Developmentally regulated mitochondrial biogenesis and cell death competence in maize pollen
Abstract Background Cytoplasmic male sterility (CMS) is a maternally inherited failure to produce functional pollen that most commonly results from expression of novel, chimeric mitochondrial genes. In Zea mays, cytoplasmic male sterility type S (CMS-S) is characterized by the collapse of immature,...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2022-11-01
|
| Series: | BMC Plant Biology |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12870-022-03897-y |
| _version_ | 1797984590321680384 |
|---|---|
| author | Karen C. Chamusco May N. Milazzo Kanchan S. Bhan Terry L. Kamps Prestina Smith Modupeoluwa Durojaiye Cristina D. Moreira Maria Gallo Christine D. Chase |
| author_facet | Karen C. Chamusco May N. Milazzo Kanchan S. Bhan Terry L. Kamps Prestina Smith Modupeoluwa Durojaiye Cristina D. Moreira Maria Gallo Christine D. Chase |
| author_sort | Karen C. Chamusco |
| collection | DOAJ |
| description | Abstract Background Cytoplasmic male sterility (CMS) is a maternally inherited failure to produce functional pollen that most commonly results from expression of novel, chimeric mitochondrial genes. In Zea mays, cytoplasmic male sterility type S (CMS-S) is characterized by the collapse of immature, bi-cellular pollen. Molecular and cellular features of developing CMS-S and normal (N) cytoplasm pollen were compared to determine the role of mitochondria in these differing developmental fates. Results Terminal deoxynucleotidyl transferase dUTP nick end labeling revealed both chromatin and nuclear fragmentation in the collapsed CMS-S pollen, demonstrating a programmed cell death (PCD) event sharing morphological features with mitochondria-signaled apoptosis in animals. Maize plants expressing mitochondria-targeted green fluorescent protein (GFP) demonstrated dynamic changes in mitochondrial morphology and association with actin filaments through the course of N-cytoplasm pollen development, whereas mitochondrial targeting of GFP was lost and actin filaments were disorganized in developing CMS-S pollen. Immunoblotting revealed significant developmental regulation of mitochondrial biogenesis in both CMS-S and N mito-types. Nuclear and mitochondrial genome encoded components of the cytochrome respiratory pathway and ATP synthase were of low abundance at the microspore stage, but microspores accumulated abundant nuclear-encoded alternative oxidase (AOX). Cytochrome pathway and ATP synthase components accumulated whereas AOX levels declined during the maturation of N bi-cellular pollen. Increased abundance of cytochrome pathway components and declining AOX also characterized collapsed CMS-S pollen. The accumulation and robust RNA editing of mitochondrial transcripts implicated translational or post-translational control for the developmentally regulated accumulation of mitochondria-encoded proteins in both mito-types. Conclusions CMS-S pollen collapse is a PCD event coincident with developmentally programmed mitochondrial events including the accumulation of mitochondrial respiratory proteins and declining protection against mitochondrial generation of reactive oxygen species. |
| first_indexed | 2024-04-11T07:05:14Z |
| format | Article |
| id | doaj.art-0f0beb04e4fa44a78bb9440212895064 |
| institution | Directory Open Access Journal |
| issn | 1471-2229 |
| language | English |
| last_indexed | 2024-04-11T07:05:14Z |
| publishDate | 2022-11-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Plant Biology |
| spelling | doaj.art-0f0beb04e4fa44a78bb94402128950642022-12-22T04:38:25ZengBMCBMC Plant Biology1471-22292022-11-0122111610.1186/s12870-022-03897-yDevelopmentally regulated mitochondrial biogenesis and cell death competence in maize pollenKaren C. Chamusco0May N. Milazzo1Kanchan S. Bhan2Terry L. Kamps3Prestina Smith4Modupeoluwa Durojaiye5Cristina D. Moreira6Maria Gallo7Christine D. Chase8Horticultural Sciences Department, University of FloridaEmergency Department, Baton Rouge General Medical CenterDepartment of Plant Molecular Biology and Biotechnology, Indira Gandhi Agricultural UniversityHorticultural Sciences Department, University of FloridaDivision of Pulmonary, Allergy, Critical Care and Sleep Medicine, Emory University School of MedicineDepartment of Family and Community Medicine, University of Cincinnati College of MedicineDepartment of Biology, University of North Carolina GreensboroDepartment of Plant and Earth Science, University of