Skip to main content
SpringerLink
Log in

Additional Signalling Compounds are Required to Orchestrate Plant Development

  • Thematic Article
  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Plants are necessarily complex systems that require monitoring of multiple environmental signals and, in response to those signals, coordination of differentiation and development of an extensive array of cell types at multiple locations. This coordination must rely on integration of long-distance signals that provide a means of communication among different plant parts. We propose that the relatively well-characterized classical phytohormones must act with several other long-distance signals to achieve this level of organization with dynamic yet measured responses. This is supported by observations that classical phytohormones: (i) operate in complex yet experimentally unresolved networks involving cross-talk and feedback, (ii) are generally multifunctional and nonspecific and hence must rely on other long-distance cues or pre-set conditions to achieve specificity and (iii) are likely to mask roles of other long-distance signals in several experimental contexts. We present evidence for involvement of novel long-distance signals in three developmental processes—branching, flowering and nodulation, and discuss the possible identities of novel signalling molecules.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5

Similar content being viewed by others

References

  1. T Araki Y Komeda (1993) ArticleTitleFlowering in darkness in Arabidopsis thaliana. Plant J 4 801–811 Occurrence Handle10.1046/j.1365-313X.1993.04050801.x

    Article  Google Scholar 

  2. MJ Aukerman RM Amasino (1998) ArticleTitleFloral induction and florigen. Cell 93 491–494 Occurrence Handle1:CAS:528:DyaK1cXjsFWhsrw%3D Occurrence Handle9604924 Occurrence Handle10.1016/S0092-8674(00)81178-2

    Article  CAS  PubMed  Google Scholar 

  3. G Bernier A Havelange C Houssa A Petitjean P Lejeune (1993) ArticleTitlePhysiological signals that induce flowering. Plant Cell 5 1147–1155 Occurrence Handle1:CAS:528:DyaK2cXntlaqtA%3D%3D Occurrence Handle12271018 Occurrence Handle10.1105/tpc.5.10.1147

    Article  CAS  PubMed  Google Scholar 

  4. CA Beveridge IC Murfet (1996) ArticleTitleThe gigas mutant in pea is deficient in the floral stimulus. Physiol Plant 96 637–645 Occurrence Handle1:CAS:528:DyaK28Xisleqsbk%3D Occurrence Handle10.1111/j.1399-3054.1996.tb00237.x

    Article  CAS  Google Scholar 

  5. CA Beveridge IC Murfet L Kerhoas B Sotta E Miginiac C Rameau (1997a) ArticleTitleThe shoot controls zeatin riboside export from pea roots. Evidence from the branching mutant rms4. Plant J 11 339–345 Occurrence Handle1:CAS:528:DyaK2sXitFCktbc%3D Occurrence Handle10.1046/j.1365-313X.1997.11020339.x

    Article  CAS  Google Scholar 

  6. CA Beveridge JJ Ross IC Murfet (1992) ArticleTitleMutant dn influences dry matter distribution, assimilate partitioning and flowering in Lathyrus odoratus L. J Exp Bot 43 55–62 Occurrence Handle10.1093/jxb/43.1.55

    Article  Google Scholar 

  7. CA Beveridge JJ Ross IC Murfet (1996) ArticleTitleBranching in pea. Action of genes Rms3 and Rms4. Plant Physiol 110 859–865 Occurrence Handle1:CAS:528:DyaK28Xhs1GisLY%3D Occurrence Handle12226224

    CAS  PubMed  Google Scholar 

  8. CA Beveridge GM Symons IC Murfet JJ Ross C Rameau (1997b) ArticleTitleThe rms1 mutant of pea has elevated indole-3-acetic acid levels and reduced root-sap zeatin riboside content but increased branching controlled by graft-transmissible signal(s). Plant Physiol 115 1251–1258 Occurrence Handle1:CAS:528:DyaK2sXns1ykurY%3D

