Albugo candida race diversity, ploidy and host-associated microbes revealed using DNA sequence capture on diseased plants in the field

Agathe Jouet, Diane G. O. Saunders, Mark McMullan, Ben Ward , Oliver Furzer, Florian Jupe, Volkan Cevik, Ingo Hein, Gaëtan J. A. Thilliez, Eric Holub, Cock van Oosterhout, Jonathan D. G. Jones

Research output: Contribution to journalArticle

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Abstract

Physiological races of the oomycete Albugo candida are biotrophic pathogens of diverse plant species, primarily the Brassicaceae, and cause infections that suppress host immunity to other pathogens. However, A. candida race diversity and the consequences of host immunosuppression are poorly understood in the field.

We report a method that enables sequencing of DNA of plant pathogens and plantassociated microbes directly from field samples (Pathogen Enrichment Sequencing: PenSeq). We apply this method to explore race diversity in A. candida and to detect A. candidaassociated microbes in the field (91 A. candida-infected plants).

We show with unprecedented resolution that each host plant species supports colonization by one of 17 distinct phylogenetic lineages, each with an unique repertoire of effector candidate alleles. These data reveal the crucial role of sexual and asexual reproduction, polyploidy and host domestication in A. candida specialization on distinct plant species. Our bait design also enabled phylogenetic assignment of DNA sequences from bacteria and fungi from plants in the field.

This paper shows that targeted sequencing has a great potential for the study of pathogen populations while they are colonizing their hosts. This method could be applied to other microbes, especially to those that cannot be cultured.
Original languageEnglish
Pages (from-to)1529-1543
Number of pages15
JournalNew Phytologist
Volume221
Issue number3
Early online date5 Oct 2018
DOIs
Publication statusPublished - 1 Feb 2019

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Albugo candida
Plant Diseases
Ploidies
ploidy
Candida
microorganisms
nucleotide sequences
plant pathogens
pathogens
Asexual Reproduction
Oomycetes
Plant DNA
Brassicaceae
Polyploidy
asexual reproduction
immunosuppression
phylogeny
pathotypes
domestication
sexual reproduction

Keywords

  • Albugo candida
  • DNA sequence capture
  • microbiome
  • oomycete
  • PenSeq
  • plant–pathogen coevolution
  • suppression of plant defence

Cite this

Jouet, A., Saunders, D. G. O., McMullan, M., Ward , B., Furzer, O., Jupe, F., ... Jones, J. D. G. (2019). Albugo candida race diversity, ploidy and host-associated microbes revealed using DNA sequence capture on diseased plants in the field. New Phytologist, 221(3), 1529-1543. https://doi.org/10.1111/nph.15417
Jouet, Agathe ; Saunders, Diane G. O. ; McMullan, Mark ; Ward , Ben ; Furzer, Oliver ; Jupe, Florian ; Cevik, Volkan ; Hein, Ingo ; Thilliez, Gaëtan J. A. ; Holub, Eric ; Oosterhout, Cock van ; Jones, Jonathan D. G. / Albugo candida race diversity, ploidy and host-associated microbes revealed using DNA sequence capture on diseased plants in the field. In: New Phytologist. 2019 ; Vol. 221, No. 3. pp. 1529-1543.
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abstract = "Physiological races of the oomycete Albugo candida are biotrophic pathogens of diverse plant species, primarily the Brassicaceae, and cause infections that suppress host immunity to other pathogens. However, A. candida race diversity and the consequences of host immunosuppression are poorly understood in the field. We report a method that enables sequencing of DNA of plant pathogens and plantassociated microbes directly from field samples (Pathogen Enrichment Sequencing: PenSeq). We apply this method to explore race diversity in A. candida and to detect A. candidaassociated microbes in the field (91 A. candida-infected plants).We show with unprecedented resolution that each host plant species supports colonization by one of 17 distinct phylogenetic lineages, each with an unique repertoire of effector candidate alleles. These data reveal the crucial role of sexual and asexual reproduction, polyploidy and host domestication in A. candida specialization on distinct plant species. Our bait design also enabled phylogenetic assignment of DNA sequences from bacteria and fungi from plants in the field.This paper shows that targeted sequencing has a great potential for the study of pathogen populations while they are colonizing their hosts. This method could be applied to other microbes, especially to those that cannot be cultured.",
keywords = "Albugo candida, DNA sequence capture, microbiome, oomycete, PenSeq, plant–pathogen coevolution, suppression of plant defence",
author = "Agathe Jouet and Saunders, {Diane G. O.} and Mark McMullan and Ben Ward and Oliver Furzer and Florian Jupe and Volkan Cevik and Ingo Hein and Thilliez, {Ga{\"e}tan J. A.} and Eric Holub and Oosterhout, {Cock van} and Jones, {Jonathan D. G.}",
note = "This work was supported by Earth & Life Alliance Systems (to A.J. and C.v.O); the Gordon and Betty Moore foundation (T2361-W03-H to A.J. and J.D.G.J.); the BBSRC (BB/L011646/1 to E.H. and BB/N02317X/1 to C.v.O.) and by the Norwich Biosciences Institutes Computing infrastructure for Science (CiS) group. Reads generated using PenSeq were made publicly available at the European Nucleotide Archive (ENA) under the study accession number: PRJEB21033. We thank Tove H Jorgensen (Aarhus University, Arhus, Denmark), Ulrike Miersch and Annemarie Lokerse (Rijk Zwaan, De Lier, the Netherlands), Deepak Pental and Abha Agnihotri (University of Delhi and Amity University, India, respectively), Hossein Borhan (Agriculture and Agri-Food Canada, Saskatoon), Yan Ma and Chih-Hang Wu (The Sainsbury Laboratory, Norwich, UK), Mark Wilson (through the White Rust Survey website: http://agathejouet.wixsite.com/white-rust-survey) and Quentin Dupriez for collecting A. candida samples. Thanks to Marco Thines and Young-Joon Choi for their help with A. candida samples collection (Goethe University, Frankfurt, Germany).",
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Jouet, A, Saunders, DGO, McMullan, M, Ward , B, Furzer, O, Jupe, F, Cevik, V, Hein, I, Thilliez, GJA, Holub, E, Oosterhout, CV & Jones, JDG 2019, 'Albugo candida race diversity, ploidy and host-associated microbes revealed using DNA sequence capture on diseased plants in the field', New Phytologist, vol. 221, no. 3, pp. 1529-1543. https://doi.org/10.1111/nph.15417

