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Two CLE genes are induced by phosphate in roots of Lotus japonicus

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Abstract

Genes of CLE (CLAVATA3/ESR-related) family encode peptide ligands that regulate plant development in response to external stimuli such as rhizobial infection and the nitrate application as well as various internal stimuli. To investigate whether LjCLE gene(s) may involve in plant response to inorganic phosphate (Pi), we analyzed Pi responses of 39 LjCLE genes in hydroponically grown Lotus japonicus plants (ecotype Miyakojima ‘MG-20’). Two LjCLE genes, LjCLE19 and 20, were up-regulated specifically and greatly in roots of L. japonicus by Pi addition to the hydroponic solution. When the external Pi level increased, expressions of LjCLE19 and 20 increased before the increase in the Pi content in plants. On the other hand, when the external Pi level decreased, the Pi content in plants decreased first, then expression levels of LjCLE19 and 20 decreased. Based on our results, we discuss the relationship between LjCLE19 and 20 and the tissue Pi levels in plants. This is the first report showing induction of specific CLE genes by phosphate.

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Abbreviations

CLE:

CLAVATA3/ESR-related

FW:

Fresh weight

P:

Phosphorus

Pi:

Inorganic phosphate

References

  • Bates TR, Lynch JP (1996) Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell Environ 19:529–538. doi:10.1111/j.1365-3040.1996.tb00386.x

    Article  CAS  Google Scholar 

  • Bencini DA, Wild JR, O’Donovan GA (1983) Linear one-step assay for the determination of orthophosphate. Anal Biochem 132:254–258. doi:10.1016/0003-2697(83)90004-0

    Article  CAS  PubMed  Google Scholar 

  • Bieleski RL (1968) Effect of phosphorus deficiency on levels of phosphorus compounds in Spirodela. Plant Physiol 43:1309–1316. doi:10.1104/pp.43.8.1309

    Article  CAS  PubMed  Google Scholar 

  • Bieleski RL (1973) Phosphate, pools, phosphate transport, and phosphate availability. Annu Rev Plant Physiol 24:225–252. doi:10.1146/annurev.pp.24.060173.001301

    Article  CAS  Google Scholar 

  • Broughton WJ, Dilworth MJ (1971) Control of leghaemoglobin synthesis in snake beans. Biochem J 125:1075–1080

    CAS  PubMed  Google Scholar 

  • Chapin III FS, Bieleski RL (1982) Mild phosphorus stress in barley and a related low-phosphorus-adapted barleygrass: phosphorus fractions and phosphate absorption in relation to growth. Physiol Plant 54:309–317. doi:10.1111/j.1399-3054.1982.tb00264.x

  • Chiou T-J (2007) The role of microRNAs in sensing nutrient stress. Plant Cell Environ 30:323–332. doi:10.1111/j.1365-3040.2007.01643.x

    Article  CAS  PubMed  Google Scholar 

  • Colebatch G, Desbrosses G, Ott T, Krusell L, Montanari O, Kloska S, Kopka J, Udvardi MK (2004) Global changes in transcription orchestrate metabolic differentiation during symbiotic nitrogen fixation in Lotus japonicus. Plant J 39:487–512. doi:10.1111/j.1365-313X.2004.02150.x

    Article  PubMed  Google Scholar 

  • Fiers M, Ku KL, Liu C-M (2007) CLE peptide ligands and their roles in establishing meristems. Curr Opin Plant Biol 10:39–43. doi:10.1016/j.pbi.2006.11.003

    Article  CAS  PubMed  Google Scholar 

  • Fukuda H, Hirakara Y, Sawa S (2007) Peptide signaling in vascular development. Curr Opin Plant Biol 10:477–482. doi:10.1016/j.pbi.2007.08.013

    Article  CAS  PubMed  Google Scholar 

  • Hirakawa Y, Shinohara H, Kondo Y, Inoue A, Nakanomyo I, Ogawa M, Sawa S, Ohashi-Ito K, Matsubayashi Y, Fukuda H (2008) Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system. Proc Natl Acad Sci USA 105:15208–15213. doi:10.1073/pnas.0808444105

    Article  CAS  PubMed  Google Scholar 

  • Johnson JF, Vance CP, Allan DL (1996) Phosphorus deficiency in Lupinus albus (Altered lateral root development and enhanced expression of phosphoenolpyruvate carboxylase). Plant Physiol 112:31–41. doi:10.1104/pp.112.1.31