    CAS  Google Scholar 

  9. CA Beveridge GM Symons CGN Turnbull (2000) ArticleTitleAuxin inhibition of decapitation induced branching is dependent on graft-transmissible signals regulated by genes Rms1 and Rms2. Plant Physiol 123 689–697 Occurrence Handle1:CAS:528:DC%2BD3cXktlWnur4%3D Occurrence Handle10859199 Occurrence Handle10.1104/pp.123.2.689

    Article  CAS  PubMed  Google Scholar 

  10. CA Beveridge JL Weller SR Singer JMI Hofer (2003) ArticleTitleAxillary meristem development: budding relationships between networks controlling flowering, branching and photoperiod responsiveness. Plant Physiol in press in press

    Google Scholar 

  11. CA Beveridge (2000) ArticleTitleLong distance signalling and a mutational analysis of branching in pea. Plant Growth Regul 32 193–203 Occurrence Handle1:CAS:528:DC%2BD3MXisFWmtLo%3D Occurrence Handle10.1023/A:1010718020095

    Article  CAS  Google Scholar 

  12. JM Caba M Luz-Centeno B Fernández PM Gresshoff F Ligero (2000) ArticleTitleInoculation and nitrate alter phytohormone levels in soybean roots:differences between a supernodulating mutant and the wild type. Planta 211 98–104 Occurrence Handle1:CAS:528:DC%2BD3cXjvVyhsLk%3D Occurrence Handle10923709 Occurrence Handle10.1007/s004250000265

    Article  CAS  PubMed  Google Scholar 

  13. JD Cancel PB Larsen (2002) ArticleTitleLoss-of-function mutations in the ethylene receptor ETR1 cause enhanced sensitivity and exaggerated response to ethylene in Arabidopsis. Plant Physiol 129 1557–1567 Occurrence Handle1:CAS:528:DC%2BD38Xmtl2gsbg%3D Occurrence Handle12177468 Occurrence Handle10.1104/pp.003780

    Article  CAS  PubMed  Google Scholar 

  14. BJ Carroll DL McNeil PM Gresshoff (1985) ArticleTitleIsolation and properties of soybean mutants which nodulate in the presence of high nitrate concentrations. Proc Natl Acad Sci USA 82 4162–4166 Occurrence Handle1:CAS:528:DyaL2MXkvVGhsLo%3D Occurrence Handle16593577 Occurrence Handle10.1073/pnas.82.12.4162

    Article  CAS  PubMed  Google Scholar 

  15. WH Cheng A Endo L Zhou J Penney HC Chen A Arroyo P Leon E Nambara T Asami M Seo T Koshiba J Sheen (2002) ArticleTitleA unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and functions. Plant Cell 14 2723–2743 Occurrence Handle1:CAS:528:DC%2BD38XovF2qtbc%3D Occurrence Handle12417697 Occurrence Handle10.1105/tpc.006494

    Article  CAS  PubMed  Google Scholar 

  16. SE Clark (2001) ArticleTitleCell signalling at the shoot meristem. Nature Reviews. Mol Cell Biol 2 276–284 Occurrence Handle1:CAS:528:DC%2BD3MXis12jtLk%3D

    CAS  Google Scholar 

  17. J Colasanti V Sundaresan (2000) ArticleTitle‘Florigen’ enters the molecular age: long-distance signals that cause plants to flower. Trends Biochem Sci 25 236–240 Occurrence Handle1:CAS:528:DC%2BD3cXjtVeru7k%3D Occurrence Handle10782094 Occurrence Handle10.1016/S0968-0004(00)01542-5

    Article  CAS  PubMed  Google Scholar 

  18. J Colasanti Z Yuan V Sundaresan (1998) ArticleTitleThe indeterminate gene encodes a zinc finger protein and regulates a leaf-generated signal required for the transition to flowering in maize. Cell 93 593–603 Occurrence Handle1:CAS:528:DyaK1cXjsFWhs7w%3D Occurrence Handle9604934 Occurrence Handle10.1016/S0092-8674(00)81188-5

    Article  CAS  PubMed  Google Scholar 

  19. C Curie J-F Briat (2003) ArticleTitleIron transport and signaling in plants. Annu Rev Plant Biol 54 07.1–07.24 Occurrence Handle10.1146/annurev.arplant.54.031902.135018

