Nature 462, 514-517 (26 November 2009) | doi:10.1038/nature08594; Received 24 September 2009; Accepted 19 October 2009

Host plant genome overcomes the lack of a bacterial gene for symbiotic nitrogen fixation

Tsuneo Hakoyama1,2, Kaori Niimi2, Hirokazu Watanabe2, Ryohei Tabata2, Junichi Matsubara2, Shusei Sato3, Yasukazu Nakamura3, Satoshi Tabata3, Li Jichun4, Tsuyoshi Matsumoto4, Kazuyuki Tatsumi4, Mika Nomura5, Shigeyuki Tajima5, Masumi Ishizaka6, Koji Yano1, Haruko Imaizumi-Anraku1, Masayoshi Kawaguchi7, Hiroshi Kouchi1 & Norio Suganuma2

  1. National Institute of Agrobiological Sciences, Tsukuba, Ibaraki 305-8602, Japan
  2. Department of Life Science, Aichi University of Education, Kariya, Aichi 448-8542, Japan
  3. Kazusa DNA Research Institute, Kisarazu, Chiba 292-0812, Japan
  4. Research Center for Materials Science and Department of Chemistry, Graduate School of Science, Nagoya University, Nagoya, Aichi 464-8602, Japan
  5. Faculty of Agriculture, Kagawa University, Kita, Kagawa 761-0795, Japan
  6. National Institute of Agro-Environmental Sciences, Tsukuba, Ibaraki 305-8604, Japan
  7. National Institute for Basic Biology, Okazaki, Aichi 444-8585, Japan

Correspondence to: Norio Suganuma2 Correspondence and requests for materials should be addressed to N.S. (Email: nsuganum@auecc.aichi-edu.ac.jp).

Homocitrate is a component of the iron–molybdenum cofactor in nitrogenase, where nitrogen fixation occurs1, 2. NifV, which encodes homocitrate synthase (HCS)3, has been identified from various diazotrophs but is not present in most rhizobial species that perform efficient nitrogen fixation only in symbiotic association with legumes. Here we show that the FEN1 gene of a model legume, Lotus japonicus, overcomes the lack of NifV in rhizobia for symbiotic nitrogen fixation. A Fix- (non-fixing) plant mutant, fen1, forms morphologically normal but ineffective nodules4, 5. The causal gene, FEN1, was shown to encode HCS by its ability to complement a HCS-defective mutant of Saccharomyces cerevisiae. Homocitrate was present abundantly in wild-type nodules but was absent from ineffective fen1 nodules. Inoculation with Mesorhizobium loti carrying FEN1 or Azotobacter vinelandii NifV rescued the defect in nitrogen-fixing activity of the fen1 nodules. Exogenous supply of homocitrate also recovered the nitrogen-fixing activity of the fen1 nodules through de novo nitrogenase synthesis in the rhizobial bacteroids. These results indicate that homocitrate derived from the host plant cells is essential for the efficient and continuing synthesis of the nitrogenase system in endosymbionts, and thus provide a molecular basis for the complementary and indispensable partnership between legumes and rhizobia in symbiotic nitrogen fixation.


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