Albugo candida race diversity, ploidy and host-associated microbes revealed using DNA sequence capture on diseased plants in the field. / Jouet, Agathe ; Saunders, Diane G. O. ; McMullan, Mark ; Ward , Ben ; Furzer, Oliver; Jupe, Florian; Cevik, Volkan ; Hein, Ingo; Thilliez, Gaëtan J. A.; Holub, Eric ; Oosterhout, Cock van ; Jones, Jonathan D. G.

In: New Phytologist, Vol. 221, No. 3, 01.02.2019, p. 1529-1543.

Research output: Contribution to journalArticle

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T1 - Albugo candida race diversity, ploidy and host-associated microbes revealed using DNA sequence capture on diseased plants in the field

AU - Jouet, Agathe

AU - Saunders, Diane G. O.

AU - McMullan, Mark

AU - Ward , Ben

AU - Furzer, Oliver

AU - Jupe, Florian

AU - Cevik, Volkan

AU - Hein, Ingo

AU - Thilliez, Gaëtan J. A.

AU - Holub, Eric

AU - Oosterhout, Cock van

AU - Jones, Jonathan D. G.

N1 - This work was supported by Earth & Life Alliance Systems (to A.J. and C.v.O); the Gordon and Betty Moore foundation (T2361-W03-H to A.J. and J.D.G.J.); the BBSRC (BB/L011646/1 to E.H. and BB/N02317X/1 to C.v.O.) and by the Norwich Biosciences Institutes Computing infrastructure for Science (CiS) group. Reads generated using PenSeq were made publicly available at the European Nucleotide Archive (ENA) under the study accession number: PRJEB21033. We thank Tove H Jorgensen (Aarhus University, Arhus, Denmark), Ulrike Miersch and Annemarie Lokerse (Rijk Zwaan, De Lier, the Netherlands), Deepak Pental and Abha Agnihotri (University of Delhi and Amity University, India, respectively), Hossein Borhan (Agriculture and Agri-Food Canada, Saskatoon), Yan Ma and Chih-Hang Wu (The Sainsbury Laboratory, Norwich, UK), Mark Wilson (through the White Rust Survey website: http://agathejouet.wixsite.com/white-rust-survey) and Quentin Dupriez for collecting A. candida samples. Thanks to Marco Thines and Young-Joon Choi for their help with A. candida samples collection (Goethe University, Frankfurt, Germany).

PY - 2019/2/1

Y1 - 2019/2/1

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AB - Physiological races of the oomycete Albugo candida are biotrophic pathogens of diverse plant species, primarily the Brassicaceae, and cause infections that suppress host immunity to other pathogens. However, A. candida race diversity and the consequences of host immunosuppression are poorly understood in the field. We report a method that enables sequencing of DNA of plant pathogens and plantassociated microbes directly from field samples (Pathogen Enrichment Sequencing: PenSeq). We apply this method to explore race diversity in A. candida and to detect A. candidaassociated microbes in the field (91 A. candida-infected plants).We show with unprecedented resolution that each host plant species supports colonization by one of 17 distinct phylogenetic lineages, each with an unique repertoire of effector candidate alleles. These data reveal the crucial role of sexual and asexual reproduction, polyploidy and host domestication in A. candida specialization on distinct plant species. Our bait design also enabled phylogenetic assignment of DNA sequences from bacteria and fungi from plants in the field.This paper shows that targeted sequencing has a great potential for the study of pathogen populations while they are colonizing their hosts. This method could be applied to other microbes, especially to those that cannot be cultured.

KW - Albugo candida

KW - DNA sequence capture

KW - microbiome

KW - oomycete

KW - PenSeq

KW - plant–pathogen coevolution

KW - suppression of plant defence

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