Skip to main content
SpringerLink
Log in

Regulatory Factors in Pochonia chlamydosporia-Induced Gene Expression

  • Chapter
  • First Online:
Perspectives in Sustainable Nematode Management Through Pochonia chlamydosporia Applications for Root and Rhizosphere Health

Part of the book series: Sustainability in Plant and Crop Protection ((SUPP))

  • 658 Accesses

Abstract

Soil microorganisms respond to, and release signals in, the rhizosphere, affecting root growth and their interactions with parasites. Understanding the gene expression patterns that are active in roots is fundamental for successful exploitation of beneficial associations. Pochonia chlamydosporia is a facultative parasite of nematode eggs and a growth-promoting endophyte. Transcriptomic studies from roots colonized by P. chlamydosporia showed that the fungus differentially regulates several genes. These included transcription factors and microRNAs differentially expressed during root endophytism. Both are transcriptional regulators and form integral parts of signalling webs, modulating many biological processes. The transcription factors involved in defence, resistance and plant growth include WRKYs, a family of genes expressed either in P. chlamydosporia-colonized or control roots. In vitro studies on endophytism also showed differential expression of 26 miRNAs, with 154 potential target genes involved in apoptosis, metabolism and binding, including transcription factors. The differential gene expression induced by P. chlamydosporia in the presence of nematodes or other pathogens may disclose novel pest and disease management strategies. The fungus transcriptomic analyses also support the production of industrial and commercial bioformulations for plant protection, through the induction of endogenous plant defence mechanisms.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Notes

  1. 1.

    WRKY : a superfamily of TFs unique for plants, involved in regulation of plant development and response to biotic or abiotic stress.

References

  • Abad, L. R., D’Urzo, M. P., Liu, D., et al. (1996). Antifungal activity of tobacco osmotin has specificity and involves plasma membrane permeabilization. Plant Science, 118, 11–23.

    Article  CAS  Google Scholar 

  • Anžlovar, S., & Dermastia, M. (2003). The comparative analysis of osmotins and osmotin-like PR-5 proteins. Plant Biology, 5, 116–124.

    Article  Google Scholar 

  • Anžlovar, S., Serra, M. D., Dermastia, M., et al. (1998). Membrane permeabilizing activity of pathogenesis-related protein linusitin from flax grain. Molecular Plant-Microbe Interactions, 11, 610–617.

    Article  Google Scholar 

  • Axtell, M. J., Westholm, J. O., & Lai, E. C. (2011). Vive la difference: Biogenesis and evolution of microRNAs in plants and animals. Genome Biology, 12, 221. doi:10.1186/gb-2011-12-4-221.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Behie, S. W., Zelisko, P. M., & Bidochka, M. J. (2012). Endophytic insect-parasitic fungi translocate nitrogen directly from insects to plants. Science, 336, 1576–1577.

    Article  CAS  PubMed  Google Scholar 

  • Belkhadir, Y., Subramaniam, R., & Dangl, J. L. (2004). Plant disease resistance protein signaling: NBS-LRR proteins and their partners. Current Opinion in Plant Biology, 7, 391–399.

    Article  CAS  PubMed  Google Scholar 

  • Bhattarai, K. K., Xie, Q. G., Mantelin, S., et al. (2008). Tomato susceptibility to root-knot nematodes requires an intact jasmonic acid signaling pathway. Molecular Plant-Microbe Interactions, 21, 1205–1214.

    Article  CAS  PubMed  Google Scholar 

  • Bhattarai, K. K., Atamian, H. S., Kaloshian, I., et al. (2010). WRKY72-type transcription factors contribute to basal immunity in tomato and Arabidopsis as well as gene-for-gene resistance mediated by the tomato R gene Mi-1. The Plant Journal, 63, 229–240.

    Article  CAS  PubMed  Google Scholar 

  • Branch, C., Hwang, C. F., Navarre, D. A., & Williamson, V. M. (2004). Salicylic acid is part of the mi-1-mediated defense response to root-knot nematode in tomato. Molecular Plant-Microbe Interactions, 17, 351–356.

