Quantitative proteomic analysis of Malus halliana exposed to salt-alkali mixed stress reveals alterations in energy metabolism and stress regulation

Abstract

Soil salinization is a major abiotic stress in apple production; consequently, it is important to improve the salt tolerance of apple trees. Here, a physiological analysis and isobaric tags for relative and absolute quantitation-based proteomics were combined, with a particular interest in proteomic changes in seedling leaves of the apple rootstock Malus halliana induced by a mixed salt–alkali (100 mM NaCl + NaHCO3) stress. The salt–alkali stress produced significant stress symptoms with time, including decreased chlorophyll and leaf water contents. Using proteomics, 179 differentially expressed salt–alkali-responsive proteins were identified. These proteins were involved in the TCA cycle, glycolysis, oxidative phosphorylation, pentose phosphate pathway, starch and sucrose metabolism, and amino sugar and nucleotide sugar metabolism, revealing that M. halliana likely regulated carbohydrate metabolism to satisfy energy and substrate needs. Additionally, Photosystem I and II proteins were up-regulated, enhancing the photosynthetic capacity. The related catalase, superoxide dismutase and peroxidase proteins facilitated the detoxification of reactive oxygen species and maintained redox homeostasis. Auxin, salicylic acid and abscisic acid promoted cell enlargement, resistance and stomatal closure. Additionally, the plants were better adapted to stress owing to enhanced protein processing and synthesis, as well as accelerated protein replacement. This study provides new information on the molecular networks of energy metabolism and stress regulation that can be used to develop salt–alkali-tolerant apple rootstocks.