Dataset Information

Auxin-activated MdARF5 induces the expression of ethylene biosynthetic genes to initiate apple fruit ripening.

ABSTRACT: The gaseous plant hormone ethylene induces the ripening of climacteric fruit, including apple (Malus domestica). Another phytohormone, auxin, is known to promote ethylene production in many horticultural crops, but the regulatory mechanism remains unclear. Here, we found that auxin application induces ethylene production in apple fruit before the stage of commercial harvest, when they are not otherwise capable of ripening naturally. The expression of MdARF5, a member of the auxin response factor transcription factor (TF) family involved in the auxin signaling pathway, was enhanced by treatment with the synthetic auxin naphthaleneacetic acid (NAA). Further studies revealed that MdARF5 binds to the promoter of MdERF2, encoding a TF in the ethylene signaling pathway, as well as the promoters of two 1-aminocyclopropane-1-carboxylic acid synthase (ACS) genes (MdACS3a and MdACS1) and an ACC oxidase (ACO) gene, MdACO1, all of which encode key steps in ethylene biosynthesis, thereby inducing their expression. We also observed that auxin-induced ethylene production was dependent on the methylation of the MdACS3a promoter. Our findings reveal that auxin induces ethylene biosynthesis in apple fruit through activation of MdARF5 expression.

SUBMITTER: Yue P

PROVIDER: S-EPMC7317826 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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Auxin-activated MdARF5 induces the expression of ethylene biosynthetic genes to initiate apple fruit ripening.

Yue Pengtao P Lu Qian Q Liu Zhi Z Lv Tianxing T Li Xinyue X Bu Haidong H Liu Weiting W Xu Yaxiu Y Yuan Hui H Wang Aide A

The New phytologist 20200328 6

The gaseous plant hormone ethylene induces the ripening of climacteric fruit, including apple (Malus domestica). Another phytohormone, auxin, is known to promote ethylene production in many horticultural crops, but the regulatory mechanism remains unclear. Here, we found that auxin application induces ethylene production in apple fruit before the stage of commercial harvest, when they are not otherwise capable of ripening naturally. The expression of MdARF5, a member of the auxin response factor ...[more]

PMID: 32083754

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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.

Project description:Fruit ripening is a highly coordinated developmental process driven by a complex hormonal network. Ethylene is the main regulator of climacteric fruit ripening. However, a putative role of other key phytohormones in this process cannot be excluded. We previously observed an increasing level of auxin during the post-harvest ripening of the durian fruit, which occurred concomitantly with the rise in the climacteric ethylene biosynthesis. Herein, we connect the key auxin signaling component, auxin response factors (ARFs), with the regulatory network that controls fruit ripening in durian through the identification and functional characterization of a candidate ripening-associated ARF. Our transcriptome-wide analysis identified 15 ARF members in durian (DzARFs), out of which 12 were expressed in the fruit pulp. Most of these DzARFs showed a differential expression, but DzARF2A had a marked ripening-associated expression pattern during post-harvest ripening in Monthong, a commercial durian cultivar from Thailand. Phylogenetic analysis of DzARF2A based on its tomato orthologue predicted a role in ripening through the regulation of ethylene biosynthesis. Transient expression of DzARF2A in Nicotiana benthamiana leaves significantly upregulated the expression levels of ethylene biosynthetic genes, pointing to a ripening-associated role of DzARF2A through the transcriptional regulation of ethylene biosynthesis. Dual-luciferase reporter assay determined that DzARF2A trans-activates durian ethylene biosynthetic genes. We previously reported significantly higher auxin level during post-harvest ripening in a fast-ripening cultivar (Chanee) compared to a slow-ripening one (Monthong). DzARF2A expression was significantly higher during post-harvest ripening in the fast-ripening cultivars (Chanee and Phuangmanee) compared to that of the slow-ripening ones (Monthong and Kanyao). Thus, higher auxin level could upregulate the expression of DzARF2A during ripening of a fast-ripening cultivar. The auxin-induced expression of DzARF2A confirmed its responsiveness to exogenous auxin treatment in a dose-dependent manner, suggesting an auxin-mediated role of DzARF2A in fruit ripening. We suggest that high DzARF2A expression would activate ARF2A-mediated transcription of ethylene biosynthetic genes, leading to increased climacteric ethylene biosynthesis (auxin-ethylene crosstalk) and faster ripening. Hence, we demonstrated DzARF2A as a new component of the regulatory network possibly mediating durian fruit ripening through transcriptional regulation of ethylene biosynthetic genes.

Dataset Information

Auxin-activated MdARF5 induces the expression of ethylene biosynthetic genes to initiate apple fruit ripening.

Publications

Auxin-activated MdARF5 induces the expression of ethylene biosynthetic genes to initiate apple fruit ripening.

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