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Protoplasma

, Volume 247, Issue 3–4, pp 145–161 | Cite as

The vascular cambium: molecular control of cellular structure

  • Juan Pablo Matte Risopatron
  • Yuqiang Sun
  • Brian Joseph Jones
Review Article

Abstract

Indeterminate growth and the production of new organs in plants require a constant supply of new cells. The majority of these cells are produced in mitotic regions called meristems. For primary or tip growth of the roots and shoots, the meristems are located in the apices. These apical meristems have been shown to function as developmentally regulated and environmentally responsive stem cell niches. The principle requirements to maintain a functioning meristem in a dynamic system are a balance of cell division and differentiation and the regulation of the planes of cell division and expansion. Woody plants also have secondary indeterminate mitotic regions towards the exterior of roots, stems and branches that produce the cells for continued growth in girth. The chief secondary meristem is the vascular cambium (VC). As its name implies, cells produced in the VC contribute to the growth in girth via the production of secondary vascular elements. Although we know a considerable amount about the cellular and molecular basis of the apical meristems, our knowledge of the cellular basis and molecular functioning of the VC has been rudimentary. This is now changing as a growing body of research shows that the primary and secondary meristems share some common fundamental regulatory mechanisms. In this review, we outline recent research that is leading to a better understanding of the molecular forces that shape the cellular structure and function of the VC.

Keywords

Vascular cambium Secondary growth Stem cell WOX CLE Class III HD-Zip KANADI 

Notes

Acknowledgements

This work was supported in part by a Ph.D. scholarship for Matte J.P. by Advanced Human Capital Program of the National Commission for Scientific and Technological Research (CONICYT) Bicentennial Becas-Chile Scholarship and the Swedish Research Council FORMAS centre of excellence program, FUNCFIBER. Thanks to Göran Sandberg for the opportunity and inspiration.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

709_2010_211_Fig6_ESM.gif (17 kb)
Supplemental Fig. 1

Sampling position for global gene expression profiling data in Table 1 (Sjödin et al. 2009). A1, B4, phloem; A2, phloem cambial transition; A3, B6, A4, B7, cambial zone; A5, cambial zone xylem transition zone; and B8, xylem (Schrader et al. 2004). (GIF 17 kb)

709_2010_211_MOESM1_ESM.eps (493 kb)
High resolution image file (EPS 493 kb)
709_2010_211_MOESM2_ESM.doc (1.9 mb)
Supplemental Table 1 Candidate genes for vascular cambium structure and function. The gene list was derived from various sources (Chaffey et al. 2002; Baima et al. 2001; Zhao et al. 2000, 2005; Nieminen et al. 2004; Groover 2005; Baucher et al. 2007; Demura and Fukuda 2007; Helariutta and Bhalerao 2003; Ariel et al. 2007; and others). Annotation data was obtained from NCBI. Populus trichocarpa (Pop. Ort.) and orthology data was obtained from KEGG (Kanehisa and Goto 2000), UniProt (NCBI-GeneID) and JGI. (GIF 17 kb) (DOC 1898 kb)

