Allelic variation in the thioredoxin TRX-M4 determines carbon partitioning to control soluble sugar content in apple fruit.
Yuan, Jing; Wang, Hongtao; Lin, Wenyi; Liang, Yonghui; Qu, Shengtao; Zhu, Lingcheng; Zhao, Haiyan; Wei, Xiaoyu; Yuan, Yulin; Zhao, Wei; Ruan, Yongling; Ma, Fengwang; Li, Mingjun
DOI：10.1016/j.xplc.2026.101893
Abstract
Sugar content is a key determinant of apple (Malus * domestica) fruit quality, yet the genetic control of sugar composition remains poorly understood. Here, through QTL mapping in a 'Honeycrisp' * 'Qinguan' F1 population, we identified a genetic switch governing carbon partitioning during fruit maturation: THIOREDOXIN M-TYPE 4 (TRX-M4). Furthermore, a coding-region SNP revealed the genetic basis for the contrasting carbohydrate profiles-high starch/low sugar in 'Qinguan' versus high sugar/low starch in 'Honeycrisp'. The TRX-M4Y139 allele in 'Qinguan' exhibited enhanced thioredoxin activity. Transgenic lines carrying this allele showed increased activities of two starch synthesis enzymes-ADP-glucose pyrophosphorylase and starch synthase 1 (SS1). Consequently, TRX-M4Y139 promoted starch synthesis, diverting photoassimilates into a large transient starch pool and reducing sugar accumulation in developing fruits. In contrast, the TRX-M4F139 allele showed attenuated catalytic efficiency and weaker promotion of ADP-glucose pyrophosphorylase and SS1, leading to less starch accumulation and allowing a greater share of carbon to bypass the starch pool and accumulate as soluble sugars in fruit cells. This study advances our understanding of carbon flux in fruits and demonstrates how a naturally occurring thioredoxin variant functions as a molecular switch for carbon partitioning, ultimately determining fruit sweetness. The derived dCAPS marker enables rapid marker-assisted selection or precision editing of fruit sweetness, offering immediate applications for apple breeding.