Evolutionary analysis of the LORELEI gene family in plants reveals regulatory subfunctionalization

Noble, Jennifer A., Bielski, Nicholas V., Liu, Ming-Che James, DeFalco, Thomas A., Stegmann, Martin, Nelson, Andrew D. L., McNamara, Kara, Sullivan, Brooke, Dinh, Khanhlinh K., Khuu, Nicholas, Hancock, Sarah, Shiu, Shin-Han, Zipfel, Cyril, Cheung, Alice Y., Beilstein, Mark A. and Palanivelu, Ravishankar (2022) Evolutionary analysis of the LORELEI gene family in plants reveals regulatory subfunctionalization. Plant Physiology, 190 (4). pp. 2539-2556. ISSN 0032-0889

Full text not available from this repository. (Request a copy)

Abstract

A signaling complex comprising members of the LORELEI (LRE)-LIKE GPI-anchored protein (LLG) and Catharanthus roseus RECEPTOR-LIKE KINASE 1-LIKE (CrRLK1L) families perceive RAPID ALKALINIZATION FACTOR (RALF) peptides and regulate growth, reproduction, immunity, and stress responses in Arabidopsis (Arabidopsis thaliana). Genes encoding these proteins are members of multigene families in most angiosperms and could generate thousands of signaling complex variants. However, the links between expansion of these gene families and the functional diversification of this critical signaling complex as well as the evolutionary factors underlying the maintenance of gene duplicates remain unknown. Here, we investigated LLG gene family evolution by sampling land plant genomes and explored the function and expression of angiosperm LLGs. We found that LLG diversity within major land plant lineages is primarily due to lineage-specific duplication events, and that these duplications occurred both early in the history of these lineages and more recently. Our complementation and expression analyses showed that expression divergence (i.e. regulatory subfunctionalization), rather than functional divergence, explains the retention of LLG paralogs. Interestingly, all but one monocot and all eudicot species examined had an LLG copy with preferential expression in male reproductive tissues, while the other duplicate copies showed highest levels of expression in female or vegetative tissues. The single LLG copy in Amborella trichopoda is expressed vastly higher in male compared to in female reproductive or vegetative tissues. We propose that expression divergence plays an important role in retention of LLG duplicates in angiosperms.

Item Type: Article
Additional Information: Funding Information: J.A.N. was supported by the following: IGERT Comparative Genomics Program at the University of Arizona (Award ID: 0654435); NSF Graduate Research Fellowship: Grant DGE-1143953; the Boynton Graduate Fellowship; and the University of Arizona Graduate College Office of Diversity and Inclusion. N.V.B. was supported by a University of Arizona Graduate College University Fellowship, an NSF grant to M.A.B. (IOS-1546825), and NIH-funded Institutional Training Grant in Biochemistry and Molecular Biology (T32 GM136536). Additional support for this work was provided by an NSF grant to R.P. (IOS-1146090), University of Arizona Undergraduate Biology Research Program fellowship to S.H. (private donors), and an NSF Science and Technology Center award (DBI-2019674). This work was also supported by the Gatsby Charitable Foundation (C.Z.), the University of Zürich (C.Z.), the European Research Council under the European Union (EU)’s Horizon 2020 research and innovation pro-gramme (grant agreement No 773153, project “IMMUNOPEPTALK”), as well as fellowships from the European Molecular Biology Organization, the Natural Sciences and Engineering Research Council of Canada and the Deutsche Forschungsgemeinschaft (fellowships EMBO-LTF 100-2017 and NSERC PDF-532561-2019 to T.A.D.; DFG STE 2448/1 to M.S.T.). Work in A.Y.C. lab was supported by Natural Science Foundation (IOS-1645854 and MCB-1715764) to A.Y.C. and Hen-Ming Wu, and the National Institute of Food and Agriculture, U.S. Department of Agriculture, the Center for Agriculture, Food, and the Environment under project number MAS00525. The contents are solely the responsibility of the authors and do not necessarily represent the official views of the USDA or NIFA. K.M. was supported by the Torrey Summer Research Scholarship from UMass Plant Biology Program and the Linda Slakey Summer Research Scholarship from UMass BMB department. We also acknowledge funding from NSF pollen RCN grant (MCB0955910) for sponsoring activities and meetings that forged collaborations between A.Y.C. and R.P. labs. Work in the A.D.L.N. lab was supported by the National Science Foundation (PGRP-IOS 2023310 and PGRP-IOS 1758532). Work in the Shiu lab was partly supported by the National Science Foundation (IOS-2107215 and MCB-2210431) and U.S. Department of Energy (Great Lakes Bioenergy Research Center BER DE-SC0018409). Funding Information: J.A.N. was supported by the following: IGERT Comparative Genomics Program at the University of Arizona (Award ID: 0654435); NSF Graduate Research Fellowship: Grant DGE-1143953; the Boynton Graduate Fellowship; and the University of Arizona Graduate College Office of Diversity and Inclusion. N.V.B. was supported by a University of Arizona Graduate College University Fellowship, an NSF grant to M.A.B. (IOS-1546825), and NIH-funded Institutional Training Grant in Biochemistry and Molecular Biology (T32 GM136536). Additional support for this work was provided by an NSF grant to R.P. (IOS-1146090), University of Arizona Undergraduate Biology Research Program fellowship to S.H. (private donors), and an NSF Science and Technology Center award (DBI-2019674). This work was also supported by the Gatsby Charitable Foundation (C.Z.), the University of Zürich (C.Z.), the European Research Council under the European Union (EU)’s Horizon 2020 research and innovation programme (grant agreement No 773153, project “IMMUNO-PEPTALK”), as well as fellowships from the European Molecular Biology Organization, the Natural Sciences and Engineering Research Council of Canada and the Deutsche Forschungsgemeinschaft (fellowships EMBO-LTF 100-2017 and NSERC PDF-532561-2019 to T.A.D.; DFG STE 2448/1 to M.S.T.). Work in A.Y.C. lab was supported by Natural Science Foundation (IOS-1645854 and MCB-1715764) to A.Y.C. and Hen-Ming Wu, and the National Institute of Food and Agriculture, U.S. Department of Agriculture, the Center for Agriculture, Food, and the Environment under project number MAS00525. The contents are solely the responsibility of the authors and do not necessarily represent the official views of the USDA or NIFA. K.M. was supported by the Torrey Summer Research Scholarship from UMass Plant Biology Program and the Linda Slakey Summer Research Scholarship from UMass BMB department. We also acknowledge funding from NSF pollen RCN grant (MCB0955910) for sponsoring activities and meetings that forged collaborations between A.Y.C. and R.P. labs. Work in the A.D.L.N. lab was supported by the National Science Foundation (PGRP-IOS 2023310 and PGRP-IOS 1758532). Work in the Shiu lab was partly supported by the National Science Foundation (IOS-2107215 and MCB-2210431) and U.S. Department of Energy (Great Lakes Bioenergy Research Center BER DE-SC0018409). Publisher Copyright: © American Society of Plant Biologists 2022. All rights reserved.
Uncontrolled Keywords: physiology,genetics,plant science ,/dk/atira/pure/subjectarea/asjc/1300/1314
Faculty \ School: Faculty of Science > The Sainsbury Laboratory
UEA Research Groups: Faculty of Science > Research Groups > Plant Sciences
Related URLs:
Depositing User: LivePure Connector
Date Deposited: 03 Dec 2024 01:35
Last Modified: 03 Dec 2024 01:35
URI: https://ueaeprints.uea.ac.uk/id/eprint/97861
DOI: 10.1093/plphys/kiac444

Actions (login required)

View Item View Item