Cytosolic glyceraldehyde-3-phosphate dehydrogenases play crucial roles in controlling cold-induced sweetening and apical dominance of potato (Solanum tuberosum L.) tubers

Glyceraldehyde-3-phosphate dehydrogenase (GAPDH) is an important enzyme that functions in producing energy and supplying intermediates for cellular metabolism. Recent researches indicate that GAPDHs have multiple functions beside glycolysis. However, little information is available for functions of GAPDHs in potato. Here, we identified 4 putative cytosolic GAPDH genes in potato genome and demonstrated that the StGAPC1, StGAPC2, and StGAPC3, which are constitutively expressed in potato tissues and cold inducible in tubers, encode active cytosolic GAPDHs. Cosuppression of these 3 GAPC genes resulted in low tuber GAPDH activity, consequently the accumulation of reducing sugars in cold stored tubers by altering the tuber metabolite pool sizes favoring the sucrose pathway. Furthermore, GAPCs-silenced tubers exhibited a loss of apical dominance dependent on cell death of tuber apical bud meristem (TAB-meristem). It was also confirmed that StGAPC1, StGAPC2, and StGAPC3 interacted with the autophagy-related protein 3 (ATG3), implying that the occurrence of cell death in TAB-meristem could be induced by ATG3 associated events. Collectively, the present research evidences first that the GAPC genes play crucial roles in diverse physiological and developmental processes in potato tubers. Glyceraldehyde-3-phosphate dehydrogenase (GAPDH) is an important enzyme that functions in producing energy and supplying intermediates for cellular metabolism. Recent researches indicate that GAPDHs have multiple functions beside glycolysis. However, little information is available for the function of GAPDHs in potato. Cold-induced sweetening (CIS) during low temperature storage of raw materials and sprouting control are still the two biggest challenges for potato industry. In this paper, we identify four genes that encode putative GAPC proteins in potato genome, and demonstrated that StGAPC1, StGAPC2 and StGAPC3, which are expressed in tubers and induced by cold, were active cytosolic GAPDHs. Cosuppression of these three GAPC genes a low GAPDH activity in potato tubers, promoting carbon flux shift from glycolysis toward sucrose synthesis and cleavage, hence accumulating reducing sugars in cold stored tubers. Furthermore, GAPCs-silenced tubers exhibited loss of apical dominance (AD) during potato tuber sprouting, and this special phenotype was association with cell death occurrence in tuber apical bud meristem which possible induced by autophagy-related protein 3 (ATG3)-dependent autophagy. Our results provide novel functions of GAPC genes in regulation potato quality traits, including CIS and apical dominance during sprouting.