First published online October 27, 2006; 10.1104/pp.106.089508
Plant Physiology 142:1739-1750 (2006)
© 2006 American Society of Plant Biologists
PLANTS INTERACTING WITH OTHER ORGANISMS
Lotus japonicus Nodulation Requires Two GRAS Domain Regulators, One of Which Is Functionally Conserved in a Non-Legume1,[C],[W]
Anne B. Heckmann,
Fabien Lombardo,
Hiroki Miwa2,
Jillian A. Perry,
Sue Bunnewell,
Martin Parniske3,
Trevor L. Wang and
J. Allan Downie*
Department of Molecular Microbiology (A.B.H., F.L., H.M., J.A.D.), Department of Metabolic Biology (J.A.P., T.L.W.), and Department of Cell and Developmental Biology (S.B.), John Innes Centre, Norwich NR4 7UH, United Kingdom; and Sainsbury Laboratory, Norwich, NR4 7UH United Kingdom (M.P.)
A new nodulation-defective mutant of Lotus japonicus does not initiate nodule cortical cell division in response to Mesorhizobium loti, but induces root hair deformation, Nod factor-induced calcium spiking, and mycorrhization. This phenotype, together with mapping data, suggested that the mutation could be in the ortholog of the Medicago truncatula NSP1 gene (MtNSP1). The sequence of the orthologous gene (LjNSP1) in the L. japonicus mutant (Ljnsp1-1) revealed a mutation causing a premature stop resulting in loss of the C-terminal 23 amino acids. We also sequenced the NSP2 gene from L. japonicus (LjNSP2). A mutant (Ljnsp2-3) with a premature stop codon was identified by TILLING showing a similar phenotype to Ljnsp1-1. Both LjNSP1 and LjNSP2 are predicted GRAS (GAI, RGA, SCR) domain transcriptional regulators. Transcript steady-state levels of LjNSP1 and LjNSP2 initially decreased and then increased following infection by M. loti. In hairy root transformations, LjNSP1 and MtNSP1 complemented both Mtnsp1-1 and Ljnsp1-1 mutants, demonstrating that these orthologous proteins have a conserved biochemical function. A Nicotiana benthamiana NSP1-like gene (NbNSP1) was shown to restore nodule formation in both Ljnsp1-1 and Mtnsp1-1 mutants, indicating that NSP1 regulators from legumes and non-legumes can propagate the Nod factor-induced signal, activating appropriate downstream targets. The L. japonicus nodules complemented with NbNSP1 contained some cells with abnormal bacteroids and could fix nitrogen. However, the NbNSP1-complemented M. truncatula nodules did not fix nitrogen and contained very few bacteria released from infection threads. These observations suggest that NSP1 is also involved in infection, bacterial release, and normal bacteroid formation in nodule cells.
1 This work was supported by the European Union (Marie Curie Ph.D. fellowship RTN–CT–2003–505227 to A.B.H.) via the INTEGRAL network, by the Biotechnology and Biological Sciences Research Council, by the Gatsby Charitable Foundation (to the Sainsbury Laboratory), by the John Innes Foundation, and by the Universities UK Overseas Research Students Awards Scheme (H.M.).
2 Present address: Biotechnology Research Centre, University of Tokyo, Yayoi 1-1-1 Bunkyo-ku, Tokyo 113–8657, Japan.
3 Present address: University of Munich, Department of Biology, Genetics, Marie-Ward-Str. 1a, D–80638 Munich, Germany.
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: J. Allan Downie (allan.downie{at}bbsrc.ac.uk).
[C] Some figures in this article are displayed in color online but in black and white in the print edition.
[W] The online version of this article contains Web-only data.
www.plantphysiol.org/cgi/doi/10.1104/pp.106.089508
* Corresponding author; e-mail allan.downie{at}bbsrc.ac.uk; fax 44(0)1603–450045.
Received September 5, 2006;
accepted October 19, 2006;
published October 27, 2006.
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