ShWRKY55 enhances the cold resistance of wild tomato LA1777 by regulating the expression of the key gene ShSAMDC2 involved in polyamine synthesis

Abstract

Wild tomatoes, which are the natural ancestors of the tomato genus, exhibit a wide range of genetic diversity and adaptability. They possess unique characteristics in terms of their ability to withstand cold stress, which sets them apart from cultivated tomatoes. However, the specific mechanisms underlying the differences in cold tolerance between wild and cultivated tomatoes remain unclear. Studies have shown that the expression of SAMDC2, a gene involved in the synthesis of spermidine (Spd), significantly increases in both wild tomato (S. habrochaites) LA1777 and cultivated tomato (S. lycopersicum) AC after exposure to cold stress. Additionally, the content of Spd also increases significantly in these materials, particularly in wild tomato LA1777. Further analysis, involving the use of exogenous Spd and the polyamine synthesis inhibitor MGBG under cold stress conditions, has revealed that the application of exogenous Spd enhances the plant’s cold tolerance by increasing the endogenous Spd content, while the use of MGBG inhibits Spd accumulation and reduces the plant’s cold tolerance. By comparing the cis-acting regulatory elements in the SAMDC2 promoter of both materials, we discovered that wild tomato LA1777 possesses an extra W-box compared to cultivated tomato AC. Through yeast one-hybrid, EMSA, and dual-luciferase assays, we demonstrated that ShWRKY55 can target the promoter of ShSAMDC2 and regulate its upregulation expression. Our study suggests that the stronger cold resistance observed in wild tomato LA1777, as compared to cultivated tomato AC, can be attributed to the regulation of ShSAMDC2 expression through ShWRKY55 after exposure to cold stress, which leads to higher Spd accumulation. However, this regulatory mechanism is absent in cultivated tomatoes. This research contributes to our understanding of the distinct adaptation mechanisms of wild and cultivated tomatoes to cold stress and provides novel insights and strategies for improving the cold tolerance of cultivated tomatoes.