Transcriptomic reprogramming and epigenetic regulation underlying pollination-dependent and auxin-induced fruit set in tomato
The transition from flower to fruit, naturally triggered by flower pollination and known as fruit set, is instrumental for plant reproduction, seed formation, and crop yield. Notably, this developmental process can also proceed in the absence of flower fertilization, although it remains unclear whet...
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Frontiers Media S.A.
2025-02-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2025.1495494/full |
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| author | Xiaohan Li Xiaohan Li Xiaohan Li Bing He Anis Djari Pierre Frasse Elie Maza Farid Regad Julien Pirrello Guojian Hu Guojian Hu Guojian Hu Guojian Hu Mondher Bouzayen |
| author_facet | Xiaohan Li Xiaohan Li Xiaohan Li Bing He Anis Djari Pierre Frasse Elie Maza Farid Regad Julien Pirrello Guojian Hu Guojian Hu Guojian Hu Guojian Hu Mondher Bouzayen |
| author_sort | Xiaohan Li |
| collection | DOAJ |
| description | The transition from flower to fruit, naturally triggered by flower pollination and known as fruit set, is instrumental for plant reproduction, seed formation, and crop yield. Notably, this developmental process can also proceed in the absence of flower fertilization, although it remains unclear whether pollination-dependent and pollination-independent fruit sets undergo similar transcriptomic reprogramming. Genome-wide transcriptomic profiling of the flower-to-fruit transition, either pollination-induced or triggered by auxin treatment, shows that both types of triggers modulate the expression of a common large set of genes primarily expressed in maternal tissues. These include genes related to auxin, gibberellin, brassinosteroid, and ethylene signaling. Furthermore, analysis of changes in histone marking during this transition phase indicated that gene reprogramming underlying both types of fruit set primarily correlated with dynamic changes in H3K9ac and H3K4me3 histone marks. Notably, MCM1, AG, DEFA and SRF (MADS)-box and NAM, ATAF1/2, and CUC2 (NAC) genes were extensively downregulated during the transition from flower to fruit, suggesting their negative roles in fruit initiation. In contrast, Teosinte branched1/Cincinnata/proliferating cell factor (TCP), SQUAMOSA -promoter binding proteins (SBP), Sucrose nonfermenting 2 (SNF2), Growth-regulating factor (GRF), and Su (var)3-9, Enhancer-of-zeste and Trithorax (SET) family genes were significantly upregulated in both pollinated and auxin-treated young developing fruits, suggesting their active roles in promoting fruit sets. Despite these similarities, a comparative analysis of the effects of natural pollination and auxin treatment revealed several differences, primarily related to seed development and hormone signaling. Taken together, the data support the idea that auxin serves as the central hormone orchestrating the extensive gene reprogramming associated with fruit initiation in tomato. |
| format | Article |
| id | doaj-art-8275284df59f4999bd9ce3d162baf868 |
| institution | Kabale University |
| issn | 1664-462X |
| language | English |
| publishDate | 2025-02-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Plant Science |
| spelling | doaj-art-8275284df59f4999bd9ce3d162baf8682025-02-11T06:59:04ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2025-02-011610.3389/fpls.2025.14954941495494Transcriptomic reprogramming and epigenetic regulation underlying pollination-dependent and auxin-induced fruit set in tomatoXiaohan Li0Xiaohan Li1Xiaohan Li2Bing He3Anis Djari4Pierre Frasse5Elie Maza6Farid Regad7Julien Pirrello8Guojian Hu9Guojian Hu10Guojian Hu11Guojian Hu12Mondher Bouzayen13College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, ChinaZhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology, Zhejiang University, Hangzhou, ChinaThe State Agriculture Ministry Laboratory of Horticultural Plant Growth, Development and Quality Improvement, Zhejiang University, Hangzhou, ChinaCollege of Horticulture, China Agricultural University, Beijing, ChinaLaboratoire de Recherche en Sciences Végétales—Génomique et Biotechnologie des Fruits—UMR5546, Université de Toulouse, Centre national de la recherche scientifique (CNRS), Université de Toulouse 3 - Paul Sabatier (UPS), Toulouse-Institut National Polytechnique (INP), Toulouse, FranceLaboratoire de Recherche en Sciences Végétales—Génomique et Biotechnologie des Fruits—UMR5546, Université de Toulouse, Centre national de la recherche scientifique (CNRS), Université de Toulouse 3 - Paul Sabatier (UPS), Toulouse-Institut National Polytechnique (INP), Toulouse, FranceLaboratoire de Recherche en Sciences Végétales—Génomique et Biotechnologie des Fruits—UMR5546, Université de Toulouse, Centre national de la recherche scientifique (CNRS), Université de Toulouse 3 - Paul Sabatier (UPS), Toulouse-Institut National Polytechnique (INP), Toulouse, FranceLaboratoire de Recherche en Sciences Végétales—Génomique et