Arabidopsis thaliana MIRO1 and MIRO2 GTPases are unequally redundant in pollen tube growth and fusion of polar nuclei during female gametogenesis.
MIRO GTPases have evolved to regulate mitochondrial trafficking and morphology in eukaryotic organisms. A previous study showed that T-DNA insertion in the Arabidopsis MIRO1 gene is lethal during embryogenesis and affects pollen tube growth and mitochondrial morphology in pollen, whereas T-DNA inser...
| Main Authors: | , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2011-01-01
|
| Series: | PLoS ONE |
| Online Access: | http://europepmc.org/articles/PMC3073945?pdf=render |
| _version_ | 1818024702388469760 |
|---|---|
| author | Christopher G Sørmo Tore Brembu Per Winge Atle M Bones |
| author_facet | Christopher G Sørmo Tore Brembu Per Winge Atle M Bones |
| author_sort | Christopher G Sørmo |
| collection | DOAJ |
| description | MIRO GTPases have evolved to regulate mitochondrial trafficking and morphology in eukaryotic organisms. A previous study showed that T-DNA insertion in the Arabidopsis MIRO1 gene is lethal during embryogenesis and affects pollen tube growth and mitochondrial morphology in pollen, whereas T-DNA insertion in MIRO2 does not affect plant development visibly. Phylogenetic analysis of MIRO from plants revealed that MIRO 1 and 2 orthologs in dicots cluster in two separate groups due to a gene/genome duplication event, suggesting that functional redundancy may exists between the two MIRO genes. To investigate this possibility, we generated miro1(+/-)/miro2-2(-/-) plants. Compared to miro1(+/-) plants, the miro1(+/-)/miro2-2(-/-) plants showed increased segregation distortion. miro1(+/-)/miro2-2(-/-) siliques contained less aborted seeds, but more than 3 times the number of undeveloped ovules. In addition, reciprocal crosses showed that co-transmission through the male gametes was nearly absent, whereas co-transmission through the female gametes was severely reduced in miro1(+/-)/miro2-2(-/-) plants. Further investigations revealed that loss of MIRO2 (miro2(-/-)) function in the miro1(+/-) background enhanced pollen tube growth defects. In developing miro1(+/-)/miro2(-/-) embryo sacs, fusion of polar nuclei was further delayed or impaired compared to miro1 plants. This phenotype has not been reported previously for miro1 plants and coincides with studies showing that defects in some mitochondria-targeted genes results in the same phenotype. Our observations show that loss of function in MIRO2 in a miro1(+/-) background enhances the miro1(+/-) phenotype significantly, even though miro2(-/-) plants alone does not display any phenotypes. Based on these findings, we conclude that MIRO1 and MIRO2 are unequally redundant and that a proportion of the miro1(+/-)/miro2(-/-) plants haploid gametes displays the complete null phenotype of MIRO GTPase function at key developmental stages. |
| first_indexed | 2024-12-10T04:04:25Z |
| format | Article |
| id | doaj.art-bb0743e558ad487b9327eb4d33d338d8 |
| institution | Directory Open Access Journal |
| issn | 1932-6203 |
| language | English |
| last_indexed | 2024-12-10T04:04:25Z |
| publishDate | 2011-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS ONE |
