Cargando…
Phytochrome-Mediated Light Perception Affects Fruit Development and Ripening Through Epigenetic Mechanisms
Phytochrome (PHY)-mediated light and temperature perception has been increasingly implicated as important regulator of fruit development, ripening, and nutritional quality. Fruit ripening is also critically regulated by chromatin remodeling via DNA demethylation, though the molecular basis connectin...
Autores principales: | , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Frontiers Media S.A.
2022
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9096621/ https://www.ncbi.nlm.nih.gov/pubmed/35574124 http://dx.doi.org/10.3389/fpls.2022.870974 |
_version_ | 1784706018139176960 |
---|---|
author | Bianchetti, Ricardo Bellora, Nicolas de Haro, Luis A. Zuccarelli, Rafael Rosado, Daniele Freschi, Luciano Rossi, Magdalena Bermudez, Luisa |
author_facet | Bianchetti, Ricardo Bellora, Nicolas de Haro, Luis A. Zuccarelli, Rafael Rosado, Daniele Freschi, Luciano Rossi, Magdalena Bermudez, Luisa |
author_sort | Bianchetti, Ricardo |
collection | PubMed |
description | Phytochrome (PHY)-mediated light and temperature perception has been increasingly implicated as important regulator of fruit development, ripening, and nutritional quality. Fruit ripening is also critically regulated by chromatin remodeling via DNA demethylation, though the molecular basis connecting epigenetic modifications in fruits and environmental cues remains largely unknown. Here, to unravel whether the PHY-dependent regulation of fruit development involves epigenetic mechanisms, an integrative analysis of the methylome, transcriptome and sRNAome of tomato fruits from phyA single and phyB1B2 double mutants was performed in immature green (IG) and breaker (BK) stages. The transcriptome analysis showed that PHY-mediated light perception regulates more genes in BK than in the early stages of fruit development (IG) and that PHYB1B2 has a more substantial impact than PHYA in the fruit transcriptome, in both analyzed stages. The global profile of methylated cytosines revealed that both PHYA and PHYB1B2 affect the global methylome, but PHYB1B2 has a greater impact on ripening-associated methylation reprogramming across gene-rich genomic regions in tomato fruits. Remarkably, promoters of master ripening-associated transcription factors (TF) (RIN, NOR, CNR, and AP2a) and key carotenoid biosynthetic genes (PSY1, PDS, ZISO, and ZDS) remained highly methylated in phyB1B2 from the IG to BK stage. The positional distribution and enrichment of TF binding sites were analyzed over the promoter region of the phyB1B2 DEGs, exposing an overrepresentation of binding sites for RIN as well as the PHY-downstream effectors PIFs and HY5/HYH. Moreover, phyA and phyB1B2 mutants showed a positive correlation between the methylation level of sRNA cluster-targeted genome regions in gene bodies and mRNA levels. The experimental evidence indicates that PHYB1B2 signal transduction is mediated by a gene expression network involving chromatin organization factors (DNA methylases/demethylases, histone-modifying enzymes, and remodeling factors) and transcriptional regulators leading to altered mRNA profile of ripening-associated genes. This new level of understanding provides insights into the orchestration of epigenetic mechanisms in response to environmental cues affecting agronomical traits. |
format | Online Article Text |
id | pubmed-9096621 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-90966212022-05-13 Phytochrome-Mediated Light Perception Affects Fruit Development and Ripening Through Epigenetic Mechanisms Bianchetti, Ricardo Bellora, Nicolas de Haro, Luis A. Zuccarelli, Rafael Rosado, Daniele Freschi, Luciano Rossi, Magdalena Bermudez, Luisa Front Plant Sci Plant Science Phytochrome (PHY)-mediated light and temperature perception has been increasingly implicated as important regulator of fruit development, ripening, and nutritional quality. Fruit ripening is also critically regulated by chromatin remodeling via DNA demethylation, though the molecular basis connecting epigenetic modifications in fruits and environmental cues remains largely unknown. Here, to unravel whether the PHY-dependent regulation of