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Evolution of NLR Resistance Genes in Magnoliids: Dramatic Expansions of CNLs and Multiple Losses of TNLs

Magnoliids are the third-largest group of angiosperms and occupy a critical position in angiosperm evolution. In the past years, due to the lack of sequenced genomes, the disease resistance gene (R gene) profile of magnoliids remains poorly understood. By the genome-wide identification of 1,832 NLR...

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Autores principales: Wu, Jia-Yi, Xue, Jia-Yu, Van de Peer, Yves
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8724549/
https://www.ncbi.nlm.nih.gov/pubmed/34992620
http://dx.doi.org/10.3389/fpls.2021.777157
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author Wu, Jia-Yi
Xue, Jia-Yu
Van de Peer, Yves
author_facet Wu, Jia-Yi
Xue, Jia-Yu
Van de Peer, Yves
author_sort Wu, Jia-Yi
collection PubMed
description Magnoliids are the third-largest group of angiosperms and occupy a critical position in angiosperm evolution. In the past years, due to the lack of sequenced genomes, the disease resistance gene (R gene) profile of magnoliids remains poorly understood. By the genome-wide identification of 1,832 NLR genes from seven magnoliid genomes, we built a framework for the evolution of magnoliid R genes. TNL genes were completely absent from five magnoliids, presumably due to immune pathway deficiencies. A total of 74 ancestral R genes (70 CNLs, 3 TNLs, and 1 RNL) were recovered in a common ancestor of magnoliids, from which all current NLR gene repertoires were derived. Tandem duplication served as the major drive for NLR genes expansion in seven magnoliid genomes, as most surveyed angiosperms. Due to recent rapid expansions, most magnoliids exhibited “a first expansion followed by a slight contraction and a further stronger expansion” evolutionary pattern, while both Litsea cubeba and Persea americana showed a two-times-repeated pattern of “expansion followed by contraction.” The transcriptome analysis of seven different tissues of Saururus chinensis revealed a low expression of most NLR genes, with some R genes displaying a relatively higher expression in roots and fruits. Overall, our study sheds light on the evolution of NLR genes in magnoliids, compensates for insufficiency in major angiosperm lineages, and provides an important reference for a better understanding of angiosperm NLR genes.
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spelling pubmed-87245492022-01-05 Evolution of NLR Resistance Genes in Magnoliids: Dramatic Expansions of CNLs and Multiple Losses of TNLs Wu, Jia-Yi Xue, Jia-Yu Van de Peer, Yves Front Plant Sci Plant Science Magnoliids are the third-largest group of angiosperms and occupy a critical position in angiosperm evolution. In the past years, due to the lack of sequenced genomes, the disease resistance gene (R gene) profile of magnoliids remains poorly understood. By the genome-wide identification of 1,832 NLR genes from seven magnoliid genomes, we built a framework for the evolution of magnoliid R genes. TNL genes were completely absent from five magnoliids, presumably due to immune pathway deficiencies. A total of 74 ancestral R genes (70 CNLs, 3 TNLs, and 1 RNL) were recovered in a common ancestor of magnoliids, from which all current NLR gene repertoires were derived. Tandem duplication served as the major drive for NLR genes expansion in seven magnoliid genomes, as most surveyed angiosperms. Due to recent rapid expansions, most magnoliids exhibited “a first expansion followed by a slight contraction and a further stronger expansion” evolutionary pattern, while both Litsea cubeba and Persea americana showed a two-times-repeated pattern of “expansion followed by contraction.” The transcriptome analysis of seven different tissues of Saururus chinensis revealed a low expression of most NLR genes, with some R genes displaying a relatively higher expression in roots and fruits. Overall, our study sheds light on the evolution of NLR genes in magnoliids, compensates for insufficiency in major angiosperm lineages, and provides an important reference for a better understanding of angiosperm NLR genes. Frontiers Media S.A. 2021-12-21 /pmc/articles/PMC8724549/ /pubmed/34992620 http://dx.doi.org/10.3389/fpls.2021.777157 Text en Copyright © 2021 Wu, Xue and Van de Peer. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Wu, Jia-Yi
Xue, Jia-Yu
Van de Peer, Yves
Evolution of NLR Resistance Genes in Magnoliids: Dramatic Expansions of CNLs and Multiple Losses of TNLs
title Evolution of NLR Resistance Genes in Magnoliids: Dramatic Expansions of CNLs and Multiple Losses of TNLs
title_full Evolution of NLR Resistance Genes in Magnoliids: Dramatic Expansions of CNLs and Multiple Losses of TNLs
title_fullStr Evolution of NLR Resistance Genes in Magnoliids: Dramatic Expansions of CNLs and Multiple Losses of TNLs
title_full_unstemmed Evolution of NLR Resistance Genes in Magnoliids: Dramatic Expansions of CNLs and Multiple Losses of TNLs
title_short Evolution of NLR Resistance Genes in Magnoliids: Dramatic Expansions of CNLs and Multiple Losses of TNLs
title_sort evolution of nlr resistance genes in magnoliids: dramatic expansions of cnls and multiple losses of tnls
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8724549/
https://www.ncbi.nlm.nih.gov/pubmed/34992620
http://dx.doi.org/10.3389/fpls.2021.777157
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