SlMPK1‐ and SlMPK2‐mediated SlBBX17 phosphorylation positively regulates CBF‐dependent cold tolerance in tomato

Abstract

Summary B‐box (BBX) proteins are an important class of zinc finger transcription factors that play a critical role in plant growth and stress response. However, the mechanisms of how BBX proteins participate in the cold response in tomato remain unclear. Here, using approaches of reverse genetics, biochemical and molecular biology we characterized a BBX transcription factor, SlBBX17, which positively regulates cold tolerance in tomato (Solanum lycopersicum). Overexpressing SlBBX17 enhanced C‐repeat binding factor (CBF)‐dependent cold tolerance in tomato plants, whereas silencing SlBBX17 increased plant susceptibility to cold stress. Crucially, the positive role of SlBBX17 in CBF‐dependent cold tolerance was dependent on ELONGATED HYPOCOTYL5 (HY5). SlBBX17 physically interacted with SlHY5 to directly promote the protein stability of SlHY5 and subsequently increased the transcriptional activity of SlHY5 on SlCBF genes under cold stress. Further experiments showed that cold‐activated mitogen‐activated protein kinases, SlMPK1 and SlMPK2, also physically interact with and phosphorylate SlBBX17 to enhance the interaction between SlBBX17 and SlHY5, leading to enhanced CBF‐dependent cold tolerance. Collectively, the study unveiled a mechanistic framework by which SlMPK1/2‐SlBBX17‐SlHY5 regulated transcription of SlCBFs to enhance cold tolerance, thereby shedding light on the molecular mechanisms of how plants respond to cold stress via multiple transcription factors.

A B‐box transcription factor OsBBX17 regulates saline‐alkaline tolerance through the MAPK cascade pathway in rice

“…Due to the large number of members of its large family, they will inevitably be positively or negatively regulated by TFs. Some key ion channel proteins are required to remain silent under normal conditions and are activated when stress is generated, such as the above-mentioned that OsWRKY53 acts directly on OsHKT1;5 and deregulates transcriptional repression of OsHKT1;5 under salt stress (Yu et al, 2023). Here, we clearly showed that the Cluster IIA HAK transporters OsHAK2 and OsHAK7 were directly transcriptionally regulated by OsBBX17 (Fig.…”

“…Interestingly, our study followed a very similar pattern to a recent study on OsWRKY53, which trans-repressed OsHKT1;5 to negatively regulate rice salt tolerance. Meanwhile, OsMKK10.2 and OsMPK6 are positive regulators of salt tolerance (Yu et al, 2023). Differently, OsMPK6 activates OsWRKY53 to weaken OsMKK10.2-OsMPK6 signaling and protect plants from overreacting to salinity (Yu et al, 2023).…”

“…Meanwhile, OsMKK10.2 and OsMPK6 are positive regulators of salt tolerance (Yu et al, 2023). Differently, OsMPK6 activates OsWRKY53 to weaken OsMKK10.2-OsMPK6 signaling and protect plants from overreacting to salinity (Yu et al, 2023). Meanwhile, direct overexpression of SlBBX17 can improve heat tolerance in tomato (Xu et al, 2022).…”

“…Protein kinase‐mediated phosphorylation toward downstream TFs and TF‐mediated transcriptional regulation on downstream genes in planta play vital roles during signal transduction in response to outside environmental stimuli (Kim et al ., 2017; Song et al ., 2023). The B‐box (BBX) zinc finger TF family has 32 members in Arabidopsis and 30 members in rice, with one or two conservative B‐box domains at the N‐terminal and sometimes a CCT (CONSTANS, CO‐like, and TOC1) domain at the C‐terminal (Khanna et al ., 2009; Gangappa & Botto, 2014), which can be divided into five subgroups based on their structural domains (Huang et al ., 2012; Bandara et al ., 2022).…”

“…CmBBX19 and CmBBX22 negatively regulate drought tolerance by modulating the expression of abiotic stress‐responsive genes in the ABA‐dependent pathway (Xu et al ., 2020; Liu et al ., 2022). Overexpression of SlBBX17 affects plant growth and enhances heat tolerance (Xu et al ., 2022), and phosphorylation of SlBBX17 by SlMPK1 and SlMPK2 positively regulates CBF‐dependent cold tolerance in tomato (Song et al ., 2023). In rice, different OsBBXs are strongly induced by abiotic stresses such as drought, cold, heavy metals, and salt stresses.…”