The structure and activity of nodulation-suppressing CLE peptide hormones of legumes
April H. Hastwell A , Peter M. Gresshoff A and Brett J. Ferguson A B
+ Author Affiliations
- Author Affiliations
A Centre for Integrative Legume Research, School of Agricultural and Food Sciences, The University of Queensland, St Lucia, Brisbane, Qld 4072, Australia.
B Corresponding author. Email: b.ferguson1@uq.edu.au
Functional Plant Biology 42(3) 229-238 https://doi.org/10.1071/FP14222
Submitted: 8 August 2014 Accepted: 3 November 2014 Published: 12 December 2014
Abstract
Legumes form a highly-regulated symbiotic relationship with specific soil bacteria known as rhizobia. This interaction results in the de novo formation of root organs called nodules, in which the rhizobia fix atmospheric di-nitrogen (N2) for the plant. Molecular mechanisms that regulate the nodulation process include the systemic ‘autoregulation of nodulation’ and the local nitrogen-regulation of nodulation pathways. Both pathways are mediated by novel peptide hormones called CLAVATA/ESR-related (CLE) peptides that act to suppress nodulation via negative feedback loops. The mature peptides are 12–13 amino acids in length and are post-translationally modified from the C-terminus of tripartite-domain prepropeptides. Structural redundancy between the prepropeptides exists; however, variations in external stimuli, timing of expression, tissue specificity and presence or absence of key functional domains enables them to act in a specific manner. To date, nodulation-regulating CLE peptides have been identified in Glycine max (L.) Merr., Medicago truncatula Gaertn., Lotus japonicus (Regel) K.Larsen and Phaseolus vulgaris L. One of the L. japonicus peptides, called LjCLE-RS2, has been structurally characterised and found to be an arabinosylated glycopeptide. All of the known nodulation CLE peptides act via an orthologous leucine rich repeat (LRR) receptor kinase. Perception of the peptide results in the production of a novel, unidentified inhibitor signal that acts to suppress further nodulation events. Here, we contrast and compare the various nodulation-suppressing CLE peptides of legumes.
Additional keywords: autoregulation of nodulation, legume nodulation, nitrate-regulation of nodulation, nodule, plant peptide signalling, symbiosis.
References
Araya T, Miyamoto M, Wibowo J, Suzuki A, Kojima S, Tsuchiya YN, Sawa S, Fukuda H, Von Wirén N, Takahashi H (2014) CLE-CLAVATA1 peptide-receptor signaling module regulates the expansion of plant root systems in a nitrogen-dependent manner. Proceedings of the National Academy of Sciences of the United States of America 111, 2029–2034.| CLE-CLAVATA1 peptide-receptor signaling module regulates the expansion of plant root systems in a nitrogen-dependent manner.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitFOnt7o%3D&md5=547789e0ecf8b630638ccf11aefa6990CAS | 24449877PubMed |
Bakhetia M, Urwin PE, Atkinson HJ (2007) qPCR analysis and RNAi define pharyngeal gland cell-expressed genes of Heterodera glycines required for initial interactions with the host. Molecular Plant-Microbe Interactions 20, 306–312.
| qPCR analysis and RNAi define pharyngeal gland cell-expressed genes of Heterodera glycines required for initial interactions with the host.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXitVerurk%3D&md5=a706db2b445f71ce7fd467afa6e0ad1eCAS | 17378433PubMed |
Carroll BJ, McNeil DL, Gresshoff PM (1985a) A supernodulation and nitrate-tolerant symbiotic (nts) soybean mutant. Plant Physiology 78, 34–40.
| A supernodulation and nitrate-tolerant symbiotic (nts) soybean mutant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXktVerur0%3D&md5=92d105d20482d7cc9dd9b9b90cdd821aCAS | 16664203PubMed |
Carroll BJ, McNeil DL, Gresshoff PM (1985b) Isolation and properties of soybean (Glycine max (L) Merr.) mutants that nodulate in the presence of high nitrate concentrations. Proceedings of the National Academy of Sciences of the United States of America 82, 4162–4166.
| Isolation and properties of soybean (Glycine max (L) Merr.) mutants that nodulate in the presence of high nitrate concentrations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXkvVGhsLo%3D&md5=0c3811e1fbc4bc405bc980fda122a808CAS | 16593577PubMed |
Clark SE, Williams RW, Meyerowitz EM (1997) The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89, 575–585.
| The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjsVShur0%3D&md5=5071bd36bf485154fe7eb0e3214c4b76CAS | 9160749PubMed |
Cock JM, McCormick S (2001) A large family of genes that share homology with CLAVATA3. Plant Physiology 126, 939–942.
