The mitochondrial orf117Sha gene desynchronizes pollen development and causes pollen abortion in Arabidopsis Sha cytoplasmic male sterility
Cytoplasmic male sterility (CMS) is of major agronomical relevance in hybrid breeding. In gametophytic CMS, abortion of pollen is determined by the grain genotype, while in sporophytic CMS, it is determined by the mother plant genotype. While several CMS mechanisms have been dissected at the molecul...
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| Vydané v: | Journal of experimental botany Ročník 75; číslo 16; s. 4851 |
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| Hlavní autori: | , , , , , , , , , , , , , , |
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28.08.2024
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| Abstract | Cytoplasmic male sterility (CMS) is of major agronomical relevance in hybrid breeding. In gametophytic CMS, abortion of pollen is determined by the grain genotype, while in sporophytic CMS, it is determined by the mother plant genotype. While several CMS mechanisms have been dissected at the molecular level, gametophytic CMS has not been straightforwardly accessible. We used the gametophytic Sha-CMS in Arabidopsis to characterize the cause and process of pollen abortion by implementing in vivo biosensing in single pollen and mitoTALEN mutagenesis. We obtained conclusive evidence that orf117Sha is the CMS-causing gene, despite distinct characteristics from other CMS genes. We measured the in vivo cytosolic ATP content in single pollen, followed pollen development, and analyzed pollen mitochondrial volume in two genotypes that differed only by the presence of the orf117Sha locus. Our results showed that the Sha-CMS is not triggered by ATP deficiency. Instead, we observed desynchronization of a pollen developmental program. Pollen death occurred independently in pollen grains at diverse stages and was preceded by mitochondrial swelling. We conclude that pollen death is grain-autonomous in Sha-CMS and propose that mitochondrial permeability transition, which was previously described as a hallmark of developmental and environmental-triggered cell death programs, precedes pollen death in Sha-CMS. |
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| AbstractList | Cytoplasmic male sterility (CMS) is of major agronomical relevance in hybrid breeding. In gametophytic CMS, abortion of pollen is determined by the grain genotype, while in sporophytic CMS, it is determined by the mother plant genotype. While several CMS mechanisms have been dissected at the molecular level, gametophytic CMS has not been straightforwardly accessible. We used the gametophytic Sha-CMS in Arabidopsis to characterize the cause and process of pollen abortion by implementing in vivo biosensing in single pollen and mitoTALEN mutagenesis. We obtained conclusive evidence that orf117Sha is the CMS-causing gene, despite distinct characteristics from other CMS genes. We measured the in vivo cytosolic ATP content in single pollen, followed pollen development, and analyzed pollen mitochondrial volume in two genotypes that differed only by the presence of the orf117Sha locus. Our results showed that the Sha-CMS is not triggered by ATP deficiency. Instead, we observed desynchronization of a pollen developmental program. Pollen death occurred independently in pollen grains at diverse stages and was preceded by mitochondrial swelling. We conclude that pollen death is grain-autonomous in Sha-CMS and propose that mitochondrial permeability transition, which was previously described as a hallmark of developmental and environmental-triggered cell death programs, precedes pollen death in Sha-CMS.Cytoplasmic male sterility (CMS) is of major agronomical relevance in hybrid breeding. In gametophytic CMS, abortion of pollen is determined by the grain genotype, while in sporophytic CMS, it is determined by the mother plant genotype. While several CMS mechanisms have been dissected at the molecular level, gametophytic CMS has not been straightforwardly accessible. We used the gametophytic Sha-CMS in Arabidopsis to characterize the cause and process of pollen abortion by implementing in vivo biosensing in single pollen and mitoTALEN mutagenesis. We obtained conclusive evidence that orf117Sha is the CMS-causing gene, despite distinct characteristics from other CMS genes. We measured the in vivo cytosolic ATP content in single pollen, followed pollen development, and analyzed pollen mitochondrial volume in two genotypes that differed only by the presence of the orf117Sha locus. Our results showed that the Sha-CMS is not triggered by ATP deficiency. Instead, we observed desynchronization of a pollen developmental program. Pollen death occurred independently in pollen grains at diverse stages and was preceded by mitochondrial swelling. We conclude that pollen death is grain-autonomous in Sha-CMS and propose that mitochondrial permeability transition, which was previously described as a hallmark of developmental and environmental-triggered cell death programs, precedes pollen death in Sha-CMS. Cytoplasmic male sterility (CMS) is of major agronomical relevance in hybrid breeding. In gametophytic CMS, abortion of pollen is determined by the grain genotype, while in sporophytic CMS, it is determined by the mother plant genotype. While several CMS mechanisms have been dissected at the molecular level, gametophytic CMS has not been straightforwardly accessible. We used the gametophytic Sha-CMS in Arabidopsis to characterize the cause and process of pollen abortion by