Comparative genomics of downy mildews reveals potential adaptations to biotrophy

Kyle Fletcher, Steven J. Klosterman, Lida Derevnina, Frank Martin, Lien D. Bertier, Steven Koike, Sebastian Reyes-Chin-Wo, Beiquan Mou, Richard W Michelmore

Research output: Contribution to journalArticle

6 Citations (Scopus)

Abstract

Background: Spinach downy mildew caused by the oomycete Peronospora effusa is a significant burden on the expanding spinach production industry, especially for organic farms where synthetic fungicides cannot be deployed to control the pathogen. P. effusa is highly variable and 15 new races have been recognized in the past 30 years. Results: We virulence phenotyped, sequenced, and assembled two isolates of P. effusa from the Salinas Valley, California, U.S.A. that were identified as race 13 and 14. These assemblies are high quality in comparison to assemblies of other downy mildews having low total scaffold count (784 & 880), high contig N50s (48 kb & 52 kb), high BUSCO completion and low BUSCO duplication scores and share many syntenic blocks with Phytophthora species. Comparative analysis of four downy mildew and three Phytophthora species revealed parallel absences of genes encoding conserved domains linked to transporters, pathogenesis, and carbohydrate activity in the biotrophic species. Downy mildews surveyed that have lost the ability to produce zoospores have a common loss of flagella/motor and calcium domain encoding genes. Our phylogenomic data support multiple origins of downy mildews from hemibiotrophic progenitors and suggest that common gene losses in these downy mildews may be of genes involved in the necrotrophic stages of Phytophthora spp. Conclusions: We present a high-quality draft genome of Peronospora effusa that will serve as a reference for Peronospora spp. We identified several Pfam domains as under-represented in the downy mildews consistent with the loss of zoosporegenesis and necrotrophy. Phylogenomics provides further support for a polyphyletic origin of downy mildews.

Original languageEnglish (US)
Article number5214
JournalBMC Genomics
Volume19
Issue number1
DOIs
StatePublished - Nov 29 2018

Fingerprint

Peronospora
Phytophthora
Genomics
Spinacia oleracea
Genes
Oomycetes
Organic Agriculture
Flagella
Virulence
Industry
Carbohydrates
Genome
Calcium

Keywords

  • Biotrophy
  • Gene loss
  • Genomics
  • Oomycete
  • Peronospora effusa
  • Peronospora farinosa
  • Peronospora lineage
  • Spinach downy mildew

ASJC Scopus subject areas

  • Biotechnology
  • Genetics

Cite this

Fletcher, K., Klosterman, S. J., Derevnina, L., Martin, F., Bertier, L. D., Koike, S., ... Michelmore, R. W. (2018). Comparative genomics of downy mildews reveals potential adaptations to biotrophy. BMC Genomics, 19(1), [5214]. https://doi.org/10.1186/s12864-018-5214-8

Comparative genomics of downy mildews reveals potential adaptations to biotrophy. / Fletcher, Kyle; Klosterman, Steven J.; Derevnina, Lida; Martin, Frank; Bertier, Lien D.; Koike, Steven; Reyes-Chin-Wo, Sebastian; Mou, Beiquan; Michelmore, Richard W.

In: BMC Genomics, Vol. 19, No. 1, 5214, 29.11.2018.

Research output: Contribution to journalArticle

Fletcher, K, Klosterman, SJ, Derevnina, L, Martin, F, Bertier, LD, Koike, S, Reyes-Chin-Wo, S, Mou, B & Michelmore, RW 2018, 'Comparative genomics of downy mildews reveals potential adaptations to biotrophy', BMC Genomics, vol. 19, no. 1, 5214. https://doi.org/10.1186/s12864-018-5214-8
Fletcher K, Klosterman SJ, Derevnina L, Martin F, Bertier LD, Koike S et al. Comparative genomics of downy mildews reveals potential adaptations to biotrophy. BMC Genomics. 2018 Nov 29;19(1). 5214. https://doi.org/10.1186/s12864-018-5214-8
Fletcher, Kyle ; Klosterman, Steven J. ; Derevnina, Lida ; Martin, Frank ; Bertier, Lien D. ; Koike, Steven ; Reyes-Chin-Wo, Sebastian ; Mou, Beiquan ; Michelmore, Richard W. / Comparative genomics of downy mildews reveals potential adaptations to biotrophy. In: BMC Genomics. 2018 ; Vol. 19, No. 1.
@article{53bfa82d709f4ab8a968f7e77fbeac9a,
title = "Comparative genomics of downy mildews reveals potential adaptations to biotrophy",
abstract = "Background: Spinach downy mildew caused by the oomycete Peronospora effusa is a significant burden on the expanding spinach production industry, especially for organic farms where synthetic fungicides cannot be deployed to control the pathogen. P. effusa is highly variable and 15 new races have been recognized in the past 30 years. Results: We virulence phenotyped, sequenced, and assembled two isolates of P. effusa from the Salinas Valley, California, U.S.A. that were identified as race 13 and 14. These assemblies are high quality in comparison to assemblies of other downy mildews having low total scaffold count (784 & 880), high contig N50s (48 kb & 52 kb), high BUSCO completion and low BUSCO duplication scores and share many syntenic blocks with Phytophthora species. Comparative analysis of four downy mildew and three Phytophthora species revealed parallel absences of genes encoding conserved domains linked to transporters, pathogenesis, and carbohydrate activity in the biotrophic species. Downy mildews surveyed that have lost the ability to produce zoospores have a common loss of flagella/motor and calcium domain encoding genes. Our phylogenomic data support multiple origins of downy mildews from hemibiotrophic progenitors and suggest that common gene losses in these downy mildews may be of genes involved in the necrotrophic stages of Phytophthora spp. Conclusions: We present a high-quality draft genome of Peronospora effusa that will serve as a reference for Peronospora spp. We identified several Pfam domains as under-represented in the downy mildews consistent with the loss of zoosporegenesis and necrotrophy. Phylogenomics provides further support for a polyphyletic origin of downy mildews.",
keywords = "Biotrophy, Gene loss, Genomics, Oomycete, Peronospora effusa, Peronospora farinosa, Peronospora lineage, Spinach downy mildew",
author = "Kyle Fletcher and Klosterman, {Steven J.} and Lida Derevnina and Frank Martin and Bertier, {Lien D.} and Steven Koike and Sebastian Reyes-Chin-Wo and Beiquan Mou and Michelmore, {Richard W}",
year = "2018",
month = "11",
day = "29",
doi = "10.1186/s12864-018-5214-8",
language = "English (US)",
volume = "19",
journal = "BMC Genomics",
issn = "1471-2164",
publisher = "BioMed Central",
number = "1",

