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Identification of the genes at S and Z reveals the molecular basis and evolution of grass self-incompatibility

Self-incompatibility (SI) is a feature of many flowering plants, whereby self-pollen is recognized and rejected by the stigma. In grasses (Poaceae), the genes controlling this phenomenon have not been fully elucidated. Grasses have a unique two-locus system, in which two independent genetic loci (S...

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Autores principales: Herridge, Rowan, McCourt, Tyler, Jacobs, Jeanne M. E., Mace, Peter, Brownfield, Lynette, Macknight, Richard
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9623065/
https://www.ncbi.nlm.nih.gov/pubmed/36330270
http://dx.doi.org/10.3389/fpls.2022.1011299
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author Herridge, Rowan
McCourt, Tyler
Jacobs, Jeanne M. E.
Mace, Peter
Brownfield, Lynette
Macknight, Richard
author_facet Herridge, Rowan
McCourt, Tyler
Jacobs, Jeanne M. E.
Mace, Peter
Brownfield, Lynette
Macknight, Richard
author_sort Herridge, Rowan
collection PubMed
description Self-incompatibility (SI) is a feature of many flowering plants, whereby self-pollen is recognized and rejected by the stigma. In grasses (Poaceae), the genes controlling this phenomenon have not been fully elucidated. Grasses have a unique two-locus system, in which two independent genetic loci (S and Z) control self-recognition. S and Z are thought to have arisen from an ancient duplication, common to all grasses. With new chromosome-scale genome data, we examined the genes present at S- and Z-loci, firstly in ryegrass (Lolium perenne), and subsequently in ~20 other grass species. We found that two DUF247 genes and a short unstructured protein (SP/ZP) were present at both S- and Z- in all SI species, while in self-compatible species these genes were often lost or mutated. Expression data suggested that DUF247 genes acted as the male components and SP/ZP were the female components. Consistent with their role in distinguishing self- from non-self, all genes were hypervariable, although key secondary structure features were conserved, including the predicted N-terminal cleavage site of SP/ZP. The evolutionary history of these genes was probed, revealing that specificity groups at the Z-locus arose before the advent of various grass subfamilies/species, while specificity groups at the S-locus arose after the split of Panicoideae, Chloridoideae, Oryzoideae and Pooideae. Finally, we propose a model explaining how the proteins encoded at the S and Z loci might function to specify self-incompatibility.
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spelling pubmed-96230652022-11-02 Identification of the genes at S and Z reveals the molecular basis and evolution of grass self-incompatibility Herridge, Rowan McCourt, Tyler Jacobs, Jeanne M. E. Mace, Peter Brownfield, Lynette Macknight, Richard Front Plant Sci Plant Science Self-incompatibility (SI) is a feature of many flowering plants, whereby self-pollen is recognized and rejected by the stigma. In grasses (Poaceae), the genes controlling this phenomenon have not been fully elucidated. Grasses have a unique two-locus system, in which two independent genetic loci (S and Z) control self-recognition. S and Z are thought to have arisen from an ancient duplication, common to all grasses. With new chromosome-scale genome data, we examined the genes present at S- and Z-loci, firstly in ryegrass (Lolium perenne), and subsequently in ~20 other grass species. We found that two DUF247 genes and a short unstructured protein (SP/ZP) were present at both S- and Z- in all SI species, while in self-compatible species these genes were often lost or mutated. Expression data suggested that DUF247 genes acted as the male components and SP/ZP were the female components. Consistent with their role in distinguishing self- from non-self, all genes were hypervariable, although key secondary structure features were conserved, including the predicted N-terminal cleavage site of SP/ZP. The evolutionary history of these genes was probed, revealing that specificity groups at the Z-locus arose before the advent of various grass subfamilies/species, while specificity groups at the S-locus arose after the split of Panicoideae, Chloridoideae, Oryzoideae and Pooideae. Finally, we propose a model explaining how the proteins encoded at the S and Z loci might function to specify self-incompatibility. Frontiers Media S.A. 2022-10-18 /pmc/articles/PMC9623065/ /pubmed/36330270 http://dx.doi.org/10.3389/fpls.2022.1011299 Text en Copyright © 2022 Herridge, McCourt, Jacobs, Mace, Brownfield and Macknight 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
Herridge, Rowan
McCourt, Tyler
Jacobs, Jeanne M. E.
Mace, Peter
Brownfield, Lynette
Macknight, Richard
Identification of the genes at S and Z reveals the molecular basis and evolution of grass self-incompatibility
title Identification of the genes at S and Z reveals the molecular basis and evolution of grass self-incompatibility
title_full Identification of the genes at S and Z reveals the molecular basis and evolution of grass self-incompatibility
title_fullStr Identification of the genes at S and Z reveals the molecular basis and evolution of grass self-incompatibility
title_full_unstemmed Identification of the genes at S and Z reveals the molecular basis and evolution of grass self-incompatibility
title_short Identification of the genes at S and Z reveals the molecular basis and evolution of grass self-incompatibility
title_sort identification of the genes at s and z reveals the molecular basis and evolution of grass self-incompatibility
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9623065/
https://www.ncbi.nlm.nih.gov/pubmed/36330270
http://dx.doi.org/10.3389/fpls.2022.1011299
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