Fine-mapping and comparative genomic analysis reveal the gene composition at the S and Z self-incompatibility loci in grasses

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Fine-mapping and comparative genomic analysis reveal the gene composition at the S and Z self-incompatibility loci in grasses. / Rohner, Marius ; Manzanares, Chloé; Yates, Steven Andrew et al.

In: Molecular Biology and Evolution, Vol. 40, No. 1, msac259, 04.01.2023.

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Vancouver

Rohner M, Manzanares C, Yates SA, Thorogood D, Copetti D, Lübberstedt T et al. Fine-mapping and comparative genomic analysis reveal the gene composition at the S and Z self-incompatibility loci in grasses. Molecular Biology and Evolution. 2023 Jan 4;40(1):msac259. Epub 2022 Dec 8. doi: 10.1093/molbev/msac259, 10.5281/zenodo.7289792, 10.5281/zenodo.7015164, 10.5281/zenodo.7290695

Author

Rohner, Marius ; Manzanares, Chloé ; Yates, Steven Andrew et al. / Fine-mapping and comparative genomic analysis reveal the gene composition at the S and Z self-incompatibility loci in grasses. In: Molecular Biology and Evolution. 2023 ; Vol. 40, No. 1.

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@article{a621aaff021c467e9c3eb789deb0c73d,
title = "Fine-mapping and comparative genomic analysis reveal the gene composition at the S and Z self-incompatibility loci in grasses",
abstract = "Self-incompatibility (SI) is a genetic mechanism of hermaphroditic plants to prevent inbreeding after self-pollination. Allogamous Poaceae species exhibit a unique gametophytic SI system controlled by two multi-allelic and independent loci, S and Z. Despite intense research efforts in the last decades, the genes that determine the initial recognition mechanism are yet to be identified. Here, we report the fine-mapping of the Z-locus in perennial ryegrass (Lolium perenne L.) and provide evidence that the pollen and stigma components are determined by two genes encoding DUF247 domain proteins (ZDUF247-I and ZDUF247-II) and the gene sZ, respectively. The pollen and stigma determinants are located side-by-side and were genetically linked in 10,245 individuals of two independent mapping populations segregating for Z. Moreover, they exhibited high allelic diversity as well as tissue-specific gene expression, matching the expected characteristics of SI determinants known from other systems. Revisiting the S-locus using the latest high-quality whole-genome assemblies revealed a similar gene composition and structure as found for Z, supporting the hypothesis of a duplicated origin of the two-locus SI system of grasses. Ultimately, comparative genomic analyses across a wide range of self-compatible and self-incompatible Poaceae species revealed that the absence of a functional copy of at least one of the six putative SI determinants is accompanied by a self-compatible phenotype. Our study provides new insights into the origin and evolution of the unique gametophytic SI system in one of the largest and economically most important plant families.",
keywords = "Genomics, Lolium/genetics, Plants, Poaceae/genetics, Pollen/genetics",
author = "Marius Rohner and Chlo{\'e} Manzanares and Yates, {Steven Andrew} and Daniel Thorogood and Dario Copetti and Thomas L{\"u}bberstedt and Torben Asp and Bruno Studer",
note = "{\textcopyright} The Author(s) 2022. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.",
year = "2023",
month = jan,
day = "4",
doi = "10.1093/molbev/msac259",
language = "English",
volume = "40",
journal = "Molecular Biology and Evolution",
issn = "0737-4038",
publisher = "Oxford University Press",
number = "1",

}

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TY - JOUR

T1 - Fine-mapping and comparative genomic analysis reveal the gene composition at the S and Z self-incompatibility loci in grasses

AU - Rohner, Marius

AU - Manzanares, Chloé

AU - Yates, Steven Andrew

AU - Thorogood, Daniel

AU - Copetti, Dario

AU - Lübberstedt, Thomas

AU - Asp, Torben

AU - Studer, Bruno

N1 - © The Author(s) 2022. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.

PY - 2023/1/4

Y1 - 2023/1/4

N2 - Self-incompatibility (SI) is a genetic mechanism of hermaphroditic plants to prevent inbreeding after self-pollination. Allogamous Poaceae species exhibit a unique gametophytic SI system controlled by two multi-allelic and independent loci, S and Z. Despite intense research efforts in the last decades, the genes that determine the initial recognition mechanism are yet to be identified. Here, we report the fine-mapping of the Z-locus in perennial ryegrass (Lolium perenne L.) and provide evidence that the pollen and stigma components are determined by two genes encoding DUF247 domain proteins (ZDUF247-I and ZDUF247-II) and the gene sZ, respectively. The pollen and stigma determinants are located side-by-side and were genetically linked in 10,245 individuals of two independent mapping populations segregating for Z. Moreover, they exhibited high allelic diversity as well as tissue-specific gene expression, matching the expected characteristics of SI determinants known from other systems. Revisiting the S-locus using the latest high-quality whole-genome assemblies revealed a similar gene composition and structure as found for Z, supporting the hypothesis of a duplicated origin of the two-locus SI system of grasses. Ultimately, comparative genomic analyses across a wide range of self-compatible and self-incompatible Poaceae species revealed that the absence of a functional copy of at least one of the six putative SI determinants is accompanied by a self-compatible phenotype. Our study provides new insights into the origin and evolution of the unique gametophytic SI system in one of the largest and economically most important plant families.

AB - Self-incompatibility (SI) is a genetic mechanism of hermaphroditic plants to prevent inbreeding after self-pollination. Allogamous Poaceae species exhibit a unique gametophytic SI system controlled by two multi-allelic and independent loci, S and Z. Despite intense research efforts in the last decades, the genes that determine the initial recognition mechanism are yet to be identified. Here, we report the fine-mapping of the Z-locus in perennial ryegrass (Lolium perenne L.) and provide evidence that the pollen and stigma components are determined by two genes encoding DUF247 domain proteins (ZDUF247-I and ZDUF247-II) and the gene sZ, respectively. The pollen and stigma determinants are located side-by-side and were genetically linked in 10,245 individuals of two independent mapping populations segregating for Z. Moreover, they exhibited high allelic diversity as well as tissue-specific gene expression, matching the expected characteristics of SI determinants known from other systems. Revisiting the S-locus using the latest high-quality whole-genome assemblies revealed a similar gene composition and structure as found for Z, supporting the hypothesis of a duplicated origin of the two-locus SI system of grasses. Ultimately, comparative genomic analyses across a wide range of self-compatible and self-incompatible Poaceae species revealed that the absence of a functional copy of at least one of the six putative SI determinants is accompanied by a self-compatible phenotype. Our study provides new insights into the origin and evolution of the unique gametophytic SI system in one of the largest and economically most important plant families.

KW - Genomics

KW - Lolium/genetics

KW - Plants

KW - Poaceae/genetics

KW - Pollen/genetics

UR - http://www.scopus.com/inward/record.url?scp=85145955620&partnerID=8YFLogxK

U2 - 10.1093/molbev/msac259

DO - 10.1093/molbev/msac259

M3 - Article

C2 - 36477354

VL - 40

JO - Molecular Biology and Evolution

JF - Molecular Biology and Evolution

SN - 0737-4038

IS - 1

M1 - msac259

ER -

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