    Article  CAS  PubMed  Google Scholar 

  • Kinoshita A, Nakamura Y, Sasaki E, Kyozuka J, Fukuda H, Sawa S (2007) Gain-of-function phenotypes of chemically synthetic CLAVATA3/ESR-related (CLE) peptides in Arabidopsis thaliana and Oryza sativa. Plant Cell Physiol 48:1821–1825. doi:10.1093/pcp/pcm154

    Article  CAS  PubMed  Google Scholar 

  • Krusell L, Madsen LH, Sato S, Aubert G, Genua A, Szczyglowski K, Duc G, Kaneko T, Tabata S, de Bruijn F, Pajuelo E, Sandal N, Stougaard J (2002) Shoot control of root development and nodulation is mediated by a receptor-like kinase. Nature 420:422–426. doi:10.1038/nature01207

    Article  CAS  PubMed  Google Scholar 

  • Lee RB, Ratcliffe RG (1993) Subcellular distribution of inorganic phosphate, and levels of nucleoside triphosphate, in mature maize roots at low external phosphate concentrations: measurements with 31P-NMR. J Exp Bot 44:587–598

    Article  CAS  Google Scholar 

  • Lee RB, Ratcliffe RG, Southon TE (1990) 31P NMR measurements of the cytoplasmic and vacuolar Pi content of mature maize roots: relationships with phosphorus status and phosphate fluxes. J Exp Bot 41:1063–1078

    Article  CAS  Google Scholar 

  • Li D, Zhu H, Liu K, Liu X, Leggewie G, Udvardi M, Wang D (2002) Purple acid phosphatases of Arabidopsis thaliana: comparative analysis and differential regulation by phosphate deprivation. J Biol Chem 277:27772–27781. doi:10.1074/jbc.M204183200

    Google Scholar 

  • Lin W-Y, Lin S-I, Chiou T-J (2009) Molecular regulators of phosphate homeostasis in plants. J Exp Bot 60:1427–1438. doi:10.1093/jxb/ern303

    Article  CAS  PubMed  Google Scholar 

  • Liu C, Muchhal US, Uthappa M, Kononowicz AK, Raghothama KG (1998) Tomato phosphate transporter genes are differentially regulated in plant tissues by phosphorus. Plant Physiol 116:91–99. doi:10.1104/pp.116.1.91

    Article  CAS  PubMed  Google Scholar 

  • López-Bucio J, Cruz-Ramírez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287. doi:10.1016/S1369-5266(03)00035-9

    Article  PubMed  Google Scholar 

  • Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant Soil 159:89–102. doi:10.1007/BF00000098

    CAS  Google Scholar 

  • Mimura T (1999) Regulation of phosphate transport and homeostasis in plant cells. Int Rev Cytol 191:149–200

    Article  CAS  Google Scholar 

  • Mimura T, Sakano K, Shimmen T (1996) Studies on the distribution, re-translocation and homeostasis of inorganic phosphate in barley leaves. Plant Cell Environ 19:311–320. doi:10.1111/j.1365-3040.1996.tb00253.x

    Article  CAS  Google Scholar 

  • Miwa H, Kinoshita A, Fukuda H, Sawa S (2009) Plant meristems: CLAVATA3/ESR-related signaling in the shoot apical meristem and the root apical meristem. J Plant Res 122:31–39. doi:10.1007/s10265-008-0207-3

    Article  CAS  PubMed  Google Scholar 

  • Morcuende R, Bari R, Gibon Y, Zheng W, Pant BD, Bläsing O, Usadel B, Czechowski T, Udvardi MK, Stitt M, Scheible W-R (2007) Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant Cell Environ 30:85–112. doi:10.1111/j.1365-3040.2006.01608.x

    Article  CAS  PubMed  Google Scholar 

  • Nakagawa T, Izumi T, Banba M, Umehara Y, Kouchi H, Izui K, Hata S (2003) Characterization and expression analysis of genes encoding phosphoenolpyruvate carboxylase and phosphoenolpyruvate carboxylase kinase of Lotus japonicus, a model legume. Mol Plant Microbe Interact 16:281–288. doi:10.1094/MPMI.2003.16.4.281

    Article  CAS  PubMed  Google Scholar 

  • Nishimura R, Hayashi M, Wu G-J, Kouchi H, Imaizumi-Anraku H, Murakami Y, Kawasaki S, Akao S, Ohmori M, Nagasawa M, Harada K, Kawaguchi M (2002) HAR1 mediates systemic regulation of symbiotic organ development. Nature 420:426–429. doi:10.1038/nature01231

