A citrate efflux transporter important for manganese distribution and phosphorus uptake in rice

Plant J. 2023 Dec;116(6):1748-1765. doi: 10.1111/tpj.16463. Epub 2023 Sep 16.

Abstract

The plant citrate transporters, functional in mineral nutrient uptake and homeostasis, usually belong to the multidrug and toxic compound extrusion transporter family. We identified and functionally characterized a rice (Oryza sativa) citrate transporter, OsCT1, which differs from known plant citrate transporters and is structurally close to rice silicon transporters. Domain analysis depicted that OsCT1 carries a bacterial citrate-metal transporter domain, CitMHS. OsCT1 showed citrate efflux activity when expressed in Xenopus laevis oocytes and is localized to the cell plasma membrane. It is highly expressed in the shoot and reproductive tissues of rice, and its promoter activity was visible in cells surrounding the vasculature. The OsCT1 knockout (KO) lines showed a reduced citrate content in the shoots and the root exudates, whereas overexpression (OE) line showed higher citrate exudation from their roots. Further, the KO and OE lines showed variations in the manganese (Mn) distribution leading to changes in their agronomical traits. Under deficient conditions (Mn-sufficient conditions followed by 8 days of 0 μm MnCl2 · 4H2 O treatment), the supply of manganese towards the newer leaf was found to be obstructed in the KO line. There were no significant differences in phosphorus (P) distribution; however, P uptake was reduced in the KO and increased in OE lines at the vegetative stage. Further, experiments in Xenopus oocytes revealed that OsCT1 could efflux citrate with Mn. In this way, we provide insights into a mechanism of citrate-metal transport in plants and its role in mineral homeostasis, which remains conserved with their bacterial counterparts.

Keywords: CitMHS; Mn; P; citrate transporter; mineral homeostasis; rice.

MeSH terms

  • Citric Acid / metabolism
  • Gene Expression Regulation, Plant
  • Manganese / metabolism
  • Membrane Transport Proteins / metabolism
  • Minerals / metabolism
  • Oryza* / genetics
  • Oryza* / metabolism
  • Phosphorus / metabolism
  • Plant Proteins / genetics
  • Plant Proteins / metabolism
  • Plant Roots / genetics
  • Plant Roots / metabolism

Substances

  • citrate-binding transport protein
  • Manganese
  • Phosphorus
  • Membrane Transport Proteins
  • Citric Acid
  • Minerals
  • Plant Proteins