Abstract
In soybeans, eighteen members constitute the serine hydroxymethyltransferase (GmSHMT) gene family, of which the cytosolic-targeted GmSHMT08c member has been reported to mediate resistance to soybean cyst nematode (SCN). This work presents a comprehensive study of the SHMT gene family members, including synteny, phylogeny, subcellular localizations, haplotypes, protein homology modeling, mutational, and expression analyses. Phylogenetic analysis showed that SHMT genes are divided into four classes reflecting their subcellular distribution (cytosol, nucleus, mitochondrion, and chloroplast). Subcellular localization of selected GmSHMT members supports their in-silico predictions and phylogenetic distribution. Expression and functional analyses showed that GmSHMT genes display many overlapping, but some divergent responses during SCN infection. Furthermore, mutational analysis reveals that all isolated EMS mutants that lose their resistance to SCN carry missense and nonsense mutations at the GmSHMT08c, but none of the Gmshmt08c mutants carried mutations in the other GmSHMT genes. Haplotype clustering analysis using the whole genome resequencing data from a collection of 106 diverse soybean germplams (15X) was performed to identify allelic variants and haplotypes within the GmSHMT gene family. Interestingly, only the cytosolic-localized GmSHMT08c presented SNP clusters that were associated with SCN resistance, supporting our mutational analysis. Although eight GmSHMT members respond to the nematode infestation, functional and mutational analysis has shown the absence of functional redundancy in resistance to SCN. Structural analysis and protein homology modeling showed the presence of spontaneous mutations at important residues within the GmSHMT proteins, suggesting the presence of altered enzyme activities based on substrate affinities. Due to the accumulation of mutations during the evolution of the soybean genome, the other GmSHMT members have undergone neofunctionalization and subfunctionalization events.
Highlights
Soybean [Glycine max (L.) Merr.] is the most widely consumed legume crop worldwide
GmSHMT gene family members encode proteins that vary in size between 471aa and 603aa, except the GmSHMT15 gene that encodes a truncated protein resulting in 244aa (Supplementary Fig. S1)
The soybean genome contains a high number of serine hydroxylmethyltransferase (SHMT) genes, compared to the plant model A. thaliana (7 members), S. lycopersicum (7), or M. truncatula (12) (Supplementary Table S2)
Summary
Soybean [Glycine max (L.) Merr.] is the most widely consumed legume crop worldwide. soybean production is limited by the presence of the soybean cyst nematode (SCN; Heterodera glycines I.), causing over $1 billion in yield losses annually in the U.S.1. A member of the dicot gene family (GmSHMT08c) underlying the Rhg[4] loci has been reported to be involved in SCN resistance. Little is known about the role of the other GmSHMT genes in plant abiotic stresses, and if the rest of the GmSHMT gene family (or some members) can play similar roles as the GmSHMT08 and may present functional redundancy or additive effect in resistance to SCN, as it has been reported recently in case of the GmSNAP gene family[19]. Mutations at the cytosol-targeted GmSHMT08c but not on the other GmSHMT members result in the loss of resistance to SCN in the resistant c.v Forrest lines[3]. We report a detailed characterization of the GmSHMT gene family in soybean including structure, synteny, phylogeny, expression, homology modeling, subcellular localization, and mutational analyses
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