Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots

The roots of most higher plants form arbuscular mycorrhiza, an ancient, phosphate-acquiring symbiosis with fungi, whereas only four related plant orders are able to engage in the evolutionary younger nitrogen-fixing root-nodule symbiosis with bacteria. Plant symbioses with bacteria and fungi require a set of common signal transduction components that redirect root cell development. Here we present two highly homologous genes from Lotus japonicus, CASTOR and POLLUX, that are indispensable for microbial admission into plant cells and act upstream of intracellular calcium spiking, one of the earliest plant responses to symbiotic stimulation. Surprisingly, both twin proteins are localized in the plastids of root cells, indicating a previously unrecognized role of this ancient endosymbiont in controlling intracellular symbioses that evolved more recently.

[1]  M. Shimizu,et al.  Leaf-specifically expressed genes for polypeptides destined for chloroplasts with domains of sigma70 factors of bacterial RNA polymerases in Arabidopsis thaliana. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[2]  M. Parniske,et al.  Evolution of signal transduction in intracellular symbiosis. , 2002, Trends in plant science.

[3]  Maureen R. Hanson,et al.  Plastids and stromules interact with the nucleus and cell membrane in vascular plants , 2004, Plant Cell Reports.

[4]  W. Webb,et al.  Exchange of protein molecules through connections between higher plant plastids. , 1997, Science.

[5]  S. Akao,et al.  Root, root hair, and symbiotic mutants of the model legume Lotus japonicus. , 2002, Molecular plant-microbe interactions : MPMI.

[6]  T L Blundell,et al.  FUGUE: sequence-structure homology recognition using environment-specific substitution tables and structure-dependent gap penalties. , 2001, Journal of molecular biology.

[7]  D. Ehrhardt,et al.  Calcium Spiking in Plant Root Hairs Responding to Rhizobium Nodulation Signals , 1996, Cell.

[8]  G. Oldroyd Dissecting Symbiosis: Developments in Nod Factor Signal Transduction , 2001 .

[9]  Martin Parniske,et al.  A TILLING Reverse Genetics Tool and a Web-Accessible Collection of Mutants of the Legume Lotus japonicus 1 , 2003, Plant Physiology.

[10]  F. Dazzo,et al.  Nodule Organogenesis and Symbiotic Mutants of the Model Legume Lotus japonicus , 1998 .

[11]  Y. Nakamura,et al.  Structural analysis of a Lotus japonicus genome. I. Sequence features and mapping of fifty-six TAC clones which cover the 5.4 mb regions of the genome. , 2001, DNA research : an international journal for rapid publication of reports on genes and genomes.

[12]  B. Roe,et al.  Medicago truncatula DMI1 Required for Bacterial and Fungal Symbioses in Legumes , 2004, Science.

[13]  M. Kawaguchi,et al.  Providing the basis for genomics in Lotus japonicus: the accessions Miyakojima and Gifu are appropriate crossing partners for genetic analyses , 2001, Molecular Genetics and Genomics.

[14]  S. Kawasaki,et al.  Genome Analysis of Lotus japonicus , 2000, Journal of Plant Research.

[15]  M. Parniske,et al.  Dual requirement of the LjSym4 gene for mycorrhizal development in epidermal and cortical cells of Lotus japonicus roots. , 2002, The New phytologist.

[16]  J. Feijó,et al.  Ion changes in legume root hairs responding to Nod factors. , 2000, Plant physiology.

[17]  P. Lerouge,et al.  Sulphated lipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa , 1991, Nature.

[18]  W. Broughton,et al.  Control of leghaemoglobin synthesis in snake beans. , 1971, The Biochemical journal.

[19]  H. Kouchi,et al.  Responses of a model legume Lotus japonicus to lipochitin oligosaccharide nodulation factors purified from Mesorhizobium loti JRL501. , 2001, Molecular plant-microbe interactions : MPMI.

[20]  T. Thykjær,et al.  Symbiotic mutants deficient in nodule establishment identified after T-DNA transformation of Lotus japonicus , 1998, Molecular and General Genetics MGG.

[21]  J. Downie,et al.  Resistance to nodulation of cv. Afghanistan peas is overcome by nodX, which mediates an O‐acetylation of the Rhizobium leguminosarum lipo‐oligosaccharide nodulation factor , 1993, Molecular microbiology.

[22]  S. Akao,et al.  Isolation of two different phenotypes of mycorrhizal mutants in the model legume plant Lotus japonicus after EMS-treatment. , 2000, Plant & cell physiology.

[23]  L. Schauser,et al.  The Lotus japonicus LjSym4 gene is required for the successful symbiotic infection of root epidermal cells. , 2000, Molecular plant-microbe interactions : MPMI.

[24]  S. Long,et al.  Rhizobium-lnduced calcium spiking in Lotus japonicus. , 2003, Molecular plant-microbe interactions : MPMI.

[25]  S. Tabata,et al.  A plant receptor-like kinase required for both bacterial and fungal symbiosis , 2002, Nature.

[26]  S. Tabata,et al.  Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases , 2003, Nature.

[27]  Youxing Jiang,et al.  Structure of the RCK Domain from the E. coli K+ Channel and Demonstration of Its Presence in the Human BK Channel , 2001, Neuron.

[28]  Youxing Jiang,et al.  Crystal structure and mechanism of a calcium-gated potassium channel , 2002, Nature.

[29]  M Taketa,et al.  Construction of a genetic linkage map of the model legume Lotus japonicus using an intraspecific F2 population. , 2001, DNA research : an international journal for rapid publication of reports on genes and genomes.

[30]  S. Tabata,et al.  Structural analysis of a Lotus japonicus genome. II. Sequence features and mapping of sixty-five TAC clones which cover the 6.5-mb regions of the genome. , 2002, DNA research : an international journal for rapid publication of reports on genes and genomes.