    Article  Google Scholar 

  20. AC Delves A Mathews D Day AS Carter BJ Carroll PM Gresshoff (1986) ArticleTitleRegulation of the soybean-Rhizobium symbiosis by shoot and root factors. Plant Physiol 82 588–590 Occurrence Handle1:STN:280:DC%2BC3cnhslagtQ%3D%3D Occurrence Handle16665072 Occurrence Handle10.1104/pp.82.2.588

    Article  CAS  PubMed  Google Scholar 

  21. AC Delves A Higgins PM Gresshoff (1992) ArticleTitleThe shoot apex is not the source of the systemic signal controlling nodule numbers in soybean. Plant Cell Environ 15 249–254 Occurrence Handle10.1111/j.1365-3040.1992.tb01479.x

    Article  Google Scholar 

  22. J Dénarié F Debellé J-C Promé (1996) ArticleTitle Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Ann Rev Biochem 65 503–535 Occurrence Handle8811188 Occurrence Handle10.1146/annurev.bi.65.070196.002443

    Article  PubMed  Google Scholar 

  23. IC Dodd (2003) ArticleTitleHormonal interactions and stomatal responses. J Plant Growth Regul 22 32–46 Occurrence Handle1:CAS:528:DC%2BD3sXosF2ktbk%3D Occurrence Handle10.1007/s00344-003-0023-x

    Article  CAS  Google Scholar 

  24. G Endre A Kereszt Z Kevei S Mihacea P Kalo GB Kiss (2002) ArticleTitleA receptor kinase regulating symbiotic nodule development. Nature 417 962–966 Occurrence Handle1:CAS:528:DC%2BD38XkvVagsbk%3D Occurrence Handle12087406 Occurrence Handle10.1038/nature00842

    Article  CAS  PubMed  Google Scholar 

  25. BJ Ferguson U Mathesius (2003) ArticleTitleSignaling interactions during nodule development. J Plant Growth Regul 22 47–72 Occurrence Handle1:CAS:528:DC%2BD3sXosF2ktbY%3D Occurrence Handle10.1007/s00344-003-0032-9

    Article  CAS  Google Scholar 

  26. AR Fernie L Willmitzer (2001) ArticleTitleMolecular and biochemical triggers of potato tuber development. Plant Physiol 127 1459–1465 Occurrence Handle1:CAS:528:DC%2BD38XjtVWgsA%3D%3D Occurrence Handle11743089 Occurrence Handle10.1104/pp.010764

    Article  CAS  PubMed  Google Scholar 

  27. JC Fletcher (2002) ArticleTitleShoot and floral meristem maintenance in Arabidopsis. Annu Rev Plant Biol 53 45–66 Occurrence Handle1:CAS:528:DC%2BD38XlsVWhtb8%3D Occurrence Handle12221985 Occurrence Handle10.1146/annurev.arplant.53.092701.143332

    Article  CAS  PubMed  Google Scholar 

  28. E Foo CGN Turnbull CA Beveridge (2001) ArticleTitleLong-distance signalling and control of branching in the rms1 mutant of pea. Plant Physiol 126 203–209 Occurrence Handle1:CAS:528:DC%2BD3MXjslWjsb8%3D Occurrence Handle11351083 Occurrence Handle10.1104/pp.126.1.203

    Article  CAS  PubMed  Google Scholar 

  29. PM Gresshoff (1993) ArticleTitleMolecular genetic analysis of nodulation genes in soybean. Plant Breeding Rev 11 275–318

    Google Scholar 

  30. PM Gresshoff (2003) ArticleTitlePost-genomic insights into plant nodulation symbioses. Genome Biol 4 201 Occurrence Handle12540294 Occurrence Handle10.1186/gb-2003-4-1-201

    Article  PubMed  Google Scholar 

  31. SL Harmer JB Hogenesch M Straume HS Chang B Han T Zhu X Wang JA Kreps SA Kay (2000) ArticleTitleOrchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290 2110–2113 Occurrence Handle1:CAS:528:DC%2BD3cXptVyisrw%3D Occurrence Handle11118138 Occurrence Handle10.1126/science.290.5499.2110

