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A Maize Male Gametophyte-Specific Gene Encodes ZmLARP6c1, a Potential RNA-Binding Protein Required for Competitive Pollen Tube Growth

Members of the La-related protein family (LARPs) contain a conserved La module, which has been associated with RNA-binding activity. Expression of the maize gene GRMZM2G323499/Zm00001d018613, a member of the LARP family, is highly specific to pollen, based on both transcriptomic and proteomic assays...

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Autores principales: Zhou, Lian, Vejlupkova, Zuzana, Warman, Cedar, Fowler, John E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7947365/
https://www.ncbi.nlm.nih.gov/pubmed/33719310
http://dx.doi.org/10.3389/fpls.2021.635244
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author Zhou, Lian
Vejlupkova, Zuzana
Warman, Cedar
Fowler, John E.
author_facet Zhou, Lian
Vejlupkova, Zuzana
Warman, Cedar
Fowler, John E.
author_sort Zhou, Lian
collection PubMed
description Members of the La-related protein family (LARPs) contain a conserved La module, which has been associated with RNA-binding activity. Expression of the maize gene GRMZM2G323499/Zm00001d018613, a member of the LARP family, is highly specific to pollen, based on both transcriptomic and proteomic assays. This suggests a pollen-specific RNA regulatory function for the protein, designated ZmLARP6c1 based on sequence similarity to the LARP6 subfamily in Arabidopsis. To test this hypothesis, a Ds-GFP transposable element insertion in the ZmLarp6c1 gene (tdsgR82C05) was obtained from the Dooner/Du mutant collection. Sequencing confirmed that the Ds-GFP insertion is in an exon, and thus likely interferes with ZmLARP6c1 function. Tracking inheritance of the insertion via its endosperm-expressed GFP indicated that the mutation was associated with reduced transmission from a heterozygous plant when crossed as a male (ranging from 0.5 to 26.5% transmission), but not as a female. Furthermore, this transmission defect was significantly alleviated when less pollen was applied to the silk, reducing competition between mutant and wild-type pollen. Pollen grain diameter measurements and nuclei counts showed no significant differences between wild-type and mutant pollen. However, in vitro, mutant pollen tubes were significantly shorter than those from sibling wild-type plants, and also displayed altered germination dynamics. These results are consistent with the idea that ZmLARP6c1 provides an important regulatory function during the highly competitive progamic phase of male gametophyte development following arrival of the pollen grain on the silk. The conditional, competitive nature of the Zmlarp6c1::Ds male sterility phenotype (i.e., reduced ability to produce progeny seed) points toward new possibilities for genetic control of parentage in crop production.
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spelling pubmed-79473652021-03-12 A Maize Male Gametophyte-Specific Gene Encodes ZmLARP6c1, a Potential RNA-Binding Protein Required for Competitive Pollen Tube Growth Zhou, Lian Vejlupkova, Zuzana Warman, Cedar Fowler, John E. Front Plant Sci Plant Science Members of the La-related protein family (LARPs) contain a conserved La module, which has been associated with RNA-binding activity. Expression of the maize gene GRMZM2G323499/Zm00001d018613, a member of the LARP family, is highly specific to pollen, based on both transcriptomic and proteomic assays. This suggests a pollen-specific RNA regulatory function for the protein, designated ZmLARP6c1 based on sequence similarity to the LARP6 subfamily in Arabidopsis. To test this hypothesis, a Ds-GFP transposable element insertion in the ZmLarp6c1 gene (tdsgR82C05) was obtained from the Dooner/Du mutant collection. Sequencing confirmed that the Ds-GFP insertion is in an exon, and thus likely interferes with ZmLARP6c1 function. Tracking inheritance of the insertion via its endosperm-expressed GFP indicated that the mutation was associated with reduced transmission from a heterozygous plant when crossed as a male (ranging from 0.5 to 26.5% transmission), but not as a female. Furthermore, this transmission defect was significantly alleviated when less pollen was applied to the silk, reducing competition between mutant and wild-type pollen. Pollen grain diameter measurements and nuclei counts showed no significant differences between wild-type and mutant pollen. However, in vitro, mutant pollen tubes were significantly shorter than those from sibling wild-type plants, and also displayed altered germination dynamics. These results are consistent with the idea that ZmLARP6c1 provides an important regulatory function during the highly competitive progamic phase of male gametophyte development following arrival of the pollen grain on the silk. The conditional, competitive nature of the Zmlarp6c1::Ds male sterility phenotype (i.e., reduced ability to produce progeny seed) points toward new possibilities for genetic control of parentage in crop production. Frontiers Media S.A. 2021-02-25 /pmc/articles/PMC7947365/ /pubmed/33719310 http://dx.doi.org/10.3389/fpls.2021.635244 Text en Copyright © 2021 Zhou, Vejlupkova, Warman and Fowler. http://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
Zhou, Lian
Vejlupkova, Zuzana
Warman, Cedar
Fowler, John E.
A Maize Male Gametophyte-Specific Gene Encodes ZmLARP6c1, a Potential RNA-Binding Protein Required for Competitive Pollen Tube Growth
title A Maize Male Gametophyte-Specific Gene Encodes ZmLARP6c1, a Potential RNA-Binding Protein Required for Competitive Pollen Tube Growth
title_full A Maize Male Gametophyte-Specific Gene Encodes ZmLARP6c1, a Potential RNA-Binding Protein Required for Competitive Pollen Tube Growth
title_fullStr A Maize Male Gametophyte-Specific Gene Encodes ZmLARP6c1, a Potential RNA-Binding Protein Required for Competitive Pollen Tube Growth
title_full_unstemmed A Maize Male Gametophyte-Specific Gene Encodes ZmLARP6c1, a Potential RNA-Binding Protein Required for Competitive Pollen Tube Growth
title_short A Maize Male Gametophyte-Specific Gene Encodes ZmLARP6c1, a Potential RNA-Binding Protein Required for Competitive Pollen Tube Growth
title_sort maize male gametophyte-specific gene encodes zmlarp6c1, a potential rna-binding protein required for competitive pollen tube growth
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7947365/
https://www.ncbi.nlm.nih.gov/pubmed/33719310
http://dx.doi.org/10.3389/fpls.2021.635244
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