RRC ID 4676
Author Yano K, Yoshida S, Müller J, Singh S, Banba M, Vickers K, Markmann K, White C, Schuller B, Sato S, Asamizu E, Tabata S, Murooka Y, Perry J, Wang TL, Kawaguchi M, Imaizumi-Anraku H, Hayashi M, Parniske M.
Title CYCLOPS, a mediator of symbiotic intracellular accommodation.
Journal Proc. Natl. Acad. Sci. U.S.A.
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.
Volume 105(51)
Pages 20540-5
Published 2008-12-23
DOI 10.1073/pnas.0806858105
PII 0806858105
PMID 19074278
PMC PMC2629324
MeSH Calcium Signaling Fabaceae / microbiology* Intracellular Signaling Peptides and Proteins / classification Intracellular Signaling Peptides and Proteins / genetics Intracellular Signaling Peptides and Proteins / physiology* Lotus / microbiology Lotus / physiology Molecular Sequence Data Mutation Nuclear Localization Signals Oryza / chemistry Plant Diseases / microbiology Plant Proteins / chemistry Plant Proteins / genetics Plant Proteins / physiology* Rhizobiaceae / physiology Signal Transduction Symbiosis / genetics*
IF 9.504
Times Cited 162
WOS Category BIOCHEMISTRY & MOLECULAR BIOLOGY
Resource
Lotus / Glycine L. japonicus