    Article  CAS  PubMed  Google Scholar 

  32. A Havelange P Lejeune G Bernier (2000) ArticleTitleSucrose/cytokinin interaction in Sinapis alba at floral induction: a shoot-to-root-to-shoot physiological loop. Physiol Plant 109 343–350 Occurrence Handle1:CAS:528:DC%2BD3cXkvFCqsrw%3D Occurrence Handle10.1034/j.1399-3054.2000.100316.x

    Article  CAS  Google Scholar 

  33. S Hoffmann-Benning DA Gage L McIntosh H Kende JA Zeevaart (2002) ArticleTitleComparison of peptides in the phloem sap of flowering and non-flowering Perilla and lupine plants using microbore HPLC followed by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Planta 216 140–147 Occurrence Handle1:CAS:528:DC%2BD38Xps1ehtLs%3D Occurrence Handle12430023 Occurrence Handle10.1007/s00425-002-0916-0

    Article  CAS  PubMed  Google Scholar 

  34. TJ Ingram JB Reid J MacMillan (1986) ArticleTitleThe quantitative relationship between gibberellin A1 and internode growth in Pisum sativum L. Planta 168 414–420 Occurrence Handle1:CAS:528:DyaL28XlsV2rt7w%3D Occurrence Handle10.1007/BF00392370

    Article  CAS  Google Scholar 

  35. SD Jackson (1999) ArticleTitleMultiple signaling pathways control tuber induction in potato. Plant Physiol 119 1–8 Occurrence Handle1:CAS:528:DyaK1MXmt1Gmsw%3D%3D Occurrence Handle9880339 Occurrence Handle10.1104/pp.119.1.1

    Article  CAS  PubMed  Google Scholar 

  36. Q Jiang PM Gresshoff (2002) ArticleTitleShoot-control and genetic mapping of the har1-1 (hypernodulation and aberrant root formation) mutant of Lotus japonicus. Funct Plant Biol. 29 1371–1376 Occurrence Handle1:CAS:528:DC%2BD38Xps1ygtLY%3D Occurrence Handle10.1071/PP01097

    Article  CAS  Google Scholar 

  37. RA Jorgensen (2002) ArticleTitleRNA traffics information systemically in plants. Proc Natl Acad Sci USA 99 11561–11563 Occurrence Handle1:CAS:528:DC%2BD38XntFWqs7w%3D Occurrence Handle12195023 Occurrence Handle10.1073/pnas.192449099

    Article  CAS  PubMed  Google Scholar 

  38. MO Kelly PJ Davies (1988) ArticleTitlePhotoperiodic and genetic control of carbon partitioning in peas and its relationship to apical senescence. Plant Physiol 86 978–982 Occurrence Handle1:CAS:528:DyaL1cXhvVektL8%3D Occurrence Handle16666020 Occurrence Handle10.1104/pp.86.3.978

    Article  CAS  PubMed  Google Scholar 

  39. RW King LT Evans (2003) ArticleTitleGibberellins and flowering of grasses and cereals: prizing open the lid of the “florigen” black box. Annu Rev Plant Biol 54 12.1–12.22 Occurrence Handle10.1146/annurev.arplant.54.031902.135029

    Article  Google Scholar 

  40. RW King LT Evans LN Mander T Moritz RP Pharis B Twitchin (2003) ArticleTitleSynthesis of gibberellin GA(6) and its role in flowering of Lolium temulentum. Phytochemistry 62 77–82 Occurrence Handle1:CAS:528:DC%2BD38XptlCktrc%3D Occurrence Handle12475622 Occurrence Handle10.1016/S0031-9422(02)00447-8

    Article  CAS  PubMed  Google Scholar 

  41. RW King T Moritz LT Evans O Junttila AJ Herlt (2001) ArticleTitleLong-day induction of flowering in Lolium temulentum involves sequential increases in specific gibberellins at the shoot apex. Plant Physiol 127 624–632 Occurrence Handle1:CAS:528:DC%2BD3MXnslGlu78%3D Occurrence Handle11598236 Occurrence Handle10.1104/pp.010378

