Multi-omics and physiological analyses provide insights into the mechanism of Golgi manganese homeostasis in regulating the development of young tissues in rice

Abstract

Manganese (Mn) is indispensable for numerous Golgi-resident enzymatic reactions, and disruption of its homeostasis severely impairs plant growth. However, the regulatory mechanisms through which Mn dysregulation affects these metabolic processes remain largely uncharacterized. In this study, we conducted integrative physiological, transcriptomic, and N-glycoproteomic analyses of young rice tissues under Mn-deficient conditions using wild-type (WT) rice and single-knockout ( pml3 ) lines of the Golgi-localized Mn transporter PML3. Compared to WT, pml3 lines exhibited a substantial number of differentially expressed genes (DEGs) in young leaves and root tips under Mn- deficiency. In root tips, GO and KEGG enrichment analyses revealed that pml3 -upregulated DEGs were significantly enriched in polysaccharide metabolism and hormone regulatory processes, while the pml3 -downregulated DEGs were mainly associated with pathways including photosynthesis and cellular detoxification. In young leaves, GO and KEGG enrichment analyses revealed that pml3 -upregulated DEGs were significantly enriched in N-glycan biosynthesis and polysaccharide binding. The pml3- downregulated DEGs were linked to pathways such as plant-pathogen interaction and cell wall organization/biogenesis. Furthermore, the content of mannose and galacturonic acid in young leaves of pml3 lines was significantly altered under Mn deficiency. N-glycoproteomic profiling further indicated that the disruption of Golgi Mn homeostasis leads to an accumulation of complex-type N-glycans in young leaves. In conclusion, these findings advance our understanding of the physiological and molecular regulatory mechanisms underlying the response of young rice tissues to Mn deficiency.