Ethylene inhibits malate accumulation in apple by transcriptional repression of aluminum‐activated malate transporter 9 via the WRKY31‐ERF72 network

Summary Malic acid accumulation in the vacuole largely determines acidity and perception of sweetness of apple. It has long been observed that reduction in malate level is associated with increase in ethylene production during the ripening process of climacteric fruits, but the molecular mechanism l...

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Published in:The New phytologist 2023-08, Vol.239 (3), p.1014-1034
Main Authors: Wang, Jia‐Hui, Gu, Kai‐Di, Zhang, Quan‐Yan, Yu, Jian‐Qiang, Wang, Chu‐Kun, You, Chun‐Xiang, Cheng, Lailiang, Hu, Da‐Gang
Format: Article
Language:English
Subjects:
Accumulation
Acidity
Aluminium
Aluminum
Aluminum - metabolism
Apples
Ethene
Ethylene
Ethylenes - metabolism
Fruit - genetics
Fruit - metabolism
Fruits
Gene Expression Regulation, Plant
Gene silencing
Malate
Malates - metabolism
Malic acid
Malus - genetics
Malus - metabolism
Malus domestica
MdALMT9
MdERF72
MdWRKY31
Molecular modelling
Plant Proteins - genetics
Plant Proteins - metabolism
Reduction
Ripening
Sweetness
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Summary:Summary Malic acid accumulation in the vacuole largely determines acidity and perception of sweetness of apple. It has long been observed that reduction in malate level is associated with increase in ethylene production during the ripening process of climacteric fruits, but the molecular mechanism linking ethylene to malate reduction is unclear. Here, we show that ethylene‐modulated WRKY transcription factor 31 (WRKY31)–Ethylene Response Factor 72 (ERF72)–ALUMINUM ACTIVATED MALATE TRANSPORTER 9 (Ma1) network regulates malate accumulation in apple fruit. ERF72 binds to the promoter of ALMT9, a key tonoplast transporter for malate accumulation of apple, transcriptionally repressing ALMT9 expression in response to ethylene. WRKY31 interacts with ERF72, suppressing its transcriptional inhibition activity on ALMT9. In addition, WRKY31 directly binds to the promoters of ERF72 and ALMT9, transcriptionally repressing and activating ERF72 and ALMT9, respectively. The expression of WRKY31 decreases in response to ethylene, lowering the transcription of ALMT9 directly and via its interactions with ERF72. These findings reveal that the regulatory complex WRKY31 forms with ERF72 responds to ethylene, linking the ethylene signal to ALMT9 expression in reducing malate transport into the vacuole during fruit ripening. See also the Commentary on this article by Martinoia & Neuhaus, 239: 821–823.
ISSN:0028-646X
1469-8137
DOI:10.1111/nph.18795