[KSCI] Korea Science Citation Index Service

http://dx.doi.org/10.4490/algae.2020.35.6.4

The gene repertoire of Pythium porphyrae (Oomycota) suggests an adapted plant pathogen tackling red algae

Badis, Yacine (The Scottish Association for Marine Science, Scottish Marine Institute)
Han, Jong Won (National Marine Biodiversity Institute of Korea)
Klochkova, Tatyana A. (Kamchatka State Technical University, Petropavlovsk-Kamchatsky)
Gachon, Claire M.M. (The Scottish Association for Marine Science, Scottish Marine Institute)
Kim, Gwang Hoon (National Marine Biodiversity Institute of Korea)

Publication Information

ALGAE / v.35, no.2, 2020 , pp. 133-144 More about this Journal

Abstract

Pythium porphyrae is responsible for devastating outbreaks in seaweed farms of Pyropia, the most valuable cultivated seaweed worldwide. While the genus Pythium contains many well studied pathogens, the genome of P. porphyrae has yet to be sequenced. Here we report the first available gene repertoire of P. porphyrae and a preliminary analysis of pathogenicity-related genes. Using ab initio detection strategies, similarity based and manual annotation, we found that the P. porphyrae gene repertoire is similar to classical phytopathogenic Pythium species. This includes the absence of expanded RxLR effector family and the detection of classical pathogenicity-related genes like crinklers, glycoside hydrolases, cellulose-binding elicitor lectin-like proteins and elicitins. We additionally compared this dataset to the proteomes of 8 selected Pythium species. While 34% of the predicted proteome appeared specific to P. porphyrae, we could not attribute specific enzymes to the degradation of red algal biomass. Conversely, we detected several cellulases and a cutinase conserved with plant-pathogenic Pythium species. Together with the recent report of P. porphyrae triggering disease symptoms on several plant species in lab-controlled conditions, our findings add weight to the hypothesis that P. porphyrae is a reformed plant pathogen.

Keywords

aquaculture; disease; oomycete; Pyropia; Pythium; transcriptome;