| A large family of genes that share homology with CLAVATA3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsVartLY%3D&md5=8d7d5fabc1f77441755a3acf1f5acb73CAS | 11457943PubMed |
Delves AC, Mathews A, Day DA, Carter AS, Carroll BJ, Gresshoff PM (1986) Regulation of the soybean-Rhizobium nodule symbiosis by shoot and root factors. Plant Physiology 82, 588–590.
| Regulation of the soybean-Rhizobium nodule symbiosis by shoot and root factors.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cnhslagtQ%3D%3D&md5=e378df32885efb5310b2a36f2de870cdCAS | 16665072PubMed |
Desbrosses GJ, Stougaard J (2011) Root nodulation: a paradigm for how plant-microbe symbiosis influences host developmental pathways. Cell Host & Microbe 10, 348–358.
| Root nodulation: a paradigm for how plant-microbe symbiosis influences host developmental pathways.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlKitr%2FO&md5=c2f7d6232d2b103b80e1589cb23956e1CAS |
Djordjevic MA, Oakes M, Wong CE, Singh M, Bhalla P, Kusumawati L, Imin N (2011) Border sequences of Medicago truncatula CLE36 are specifically cleaved by endoproteases common to the extracellular fluids of Medicago and soybean. Journal of Experimental Botany 62, 4649–4659.
| Border sequences of Medicago truncatula CLE36 are specifically cleaved by endoproteases common to the extracellular fluids of Medicago and soybean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFKisb3O&md5=77a3eb31f781c66cee3bf8996a5a7569CAS | 21633083PubMed |
Erisman JW, Sutton MA, Galloway J, Klimont Z, Winiwarter W (2008) How a century of ammonia synthesis changed the world. Nature Geoscience 1, 636–639.
| How a century of ammonia synthesis changed the world.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFOlur%2FM&md5=2a715f81a5cb1aeeadfe207c05d70b56CAS |
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.
| Confidence limits on phylogenies: an approach using the bootstrap.Crossref | GoogleScholarGoogle Scholar |
Ferguson BJ, Mathesius U (2003) Signaling interactions during nodule development. Journal of Plant Growth Regulation 22, 47–72.
| Signaling interactions during nodule development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXosF2ktbY%3D&md5=32020f2d2ee20a702dd2a5886f4b978cCAS |
Ferguson BJ, Mathesius U (2014) Phytohormone regulation of legume-rhizobia interactions. Journal of Chemical Ecology
| Phytohormone regulation of legume-rhizobia interactions.Crossref | GoogleScholarGoogle Scholar | 25052910PubMed |
Ferguson BJ, Indrasumunar A, Hayashi S, Lin M-H, Lin Y-H, Reid DE, Gresshoff PM (2010) Molecular analysis of legume nodule development and autoregulation. Journal of Integrative Plant Biology 52, 61–76.
| Molecular analysis of legume nodule development and autoregulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitVOhsLo%3D&md5=c1170a0ccbd514abd34c4c6228d3618aCAS | 20074141PubMed |
Ferguson BJ, Lin MH, Gresshoff PM (2013) Regulation of legume nodulation by acidic growth conditions. Plant Signaling & Behavior 8, e23426
| Regulation of legume nodulation by acidic growth conditions.Crossref | GoogleScholarGoogle Scholar |
Ferguson BJ, Li D, Hastwell AH, Reid DE, Li Y, Jackson SA, Gresshoff PM (2014) The soybean (Glycine max) nodulation-suppressive CLE peptide, GmRIC1, functions interspecifically in common white bean (Phaseolus vulgaris), but not in a supernodulating line mutated in the receptor PvNARK. Plant Biotechnology Journal
| The soybean (Glycine max) nodulation-suppressive CLE peptide, GmRIC1, functions interspecifically in common white bean (Phaseolus vulgaris), but not in a supernodulating line mutated in the receptor PvNARK.Crossref | GoogleScholarGoogle Scholar | 25040127PubMed |
Fiers M, Golemiec E, Van Der Schors R, Van Der Geest L, Li KW, Stiekema WJ, Liu C-M (2006) The CLAVATA3/ESR motif of CLAVATA3 Is functionally independent from the nonconserved flanking sequences. Plant Physiology 141, 1284–1292.
| The CLAVATA3/ESR motif of CLAVATA3 Is functionally independent from the nonconserved flanking sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XosVKitr0%3D&md5=8f432c521ca529ba428a5dc71318bc2dCAS | 16751438PubMed |
Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM (1999) Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283, 1911–1914.
| Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXitVantb4%3D&md5=fbe83b816fe888259f423775e6d61cfaCAS | 10082464PubMed |
Funayama-Noguchi S, Noguchi K, Yoshida C, Kawaguchi M (2011) Two CLE genes are induced by phosphate in roots of Lotus japonicus. Journal of Plant Research 124, 155–163.
