RanGAP2 mediates nucleocytoplasmic partitioning of the NB-LRR immune receptor Rx in the Solanaceae, thereby dictating Rx function

W.I.L. Tameling, C. Nooijen, N. Ludwig, M. Boter, E.J. Slootweg, A. Goverse, K. Shirasu, M.H.A.J. Joosten

Research output: Contribution to journalArticleAcademicpeer-review

98 Citations (Scopus)

Abstract

The potato (Solanum tuberosum) nucleotide binding–leucine-rich repeat immune receptor Rx confers resistance to Potato virus X (PVX) and requires Ran GTPase-activating protein 2 (RanGAP2) for effective immune signaling. Although Rx does not contain a discernible nuclear localization signal, the protein localizes to both the cytoplasm and nucleus in Nicotiana benthamiana. Transient coexpression of Rx and cytoplasmically localized RanGAP2 sequesters Rx in the cytoplasm. This relocation of the immune receptor appeared to be mediated by the physical interaction between Rx and RanGAP2 and was independent of the concomitant increased GAP activity. Coexpression with RanGAP2 also potentiates Rx-mediated immune signaling, leading to a hypersensitive response (HR) and enhanced resistance to PVX. Besides sequestration, RanGAP2 also stabilizes Rx, a process that likely contributes to enhanced defense signaling. Strikingly, coexpression of Rx with the Rx-interacting WPP domain of RanGAP2 fused to a nuclear localization signal leads to hyperaccumulation of both the WPP domain and Rx in the nucleus. As a consequence, both Rx-mediated resistance to PVX and the HR induced by auto-active Rx mutants are significantly suppressed. These data show that a balanced nucleocytoplasmic partitioning of Rx is required for proper regulation of defense signaling. Furthermore, our data indicate that RanGAP2 regulates this partitioning by serving as a cytoplasmic retention factor for Rx
Original languageEnglish
Pages (from-to)4176-4194
JournalThe Plant Cell
Volume22
DOIs
Publication statusPublished - 2010

Keywords

  • disease resistance protein
  • potato-virus-x
  • gtpase-activating protein
  • leucine-rich repeat
  • nuclear transport factor-2
  • gene confers resistance
  • plant innate immunity
  • tobacco-mosaic-virus
  • cell-death
  • ran-gtpase

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