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SlGRAS4 accelerates fruit ripening by regulating ethylene biosynthesis genes and SlMADS1 in tomato.

ABSTRACT: GRAS proteins are plant-specific transcription factors that play crucial roles in plant development and stress responses. However, their involvement in the ripening of economically important fruits and their transcriptional regulatory mechanisms remain largely unclear. Here, we demonstrated that SlGRAS4, encoding a transcription factor of the GRAS family, was induced by the tomato ripening process and regulated by ethylene. Overexpression of SlGRAS4 accelerated fruit ripening, increased the total carotenoid content and increased PSY1 expression in SlGRAS4-OE fruit compared to wild-type fruit. The expression levels of key ethylene biosynthesis genes (SlACS2, SlACS4, SlACO1, and SlACO3) and crucial ripening regulators (RIN and NOR) were increased in SlGRAS4-OE fruit. The negative regulator of tomato fruit ripening, SlMADS1, was repressed in OE fruit. Exogenous ethylene and 1-MCP treatment revealed that more endogenous ethylene was derived in SlGRAS4-OE fruit. More obvious phenotypes were observed in OE seedlings after ACC treatment. Yeast one-hybrid and dual-luciferase assays confirmed that SlGRAS4 can directly bind SlACO1 and SlACO3 promoters to activate their transcription, and SlGRAS4 can also directly repress SlMADS1 expression. Our study identified that SlGRAS4 acts as a new regulator of fruit ripening by regulating ethylene biosynthesis genes in a direct manner. This provides new knowledge of GRAS transcription factors involved in regulating fruit ripening.

SUBMITTER: Liu Y

PROVIDER: S-EPMC7775462 | biostudies-literature | 2021 Jan

REPOSITORIES: biostudies-literature

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SlGRAS4 accelerates fruit ripening by regulating ethylene biosynthesis genes and SlMADS1 in tomato.

Liu Yudong Y Shi Yuan Y Su Deding D Lu Wang W Li Zhengguo Z

Horticulture research 20210101 1

GRAS proteins are plant-specific transcription factors that play crucial roles in plant development and stress responses. However, their involvement in the ripening of economically important fruits and their transcriptional regulatory mechanisms remain largely unclear. Here, we demonstrated that SlGRAS4, encoding a transcription factor of the GRAS family, was induced by the tomato ripening process and regulated by ethylene. Overexpression of SlGRAS4 accelerated fruit ripening, increased the tota ...[more]

PMID: 33384413

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Project description:Light signaling and plant hormones, particularly ethylene and auxins, have been identified as important regulators of carotenoid biosynthesis during tomato fruit ripening. However, whether and how the light and hormonal signaling cascades crosstalk to control this metabolic route remain poorly elucidated. Here, the potential involvement of ethylene and auxins in the light-mediated regulation of tomato fruit carotenogenesis was investigated by comparing the impacts of light treatments and the light-hyperresponsive high pigment-2 (hp2) mutation on both carotenoid synthesis and hormonal signaling. Under either light or dark conditions, the overaccumulation of carotenoids in hp2 ripening fruits was associated with disturbed ethylene production, increased expression of genes encoding master regulators of ripening and higher ethylene sensitivity and signaling output. The increased ethylene sensitivity observed in hp2 fruits was associated with the differential expression of genes encoding ethylene receptors and downstream signaling transduction elements, including the downregulation of the transcription factor ETHYLENE RESPONSE FACTOR.E4, a repressor of carotenoid synthesis. Accordingly, treatments with exogenous ethylene promoted carotenoid biosynthetic genes more intensively in hp2 than in wild-type fruits. Moreover, the loss of HP2 function drastically altered auxin signaling in tomato fruits, resulting in higher activation of the auxin-responsive promoter DR5, severe down-regulation of AUXIN/INDOLE-3-ACETIC ACID (Aux/IAA) genes and altered accumulation of AUXIN RESPONSE FACTOR (ARF) transcripts. Both tomato ARF2 paralogues (Sl-ARF2a and SlARF2b) were up-regulated in hp2 fruits, which agrees with the promotive roles played by these ARFs in tomato fruit ripening and carotenoid biosynthesis. Among the genes differentially expressed in hp2 fruits, the additive effect of light treatment and loss of HP2 function was particularly evident for those encoding carotenoid biosynthetic enzymes, ethylene-related transcription factors, Aux/IAAs and ARFs. Altogether, the data uncover the involvement of ethylene and auxin as part of the light signaling cascades controlling tomato fruit metabolism and provide a new link between light signaling, plant hormone sensitivity and carotenoid metabolism in ripening fruits.

Dataset Information

SlGRAS4 accelerates fruit ripening by regulating ethylene biosynthesis genes and SlMADS1 in tomato.

Publications

SlGRAS4 accelerates fruit ripening by regulating ethylene biosynthesis genes and SlMADS1 in tomato.

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