| Two CLE genes are induced by phosphate in roots of Lotus japonicus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsF2hu7zI&md5=3280bbc4b9f13466af0005e8a454d2a1CAS | 20428922PubMed |
Gresshoff PM, Delves AC (1986). Plant genetic approaches to symbiotic nodulation and nitrogen fixation in legumes. In ‘Plant gene research’. (Eds AD Blaustein, PJ King) pp. 159–206. (Springer-Verlag: New York)
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.
| A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood.Crossref | GoogleScholarGoogle Scholar | 14530136PubMed |
Hayashi S, Reid DE, Lorenc MT, Stiller J, Edwards D, Gresshoff PM, Ferguson BJ (2012) Transient Nod factor-dependent gene expression in the nodulation-competent zone of soybean (Glycine max (L.) Merr.) roots. Plant Biotechnology Journal 10, 995–1010.
| Transient Nod factor-dependent gene expression in the nodulation-competent zone of soybean (Glycine max (L.) Merr.) roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1art77N&md5=6ccc39fb459d6d8f5f01005e13cd9495CAS | 22863334PubMed |
Herridge D, Peoples M, Boddey R (2008) Global inputs of biological nitrogen fixation in agricultural systems. Plant and Soil 311, 1–18.
| Global inputs of biological nitrogen fixation in agricultural systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVyju73M&md5=6a13cd768f22ac011e2df0673956f6e3CAS |
Ito Y, Nakanomyo I, Motose H, Iwamoto K, Sawa S, Dohmae N, Fukuda H (2006) Dodeca-CLE peptides as suppressors of plant stem cell differentiation. Science 313, 842–845.
| Dodeca-CLE peptides as suppressors of plant stem cell differentiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnvVynt7o%3D&md5=c510662e62f55075f946ca09b29dda2cCAS | 16902140PubMed |
Jacobsen E, Feenstra WJ (1984) A new pea mutant with efficient nodulation in the presence of nitrate. Plant Science Letters 33, 337–344.
| A new pea mutant with efficient nodulation in the presence of nitrate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXhvVyqtrw%3D&md5=4bc44d74507877f31219a1e9f46c0bebCAS |
Jensen E, Peoples M, Boddey R, Gresshoff P, Hauggaard-Nielsen H, Alves B, Morrison M (2012) Legumes for mitigation of climate change and feedstock in a bio-based economy – a review. Agronomy for Sustainable Development 32, 329–364.
| Legumes for mitigation of climate change and feedstock in a bio-based economy – a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XksVOgt78%3D&md5=9a5f573d6c29cf5999ba2b8b3cd86f70CAS |
Jeudy C, Ruffel S, Freixes S, Tillard P, Santoni AL, Morel S, Journet E-P, Duc G, Gojon A, Lepetit M, Salon C (2010) Adaptation of Medicago truncatula to nitrogen limitation is modulated via local and systemic nodule developmental responses. New Phytologist 185, 817–828.
| Adaptation of Medicago truncatula to nitrogen limitation is modulated via local and systemic nodule developmental responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitFKns7k%3D&md5=420d5f942614eac9f1981fb403e1114bCAS | 20015066PubMed |
Kondo T, Sawa S, Kinoshita A, Mizuno S, Kakimoto T, Fukuda H, Sakagami Y (2006) A plant peptide encoded by CLV3 identified by in situ MALDI-TOF MS analysis. Science 313, 845–848.
| A plant peptide encoded by CLV3 identified by in situ MALDI-TOF MS analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnvVynt7s%3D&md5=0a3fa4726970055b586a4ec595538ce8CAS | 16902141PubMed |
Kondo T, Nakamura T, Yokomine K, Sakagami Y (2008) Dual assay for MCLV3 activity reveals structure-activity relationship of CLE peptides. Biochemical and Biophysical Research Communications 377, 312–316.
| Dual assay for MCLV3 activity reveals structure-activity relationship of CLE peptides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlaqsb3L&md5=4580637ce158e4e73951136d0c7c7619CAS | 18848920PubMed |
Kosslak RM, Bohlool BB (1984) Suppression of nodule development of one side of a split-root system of soybeans caused by prior inoculation of the other side. Plant Physiology 75, 125–130.
| Suppression of nodule development of one side of a split-root system of soybeans caused by prior inoculation of the other side.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cnhsFOhtA%3D%3D&md5=dc4a52cba455da6bdab7f9538ea48cadCAS | 16663555PubMed |
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.