Biotechnologie des Fruits—UMR5546, Université de Toulouse, Centre national de la recherche scientifique (CNRS), Université de Toulouse 3 - Paul Sabatier (UPS), Toulouse-Institut National Polytechnique (INP), Toulouse, FranceLaboratoire de Recherche en Sciences Végétales—Génomique et Biotechnologie des Fruits—UMR5546, Université de Toulouse, Centre national de la recherche scientifique (CNRS), Université de Toulouse 3 - Paul Sabatier (UPS), Toulouse-Institut National Polytechnique (INP), Toulouse, FranceCollege of Agriculture and Biotechnology, Zhejiang University, Hangzhou, ChinaZhejiang Provincial Key Laboratory of Horticultural Plant Integrative Biology, Zhejiang University, Hangzhou, ChinaThe State Agriculture Ministry Laboratory of Horticultural Plant Growth, Development and Quality Improvement, Zhejiang University, Hangzhou, ChinaLaboratoire de Recherche en Sciences Végétales—Génomique et Biotechnologie des Fruits—UMR5546, Université de Toulouse, Centre national de la recherche scientifique (CNRS), Université de Toulouse 3 - Paul Sabatier (UPS), Toulouse-Institut National Polytechnique (INP), Toulouse, FranceLaboratoire de Recherche en Sciences Végétales—Génomique et Biotechnologie des Fruits—UMR5546, Université de Toulouse, Centre national de la recherche scientifique (CNRS), Université de Toulouse 3 - Paul Sabatier (UPS), Toulouse-Institut National Polytechnique (INP), Toulouse, FranceThe transition from flower to fruit, naturally triggered by flower pollination and known as fruit set, is instrumental for plant reproduction, seed formation, and crop yield. Notably, this developmental process can also proceed in the absence of flower fertilization, although it remains unclear whether pollination-dependent and pollination-independent fruit sets undergo similar transcriptomic reprogramming. Genome-wide transcriptomic profiling of the flower-to-fruit transition, either pollination-induced or triggered by auxin treatment, shows that both types of triggers modulate the expression of a common large set of genes primarily expressed in maternal tissues. These include genes related to auxin, gibberellin, brassinosteroid, and ethylene signaling. Furthermore, analysis of changes in histone marking during this transition phase indicated that gene reprogramming underlying both types of fruit set primarily correlated with dynamic changes in H3K9ac and H3K4me3 histone marks. Notably, MCM1, AG, DEFA and SRF (MADS)-box and NAM, ATAF1/2, and CUC2 (NAC) genes were extensively downregulated during the transition from flower to fruit, suggesting their negative roles in fruit initiation. In contrast, Teosinte branched1/Cincinnata/proliferating cell factor (TCP), SQUAMOSA -promoter binding proteins (SBP), Sucrose nonfermenting 2 (SNF2), Growth-regulating factor (GRF), and Su (var)3-9, Enhancer-of-zeste and Trithorax (SET) family genes were significantly upregulated in both pollinated and auxin-treated young developing fruits, suggesting their active roles in promoting fruit sets. Despite these similarities, a comparative analysis of the effects of natural pollination and auxin treatment revealed several differences, primarily related to seed development and hormone signaling. Taken together, the data support the idea that auxin serves as the central hormone orchestrating the extensive gene reprogramming associated with fruit initiation in tomato.https://www.frontiersin.org/articles/10.3389/fpls.2025.1495494/fullfruit setauxinpollinationtranscriptomic reprogrammingepigenetic regulationtomato |
| spellingShingle | Xiaohan Li Xiaohan Li Xiaohan Li Bing He Anis Djari Pierre Frasse Elie Maza Farid Regad Julien Pirrello Guojian Hu Guojian Hu Guojian Hu Guojian Hu Mondher Bouzayen Transcriptomic reprogramming and epigenetic regulation underlying pollination-dependent and auxin-induced fruit set in tomato Frontiers in Plant Science fruit set auxin pollination transcriptomic reprogramming epigenetic regulation tomato |
| title | Transcriptomic reprogramming and epigenetic regulation underlying pollination-dependent and auxin-induced fruit set in tomato |
| title_full | Transcriptomic reprogramming and epigenetic regulation underlying pollination-dependent and auxin-induced fruit set in tomato |
| title_fullStr | Transcriptomic reprogramming and epigenetic regulation underlying pollination-dependent and auxin-induced fruit set in tomato |
| title_full_unstemmed | Transcriptomic reprogramming and epigenetic regulation underlying pollination-dependent and auxin-induced fruit set in tomato |
| title_short | Transcriptomic reprogramming and epigenetic regulation underlying pollination-dependent and auxin-induced fruit set in tomato |
| title_sort | transcriptomic reprogramming and epigenetic regulation underlying pollination dependent and auxin induced fruit set in tomato |
| topic | fruit set auxin pollination transcriptomic reprogramming epigenetic regulation tomato |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2025.1495494/full |
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