    Article  CAS  PubMed  Google Scholar 

  42. WM King IC Murfet (1985) ArticleTitleFlowering in Pisum: a sixth locus, Dne. Ann Bot 56 835–846

    Google Scholar 

  43. H Kitano (2002) ArticleTitleComputational systems biology. Nature 420 206–210 Occurrence Handle1:CAS:528:DC%2BD38Xos1Gnsbo%3D Occurrence Handle12432404 Occurrence Handle10.1038/nature01254

    Article  CAS  PubMed  Google Scholar 

  44. L Krusell LH Madsen S Sato G Aubert A Genua K Szczyglowski G Duc T Kaneko S Tabata F de Bruijn E Pajuelo N Sandal J Stougaard (2002) ArticleTitleShoot control of root development is mediated by a receptor-like kinase. Nature 420 422–426 Occurrence Handle1:CAS:528:DC%2BD38XptFCis7w%3D Occurrence Handle12442170 Occurrence Handle10.1038/nature01207

    Article  CAS  PubMed  Google Scholar 

  45. A Lang (1977) ArticleTitlePromotion and inhibition of flower formation in a day-neutral plant in grafts with a short-day plant and a long-day plant. Proc Natl Acad Sci USA 74 2412–2416 Occurrence Handle1:STN:280:DC%2BC3cngslKhug%3D%3D Occurrence Handle16592404 Occurrence Handle10.1073/pnas.74.6.2412

    Article  CAS  PubMed  Google Scholar 

  46. HMO Leyser (2001) ArticleTitleAuxin. Curr Biol 11 R728 Occurrence Handle1:CAS:528:DC%2BD3MXntV2gsbo%3D Occurrence Handle10.1016/S0960-9822(01)00431-6

    Article  CAS  Google Scholar 

  47. O Leyser X-W Deng (2000) ArticleTitleCell signalling and gene regulation: new directions in plant signalling. Curr Opin Plant Biol 3 351–352 Occurrence Handle10.1016/S1369-5266(00)00095-9

    Article  Google Scholar 

  48. K Lindsey S Casson P Chilley (2002) ArticleTitlePeptides: new signalling molecules in plants. Trends Plant Sci 7 78–83 Occurrence Handle1:CAS:528:DC%2BD38XhvFyku7o%3D Occurrence Handle11832279 Occurrence Handle10.1016/S1360-1385(01)02194-X

    Article  CAS  PubMed  Google Scholar 

  49. J Liu J Yu L McIntosh H Kende JA Zeevaart (2001) ArticleTitleIsolation of a CONSTANS ortholog from Pharbitis nil and its role in flowering. Plant Physiol 125 1821–1830 Occurrence Handle1:CAS:528:DC%2BD3MXjtFKqtLY%3D Occurrence Handle11299362 Occurrence Handle10.1104/pp.125.4.1821

    Article  CAS  PubMed  Google Scholar 

  50. JF Martinez-Garcia JL Garcia-Martinez J Bou S Prat (2002a) ArticleTitleThe interaction of gibberellins and photoperiod in the control of potato tuberization. J Plant Growth Regul 20 377–386

    Google Scholar 

  51. JF Martinez-Garcia A Virgos-Soler S Prat (2002b) ArticleTitleControl of photoperiod-regulated tuberization in potato by the Arabidopsis flowering-time gene CONSTANS. Proc Natl Acad Sci USA 99 15211–15216 Occurrence Handle1:CAS:528:DC%2BD38Xpt1yqtb4%3D Occurrence Handle10.1073/pnas.222390599

    Article  CAS  Google Scholar 

  52. Y Matsubayashi Y Sakagami (1996) ArticleTitlePhytosulfokine, sulfated peptides that induce the proliferation of single mesophyll cells of Asparagus officinalis L. Proc Natl Acad Sci USA 93 7623–7627 Occurrence Handle1:CAS:528:DyaK28XksFSrsL4%3D Occurrence Handle8755525 Occurrence Handle10.1073/pnas.93.15.7623

