Skip to main content
SpringerLink
Log in

Unraveling the Genetic Complexities in Gene Set of Sugarcane Red Rot Pathogen Colletotrichum falcatum Through Transcriptomic Approach

  • Research article
  • Published:
Sugar Tech Aims and scope Submit manuscript

Abstract

The transcriptome-based gene set expression of a unique sugarcane stalk infecting fungal pathogen reveals novels insights in deciphering the class of pathogenicity genes present in Colletotrichum falcatum. This study gains significance in understanding the genetic signature of this pathogen using RNA-Seq technology. A total of 53,410,513 reads (24,732 transcripts) specific to C. falcatum were generated, and 13,320 genes were predicted. Gene ontology distributions have been grouped into three domains as biological (3053), cellular (1601) and molecular functions (3444). KEGG annotations represented pathway biomolecules such as carbohydrates, lipids, nucleotides, amino acids, glycans, cofactors, vitamins, terpenoids and polyketides. The genes for virulence have been classified and grouped into candidate effectors, transition-specific and secondary metabolites, proteases, transporters and peptidases which revealed that C. falcatum transcripts encode a large number of secondary metabolites and membrane transporters. Gene enrichment analysis revealed that the number of transporters encoded by C. falcatum is significantly more as compared to that encoded by several other Colletotrichum spp. Phylogenomics analysis indicated that C. falcatum is closely related to C. graminicola and C. sublineola infecting related host plants, maize and sorghum, respectively. This study provides a comprehensive understanding of C. falcatum pathobiology and has identified many candidate genes/putative functions possibly required for its pathogenesis .

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
Fig. 6

Similar content being viewed by others

References

  • Baroncelli, R., J.M. Sanz-martín, G.E. Rech, S.A. Sukno, and M. Thon. 2014. Draft genome sequence of Colletotrichum sublineola a destructive pathogen of cultivated sorghum. Genome Announcement 2 (3): 10–11.

    Article  Google Scholar 

  • Cannon, P.F., U. Damm, P.R. Johnston, and B.S. Weir. 2012. Colletotrichum—Current status and future directions. Studies in Mycology 73: 181–213.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cantarel, B.L., P.M. Coutinho, C. Rancurel, T. Bernard, V. Lombard, and B. Henrissat. 2009. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Research 37: D233–D238.

    Article  CAS  PubMed  Google Scholar 

  • Casado-Díaz, A., S. Encinas-Villarejo, B.D.L. Santos, E. Schilirò, E.M. Yubero Serrano, F. Amil Ruíz, and J.L. Caballero. 2006. Analysis of strawberry genes differentially expressed in response to Colletotrichum infection. Physiologia Plantarum 128: 633–650.

    Article  Google Scholar 

  • Damm, U., R. Barroncelli, L. Cai, Y. Kubo, R.J. O’Connell, B. Weir, K. Yoshino, and P.F. Cannon. 2010. Colletotrichum: Species, ecology and interactions. IMA Fungus 1 (2): 161–165.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gan, P., K. Ikeda, H. Irieda, M. Narusaka, R.J. O’Connell, Y. Narusaka, and K. Shirasu. 2013. Comparative genomic and transcriptomic analyses reveal the hemibiotrophic stage shift of Colletotrichum fungi. New Phytologist 197: 1236–1249.

    Article  CAS  PubMed  Google Scholar 

  • Houterman, P.M., B.J. Cornelissen, and M. Rep. 2008. Suppression of plant resistance gene-based immunity by a fungal effector. PLoS Pathogens 4: e1000061.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jupe, J., R. Stam, A.J. Howden, J.A. Morris, R. Zhang, P.E. Hedley, and E. Huitema. 2013. Phytophthora capsici-tomato interaction features dramatic shifts in gene expression associated with a hemi-biotrophic lifestyle. Genome Biology 14: R63.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kanehisa, M., and S. Goto. 2000. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Research 28: 27–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kanehisa, M., S. Goto, Y. Sato, M. Furumichi, and M. Tanabe. 2012. KEGG for integration and interpretation of large-scale molecular datasets. Nucleic Acids Research 40: D109–D114.

    Article  CAS  PubMed  Google Scholar 

  • Kleemann, J., L.J. Rincon-Rivera, H. Takahara, U. Neumann, E.V.L. van Themaat, and R.J. O’Connell. 2012. Sequential delivery of host-induced virulence effectors by appressoria and intracellular hyphae of the phytopathogen Colletotrichum higginsianum. PLoS Pathogens 8 (4): e1002643.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krogh, A., B. Larsson, G. von Heijne, and E.L. Sonnhammer. 2001. Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. Journal of Molecular Biology 305: 567–580.

    Article  CAS  PubMed  Google Scholar 

  • Lister, R., B.D. Gregory, and J.R. Ecker. 2009. Next is now: New technologies for sequencing of genomes, transcriptomes, and beyond. Current Opinion in Plant Biology 12 (2): 107–118.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Malathi, P., R. Viswanathan, and R. Jothi. 2006. Specific adaptation of Colletotrichum falcatum pathotypes to sugarcane cultivars. Sugar Tech 8: 52–56.

