani AG2-2IIIB revealed high numbers in secreted proteins and cell wall degrading enzymes. BMC Genomics 17:245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xue M, Yang J, Li Z et al (2012) Comparative analysis of the genomes of two field isolates of the rice blast fungus Magnaporthe oryzae. PLoS Genet 8:1002869

    Article  CAS  Google Scholar 

  • Yamauchi Y, Hasegawa A, Taninaka A, Mizutani M, Sugimoto Y (2011) NADPH-dependent reductases involved in the detoxification of reactive carbonyls in plants. J Biol Chem 286:6999–7009

    Article  CAS  PubMed  Google Scholar 

  • Yang G, Li C (2012) General description of Rhizoctonia species complex. In: Cumagun CJ (ed) Plant pathology, pp 41–52

    Google Scholar 

  • Yoshida K, Saunders DGO, Mitsuoka C, Natsume S, Kosugi S, Saitoh H, Inoue Y, Chuma I, Tosa Y, Cano LM, Kamoun S, Terauchi R (2016) Host specialization of the blast fungus Magnaporthe oryzae is associated with dynamic gain and loss of genes linked to transposable elements. BMC Genomics 17:370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao Z, Liu H, Wang C, Xu JR (2013) Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi. BMC Genomics 14:274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng A, Lin R, Zhang D, Qin P, Xu L, Ai P, Ding L, Wang Y, Chen Y, Liu Y, Sun Z, Feng H, Liang X, Fu R, Tang C, Li Q, Zhang J, Xie Z, Deng Q, Li S, Wang S, Zhu J, Wang L, Liu H, Li P (2013) The evolution and pathogenic mechanisms of the rice sheath blight pathogen. Nat Commun 4:1424

    Article  CAS  PubMed  Google Scholar 

  • Zhou B, Bailey A, Niblett CL, Qu R (2016) Control of brown patch (Rhizoctonia solani) in tall fescue (Festuca arundinacea Schreb.) by host induced gene silencing. Plant Cell Rep 35:791–802

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

SG acknowledges SPM fellowship from CSIR (Council of Scientific and Industrial Research, Govt. of India) while KT and PK acknowledge the SRF and Post-Doctoral Research fellowship from DBT (Department of Biotechnology, Govt of India) respectively. We are thankful to Dr. G.S. Laha, IIRR (Indian Institute of Rice Research, Hyderabad, India) and ITCC (Indian Type Culture Collection, New Delhi, India) for providing some of the R. solani strains used in this study. We also acknowledge Nucleome Informatics Pvt. Ltd. (Hyderabad) for assistance in genome sequencing. Further, the assistance of confocal microscopy, sequencing, plant growth and central instrumentation facilities at National Institute of Plant Genome Research (NIPGR) is acknowledged.

Funding

This work was supported by DBT, Government of India (BT/PR11532/AGIII/103/885/2014) as well as core research grant from NIPGR. The funders had no role in study design, data collection and analysis, decision to publish the manuscript.

Author information

Author notes

  1. Srayan Ghosh, Neelofar Mirza and Poonam Kanwar contributed equally to this work.

Authors and Affiliations

  1. Plant Microbe Interactions Laboratory, National Institute of Plant Genome Research, Aruna Asaf Ali Marg, New Delhi, 110067, India

    Srayan Ghosh, Neelofar Mirza, Poonam Kanwar, Kriti Tyagi & Gopaljee Jha

Authors
  1. Srayan Ghosh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Neelofar Mirza
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Poonam Kanwar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kriti Tyagi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gopaljee Jha
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

SG performed the isolation and characterization of Indian strains. NM and SG carried out genome analysis. SG and PK performed wet lab experiments and compiled the manuscript. SG, PK, NM, KT, and GJ drafted the manuscript. GJ planned and supervised the experiments.

Corresponding author

Correspondence to Gopaljee Jha.

Additional information

Publisher’s note

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

Accession Number

The Illumina sequence data from this study have been submitted as BioProject ID: PRJNA417898 for BRS11 and PRJNA417899 for BRS13 to the NCBI Sequence read archive.

Electronic supplementary material

Online Resource 1

Bioinformatics pipeline used in this study. The flowchart reflects strategies used for identification of i. SNPs and small Indels, ii. expansion and emergence of gene families and iii. Identification of potential pathogenicity determinants in BRS11 and BRS13. (PNG 135 kb)

High Resolution Image (TIF 260 kb)

Online Resource 2

Geographical distribution of different Indian R. solani strains used in the study. (PNG 1886 kb)

High Resolution Image (TIF 4562 kb)

Online Resource 3

The growth pattern of different Indian R. solani strains on PDA plates. The fungal sclerotia were grown on PDA plates and representative photographs of the plates during 6 and 10 days of incubation is provided. (PNG 24254 kb)

High Resolution Image (TIF 33692 kb)

Online Resource 4

Polymorphisms detected in BRS11 genome. (XLSX 1163 kb)

Online Resource 5

Polymorphisms detected in BRS13 genome. (XLSX 1161 kb)

Online Resource 6

Assembly statistics of unmapped reads. (XLSX 10 kb)

Online Resource 7

Emerged orthogroups (gene families) in BRS11 and BRS13. (XLSX 18 kb)

Online Resource 8

Expanded orthogroups (gene families) in BRS11 and BRS13. (XLSX 15 kb)

Online Resource 9

List of pseudogenes containing premature stop codon under expanded category. (XLSX 10 kb)

Online Resource 10

Prominent gene functions that have expanded/emerged in BRS11 and BRS13. The genes related to functions such as cell wall degradation, chromosomal rearrangement, multi-drug resistance, oxalate degradation, gene regulation, signaling, protein degradation and autophagy along with cellular detoxification were shown in different colored pies. Red arc depicts expanded and yellow arc represents emerged orthogroups. GCS: Gamma-glutamyl Cysteine Synthetase. (PNG 1563 kb)

High Resolution Image (TIF 3297 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ghosh, S., Mirza, N., Kanwar, P. et al. Genome analysis provides insight about pathogenesis of Indian strains of Rhizoctonia solani in rice. Funct Integr Genomics 19, 799–810 (2019). https://doi.org/10.1007/s10142-019-00687-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10142-019-00687-y

Keywords

Search

Navigation