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The kinome of Phytophthora infestans reveals oomycete-specific innovations and links to other taxonomic groups.
BMC Genomics. 2010 Dec 09; 11:700.BG

Abstract

BACKGROUND

Oomycetes are a large group of economically and ecologically important species. Its most notorious member is Phytophthora infestans, the cause of the devastating potato late blight disease. The life cycle of P. infestans involves hyphae which differentiate into spores used for dispersal and host infection. Protein phosphorylation likely plays crucial roles in these stages, and to help understand this we present here a genome-wide analysis of the protein kinases of P. infestans and several relatives. The study also provides new insight into kinase evolution since oomycetes are taxonomically distant from organisms with well-characterized kinomes.

RESULTS

Bioinformatic searches of the genomes of P. infestans, P. ramorum, and P. sojae reveal they have similar kinomes, which for P. infestans contains 354 eukaryotic protein kinases (ePKs) and 18 atypical kinases (aPKs), equaling 2% of total genes. After refining gene models, most were classifiable into families seen in other eukaryotes. Some ePK families are nevertheless unusual, especially the tyrosine kinase-like (TKL) group which includes large oomycete-specific subfamilies. Also identified were two tyrosine kinases, which are rare in non-metazoans. Several ePKs bear accessory domains not identified previously on kinases, such as cyclin-dependent kinases with integral cyclin domains. Most ePKs lack accessory domains, implying that many are regulated transcriptionally. This was confirmed by mRNA expression-profiling studies that showed that two-thirds vary significantly between hyphae, sporangia, and zoospores. Comparisons to neighboring taxa (apicomplexans, ciliates, diatoms) revealed both clade-specific and conserved features, and multiple connections to plant kinases were observed. The kinome of Hyaloperonospora arabidopsidis, an oomycete with a simpler life cycle than P. infestans, was found to be one-third smaller. Some differences may be attributable to gene clustering, which facilitates subfamily expansion (or loss) through unequal crossing-over.

CONCLUSION

The large sizes of the Phytophthora kinomes imply that phosphorylation plays major roles in their life cycles. Their kinomes also include many novel ePKs, some specific to oomycetes or shared with neighboring groups. Little experimentation to date has addressed the biological functions of oomycete kinases, but this should be stimulated by the structural, evolutionary, and expression data presented here. This may lead to targets for disease control.

Authors+Show Affiliations

Department of Plant Pathology and Microbiology, University of California, Riverside, California 92521, USA. howard.judelson@ucr.eduNo affiliation info available

Pub Type(s)

Journal Article
Research Support, U.S. Gov't, Non-P.H.S.

Language

eng

PubMed ID

21143935

Citation

Judelson, Howard S., and Audrey M V. Ah-Fong. "The Kinome of Phytophthora Infestans Reveals Oomycete-specific Innovations and Links to Other Taxonomic Groups." BMC Genomics, vol. 11, 2010, p. 700.
Judelson HS, Ah-Fong AM. The kinome of Phytophthora infestans reveals oomycete-specific innovations and links to other taxonomic groups. BMC Genomics. 2010;11:700.
Judelson, H. S., & Ah-Fong, A. M. (2010). The kinome of Phytophthora infestans reveals oomycete-specific innovations and links to other taxonomic groups. BMC Genomics, 11, 700. https://doi.org/10.1186/1471-2164-11-700
Judelson HS, Ah-Fong AM. The Kinome of Phytophthora Infestans Reveals Oomycete-specific Innovations and Links to Other Taxonomic Groups. BMC Genomics. 2010 Dec 9;11:700. PubMed PMID: 21143935.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - The kinome of Phytophthora infestans reveals oomycete-specific innovations and links to other taxonomic groups. AU - Judelson,Howard S, AU - Ah-Fong,Audrey M V, Y1 - 2010/12/09/ PY - 2010/05/18/received PY - 2010/12/09/accepted PY - 2010/12/15/entrez PY - 2010/12/15/pubmed PY - 2011/3/8/medline SP - 700 EP - 700 JF - BMC genomics JO - BMC Genomics VL - 11 N2 - BACKGROUND: Oomycetes are a large group of economically and ecologically important species. Its most notorious member is Phytophthora infestans, the cause of the devastating potato late blight disease. The life cycle of P. infestans involves hyphae which differentiate into spores used for dispersal and host infection. Protein phosphorylation likely plays crucial roles in these stages, and to help understand this we present here a genome-wide analysis of the protein kinases of P. infestans and several relatives. The study also provides new insight into kinase evolution since oomycetes are taxonomically distant from organisms with well-characterized kinomes. RESULTS: Bioinformatic searches of the genomes of P. infestans, P. ramorum, and P. sojae reveal they have similar kinomes, which for P. infestans contains 354 eukaryotic protein kinases (ePKs) and 18 atypical kinases (aPKs), equaling 2% of total genes. After refining gene models, most were classifiable into families seen in other eukaryotes. Some ePK families are nevertheless unusual, especially the tyrosine kinase-like (TKL) group which includes large oomycete-specific subfamilies. Also identified were two tyrosine kinases, which are rare in non-metazoans. Several ePKs bear accessory domains not identified previously on kinases, such as cyclin-dependent kinases with integral cyclin domains. Most ePKs lack accessory domains, implying that many are regulated transcriptionally. This was confirmed by mRNA expression-profiling studies that showed that two-thirds vary significantly between hyphae, sporangia, and zoospores. Comparisons to neighboring taxa (apicomplexans, ciliates, diatoms) revealed both clade-specific and conserved features, and multiple connections to plant kinases were observed. The kinome of Hyaloperonospora arabidopsidis, an oomycete with a simpler life cycle than P. infestans, was found to be one-third smaller. Some differences may be attributable to gene clustering, which facilitates subfamily expansion (or loss) through unequal crossing-over. CONCLUSION: The large sizes of the Phytophthora kinomes imply that phosphorylation plays major roles in their life cycles. Their kinomes also include many novel ePKs, some specific to oomycetes or shared with neighboring groups. Little experimentation to date has addressed the biological functions of oomycete kinases, but this should be stimulated by the structural, evolutionary, and expression data presented here. This may lead to targets for disease control. SN - 1471-2164 UR - https://www.unboundmedicine.com/medline/citation/21143935/The_kinome_of_Phytophthora_infestans_reveals_oomycete_specific_innovations_and_links_to_other_taxonomic_groups_ L2 - https://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-11-700 DB - PRIME DP - Unbound Medicine ER -