    Article  Google Scholar 

  • Malathi, P., R. Viswanathan, A. Ramesh Sundar, N. Prakasam, P. Padmanaban, R. Jothi, S.R. Renuka Devi, and M. Poongothai. 2010. Variability among Colletotrichum falcatum pathotypes used for screening red rot resistance in sugarcane. Sugar Cane International 28 (2): 47–52.

    Google Scholar 

  • Mardis, E.R. 2013. Next-generation sequencing platforms. Annual Reviews of Analytical Chemistry 6 (1): 287–303.

    Article  CAS  Google Scholar 

  • McDowell, J.M. 2013. Genomic and transcriptomic insights into lifestyle transitions of a hemi-biotrophic fungal pathogen. New Phytologist 197: 1032–1034.

    Article  CAS  PubMed  Google Scholar 

  • Meinhardt, L.W., G. Gilson, L. Costa, D.P.T. Thomazella, P. José, P.L. Teixeira, and B.A. Bailey. 2014. Genome and secretome analysis of the hemibiotrophic fungal pathogen Moniliophthora roreri, which causes frosty pod rot disease of cacao: Mechanisms of the biotrophic and necrotrophic phases. BMC Genomics 15: 164. doi:10.1186/1471-2164-15-164.

    Article  PubMed  PubMed Central  Google Scholar 

  • Moriya, Y., M. Itoh, S. Okuda, A.C. Yoshizawa, and M. Kanehisa. 2007. KAAS: An automatic genome annotation and pathway reconstruction server. Nucleic Acids Research 35 (Suppl 2): 182–185.

    Article  Google Scholar 

  • Morozova, O., and M. Marra. 2008. Applications of next-generation sequencing technologies in functional genomics. Genomics 92: 255–264.

    Article  CAS  PubMed  Google Scholar 

  • Münch, S., U. Lingner, D.S. Floss, N. Ludwig, N. Sauer, and H.B. Deising. 2008. The hemibiotrophic lifestyle of Colletotrichum species. Journal of Plant Physiology 165: 41–51.

    Article  PubMed  Google Scholar 

  • O’Connell, R.J., M.R. Thon, S. Hacquard, S.G. Amyotte, J. Kleemann, M.F. Torres, and L.J. Vaillancourt. 2012. Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nature Genetics 44: 1055–1060.

    Google Scholar 

  • Oh, Y., N. Donofrio, H. Pan, S. Coughlan, D. Brown, S. Meng, and R.A. Dean. 2000. Transcriptome analysis reveals new insight into appressorium formation and function in the rice blast fungus Magnaporthe oryzae. Genome Biology. doi:10.1186/gb-2008-9-5-r85.

    Google Scholar 

  • Park, J., S. Lee, J. Choi, K. Ahn, B. Park, S. Kang, and Y.H. Lee. 2008. Fungal cytochrome P450 database. BMC Genomics 9: 402.

    Article  PubMed  PubMed Central  Google Scholar 

  • Petersen, T.N., S. Brunak, G. von Heijne, and H. Nielsen. 2011. SignalP 4.0: Discriminating signal peptides from transmembrane regions. Nature Methods 8: 785–786.

    Article  CAS  PubMed  Google Scholar 

  • Punta, M., P.C. Coggill, R.Y. Eberhardt, J. Mistry, J. Tate, C. Boursnell, N. Pang, K. Forslund, G. Ceric, J. Clement, A. Heger, L. Holm, E.L. Sonnhammer, S.R. Eddy, A. Bateman, and R.D. Finn. 2012. The Pfam protein families database. Nucleic Acids Research 40: D290–D301.

    Article  CAS  PubMed  Google Scholar 

  • Quevillon, E., V. Silventoinen, S. Pillai, N. Harte, N. Mulder, R. Apweiler, and R. Lopez. 2005. InterProScan: Protein domains identifier. Nucleic Acids Research 33: 6W116–6W120.

    Article  Google Scholar 

  • Rawlings, N.D., A.J. Barrett, and A. Bateman. 2012. MEROPS: The database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Research 40: D343–D350.

    Article  CAS  PubMed  Google Scholar 

  • Schafer, W. 1994. Molecular mechanisms of fungal pathogenicity to plants. Annual Review of Phytopathology 32: 461–477.

    Article  Google Scholar 

  • Stephenson, S., C.M. Stephens, D.J. Maclean, and J.M. Manners. 2005. CgDN24: A gene involved in hyphal development in the fungal phytopathogen Colletotrichum gloeosporioides. Microbiological Research 160: 389–397.

    Article  CAS  PubMed  Google Scholar 

  • Stergiopoulos, I., and P.J. de Wit. 2009. Fungal effector proteins. Annual Review of Phytopathology 47: 233–263.