    Article  CAS  PubMed  Google Scholar 

  53. Y Matsubayashi M Ogawa A Morita Y Sakagami (2002) ArticleTitleAn LRR receptor kinase involved in perception of a peptide plant hormone, phytosulfokine. Science 296 1470–1472 Occurrence Handle1:CAS:528:DC%2BD38XktFanurY%3D Occurrence Handle12029134 Occurrence Handle10.1126/science.1069607

    Article  CAS  PubMed  Google Scholar 

  54. AE Men TS Laniya IR Searle I Iturbe-Ormaetxe I Gresshoff Q Jiang BJ Carroll PM Gresshoff (2003) ArticleTitleFast neutron mutagenesis of soybean. Glycine soja L. produces a supernodulating mutant containing a large deletion in Linkage Group H. Genome Lett 1 1–9

    Google Scholar 

  55. SD Michaels RM Amasino (1999) ArticleTitle FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a represser of flowering. Plant Cell 11 949–956 Occurrence Handle1:CAS:528:DyaK1MXjvVajsLc%3D Occurrence Handle10330478 Occurrence Handle10.1105/tpc.11.5.949

    Article  CAS  PubMed  Google Scholar 

  56. S Mlotshwa O Voinnet MF Mette M Matzke H Vaucheret SW Ding G Pruss VB Vance (2002) ArticleTitleRNA silencing and the mobile silencing signal. Plant Cell 14 IssueIDSupp S289–301 Occurrence Handle1:CAS:528:DC%2BD38XksV2hu7s%3D Occurrence Handle12045284

    CAS  PubMed  Google Scholar 

  57. SE Morris CGN Turnbull IC Murfet CA Beveridge (2001) ArticleTitleMutational analysis of branching in pea, Pisum sativum L: evidence that Rms1 and Rms5 regulate the same novel signal. Plant Physiol 126 1205–1213 Occurrence Handle1:CAS:528:DC%2BD3MXlsFegur0%3D Occurrence Handle11457970 Occurrence Handle10.1104/pp.126.3.1205

    Article  CAS  PubMed  Google Scholar 

  58. A Mouradov F Cremer G Coupland (2002) ArticleTitleControl of flowering time: interacting pathways as a basis for diversity. Plant Cell 14 IssueIDSuppl S111–S130 Occurrence Handle1:CAS:528:DC%2BD38XksV2huro%3D Occurrence Handle12045273

    CAS  PubMed  Google Scholar 

  59. IC Murfet (1971) ArticleTitleFlowering in Pisum. Reciprocal grafts between known genotypes. Aust J Biol Sci 24 1089–1101

    Google Scholar 

  60. IC Murfet JB Reid (1993) Developmental mutants. R Casey DR Davies (Eds) Peas-genetics, molecular biology and biotechnology. CAB International Wallingford, UK 165–216

    Google Scholar 

  61. CA Napoli (1996) ArticleTitleHighly branched phenotype of the petunia dad1-1 mutant is reversed by grafting. Plant Physiol 111 27–37 Occurrence Handle1:CAS:528:DyaK28XivFektLw%3D Occurrence Handle12226274

    CAS  PubMed  Google Scholar 

  62. R Nishimura M Hayashi G-J Wu H Kouchi H Imaizumi-Anraku Y Murakami S Kawasaki S Akao M Ohmori M Nagasawa K Harada M Kawaguchi (2002) ArticleTitle HAR1 mediates systemic regulation of symbiotic organ development. Nature 420 426–429 Occurrence Handle1:CAS:528:DC%2BD38XptFCis7k%3D Occurrence Handle12442172 Occurrence Handle10.1038/nature01231

    Article  CAS  PubMed  Google Scholar 

  63. T Nomura M Nakayama JB Reid Y Takeuchi T Yokota (1997) ArticleTitleBlockage of brassinosteriod biosynthesis and sensitivity causes dwarfism in garden pea. Plant Physiol 113 31–37 Occurrence Handle1:CAS:528:DyaK2sXnt1OqtQ%3D%3D Occurrence Handle12223591

