Planta

, Volume 238, Issue 5, pp 819–830 | Cite as

Role of hormones in controlling vascular differentiation and the mechanism of lateral root initiation

Review

Abstract

The vascular system in plants is induced and controlled by streams of inductive hormonal signals. Auxin produced in young leaves is the primary controlling signal in vascular differentiation. Its polar and non-polar transport pathways and major controlling mechanisms are clarified. Ethylene produced in differentiating protoxylem vessels is the signal that triggers lateral root initiation, while tumor-induced ethylene is a limiting and controlling factor of crown gall development and its vascular differentiation. Gibberellin produced in mature leaves moves non-polarly and promotes elongation, regulates cambium activity and induces long fibers. Cytokinin from the root cap moves upward to promote cambial activity and stimulate shoot growth and branching, while strigolactone from the root inhibits branching. Furthermore, the role of the hormonal signals in controlling the type of differentiating vascular elements and gradients of conduit size and density, and how they regulate plant adaptation and have shaped wood evolution are elucidated.

Keywords

Auxin-transport pathways Ethylene signaling Lateral root initiation Mobile gibberellin signal Cambium activity Vessel diameter Xylem adaptation 

Abbreviations

CK

Cytokinin

GA

Gibberellin

IAA

Indole-3-acetic acid

LRi

Lateral root initiation

SL

Strigolactone

TE

Tracheary elements

References

  1. Agusti J, Herold S, Schwarz M, Sanchez P, Ljung K, Dun EA, Brewer PB, Beveridge CA, Sieberer T, Sehr EM, Greb T (2011) Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. Proc Natl Acad Sci USA 108:20242–20247PubMedCrossRefGoogle Scholar
  2. Aloni R (1979) Role of auxin and gibberellin in differentiation of primary phloem fibers. Plant Physiol 63:609–614PubMedCrossRefGoogle Scholar
  3. Aloni R (1980) Role of auxin and sucrose in the differentiation of sieve and tracheary elements in plant tissue cultures. Planta 150:255–263CrossRefGoogle Scholar
  4. Aloni R (1987) Differentiation of vascular tissues. Annu Rev Plant Physiol 38:179–204CrossRefGoogle Scholar
  5. Aloni R (2001) Foliar and axial aspects of vascular differentiation: hypotheses and evidence. J Plant Growth Regul 20:22–34CrossRefGoogle Scholar
  6. Aloni R (2010) The induction of vascular tissues by auxin. In: Davies PJ (ed) Plant hormones: biosynthesis, signal transduction, action!. Kluwer Academic Publishers, Dordrecht, pp 485–506Google Scholar
  7. Aloni R (2013) The role of hormones in controlling vascular differentiation. In: Fromm J (ed) Cellular aspects of wood formation. Springer, Berlin, pp 99–139CrossRefGoogle Scholar
  8. Aloni R, Sachs T (1973) The three-dimensional structure of primary phloem systems. Planta 113:343–353CrossRefGoogle Scholar
  9. Aloni R, Ullrich CI (2007) Biology of crown gall tumors. In: Tzfira T, Citovsky V (eds) Agrobacterium. Springer, Berlin, pp 525–549Google Scholar
  10. Aloni R, Zimmermann MH (1983) The control of vessel size and density along the plant axis: a new hypothesis. Differentiation 24:203–208CrossRefGoogle Scholar
  11. Aloni R, Tollier T, Monties B (1990) The role of auxin and gibberellin in controlling lignin formation in primary phloem fibers and in xylem of Coleus blumei stems. Plant Physiol 94:1743–1747PubMedCrossRefGoogle Scholar
  12. Aloni R, Pradel KS, Ullrich CI (1995) The three-dimensional structure of vascular tissues in Agrobacterium tumefaciens-induced crown galls and in the host stem of Ricinus communis L. Planta 196:597–605CrossRefGoogle Scholar
