Regulation of spikelet developmental responses to chilling and freezing stress mediated by differential sugar metabolism in winter wheat

Spring cold stress poses a great threat to wheat reproductive growth, leading to compromised spike development and grain yield. There are two types of cold stress i.e. chilling stress (CS, above zero) and freezing stress (FS, below zero). However, it is unclear whether there is a difference in the mechanism of CS and FS in regulating spikelet development. This study aimed to unravel the underlying regulation in determining the difference for wheat spikelet exposed to CS at 2 °C and FS at −2°C by integrative analyses of transcriptome, metabolome, and physiology. Delayed floret development and shrunken cellular morphology in both CS and FS were observed, even malformation and degradation of anther cells occurred in FS. Kyoto Encyclopedia of gene and genomes (KEGG) analyses revealed that the most abundantly enriched pathways are phytohormone biosynthesis, starch and sucrose metabolism, and phenylpropanoid biosynthesis. Further physiological assays related to the identified pathways were performed. Compared to CS, the signal of abscisic acid (ABA), salicylic acid (SA) and jasmonic acid (JA) was more pronounced, and the signal of auxin (IAA) and gibberellin (GA) was inhibited further in FS. In addition, the contents of glucose, fructose and trehalose were elevated in CS, owing to greater activities of cell wall invertase and sucrose synthase, while the hexose content was decreased owing to lower activities of such enzymes in FS, concomitantly, flavonoid barely changed in CS, but it dramatically amounted in FS. Taken together, the glucose and trehalose pathway, along with induced ABA and SA signal were intensified in CS to maintain growth, while greater flavonoid and promoted JA synthesis were induced in FS for cold survival. Understanding the molecular of growth-defense under cold stress would provide a foundation for the development of breeding strategies.