    CAS  PubMed  Google Scholar 

  64. GED Oldroyd (2001) ArticleTitleDissecting symbiosis: developments in nod factor perception. Ann Bot 87 709–718 Occurrence Handle1:CAS:528:DC%2BD3MXjslChtbY%3D Occurrence Handle10.1006/anbo.2001.1410

    Article  CAS  Google Scholar 

  65. G Pearce D Strydom S Johnson CA Ryan (1991) ArticleTitleA polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science 253 895–898 Occurrence Handle1:CAS:528:DyaK3MXmt1ygu78%3D Occurrence Handle17751827 Occurrence Handle10.1126/science.253.5022.895

    Article  CAS  PubMed  Google Scholar 

  66. JB Reid IC Murfet (1975) ArticleTitleFlowering in Pisum: the sites and possible mechanisms of the vernalisation responses. J Exp Bot 26 860–867 Occurrence Handle10.1093/jxb/26.6.860

    Article  Google Scholar 

  67. F Rolland B Moore J Sheen (2002) ArticleTitleSugar sensing and signaling in plants. Plant Cell 14 IssueIDsuppl S185–S205 Occurrence Handle1:CAS:528:DC%2BD38XksV2hurY%3D Occurrence Handle12045277

    CAS  PubMed  Google Scholar 

  68. JJ Ross DP O’Neill DA Rathbone (2003) ArticleTitleAuxin-gibberellin interactions in pea: integrating the old with the new. J Plant Growth Regul 22 99–108 Occurrence Handle1:CAS:528:DC%2BD3sXosF2kur0%3D Occurrence Handle10.1007/s00344-003-0021-z

    Article  CAS  Google Scholar 

  69. R Ruiz-Medrano B Xoconostle-Cazares WJ Luca (1999) ArticleTitlePhloem long-distance transport of CmNACP mRNA: implications for supracellular regulation in plants. Development 126 4405–4419 Occurrence Handle1:CAS:528:DyaK1MXns1emsb4%3D Occurrence Handle10498677

    CAS  PubMed  Google Scholar 

  70. CA Ryan G Pearce J Scheer DS Moura (2002) ArticleTitlePolypeptide hormones. Plant Cell Suppl S251–S264

    Google Scholar 

  71. A Samach A Gover (2001) ArticleTitlePhotoperiodism: the consistent use of CONSTANS. Curr Biol. 11 IssueID16 R651–4 Occurrence Handle1:CAS:528:DC%2BD3MXmsFersr8%3D Occurrence Handle11525758 Occurrence Handle10.1016/S0960-9822(01)00384-0

    Article  CAS  PubMed  Google Scholar 

  72. T Schmülling (2002) ArticleTitleNew insights into the functions of cytokinins in plant development. J Plant Growth Reg 21 40–49 Occurrence Handle10.1007/s003440010046

    Article  Google Scholar 

  73. IR Searle AE Men TS Laniya DM Buzas I Iturbe-Ormaetxe BJ Carroll PM Gresshoff (2003) ArticleTitleLong distance signaling in nodulation directed by a CLAVATA1-like receptor kinase. Science 299 109–112 Occurrence Handle1:CAS:528:DC%2BD38XpvVensLo%3D Occurrence Handle12411574 Occurrence Handle10.1126/science.1077937

    Article  CAS  PubMed  Google Scholar 

  74. S Stracke C Kistner S Yoshida I Mulder S Sato T Kaneko S Tabata N Sandal J Stougaard K Szczyglowski M Parniske (2002) ArticleTitleA plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417 959–962 Occurrence Handle1:CAS:528:DC%2BD38XkvVagsbg%3D Occurrence Handle12087405 Occurrence Handle10.1038/nature00841

    Article  CAS  PubMed  Google Scholar 

  75. P Suarez-Lopez K Wheatley F Robson H Onouchi F Valverde G Coupland (2001) ArticleTitleCONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410 1116–1120 Occurrence Handle1:CAS:528:DC%2BD3MXjsVCrtrY%3D Occurrence Handle11323677 Occurrence Handle10.1038/35074138

