Transcriptomic analysis reveals potential roles of polyamine and proline metabolism in waterlogged peach roots inoculated with Funneliformis mosseae and Serendipita indica

Abstract Root-associated endophytic fungi can create symbiotic relationships with trees to enhance stress tolerance, but the underlying mechanisms, especially with regard to waterlogging tolerance, remain unclear. This study aimed to elucidate the effects of Funneliformis mosseae and Serendipita indica on the growth, root cross-section structure, and root transcriptional responses of peach under waterlogging stress, with a focus on polyamine and proline metabolism. Genes and transcription factors associated with secondary cell wall biosynthesis were selected, and their expression profiles were analyzed. F. mosseae significantly increased the height, stem diameter, and leaf number of peach seedlings subjected to two weeks of waterlogging stress, whereas S. indica only significantly improved stem diameter. Both fungal species substantially increased root diameter, stele diameter, the number of late metaxylem inside the stele, and late metaxylem diameter, thus improving aeration within inoculated roots under waterlogging stress. Transcriptomic analysis of waterlogged roots identified 5425 and 5646 differentially expressed genes following inoculation with F. mosseae and S. indica, respectively. The arginine and proline metabolism and arginine biosynthesis pathways were enriched following fungal inoculations. Both fungi reduced the conversion of glutamate and ornithine for proline synthesis. However, S. indica promoted peptide-to-proline conversion by up-regulating the expression of PIPs. Although both fungi promoted the expression of genes involved in arginine and ornithine synthesis pathway, only F. mosseae led to increased levels of arginine and ornithine. Additionally, F. mosseae promoted the accumulation of putrescine and maintained polyamine homeostasis by down-regulating PAO2 and SAMDC. Moreover, F. mosseae facilitated the metabolism of cadaverine. In conclusion, both F. mosseae and S. indica formed symbiotic relationships with peach, with F. mosseae primarily improving polyamine accumulation and S. indica predominantly facilitating proline accumulation for enhanced waterlogging resistance.