Wisconsin-River FallsHorticultural Sciences Department, University of FloridaAbstract Background Cytoplasmic male sterility (CMS) is a maternally inherited failure to produce functional pollen that most commonly results from expression of novel, chimeric mitochondrial genes. In Zea mays, cytoplasmic male sterility type S (CMS-S) is characterized by the collapse of immature, bi-cellular pollen. Molecular and cellular features of developing CMS-S and normal (N) cytoplasm pollen were compared to determine the role of mitochondria in these differing developmental fates. Results Terminal deoxynucleotidyl transferase dUTP nick end labeling revealed both chromatin and nuclear fragmentation in the collapsed CMS-S pollen, demonstrating a programmed cell death (PCD) event sharing morphological features with mitochondria-signaled apoptosis in animals. Maize plants expressing mitochondria-targeted green fluorescent protein (GFP) demonstrated dynamic changes in mitochondrial morphology and association with actin filaments through the course of N-cytoplasm pollen development, whereas mitochondrial targeting of GFP was lost and actin filaments were disorganized in developing CMS-S pollen. Immunoblotting revealed significant developmental regulation of mitochondrial biogenesis in both CMS-S and N mito-types. Nuclear and mitochondrial genome encoded components of the cytochrome respiratory pathway and ATP synthase were of low abundance at the microspore stage, but microspores accumulated abundant nuclear-encoded alternative oxidase (AOX). Cytochrome pathway and ATP synthase components accumulated whereas AOX levels declined during the maturation of N bi-cellular pollen. Increased abundance of cytochrome pathway components and declining AOX also characterized collapsed CMS-S pollen. The accumulation and robust RNA editing of mitochondrial transcripts implicated translational or post-translational control for the developmentally regulated accumulation of mitochondria-encoded proteins in both mito-types. Conclusions CMS-S pollen collapse is a PCD event coincident with developmentally programmed mitochondrial events including the accumulation of mitochondrial respiratory proteins and declining protection against mitochondrial generation of reactive oxygen species.https://doi.org/10.1186/s12870-022-03897-yMaizeMitochondriaPollen developmentCytoplasmic male sterilityProgrammed cell death |
| spellingShingle | Karen C. Chamusco May N. Milazzo Kanchan S. Bhan Terry L. Kamps Prestina Smith Modupeoluwa Durojaiye Cristina D. Moreira Maria Gallo Christine D. Chase Developmentally regulated mitochondrial biogenesis and cell death competence in maize pollen BMC Plant Biology Maize Mitochondria Pollen development Cytoplasmic male sterility Programmed cell death |
| title | Developmentally regulated mitochondrial biogenesis and cell death competence in maize pollen |
| title_full | Developmentally regulated mitochondrial biogenesis and cell death competence in maize pollen |
| title_fullStr | Developmentally regulated mitochondrial biogenesis and cell death competence in maize pollen |
| title_full_unstemmed | Developmentally regulated mitochondrial biogenesis and cell death competence in maize pollen |
| title_short | Developmentally regulated mitochondrial biogenesis and cell death competence in maize pollen |
| title_sort | developmentally regulated mitochondrial biogenesis and cell death competence in maize pollen |
| topic | Maize Mitochondria Pollen development Cytoplasmic male sterility Programmed cell death |
| url | https://doi.org/10.1186/s12870-022-03897-y |
| work_keys_str_mv | AT karencchamusco developmentallyregulatedmitochondrialbiogenesisandcelldeathcompetenceinmaizepollen AT maynmilazzo developmentallyregulatedmitochondrialbiogenesisandcelldeathcompetenceinmaizepollen AT kanchansbhan developmentallyregulatedmitochondrialbiogenesisandcelldeathcompetenceinmaizepollen AT terrylkamps developmentallyregulatedmitochondrialbiogenesisandcelldeathcompetenceinmaizepollen AT prestinasmith developmentallyregulatedmitochondrialbiogenesisandcelldeathcompetenceinmaizepollen AT modupeoluwadurojaiye developmentallyregulatedmitochondrialbiogenesisandcelldeathcompetenceinmaizepollen AT cristinadmoreira developmentallyregulatedmitochondrialbiogenesisandcelldeathcompetenceinmaizepollen AT mariagallo developmentallyregulatedmitochondrialbiogenesisandcelldeathcompetenceinmaizepollen AT christinedchase developmentallyregulatedmitochondrialbiogenesisandcelldeathcompetenceinmaizepollen |