Cryoimmobilized anther analysis reveals new ultrastructural insights into Rhynchospora (Cyperaceae) asymmetrical microsporogenesis
IntroductionThe Cyperaceae family is distinguished by holocentric chromosomes and a distinctive microsporogenesis process, which includes inverted meiosis, asymmetric tetrad formation, selective cell death, and the formation of pseudomonad pollen. Despite significant advances, the ultrastructural de...
Saved in:
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2025-01-01
|
| Series: | Frontiers in Plant Science |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2024.1518369/full |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1832592443262894080 |
|---|---|
| author | Danilo M. Rocha Ulla Neumann Fernanda M. Nogueira Georgios Tsipas André L. L. Vanzela André Marques |
| author_facet | Danilo M. Rocha Ulla Neumann Fernanda M. Nogueira Georgios Tsipas André L. L. Vanzela André Marques |
| author_sort | Danilo M. Rocha |
| collection | DOAJ |
| description | IntroductionThe Cyperaceae family is distinguished by holocentric chromosomes and a distinctive microsporogenesis process, which includes inverted meiosis, asymmetric tetrad formation, selective cell death, and the formation of pseudomonad pollen. Despite significant advances, the ultrastructural details of these processes remain poorly understood.MethodsThis study provides a detailed analysis of microsporogenesis in Rhynchospora pubera using high-pressure freezing, freeze substitution, and transmission electron microscopy, significantly enhancing ultrastructural resolution.Results and discussionOur findings reveal that intracellular organization differs from model species Arabidopsis thaliana and drives nuclear selection, with endoplasmic reticulum vesicles organizing meiotic spindles. Microtubules attach to centromeres located deep within holocentric chromosomes, while extensive cytoplasmic connections facilitate material exchange until callose deposition encloses meiocytes. Lipid distribution contributes to cell asymmetry, resulting in the characteristic asymmetric tetrads. Following meiosis, cytoskeletal elements coordinate nuclear migration and cell plate formation. Pseudomonads exhibit reconfigurations in the endomembrane system, particularly involving the endoplasmic reticulum, which supports functional cell differentiation. Complementary histochemical analyses corroborate these findings, providing insights into the cellular processes governing Rhynchospora microsporogenesis. These findings contribute to a deeper understanding of the developmental processes of Cyperaceae pollen, thereby facilitating future investigations of the underlying molecular mechanisms. |
| format | Article |
| id | doaj-art-fbbf01d316ea4b38ab3fc1f4f46f1c18 |
| institution | Kabale University |
| issn | 1664-462X |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj-art-fbbf01d316ea4b38ab3fc1f4f46f1c182025-01-21T08:36:54ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2025-01-011510.3389/fpls.2024.15183691518369Cryoimmobilized anther analysis reveals new ultrastructural insights into Rhynchospora (Cyperaceae) asymmetrical microsporogenesisDanilo M. Rocha0Ulla Neumann1Fernanda M. Nogueira2Georgios Tsipas3André L. L. Vanzela4André Marques5Laboratório de Citogenética e Diversidade Vegetal, Departamento de Biologia Geral, Centro de Ciências Biológicas, Universidade Estadual de Londrina, Londrina, Paraná, BrazilDepartment of Chromosome Biology, Max Planck Institute for Plant Breeding Research, Cologne, GermanyDepartamento de Biologia, Faculdade de Filosofia Ciências e Letras de Ribeirão Preto (FFCLRP) – Universidade de São Paulo—USP, Ribeirão Preto, BrazilDepartment of Chromosome Biology, Max Planck Institute for Plant Breeding Research, Cologne, GermanyLaboratório de Citogenética e Diversidade Vegetal, Departamento de Biologia Geral, Centro de Ciências Biológicas, Universidade Estadual de Londrina, Londrina, Paraná, BrazilDepartment of Chromosome Biology, Max Planck Institute for Plant Breeding Research, Cologne, GermanyIntroductionThe Cyperaceae family is distinguished by holocentric