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Putative pathogenicity genes of Phytophthora cinnamomi identified via RNA-Seq analysis of pre-infection structures

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Abstract

Phytophthora cinnamomi is an economically important oomycete that infects more than 3,000 plant species. We aimed to identify the repertoire of genes expressed during pre-infection stages by analysing an RNA-Seq library of cysts and germinating cysts of a P. cinnamomi isolate, originating from Persea americana. Over 70,000 transcripts were identified from 225,049 contigs, assembled from 13 million Illumina paired-end reads. Contaminant sequences were eliminated, resulting in 37,534 transcripts used in further analysis. A total of 1394 transcripts had a putative role in pathogenesis. Genes aiding in detoxification and metabolite transport (cytochrome P450 and ABC transporters) and protection against oxidative stress were most abundant, followed by the genes coding cell wall degrading enzymes. The transcript set included 44 putative RXLR effector genes and genes encoding elicitin and necrosis-inducing proteins. Expression patterns of seven putative pathogenicity genes (encoding RXLR-, necrosis-inducing Phytophthora protein 1 (NPP1), elicitin, polygalacturonase, cellulose binding and elicitor lectin (CBEL), mucin, and adhesion proteins) were assessed across four in vitro developmental stages of P. cinnamomi. High expression of these genes in zoospores suggests their functional importance in the subsequent developmental stage, germination of cysts, implying a role in pre-infection. This work is the first step towards understanding the molecular basis of infection strategies employed by P. cinnamomi.

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References

  • Baxter, L., Tripathy, S., Ishaque, N., Boot, N., Cabral, A., Kemen, E., et al. (2010). Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome. Science, 330(6010), 1549–1551.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bendtsen, J. D., Nielsen, H., von Heijne, G., & Brunak, S. (2004). Improved prediction of signal peptides: SignalP 3.0. Journal of Molecular Biology, 340(4), 783–795.

    Article  PubMed  Google Scholar 

  • Benhamou, N., & Nicole, M. (1999). Cell biology of plant immunization against microbial infection: the potential of induced resistance in controlling plant diseases. Plant Physiology and Biochemistry, 37(10), 703–719.

    Article  CAS  Google Scholar 

  • Blair, J. E., Coffey, M. D., Park, S., Geiser, D. M., & Kang, S. (2008). A multi-locus phylogeny for Phytophthora utilizing markers derived from complete genome sequences. Fungal Genetics and Biology, 45(3), 266–277.

    Article  CAS  PubMed  Google Scholar 

  • Bos, J. I. B., Armstrong, M. R., Gilroy, E. M., Boevink, P. C., Hein, I., Taylor, R. M., et al. (2010). Phytophthora infestans Effector AVR3a is essential for virulence and manipulates plant immunity by stabilizing host E3 ligase CMPG1. Proceedings of the National Academy of Sciences of the United States of America, 107(21), 9909–9914.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bozkurt, T. O., Schornack, S., Win, J., Shindo, T., Ilyas, M., Oliva, R., et al. (2011). Phytophthora infestans Effector AVRblb2 prevents secretion of a plant immune protease at the haustorial interface. Proceedings of the National Academy of Sciences of the United States of America, 108(51), 20832–20837.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cahill, D. M., Rookes, J. E., Wilson, B. A., Gibson, L., & McDougall, K. L. (2008). Phytophthora cinnamomi and Australia's biodiversity: impacts, predictions and progress towards control. Australian Journal of Botany, 56(4), 279–310.

    Article  Google Scholar 

  • Cavalier-Smith, T. (1993). Kingdom protozoa and its 18 phyla. Microbiological Reviews, 57(4), 953–994.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chang, S., Puryear, J., & Cairney, J. (1993). A simple and efficient method for isolating RNA from pine trees. Plant Molecular Biology Reporter, 11(2), 113–116.

    Article  CAS  Google Scholar 

  • Chen, D., & Zentmyer, G. A. (1970). Production of sporangia by Phytophthora cinnamomi in axenic culture. Mycologia, 62(2), 397–402.

    Article  Google Scholar 

  • Chen, X., Shen, G., Wang, Y., Zheng, X., & Wang, Y. (2007). Identification of Phytophthora sojae genes upregulated during the early stage of soybean infection. Federation of European Microbiological Societies Microbiology Letters, 269(2), 280–288.

    Article  CAS  Google Scholar 

  • Chen, X., Klemsdal, S. S., & Brurberg, M. B. (2011). Identification and analysis of Phytophthora cactorum genes up-regulated during cyst germination and strawberry infection. Current Genetics, 57, 297–315.

