Journal Article

MaHsf24, a novel negative modulator, regulates cold tolerance in banana fruits by repressing the expression of HSPs and antioxidant enzyme genes

Shan, Wei, Fan, Zhong‐qi, Si, Jia, Kuang, Jian‐fei, Lu, Wang‐jin, Wei, Wei, Wu, Chao‐jie, Chen, Jian‐ye, Yang, Ying‐ying

2024

Overview

Summary Transcriptional regulation mechanisms underlying chilling injury (CI) development have been widely investigated in model plants and cold‐sensitive fruits, such as banana (Musa acuminata). However, unlike the well‐known NAC and WRKY transcription factors (TFs), the function and deciphering mechanism of heat shock factors (HSFs) involving in cold response are still fragmented. Here, we showed that hot water treatment (HWT) alleviated CI in harvested banana fruits accomplishing with reduced reactive oxygen species (ROS) accumulation and increased antioxidant enzyme activities. A cold‐inducible but HWT‐inhibited HSF, MaHsf24, was identified. Using DNA affinity purification sequencing (DAP‐seq) combined with RNA‐seq analyses, we found three heat shock protein (HSP) genes (MaHSP23.6, MaHSP70‐1.1 and MaHSP70‐1.2) and three antioxidant enzyme genes (MaAPX1, MaMDAR4 and MaGSTZ1) were the potential targets of MaHsf24. Subsequent electrophoretic mobility shift assay (EMSA), chromatin immunoprecipitation coupled with quantitative PCR (ChIP‐qPCR) and dual‐luciferase reporter (DLR) analyses demonstrated that MaHsf24 repressed the transcription of these six targets via directly binding to their promoters. Moreover, stably overexpressing MaHsf24 in tomatoes increased cold sensitivity by suppressing the expressions of HSPs and antioxidant enzyme genes, while HWT could recover cold tolerance, maintaining higher levels of HSPs and antioxidant enzyme genes, and activities of antioxidant enzymes. In contrast, transiently silencing MaHsf24 by virus‐induced gene silencing (VIGS) in banana peels conferred cold resistance with the upregulation of MaHSPs and antioxidant enzyme genes. Collectively, our findings support the negative role of MaHsf24 in cold tolerance, and unravel a novel regulatory network controlling bananas CI occurrence, concerning MaHsf24‐exerted inhibition of MaHSPs and antioxidant enzyme genes.

• Publisher: John Wiley & Sons, Inc,John Wiley and Sons Inc
• Subject: Abiotic stress / antioxidant enzyme genes / antioxidant enzymes / Antioxidants / Antioxidants - metabolism / banana fruits / Bananas / biotechnology / Chromatin / chromatin immunoprecipitation / cold / Cold resistance / Cold shock / Cold storage / Cold Temperature / Cold tolerance / Disease resistance / DNA / DNA sequencing / Electrophoretic mobility / Enzymatic activity / Enzymes / Fruit - genetics / Fruit - metabolism / Fruits / gel electrophoresis / Gene expression / Gene Expression Regulation, Plant / Gene regulation / Gene sequencing / Gene silencing / Genes / Heat / Heat shock factors / Heat shock proteins / heat stress / Heat-Shock Proteins - genetics / Heat-Shock Proteins - metabolism / hot water treatment / Hsf / Immunoprecipitation / Low temperature resistance / Musa - genetics / Musa - metabolism / Musa acuminata / Plant Proteins - genetics / Plant Proteins - metabolism / Protein purification / quantitative polymerase chain reaction / Reactive oxygen species / Reactive Oxygen Species - metabolism / sequence analysis / Signal transduction / Tobacco / Tomatoes / transcription (genetics) / Transcription factors / Transcription Factors - genetics / Transcription Factors - metabolism / transcriptional regulation / Water treatment / Yeast