    Article  CAS  PubMed  Google Scholar 

  76. A Trewavas (2002a) ArticleTitlePlant cell signal transduction: the emerging phenotype. Plant Cell 14 IssueIDsuppl S3–S4 Occurrence Handle1:CAS:528:DC%2BD38XksV2htbg%3D

    CAS  Google Scholar 

  77. A Trewavas (2002b) ArticleTitleMindless mastery. Nature 415 841 Occurrence Handle1:CAS:528:DC%2BD38Xhs1yitL0%3D Occurrence Handle10.1038/415841a

    Article  CAS  Google Scholar 

  78. AE Trotochaud S Jeong SE Clark (2000) ArticleTitleCLAVATA3, a multimeric ligand of the CLAVATA1 receptor-kinase. Science 289 613–617 Occurrence Handle1:CAS:528:DC%2BD3cXls1ersrw%3D Occurrence Handle10915623 Occurrence Handle10.1126/science.289.5479.613

    Article  CAS  PubMed  Google Scholar 

  79. CGN Turnbull JP Booker HMO Leyser (2002) ArticleTitleMicrografting techniques for testing long-distance signaling in Arabidopsis. Plant J 32 255–262 Occurrence Handle1:CAS:528:DC%2BD38XovFGqtrc%3D Occurrence Handle12383090 Occurrence Handle10.1046/j.1365-313X.2002.01419.x

    Article  CAS  PubMed  Google Scholar 

  80. H Vogler C Kuhlemeier (2003) ArticleTitleSimple hormones but complex signalling. Curr Opin Plant Biol 6 51–56 Occurrence Handle1:CAS:528:DC%2BD38XpsFegs7o%3D Occurrence Handle12495751 Occurrence Handle10.1016/S1369-5266(02)00013-4

    Article  CAS  PubMed  Google Scholar 

  81. JL Weller JB Reid SA Taylor IC Murfet (1997) ArticleTitleThe genetic control of flowering in pea. Trends Plant Sci 2 412–418 Occurrence Handle10.1016/S1360-1385(97)85580-X

    Article  Google Scholar 

  82. B Xonconostle-Cazares Y Xiang R Ruiz-Medrano H-L Wang B-C Yoo KC McFarland VR Franceschi WJ Lucas (1999) ArticleTitlePlant paralog to viral movement protein potentiates transport of mRNA into the phloem. Science 283 94–98 Occurrence Handle10.1126/science.283.5398.94

    Article  Google Scholar 

  83. M Yano Y Katayose M Ashikari U Yamanouchi L Monna T Fuse T Baba K Yamamoto Y Umehara Y Nagamura T Sasaki (2000) ArticleTitle Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 12 2473–2484 Occurrence Handle1:CAS:528:DC%2BD3MXns1SgsQ%3D%3D Occurrence Handle11148291 Occurrence Handle10.1105/tpc.12.12.2473

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Jim Weller for discussions on flowering, John Ross for comments on the manuscript, Jennifer Williams for editorial comment and the Australian Research Council for financial support.

Author information

Authors and Affiliations

  1. Australian Research Council Centre of Excellence For Integrative Legume Research and School of Life Sciences, The University of Queensland, St Lucia, QLD 4072, Australia

    Christine A. Beveridge & Peter M. Gresshoff

  2. Génétique et Amélioration des Plantes, INRA, rte de St Cyr, 78000 Versailles, France

    Catherine Rameau

  3. Department of Agricultural Sciences, Imperial College London, Wye Campus, Wye, Kent TN25 5AH, UK

    Colin G. N. Turnbull

Authors
  1. Christine A. Beveridge
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peter M. Gresshoff
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Catherine Rameau
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Colin G. N. Turnbull
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christine A. Beveridge.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Beveridge, C.A., Gresshoff, P.M., Rameau, C. et al. Additional Signalling Compounds are Required to Orchestrate Plant Development . J Plant Growth Regul 22, 15–24 (2003). https://doi.org/10.1007/s00344-003-0036-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-003-0036-5

Keywords

Search

Navigation