  13. Aloni R, Wolf A, Feigenbaum P, Avni A, Klee HJ (1998) The Never ripe mutant provides evidence that tumor-induced ethylene controls the morphogenesis of Agrobacterium tumefaciens-induced crown galls on tomato stems. Plant Physiol 117:841–847PubMedCrossRefGoogle Scholar
  14. Aloni R, Schwalm K, Langhans M, Ullrich CI (2003) Gradual shifts in sites of free-auxin production during leaf-primordium development and their role in vascular differentiation and leaf morphogenesis in Arabidopsis. Planta 216:841–853PubMedGoogle Scholar
  15. Aloni R, Langhans M, Aloni E, Dreieicher E, Ullrich CI (2005) Root-synthesized cytokinin in Arabidopsis is distributed in the shoot by the transpiration stream. J Exp Bot 56:1535–1544PubMedCrossRefGoogle Scholar
  16. Aloni R, Aloni E, Langhans M, Ullrich CI (2006) Role of cytokinin and auxin in shaping root architecture: regulating vascular differentiation, lateral root initiation, root apical dominance and root gravitropism. Ann Bot 97:883–893PubMedCrossRefGoogle Scholar
  17. Anfodillo T, Deslauriers A, Menardi R, Tedoldi L, Petit G, Rossi S (2012) Widening of xylem conduits in a conifer tree depends on the longer time of cell expansion downwards along the stem. J Exp Bot 63:837–845PubMedCrossRefGoogle Scholar
  18. Barbez E, Kubeš M, Rolčík J, Béziat C, Pěnčík A, Wang B, Rosquete MR, Zhu J, Dobrev PI, Lee Y, Zažímalovà E, Petrášek J, Geisler M, Friml J, Kleine-Vehn J (2012) A novel putative auxin carrier family regulates intracellular auxin homeostasis in plants. Nature 485:119–122PubMedCrossRefGoogle Scholar
  19. Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602PubMedCrossRefGoogle Scholar
  20. Berleth T, Mattsson J, Hardtke CS (2000) Vascular continuity and auxin signals. Trends Plant Sci 5:387–393PubMedCrossRefGoogle Scholar
  21. Biemelt S, Tschiersch H, Sonnewald U (2004) Impact of altered gibberellin metabolism on biomass accumulation, lignin biosynthesis, and photosynthesis in transgenic tobacco plants. Plant Physiol 135:254–265PubMedCrossRefGoogle Scholar
  22. Bollhöner B, Prestele J, Tuominen H (2012) Xylem cell death: emerging understanding of regulation and function. J Exp Bot 63:1081–1094PubMedCrossRefGoogle Scholar
  23. Booker J, Chatfield S, Leyser O (2003) Auxin acts in xylem-associated or medullary cells to mediate apical dominance. Plant Cell 15:495–507PubMedCrossRefGoogle Scholar
  24. Caño-Delgado A, Lee JY, Demura T (2010) Regulatory mechanisms for specification and patterning of plant vascular tissues. Annu Rev Cell Dev Biol 26:605–637PubMedCrossRefGoogle Scholar
  25. Capron A, Chang XF, Hall H, Ellis B, Beatson RP, Berleth T (2013) Identification of quantitative trait loci controlling fibre length and lignin content in Arabidopsis thaliana stems. J Exp Bot 64:185–197PubMedCrossRefGoogle Scholar
  26. Dayan J, Schwarzkopf M, Avni A, Aloni R (2010) Enhancing plant growth and fiber production by silencing GA 2-oxidase. Plant Biotechnol J 8:425–435PubMedCrossRefGoogle Scholar
  27. Dayan J, Voronin N, Gong F, Sun TP, Hedden P, Fromm H, Aloni R (2012) Leaf-induced gibberellin signaling is essential for internode elongation, cambial activity, and fiber differentiation in tobacco stems. Plant Cell 24:66–79PubMedCrossRefGoogle Scholar
  28. De Smet I (2012) Lateral root initiation: one step at a time. New Phytol 193:867–873PubMedCrossRefGoogle Scholar
  29. Deslauriers A, Giovannelli A, Rossi S, Castro G, Fragnelli G, Traversi L (2009) Intra-annual cambial activity and carbon availability in stem of poplar. Tree Physiol 29:1223–1235PubMedCrossRefGoogle Scholar
  30. Dubrovsky JG, Doerner PW, Colon-Carmona A, Rost TL (2000) Pericycle cell proliferation and lateral root initiation in Arabidopsis. Plant Physiol 124:1648–1657PubMedCrossRefGoogle Scholar
