NSP1 is a component of the Myc signaling pathway.

Nodulation and arbuscular mycorrhization require the activation of plant host symbiotic programs by Nod factors, and Myc-LCOs and COs, respectively. The pathways involved in the perception and downstream signaling of these signals include common and distinct components. Among the distinct components, NSP1, a GRAS transcription factor, has been considered for years to be specifically involved in nodulation. Here, we analyzed the degree of conservation of the NSP1 sequence in arbuscular mycorrhizal (AM) host and non-AM host plants and carefully examined the ability of Medicago truncatula nsp1 mutants to respond to Myc-LCOs and to be colonized by an arbuscular mycorrhizal fungus. In AM-host plants, the selection pressure on NSP1 is stronger than in non-AM host ones. The response to Myc-LCOs and the frequency of mycorrhizal colonization are significantly reduced in the nsp1 mutants. Our results reveal that NSP1, previously described for its involvement in the Nod factor signaling pathway, is also involved in the Myc-LCO signaling pathway. They bring additional evidence on the evolutionary relatedness between nodulation and mycorrhization.

[1]  Andrea Genre,et al.  Short-chain chitin oligomers from arbuscular mycorrhizal fungi trigger nuclear Ca2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. , 2013, The New phytologist.

[2]  Y. Kamiya,et al.  Inhibition of shoot branching by new terpenoid plant hormones , 2008, Nature.

[3]  A. Muñoz,et al.  GRAS Proteins Form a DNA Binding Complex to Induce Gene Expression during Nodulation Signaling in Medicago truncatula[W] , 2009, The Plant Cell Online.

[4]  E. Journet,et al.  MtENOD11 gene activation during rhizobial infection and mycorrhizal arbuscule development requires a common AT-rich-containing regulatory sequence. , 2005, Molecular plant-microbe interactions : MPMI.

[5]  G. Oldroyd,et al.  Identification and characterization of nodulation-signaling pathway 2, a gene of Medicago truncatula involved in Nod actor signaling. , 2003, Plant physiology.

[6]  S. W. Khade,et al.  Symbiotic interactions between arbuscular mycorrhizal (AM) fungi and male papaya plants: its status, role and implications. , 2010, Plant physiology and biochemistry : PPB.

[7]  G. Bécard,et al.  Evolution of the plant-microbe symbiotic 'toolkit'. , 2013, Trends in plant science.

[8]  E. Journet,et al.  Four Genes of Medicago truncatula Controlling Components of a Nod Factor Transduction Pathway , 2000, Plant Cell.

[9]  E. Engstrom.  Phylogenetic analysis of GRAS proteins from moss, lycophyte and vascular plant lineages reveals that GRAS genes arose and underwent substantial diversification in the ancestral lineage common to bryophytes and vascular plants , 2011, Plant signaling & behavior.

[10]  A. Trouvelot,et al.  Mesure du taux de mycorhization VA d'un systeme radiculaire. Recherche de methodes d'estimation ayant une significantion fonctionnelle , 1986 .

[11]  K. Akiyama,et al.  Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi , 2005, Nature.

[12]  Z. Yang,et al.  Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. , 1998, Molecular biology and evolution.

[13]  G. Bécard,et al.  The microRNA miR171h modulates arbuscular mycorrhizal colonization of Medicago truncatula by targeting NSP2. , 2012, The Plant journal : for cell and molecular biology.

[14]  M. Nei,et al.  MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. , 2011, Molecular biology and evolution.

[15]  C. Delwiche,et al.  Origin of strigolactones in the green lineage. , 2012, The New phytologist.

[16]  Jean Dénarié,et al.  Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza , 2011, Nature.

[17]  B. Horváth,et al.  Medicago truncatula IPD3 is a member of the common symbiotic signaling pathway required for rhizobial and mycorrhizal symbioses. , 2011, Molecular plant-microbe interactions : MPMI.

[18]  P. Benfey,et al.  The SCARECROW Gene Regulates an Asymmetric Cell Division That Is Essential for Generating the Radial Organization of the Arabidopsis Root , 1996, Cell.

[19]  T. Bisseling,et al.  NSP1 of the GRAS Protein Family Is Essential for Rhizobial Nod Factor-Induced Transcription , 2005, Science.

[20]  K. Mysore,et al.  A GRAS-Type Transcription Factor with a Specific Function in Mycorrhizal Signaling , 2012, Current Biology.

[21]  C. Delwiche,et al.  Broad Phylogenomic Sampling and the Sister Lineage of Land Plants , 2012, PloS one.

[22]  J. F. Marsh,et al.  Nodulation Signaling in Legumes Requires NSP2, a Member of the GRAS Family of Transcriptional Regulators , 2005, Science.

[23]  N. Chua,et al.  PAT1, a new member of the GRAS family, is involved in phytochrome A signal transduction. , 2000, Genes & development.

[24]  Susana Rivas,et al.  Trans-regulation of the expression of the transcription factor MtHAP2-1 by a uORF controls root nodule development. , 2008, Genes & development.

[25]  I. Al‐Shehbaz,et al.  Cabbage family affairs: the evolutionary history of Brassicaceae. , 2011, Trends in plant science.

[26]  Andrew J. Heidel,et al.  Origin of land plants: Do conjugating green algae hold the key? , 2011, BMC Evolutionary Biology.

[27]  Sébastien Roy,et al.  Strigolactones Stimulate Arbuscular Mycorrhizal Fungi by Activating Mitochondria , 2006, PLoS biology.

[28]  P. Benfey,et al.  Root development in Arabidopsis: four mutants with dramatically altered root morphogenesis. , 1993, Development.

[29]  Arnaud Besserer,et al.  GR24, a Synthetic Analog of Strigolactones, Stimulates the Mitosis and Growth of the Arbuscular Mycorrhizal Fungus Gigaspora rosea by Boosting Its Energy Metabolism[C][W] , 2008, Plant Physiology.

[30]  G. Oldroyd,et al.  Identification and Characterization of Nodulation-Signaling Pathway 2, a Gene of Medicago truncatula Involved in Nod Factor Signaling1 , 2003, Plant Physiology.

[31]  Philippe Roche,et al.  Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal , 1990, Nature.

[32]  Wei Liu,et al.  Strigolactone Biosynthesis in Medicago truncatula and Rice Requires the Symbiotic GRAS-Type Transcription Factors NSP1 and NSP2[W][OA] , 2011, Plant Cell.

[33]  Jean-Charles Portais,et al.  Strigolactone inhibition of shoot branching , 2008, Nature.

[34]  Maria J. Harrison,et al.  Reprogramming Plant Cells for Endosymbiosis , 2009, Science.