| Shoot control of root development and nodulation is mediated by a receptor-like kinase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XptFCis7w%3D&md5=6c61bafbfcba361b0cdf1919632019f1CAS | 12442170PubMed |
Krusell L, Sato N, Fukuhara I, Koch BEV, Grossmann C, Okamoto S, Oka-Kira E, Otsubo Y, Aubert G, Nakagawa T, Sato S, Tabata S, Duc G, Parniske M, Wang TL, Kawaguchi M, Stougaard J (2011) The Clavata2 genes of pea and Lotus japonicus affect autoregulation of nodulation. The Plant Journal 65, 861–871.
| The Clavata2 genes of pea and Lotus japonicus affect autoregulation of nodulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXkvVais7c%3D&md5=683c6555ea0afe96eb6a940b5ea84ca2CAS | 21276104PubMed |
la Cour T, Kiemer L, Mølgaard A, Gupta R, Skriver K, Brunak S (2004) Analysis and prediction of leucine-rich nuclear export signals. Protein Engineering, Design & Selection 17, 527–536.
| Analysis and prediction of leucine-rich nuclear export signals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXos1GisLc%3D&md5=c6523ad8d9eed346057e1b3851931465CAS |
Larkin MA, Blackshields G, Brown NP, Chenna R, Mcgettigan PA, Mcwilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948.
| Clustal W and Clustal X version 2.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlaqsL%2FM&md5=a7e5427f5948a5538b27ba99db4e46c4CAS | 17846036PubMed |
Li D, Kinkema M, Gresshoff PM (2009) Autoregulation of nodulation (AON) in Pisum sativum (pea) involves signalling events associated with both nodule primordia development and nitrogen fixation. Journal of Plant Physiology 166, 955–967.
| Autoregulation of nodulation (AON) in Pisum sativum (pea) involves signalling events associated with both nodule primordia development and nitrogen fixation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmslarur8%3D&md5=5602d512011b6d459a8b867b9904edd5CAS | 19403196PubMed |
Lim CW, Lee YW, Hwang CH (2011) Soybean nodule-enhanced CLE peptides in roots act as signals in GmNARK-mediated nodulation suppression. Plant & Cell Physiology 52, 1613–1627.
| Soybean nodule-enhanced CLE peptides in roots act as signals in GmNARK-mediated nodulation suppression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1SiurrJ&md5=377c570f003f5cc6b3c3e2fa6d648d15CAS |
Lin Y-H, Ferguson BJ, Kereszt A, Gresshoff PM (2010) Suppression of hypernodulation in soybean by a leaf-extracted, NARK- and Nod factor-dependent, low molecular mass fraction. New Phytologist 185, 1074–1086.
| Suppression of hypernodulation in soybean by a leaf-extracted, NARK- and Nod factor-dependent, low molecular mass fraction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXksFCrt7Y%3D&md5=697580f860a786edd0dc9e3a563365adCAS | 20100211PubMed |
Lin Y-H, Lin M-H, Gresshoff PM, Ferguson BJ (2011) An efficient petiole-feeding bioassay for introducing aqueous solutions into dicotyledonous plants. Nature Protocols 6, 36–45.
| An efficient petiole-feeding bioassay for introducing aqueous solutions into dicotyledonous plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXisVShsQ%3D%3D&md5=1dec4c966e6a9a4feb1756ee1e26f25cCAS | 21212781PubMed |
Lin M-H, Gresshoff PM, Ferguson BJ (2012) Systemic regulation of soybean nodulation by acidic growth conditions. Plant Physiology 160, 2028–2039.
| Systemic regulation of soybean nodulation by acidic growth conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVKmt7fM&md5=0f9a68c07585bcb3eccd60edd2455aeaCAS | 23054568PubMed |
Magori S, Kawaguchi M (2010) Analysis of two potential long-distance signaling molecules, LjCLE-RS1/2and jasmonic acid, in a hypernodulating mutant too much love. Plant Signaling & Behavior 5, 403–405.
| Analysis of two potential long-distance signaling molecules, LjCLE-RS1/2and jasmonic acid, in a hypernodulating mutant too much love.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFemu73K&md5=7432168155ca38fec35e9b55f6336319CAS |
Magori S, Oka-Kira E, Shibata S, Umehara Y, Kouchi H, Hase Y, Tanaka A, Sato S, Tabata S, Kawaguchi M (2009) TOO MUCH LOVE, a root regulator associated with the long-distance control of nodulation in Lotus japonicus. Molecular Plant-Microbe Interactions 22, 259–268.
| TOO MUCH LOVE, a root regulator associated with the long-distance control of nodulation in Lotus japonicus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXisVWmsrs%3D&md5=dc2d472db13d6aa3d22308edfdde73b8CAS | 19245320PubMed |
Matsubayashi Y (2014) Posttranslationally modified small-peptide signals in plants. Annual Review of Plant Biology 65, 385–413.
