Oligo-painting and GISH reveal meiotic chromosome biases and increased meiotic stability in synthetic allotetraploid Cucumis ×hytivus with dysploid parental karyotypes

Abstract Background Meiosis of newly formed allopolyploids frequently encounter perturbations induced by the merging of divergent and hybridizable genomes. However, to date, the meiotic properties of allopolyploids with dysploid parental karyotypes have not been studied in detail. The allotetraploid...

Full description

Bibliographic Details
Main Authors: Qinzheng Zhao, Yunzhu Wang, Yunfei Bi, Yufei Zhai, Xiaqing Yu, Chunyan Cheng, Panqiao Wang, Ji Li, Qunfeng Lou, Jinfeng Chen
Format: Article
Language:English
Published: BMC 2019-11-01
Series:BMC Plant Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12870-019-2060-z
_version_ 1818530569496035328
author Qinzheng Zhao
Yunzhu Wang
Yunfei Bi
Yufei Zhai
Xiaqing Yu
Chunyan Cheng
Panqiao Wang
Ji Li
Qunfeng Lou
Jinfeng Chen
author_facet Qinzheng Zhao
Yunzhu Wang
Yunfei Bi
Yufei Zhai
Xiaqing Yu
Chunyan Cheng
Panqiao Wang
Ji Li
Qunfeng Lou
Jinfeng Chen
author_sort Qinzheng Zhao
collection DOAJ
description Abstract Background Meiosis of newly formed allopolyploids frequently encounter perturbations induced by the merging of divergent and hybridizable genomes. However, to date, the meiotic properties of allopolyploids with dysploid parental karyotypes have not been studied in detail. The allotetraploid Cucumis ×hytivus (HHCC, 2n = 38) was obtained from interspecific hybridization between C. sativus (CC, 2n = 14) and C. hystrix (HH, 2n = 24) followed by chromosome doubling. The results of this study thus offer an excellent opportunity to explore the meiotic properties of allopolyploids with dysploid parental karyotypes. Results In this report, we describe the meiotic properties of five chromosomes (C5, C7, H1, H9 and H10) and two genomes in interspecific hybrids and C. ×hytivus (the 4th and 14th inbred family) through oligo-painting and genomic in situ hybridization (GISH). We show that 1) only two translocations carrying C5-oligo signals were detected on the chromosomes C2 and C4 of one 14th individual by the karyotyping of eight 4th and 36 14th plants based on C5- and C7-oligo painting, and possible cytological evidence was observed in meiosis of the 4th generation; 2) individual chromosome have biases for homoeologous pairing and univalent formation in F1 hybrids and allotetraploids; 3) extensive H-chromosome autosyndetic pairings (e.g., H-H, 25.5% PMCs) were observed in interspecific F1 hybrid, whereas no C-chromosome autosyndetic pairings were observed (e.g. C-C); 4) the meiotic properties of two subgenomes have significant biases in allotetraploids: H-subgenome exhibits higher univalent and chromosome lagging frequencies than C-subgenome; and 5) increased meiotic stability in the S14 generation compared with the S4 generation, including synchronous meiosis behavior, reduced incidents of univalent and chromosome lagging. Conclusions These results suggest that the meiotic behavior of two subgenomes has dramatic biases in response to interspecific hybridization and allopolyploidization, and the meiotic behavior harmony of subgenomes is a key subject of meiosis evolution in C. ×hytivus. This study helps to elucidate the meiotic properties and evolution of nascent allopolyploids with the dysploid parental karyotypes.
first_indexed 2024-12-11T17:21:22Z
format Article
id doaj.art-dda40e26f5e34c5fbb73b301f8960844
institution Directory Open Access Journal
issn 1471-2229
language English
last_indexed 2024-12-11T17:21:22Z
publishDate 2019-11-01
publisher BMC
record_format Article
series BMC Plant Biology
spelling doaj.art-dda40e26f5e34c5fbb73b301f89608442022-12-22T00:57:08ZengBMCBMC Plant Biology1471-22292019-11-0119111610.1186/s12870-019-2060-zOligo-painting and GISH reveal meiotic chromosome biases and increased meiotic stability in synthetic allotetraploid Cucumis ×hytivus with dysploid parental karyotypesQinzheng Zhao0Yunzhu Wang1Yunfei Bi2Yufei Zhai3Xiaqing Yu4Chunyan Cheng5Panqiao Wang6Ji Li7Qunfeng Lou8Jinfeng Chen9State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural UniversityInstitue of Horticulture, Zhejiang Academy of Agriculture SciencesState Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural UniversityState Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural UniversityState Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural UniversityState Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural UniversityState Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural UniversityState Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural UniversityState Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural UniversityState Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural UniversityAbstract Background Meiosis of newly formed allopolyploids frequently encounter perturbations induced by the merging of divergent and hybridizable genomes. However, to date, the meiotic properties of allopolyploids with dysploid parental karyotypes have not been studied in detail. The allotetraploid Cucumis ×hytivus (HHCC, 2n = 38) was obtained from interspecific hybridization between C. sativus (CC, 2n = 14) and C. hystrix (HH, 2n = 24) followed by chromosome doubling. The results of this study thus offer an excellent opportunity to explore the meiotic properties of allopolyploids with dysploid parental karyotypes. Results In this report, we describe the meiotic properties of five chromosomes (C5, C7, H1, H9 and H10) and two genomes in interspecific hybrids and C. ×hytivus (the 4th and 14th inbred family) through oligo-painting and genomic in situ hybridization (GISH). We show that 1) only two translocations carrying C5-oligo signals were detected on the chromosomes C2 and C4 of one 14th individual by the karyotyping of eight 4th and 36 14th plants based on C5- and C7-oligo painting, and possible cytological evidence was observed in meiosis of the 4th generation; 2) individual chromosome have biases for homoeologous pairing and univalent formation in F1 hybrids and allotetraploids; 3) extensive H-chromosome autosyndetic pairings (e.g., H-H, 25.5% PMCs) were observed in interspecific F1 hybrid, whereas no C-chromosome autosyndetic pairings were observed (e.g. C-C); 4) the meiotic properties of two subgenomes have significant biases in allotetraploids: H-subgenome exhibits higher univalent and chromosome lagging frequencies than C-subgenome; and 5) increased meiotic stability in the S14 generation compared with the S4 generation, including synchronous meiosis behavior, reduced incidents of univalent and chromosome lagging. Conclusions These results suggest that the meiotic behavior of two subgenomes has dramatic biases in response to interspecific hybridization and allopolyploidization, and the meiotic behavior harmony of subgenomes is a key subject of meiosis evolution in C. ×hytivus. This study helps to elucidate the meiotic properties and evolution of nascent allopolyploids with the dysploid parental karyotypes.http://link.springer.com/article/10.1186/s12870-019-2060-zAllopolyploidInterspecies hybridizationMeiotic instabilityKaryotype variationOligo-FISH
spellingShingle Qinzheng Zhao
Yunzhu Wang
Yunfei Bi
Yufei Zhai
Xiaqing Yu
Chunyan Cheng
Panqiao Wang
Ji Li
Qunfeng Lou
Jinfeng Chen
Oligo-painting and GISH reveal meiotic chromosome biases and increased meiotic stability in synthetic allotetraploid Cucumis ×hytivus with dysploid parental karyotypes
BMC Plant Biology
Allopolyploid
Interspecies hybridization
Meiotic instability
Karyotype variation
Oligo-FISH
title Oligo-painting and GISH reveal meiotic chromosome biases and increased meiotic stability in synthetic allotetraploid Cucumis ×hytivus with dysploid parental karyotypes
title_full Oligo-painting and GISH reveal meiotic chromosome biases and increased meiotic stability in synthetic allotetraploid Cucumis ×hytivus with dysploid parental karyotypes
title_fullStr Oligo-painting and GISH reveal meiotic chromosome biases and increased meiotic stability in synthetic allotetraploid Cucumis ×hytivus with dysploid parental karyotypes
title_full_unstemmed Oligo-painting and GISH reveal meiotic chromosome biases and increased meiotic stability in synthetic allotetraploid Cucumis ×hytivus with dysploid parental karyotypes
title_short Oligo-painting and GISH reveal meiotic chromosome biases and increased meiotic stability in synthetic allotetraploid Cucumis ×hytivus with dysploid parental karyotypes
title_sort oligo painting and gish reveal meiotic chromosome biases and increased meiotic stability in synthetic allotetraploid cucumis hytivus with dysploid parental karyotypes
topic Allopolyploid
Interspecies hybridization
Meiotic instability
Karyotype variation
Oligo-FISH
url http://link.springer.com/article/10.1186/s12870-019-2060-z
work_keys_str_mv AT qinzhengzhao oligopaintingandgishrevealmeioticchromosomebiasesandincreasedmeioticstabilityinsyntheticallotetraploidcucumishytivuswithdysploidparentalkaryotypes
AT yunzhuwang oligopaintingandgishrevealmeioticchromosomebiasesandincreasedmeioticstabilityinsyntheticallotetraploidcucumishytivuswithdysploidparentalkaryotypes
AT yunfeibi oligopaintingandgishrevealmeioticchromosomebiasesandincreasedmeioticstabilityinsyntheticallotetraploidcucumishytivuswithdysploidparentalkaryotypes
AT yufeizhai oligopaintingandgishrevealmeioticchromosomebiasesandincreasedmeioticstabilityinsyntheticallotetraploidcucumishytivuswithdysploidparentalkaryotypes
AT xiaqingyu oligopaintingandgishrevealmeioticchromosomebiasesandincreasedmeioticstabilityinsyntheticallotetraploidcucumishytivuswithdysploidparentalkaryotypes
AT chunyancheng oligopaintingandgishrevealmeioticchromosomebiasesandincreasedmeioticstabilityinsyntheticallotetraploidcucumishytivuswithdysploidparentalkaryotypes
AT panqiaowang oligopaintingandgishrevealmeioticchromosomebiasesandincreasedmeioticstabilityinsyntheticallotetraploidcucumishytivuswithdysploidparentalkaryotypes
AT jili oligopaintingandgishrevealmeioticchromosomebiasesandincreasedmeioticstabilityinsyntheticallotetraploidcucumishytivuswithdysploidparentalkaryotypes
AT qunfenglou oligopaintingandgishrevealmeioticchromosomebiasesandincreasedmeioticstabilityinsyntheticallotetraploidcucumishytivuswithdysploidparentalkaryotypes
AT jinfengchen oligopaintingandgishrevealmeioticchromosomebiasesandincreasedmeioticstabilityinsyntheticallotetraploidcucumishytivuswithdysploidparentalkaryotypes