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Attah, Victoria, Milner, David S., Fang, Yufeng, Yan, Xia, Leonard, Guy, Heitman, Joseph, Talbot, Nicholas J. 
ORCID: https://orcid.org/0000-0001-6434-7757 and Richards, Thomas A.
(2024)
Duplication and neofunctionalization of a horizontally transferred xyloglucanase as a facet of the Red Queen coevolutionary dynamic.
Proceedings of the National Academy of Sciences of the United States of America, 121 (24).
ISSN 0027-8424
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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.
| Item Type: | Article |
|---|---|
| Additional Information: | Data, Materials, and Software Availability: The sequence alignments and underlying data for all plots are available at https://doi.org/10.6084/m9.figshare.21524886. Funding Information: V.A. and this research was supported by a Philip Leverhulme Award (PLP-2014-147) to T.A.R. T.A.R. is supported by a Royal Society University Research Fellowship (URF/R/191005). X.Y. is supported by an award from The Gatsby Charitable Foundation and Biological Sciences Research Council BBS/E/J/000PR9797 to N.J.T. Y.F. and J.H. were supported by NIH/NIAID R01 AI039115-26. |
| Uncontrolled Keywords: | gene duplication,horizontal gene transfer,host parasite interaction,plant cell wall |
| Faculty \ School: | Faculty of Science > The Sainsbury Laboratory |
| UEA Research Groups: | Faculty of Medicine and Health Sciences > Research Centres > Norwich Institute for Healthy Aging |
| Related URLs: | |
| Depositing User: | LivePure Connector |
| Date Deposited: | 24 Oct 2024 09:30 |
| Last Modified: | 17 Dec 2024 01:41 |
| URI: | https://ueaeprints.uea.ac.uk/id/eprint/97177 |
| DOI: | 10.1073/pnas.2218927121 |
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