| Posttranslationally modified small-peptide signals in plants.Crossref | GoogleScholarGoogle Scholar | 24779997PubMed |
Meng L, Ruth KC, Fletcher JC, Feldman L (2010) The roles of different CLE domains in Arabidopsis CLE polypeptide activity and functional specificity. Molecular Plant 3, 760–772.
| The roles of different CLE domains in Arabidopsis CLE polypeptide activity and functional specificity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpsFKktrY%3D&md5=4f87ced4a1173961fe6122ca47c1509dCAS | 20494950PubMed |
Mitchum MG, Wang X, Wang J, Davis EL (2012) Role of nematode peptides and other small molecules in plant parasitism. Annual Review of Phytopathology 50, 175–195.
| Role of nematode peptides and other small molecules in plant parasitism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVWht7zE&md5=f3f224515cc3f580ad672d8186a81afdCAS | 22578179PubMed |
Miyahara A, Hirani TA, Oakes M, Kereszt A, Kobe B, Djordjevic MA, Gresshoff PM (2008) Soybean nodule autoregulation receptor kinase phosphorylates two kinase-associated protein phosphatases in vitro. The Journal of Biological Chemistry 283, 25381–25391.
| Soybean nodule autoregulation receptor kinase phosphorylates two kinase-associated protein phosphatases in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVyisLvK&md5=b985927ceffd766be6dcb8dbb709d9d4CAS | 18606823PubMed |
Miyazawa H, Oka-Kira E, Sato N, Takahashi H, Wu G-J, Sato S, Hayashi M, Betsuyaku S, Nakazono M, Tabata S, Harada K, Sawa S, Fukuda H, Kawaguchi M (2010) The receptor-like kinase KLAVIER mediates systemic regulation of nodulation and non-symbiotic shoot development in Lotus japonicus. Development 137, 4317–4325.
| The receptor-like kinase KLAVIER mediates systemic regulation of nodulation and non-symbiotic shoot development in Lotus japonicus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFGmurk%3D&md5=65ebf69aea34e0340cb41677663276e9CAS | 21098572PubMed |
Mortier V, Den Herder G, Whitford R, Van De Velde W, Rombauts S, D’haeseleer K, Holsters M, Goormachtig S (2010) CLE peptides control Medicago truncatula nodulation locally and systemically. Plant Physiology 153, 222–237.
| CLE peptides control Medicago truncatula nodulation locally and systemically.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnt1Ggs74%3D&md5=514c973fce7405edd87e8c4421490bd2CAS | 20348212PubMed |
Mortier V, De Wever E, Vuylsteke M, Holsters M, Goormachtig S (2012) Nodule numbers are governed by interaction between CLE peptides and cytokinin signaling. The Plant Journal 70, 367–376.
| Nodule numbers are governed by interaction between CLE peptides and cytokinin signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmslOgtbc%3D&md5=33e60135fc842f3acbe46814fdf17c12CAS | 22168914PubMed |
Ni J, Clark SE (2006) Evidence for functional conservation, sufficiency, and proteolytic processing of the CLAVATA3 CLE domain. Plant Physiology 140, 726–733.
| Evidence for functional conservation, sufficiency, and proteolytic processing of the CLAVATA3 CLE domain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjsV2iu7w%3D&md5=23d058ce2b5a3d85f9bba7a3e2ca4710CAS | 16407446PubMed |
Ni J, Guo Y, Jin H, Hartsell J, Clark S (2011) Characterization of a CLE processing activity. Plant Molecular Biology 75, 67–75.
| Characterization of a CLE processing activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsF2gsbnF&md5=4b4d1bd9e3e1571c014a47e217a858e5CAS | 21052783PubMed |
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.
| HAR1 mediates systemic regulation of symbiotic organ development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XptFCis7k%3D&md5=07ae29a28244fd52d5f1ca34101c4068CAS | 12442172PubMed |
Nontachaiyapoom S, Scott PT, Men AE, Kinkema M, Schenk PM, Gresshoff PM (2007) Promoters of orthologous Glycine max and Lotus japonicus nodulation autoregulation genes interchangeably drive phloem-specific expression in transgenic plants. Molecular Plant-Microbe Interactions 20, 769–780.