implementing in vivo biosensing in single pollen and mitoTALEN mutagenesis. We obtained conclusive evidence that orf117Sha is the CMS-causing gene, despite distinct characteristics from other CMS genes. We measured the in vivo cytosolic ATP content in single pollen, followed pollen development, and analyzed pollen mitochondrial volume in two genotypes that differed only by the presence of the orf117Sha locus. Our results showed that the Sha-CMS is not triggered by ATP deficiency. Instead, we observed desynchronization of a pollen developmental program. Pollen death occurred independently in pollen grains at diverse stages and was preceded by mitochondrial swelling. We conclude that pollen death is grain-autonomous in Sha-CMS and propose that mitochondrial permeability transition, which was previously described as a hallmark of developmental and environmental-triggered cell death programs, precedes pollen death in Sha-CMS. |
| Author | Schwarzländer, Markus Boussardon, Clément Charif, Delphine Andrey, Philippe Ricou, Anthony Dehaene, Noémie Camilleri, Christine Simon, Matthieu Nietzel, Thomas Arimura, Shin-Ichi Budar, Françoise Brandt, Dennis Vezon, Daniel Gilouppe Taillefer, Clémence Tran, Joseph |
| Author_xml | – sequence: 1 givenname: Noémie surname: Dehaene fullname: Dehaene, Noémie organization: Université Paris-Saclay, INRAE, AgroParisTech, Institut Jean-Pierre Bourgin (IJPB), 78000, Versailles, France – sequence: 2 givenname: Clément orcidid: 0000-0001-8313-3535 surname: Boussardon fullname: Boussardon, Clément organization: Université Paris-Saclay, INRAE, AgroParisTech, Institut Jean-Pierre Bourgin (IJPB), 78000, Versailles, France – sequence: 3 givenname: Philippe orcidid: 0000-0001-5932-6863 surname: Andrey fullname: Andrey, Philippe organization: Université Paris-Saclay, INRAE, AgroParisTech, Institut Jean-Pierre Bourgin (IJPB), 78000, Versailles, France – sequence: 4 givenname: Delphine orcidid: 0000-0002-1949-5969 surname: Charif fullname: Charif, Delphine organization: Université Paris-Saclay, INRAE, AgroParisTech, Institut Jean-Pierre Bourgin (IJPB), 78000, Versailles, France – sequence: 5 givenname: Dennis orcidid: 0009-0009-0948-4295 surname: Brandt fullname: Brandt, Dennis organization: Institute of Plant Biology and Biotechnology, University of Münster, Schlossplatz 8, D-48143 Münster, Germany – sequence: 6 givenname: Clémence surname: Gilouppe Taillefer fullname: Gilouppe Taillefer, Clémence organization: Université Paris-Saclay, INRAE, AgroParisTech, Institut Jean-Pierre Bourgin (IJPB), 78000, Versailles, France – sequence: 7 givenname: Thomas orcidid: 0000-0002-1934-1732 surname: Nietzel fullname: Nietzel, Thomas organization: Institute of Plant Biology and Biotechnology, University of Münster, Schlossplatz 8, D-48143 Münster, Germany – sequence: 8 givenname: Anthony surname: Ricou fullname: Ricou, Anthony organization: Université Paris-Saclay, INRAE, AgroParisTech, Institut Jean-Pierre Bourgin (IJPB), 78000, Versailles, France – sequence: 9 givenname: Matthieu surname: Simon fullname: Simon, Matthieu organization: Université Paris-Saclay, INRAE, AgroParisTech, Institut Jean-Pierre Bourgin (IJPB), 78000, Versailles, France – sequence: 10 givenname: Joseph orcidid: 0000-0002-4624-0363 surname: Tran fullname: Tran, Joseph organization: Université Paris-Saclay, INRAE, AgroParisTech, Institut Jean-Pierre Bourgin (IJPB), 78000, Versailles, France – sequence: 11 givenname: Daniel surname: Vezon fullname: Vezon, Daniel organization: Université Paris-Saclay, INRAE, AgroParisTech, Institut Jean-Pierre Bourgin (IJPB), 78000, Versailles, France – sequence: 12 givenname: Christine orcidid: 0000-0002-5535-0281 surname: Camilleri fullname: Camilleri, Christine organization: Université Paris-Saclay, INRAE, AgroParisTech, Institut Jean-Pierre Bourgin (IJPB), 78000, Versailles, France – sequence: 13 givenname: Shin-Ichi orcidid: 0000-0002-9537-1626 surname: Arimura fullname: Arimura, Shin-Ichi organization: Laboratory of Plant Molecular Genetics, Graduate School of Agricultural and Life Science, The University of Tokyo, Tokyo, 113-8657, Japan – sequence: 14 givenname: Markus orcidid: 0000-0003-0796-8308 surname: Schwarzländer fullname: Schwarzländer, Markus organization: Institute of Plant Biology and Biotechnology, University of Münster, Schlossplatz 8, D-48143 Münster, Germany – sequence: 15 givenname: Françoise orcidid: 0000-0002-4328-5670 surname: Budar fullname: Budar, Françoise organization: Université Paris-Saclay, INRAE, AgroParisTech, Institut Jean-Pierre Bourgin (IJPB), 78000, Versailles, France |
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| Keywords | mitoTALEN mutagenesis pollen development cytoplasmic male sterility male germline mitochondrial morphology gametophytic mitochondrial genome ATP content |
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| Snippet | Cytoplasmic male sterility (CMS) is of major agronomical relevance in hybrid breeding. In gametophytic CMS, abortion of pollen is determined by the grain... |
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| SubjectTerms | Arabidopsis - genetics Arabidopsis - growth & development Arabidopsis - physiology Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Genes, Mitochondrial Mitochondria - genetics Mitochondria - metabolism Plant Infertility - genetics Pollen - genetics Pollen - growth & development |
| Title | The mitochondrial orf117Sha gene desynchronizes pollen development and causes pollen abortion in Arabidopsis Sha cytoplasmic male sterility |
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