  31. Dubrovsky JG, Napsucialy-Mendivil S, Duclercq J, Cheng Y, Shishkova S, Ivanchenko MG, Friml J, Murphy AS, Benková E (2011) Auxin minimum defines a developmental window for lateral root initiation. New Phytol 191:970–983PubMedCrossRefGoogle Scholar
  32. Eriksson ME, Moritz T (2002) Day length and special expression of gibberellin 20-oxidase isolated from hybrid aspen (Populus termulata x P. termuloides Michx.). Planta 214:920–930PubMedCrossRefGoogle Scholar
  33. Eriksson ME, Israelsson M, Olsson O, Moritz T (2000) Increased gibberellin biosynthesis in transgenic trees promotes growth, biomass production and xylem fiber length. Nat Biotechnol 18:784–788PubMedCrossRefGoogle Scholar
  34. Evert RF (2006) Esau’s plant anatomy, meristems, cells, and tissues of the plant body: their structure, function, and development. Wiley, HobokenCrossRefGoogle Scholar
  35. Friml J, Plame K (2002) Polar auxin transport: old questions and new concepts? Plant Mol Biol 49:273–284PubMedCrossRefGoogle Scholar
  36. Geldner N, Anders N, Wolters H, Keicher J, Kornberger W, Muller P, Delbarre A, Ueda T, Nakano A, Jürgens G (2003) The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112:219–230PubMedCrossRefGoogle Scholar
  37. Goldsmith MHM, Catealdo DA, Karn J, Brenneman T, Trip P (1974) The nonpolar transport of auxin in the phloem of intact Coleus plants. Planta 116:301–317CrossRefGoogle Scholar
  38. Hagen G, Martin G, Li Y, Guilfoyle TJ (1991) Auxin-induced expression of the soybean GH3 promoter in transgenic tobacco plants. Plant Mol Biol 17:567–579PubMedCrossRefGoogle Scholar
  39. Hess T, Sachs T (1972) The influence of a mature leaf on xylem differentiation. New Phytol 71:903–914CrossRefGoogle Scholar
  40. Hirota A, Kato T, Fukaki H, Aida M, Tasaka M (2007) The auxin-regulated AP2/EREBP gene PUCHI is required for morphogenesis in the early lateral root primordium of Arabidopsis. Plant Cell 19:2156–2168PubMedCrossRefGoogle Scholar
  41. Ivanchenko MG, Muday GK, Dubrovsky JG (2008) Ethylene–auxin interactions regulate lateral root initiation and emergence in Arabidopsis thaliana. Plant J 55:335–347PubMedCrossRefGoogle Scholar
  42. Jacobs WP (1952) The role of auxin in differentiation of xylem around a wound. Am J Bot 39:301–309CrossRefGoogle Scholar
  43. Kalev N, Aloni R (1998) Role of auxin and gibberellin in regenerative differentiation of tracheids in Pinus pinea L. seedlings. New Phytol 138:461–468CrossRefGoogle Scholar
  44. Kleine-Vehn J, Wabnik K, Martinière A, Łangowski Ł, Willig K, Naramoto S, Leitner J, Tanaka H, Jakobs S, Robert S, Luschnig C, Govaerts W, Hell SW, Runions J, Friml J (2011) Recycling, clustering, and endocytosis jointly maintain PIN auxin carrier polarity at the plasma membrane. Mol Syst Biol 7:540PubMedCrossRefGoogle Scholar
  45. Kohlen W, Charnikhova T, Liu Q, Bours R, Domagalska MA, Beguerie S, Verstappen F, Leyser O, Bouwmeester H, Ruyter-Spira C (2011) Strigolactones are transported through the xylem and play a key role in shoot architectural response to phosphate deficiency in nonarbuscular mycorrhizal host Arabidopsis. Plant Physiol 155:974–987PubMedCrossRefGoogle Scholar
  46. Kudo T, Kiba T, Sakakibara H (2010) Metabolism and long-distance translocation of cytokinins. J Integr Plant Biol 52:53–60PubMedCrossRefGoogle Scholar
  47. Larkin PJ, Gibson JM, Mathesius U, Weinmann JJ, Gärtner E, Hall E, Tanner GJ, Rolfe BG, Djordjevic MA (1996) Transgenic white clover. Studies with the auxin-responsive promoter, GH3, in root gravitropism and lateral root development. Transgenic Res 5:325–335PubMedCrossRefGoogle Scholar
  48. Leitch MA (2001) Vessel-element dimensions and frequency within the most current growth increment along the length of Eucalyptus globules stems. Trees 15:353–357CrossRefGoogle Scholar
