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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. 2017 Oct 10; 18(1):764.BG

Abstract

BACKGROUND

How pathogen genomes evolve to support distinct lifestyles is not well-understood. The oomycete Phytophthora infestans, the potato blight agent, is a largely biotrophic pathogen that feeds from living host cells, which become necrotic only late in infection. The related oomycete Pythium ultimum grows saprophytically in soil and as a necrotroph in plants, causing massive tissue destruction. To learn what distinguishes their lifestyles, we compared their gene contents and expression patterns in media and a shared host, potato tuber.

RESULTS

Genes related to pathogenesis varied in temporal expression pattern, mRNA level, and family size between the species. A family's aggregate expression during infection was not proportional to size due to transcriptional remodeling and pseudogenization. Ph. infestans had more stage-specific genes, while Py. ultimum tended towards more constitutive expression. Ph. infestans expressed more genes encoding secreted cell wall-degrading enzymes, but other categories such as secreted proteases and ABC transporters had higher transcript levels in Py. ultimum. Species-specific genes were identified including new Pythium genes, perforins, which may disrupt plant membranes. Genome-wide ortholog analyses identified substantial diversified expression, which correlated with sequence divergence. Pseudogenization was associated with gene family expansion, especially in gene clusters.

CONCLUSION

This first large-scale analysis of transcriptional divergence within oomycetes revealed major shifts in genome composition and expression, including subfunctionalization within gene families. Biotrophy and necrotrophy seem determined by species-specific genes and the varied expression of shared pathogenicity factors, which may be useful targets for crop protection.

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.Department of Plant Pathology and Microbiology, University of California, Riverside, CA, 92521, USA. howard.judelson@ucr.edu.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

29017458

Citation

Ah-Fong, Audrey M V., et al. "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, vol. 18, no. 1, 2017, p. 764.
Ah-Fong AMV, Shrivastava J, Judelson HS. 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. 2017;18(1):764.
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(1), 764. https://doi.org/10.1186/s12864-017-4151-2
Ah-Fong AMV, Shrivastava J, Judelson HS. 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. 2017 Oct 10;18(1):764. PubMed PMID: 29017458.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Lifestyle, gene gain and loss, and transcriptional remodeling cause divergence in the transcriptomes of Phytophthora infestans and Pythium ultimum during potato tuber colonization. AU - Ah-Fong,Audrey M V, AU - Shrivastava,Jolly, AU - Judelson,Howard S, Y1 - 2017/10/10/ PY - 2017/04/28/received PY - 2017/10/02/accepted PY - 2017/10/12/entrez PY - 2017/10/12/pubmed PY - 2018/5/23/medline KW - Comparative genomics KW - Evolution KW - Gene family KW - Oomycete KW - Plant pathogen KW - RNA-seq KW - Regulatory subfunctionalization SP - 764 EP - 764 JF - BMC genomics JO - BMC Genomics VL - 18 IS - 1 N2 - BACKGROUND: How pathogen genomes evolve to support distinct lifestyles is not well-understood. The oomycete Phytophthora infestans, the potato blight agent, is a largely biotrophic pathogen that feeds from living host cells, which become necrotic only late in infection. The related oomycete Pythium ultimum grows saprophytically in soil and as a necrotroph in plants, causing massive tissue destruction. To learn what distinguishes their lifestyles, we compared their gene contents and expression patterns in media and a shared host, potato tuber. RESULTS: Genes related to pathogenesis varied in temporal expression pattern, mRNA level, and family size between the species. A family's aggregate expression during infection was not proportional to size due to transcriptional remodeling and pseudogenization. Ph. infestans had more stage-specific genes, while Py. ultimum tended towards more constitutive expression. Ph. infestans expressed more genes encoding secreted cell wall-degrading enzymes, but other categories such as secreted proteases and ABC transporters had higher transcript levels in Py. ultimum. Species-specific genes were identified including new Pythium genes, perforins, which may disrupt plant membranes. Genome-wide ortholog analyses identified substantial diversified expression, which correlated with sequence divergence. Pseudogenization was associated with gene family expansion, especially in gene clusters. CONCLUSION: This first large-scale analysis of transcriptional divergence within oomycetes revealed major shifts in genome composition and expression, including subfunctionalization within gene families. Biotrophy and necrotrophy seem determined by species-specific genes and the varied expression of shared pathogenicity factors, which may be useful targets for crop protection. SN - 1471-2164 UR - https://www.unboundmedicine.com/medline/citation/29017458/Lifestyle_gene_gain_and_loss_and_transcriptional_remodeling_cause_divergence_in_the_transcriptomes_of_Phytophthora_infestans_and_Pythium_ultimum_during_potato_tuber_colonization_ L2 - https://bmcgenomics.biomedcentral.com/articles/10.1186/s12864-017-4151-2 DB - PRIME DP - Unbound Medicine ER -