Arabidopsis NPF2.13 functions as a critical transporter of bacterial natural compound tunicamycin in plant–microbe interaction

• Published in: The New phytologist 2023-04, Vol.238 (2), p.765-780
• Main Authors: Liu, Chuanfa, Hao, Dongdong, Sun, Ruixue, Zhang, Yi, Peng, Yang, Yuan, Yang, Jiang, Kai, Li, Wenyang, Wen, Xing, Guo, Hongwei
• Format: Article
• Language: English
• Subjects: Allelochemicals; Anion Transport Proteins - metabolism; Antibiotics; Arabidopsis; Arabidopsis - genetics; Arabidopsis - metabolism; Arabidopsis Proteins - metabolism; Arabidopsis thaliana; Bacteria; bacterial metabolites; Biological activity; Gene expression; Gene Expression Regulation, Plant; Glycosylation; Host plants; Hypersensitivity; Identities; Metabolites; Microorganisms; Nitrates; Nitrates - metabolism; NPF2.13; Nutrition; Pathogens; Plant bacterial diseases; Plant nutrition; Plant Proteins - metabolism; Plants; plant–microbe interaction; Protein transport; Proteins; Streptomyces; Streptomyces sp; Substrates; Transport; Tunicamycin; Tunicamycin - pharmacology; Uptake; Volatile compounds; Volatiles
• ISSN: 0028-646X; 1469-8137
• DOI: 10.1111/nph.18752

Summary Metabolites including antibiotics, enzymes, and volatiles produced by plant‐associated bacteria are key factors in plant–microbiota interaction that regulates various plant biological processes. There should be crucial mediators responsible for their entry into host plants. However, less is known about the identities of these plant transporters. We report that the Arabidopsis Nitrate Transporter1 (NRT1)/NPF protein NPF2.13 functions in plant uptake of tunicamycin (TM), a natural antibiotic produced by several Streptomyces spp., which inhibits protein N‐glycosylation. Loss of NPF2.13 function resulted in enhanced TM tolerance, whereas NPF2.13 overexpression led to TM hypersensitivity. Transport assays confirmed that NPF2.13 is a H+/TM symporter and the transport is not affected by other substrates like nitrate. NPF2.13 exclusively showed TM transport activity among tested NPFs. Tunicamycin uptake from TM‐producing Streptomyces upregulated the expression of nitrate‐related genes including NPF2.13. Moreover, nitrate allocation to younger leaves was promoted by TM in host plants. Tunicamycin could also benefit plant defense against the pathogen. Notably, the TM effects were significantly repressed in npf2.13 mutant. Overall, this study identifies NPF2.13 protein as an important TM transporter in plant–microbe interaction and provides insights into multiple facets of NPF proteins in modulating plant nutrition and defense by transporting exterior bacterial metabolites.