  49. Lilley JL, Gee CW, Sairanen I, Ljung K, Nemhauser JL (2012) An endogenous carbon-sensing pathway triggers increased auxin flux and hypocotyl elongation. Plant Physiol 160:2261–2270PubMedCrossRefGoogle Scholar
  50. Lucas WJ, Groover A, Lichtenberger R, Furuta K, Yadav SR, Helariutta Y, He XQ, Fukuda H, Kang J, Brady SM, Patrick JW, Sperry J, Yoshida A, López-Millán AF, Grusak MA, Kachroo P (2013) The plant vascular system: evolution, development and functions. J Integr Plant Biol 55:294–388PubMedCrossRefGoogle Scholar
  51. Marhavý P, Vanstraelen M, De Rybel B, Zhaojun D, Bennett MJ, Beeckman T, Benková E (2013) Auxin reflux between the endodermis and pericycle promotes lateral root initiation. EMBO J 32:149–158PubMedCrossRefGoogle Scholar
  52. Mattsson J, Sung ZR, Berleth T (1999) Responses of plant vascular systems to auxin transport inhibition. Development 126:2979–2991PubMedGoogle Scholar
  53. Milhinhos A, Miguel CM (2013) Hormone interactions in xylem development: a matter of signals. Plant Cell Rep 32:867–883PubMedCrossRefGoogle Scholar
  54. Miyashima S, Sebastian J, Lee JY, Helariutta Y (2013) Stem cell function during plant vascular development. EMBO J 32:178–193PubMedCrossRefGoogle Scholar
  55. Morris DA, Kadir GO, Barry AJ (1973) Auxin transport in intact pea seedlings (Pisum sativum L.): the inhibition of transport by 2,3,5-triiodobenzoic acid. Planta 110:173–182CrossRefGoogle Scholar
  56. Muraro D, Byrne H, King J, Bennett M (2013) The role of auxin and cytokinin signalling in specifying the root architecture of Arabidopsis thaliana. J Theor Biol 317:71–86PubMedCrossRefGoogle Scholar
  57. Negi S, Ivanchenko MG, Muday GK (2008) Ethylene regulates lateral root formation and auxin transport in Arabidopsis thaliana. Plant J 55:175–187PubMedCrossRefGoogle Scholar
  58. Oda Y, Fukuda H (2012) Secondary cell wall patterning during xylem differentiation. Curr Opin Plant Biol 15:38–44PubMedCrossRefGoogle Scholar
  59. Olson ME, Rosell JA (2013) Vessel diameter–stem diameter scaling across woody angiosperms and the ecological causes of xylem vessel diameter variation. New Phytol 197:1204–1213PubMedCrossRefGoogle Scholar
  60. Pesquet E, Tuominen H (2011) Ethylene stimulates tracheary element differentiation in Zinnia elegans cell cultures. New Phytol 190:138–149PubMedCrossRefGoogle Scholar
  61. Pesquet E, Zhang B, Gorzsás A, Puhakainen T, Serk H, Escamez S, Barbier O, Gerber L, Courtois-Moreau C, Alatalo E, Paulin L, Kangasjärvi J, Sundberg B, Goffner D, Tuominen H (2013) Non-cell-autonomous postmortem lignification of tracheary elements in Zinnia elegans. Plant Cell 25:1314–1328PubMedCrossRefGoogle Scholar
  62. Ragni L, Nieminen K, Pacheco-Villalobos D, Sibout R, Schwechheimer C, Hardtke CS (2011) Mobile gibberellin directly stimulates Arabidopsis hypocotyl xylem expansion. Plant Cell 23:1322–1336PubMedCrossRefGoogle Scholar
  63. Rathgeber CB, Rossi S, Bontemps JD (2011) Cambial activity related to tree size in a mature silver-fir plantation. Ann Bot 108:429–438PubMedCrossRefGoogle Scholar
  64. Raven PH, Evert RF, Eichhorn SE (2005) Biology of plants, 7th edn. Freeman, New YorkGoogle Scholar
  65. Ruffel S, Krouk G, Ristova D, Shasha D, Birnbaum KD, Coruzzi GM (2011) Nitrogen economics of root foraging: transitive closure of the nitrate–cytokinin relay and distinct systemic signaling for N supply vs. demand. Proc Natl Acad Sci USA 108:18524–18529PubMedCrossRefGoogle Scholar
  66. Sachs T (1981) The control of patterned differentiation of vascular tissues. Adv Bot Res 9:151–262CrossRefGoogle Scholar
  67. Sachs T (1991) Callus and tumor development. In: Sachs T (ed) Pattern formation in plant tissues. Cambridge University Press, Cambridge, pp 38–55CrossRefGoogle Scholar
