ABSCISIC ACID INSENSITIVE 5 confers cold tolerance by regulating <i>MdCBF3</i> and <i>MdJAZ1/3</i> in apple

Apple (Malus × domestica) trees suffer from low-temperature-induced cold stress, leading to huge production and economic losses. Understanding the molecular mechanism of apple plants under cold stress is the basis of cold-resistance improvement. Here, we report that a basic region/leucine zipper (bZIP) transcription factor gene, ABSCISIC ACID INSENSITIVE 5 (MdABI5), involved in ABA signaling can positively contribute to cold tolerance in apple. MdABI5 directly binds to the promoters of C-Repeat Binding Factor 3 (MdCBF3) and jasmonate ZIM domain 1/3 (MdJAZ1/3), activating the expression of MdCBF3 but inhibiting the expression of MdJAZ1/3 to regulate cold responses in apple. Because previous studies have verified that MdABI5 can interact with the transcriptional factor TEOSINTE BRANCHED/CYCLOIDEA/PROLIFERATING CELL FACTOR 15 (MdTCP15) and histone deacetylase 6 (MdHDA6), we investigated the coordinated regulations of MdTCP15-MdABI5 and MdHDA6-MdABI5 on MdCBF3 and MdJAZ1/3. MdTCP15 suppressed the transcriptional regulation of MdABI5 on MdCBF3 and MdJAZ1/3, corresponding with the negative regulatory role of MdTCP15 in response to cold stress. MdHDA6 enhanced the repression of MdABI5 on MdJAZ1/3 expression to positively regulate cold response in apple. However, MdABI5 also interacted with and recruited MdHDA6 to the promoter regions of MdJAZ1/3, resulting in histone deacetylation around MdJAZ1/3, reinforcing the repression of MdABI5 on MdJAZ1/3, and enhancing cold tolerance in apple. Our findings provide insights into the involvement of MdABI5 in apple response to cold stress, providing the basis of genetic improvement for cold-resistant germplasm using a molecular approach.