Gene co-expression analysis of tomato seed maturation reveals tissue-specific regulatory networks and hubs associated with the acquisition of desiccation tolerance and seed vigour
Abstract Background During maturation seeds acquire several physiological traits to enable them to survive drying and disseminate the species. Few studies have addressed the regulatory networks controlling acquisition of these traits at the tissue level particularly in endospermic seeds such as toma...
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| Format: | Article |
| Language: | English |
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BMC
2021-03-01
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| Series: | BMC Plant Biology |
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| Online Access: | https://doi.org/10.1186/s12870-021-02889-8 |
| _version_ | 1797795788183568384 |
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| author | Elise Bizouerne Julia Buitink Benoît Ly Vu Joseph Ly Vu Eddi Esteban Asher Pasha Nicholas Provart Jérôme Verdier Olivier Leprince |
| author_facet | Elise Bizouerne Julia Buitink Benoît Ly Vu Joseph Ly Vu Eddi Esteban Asher Pasha Nicholas Provart Jérôme Verdier Olivier Leprince |
| author_sort | Elise Bizouerne |
| collection | DOAJ |
| description | Abstract Background During maturation seeds acquire several physiological traits to enable them to survive drying and disseminate the species. Few studies have addressed the regulatory networks controlling acquisition of these traits at the tissue level particularly in endospermic seeds such as tomato, which matures in a fully hydrated environment and does not undergo maturation drying. Using temporal RNA-seq analyses of the different seed tissues during maturation, gene network and trait-based correlations were used to explore the transcriptome signatures associated with desiccation tolerance, longevity, germination under water stress and dormancy. Results During maturation, 15,173 differentially expressed genes were detected, forming a gene network representing 21 expression modules, with 3 being specific to seed coat and embryo and 5 to the endosperm. A gene-trait significance measure identified a common gene module between endosperm and embryo associated with desiccation tolerance and conserved with non-endospermic seeds. In addition to genes involved in protection such LEA and HSP and ABA response, the module included antioxidant and repair genes. Dormancy was released concomitantly with the increase in longevity throughout fruit ripening until 14 days after the red fruit stage. This was paralleled by an increase in SlDOG1–2 and PROCERA transcripts. The progressive increase in seed vigour was captured by three gene modules, one in common between embryo and endosperm and two tissue-specific. The common module was enriched with genes associated with mRNA processing in chloroplast and mitochondria (including penta- and tetratricopeptide repeat-containing proteins) and post-transcriptional regulation, as well several flowering genes. The embryo-specific module contained homologues of ABI4 and CHOTTO1 as hub genes associated with seed vigour, whereas the endosperm-specific module revealed a diverse set of processes that were related to genome stability, defence against pathogens and ABA/GA response genes. Conclusion The spatio-temporal co-expression atlas of tomato seed maturation will serve as a valuable resource for the in-depth understanding of the dynamics of gene expression associated with the acquisition of seed vigour at the tissue level. |
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| institution | Directory Open Access Journal |
| issn | 1471-2229 |
| language | English |
| last_indexed | 2024-03-13T03:23:19Z |
| publishDate | 2021-03-01 |
| publisher | BMC |
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| spelling | doaj.art-8eefc9c827734c1fa9d731a286abfcd52023-06-25T11:13:05ZengBMCBMC Plant Biology1471-22292021-03-0121112310.1186/s12870-021-02889-8Gene co-expression analysis of tomato seed maturation reveals tissue-specific regulatory networks and hubs associated with the acquisition of desiccation tolerance and seed vigourElise Bizouerne0Julia Buitink1Benoît Ly Vu2Joseph Ly Vu3Eddi Esteban4Asher Pasha5Nicholas Provart6Jérôme Verdier7Olivier Leprince8Institut Agro, Univ Angers, INRAE, IRHS, SFR 4207 QuaSaVInstitut Agro, Univ Angers, INRAE, IRHS, SFR 4207 QuaSaVInstitut Agro, Univ Angers, INRAE, IRHS, SFR 4207 QuaSaVInstitut Agro, Univ Angers, INRAE, IRHS, SFR 4207 QuaSaVDepartment of Cell and Systems Biology / Centre for the Analysis of Genome Evolution and Function, University of TorontoDepartment of Cell and Systems Biology / Centre for the Analysis of Genome Evolution and Function, University of TorontoDepartment of Cell and Systems Biology / Centre for the Analysis of Genome Evolution and Function, University of TorontoInstitut Agro, Univ Angers, INRAE, IRHS, SFR 4207 QuaSaVInstitut Agro, Univ Angers, INRAE, IRHS, SFR 4207 QuaSaVAbstract Background During maturation seeds acquire several physiological traits to enable them to survive drying and disseminate the species. Few studies have addressed the regulatory networks controlling acquisition of these traits at the tissue level particularly in endospermic seeds such as tomato, which matures in a fully hydrated environment and does not undergo maturation drying. Using temporal RNA-seq analyses of the different seed tissues during maturation, gene network and trait-based correlations were used to explore the transcriptome signatures associated with desiccation tolerance, longevity, germination under water stress and dormancy. Results During maturation, 15,173 differentially expressed genes were detected, forming a gene network representing 21 expression modules, with 3 being specific to seed coat and embryo and 5 to the endosperm. A gene-trait significance measure identified a common gene module between endosperm and embryo associated with desiccation tolerance and conserved with non-endospermic seeds. In addition to genes involved in protection such LEA and HSP and ABA response, the module included antioxidant and repair genes. Dormancy was released concomitantly with the increase in longevity throughout fruit ripening until 14 days after the red fruit stage. This was paralleled by an increase in SlDOG1–2 and PROCERA transcripts. The progressive increase in seed vigour was captured by three gene modules, one in common between embryo and endosperm and two tissue-specific. The common module was enriched with genes associated with mRNA processing in chloroplast and mitochondria (including penta- and tetratricopeptide repeat-containing proteins) and post-transcriptional regulation, as well several flowering genes. The embryo-specific module contained homologues of ABI4 and CHOTTO1 as hub genes associated with seed vigour, whereas the endosperm-specific module revealed a diverse set of processes that were related to genome stability, defence against pathogens and ABA/GA response genes. Conclusion The spatio-temporal co-expression atlas of tomato seed maturation will serve as a valuable resource for the in-depth understanding of the dynamics of gene expression associated with the acquisition of seed vigour at the tissue level.https://doi.org/10.1186/s12870-021-02889-8DormancyEmbryoEndospermLongevityMaturationTranscriptome |
| spellingShingle | Elise Bizouerne Julia Buitink Benoît Ly Vu Joseph Ly Vu Eddi Esteban Asher Pasha Nicholas Provart Jérôme Verdier Olivier Leprince Gene co-expression analysis of tomato seed maturation reveals tissue-specific regulatory networks and hubs associated with the acquisition of desiccation tolerance and seed vigour BMC Plant Biology Dormancy Embryo Endosperm Longevity Maturation Transcriptome |
| title | Gene co-expression analysis of tomato seed maturation reveals tissue-specific regulatory networks and hubs associated with the acquisition of desiccation tolerance and seed vigour |
| title_full | Gene co-expression analysis of tomato seed maturation reveals tissue-specific regulatory networks and hubs associated with the acquisition of desiccation tolerance and seed vigour |
| title_fullStr | Gene co-expression analysis of tomato seed maturation reveals tissue-specific regulatory networks and hubs associated with the acquisition of desiccation tolerance and seed vigour |
| title_full_unstemmed | Gene co-expression analysis of tomato seed maturation reveals tissue-specific regulatory networks and hubs associated with the acquisition of desiccation tolerance and seed vigour |
| title_short | Gene co-expression analysis of tomato seed maturation reveals tissue-specific regulatory networks and hubs associated with the acquisition of desiccation tolerance and seed vigour |
| title_sort | gene co expression analysis of tomato seed maturation reveals tissue specific regulatory networks and hubs associated with the acquisition of desiccation tolerance and seed vigour |
| topic | Dormancy Embryo Endosperm Longevity Maturation Transcriptome |
| url | https://doi.org/10.1186/s12870-021-02889-8 |
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