First published online March 16, 2007; 10.1104/pp.106.093021
Plant Physiology 144:324-335 (2007)
© 2007 American Society of Plant Biologists
PLANTS INTERACTING WITH OTHER ORGANISMS
Medicago truncatula NIN Is Essential for Rhizobial-Independent Nodule Organogenesis Induced by Autoactive Calcium/Calmodulin-Dependent Protein Kinase1
John F. Marsh*,
Alexandra Rakocevic,
Raka M. Mitra2,
Lysiane Brocard,
Jongho Sun,
Alexis Eschstruth,
Sharon R. Long,
Michael Schultze,
Pascal Ratet and
Giles E.D. Oldroyd
John Innes Centre, Norwich Research Park, Colney, Norwich NR4 7UH, United Kingdom (J.F.M., J.S., G.E.D.O.); Institut des Sciences du Vegetale, Centre National de la Recherche Scientifique, 91198, Gif sur Yvette, France (A.R., L.B., A.E., P.R.); Department of Biological Sciences, Stanford University, Stanford, California 94305–5020 (R.M.M., S.R.L.); and Department of Biology, University of York, York YO10 5YW, United Kingdom (M.S.)
The symbiotic association between legumes and nitrogen-fixing bacteria collectively known as rhizobia results in the formation of a unique plant root organ called the nodule. This process is initiated following the perception of rhizobial nodulation factors by the host plant. Nod factor (NF)-stimulated plant responses, including nodulation-specific gene expression, is mediated by the NF signaling pathway. Plant mutants in this pathway are unable to nodulate. We describe here the cloning and characterization of two mutant alleles of the Medicago truncatula ortholog of the Lotus japonicus and pea (Pisum sativum) NIN gene. The Mtnin mutants undergo excessive root hair curling but are impaired in infection and fail to form nodules following inoculation with Sinorhizobium meliloti. Our investigation of early NF-induced gene expression using the reporter fusion ENOD11::GUS in the Mtnin-1 mutant demonstrates that MtNIN is not essential for early NF signaling but may negatively regulate the spatial pattern of ENOD11 expression. It was recently shown that an autoactive form of a nodulation-specific calcium/calmodulin-dependent protein kinase is sufficient to induce nodule organogenesis in the absence of rhizobia. We show here that MtNIN is essential for autoactive calcium/calmodulin-dependent protein kinase-induced nodule organogenesis. The non-nodulating hcl mutant has a similar phenotype to Mtnin, but we demonstrate that HCL is not required in this process. Based on our data, we suggest that MtNIN functions downstream of the early NF signaling pathway to coordinate and regulate the correct temporal and spatial formation of root nodules.
1 This work was supported by the Royal Society and the Biotechnology and Biological Sciences Research Council (David Phillips Fellowship and a grant in aid to G.E.D.O.), by the U.S. Department of Energy (DE–FG03–90ER20010 to S.R.L.), by Howard Hughes Medical Institute (predoctoral fellowship to R.M.M.), by the Grain Legumes Integrated Project (grant no. FOOD–CT–2004–506223 to L.B. and A.E.), and by the French Ministere de l'education National, de l'Enseignement Superieur, Recherche (fellowship to A.R.).
2 Present address: Department of Plant Biology, University of Minnesota, 220 BioSci Center, 1445 Gortner Avenue, St. Paul, MN 55108.
The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Giles E.D. Oldroyd (giles.oldroyd{at}bbsrc.ac.uk).
www.plantphysiol.org/cgi/doi/10.1104/pp.106.093021
* Corresponding author; e-mail john.marsh{at}bbsrc.ac.uk; fax 44–01603–450045.
Received November 14, 2006;
accepted March 7, 2007;
published March 16, 2007.
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