CYCLOPS, a mediator of symbiotic intracellular accommodation

Koji Yano, Satoko Yoshida, Judith Müller, Sylvia Singh, Mari Banba, Kate Vickers, Katharina Markmann, Catharine White, Bettina Schuller, Shusei Sato, Erika Asamizu, Satoshi Tabata, Yoshikatsu Murooka, Jillian Perry, Trevor L. Wang, Masayoshi Kawaguchi, Haruko Imaizumi-Anraku, Makoto Hayashi, Martin Parniske

Research output: Contribution to journalArticlepeer-review

264 Citations (Scopus)

Abstract

The initiation of intracellular infection of legume roots by symbiotic rhizobia bacteria and arbuscular mycorrhiza (AM) fungi is preceded by the induction of calcium signatures in and around the nucleus of root epidermal cells. Although a calcium and calmodulin-dependent kinase (CCaMK) is a key mediator of symbiotic root responses, the decoding of the calcium signal and the molecular events downstream are only poorly understood. Here, we characterize Lotus japonicus cyclops mutants on which microbial infection was severely inhibited. In contrast, nodule organogenesis was initiated in response to rhizobia, but arrested prematurely. This arrest was overcome when a deregulated CCaMK mutant version was introduced into cyclops mutants, conferring the development of full-sized, spontaneous nodules. Because cyclops mutants block symbiotic infection but are competent for nodule development, they reveal a bifurcation of signal transduction downstream of CCaMK. We identified CYCLOPS by positional cloning. CYCLOPS carries a functional nuclear localization signal and a predicted coiled-coil domain. We observed colocalization and physical interaction between CCaMK and CYCLOPS in plant and yeast cell nuclei in the absence of symbiotic stimulation. Importantly, CYCLOPS is a phosphorylation substrate of CCaMK in vitro. Cyclops mutants of rice were impaired in AM, and rice CYCLOPS could restore symbiosis in Lotus cyclops mutants, indicating a functional conservation across angiosperms. Our results suggest that CYCLOPS forms an ancient, preassembled signal transduction complex with CCaMK that is specifically required for infection, whereas organogenesis likely requires additional yet-to-be identified CCaMK interactors or substrates.

Original languageEnglish
Pages (from-to)20540-20545
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume105
Issue number51
DOIs
Publication statusPublished - 2008 Dec 23
Externally publishedYes

Keywords

  • BiFC
  • Map-based cloning
  • Plant-microbe symbiosis
  • Protein phosphorylation
  • Protein-protein interaction

ASJC Scopus subject areas

  • General

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