Molecular identification of sugarcane glyceraldehyde-3-phosphate dehydrogenases and their involvement in SCMV infection in sugarcane

Glyceraldehyde-3-phosphate dehydrogenase (GAPDH) is one of the key enzymes of glycolysis and plays important roles in plant growth, development and plant–pathogen interactions. However, studies on the characteristics and functions of sugarcane ( Saccharum spp. hybrid) GAPDH family genes are still lacking. In the present study, 24, 75 and 91 GAPDH genes were identified in Saccharum spontaneum and sugarcane cultivars R570 and XTT22 , respectively. A phylogenetic tree revealed that these genes could be divided into four groups, i.e., the GAPC group, the GAPA group, the GAPB group and the GAPCp group. These GAPDH genes contained multiple cis -acting elements related to stress and hormone response. RNA-seq analysis demonstrated that the S. spontaneum GAPDH genes and XTT22-GAPDH genes were constitutively expressed at different developmental stages or in different tissues. ScGAPA , ScGAPB , ScGAPC and ScGAPCp , representatives of each group of the GAPDH family, were isolated from the sugarcane cultivar XTT22 . RT qPCR analysis revealed that the expression levels of ScGAPA and ScGAPB were exponentially greater than those of ScGAPC or ScGAPCp in the leaves; these four genes were differentially expressed upon SCMV infection and after abiotic treatments such as NaCl, salicylic acid, H 2 O 2 or MeJA. DAB staining and detection of ATG8-I and ATG8-II demonstrated that SCMV infection induces bursts of reactive oxygen species and autophagy in sugarcane leaves. ScGAPA, ScGAPB, ScGAPC, and ScGAPCp interacted with ScATG3, thereby suppressing autophagy in Nicotiana benthamiana plants. However, oxidative stress impaired the interaction of ScATG3 with ScGAPA, ScGAPB, ScGAPC and ScGAPCp, indicating that SCMV infection activates autophagy by disrupting ScGAPDH–ScATG3 interactions. The present study reveals the origin and evolution of the GAPDH gene family in sugarcane and the potential roles of this gene family in response to sugarcane mosaic virus (SCMV) infection. Interaction of ScGAPDHs with ScATG3 balances with ROS and autophagy upon SCMV infection. Normally, ScGAPDHs interact with ScATG3, which inhibits the autophagy. ROS was generated upon SCMV infection. Under without SCMV conditions, ScGAPA, ScGAPB, ScGAPC, ScGAPCp interaction with ScATG3. Under SCMV conditions, Intracellular production of ROS in sugarcane leaves, along with upregulated expression levels of ScGAPA, ScGAPC, ScGAPCp and downregulated expression levels of ScGAPB. meanwhile, ROS inhibit the interaction of ScGAPA, ScGAPB, ScGAPC, ScGAPCp interaction with ScATG3 and thereby induce autophagy. • A total of 190 GAPDH genes were identified in S. spontaneum , R570 and XTT22 genome. • ScGAPA , ScGAPB , ScGAPC , and ScGAPCp are differently expressed upon SCMV infection. • Sugarcane GAPDHs interact with ScATG3, thereby suppressing autophagy. • ROS impairs the interaction of Sugarcane GAPDHs with ScATG3 and enhances autophagy.