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RNA-seq of life stages of the oomycete Phytophthora infestans reveals dynamic changes in metabolic, signal transduction, and pathogenesis genes and a major role for calcium signaling in development.
BMC Genomics. 2017 02 23; 18(1):198.BG

Abstract

BACKGROUND

The oomycete Phytophthora infestans causes the devastating late blight diseases of potato and tomato. P. infestans uses spores for dissemination and infection, like many other filamentous eukaryotic plant pathogens. The expression of a subset of its genes during spore formation and germination were studied previously, but comprehensive genome-wide data have not been available.

RESULTS

RNA-seq was used to profile hyphae, sporangia, sporangia undergoing zoosporogenesis, motile zoospores, and germinated cysts of P. infestans. Parallel studies of two isolates generated robust expression calls for 16,000 of 17,797 predicted genes, with about 250 transcribed in one isolate but not the other. The largest changes occurred in the transition from hyphae to sporangia, when >4200 genes were up-regulated. More than 1350 of these were induced >100-fold, accounting for 26% of total mRNA. Genes encoding calcium-binding proteins, cation channels, signaling proteins, and flagellar proteins were over-represented in genes up-regulated in sporangia. Proteins associated with pathogenicity were transcribed in waves with subclasses induced during zoosporogenesis, in zoospores, or in germinated cysts. Genes involved in most metabolic pathways were down-regulated upon sporulation and reactivated during cyst germination, although there were exceptions such as DNA replication, where transcripts peaked in zoospores. Inhibitor studies indicated that the transcription of two-thirds of genes induced during zoosporogenesis relied on calcium signaling. A sporulation-induced protein kinase was shown to bind a constitutive Gβ-like protein, which contributed to fitness based on knock-down analysis.

CONCLUSIONS

Spore formation and germination involves the staged expression of a large subset of the transcriptome, commensurate with the importance of spores in the life cycle. A comparison of the RNA-seq results with the older microarray data indicated that information is now available for about twice the number of genes than before. Analyses based on function revealed dynamic changes in genes involved in pathogenicity, metabolism, and signaling, with diversity in expression observed within members of multigene families and between isolates. The effects of calcium signaling, a spore-induced protein kinase, and an interacting Gβ-like protein were also demonstrated experimentally. The results reveal aspects of oomycete biology that underly their success as pathogens and potential targets for crop protection chemicals.

Authors+Show Affiliations

Department of Plant Pathology and Microbiology, University of California, Riverside, CA, 92521, USA.Department of Plant Pathology and Microbiology, University of California, Riverside, CA, 92521, USA. Present address: Department of Applied Biology, College of Agriculture and Life Sciences, Kangwon National University, Chuncheon, Korea.Department of Plant Pathology and Microbiology, University of California, Riverside, CA, 92521, USA. howard.judelson@ucr.edu.

Pub Type(s)

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

Language

eng

PubMed ID

28228125

Citation

Ah-Fong, Audrey M V., et al. "RNA-seq of Life Stages of the Oomycete Phytophthora Infestans Reveals Dynamic Changes in Metabolic, Signal Transduction, and Pathogenesis Genes and a Major Role for Calcium Signaling in Development." BMC Genomics, vol. 18, no. 1, 2017, p. 198.
Ah-Fong AM, Kim KS, Judelson HS. RNA-seq of life stages of the oomycete Phytophthora infestans reveals dynamic changes in metabolic, signal transduction, and pathogenesis genes and a major role for calcium signaling in development. BMC Genomics. 2017;18(1):198.
Ah-Fong, A. M., Kim, K. S., & Judelson, H. S. (2017). RNA-seq of life stages of the oomycete Phytophthora infestans reveals dynamic changes in metabolic, signal transduction, and pathogenesis genes and a major role for calcium signaling in development. BMC Genomics, 18(1), 198. https://doi.org/10.1186/s12864-017-3585-x
Ah-Fong AM, Kim KS, Judelson HS. RNA-seq of Life Stages of the Oomycete Phytophthora Infestans Reveals Dynamic Changes in Metabolic, Signal Transduction, and Pathogenesis Genes and a Major Role for Calcium Signaling in Development. BMC Genomics. 2017 02 23;18(1):198. PubMed PMID: 28228125.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - RNA-seq of life stages of the oomycete Phytophthora infestans reveals dynamic changes in metabolic, signal transduction, and pathogenesis genes and a major role for calcium signaling in development. AU - Ah-Fong,Audrey M V, AU - Kim,Kyoung Su, AU - Judelson,Howard S, Y1 - 2017/02/23/ PY - 2016/12/03/received PY - 2017/02/13/accepted PY - 2017/2/24/entrez PY - 2017/2/24/pubmed PY - 2017/9/12/medline KW - Gene regulation KW - Oomycete KW - Spore development KW - Transcriptomics KW - Zoospore SP - 198 EP - 198 JF - BMC genomics JO - BMC Genomics VL - 18 IS - 1 N2 - BACKGROUND: The oomycete Phytophthora infestans causes the devastating late blight diseases of potato and tomato. P. infestans uses spores for dissemination and infection, like many other filamentous eukaryotic plant pathogens. The expression of a subset of its genes during spore formation and germination were studied previously, but comprehensive genome-wide data have not been available. RESULTS: RNA-seq was used to profile hyphae, sporangia, sporangia undergoing zoosporogenesis, motile zoospores, and germinated cysts of P. infestans. Parallel studies of two isolates generated robust expression calls for 16,000 of 17,797 predicted genes, with about 250 transcribed in one isolate but not the other. The largest changes occurred in the transition from hyphae to sporangia, when >4200 genes were up-regulated. More than 1350 of these were induced >100-fold, accounting for 26% of total mRNA. Genes encoding calcium-binding proteins, cation channels, signaling proteins, and flagellar proteins were over-represented in genes up-regulated in sporangia. Proteins associated with pathogenicity were transcribed in waves with subclasses induced during zoosporogenesis, in zoospores, or in germinated cysts. Genes involved in most metabolic pathways were down-regulated upon sporulation and reactivated during cyst germination, although there were exceptions such as DNA replication, where transcripts peaked in zoospores. Inhibitor studies indicated that the transcription of two-thirds of genes induced during zoosporogenesis relied on calcium signaling. A sporulation-induced protein kinase was shown to bind a constitutive Gβ-like protein, which contributed to fitness based on knock-down analysis. CONCLUSIONS: Spore formation and germination involves the staged expression of a large subset of the transcriptome, commensurate with the importance of spores in the life cycle. A comparison of the RNA-seq results with the older microarray data indicated that information is now available for about twice the number of genes than before. Analyses based on function revealed dynamic changes in genes involved in pathogenicity, metabolism, and signaling, with diversity in expression observed within members of multigene families and between isolates. The effects of calcium signaling, a spore-induced protein kinase, and an interacting Gβ-like protein were also demonstrated experimentally. The results reveal aspects of oomycete biology that underly their success as pathogens and potential targets for crop protection chemicals. SN - 1471-2164 UR - https://www.unboundmedicine.com/medline/citation/28228125/RNA_seq_of_life_stages_of_the_oomycete_Phytophthora_infestans_reveals_dynamic_changes_in_metabolic_signal_transduction_and_pathogenesis_genes_and_a_major_role_for_calcium_signaling_in_development_ L2 - https://bmcgenomics.biomedcentral.com/articles/10.1186/s12864-017-3585-x DB - PRIME DP - Unbound Medicine ER -