Citations & Related Records

Reference

1	Sun, F., Kale, S. D., Azurmendi, H. F., Li, D., Tyler, B. M. & Capelluto, D. G. S. 2013. Structural basis for interactions of the Phytophthora sojae RxLR effector Avh5 with phosphatidylinositol 3-phosphate and for host cell entry. Mol. Plant-Microbe Interact. 26:330-344. DOI
2	Tyler, B. M., Tripathy, S., Zhang, X., Dehal, P., Jiang, R. H. Y., Aerts, A., Arredondo, F. D., Baxter, L., Bensasson, D., Beynon, J. L., Chapman, J., Damasceno, C. M. B., Dorrance, A. E., Dou, D., Dickerman, A. W., Dubchak, I. L., Garbelotto, M., Gijzen, M., Gordon, S. G., Govers, F., Grunwald, N. J., Huang, W., Ivors, K. L., Jones, R. W., Kamoun, S., Krampis, K., Lamour, K. H., Lee, M. -K., McDonald, W. H., Medina, M., Meijer, H. J. G., Nordberg, E. K., Maclean, D. J., Ospina-Giraldo, M. D., Morris, P. F., Phuntumart, V., Putnam, N. H., Rash, S., Rose, J. K. C., Sakihama, Y., Salamov, A. A., Savidor, A., Scheuring, C. F., Smith, B. M., Sobral, B. W. S., Terry, A., Torto-Alalibo, T. A., Win, J., Xu, Z., Zhang, H., Grigoriev, I. V., Rokhsar, D. S. & Boore, J. L. 2006. Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313:1261-1266. DOI
3	Van der Plaats-Niterink, A. J. 1981. Monograph of the genus Pythium. Stud. Mycol. 21:1-244.
4	Wawra, S., Trusch, F., Matena, A., Apostolakis, K., Linne, U., Zhukov, I., Stanek, J., Kozminski, W., Davidson, I., Secombes, C. J., Bayer, P. & van West, P. 2017. The RxLR motif of the host targeting effector AVR3a of Phytophthora infestans is cleaved before secretion. Plant Cell 29:1184-1195. DOI
5	Haas, B. J., Kamoun, S., Zody, M. C., Jiang, R. H. Y., Handsaker, R. E., Cano, L. M., Grabherr, M., Kodira, C. D., Raffaele, S., Torto-Alalibo, T., Bozkurt, T. O., Ah-Fong, A. M. V., Alvarado, L., Anderson, V. L., Armstrong, M. R., Avrova, A., Baxter, L., Beynon, J., Boevink, P. C., Bollmann, S. R., Bos, J. I. B., Bulone, V., Cai, G., Cakir, C., Carrington, J. C., Chawner, M., Conti, L., Costanzo, S., Ewan, R., Fahlgren, N., Fischbach, M. A., Fugelstad, J., Gilroy, E. M., Gnerre, S., Green, P. J., Grenville-Briggs, L. J., Griffith, J., Grünwald, N. J., Horn, K., Horner, N. R., Hu, C. -H., Huitema, E., Jeong, D. -H., Jones, A. M. E., Jones, J. D. G., Jones, R. W., Karlsson, E. K., Kunjeti, S. G., Lamour, K., Liu, Z., Ma, L., MacLean, D., Chibucos, M. C., McDonald, H., McWalters, J., Meijer, H. J. G., Morgan, W., Morris, P. F., Munro, C. A., O'Neill, K., Ospina-Giraldo, M., Pinzón, A., Pritchard, L., Ramsahoye, B., Ren, Q., Restrepo, S., Roy, S., Sadanandom, A., Savidor, A., Schornack, S., Schwartz, D. C., Schumann, U. D., Schwessinger, B., Seyer, L., Sharpe, T., Silvar, C., Song, J., Studholme, D. J., Sykes, S., Thines, M., van de Vondervoort, P. J. I., Phuntumart, V., Wawra, S., Weide, R., Win, J., Young, C., Zhou, S., Fry, W., Meyers, B. C., van West, P., Ristaino, J., Govers, F., Birch, P. R. J., Whisson, S. C., Judelson, H. S. & Nusbaum, C. 2009. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461:393-398. DOI
6	Horner, N. R., Grenville-Briggs, L. J. & Van West, P. 2012. The oomycete Pythium oligandrum expresses putative effectors during mycoparasitism of Phytophthora infestans and is amenable to transformation. Fungal Biol. 116:24-41. DOI
7	Jiang, R. H. Y. & Tyler, B. M. 2012. Mechanisms and evolution of virulence in oomycetes. Annu. Rev. Phytopathol. 50:295-318. DOI
8	Kim, G. H., Moon, K. -H., Kim, J. -Y., Shim, J. & Klochkova, T. A. 2014. A revaluation of algal diseases in Korean Pyropia (Porphyra) sea farms and their economic impact. Algae 29:249-265. DOI
9	Klochkova, T. A., Shim, J. B., Hwang, M. S. & Kim, G. H. 2012. Host-parasite interactions and host species susceptibility of the marine oomycete parasite, Olpidiopsis sp., from Korea that infects red algae. J. Appl. Phycol. 24:135-144. DOI
10	Klochkova, T. A., Jung, S. & Kim, G. -H. 2016. Host range and salinity tolerance of Pythium porphyrae may indicate its terrestrial origin. J. Appl. Phycol. 29:371-379. DOI