    Article  CAS  PubMed  Google Scholar 

  • Chen, X. R., Xing, Y. P., Li, Y. P., Tong, Y. H., & Xu, J. Y. (2013). RNA-Seq reveals infection-related gene expression changes in Phytophthora capsici. PloS One, 8(9), e74588.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen, X. R., Zhang, B.-Y., Xing, Y. P., Li, Q. Y., Li, Y. P., Tong, Y. H., et al. (2014). Transcriptomic analysis of the phytopathogenic oomycete Phytophthora cactorum provides insights into infection-related effectors. BMC Genomics, 15(1), 1–24.

    Article  Google Scholar 

  • Chen, X. R., Li, Y. P., Li, Q. Y., Xing, Y. P., Liu, B. B., Tong, Y. H., et al. (2015). SCR96, a small cysteine-rich secretory protein of Phytophthora cactorum, can trigger cell death in the Solanaceae and is important for pathogenicity and oxidative stress tolerance. Molecular Plant Pathology. doi:10.1111/mpp.12303.

    Google Scholar 

  • Darvas, J., Toerien, J., & Milne, D. (1984). Control of avocado root rot by trunk injection with fosetyl-Al. Plant Disease, 68(8), 691–693.

    Article  CAS  Google Scholar 

  • Emanuelsson, O., Brunak, S., von Heijne, G., & Nielsen, H. (2007). Locating proteins in the cell using target P, signal P, and related tools. Nature Protocols, 2(4), 953–971.

    Article  CAS  PubMed  Google Scholar 

  • Gaulin, E., Jauneau, A., Villalba, F., Rickauer, M., Esquerré-Tugayé, M., & Bottin, A. (2002). The CBEL glycoprotein of Phytophthora parasitica Var. nicotianae is involved in cell wall deposition and adhesion to cellulosic substrates. Journal of Cell Science, 115(23), 4565–4575.

    Article  CAS  PubMed  Google Scholar 

  • Gaulin, E., Dramé, N., Lafitte, C., Torto-Alalibo, T., Martinez, Y., Ameline-Torregrosa, C., et al. (2006). Cellulose binding domains of a Phytophthora cell wall protein are novel pathogen-associated molecular patterns. Plant Cell, 18(7), 1766–1777.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grabherr, M. G., Haas, B. J., Yassour, M., Levin, J. Z., Thompson, D. A., Amit, I., et al. (2011). Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology, 29(7), 644–652.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haas, B. J., Kamoun, S., Zody, M. C., Jiang, R. H. Y., Handsaker, R. E., Cano, L. M., et al. (2009). Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature, 461(7262), 393–398.

    Article  CAS  PubMed  Google Scholar 

  • Hardham, A. R. (2005). Phytophthora Cinnamomi. Molecular Plant Pathology, 6(6), 589–604.

    Article  CAS  PubMed  Google Scholar 

  • Have, A., Tenberge, K., Benen, J. E., Tudzynski, P., Visser, J., & Kan, J. L. (2002). The contribution of cell wall degrading enzymes to pathogenesis of fungal plant pathogens. In F. Kempken (Ed.), Agricultural Applications (Vol. 11, pp. 341–358, The Mycota). Berlin Heidelberg: Springer.

  • Hosseini, S., Resjö, S., Liu, Y., Durling, M., Heyman, M., Levander, F., et al. (2015). Comparative proteomic analysis of hyphae and germinating cysts of Phytophthora pisi and Phytophthora sojae. Journal of Proteomics. doi:10.1016/j.jprot.2015.01.006.

    PubMed  Google Scholar 

  • Iseli, C., Jongeneel, C. V., & Bucher, P. (1999). ESTScan: a program for detecting, evaluating, and reconstructing potential coding regions in EST sequences. In Proceedings of the Seventh International Conference on Intelligent Systems for Molecular Biology, 99 (pp. 138–148).

    Google Scholar 

  • Jiang, R. H. Y., Tyler, B. M., Whisson, S. C., Hardham, A. R., & Govers, F. (2006). Ancient origin of elicitin gene clusters in Phytophthora genomes. Molecular Biology and Evolution, 23(2), 338–351.

    Article  CAS  PubMed  Google Scholar 

  • Jiang, R. H. Y., Tripathy, S., Govers, F., & Tyler, B. M. (2008). RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving superfamily with more than 700 members. Proceedings of the National Academy of Sciences. doi:10.1073/pnas.0709303105.

