Courtship Ritual of Male and Female Nuclei during Fertilization in Neurospora crassa
ABSTRACT Sexual reproduction is a key process influencing the evolution and adaptation of animals, plants, and many eukaryotic microorganisms, such as fungi. However, the sequential cell biology of fertilization and the associated nuclear dynamics after plasmogamy are poorly understood in filamentou...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2021-10-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/Spectrum.00335-21 |
| _version_ | 1818755098063405056 |
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| author | Sylvain Brun Hsiao-Che Kuo Chris E. Jeffree Darren D. Thomson Nick Read |
| author_facet | Sylvain Brun Hsiao-Che Kuo Chris E. Jeffree Darren D. Thomson Nick Read |
| author_sort | Sylvain Brun |
| collection | DOAJ |
| description | ABSTRACT Sexual reproduction is a key process influencing the evolution and adaptation of animals, plants, and many eukaryotic microorganisms, such as fungi. However, the sequential cell biology of fertilization and the associated nuclear dynamics after plasmogamy are poorly understood in filamentous fungi. Using histone-fluorescent parental isolates, we tracked male and female nuclei during fertilization in the model ascomycete Neurospora crassa using live-cell imaging. This study unravels the behavior of trichogyne resident female nuclei and the extraordinary manner in which male nuclei migrate up the trichogyne to the protoperithecium. Our observations raise new fundamental questions about the modus operandi of nucleus movements during sexual reproduction, male and female nuclear identity, guidance of nuclei within the trichogyne and, unexpectedly, the avoidance of “polyspermy” in fungi. The spatiotemporal dynamics of male nuclei within the trichogyne following plasmogamy are also described, where the speed and the deformation of male nuclei are of the most dramatic observed to date in a living organism. IMPORTANCE Using live-cell fluorescence imaging, for the first time we have observed live male and female nuclei during sexual reproduction in the model fungus Neurospora crassa. This study reveals the specific behavior of resident female nuclei within the trichogyne (the female organ) after fertilization and the extraordinary manner in which male nuclei migrate across the trichogyne toward their final destination, the protoperithecium, where karyogamy takes place. Importantly, the speed and deformation of male nuclei were found to be among the most dramatic ever observed in a living organism. Furthermore, we observed that entry of male nuclei into protoperithecia may block the entry of other male nuclei, suggesting that a process analogous to polyspermy avoidance could exist in fungi. Our live-cell imaging approach opens new opportunities for novel research on cell-signaling during sexual reproduction in fungi and, on a broader scale, nuclear dynamics in eukaryotes. |
| first_indexed | 2024-12-18T05:33:44Z |
| format | Article |
| id | doaj.art-c36236eaa3f647c2931ae96029fe4098 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-12-18T05:33:44Z |
| publishDate | 2021-10-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-c36236eaa3f647c2931ae96029fe40982022-12-21T21:19:22ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972021-10-019210.1128/Spectrum.00335-21Courtship Ritual of Male and Female Nuclei during Fertilization in Neurospora crassaSylvain Brun0Hsiao-Che Kuo1Chris E. Jeffree2Darren D. Thomson3Nick Read4Laboratoire Interdisciplinaire des Energies de Demain, CNRS UMR 8236, Université de Paris, Paris, FranceFungal Cell Biology Group, Institute of Cell Biology, University of Edinburgh, Edinburgh, United KingdomFungal Cell Biology Group, Institute of Cell Biology, University of Edinburgh, Edinburgh, United KingdomManchester Fungal Infection Group, Division of Infection, Immunity, and Respiratory Medicine, University of Manchester, Manchester, United KingdomManchester Fungal Infection Group, Division of Infection, Immunity, and Respiratory Medicine, University of Manchester, Manchester, United KingdomABSTRACT Sexual reproduction is a key process influencing the evolution and adaptation of animals, plants, and many eukaryotic microorganisms, such as fungi. However, the sequential cell biology of fertilization and the associated nuclear dynamics after plasmogamy are poorly understood in filamentous fungi. Using histone-fluorescent parental isolates, we tracked male and female nuclei during fertilization in the model ascomycete Neurospora crassa using live-cell imaging. This study unravels the behavior of trichogyne resident female nuclei and the extraordinary manner in which male nuclei migrate up the trichogyne to the protoperithecium. Our observations raise new fundamental questions about the modus operandi of nucleus movements during sexual reproduction, male and female nuclear identity, guidance of nuclei within the trichogyne and, unexpectedly, the avoidance of “polyspermy” in fungi. The spatiotemporal dynamics of male nuclei within the trichogyne following plasmogamy are also described, where the speed and the deformation of male nuclei are of the most dramatic observed to date in a living organism. IMPORTANCE Using live-cell fluorescence imaging, for the first time we have observed live male and female nuclei during sexual reproduction in the model fungus Neurospora crassa. This study reveals the specific behavior of resident female nuclei within the trichogyne (the female organ) after fertilization and the extraordinary manner in which male nuclei migrate across the trichogyne toward their final destination, the protoperithecium, where karyogamy takes place. Importantly, the speed and deformation of male nuclei were found to be among the most dramatic ever observed in a living organism. Furthermore, we observed that entry of male nuclei into protoperithecia may block the entry of other male nuclei, suggesting that a process analogous to polyspermy avoidance could exist in fungi. Our live-cell imaging approach opens new opportunities for novel research on cell-signaling during sexual reproduction in fungi and, on a broader scale, nuclear dynamics in eukaryotes.https://journals.asm.org/doi/10.1128/Spectrum.00335-21sexual reproductionfertilizationnucleustrichogynematinglive-cell imaging |
| spellingShingle | Sylvain Brun Hsiao-Che Kuo Chris E. Jeffree Darren D. Thomson Nick Read Courtship Ritual of Male and Female Nuclei during Fertilization in Neurospora crassa Microbiology Spectrum sexual reproduction fertilization nucleus trichogyne mating live-cell imaging |
| title | Courtship Ritual of Male and Female Nuclei during Fertilization in Neurospora crassa |
| title_full | Courtship Ritual of Male and Female Nuclei during Fertilization in Neurospora crassa |
| title_fullStr | Courtship Ritual of Male and Female Nuclei during Fertilization in Neurospora crassa |
| title_full_unstemmed | Courtship Ritual of Male and Female Nuclei during Fertilization in Neurospora crassa |
| title_short | Courtship Ritual of Male and Female Nuclei during Fertilization in Neurospora crassa |
| title_sort | courtship ritual of male and female nuclei during fertilization in neurospora crassa |
| topic | sexual reproduction fertilization nucleus trichogyne mating live-cell imaging |
| url | https://journals.asm.org/doi/10.1128/Spectrum.00335-21 |
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