11	Lee, S. J., Hwang, M. S., Park, M. A., Baek, J. M., Ha, D. -S., Lee, J. E. & Lee, S. -R. 2015. Molecular identification of the algal pathogen Pythium chondricola (Oomycetes) from Pyropia yezoensis (Rhodophyta) using ITS and cox1 markers. Algae 30:217-222. DOI
12	Krajaejun, T., Khositnithikul, R., Lerksuthirat, T., Lowhnoo, T., Rujirawat, T., Petchthong, T., Yingyong, W., Suriyaphol, P., Smittipat, N., Juthayothin, T., Phuntumart, V. & Sullivan, T. D. 2011. Expressed sequence tags reveal genetic diversity and putative virulence factors of the pathogenic oomycete Pythium insidiosum. Fungal Biol. 115:683-696. DOI
13	Krajaejun, T., Kittichotirat, W., Patumcharoenpol, P., Rujirawat, T., Lohnoo, T. & Yingyong, W. 2018. Data on whole genome sequencing of the oomycete Pythium insidiosum strain CBS 101555 from a horse with pythiosis in Brazil. BMC Res. Notes 11:880. DOI
14	Kushwaha, S. K., Vetukuri, R. R. & Grenville-Briggs, L. J. 2017. Draft genome sequence of the mycoparasitic oomycete Pythium oligandrum strain CBS 530.74. Genome Announc. 5:e00346-17.
15	Lee, S. J., Jee, B. Y., Son, M. -H. & Lee, S. -R. 2017. Infection and cox2 sequence of Pythium chondricola (Oomycetes) causing red rot disease in Pyropia yezoensis (Rhodophyta) in Korea. Algae 32:155-160. DOI
16	McGowan, J. & Fitzpatrick, D. A. 2017. Genomic, network, and phylogenetic analysis of the oomycete effector arsenal. mSphere 2:e00408-17.
17	Adhikari, B. N., Hamilton, J. P., Zerillo, M. M., Tisserat, N., Levesque, C. A. & Buell, C. R. 2013. Comparative genomics reveals insight into virulence strategies of plant pathogenic oomycetes. PLoS ONE 8:e75072. DOI
18	Ah-Fong, A. M. V., Shrivastava, J. & Judelson, H. S. 2017. Lifestyle, gene gain and loss, and transcriptional remodeling cause divergence in the transcriptomes of Phytophthora infestans and Pythium ultimum during potato tuber colonization. BMC Genomics 18:764. DOI
19	Levesque, C. A., Brouwer, H., Cano, L., Hamilton, J. P., Holt, C., Huitema, E., Raffaele, S., Robideau, G. P., Thines, M., Win, J., Zerillo, M. M., Beakes, G. W., Boore, J. L., Busam, D., Dumas, B., Ferriera, S., Fuerstenberg, S. I., Gachon, C. M. M., Gaulin, E., Govers, F., Grenville-Briggs, L., Horner, N., Hostetler, J., Jiang, R. H. Y., Johnson, J., Krajaejun, T., Lin, H., Meijer, H. J. G., Moore, B., Morris, P., Phuntmart, V., Puiu, D., Shetty, J., Stajich, J. E., Tripathy, S., Wawra, S., van West, P., Whitty, B. R., Coutinho, P. M., Henrissat, B., Martin, F., Thomas, P. D., Tyler, B. M., De Vries, R. P., Kamoun, S., Yandell, M., Tisserat, N. & Buell, C. R. 2010. Genome sequence of the necrotrophic plant pathogen Pythium ultimum reveals original pathogenicity mechanisms and effector repertoire. Genome Biol. 11:R73. DOI
20	Levesque, C. A. & de Cock, A. W. A. M. 2004. Molecular phylogeny and taxonomy of the genus Pythium. Mycol. Res. 108:1363-1383. DOI
21	Min, X. J., Butler, G., Storms, R. & Tsang, A. 2005. OrfPredictor: predicting protein-coding regions in EST-derived sequences. Nucleic Acids Res. 33:W677-W680. DOI
22	Morgan, W. & Kamoun, S. 2007. RXLR effectors of plant pathogenic oomycetes. Curr. Opin. Microbiol. 10:332-338. DOI
23	Mukai, L. S., Craigie, J. S. & Brown, R. G. 1981. Chemical composition and structure of the cell walls of the conchocelis and thallus phases of Porphyra tenera (Rhodophyceae). J. Phycol. 17:192-198. DOI
24	Petsalaki, E. I., Bagos, P. G., Litou, Z. I. & Hamodrakas, S. J. 2006. PredSL: a tool for the N-terminal sequence-based prediction of protein subcellular localization. Genomics Proteomics Bioinformatics 4:48-55. DOI
25	Berger, H., Yacoub, A., Gerbore, J., Grizard, D., Rey, P., Sessitsch, A. & Compant, S. 2016. Draft genome sequence of biocontrol agent Pythium oligandrum strain Po37, an Ooomycota. Genome Announc. 4:e00215-16.
26	Arasaki, S., Akino, K. & Tomiyama, T. 1968. A comparison of some physiological aspects in a marine Pythium on the host and on the artificial medium. Bull. Misaki Mar. Biol. Inst. Kyoto Univ. 12:203-206.
27	Ascunce, M. S., Huguet-Tapia, J. C., Ortiz-Urquiza, A., Keyhani, N. O., Braun, E. L. & Goss, E. M. 2017. Phylogenomic analysis supports multiple instances of polyphyly in the oomycete peronosporalean lineage. Mol. Phylogenet. Evol. 114:199-211. DOI