    Google Scholar 

  • Jiang, R. H. Y., de Bruijn, I., Haas, B. J., Belmonte, R., Löbach, L., Christie, J., et al. (2013). Distinctive expansion of potential virulence genes in the genome of the oomycete fish pathogen Saprolegnia parasitica. PLoS Genetics. doi:10.1371/journal.pgen.1003272.

    Google Scholar 

  • Jones, J. D. G., & Dangl, J. L. (2006). The plant immune system. Nature, 444(7117), 323–329.

    Article  CAS  PubMed  Google Scholar 

  • Judelson, H. S., & Tani, S. (2007). Transgene-induced silencing of the zoosporogenesis-specific NIFC gene cluster of Phytophthora infestans involves chromatin alterations. Eukaryotic Cell, 6(7), 1200–1209.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Judelson, H. S., Ah-Fong, A. M. V., Aux, G., Avrova, A. O., Bruce, C., Cakir, C., et al. (2008). Gene expression profiling during asexual development of the late blight pathogen Phytophthora infestans reveals a highly dynamic transcriptome. Molecular Plant-Microbe Interactions, 21(4), 433–447.

    Article  CAS  PubMed  Google Scholar 

  • Kamoun, S., Young, M., Glascock, C., & Tyler, B. M. (1993). Extracellular protein elicitors from Phytophthora: host-specificity and induction of resistance to fungal and bacterial phytopathogens. Molecular Plant-Microbe Interactions, 6(1), 15–25.

    Article  CAS  Google Scholar 

  • Katoh, K., & Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution. doi:10.1093/molbev/mst010.

    PubMed  PubMed Central  Google Scholar 

  • Kebdani, N., Pieuchot, L., Deleury, E., Panabières, F., Le Berre, J. Y., & Gourgues, M. (2010). Cellular and molecular characterization of Phytophthora parasitica appressorium-mediated penetration. New Phytologist, 185(1), 248–257.

    Article  CAS  PubMed  Google Scholar 

  • Kelley, B. S., Lee, S. J., Damasceno, C. M. B., Chakravarthy, S., Kim, B. D., Martin, G. B., et al. (2010). A secreted effector protein (SNE1) from Phytophthora infestans is a broadly acting suppressor of programmed cell death. Plant Journal, 62(3), 357–366.

    Article  CAS  PubMed  Google Scholar 

  • King, M., Reeve, W., Van der Hoek, M. B., Williams, N., McComb, J., O'Brien, P. A., et al. (2010). Defining the phosphite-regulated transcriptome of the plant pathogen Phytophthora cinnamomi. Molecular Genetics and Genomics. doi:10.1007/s00438-010-0579-7.

    PubMed  Google Scholar 

  • Kong, P., Hong, C. X., & Richardson, P. A. (2003). Rapid detection of Phytophthora cinnamomi using PCR with primers derived from the Lpv putative storage protein genes. Plant Pathology, 52(6), 681.

    Article  CAS  Google Scholar 

  • Krajaejun, T., Lerksuthirat, T., Garg, G., Lowhnoo, T., Yingyong, W., Khositnithikul, R., et al. (2014). Transcriptome analysis reveals pathogenicity and evolutionary history of the pathogenic oomycete Pythium insidiosum. Fungal Biology, 118(7), 640–653.

    Article  CAS  PubMed  Google Scholar 

  • Krogh, A., Larsson, B., von Heijne, G., & Sonnhamme, E. (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 

  • Lamour, K. H., Mudge, J., Gobena, D., Hurtado-Gonzales, O. P., Schmutz, J., Kuo, A., et al. (2012). Genome sequencing and mapping reveal loss of heterozygosity as a mechanism for rapid adaptation in the vegetable pathogen Phytophthora capsici. Molecular Plant-Microbe Interactions, 25, 1350–1360.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lévesque, C. A., Brouwer, H., Cano, L., Hamilton, J. P., Holt, C., Huitema, E., et al. (2010). Genome sequence of the necrotrophic plant pathogen Pythium ultimum reveals original pathogenicity mechanisms and effector repertoire. Genome Biology, 11, R37.

    Article  Google Scholar 

  • Misas-Villamil, J. C., & van der Hoorn, R. A. L. (2008). Enzyme–inhibitor interactions at the plant–pathogen interface. Current Opinion in Plant Biology, 11(4), 380–388.

    Article  CAS  PubMed  Google Scholar 

  • Narayan, R. D., Blackman, L. M., Shan, W., & Hardham, A. R. (2010). Phytophthora nicotianae transformants lacking dynein light chain 1 produce non-flagellate zoospores. Fungal Genetics and Biology, 47(8), 663–671.

