Unravelling structural, functional, evolutionary and genetic basis of SWEET transporters regulating abiotic stress tolerance in maize

Abstract

Sugars Will Eventually be Exported Transporters (SWEETs) are the novel sugar transporters widely distributed among living systems. SWEETs play a crucial role in various bio-physiological processes, viz., plant developmental, nectar secretion, pollen development, and regulation of biotic and abiotic stresses, in addition to their prime sugar-transporting activity. Thus, in-depth structural, evolutionary, and functional characterization of maize SWEET transporters was performed for their utility in maize improvement. The mining of SWEET genes in the latest maize genome release (v.5) showed an uneven distribution of 20 ZmSWEETs. The comprehensive structural analyses and docking of ZmSWEETs with four sugars, viz., fructose, galactose, glucose, and sucrose, revealed frequent amino acid residues forming hydrogen (asparagine, valine, serine) and hydrophobic (tryptophan, glycine, and phenylalanine) interactions. Evolutionary analyses of SWEETs showed a mixed lineage with 50–100 % commonality of ortho-groups and -sequences evolved under strong purifying selection (Ka/Ks < 0.5). The duplication analysis showed non-functionalization (ZmSWEET18 in B73) and neo- and sub-functionalization (ZmSWEET3, ZmSWEET6, ZmSWEET9, ZmSWEET19, and ZmSWEET20) events in maize. Functional analyses of ZmSWEET genes through co-expression, in silico expression and qRT-PCR assays showed the relevance of ZmSWEETs expression in regulating drought, heat, and waterlogging stress tolerances in maize. The first ever ZmSWEET-regulatory network revealed 286 direct (ZmSWEET-TF: 140 ZmSWEET-miRNA: 146) and 1226 indirect (TF-TF: 597; TF-miRNA: 629) edges. The present investigation has given new insights into the complex transcriptional and post-transcriptional regulation and the regulatory and functional relevance of ZmSWEETs in assigning stress tolerance in maize.