| Promoters of orthologous Glycine max and Lotus japonicus nodulation autoregulation genes interchangeably drive phloem-specific expression in transgenic plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmvFanurY%3D&md5=77ed933de9383d50cba910c4c095379fCAS | 17601165PubMed |
Oelkers K, Goffard N, Weiller G, Gresshoff PM, Mathesius U, Frickey T (2008) Bioinformatic analysis of the CLE signaling peptide family. BMC Plant Biology 8, 1
| Bioinformatic analysis of the CLE signaling peptide family.Crossref | GoogleScholarGoogle Scholar | 18171480PubMed |
Ogawa M, Shinohara H, Sakagami Y, Matsubayashi Y (2008) Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319, 294
| Arabidopsis CLV3 peptide directly binds CLV1 ectodomain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmt1Oqtw%3D%3D&md5=127310ceaa9216700317576513c96946CAS | 18202283PubMed |
Ogawa-Ohnishi M, Matsushita W, Matsubayashi Y (2013) Identification of three hydroxyproline O-arabinosyltransferases in Arabidopsis thaliana. Nature Chemical Biology 9, 726–730.
| Identification of three hydroxyproline O-arabinosyltransferases in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVeru7fP&md5=52ae06719c4c648dd01f85d48064f7fdCAS | 24036508PubMed |
Ohyama K, Shinohara H, Ogawa-Ohnishi M, Matsubayashi Y (2009) A glycopeptide regulating stem cell fate in Arabidopsis thaliana. Nature Chemical Biology 5, 578–580.
| A glycopeptide regulating stem cell fate in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnt1Sht70%3D&md5=fa47971b8db75f9700a20469068b1c9bCAS | 19525968PubMed |
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 Physiology 50, 67–77.
| Nod Factor/nitrate-induced CLE genes that drive HAR1-mediated systemic regulation of nodulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVegsrw%3D&md5=129484f4016e20269424aa4e497341abCAS |
Okamoto S, Nakagawa T, Kawaguchi M (2011) Expression and functional analysis of a CLV3-like gene in the model legume Lotus japonicus. Plant & Cell Physiology 52, 1211–1221.
| Expression and functional analysis of a CLV3-like gene in the model legume Lotus japonicus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXoslOisrY%3D&md5=6c4808f773633a90c73ba966a2049491CAS |
Okamoto S, Shinohara H, Mori T, Matsubayashi Y, Kawaguchi M (2013) Root-derived CLE glycopeptides control nodulation by direct binding to HAR1 receptor kinase. Nature Communications 4, 2191
| Root-derived CLE glycopeptides control nodulation by direct binding to HAR1 receptor kinase.Crossref | GoogleScholarGoogle Scholar | 23934307PubMed |
Oldroyd GED (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nature Reviews. Microbiology 11, 252–263.
| Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXktVKjtLc%3D&md5=8f6924e546ce67182911fa224e351fe3CAS |
Osipova MA, Mortier V, Demchenko KN, Tsyganov VE, Tikhonovich IA, Lutova LA, Dolgikh EA, Goormachtig S (2012) WUSCHEL-RELATED HOMEOBOX5 gene expression and interaction of CLE peptides with components of the systemic control add two pieces to the puzzle of autoregulation of nodulation. Plant Physiology 158, 1329–1341.
| WUSCHEL-RELATED HOMEOBOX5 gene expression and interaction of CLE peptides with components of the systemic control add two pieces to the puzzle of autoregulation of nodulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XltVOksbg%3D&md5=8a9687ddced2eed4c196d19ea47cb53aCAS | 22232385PubMed |
Postma JG, Jacobsen E, Feenstra WJ (1988) Three pea mutants with an altered nodulation studied by genetic analysis and grafting. Journal of Plant Physiology 132, 424–430.
| Three pea mutants with an altered nodulation studied by genetic analysis and grafting.Crossref | GoogleScholarGoogle Scholar |
Reid DE, Ferguson BJ, Gresshoff PM (2011a) Inoculation- and nitrate-induced CLE peptides of soybean control NARK-dependent nodule formation. Molecular Plant-Microbe Interactions 24, 606–618.
| Inoculation- and nitrate-induced CLE peptides of soybean control NARK-dependent nodule formation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltF2ltrY%3D&md5=796db89694ae285141ac0ca2fbdfd87dCAS | 21198362PubMed |
Reid DE, Ferguson BJ, Hayashi S, Lin Y-H, Gresshoff PM (2011b) Molecular mechanisms controlling legume autoregulation of nodulation. Annals of Botany 108, 789–795.
| Molecular mechanisms controlling legume autoregulation of nodulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1eisbrE&md5=f360a37ca6bbfde308aa7a4680cb30deCAS | 21856632PubMed |
Reid DE, Hayashi S, Lorenc M, Stiller J, Edwards D, Gresshoff PM, Ferguson BJ (2012) Identification of systemic responses in soybean nodulation by xylem sap feeding and complete transcriptome sequencing reveal a novel component of the autoregulation pathway. Plant Biotechnology Journal 10, 680–689.