    Article  CAS  PubMed  Google Scholar 

  • Nicholas, K. B., Nicolas, H. B. Jr., & Deerfield, D. W. II. (1997). Gene Doc: Analysis and visualization of genetic variation. EMBNEW.NEWS, 4, 14.

  • Nielsen, H., & Krogh, A. (1998). Prediction of signal peptides and signal anchors by a hidden Markov model. In Proceedings of the Sixth International Conference on Intelligent Systems for Molecular Biology, 6 (pp. 122–130).

    Google Scholar 

  • OEPP/EPPO (2004). Diagnostic protocols for regulated pests, Phytophthora cinnamomi. Bulletin OEPP/EPPO Bulletin, 34, 155–157.

    Article  Google Scholar 

  • Panabières, F., Amselem, J., Galiana, E., & Le Berre, J. Y. (2005). Gene identification in the oomycete pathogen Phytophthora parasitica during in vitro vegetative growth through expressed sequence tags. Fungal Genetics and Biology, 42(7), 611–623.

    Article  PubMed  Google Scholar 

  • Perez, V., Huet, J. C., O'Donohue, M., Nespoulous, C., & Pernollet, J. C. (1999). A novel elicitin necrotic site revealed by α-cinnamomin sequence and site-directed mutagenesis. Phytochemistry, 50(6), 961–966.

    Article  CAS  PubMed  Google Scholar 

  • Qutob, D., Huitema, E., Gijzen, M., & Kamoun, S. (2003). Variation in structure and activity among elicitins from Phytophthora sojae. Molecular Plant Pathology, 4(2), 119–124.

    Article  CAS  PubMed  Google Scholar 

  • Randall, T. A., Dwyer, R. A., Huitema, E., Beyer, K., Cvitanich, C., Kelkar, H., et al. (2005). Large-scale gene discovery in the oomycete Phytophthora infestans reveals likely components of phytopathogenicity shared with true fungi. Molecular Plant-Microbe Interactions, 18(3), 229–243.

    Article  PubMed  Google Scholar 

  • Rao, V. (1970). Influence of temperature upon growth and sporulation in two species of Phytophthora. Mycopathologia et Mycologia Applicata, 42(1–2), 39–48.

    Article  Google Scholar 

  • Resjö, S., Ali, A., Meijer, H. J., Seidl, M. F., Snel, B., Sandin, M., et al. (2014). Quantitative label-free phosphoproteomics of six different life stages of the late blight pathogen Phytophthora infestans reveals abundant phosphorylation of members of the CRN effector family. Journal of Proteome Research, 13. doi:10.1021/pr4009095.

  • Séjalon-Delmas, N., Villalba Mateos, F., Bottin, A., Rickauer, M., Dargent, R., & Esquerré-Tugayé, M. T. (1997). Purification, elicitor activity, and cell wall localization of a glycoprotein from Phytophthora parasitica Var. nicotianae, a fungal pathogen of tobacco. Phytopathology, 87(9), 899–909.

    Article  PubMed  Google Scholar 

  • Shan, W., Marshall, J. S., & Hardham, A. R. (2004). Gene expression in germinated cysts of Phytophthora nicotianae. Molecular Plant Pathology, 5(4), 317–330.

    Article  CAS  PubMed  Google Scholar 

  • Shearer, B. L., & Crane, C. E. (2012). Phytophthora cinnamomi visible necrotic lesion-colonisation relationships in native flora. Australasian Plant Pathology, 41(6), 633–644.

    Article  Google Scholar 

  • Shearer, B. L., & Fairman, R. G. (2007). A stem injection of phosphite protects Banksia species and Eucalyptus marginata from Phytophthora cinnamomi for at least four years. Australasian Plant Pathology, 36, 78–86.

    Article  CAS  Google Scholar 

  • Stajich, J., Harris, T., Brunk, B., Brestelli, J., Fischer, S., Harb, O., et al. (2012). FungiDB: an integrated functional genomics database for fungi. Nucleic Acids Research, 1(40), D675–D681.

    Article  Google Scholar 

  • Stam, R., Jupe, J., Howden, A. J. M., Morris, J. A., Boevink, P. C., Hedley, P. E., et al. (2013). Identification and characterisation CRN effectors in Phytophthora capsici shows modularity and functional diversity. PloS One. doi:10.1371/journal.pone.0059517.

    Google Scholar 

  • Studholme, D. J., McDougal, R. L., Sambles, C., Hansen, E., Hardy, G., Grant, M., et al. (2016). Genome sequences of six Phytophthora species associated with forests in New Zealand. Genomics Data. doi:10.1016/j.gdata.2015.11.015.