    Article  CAS  PubMed  Google Scholar 

  • Cao, H., Li, X., & Dong, X. (1998). Generation of broad-spectrum disease resistance by overexpression of an essential regulatory gene in systemic acquired resistance. Proceedings of the National Academic Sciences USA, 95, 6531–6536.

    Article  CAS  Google Scholar 

  • Chen, H., Lai, Z., Shi, J., et al. (2010). Roles of Arabidopsis WRKY18, WRKY40 and WRKY60 transcription factors in plant responses to abscisic acid and abiotic stress. BMC Plant Biology, 10, 281.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ciancio, A., Colagiero, M., Ferrara, M., et al. (2013, July 21–25). Transcriptome changes in tomato roots during colonization by the endophytic fungus Pochonia chlamydosporia. 5th congress of European Microbiologists (FEMS), Leipzig, Germany.

    Google Scholar 

  • Escudero, N., & Lopez-Llorca, L. V. (2012). Effects on plant growth and root-knot nematode infection of an endophytic GFP transformant of the nematophagous fungus Pochonia chlamydosporia. Symbiosys, 57, 33–42.

    Article  Google Scholar 

  • Eulgem, T., Rushton, P. J., Robatzek, S., et al. (2000). The WRKY superfamily of plant transcription factors. Trends in Plant Science, 5, 199–206.

    Article  CAS  PubMed  Google Scholar 

  • Glazebrook, J. (2005). Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Review of Phytopathology, 43, 205–227.

    Article  CAS  PubMed  Google Scholar 

  • Guan, Y., Meng, X., Khanna, R., et al. (2014). Phosphorylation of a WRKY transcription factor by MAPKs is required for pollen development and function in Arabidopsis. PLoS Genetics, 10, e1004384.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hammond-Kosack, K. E., & Parker, J. E. (2003). Deciphering plant-pathogen communication: Fresh perspectives for molecular resistance breeding. Current Opinion in Biotechnology, 14, 177–193.

    Article  CAS  PubMed  Google Scholar 

  • Huang, S., Gao, Y., Liu, J., et al. (2012). Genome-wide analysis of WRKY transcription factors in Solanum lycopersicum. Molecular Genetics and Genomics, 287, 495–513.

    Article  CAS  PubMed  Google Scholar 

  • Journot-Catalino, N., Somssich, I. E., Roby, D., et al. (2006). The transcription factors WRKY11 and WRKY17 act as negative regulators of basal resistance in Arabidopsis thaliana. Plant Cell, 18, 3289–3302.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kerry, B. R. (2000). Rhizosphere interactions and the exploitation of microbial agents for the biological control of plant-parasitic nematodes. Annual Review of Phytopathology, 38, 423–424.

    Article  CAS  PubMed  Google Scholar 

  • Kerry, B. R., & Bourne, J. M. (1996). The importance of rhizosphere interactions in the biological control of plant parasitic nematodes: A case study using Verticillium chlamydosporium. Pesticide Science, 47, 69–75.

    Article  CAS  Google Scholar 

  • Ketting, R. F., Fischer, S. E. J., Bernstein, E., et al. (2001). Dicer functions in RNA interference and in synthesis of small RNA involved in developmental timing in C. elegans. Genes & Development, 15, 2654e2659.

    Article  Google Scholar 

  • Larriba, E., Jaime, M. D., Carbonell-Caballero, J., et al. (2014). Sequencing and functional analysis of the genome of a nematode egg-parasitic fungus, Pochonia chlamydosporia. Fungal Genetics and Biology, 65, 69–80.

    Article  CAS  PubMed  Google Scholar 

  • Larriba, E., Jaime, M. D. L. A., Nislow, C., et al. (2015). Endophytic colonization of barley (Hordeum vulgare) roots by the nematophagous fungus Pochonia chlamydosporia reveals plant growth promotion and a general defense and stress transcriptomic response. Journal of Plant Research, 128, 665–678.