    Article  CAS  PubMed  Google Scholar 

  • Okamoto S, Ohnishi E, Sato S, Takahashi H, Nakazono M, Tabata S, Kawaguchi M (2009) Nod factor/nitrate-induced CLE genes that drive HAR1-mediated systemic regulation of nodulation. Plant Cell Physiol 50:67–77. doi:10.1093/pcp/pcn194

    Article  CAS  PubMed  Google Scholar 

  • Plaxton WC, Carswell MC (1999) Metabolic aspects of the phosphate starvation response in plants. In: Lerner HR (ed) Plant responses to environmental stresses: from phytohormones to genome reorganization. Marcel Dekker, New York, pp 349–372

    Google Scholar 

  • Raghothama KG (1999) Phosphate acquistion. Annu Rev Plant Physiol Plant Mol Biol 50:665–693. doi:10.1146/annurev.arplant.50.1.665

    Article  CAS  PubMed  Google Scholar 

  • Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116:447–453. doi:10.1104/pp.116.2.447

    Article  CAS  PubMed  Google Scholar 

  • Scheible W-R, Morcuende R, Czechowski T, Fritz C, Osuna D, Palacios-Rojas N, Schindelasch D, Thimm O, Udvardi MK, Stitt M (2004) Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol 136:2483–2499. doi:10.1104/pp.104.047019

    Article  CAS  PubMed  Google Scholar 

  • Shane MW, Cramer MD, Funayama-Noguchi S, Cawthray GR, Millar AH, Day DA, Lambers H (2004) Developmental physiology of cluster-root carboxylate synthesis and exudation in harsh hakea. Expression of phosphoenolpyruvate carboxylase and the alternative oxidase. Plant Physiol 135:549–560. doi:10.1104/pp.103.035659

    Article  CAS  PubMed  Google Scholar 

  • Sharma VK, Ramirez J, Fletcher JC (2003) The ArabidopsisCLV3-like (CLE) genes are expressed in diverse tissues and encode secreted proteins. Plant Mol Biol 51:415–425. doi:10.1023/A:1022038932376

    Article  CAS  PubMed  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. WH Freeman, New York

    Google Scholar 

  • Strabala TJ, O’donnell PJ, Smit A-M, Ampomah-Dwamena C, Martin EJ, Netzler N, Nieuwenhuizen NJ, Quinn BD, Foote HCC, Hudson KR (2006) Gain-of function phenotypes of many CLAVATA3/ESR genes, including four new family members, correlate with tandem variations in the conserved CLAVATA3/ESR domain. Plant Physiol 140:1331–1344. doi:10.1104/pp.105.075515

    Article  CAS  PubMed  Google Scholar 

  • Williamson LC, Ribrioux SPCP, Fitter AH, Leyser HMO (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol 126:875–882. doi:10.1104/pp.126.2.875

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We are grateful to Dr. M. Taira for the use of real-time PCR instrument, to Prof. T. Mimura for his advice on the measurement of Pi, to Dr. S. Yano for his advice on the measurement of root length and to Dr. S. Okamoto and Ms. E. Ohnishi for their helpful advice on the real-time PCR analysis. We also thank Prof. I. Terashima for critical reading of the manuscript, and laboratory members for the kind advice, help and encouragement. This work was supported by KAKENHI (Grant-in-Aid for Scientific Research) on Priority Areas “Comparative Genomics” from the Ministry of Education, Culture, Sports, Science and Technology of Japan.

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Authors and Affiliations

  1. Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-0033, Japan

    Sachiko Funayama-Noguchi, Ko Noguchi & Chie Yoshida

  2. Division of Symbiotic Systems, National Institute for Basic Biology, Nishigonaka 38, Myodaiji, Okazaki, Aichi, 444-8585, Japan

    Chie Yoshida & Masayoshi Kawaguchi

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  1. Sachiko Funayama-Noguchi
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  2. Ko Noguchi
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Correspondence to Sachiko Funayama-Noguchi.

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Funayama-Noguchi, S., Noguchi, K., Yoshida, C. et al. Two CLE genes are induced by phosphate in roots of Lotus japonicus . J Plant Res 124, 155–163 (2011). https://doi.org/10.1007/s10265-010-0342-5

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