    PubMed  Google Scholar 

  • Tamura, K., Dudley, J., Nei, M., & Kumar, S. (2007). MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24(8), 1596–1599.

    Article  CAS  PubMed  Google Scholar 

  • Torto-Alalibo, T. A., Tripathy, S., Smith, B. M., Arredondo, F. D., Zhou, L., Li, H., et al. (2007). Expressed sequence tags from Phytophthora sojae reveal genes specific to development and infection. Molecular Plant-Microbe Interactions, 20(7), 781–793.

    Article  PubMed  Google Scholar 

  • Tsuda, K., & Katagiri, F. (2010). Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Current Opinion in Plant Biology, 13(4), 459–465.

    Article  CAS  PubMed  Google Scholar 

  • Tyler, B. M., Tripathy, S., Zhang, X., Dehal, P., Jiang, R. H. Y., Aerts, A., et al. (2006). Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science, 313(5791).

  • Untergasser, A., Cutcutache, I., Koressaar, T., Ye, J., Faircloth, B. C., Remm, M., et al. (2012). Primer3 - new capabilities and interfaces. Nucleic Acids Research. doi:10.1093/nar/gks596.

    PubMed  PubMed Central  Google Scholar 

  • Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., et al. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology, 3(7), 1–11.

    Article  Google Scholar 

  • Vauthrin, S., Mikes, V., Milat, M. L., Ponchet, M., Maume, B., Osman, H., et al. (1999). Elicitins trap and transfer sterols from micelles, liposomes and plant plasma membranes. Biochimica et Biophysica Acta, Biomembranes, 1419(2), 335–342.

    Article  CAS  Google Scholar 

  • Wang, Q., Han, C., Ferreira, A. O., Yu, X., Ye, W., Tripathy, S., et al. (2011). Transcriptional programming and functional interactions within the Phytophthora sojae RXLR effector repertoire. Plant Cell, 23(6), 2064–2086.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ward, J. A., Ponnala, L., & Weber, C. A. (2012). Strategies for transcriptome analysis in nonmodel plants. American Journal of Botany, 99(2), 267–276.

    Article  CAS  PubMed  Google Scholar 

  • Whisson, S. C., Boevink, P. C., Moleleki, L., Avrova, A. O., Morales, J. G., Gilroy, E. M., et al. (2007). A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature, 450(7166), 115–118.

    Article  CAS  PubMed  Google Scholar 

  • Win, J., Morgan, W., Bos, J., Krasileva, K. V., Cano, L. M., Chaparro-Garcia, A., et al. (2007). Adaptive evolution has targeted the C-terminal domain of the RXLR effectors of plant pathogenic oomycetes. Plant Signaling & Behavior, 3(4), 251–253.

    Article  Google Scholar 

  • Ye, W., Wang, X., Tao, K., Lu, Y., Dai, T., Dong, S., et al. (2011). Digital gene expression profiling of the Phytophthora sojae transcriptome. Molecular Plant-Microbe Interactions, 24(12), 1530–1539.

    Article  CAS  PubMed  Google Scholar 

  • Zentmyer, G. A. (1961). Attraction of zoospores of Phytophthora cinnamomi to avocado roots. California Avocado Society 1961 Yearbook, 45, 93–95.

  • Zentmyer, G. A. (1980). Phytophthora cinnamomi and the diseases it causes. St. Paul, Minn.: American Phytopathological Society.

    Google Scholar 

  • Zentmyer, G. A., & Mircetich, S. M. (1966). Saprophytism and persistence in soil by Phytophthora cinnamomi. Phytopathology, 56, 710–712.

    Google Scholar 

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Acknowledgments

The financial assistance of the National Research Foundation (NRF) and The Hans Merensky Foundation, towards this research is hereby acknowledged. Opinions expressed and conclusions arrived at, are those of the authors and are not necessarily to be attributed to the NRF and HMF. We thank Paul Birch and Remco Stam (The James Hutton Institute, Scotland) for predicting putative RXLR proteins from contigs generated by Beijing Genomics Institute, and Fourie Joubert and Nanette Christie for assisting with general bioinformatics analysis.

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NvdB and A.R conceived and designed the experiments. A.R conducted the experiments, analysed the data and wrote the manuscript. NvdB and D.K.B provided guidance with data analysis and revised the manuscript. All authors reviewed the manuscript.

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Reitmann, A., Berger, D.K. & van den Berg, N. Putative pathogenicity genes of Phytophthora cinnamomi identified via RNA-Seq analysis of pre-infection structures. Eur J Plant Pathol 147, 211–228 (2017). https://doi.org/10.1007/s10658-016-0993-8

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