Genome-Wide Identification of the GmATG Gene Family and Its Response to Multiple Biotic and Abiotic Stresses in Soybean (Glycine max)

Abstract

Background: Autophagy plays a central role in maintaining cellular homeostasis, regulating growth and development, and responding to multiple stresses. Autophagy-related genes (ATGs) play critical roles in autophagy, yet their functional diversity in soybean (Glycine max) remains underexplored. Methods: Genome-wide identification of GmATG genes was performed using sequence similarity and domain-based searches against the Wm82.gnm4 reference genome, followed by characterization of physicochemical properties, chromosomal distribution, phylogenetic relationships, gene duplication, conserved motifs, gene structure, three-dimensional structural, and promoter cis-acting elements. Tissue-specific expression and multiple stresses response were examined using transcriptome data and profiled by RT-qPCR. Results: A total of 60 GmATG genes belonging to 20 subfamilies were identified in soybean. Gene family expansion was predominantly driven by fragment duplication (33 gene pairs), with the ATG8 family expanding to 12 members, and pan-genomic analysis uncovered prominent copy number variation (6–9 copies) in the ATG18 family. GmATG genes showed distinct expression patterns in response to multiple abiotic and biotic stresses. Specifically, GmATG18f was significantly induced by phosphorus deficiency in the low-phosphorus-tolerant soybean variety Nannong 94-156. GmATG8g, GmATG9d and GmATG13d showed a typical expression trend of initial increase followed by decrease, with expression levels peaking at 6–12 h after salt stress treatment. GmATG8g and GmATG9d were rapidly upregulated at the early drought stress stage, while GmATG13a maintained sustained upregulation. In response to Phomopsis stem rot, GmATG7a/8h/8i/11/13d/18e/18f displayed differential expression in resistant and susceptible soybean materials. Conclusions: This study systematically characterizes the composition, expansion and stress response patterns of the GmATG gene family, revealing functional differentiation among family members. The identified key candidate genes, including abiotic-stress-regulated GmATG8g/9d/13d/18f and biotic-stress-regulated GmATG7a/8h/8i/11/13d/18e/18f, provide valuable genetic resources for the molecular breeding of stress-tolerant soybean.