}

TY - JOUR

T1 - Comparative genomics of downy mildews reveals potential adaptations to biotrophy

AU - Fletcher, Kyle

AU - Klosterman, Steven J.

AU - Derevnina, Lida

AU - Martin, Frank

AU - Bertier, Lien D.

AU - Koike, Steven

AU - Reyes-Chin-Wo, Sebastian

AU - Mou, Beiquan

AU - Michelmore, Richard W

PY - 2018/11/29

Y1 - 2018/11/29

N2 - Background: Spinach downy mildew caused by the oomycete Peronospora effusa is a significant burden on the expanding spinach production industry, especially for organic farms where synthetic fungicides cannot be deployed to control the pathogen. P. effusa is highly variable and 15 new races have been recognized in the past 30 years. Results: We virulence phenotyped, sequenced, and assembled two isolates of P. effusa from the Salinas Valley, California, U.S.A. that were identified as race 13 and 14. These assemblies are high quality in comparison to assemblies of other downy mildews having low total scaffold count (784 & 880), high contig N50s (48 kb & 52 kb), high BUSCO completion and low BUSCO duplication scores and share many syntenic blocks with Phytophthora species. Comparative analysis of four downy mildew and three Phytophthora species revealed parallel absences of genes encoding conserved domains linked to transporters, pathogenesis, and carbohydrate activity in the biotrophic species. Downy mildews surveyed that have lost the ability to produce zoospores have a common loss of flagella/motor and calcium domain encoding genes. Our phylogenomic data support multiple origins of downy mildews from hemibiotrophic progenitors and suggest that common gene losses in these downy mildews may be of genes involved in the necrotrophic stages of Phytophthora spp. Conclusions: We present a high-quality draft genome of Peronospora effusa that will serve as a reference for Peronospora spp. We identified several Pfam domains as under-represented in the downy mildews consistent with the loss of zoosporegenesis and necrotrophy. Phylogenomics provides further support for a polyphyletic origin of downy mildews.

AB - Background: Spinach downy mildew caused by the oomycete Peronospora effusa is a significant burden on the expanding spinach production industry, especially for organic farms where synthetic fungicides cannot be deployed to control the pathogen. P. effusa is highly variable and 15 new races have been recognized in the past 30 years. Results: We virulence phenotyped, sequenced, and assembled two isolates of P. effusa from the Salinas Valley, California, U.S.A. that were identified as race 13 and 14. These assemblies are high quality in comparison to assemblies of other downy mildews having low total scaffold count (784 & 880), high contig N50s (48 kb & 52 kb), high BUSCO completion and low BUSCO duplication scores and share many syntenic blocks with Phytophthora species. Comparative analysis of four downy mildew and three Phytophthora species revealed parallel absences of genes encoding conserved domains linked to transporters, pathogenesis, and carbohydrate activity in the biotrophic species. Downy mildews surveyed that have lost the ability to produce zoospores have a common loss of flagella/motor and calcium domain encoding genes. Our phylogenomic data support multiple origins of downy mildews from hemibiotrophic progenitors and suggest that common gene losses in these downy mildews may be of genes involved in the necrotrophic stages of Phytophthora spp. Conclusions: We present a high-quality draft genome of Peronospora effusa that will serve as a reference for Peronospora spp. We identified several Pfam domains as under-represented in the downy mildews consistent with the loss of zoosporegenesis and necrotrophy. Phylogenomics provides further support for a polyphyletic origin of downy mildews.

KW - Biotrophy

KW - Gene loss

KW - Genomics

KW - Oomycete

KW - Peronospora effusa

KW - Peronospora farinosa

KW - Peronospora lineage

KW - Spinach downy mildew

UR - http://www.scopus.com/inward/record.url?scp=85057561860&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85057561860&partnerID=8YFLogxK

U2 - 10.1186/s12864-018-5214-8

DO - 10.1186/s12864-018-5214-8

M3 - Article

C2 - 30486780

AN - SCOPUS:85057561860

VL - 19

JO - BMC Genomics

JF - BMC Genomics

SN - 1471-2164

IS - 1

M1 - 5214

ER -