Abstract

High temperature (HT) is one of the most important environmental stress factors and seriously threatens plant growth, development, and production. VQ motif-containing proteins are transcriptional regulators that have been reported to regulate plant growth and developmental processes, including responses to biotic and abiotic stresses. However, the relationships between VQ motif-containing proteins and HT stress have not been studied in depth in plants. In this study, transgenic apple (Malus domestica) plants overexpressing the apple VQ motif-containing protein-coding gene (MdVQ37) were exposed to HT stress, and the transgenic lines exhibited a heat-sensitive phenotype. In addition, physiological and biochemical studies revealed that, compared with WT plants, transgenic lines had lower enzymatic activity and photosynthetic capacity and lower amounts of nonenzymatic antioxidant system metabolites under HT stress. Transcriptome analysis revealed 1379 genes whose expression differed between the transgenic lines and WT plants. GO and KEGG pathway analyses showed that transcription factor activity and plant hormone signaling pathways were differentially influenced and enriched in the transgenic lines. Salicylic acid (SA) content analysis indicated that overexpression of MdVQ37 reduced the content of endogenous SA by regulating the expression of SA catabolism-related genes, which ultimately resulted in disruption of the SA-dependent signaling pathway under HT stress. The application of SA slightly increased the survival rate of the transgenic lines under HT stress. Taken together, our results indicate that apple MdVQ37 has a regulatory function in basal thermotolerance by modulating the activity of transcription factors and SA homeostasis. Overall, this study provides novel insights that improve our understanding of the various functions of VQ motif-containing proteins.

Highlights

  • As sessile organisms, plants cannot escape the effects of environmental stress during their growth and development, and high temperature (HT) is among the major types of environmental stress

  • The expression of MdVQ12 increased 8.45-fold after treatment for 4 h compared with that of the control (Fig. S1); the expression level of MdVQ37 decreased 49-fold after treatment for 8 h compared with that of the control (Fig. S1). These results suggest that multiple VQ genes are involved in the response to HT stress in apples

  • VQ motif-containing proteins act as transcriptional regulators controlling a series of biological processes, such as plant growth, development, defense responses, and stress tolerance mechanisms

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Summary

Introduction

Plants cannot escape the effects of environmental stress during their growth and development, and high temperature (HT) is among the major types of environmental stress. Dong et al Horticulture Research (2021)8:220 damage to thylakoids, severely limiting the photosynthetic electron transfer rate of plant photosystems (PSs) and the activity of several related enzymes and rapidly inhibiting photosynthesis in plants[6]. HT stress disrupts the oxygen-evolving complex, resulting in an imbalance during the energy conversion between the photosystem II (PSII) oxygen-evolving complex and the receptor site of the photosystem, resulting in irreversible damage to PSII and greatly reducing its activity[6,7]. HT stress can disrupt the dynamic balance between harmful reactive oxygen species (ROS) production and removal in plants, and the accumulation of superoxide anions (O2.−), hydrogen peroxide (H2O2), singlet oxygen species (1O2), and hydroxyl radicals (OH–) increases the degree of membrane lipid peroxidation, leading to oxidative stress[6,10]

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