chromosomes and a distinctive microsporogenesis process, which includes inverted meiosis, asymmetric tetrad formation, selective cell death, and the formation of pseudomonad pollen. Despite significant advances, the ultrastructural details of these processes remain poorly understood.MethodsThis study provides a detailed analysis of microsporogenesis in Rhynchospora pubera using high-pressure freezing, freeze substitution, and transmission electron microscopy, significantly enhancing ultrastructural resolution.Results and discussionOur findings reveal that intracellular organization differs from model species Arabidopsis thaliana and drives nuclear selection, with endoplasmic reticulum vesicles organizing meiotic spindles. Microtubules attach to centromeres located deep within holocentric chromosomes, while extensive cytoplasmic connections facilitate material exchange until callose deposition encloses meiocytes. Lipid distribution contributes to cell asymmetry, resulting in the characteristic asymmetric tetrads. Following meiosis, cytoskeletal elements coordinate nuclear migration and cell plate formation. Pseudomonads exhibit reconfigurations in the endomembrane system, particularly involving the endoplasmic reticulum, which supports functional cell differentiation. Complementary histochemical analyses corroborate these findings, providing insights into the cellular processes governing Rhynchospora microsporogenesis. These findings contribute to a deeper understanding of the developmental processes of Cyperaceae pollen, thereby facilitating future investigations of the underlying molecular mechanisms.https://www.frontiersin.org/articles/10.3389/fpls.2024.1518369/fullendoplasmic reticulumhigh-pressure freezinghistochemistrymicrospore mother cellstransmission electron microscopy |
| spellingShingle | Danilo M. Rocha Ulla Neumann Fernanda M. Nogueira Georgios Tsipas André L. L. Vanzela André Marques Cryoimmobilized anther analysis reveals new ultrastructural insights into Rhynchospora (Cyperaceae) asymmetrical microsporogenesis Frontiers in Plant Science endoplasmic reticulum high-pressure freezing histochemistry microspore mother cells transmission electron microscopy |
| title | Cryoimmobilized anther analysis reveals new ultrastructural insights into Rhynchospora (Cyperaceae) asymmetrical microsporogenesis |
| title_full | Cryoimmobilized anther analysis reveals new ultrastructural insights into Rhynchospora (Cyperaceae) asymmetrical microsporogenesis |
| title_fullStr | Cryoimmobilized anther analysis reveals new ultrastructural insights into Rhynchospora (Cyperaceae) asymmetrical microsporogenesis |
| title_full_unstemmed | Cryoimmobilized anther analysis reveals new ultrastructural insights into Rhynchospora (Cyperaceae) asymmetrical microsporogenesis |
| title_short | Cryoimmobilized anther analysis reveals new ultrastructural insights into Rhynchospora (Cyperaceae) asymmetrical microsporogenesis |
| title_sort | cryoimmobilized anther analysis reveals new ultrastructural insights into rhynchospora cyperaceae asymmetrical microsporogenesis |
| topic | endoplasmic reticulum high-pressure freezing histochemistry microspore mother cells transmission electron microscopy |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2024.1518369/full |
| work_keys_str_mv | AT danilomrocha cryoimmobilizedantheranalysisrevealsnewultrastructuralinsightsintorhynchosporacyperaceaeasymmetricalmicrosporogenesis AT ullaneumann cryoimmobilizedantheranalysisrevealsnewultrastructuralinsightsintorhynchosporacyperaceaeasymmetricalmicrosporogenesis AT fernandamnogueira cryoimmobilizedantheranalysisrevealsnewultrastructuralinsightsintorhynchosporacyperaceaeasymmetricalmicrosporogenesis AT georgiostsipas cryoimmobilizedantheranalysisrevealsnewultrastructuralinsightsintorhynchosporacyperaceaeasymmetricalmicrosporogenesis AT andrellvanzela cryoimmobilizedantheranalysisrevealsnewultrastructuralinsightsintorhynchosporacyperaceaeasymmetricalmicrosporogenesis AT andremarques cryoimmobilizedantheranalysisrevealsnewultrastructuralinsightsintorhynchosporacyperaceaeasymmetricalmicrosporogenesis |