A Golgi-Located Transmembrane Nine Protein Gene TMN11 Functions in Manganese/Cadmium Homeostasis and Regulates Growth and Seed Development in Rice

Abstract

Metal transporters play crucial roles in plant nutrition, development, and metal homeostasis. To date, several multi-proteins have been identified for metal transport across the plasma membrane and tonoplast. Nevertheless, Golgi endomembrane metal carriers and their mechanisms are less documented. In this study, we identified a new transmembrane nine (TMN) family gene, TMN11, which encodes a Mn transport protein that was localized to the cis-Golgi endomembrane in rice. OsTMN11 contains a typically conserved long luminal N-terminal domain and nine transmembrane domains. OsTMN11 was ubiquitously expressed over the lifespan of rice and strongly upregulated in young rice under excess Mn(II)/Cd(II) stress. Ectopic expression of OsTMN11 in an Mn-sensitive pmr1 mutant (PMR1 is a Golgi-resident Mn exporter) yeast (Saccharomyces cerevisiae) restored the defective phenotype and transported excess Mn out of the cells. As ScPMR1 mediates cellular Mn efflux via a vesicle-secretory pathway, the results suggest that OsTMN11 functions in a similar manner. OsTMN11 knockdown (by RNAi) compromised the growth of young rice, manifested as shorter plant height, reduced biomass, and chlorosis under excessive Mn and Cd conditions. Two lifelong field trials with rice cropped in either normal Mn supply conditions or in Cd-contaminated farmland demonstrated that knockdown of OsTMN11 impaired the capacity of seed development (including panicle, spikelet fertility, seed length, grain weight, etc.). The mature RNAi plants contained less Mn but accumulated Cd in grains and rice straw, confirming that OsTMN11 plays a fundamental role in metal homeostasis associated with rice growth and development even under normal Mn supply conditions.

Golgi in and out: multifaceted role and journey of manganese

“…Thus, expanding the inventory of Golgi transporters and assigning them to specialized Golgi compartments and to synthesis of specific cellular glycosylated compounds will help tackle individual steps of the glycosylation pathway in the cell. A recent study reported Mn transport activity of a cis‐Golgi localized member of the transmembrane nine (TMN) transporter family of rice, OsTMN11, that efficiently restores growth of yeast lacking the Golgi‐resident Mn importer PMR1 (H. Li et al ., 2022). Mutation of a related member in Arabidopsis, AtTMN1/EMP12, which is also localized in Golgi, affects deposition of pectins (Hiroguchi et al ., 2021).…”