    Article  CAS  PubMed  Google Scholar 

  • Suman, A., S. Lal, A.K. Shasany, A. Gaur, and P. Singh. 2005. Molecular assessment of diversity among pathotypes of Colletotrichum falcatum prevalent in sub-tropical Indian sugarcane. World Journal of Microbiology and Biotechnology 21: 1135–1140.

    Article  CAS  Google Scholar 

  • Taniguti, L.M., P.D.C. Schaker, J. Benevenuto, L.P. Peters, G. Carvalho, A. Palhares, and C.B. Monteiro-Vitorello. 2015. Complete genome sequence of Sporisorium scitamineum and biotrophic interaction transcriptome with sugarcane. PLoS ONE 10 (6): e0129318. doi:10.1371/journal.pone.0129318.

    Article  PubMed  PubMed Central  Google Scholar 

  • Thakur, K., V. Chawla, S. Bhatti, M.K. Swarnkar, J. Kaur, R. Shankar, and G. Jha. 2013. De novo transcriptome sequencing and analysis for Venturia inaequalis, the devastating apple scab pathogen. PLoS ONE. doi:10.1371/journal.pone.0053937.

    Google Scholar 

  • Viswanathan, R. 2010. Plant disease: Red rot of sugarcane, 306. New Delhi: Anmol Publishers.

    Google Scholar 

  • Viswanathan, R., and G.P. Rao. 2011. Disease scenario and management of major sugarcane diseases in India. Sugar Tech 13: 336–353.

    Article  CAS  Google Scholar 

  • Viswanathan, R., and R. Samiyappan. 1999. Red rot disease in sugarcane: A major constraint for the Indian sugar industry. Sugar Cane 17: 9–15.

    Google Scholar 

  • Viswanathan, R., C.N. Prasanth, P. Malathi, and A.R. Sundar. 2016. Draft genome sequence of Colletotrichum falcatum—A prelude on screening of red rot pathogen in sugarcane. Journal of Genomics 4 (10): 1–3. doi:10.7150/jgen.13585.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang, Z., M. Gerstein, and M. Snyder. 2009. RNA-Seq: A revolutionary tool for transcriptomics. Nature Reviews Genetics 10 (1): 57–63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilhelm, B.T., and J.R. Landry. 2009. RNA-Seq-quantitative measurement of expression through massively parallel RNA-sequencing. Nature Methods 48: 249–257.

    CAS  Google Scholar 

  • Wu, Q., L. Xu, J. Guo, Y. Su, and Y. Que. 2013. Transcriptome profile analysis of sugarcane responses to Sporisorium scitamineum infection using Solexa sequencing technology. BioMed Research International Article ID 298920.

  • Zheng, P., Y. Xia, G. Xiao, C. Xiong, X. Hu, S. Zhang, H. Zheng, Y. Huang, Y. Zhou, S. Wang, G.P. Zhao, X. Liu, R.J. St Leger, and C. Wang. 2011. Genome sequence of the insect pathogenic fungus Cordyceps militaris, a valued traditional Chinese medicine. Genome Biology 12(11):R116. doi:10.1186/gb-2011-12-11-r116.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, Y., K. Zhang, A. Fang, Y. Han, J. Yang, M. Xue, and W. Sun. 2014. Specific adaptation of Ustilaginoidea virens in occupying host florets revealed by comparative and functional genomics. Nature Communications 5: 3849. doi:10.1038/ncomms4849.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are grateful to the Director of ICAR-Sugarcane Breeding Institute, Coimbatore, for providing facilities and encouragement.

Funding

This study was partly funded by Outreach Project of ICAR, ALCOCERA.

Author information

Authors and Affiliations

  1. Division of Crop Protection, Sugarcane Breeding Institute, Indian Council of Agricultural Research, Coimbatore, 641007, India

    C. Naveen Prasanth, R. Viswanathan, P. Malathi & A. Ramesh Sundar

  2. Indian Institute of Spices Research, Indian Council of Agricultural Research, Calicut, Kerala, 673012, India

    Neethu Krishna

  3. Xcleris Genomics Pvt. Ltd., Ahmadabad, Gujarat, 380009, India

    Tanushree Tiwari

Authors
  1. C. Naveen Prasanth
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. Viswanathan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Neethu Krishna
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. P. Malathi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. Ramesh Sundar
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tanushree Tiwari
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to R. Viswanathan.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical Standards

This article does not contain any studies with human participants or animals performed by any of the authors.

Data Access

All data contributing to this transcriptome initiative have been deposited at the NCBI under BioProject PRJNA272832. The accession number of Sequence Read Achieves (SRA) is SRR1765657.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 82 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Prasanth, C.N., Viswanathan, R., Krishna, N. et al. Unraveling the Genetic Complexities in Gene Set of Sugarcane Red Rot Pathogen Colletotrichum falcatum Through Transcriptomic Approach. Sugar Tech 19, 604–615 (2017). https://doi.org/10.1007/s12355-017-0529-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12355-017-0529-3

Keywords

Search

Navigation