Dynamic roles of small RNAs and DNA methylation associated with heterosis in allotetraploid cotton (Gossypium hirsutum L.)
Abstract Background Heterosis is a complex phenomenon wherein the hybrids outperform their parents. Understanding the underlying molecular mechanism by which hybridization leads to higher yields in allopolyploid cotton is critical for effective breeding programs. Here, we integrated DNA methylation,...
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BMC
2023-10-01
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| Series: | BMC Plant Biology |
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| Online Access: | https://doi.org/10.1186/s12870-023-04495-2 |
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| author | Rasmieh Hamid Feba Jacob Zahra Ghorbanzadeh Leila Jafari Omran Alishah |
| author_facet | Rasmieh Hamid Feba Jacob Zahra Ghorbanzadeh Leila Jafari Omran Alishah |
| author_sort | Rasmieh Hamid |
| collection | DOAJ |
| description | Abstract Background Heterosis is a complex phenomenon wherein the hybrids outperform their parents. Understanding the underlying molecular mechanism by which hybridization leads to higher yields in allopolyploid cotton is critical for effective breeding programs. Here, we integrated DNA methylation, transcriptomes, and small RNA profiles to comprehend the genetic and molecular basis of heterosis in allopolyploid cotton at three developmental stages. Results Transcriptome analysis revealed that numerous DEGs responsive to phytohormones (auxin and salicylic acid) were drastically altered in F1 hybrid compared to the parental lines. DEGs involved in energy metabolism and plant growth were upregulated, whereas DEGs related to basal defense were downregulated. Differences in homoeologous gene expression in F1 hybrid were greatly reduced after hybridization, suggesting that higher levels of parental expression have a vital role in heterosis. Small RNAome and methylome studies showed that the degree of DNA methylation in hybrid is higher when compared to the parents. A substantial number of allele-specific expression genes were found to be strongly regulated by CG allele-specific methylation levels. The hybrid exhibited higher 24-nt-small RNA (siRNA) expression levels than the parents. The regions in the genome with increased levels of 24-nt-siRNA were chiefly related to genes and their flanking regulatory regions, demonstrating a possible effect of these molecules on gene expression. The transposable elements correlated with siRNA clusters in the F1 hybrid had higher methylation levels but lower expression levels, which suggest that these non-additively expressed siRNA clusters, reduced the activity of transposable elements through DNA methylation in the hybrid. Conclusions These multi-omics data provide insights into how changes in epigenetic mechanisms and gene expression patterns can lead to heterosis in allopolyploid cotton. This makes heterosis a viable tool in cotton breeding. |
| first_indexed | 2024-03-09T15:21:45Z |
| format | Article |
| id | doaj.art-c310d7537eac4a5c8e615ffda3fd1b5f |
| institution | Directory Open Access Journal |
| issn | 1471-2229 |
| language | English |
| last_indexed | 2024-03-09T15:21:45Z |
| publishDate | 2023-10-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Plant Biology |
| spelling | doaj.art-c310d7537eac4a5c8e615ffda3fd1b5f2023-11-26T12:47:27ZengBMCBMC Plant Biology1471-22292023-10-0123112410.1186/s12870-023-04495-2Dynamic roles of small RNAs and DNA methylation associated with heterosis in allotetraploid cotton (Gossypium hirsutum L.)Rasmieh Hamid0Feba Jacob1Zahra Ghorbanzadeh2Leila Jafari3Omran Alishah4Department of Plant Breeding, Cotton Research Institute of Iran (CRII), Agricultural Research, Education and Extension Organization (AREEO)Centre for Plant Biotechnology and Molecular Biology, Kerala Agricultural UniversityDepartment of Systems Biology, Agricultural Biotechnology Research Institute of Iran (ABRII), Agricultural Research, Education and Extension Organization (AREEO)Horticultural Science Department, Faculty of Agriculture and Natural Resources, University of HormozganDepartment of Plant Breeding, Cotton Research Institute of Iran (CRII), Agricultural Research, Education and Extension Organization (AREEO)Abstract Background Heterosis is a complex phenomenon wherein the hybrids outperform their parents. Understanding the underlying molecular mechanism by which hybridization leads to higher yields in allopolyploid cotton is critical for effective breeding programs. Here, we integrated DNA methylation, transcriptomes, and small RNA profiles to comprehend the genetic and molecular basis of heterosis in allopolyploid cotton at three developmental stages. Results Transcriptome analysis revealed that numerous DEGs responsive to phytohormones (auxin and salicylic acid) were drastically altered in F1 hybrid compared to the parental lines. DEGs involved in energy metabolism and plant growth were upregulated, whereas DEGs related to basal defense were downregulated. Differences in homoeologous gene expression in F1 hybrid were greatly reduced after hybridization, suggesting that higher levels of parental expression have a vital role in heterosis. Small RNAome and methylome studies showed that the degree of DNA methylation in hybrid is higher when compared to the parents. A substantial number of allele-specific expression genes were found to be strongly regulated by CG allele-specific methylation levels. The hybrid exhibited higher 24-nt-small RNA (siRNA) expression levels than the parents. The regions in the genome with increased levels of 24-nt-siRNA were chiefly related to genes and their flanking regulatory regions, demonstrating a possible effect of these molecules on gene expression. The transposable elements correlated with siRNA clusters in the F1 hybrid had higher methylation levels but lower expression levels, which suggest that these non-additively expressed siRNA clusters, reduced the activity of transposable elements through DNA methylation in the hybrid. Conclusions These multi-omics data provide insights into how changes in epigenetic mechanisms and gene expression patterns can lead to heterosis in allopolyploid cotton. This makes heterosis a viable tool in cotton breeding.https://doi.org/10.1186/s12870-023-04495-2CottonMethylomeSmall RNA |
| spellingShingle | Rasmieh Hamid Feba Jacob Zahra Ghorbanzadeh Leila Jafari Omran Alishah Dynamic roles of small RNAs and DNA methylation associated with heterosis in allotetraploid cotton (Gossypium hirsutum L.) BMC Plant Biology Cotton Methylome Small RNA |
| title | Dynamic roles of small RNAs and DNA methylation associated with heterosis in allotetraploid cotton (Gossypium hirsutum L.) |
| title_full | Dynamic roles of small RNAs and DNA methylation associated with heterosis in allotetraploid cotton (Gossypium hirsutum L.) |
| title_fullStr | Dynamic roles of small RNAs and DNA methylation associated with heterosis in allotetraploid cotton (Gossypium hirsutum L.) |
| title_full_unstemmed | Dynamic roles of small RNAs and DNA methylation associated with heterosis in allotetraploid cotton (Gossypium hirsutum L.) |
| title_short | Dynamic roles of small RNAs and DNA methylation associated with heterosis in allotetraploid cotton (Gossypium hirsutum L.) |
| title_sort | dynamic roles of small rnas and dna methylation associated with heterosis in allotetraploid cotton gossypium hirsutum l |
| topic | Cotton Methylome Small RNA |
| url | https://doi.org/10.1186/s12870-023-04495-2 |
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