  68. Sairanen I, Novák O, Pěnčík A, Ikeda Y, Jones B, Sandberg G, Ljung K (2012) Soluble carbohydrates regulate auxin biosynthesis via PIF proteins in Arabidopsis. Plant Cell 24:4907–4916PubMedCrossRefGoogle Scholar
  69. Sauer M, Balla J, Luschnig C, Wisniewska J, Reinöhl V, Friml J, Benková E (2006) Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity. Genes Dev 20:2902–2911PubMedCrossRefGoogle Scholar
  70. Sawchuk MG, Edgar A, Scarpella E (2013) Patterning of leaf vein networks by convergent auxin transport pathways. PLoS Genet 9(2):e1003294PubMedCrossRefGoogle Scholar
  71. Scarpella E, Helariutta Y (2010) Vascular pattern formation in plants. Curr Top Dev Biol 91:221–265PubMedCrossRefGoogle Scholar
  72. Scarpella E, Marcos D, Friml J, Berleth T (2006) Control of leaf vascular patterning by polar auxin transport. Genes Dev 20:1015–1027PubMedCrossRefGoogle Scholar
  73. Schwalm K, Aloni R, Langhans M, Heller W, Stich S, Ullrich CI (2003) Flavonoid-related regulation of auxin accumulation in Agrobacterium tumefaciens-induced plant tumors. Planta 218:163–178PubMedCrossRefGoogle Scholar
  74. Shinohara N, Taylor C, Leyser O (2013) Strigolactone can promote or inhibit shoot branching by triggering rapid depletion of the auxin efflux protein PIN1 from the plasma membrane. PLoS Biol 11(1):e1001474PubMedCrossRefGoogle Scholar
  75. Sorce C, Giovannelli A, Sebastiani L, Anfodillo T (2013) Hormonal signals involved in the regulation of cambial activity, xylogenesis and vessel patterning in trees. Plant Cell Rep 32:885–898PubMedCrossRefGoogle Scholar
  76. Takei K, Ueda N, Aoki K, Kuromori T, Hirayama T, Shinozaki K, Yamaya T, Sakakibara H (2004) AtIPT3 is a key determinant of nitrate-dependent cytokinin biosynthesis in Arabidopsis. Plant Cell Physiol 45:1053–1062PubMedCrossRefGoogle Scholar
  77. Teale WD, Paponov IA, Palme K (2006) Auxin in action: signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 7:847–859PubMedCrossRefGoogle Scholar
  78. Tokunaga N, Uchimura N, Sato Y (2006) Involvement of gibberellin in tracheary element differentiation and lignification in Zinnia elegans xylogenic culture. Protoplasma 228:179–187PubMedCrossRefGoogle Scholar
  79. Trewavas AJ (1983) Is plant development regulated by changes in concentration of growth substances or by changes in the sensitivity to growth substances? TIBS 8:354–357Google Scholar
  80. Tsuchisaka A, Theologis A (2004) Unique and overlapping expression patterns among the Arabidopsis 1-amino-cyclopropane-1-carboxylate synthase gene family members. Plant Physiol 136:2982–3000PubMedCrossRefGoogle Scholar
  81. Tyree MT, Zimmermann MH (2002) Xylem structure and the ascent of sap, 2nd edn. Springer, BerlinCrossRefGoogle Scholar
  82. Uggla C, Moritz T, Sandberg G, Sundberg B (1996) Auxin as a positional signal in pattern formation in plants. Proc Nat Acad Sci USA 93:9282–9286PubMedCrossRefGoogle Scholar
  83. Ullrich CI, Aloni R (2000) Vascularization is a general requirement for growth of plant and animal tumours. J Exp Bot 51:1951–1960PubMedCrossRefGoogle Scholar
  84. Wächter R, Fischer K, Gäbler R, Kühnemann F, Urban W, Bögemann GM, Voesenek LACJ, Blom CWPM, Ullrich CI (1999) Ethylene production and ACC-accumulation in Agrobacterium tumefaciens-induced plant tumours and their impact on tumour and host stem structure and function. Plant Cell Environ 22:1263–1273CrossRefGoogle Scholar
  85. Yamamoto F, Kozlowski TT (1987) Effect of ethrel on growth and stem anatomy of Pinus halepensis seedlings. IAWA Bull NS 8:11–19Google Scholar

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© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Department of Molecular Biology and Ecology of PlantsTel Aviv UniversityTel AvivIsrael

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