Subgenome evolutionary dynamics in allotetraploid ferns: insights from the gene expression patterns in the allotetraploid species Phegopteris decursivepinnata (Thelypteridacea, Polypodiales)
Allopolyploidization often leads to disruptive conflicts among more than two sets of subgenomes, leading to genomic modifications and changes in gene expression. Although the evolutionary trajectories of subgenomes in allopolyploids have been studied intensely in angiosperms, the dynamics of subgeno...
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Frontiers Media S.A.
2024-01-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2023.1286320/full |
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| author | Natsu Katayama Natsu Katayama Takuya Yamamoto Sakura Aiuchi Yasuyuki Watano Tao Fujiwara |
| author_facet | Natsu Katayama Natsu Katayama Takuya Yamamoto Sakura Aiuchi Yasuyuki Watano Tao Fujiwara |
| author_sort | Natsu Katayama |
| collection | DOAJ |
| description | Allopolyploidization often leads to disruptive conflicts among more than two sets of subgenomes, leading to genomic modifications and changes in gene expression. Although the evolutionary trajectories of subgenomes in allopolyploids have been studied intensely in angiosperms, the dynamics of subgenome evolution remain poorly understood in ferns, despite the prevalence of allopolyploidization. In this study, we have focused on an allotetraploid fern—Phegopteris decursivepinnata—and its diploid parental species, P. koreana (K) and P. taiwaniana (T). Using RNA-seq analyses, we have compared the gene expression profiles for 9,540 genes among parental species, synthetic F1 hybrids, and natural allotetraploids. The changes in gene expression patterns were traced from the F1 hybrids to the natural allopolyploids. This study has revealed that the expression patterns observed in most genes in the F1 hybrids are largely conserved in the allopolyploids; however, there were substantial differences in certain genes between these groups. In the allopolyploids compared with the F1 hybrids, the number of genes showing a transgressive pattern in total expression levels was increased. There was a slight reduction in T-dominance and a slight increase in K-dominance, in terms of expression level dominance. Interestingly, there is no obvious bias toward the T- or K-subgenomes in the number and expression levels overall, showing the absence of subgenome dominance. These findings demonstrated the impacts of the substantial transcriptome change after hybridization and the moderate modification during allopolyploid establishment on gene expression in ferns and provided important insights into subgenome evolution in polyploid ferns. |
| first_indexed | 2024-03-08T15:51:56Z |
| format | Article |
| id | doaj.art-b0390a14b2b5425bafc68bdecf24aa78 |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-03-08T15:51:56Z |
| publishDate | 2024-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-b0390a14b2b5425bafc68bdecf24aa782024-01-09T04:33:13ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2024-01-011410.3389/fpls.2023.12863201286320Subgenome evolutionary dynamics in allotetraploid ferns: insights from the gene expression patterns in the allotetraploid species Phegopteris decursivepinnata (Thelypteridacea, Polypodiales)Natsu Katayama0Natsu Katayama1Takuya Yamamoto2Sakura Aiuchi3Yasuyuki Watano4Tao Fujiwara5Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo, JapanDepartment of Biology, Faculty of Science, Chiba University, Chiba, JapanDepartment of Biology, Graduate School of Science, Chiba University, Chiba, JapanDepartment of Biology, Graduate School of Science, Chiba University, Chiba, JapanDepartment of Biology, Faculty of Science, Chiba University, Chiba, JapanCenter for Molecular Biodiversity Research, National Museum of Nature and Science, Tsukuba, Ibaraki, JapanAllopolyploidization often leads to disruptive conflicts among more than two sets of subgenomes, leading to genomic modifications and changes in gene expression. Although the evolutionary trajectories of subgenomes in allopolyploids have been studied intensely in angiosperms, the dynamics of subgenome evolution remain poorly understood in ferns, despite the prevalence of allopolyploidization. In this study, we have focused on an allotetraploid fern—Phegopteris decursivepinnata—and its diploid parental species, P. koreana (K) and P. taiwaniana (T). Using RNA-seq analyses, we have compared the gene expression profiles for 9,540 genes among parental species, synthetic F1 hybrids, and natural allotetraploids. The changes in gene expression patterns were traced from the F1 hybrids to the natural allopolyploids. This study has revealed that the expression patterns observed in most genes in the F1 hybrids are largely conserved in the allopolyploids; however, there were substantial differences in certain genes between these groups. In the allopolyploids compared with the F1 hybrids, the number of genes showing a transgressive pattern in total expression levels was increased. There was a slight reduction in T-dominance and a slight increase in K-dominance, in terms of expression level dominance. Interestingly, there is no obvious bias toward the T- or K-subgenomes in the number and expression levels overall, showing the absence of subgenome dominance. These findings demonstrated the impacts of the substantial transcriptome change after hybridization and the moderate modification during allopolyploid establishment on gene expression in ferns and provided important insights into subgenome evolution in polyploid ferns.https://www.frontiersin.org/articles/10.3389/fpls.2023.1286320/fullallopolyploidcytonuclear coordinationexpression level dominancegenome evolutionhomoeolog expression biaspteridophyte |
| spellingShingle | Natsu Katayama Natsu Katayama Takuya Yamamoto Sakura Aiuchi Yasuyuki Watano Tao Fujiwara Subgenome evolutionary dynamics in allotetraploid ferns: insights from the gene expression patterns in the allotetraploid species Phegopteris decursivepinnata (Thelypteridacea, Polypodiales) Frontiers in Plant Science allopolyploid cytonuclear coordination expression level dominance genome evolution homoeolog expression bias pteridophyte |
| title | Subgenome evolutionary dynamics in allotetraploid ferns: insights from the gene expression patterns in the allotetraploid species Phegopteris decursivepinnata (Thelypteridacea, Polypodiales) |
| title_full | Subgenome evolutionary dynamics in allotetraploid ferns: insights from the gene expression patterns in the allotetraploid species Phegopteris decursivepinnata (Thelypteridacea, Polypodiales) |
| title_fullStr | Subgenome evolutionary dynamics in allotetraploid ferns: insights from the gene expression patterns in the allotetraploid species Phegopteris decursivepinnata (Thelypteridacea, Polypodiales) |
| title_full_unstemmed | Subgenome evolutionary dynamics in allotetraploid ferns: insights from the gene expression patterns in the allotetraploid species Phegopteris decursivepinnata (Thelypteridacea, Polypodiales) |
| title_short | Subgenome evolutionary dynamics in allotetraploid ferns: insights from the gene expression patterns in the allotetraploid species Phegopteris decursivepinnata (Thelypteridacea, Polypodiales) |
| title_sort | subgenome evolutionary dynamics in allotetraploid ferns insights from the gene expression patterns in the allotetraploid species phegopteris decursivepinnata thelypteridacea polypodiales |
| topic | allopolyploid cytonuclear coordination expression level dominance genome evolution homoeolog expression bias pteridophyte |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2023.1286320/full |
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