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Cited by 11Plant Pathogens and ResistancePlant-Microbe Interactions and ImmunityProtist diversity and phylogeny

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Duplication and neofunctionalization of a horizontally transferred xyloglucanase as a facet of the Red Queen coevolutionary dynamic

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Attah, Victoria, Milner, David S., Fang, Yufeng, Yan, Xia, Leonard, Guy, Heitman, Joseph, Talbot, Nicholas J., Richards, Thomas A.·2024·Proceedings of the National Academy of Sciences
DOI 10.1073/pnas.2218927121PMC PMC11181080

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Abstract

Oomycete protists share phenotypic similarities with fungi, including the ability to cause plant diseases, but branch in a distant region of the tree of life. It has been suggested that multiple horizontal gene transfers (HGTs) from fungi-to-oomycetes contributed to the evolution of plant-pathogenic traits. These HGTs are predicted to include secreted proteins that degrade plant cell walls, a barrier to pathogen invasion and a rich source of carbohydrates. Using a combination of phylogenomics and functional assays, we investigate the diversification of a horizontally transferred xyloglucanase gene family in the model oomycete species Phytophthora sojae . Our analyses detect 11 xyloglucanase paralogs retained in P. sojae . Using heterologous expression in yeast, we show consistent evidence that eight of these paralogs have xyloglucanase function, including variants with distinct protein characteristics, such as a long-disordered C-terminal extension that can increase xyloglucanase activity. The functional variants analyzed subtend a phylogenetic node close to the fungi-to-oomycete transfer, suggesting the horizontally transferred gene was a bona fide xyloglucanase. Expression of three xyloglucanase paralogs in Nicotiana benthamiana triggers high-reactive oxygen species (ROS) generation, while others inhibit ROS responses to bacterial immunogens, demonstrating that the paralogs differentially stimulate pattern-triggered immunity. Mass spectrometry of detectable enzymatic products demonstrates that some paralogs catalyze the production of variant breakdown profiles, suggesting that secretion of variant xyloglucanases increases efficiency of xyloglucan breakdown as well as diversifying the damage-associated molecular patterns released. We suggest that this pattern of neofunctionalization and the variant host responses represent an aspect of the Red Queen host–pathogen coevolutionary dynamic.

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Metadata

Authors
Attah, V., Milner, D. S., Fang, Y., Yan, X., Leonard, G., Heitman, J., Talbot, N. J., & Richards, T. A.
Affiliations
  • University of Oxford (GB)
  • Duke Medical Center (US)
  • The Sainsbury Laboratory, University of East Anglia, Norwich Research Park NR4 7UH, United Kingdom
  • University of East Anglia (GB)
Corresponding author
Richards, Thomas A.
ORCID
Venue
Proceedings of the National Academy of Sciences
Publisher
National Academy of Sciences
Published
2024-06-03
Volume
121
Issue
24
Pages
e2218927121-e2218927121
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
DOI
10.1073/pnas.2218927121
PMC
PMC11181080
OpenAlex
W4399281648
Cited by
11
References
2
Citations by year
2026: 3 · 2025: 4 · 2024: 4
FWCI
2.68
Type
journal article
Language
en
Open access
Licence
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion, cc-by-nc-nd)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • PubMed Central (submittedVersion, cc-by-nc-nd)
  • UEA Digital Repository (University of East Anglia) (submittedVersion)
Funders
  • Leverhulme Trust (PLP-2014-147)
  • Royal Society (URF/R/191005)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Pathogens and Resistance
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Protist diversity and phylogeny
Keywords
xyloglucanase, horizontal gene transfer, Phytophthora sojae, neofunctionalization, gene duplication, oomycete, plant-pathogen coevolution, Red Queen hypothesis, plant cell wall degradation, pattern-triggered immunity, reactive oxygen species, damage-associated molecular patterns, paralogs, plant disease

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