28	Bailey, T. L., Boden, M., Buske, F. A., Frith, M., Grant, C. E., Clementi, L., Ren, J., Li, W. W. & Noble, W. S. 2009. MEME Suite: tools for motif discovery and searching. Nucleic Acids Res. 37:W202-W208. DOI
29	Conesa, A. & Gotz, S. 2008. Blast2GO: a comprehensive suite for functional analysis in plant genomics. Int. J. Plant Genomics 2008:619832.
30	Contreras-Moreira, B. & Vinuesa, P. 2013. GET_HOMOLOGUES, a versatile software package for scalable and robust microbial pangenome analysis. Appl. Environ. Microbiol. 79:7696-7701. DOI
31	Qiu, L., Mao, Y., Tang, L., Tang, X. & Mo, Z. 2019. Characterization of Pythium chondricola associated with red rot disease of Pyropia yezoensis (Ueda) (Bangiales, Rhodophyta) from Lianyungang, China. J. Oceanol. Limnol. 37:1102-1112. DOI
32	de Cock, A. W. A. M., Lodhi, A. M., Rintoul, T. L., Bala, K., Robideau, G. P., Abad, Z. G., Coffey, M. D., Shahzad, S. & Levesque, C. A. 2015. Phytopythium: molecular phylogeny and systematics. Persoonia 34:25-39. DOI
33	Demchak, B., Hull, T., Reich, M., Liefeld, T., Smoot, M., Ideker, T. & Mesirov, J. P. 2014. Cytoscape: the network visualization tool for GenomeSpace workflows. F1000Res. 3:151. DOI
34	Eddy, S. R. 2011. Accelerated profile HMM searches. PLoS Comput. Biol. 7:e1002195. DOI
35	Promponas, V. J., Enright, A. J., Tsoka, S., Kreil, D. P., Leroy, C., Hamodrakas, S., Sander, C. & Ouzounis, C. A. 2000. CAST: an iterative algorithm for the complexity analysis of sequence tracts. Bioinformatics 16:915-922. DOI
36	Punta, M., Coggill, P. C., Eberhardt, R. Y., Mistry, J., Tate, J., Boursnell, C., Pang, N., Forslund, K., Ceric, G., Clements, J., Heger, A., Holm, L., Sonnhammer, E. L. L., Eddy, S. R., Bateman, A. & Finn, R. D. 2012. The Pfam protein families database. Nucleic Acids Res. 40:D290-D301. DOI
37	Saunders, D. G. O., Win, J., Cano, L. M., Szabo, L. J., Kamoun, S. & Raffaele, S. 2012. Using hierarchical clustering of secreted protein families to classify and rank candidate effectors of rust fungi. PLoS ONE 7:e29847. DOI
38	Savory, F. R., Milner, D. S., Miles, D. C. & Richards, T. A. 2018. Ancestral function and diversification of a horizontally acquired oomycete carboxylic acid transporter. Mol. Biol. Evol. 35:1887-1900. DOI
39	Schultz-Johansen, M., Bech, P. K., Hennessy, R. C., Glaring, M. A., Barbeyron, T., Czjzek, M. & Stougaard, P. 2018. A novel enzyme portfolio for red algal polysaccharide degradation in the marine bacterium Paraglaciecola hydrolytica S66T encoded in a sizeable polysaccharide utilization locus. Front. Microbiol. 9:839. DOI
40	Simao, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V. & Zdobnov, E. M. 2015. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31:3210-3212. DOI
41	Gachon, C. M. M., Sime-Ngando, T., Strittmatter, M., Chambouvet, A. & Kim, G. H. 2010. Algal diseases: spotlight on a black box. Trends Plant Sci. 15:633-640. DOI
42	Ellis, J. G. & Dodds, P. N. 2011. Showdown at the RXLR motif: serious differences of opinion in how effector proteins from filamentous eukaryotic pathogens enter plant cells. Proc. Natl. Acad. Sci. U. S. A. 108:14381-14382. DOI
43	Enright, A. J., Van Dongen, S. & Ouzounis, C. A. 2002. An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res. 30:1575-1584. DOI
44	Fu, X. T. & Kim, S. M. 2010. Agarase: review of major sources, categories, purification method, enzyme characteristics and applications. Mar. Drugs 8:200-218. DOI
45	Gerlt, J. A., Bouvier, J. T., Davidson, D. B., Imker, H. J., Sadkhin, B., Slater, D. R. & Whalen, K. L. 2015. Enzyme Function Initiative-Enzyme Similarity Tool (EFI-EST): a web tool for generating protein sequence similarity networks. Biochim. Biophys. Acta 1854:1019-1037. DOI
46	Gschloessl, B., Guermeur, Y. & Cock, J. M. 2008. HECTAR: a method to predict subcellular targeting in heterokonts. BMC Bioinformatics 9:393. DOI
47	Sparrow, F. K. 1931. Two new species of Pythium parasitic on green algae. Ann. Bot. 45:257-277. DOI