    Article  CAS  PubMed  Google Scholar 

  • Lee, Y., Ahn, C., Han, J. J., et al. (2003). The nuclear RNase III Drosha initiates microRNA processing. Nature, 425, 415e419.

    Google Scholar 

  • Li, J., Luan, Y., & Jin, H. (2012). The tomato SlWRKY gene plays an important role in the regulation of defense responses in tobacco. Biochemical and Biophysical Research Communications, 427, 671–676.

    Article  CAS  PubMed  Google Scholar 

  • Lopez-Llorca, L. V., Gómez-Vidal, S., Monfort, E., et al. (2010). Expression of serine proteases in egg-parasitic nematophagous fungi during barley root colonization. Fungal Genetics and Biology, 47, 342–351.

    Article  CAS  PubMed  Google Scholar 

  • Maciá-Vicente, J., Rosso, L. C., Ciancio, A., et al. (2009). Colonisation of barley roots by endophytic Fusarium equiseti and Pochonia chlamydosporia: Effects on plant growth and disease. The Annals of Applied Biology, 155, 391–401.

    Article  Google Scholar 

  • Manzanilla-López, R. H., Atkins, S. D., Clark, I., et al. (2009). Measuring abundance, diversity and parasitic ability in two populations of the nematophagous fungus Pochonia chlamydosporia var. chlamydosporia. Biocontrol Science and Technology, 19, 391–406.

    Article  Google Scholar 

  • Manzanilla-López, R. H., Esteves, I., Finetti-Sialer, M. M., et al. (2013). Pochonia chlamydosporia: Advances and challenges to improve its performance as a biological control agent of sedentary endo-parasitic nematodes. Journal of Nematology, 45, 1–7.

    PubMed  PubMed Central  Google Scholar 

  • Monfort, E., Lopez-Llorca, L. V., Jansson, H. B., et al. (2005). Colonisation of seminal roots of wheat and barley by egg-parasitic nematophagous fungi and their effects on Gaemannomyces graminis var. tritici & development of root-rot. Soil Biology and Biochemistry, 37, 1229–1235.

    Article  CAS  Google Scholar 

  • Palii, C. G., Perez-Iratxeta, C., Yao, Z., et al. (2010). Differential genomic targeting of the transcription factor TAL1 in alternate haematopoietic lineages. The EMBO Journal, 30, 494–509.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pedley, K. F., & Martin, G. B. (2005). Role of mitogen-activated protein kinases in plant immunity. Current Opinion in Plant Biology, 8, 541–547.

    Article  CAS  PubMed  Google Scholar 

  • Peláez, P., & Sanchez, F. (2013). SmallRNAs in plant defense responses during viral and bacterial interactions: Similarities and differences. Frontiers in Plant Science, 4, 343. doi:10.3389/ fpls.2013.00343.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pentimone, I., Lebrón, R., Hackeberg, M., et al. (2015a). Expression profile of non-coding small RNAs in tomato roots during Pochonia chlamydosporia endophytism. Nematropica, 45, 13–14.

    Google Scholar 

  • Pentimone, I., Rosso, L., Nigro, F. et al (2015b, June 7–11) Role and activity of miRNAs in the interaction of tomato roots with endophytic Pochonia chlamydosporia. FEMS, 6th congress of European microbiologists, Maastricht.

    Google Scholar 

  • Pietrantonio, L., Di Cillo, P., Pignoli, G., et al (2013, October 22–23) Green technologies for sustainable management of field crops: Use and potentialities of the fungus Pochonia chlamydosporia. Italian Forum on Industrial Biotechnology and Bioeconomy (IFIB), Naples, Italy.

    Google Scholar 

  • RamÅ¡ak, Ž., Baebler, Å ., Rotter, A., et al. (2014). GoMapMan: Integration, consolidation and visualization of plant gene annotations within the MapMan ontology. Nucleic Acids Research, 42(D1), D1167–D1175.

    Article  PubMed  Google Scholar 

  • Roberts, W. K., & Selitrennikoff, C. P. (1990). Zeamatin, an antifungal protein from maize with membrane-permeabilizing activity. Journal of General Microbiology, 136, 1771–1778.

