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Plant and Cell Physiology Advance Access originally published online on December 11, 2008
Plant and Cell Physiology 2009 50(1):67-77; doi:10.1093/pcp/pcn194
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© The Author 2008. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please email: journals.permissions@oxfordjournals.org

Rapid Paper

Nod Factor/Nitrate-Induced CLE Genes that Drive HAR1-Mediated Systemic Regulation of Nodulation

Satoru Okamoto1, Erika Ohnishi1, Shusei Sato2, Hirokazu Takahashi3, Mikio Nakazono3, Satoshi Tabata2 and Masayoshi Kawaguchi1,4,*

1Department of Biological Sciences, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo, Tokyo, 113-0033 Japan
2Kazusa DNA Research Institute, 2-6-7 Kazusa-kaatari, Kisarazu, Chiba, 292-0818 Japan
3Graduate School of Agricultural and Life Sciences, University of Tokyo, 1-1-1 Yayoi, Bunkyo, Tokyo, 113-8657, Japan
4Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency, 4-1-8 Honcho, Kawaguchi, Saitama, 332-0112, Japan

*Corresponding author: E-mail, masayosi{at}biol.s.u-tokyo.ac.jp; Fax, +81-81-3-5841-4458.


  Abstract

Host legumes control root nodule numbers by sensing external and internal cues. A major external cue is soil nitrate, whereas a feedback regulatory system in which earlier formed nodules suppress further nodulation through shoot–root communication is an important internal cue. The latter is known as autoregulation of nodulation (AUT), and is believed to consist of two long-distance signals: a root-derived signal that is generated in infected roots and transmitted to the shoot; and a shoot-derived signal that systemically inhibits nodulation. In Lotus japonicus, the leucine-rich repeat receptor-like kinase, HYPERNODULATION ABERRANT ROOT FORMATION 1 (HAR1), mediates AUT and nitrate inhibition of nodulation, and is hypothesized to recognize the root-derived signal. Here we identify L. japonicus CLE-Root Signal 1 (LjCLE-RS1) and LjCLE-RS2 as strong candidates for the root-derived signal. A hairy root transformation study shows that overexpressing LjCLE-RS1 and -RS2 inhibits nodulation systemically and, furthermore, that the systemic suppression depends on HAR1. Moreover, LjCLE-RS2 expression is strongly up-regulated in roots by nitrate addition. Based on these findings, we propose a simple model for AUT and nitrate inhibition of nodulation mediated by LjCLE-RS1, -RS2 peptides and the HAR1 receptor-like kinase.

Keywords: CLE genes - Lotus japonicus - Nitrate - Nod factor signaling - Nodulation - Systemic regulation

Abbreviations: AUT, autoregulation of nodulation; CLE, CLAVATA3/ESR-related; CLV, CLAVATA; DAI, days after inoculation; ENOD, early nodulin; FCP1, FON2-LIKE CLE PROTEIN 1; FON, FLORAL ORGAN NUMBER; GFP, green fluorescent protein; GUS, β-glucuronidase; HAR1, HYPERNODULATION ABERRANT ROOT FORMATION 1; LjCCaMK, L. japonicus CCaMK; LjCLE-RS, L. japonicus CLE-Root Signal; LjNSP2, L. japonicus NSP2; LM, laser microdissection; LRR, leucine-rich repeat; MALDI TOF-MS, matrix-assisted laser desorption ionization time-of-flight-mass spectrometry; NARK, NODULE AUTOREGULATION RECEPTOR KINASE; NTS1, NITROGEN-TOLERANT SYMBIOSIS 1; ORF, open reading frame; RLK, receptor-like kinase; RT–PCR, reverse transcription–PCR; SUNN, SUPER NUMERIC NODULES; SYM29, SYMBIOSIS 29; TDIF, tracheary element differentiation inhibitory factor.

The nucleotide sequences reported in this paper have been submitted to DDBJ under accession numbers: LjCLE-RS1, AP010912 [GenBank] ; LjCLE-RS2, AP010911 [GenBank] ; LjCLE3, DF093345 [GenBank] ; LjCLE4, DF093252 [GenBank] ; LjCLE5, AP009981 [GenBank] ; LjCLE6, DF093444 [GenBank] ; LjCLE7, DF093291 [GenBank] ; LjCLE8, DF093487 [GenBank] ; LjCLE9, DF093494 [GenBank] ; LjCLE10, DF093195 [GenBank] ; LjCLE11, DF093446 [GenBank] ; LjCLE12, DF093446 [GenBank] ; LjCLE13, BABK01020001; LjCLE14, BABK01015111; LjCLE15, BABK01005343; LjCLE16, BABK01007606; LjCLE17, DF093443 [GenBank] ; LjCLE18, BABK01015679; LjCLE19, DF093363 [GenBank] ; LjCLE20, DF093363 [GenBank] ; LjCLE21, AP009928 [GenBank] ; LjCLE22, BABK01008074; LjCLE23, BABK01009817; LjCLE24, AP010913 [GenBank] ; LjCLE25, DF093246 [GenBank] ; LjCLE26, DF093353 [GenBank] ; LjCLE27, BABK01010624; LjCLE28, AP010217 [GenBank] ; LjCLE29, BABK01007274; LjCLE30, BABK01023262; LjCLE31, BABK01039053; LjCLE32, DF093533 [GenBank] ; LjCLE33, BABK01016033; LjCLE34, DF093335 [GenBank] ; LjCLE35, DF093323 [GenBank] ; LjCLE36, BABK01068922; LjCLE37, BABK01043991; LjCLE38, BABK01004370; LjCLV3, AP009713.

(Received December 1, 2008; Accepted December 8, 2008)
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