| Identification of systemic responses in soybean nodulation by xylem sap feeding and complete transcriptome sequencing reveal a novel component of the autoregulation pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVWgurfK&md5=d9722f2710bbb1e31558a3cf6f53bc93CAS | 22624681PubMed |
Reid DE, Li D, Ferguson BJ, Gresshoff PM (2013) Structure–function analysis of the GmRIC1 signal peptide and CLE domain required for nodulation control in soybean. Journal of Experimental Botany 64, 1575–1585.
| Structure–function analysis of the GmRIC1 signal peptide and CLE domain required for nodulation control in soybean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlsV2ktbY%3D&md5=9a4a13f836d326788599a7c243e3714eCAS | 23386683PubMed |
Rojo E, Sharma V, Kovaleva V, Raikhel N, Fletcher J (2002) CLV3 is localized to the extracellular space, where it activates the Arabidopsis CLAVATA stem cell signaling pathway. The Plant Cell 14, 969–977.
| CLV3 is localized to the extracellular space, where it activates the Arabidopsis CLAVATA stem cell signaling pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XksVGqsbs%3D&md5=bb4c65c508218fbd6aebf9a12602eb39CAS | 12034890PubMed |
Sagan M, Duc G (1996) Sym28 and Sym29, two new genes involved in regulation of nodulation in pea (Pisum sativum L.). Symbiosis 20, 229–245.
Sasaki T, Suzaki T, Soyano T, Kojima M, Sakakibara H, Kawaguchi M (2014) Shoot-derived cytokinins systemically regulate root nodulation. Nature Communications 5, 4983
| Shoot-derived cytokinins systemically regulate root nodulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitVWgsLnM&md5=5792682d9bdb8d7e1caae93095970362CAS | 25236855PubMed |
Saur IML, Oakes M, Djordjevic MA, Imin N (2011) Crosstalk between the nodulation signaling pathway and the autoregulation of nodulation in Medicago truncatula. New Phytologist 190, 865–874.
| Crosstalk between the nodulation signaling pathway and the autoregulation of nodulation in Medicago truncatula.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXot1Crur4%3D&md5=b94ea9cdc1037da750cf875fdbb29336CAS |
Sawa S, Kinoshita A, Nakanomyo I, Fukuda H (2006) CLV3/ESR-related (CLE) peptides as intercellular signaling molecules in plants. Chemical Record 6, 303–310.
| CLV3/ESR-related (CLE) peptides as intercellular signaling molecules in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXksVWmtLk%3D&md5=bb339d0d4003ec787a8baba735fbe019CAS | 17304552PubMed |
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 Physiology 136, 2483–2499.
| Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvFOrtbc%3D&md5=bfd116c6503b4f1dc68a09764f2ce255CAS | 15375205PubMed |
Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du J, Tian Z, Zhu L, Gill N, Joshi T, Libault M, Sethuraman A, Zhang X-C, Shinozaki K, Nguyen HT, Wing RA, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker RC, Jackson SA (2010) Genome sequence of the palaeopolyploid soybean. Nature 463, 178–183.
| Genome sequence of the palaeopolyploid soybean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXntVClsQ%3D%3D&md5=26223eabf9b254cb7bb9c6268bb834d2CAS | 20075913PubMed |
Schnabel E, Journet E-P, Carvalho-Niebel DF, Duc G, Frugoli J (2005) The Medicago truncatula SUNN gene encodes a CLV1-like Leucine-rich repeat receptor kinase that regulates nodule number and root length. Plant Molecular Biology 58, 809–822.
| The Medicago truncatula SUNN gene encodes a CLV1-like Leucine-rich repeat receptor kinase that regulates nodule number and root length.Crossref | GoogleScholarGoogle Scholar | 16240175PubMed |
Schnabel E, Kassaw T, Smith L, Marsh J, Oldroyd GE, Long SR, Frugoli J (2011) ROOT DETERMINED NODULATION 1 regulates nodule number in M. truncatula and defines a highly conserved, uncharacterized plant gene family. Plant Physiology 157, 328–340.
| ROOT DETERMINED NODULATION 1 regulates nodule number in M. truncatula and defines a highly conserved, uncharacterized plant gene family.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1Sit7zK&md5=ebc25bd3485d08abf3fd1642f0c207d0CAS | 21742814PubMed |
Searle IR, Men AE, Laniya TS, Buzas DM, Iturbe-Ormaetxe I, Carroll BJ, Gresshoff PM (2003) Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase. Science 299, 109–112.
| Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XpvVensLo%3D&md5=e01908423ff2786a8e2ea992db1003d7CAS | 12411574PubMed |
Shinohara H, Matsubayashi Y (2013) Chemical synthesis of Arabidopsis CLV3 glycopeptide reveals the impact of hydroxyproline arabinosylation on peptide conformation and activity. Plant & Cell Physiology 54, 369–374.
| Chemical synthesis of Arabidopsis CLV3 glycopeptide reveals the impact of hydroxyproline arabinosylation on peptide conformation and activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjslGmtrc%3D&md5=721ae47a09fd6bc992aefd84bdbe417cCAS |
Shinohara H, Moriyama Y, Ohyama K, Matsubayashi Y (2012) Biochemical mapping of a ligand-binding domain within Arabidopsis BAM1 reveals diversified ligand recognition mechanisms of plant LRR-RKs. The Plant Journal 70, 845–854.
| Biochemical mapping of a ligand-binding domain within Arabidopsis BAM1 reveals diversified ligand recognition mechanisms of plant LRR-RKs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xps12qsb8%3D&md5=5b007856dc0097381e5c7dc2ab8be465CAS | 22321211PubMed |
Song X-F, Guo P, Ren S-C, Xu T-T, Liu C-M (2013) Antagonistic peptide technology for functional dissection of CLV3/ESR genes in Arabidopsis. Plant Physiology 161, 1076–1085.
| Antagonistic peptide technology for functional dissection of CLV3/ESR genes in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmvFKrtLw%3D&md5=719d21416e409855d90ca9861ea65be9CAS | 23321419PubMed |
Soyano T, Hirakawa H, Sato S, Hayashi M, Kawaguchi M (2014) NODULE INCEPTION creates a long-distance negative feedback loop involved in homeostatic regulation of nodule organ production. Proceedings of the National Academy of Sciences of the United States of America
| NODULE INCEPTION creates a long-distance negative feedback loop involved in homeostatic regulation of nodule organ production.Crossref | GoogleScholarGoogle Scholar | 25246578PubMed |
Stefanović S, Pfeil BE, Palmer JD, Doyle JJ (2009) Relationships among phaseoloid legumes based on sequences from eight chloroplast regions. Systematic Botany 34, 115–128.
| Relationships among phaseoloid legumes based on sequences from eight chloroplast regions.Crossref | GoogleScholarGoogle 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 Physiology 140, 1331–1344.
| Gain-of-function phenotypes of many CLAVATA3/ESR genes, including four new family members, correlate with tandem variations in the conserved CLAVATA3/ESR domain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjslyqu7k%3D&md5=b5145f611c9bb80190aab6073a0cc030CAS | 16489133PubMed |
Sutton MA, Oenema O, Erisman JW, Leip A, Van Grinsven H, Winiwarter W (2011) Too much of a good thing. Nature 472, 159–161.
| Too much of a good thing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXksFWgt74%3D&md5=c81b5195ad410c8f2fa1cf777e374997CAS | 21478874PubMed |
Takahara M, Magori S, Soyano T, Okamoto S, Yoshida C, Yano K, Sato S, Tabata S, Yamaguchi K, Shigenobu S, Takeda N, Suzaki T, Kawaguchi M (2013) TOO MUCH LOVE, a novel kelch repeat-containing F-box protein, functions in the long-distance regulation of the legume–Rhizobium symbiosis. Plant & Cell Physiology 54, 433–447.
| TOO MUCH LOVE, a novel kelch repeat-containing F-box protein, functions in the long-distance regulation of the legume–Rhizobium symbiosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlsV2mtr0%3D&md5=2212f376cfdfb8da29547df2b0a357abCAS |
Udvardi MK, Price GD, Gresshoff PM, Day DA (1988) A dicarboxylate transporter on the peribacteroid membrane of soybean nodules. FEBS Letters 231, 36–40.
| A dicarboxylate transporter on the peribacteroid membrane of soybean nodules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXktlGnsbs%3D&md5=a77244f56509314506220bd335eca254CAS |
Wong CE, Singh MB, Bhalla PL (2013) Spatial expression of CLAVATA3 in the shoot apical meristem suggests it is not a stem cell marker in soybean. Journal of Experimental Botany 64, 5641–5649.
| Spatial expression of CLAVATA3 in the shoot apical meristem suggests it is not a stem cell marker in soybean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXotlOn&md5=9d0d2ecbf52ea61d6f1c37b948fff4f3CAS | 24179098PubMed |
Xu T-T, Song X-F, Ren S-C, Liu C-M (2013) The sequence flanking the N-terminus of the CLV3 peptide is critical for its cleavage and activity in stem cell regulation in Arabidopsis. BMC Plant Biology 13, 225
| The sequence flanking the N-terminus of the CLV3 peptide is critical for its cleavage and activity in stem cell regulation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 24369789PubMed |