    Article  CAS  Google Scholar 

  • Rosso, L. C., Finetti-Sialer, M. M., Hirsch, P. R., et al. (2011). Transcriptome analysis shows differential gene expression in the saprotrophic to parasitic transition of Pochonia chlamydosporia. Applied Microbiology and Biotechnology, 90, 1981–1994.

    Article  CAS  PubMed  Google Scholar 

  • Rosso, L. C., Pentimone, I., Colagiero, M., et al. (2013). Expression of Meloidogyne incognita resistance genes induced by endophytic Pochonia chlamydosporia in tomato. Nematropica, 43, 322.

    Google Scholar 

  • Rosso, L. C., Colagiero, M., Salatino, N., et al. (2014). Effect of trophic conditions on gene expression of Pochonia chlamydosporia. The Annals of Applied Biology, 164, 232–243.

    Article  CAS  Google Scholar 

  • Ruiz-Ferrer, V., & Voinnet, O. (2009). Roles of plant small RNAs in biotic stress responses. Annual Review of Plant Biology, 60, 485–510.

    Article  CAS  PubMed  Google Scholar 

  • Schwarz, D. S., Hutvagner, G., Du, T., et al. (2003). Asymmetry in the assembly of the RNAi enzyme complex. Cell, 115, 199e208.

    Article  Google Scholar 

  • Selitrennikoff, C. P. (2001). Antifungal proteins. Applied and Environmental Microbiology, 67, 2883–2894.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tunlid, A., & Jansson, S. (1991). Proteases and their involvement in the infection and immobilization of nematodes by the nematophagous fungus Arthrobotrys oligospora. Applied and Environmental Microbiology, 57, 2868–2872.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ward, E., Kerry, B. R., Manzanilla-López, R. H., et al. (2012). The Pochonia chlamydosporia serine protease gene vcp1 is subject to regulation by carbon, nitrogen and pH: Implications for nematode biocontrol. PloS One, 7, e35657.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weiberg, A., Wang, M., Bellinger, M., et al. (2014). Small RNAs: A new paradigm in plant-microbe interactions. Annual Review of Phytopathology, 52, 495–516.

    Article  CAS  PubMed  Google Scholar 

  • Yang, L., & Huang, H. (2014). Roles of small RNAs in plant disease resistance. Journal of Integrative Plant Biology, 56, 962–970.

    Article  CAS  PubMed  Google Scholar 

  • Zang, C., Schones, D. E., Zeng, C., et al. (2009). A clustering approach for identification of enriched domains from histone modification ChIP-seq data. Bioinformatics, 25, 1952–1958.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Istituto per la Protezione Sostenibile delle Piante, CNR, Via G. Amendola 122/D, 70126, Bari, Italy

    Aurelio Ciancio, Isabella Pentimone, Mariantonietta Colagiero & Laura Rosso

Authors
  1. Aurelio Ciancio
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Isabella Pentimone
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mariantonietta Colagiero
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Laura Rosso
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aurelio Ciancio .

Editor information

Editors and Affiliations

  1. Centro de Desarrollo de Productos Bióticos (Visiting Professor), Instituto Politécnico Nacional (CEPROBI), Yautepec, Morelos, Mexico

    Rosa H. Manzanilla-López

  2. Department of Marine Sciences and Applied Biology, University of Alicante, Alicante, Spain

    Luis V. Lopez-Llorca

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Ciancio, A., Pentimone, I., Colagiero, M., Rosso, L. (2017). Regulatory Factors in Pochonia chlamydosporia-Induced Gene Expression. In: Manzanilla-López, R., Lopez-Llorca, L. (eds) Perspectives in Sustainable Nematode Management Through Pochonia chlamydosporia Applications for Root and Rhizosphere Health. Sustainability in Plant and Crop Protection. Springer, Cham. https://doi.org/10.1007/978-3-319-59224-4_5

Download citation

Publish with us

Policies and ethics

Search

Navigation