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Diploid Male Gametes Circumvent Hybrid Sterility Between Asian and African Rice Species

In F(1) hybrids of Oryza sativa (Asian rice) and Oryza glaberrima (African rice), heterozygosity leads to a complete gamete abortion because of allelic conflict at each of the 13 hybrid sterility (HS) loci. We systematically produced 19 plants from the F(1) hybrids of both the rice species by the an...

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Autores principales: Kuniyoshi, Daichi, Masuda, Itaru, Kanaoka, Yoshitaka, Shimazaki-Kishi, Yuki, Okamoto, Yoshihiro, Yasui, Hideshi, Yamamoto, Toshio, Nagaki, Kiyotaka, Hoshino, Yoichiro, Koide, Yohei, Takamure, Itsuro, Kishima, Yuji
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7674174/
https://www.ncbi.nlm.nih.gov/pubmed/33224168
http://dx.doi.org/10.3389/fpls.2020.579305
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author Kuniyoshi, Daichi
Masuda, Itaru
Kanaoka, Yoshitaka
Shimazaki-Kishi, Yuki
Okamoto, Yoshihiro
Yasui, Hideshi
Yamamoto, Toshio
Nagaki, Kiyotaka
Hoshino, Yoichiro
Koide, Yohei
Takamure, Itsuro
Kishima, Yuji
author_facet Kuniyoshi, Daichi
Masuda, Itaru
Kanaoka, Yoshitaka
Shimazaki-Kishi, Yuki
Okamoto, Yoshihiro
Yasui, Hideshi
Yamamoto, Toshio
Nagaki, Kiyotaka
Hoshino, Yoichiro
Koide, Yohei
Takamure, Itsuro
Kishima, Yuji
author_sort Kuniyoshi, Daichi
collection PubMed
description In F(1) hybrids of Oryza sativa (Asian rice) and Oryza glaberrima (African rice), heterozygosity leads to a complete gamete abortion because of allelic conflict at each of the 13 hybrid sterility (HS) loci. We systematically produced 19 plants from the F(1) hybrids of both the rice species by the anther culture (AC) method. Five of the 19 interspecific hybrid plants were partially fertile and able to produce seeds. Unlike ordinal doubled haploid plants resulting from AC, these regenerated plants showed various ploidy levels (diploid to pentaploid) and different zygosities (completely homozygous, completely heterozygous, and a combination). These properties were attributable to meiotic anomalies in the interspecific hybrid F(1) plants. Examination of the genetic structures of the regenerated plants suggested meiotic non-reduction took place in the interspecific hybrid F(1) plants. The centromeric regions in the regenerated plants revealed that the abnormal first and/or second divisions of meiosis, namely the first division restitution (FDR) and/or second division restitution (SDR), had occurred in the interspecific hybrid. Immunohistochemical observations also verified these phenomena. FDR and SDR occurrences at meiosis might strongly lead to the formation of diploid microspores. The results demonstrated that meiotic anomalies functioned as a reproductive barrier occurred before the HS genes acted in gamete of the interspecific hybrid. Although such meiotic anomalies are detrimental to pollen development, the early rescue of microspores carrying the diploid gamete resulted in the fertile regenerated plants. The five partially fertile plants carrying tetraploid genomes with heterozygous alleles of the HS loci produced fertile diploid pollens, implying that the diploid gametes circumvented the allelic conflicts at the HS loci. We also proposed how diploid male gametes avoid HS with the killer–protector model.
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spelling pubmed-76741742020-11-19 Diploid Male Gametes Circumvent Hybrid Sterility Between Asian and African Rice Species Kuniyoshi, Daichi Masuda, Itaru Kanaoka, Yoshitaka Shimazaki-Kishi, Yuki Okamoto, Yoshihiro Yasui, Hideshi Yamamoto, Toshio Nagaki, Kiyotaka Hoshino, Yoichiro Koide, Yohei Takamure, Itsuro Kishima, Yuji Front Plant Sci Plant Science In F(1) hybrids of Oryza sativa (Asian rice) and Oryza glaberrima (African rice), heterozygosity leads to a complete gamete abortion because of allelic conflict at each of the 13 hybrid sterility (HS) loci. We systematically produced 19 plants from the F(1) hybrids of both the rice species by the anther culture (AC) method. Five of the 19 interspecific hybrid plants were partially fertile and able to produce seeds. Unlike ordinal doubled haploid plants resulting from AC, these regenerated plants showed various ploidy levels (diploid to pentaploid) and different zygosities (completely homozygous, completely heterozygous, and a combination). These properties were attributable to meiotic anomalies in the interspecific hybrid F(1) plants. Examination of the genetic structures of the regenerated plants suggested meiotic non-reduction took place in the interspecific hybrid F(1) plants. The centromeric regions in the regenerated plants revealed that the abnormal first and/or second divisions of meiosis, namely the first division restitution (FDR) and/or second division restitution (SDR), had occurred in the interspecific hybrid. Immunohistochemical observations also verified these phenomena. FDR and SDR occurrences at meiosis might strongly lead to the formation of diploid microspores. The results demonstrated that meiotic anomalies functioned as a reproductive barrier occurred before the HS genes acted in gamete of the interspecific hybrid. Although such meiotic anomalies are detrimental to pollen development, the early rescue of microspores carrying the diploid gamete resulted in the fertile regenerated plants. The five partially fertile plants carrying tetraploid genomes with heterozygous alleles of the HS loci produced fertile diploid pollens, implying that the diploid gametes circumvented the allelic conflicts at the HS loci. We also proposed how diploid male gametes avoid HS with the killer–protector model. Frontiers Media S.A. 2020-11-05 /pmc/articles/PMC7674174/ /pubmed/33224168 http://dx.doi.org/10.3389/fpls.2020.579305 Text en Copyright © 2020 Kuniyoshi, Masuda, Kanaoka, Shimazaki-Kishi, Okamoto, Yasui, Yamamoto, Nagaki, Hoshino, Koide, Takamure and Kishima. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Kuniyoshi, Daichi
Masuda, Itaru
Kanaoka, Yoshitaka
Shimazaki-Kishi, Yuki
Okamoto, Yoshihiro
Yasui, Hideshi
Yamamoto, Toshio
Nagaki, Kiyotaka
Hoshino, Yoichiro
Koide, Yohei
Takamure, Itsuro
Kishima, Yuji
Diploid Male Gametes Circumvent Hybrid Sterility Between Asian and African Rice Species
title Diploid Male Gametes Circumvent Hybrid Sterility Between Asian and African Rice Species
title_full Diploid Male Gametes Circumvent Hybrid Sterility Between Asian and African Rice Species
title_fullStr Diploid Male Gametes Circumvent Hybrid Sterility Between Asian and African Rice Species
title_full_unstemmed Diploid Male Gametes Circumvent Hybrid Sterility Between Asian and African Rice Species
title_short Diploid Male Gametes Circumvent Hybrid Sterility Between Asian and African Rice Species
title_sort diploid male gametes circumvent hybrid sterility between asian and african rice species
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7674174/
https://www.ncbi.nlm.nih.gov/pubmed/33224168
http://dx.doi.org/10.3389/fpls.2020.579305
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