fruit development involves epigenetic mechanisms, an integrative analysis of the methylome, transcriptome and sRNAome of tomato fruits from phyA single and phyB1B2 double mutants was performed in immature green (IG) and breaker (BK) stages. The transcriptome analysis showed that PHY-mediated light perception regulates more genes in BK than in the early stages of fruit development (IG) and that PHYB1B2 has a more substantial impact than PHYA in the fruit transcriptome, in both analyzed stages. The global profile of methylated cytosines revealed that both PHYA and PHYB1B2 affect the global methylome, but PHYB1B2 has a greater impact on ripening-associated methylation reprogramming across gene-rich genomic regions in tomato fruits. Remarkably, promoters of master ripening-associated transcription factors (TF) (RIN, NOR, CNR, and AP2a) and key carotenoid biosynthetic genes (PSY1, PDS, ZISO, and ZDS) remained highly methylated in phyB1B2 from the IG to BK stage. The positional distribution and enrichment of TF binding sites were analyzed over the promoter region of the phyB1B2 DEGs, exposing an overrepresentation of binding sites for RIN as well as the PHY-downstream effectors PIFs and HY5/HYH. Moreover, phyA and phyB1B2 mutants showed a positive correlation between the methylation level of sRNA cluster-targeted genome regions in gene bodies and mRNA levels. The experimental evidence indicates that PHYB1B2 signal transduction is mediated by a gene expression network involving chromatin organization factors (DNA methylases/demethylases, histone-modifying enzymes, and remodeling factors) and transcriptional regulators leading to altered mRNA profile of ripening-associated genes. This new level of understanding provides insights into the orchestration of epigenetic mechanisms in response to environmental cues affecting agronomical traits. Frontiers Media S.A. 2022-04-28 /pmc/articles/PMC9096621/ /pubmed/35574124 http://dx.doi.org/10.3389/fpls.2022.870974 Text en Copyright © 2022 Bianchetti, Bellora, de Haro, Zuccarelli, Rosado, Freschi, Rossi and Bermudez. https://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 Bianchetti, Ricardo Bellora, Nicolas de Haro, Luis A. Zuccarelli, Rafael Rosado, Daniele Freschi, Luciano Rossi, Magdalena Bermudez, Luisa Phytochrome-Mediated Light Perception Affects Fruit Development and Ripening Through Epigenetic Mechanisms |
title | Phytochrome-Mediated Light Perception Affects Fruit Development and Ripening Through Epigenetic Mechanisms |
title_full | Phytochrome-Mediated Light Perception Affects Fruit Development and Ripening Through Epigenetic Mechanisms |
title_fullStr | Phytochrome-Mediated Light Perception Affects Fruit Development and Ripening Through Epigenetic Mechanisms |
title_full_unstemmed | Phytochrome-Mediated Light Perception Affects Fruit Development and Ripening Through Epigenetic Mechanisms |
title_short | Phytochrome-Mediated Light Perception Affects Fruit Development and Ripening Through Epigenetic Mechanisms |
title_sort | phytochrome-mediated light perception affects fruit development and ripening through epigenetic mechanisms |
topic | Plant Science |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9096621/ https://www.ncbi.nlm.nih.gov/pubmed/35574124 http://dx.doi.org/10.3389/fpls.2022.870974 |
work_keys_str_mv | AT bianchettiricardo phytochromemediatedlightperceptionaffectsfruitdevelopmentandripeningthroughepigeneticmechanisms AT belloranicolas phytochromemediatedlightperceptionaffectsfruitdevelopmentandripeningthroughepigeneticmechanisms AT deharoluisa phytochromemediatedlightperceptionaffectsfruitdevelopmentandripeningthroughepigeneticmechanisms AT zuccarellirafael phytochromemediatedlightperceptionaffectsfruitdevelopmentandripeningthroughepigeneticmechanisms AT rosadodaniele phytochromemediatedlightperceptionaffectsfruitdevelopmentandripeningthroughepigeneticmechanisms AT freschiluciano phytochromemediatedlightperceptionaffectsfruitdevelopmentandripeningthroughepigeneticmechanisms AT rossimagdalena phytochromemediatedlightperceptionaffectsfruitdevelopmentandripeningthroughepigeneticmechanisms AT bermudezluisa phytochromemediatedlightperceptionaffectsfruitdevelopmentandripeningthroughepigeneticmechanisms |