| spelling | doaj.art-bb0743e558ad487b9327eb4d33d338d82022-12-22T02:02:53ZengPublic Library of Science (PLoS)PLoS ONE1932-62032011-01-0164e1853010.1371/journal.pone.0018530Arabidopsis thaliana MIRO1 and MIRO2 GTPases are unequally redundant in pollen tube growth and fusion of polar nuclei during female gametogenesis.Christopher G SørmoTore BrembuPer WingeAtle M BonesMIRO GTPases have evolved to regulate mitochondrial trafficking and morphology in eukaryotic organisms. A previous study showed that T-DNA insertion in the Arabidopsis MIRO1 gene is lethal during embryogenesis and affects pollen tube growth and mitochondrial morphology in pollen, whereas T-DNA insertion in MIRO2 does not affect plant development visibly. Phylogenetic analysis of MIRO from plants revealed that MIRO 1 and 2 orthologs in dicots cluster in two separate groups due to a gene/genome duplication event, suggesting that functional redundancy may exists between the two MIRO genes. To investigate this possibility, we generated miro1(+/-)/miro2-2(-/-) plants. Compared to miro1(+/-) plants, the miro1(+/-)/miro2-2(-/-) plants showed increased segregation distortion. miro1(+/-)/miro2-2(-/-) siliques contained less aborted seeds, but more than 3 times the number of undeveloped ovules. In addition, reciprocal crosses showed that co-transmission through the male gametes was nearly absent, whereas co-transmission through the female gametes was severely reduced in miro1(+/-)/miro2-2(-/-) plants. Further investigations revealed that loss of MIRO2 (miro2(-/-)) function in the miro1(+/-) background enhanced pollen tube growth defects. In developing miro1(+/-)/miro2(-/-) embryo sacs, fusion of polar nuclei was further delayed or impaired compared to miro1 plants. This phenotype has not been reported previously for miro1 plants and coincides with studies showing that defects in some mitochondria-targeted genes results in the same phenotype. Our observations show that loss of function in MIRO2 in a miro1(+/-) background enhances the miro1(+/-) phenotype significantly, even though miro2(-/-) plants alone does not display any phenotypes. Based on these findings, we conclude that MIRO1 and MIRO2 are unequally redundant and that a proportion of the miro1(+/-)/miro2(-/-) plants haploid gametes displays the complete null phenotype of MIRO GTPase function at key developmental stages.http://europepmc.org/articles/PMC3073945?pdf=render |
| spellingShingle | Christopher G Sørmo Tore Brembu Per Winge Atle M Bones Arabidopsis thaliana MIRO1 and MIRO2 GTPases are unequally redundant in pollen tube growth and fusion of polar nuclei during female gametogenesis. PLoS ONE |
| title | Arabidopsis thaliana MIRO1 and MIRO2 GTPases are unequally redundant in pollen tube growth and fusion of polar nuclei during female gametogenesis. |
| title_full | Arabidopsis thaliana MIRO1 and MIRO2 GTPases are unequally redundant in pollen tube growth and fusion of polar nuclei during female gametogenesis. |
| title_fullStr | Arabidopsis thaliana MIRO1 and MIRO2 GTPases are unequally redundant in pollen tube growth and fusion of polar nuclei during female gametogenesis. |
| title_full_unstemmed | Arabidopsis thaliana MIRO1 and MIRO2 GTPases are unequally redundant in pollen tube growth and fusion of polar nuclei during female gametogenesis. |
| title_short | Arabidopsis thaliana MIRO1 and MIRO2 GTPases are unequally redundant in pollen tube growth and fusion of polar nuclei during female gametogenesis. |
| title_sort | arabidopsis thaliana miro1 and miro2 gtpases are unequally redundant in pollen tube growth and fusion of polar nuclei during female gametogenesis |
| url | http://europepmc.org/articles/PMC3073945?pdf=render |
| work_keys_str_mv | AT christophergsørmo arabidopsisthalianamiro1andmiro2gtpasesareunequallyredundantinpollentubegrowthandfusionofpolarnucleiduringfemalegametogenesis AT torebrembu arabidopsisthalianamiro1andmiro2gtpasesareunequallyredundantinpollentubegrowthandfusionofpolarnucleiduringfemalegametogenesis AT perwinge arabidopsisthalianamiro1andmiro2gtpasesareunequallyredundantinpollentubegrowthandfusionofpolarnucleiduringfemalegametogenesis AT atlembones arabidopsisthalianamiro1andmiro2gtpasesareunequallyredundantinpollentubegrowthandfusionofpolarnucleiduringfemalegametogenesis |