References

  1. Aggarwal P, Yadav RK, Reddy GV (2010) Identification of novel markers for stem-cell niche of Arabidopsis shoot apex. Gene Expr Patterns 10(6):259–264PubMedGoogle Scholar
  2. Altamura MM, Possenti M, Matteucci A, Baima S, Ruberti I, Morelli G (2001) Development of the vascular system in the inflorescence stem of Arabidopsis. New Phytol 151(2):381–389Google Scholar
  3. Ariel FD, Manavella PA, Dezar CA, Chan RL (2007) The true story of the hd-zip family. Trends Plant Sci 12(9):419–426. doi: 10.1016/j.tplants.2007.08.003 PubMedGoogle Scholar
  4. Avery GS, Burkholder PR, Creighton HB (1937) Production and distribution of growth hormone in shoots of aesculus and malus, and its probable role in stimulating cambial activity. Am J Bot 24(1):51–58Google Scholar
  5. Baima S, Nobili F, Sessa G, Lucchetti S, Ruberti I, Morelli G (1995) The expression of the athb-8 homeobox gene is restricted to provascular cells in Arabidopsis thaliana. Development 121(12):4171–4182PubMedGoogle Scholar
  6. Baima S, Possenti M, Matteucci A, Wisman E, Altamura MM, Ruberti I, Morelli G (2001) The Arabidopsis athb-8 hd-zip protein acts as a differentiation-promoting transcription factor of the vascular meristems. Plant Physiol 126(2):643–655PubMedGoogle Scholar
  7. Barton MK (2010) Twenty years on: the inner workings of the shoot apical meristem, a developmental dynamo. Dev Biol 341(1):95–113. doi: 10.1016/j.ydbio.2009.11.029 PubMedGoogle Scholar
  8. Baucher M, El Jaziri M, Vandeputte O (2007) From primary to secondary growth: origin and development of the vascular system. J Exp Bot 58(13):3485–3501PubMedGoogle Scholar
  9. Birnbaum K, Jung JW, Wang JY, Lambert GM, Hirst JA, Galbraith DW, Benfey PN (2005) Cell type-specific expression profiting in plants via cell sorting of protoplasts from fluorescent reporter lines. Nat Meth 2(8):615–619Google Scholar
  10. Borghi L, Bureau M, Simon R (2007) Arabidopsis jagged lateral organs is expressed in boundaries and coordinates knox and pin activity. Plant Cell 19(6):1795–1808. doi: 10.1105/tpc.106.047159 PubMedGoogle Scholar
  11. Brand U, Fletcher JC, Hobe M, Meyerowitz EM, Simon R (2000) Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by clv3 activity. Science 289(5479):617–619. doi: 8704 PubMedGoogle Scholar
  12. Busch W, Miotk A, Ariel FD, Zhao Z, Forner J, Daum G, Suzaki T, Schuster C, Schultheiss SJ, Leibfried A, Haubeiss S, Ha N, Chan RL, Lohmann JU (2010) Transcriptional control of a plant stem cell niche. Dev Cell 18(5):849–861. doi: 10.1016/j.devce1.2010.03.012 PubMedGoogle Scholar
  13. Busse JS, Evert RF (1999) Pattern of differentiation of the first vascular elements in the embryo and seedling of Arabidopsis thaliana. Int J Plant Sci 160(1):1–13Google Scholar
  14. Carlsbecker A, Lee JY, Roberts CJ, Dettmer J, Lehesranta S, Zhou J, Lindgren O, Moreno-Risueno MA, Vaten A, Thitamadee S, Campilho A, Sebastian J, Bowman JL, Helariutta Y, Benfey PN (2010) Cell signalling by microrna165/6 directs gene dose-dependent root cell fate. Nature 465(7296):316–321. doi: 10.1038/nature08977 PubMedGoogle Scholar
  15. Chaffey N, Cholewa E, Regan S, Sundberg B (2002) Secondary xylem development in Arabidopsis: a model for wood formation. Physiol Plant 114(4):594–600PubMedGoogle Scholar
  16. Chaudhuri O, Parekh SH, Lam WA, Fletcher DA (2009) Combined atomic force microscopy and side-view optical imaging for mechanical studies of cells. Nat Methods 6(5):383–387. doi: 10.1038/nmeth.1320 PubMedGoogle Scholar
  17. Clark SE, Running MP, Meyerowitz EM (1993) Clavata1, a regulator of meristem and flower development in Arabidopsis. Development 119(2):397–418PubMedGoogle Scholar
  18. 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(4):575–585PubMedGoogle Scholar
  19. Costa S, Shaw P (2006) Chromatin organization and cell fate switch respond to positional information in Arabidopsis. Nature 439(7075):493–496. doi: 10.1038/nature04269 PubMedGoogle Scholar
  20. Davis JD, Evert RF (1968) Seasonal development of secondary phloem in Populus tremuloides. Bot Gaz 129(1):1Google Scholar
  21. Demura T, Fukuda H (2007) Transcriptional regulation in wood formation. Trends Plant Sci 12(2):64–70. doi: 10.1016/j.tplants.2006.12.006 PubMedGoogle Scholar
  22. 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(10):1223–1235. doi: 10.1093/treephys/tpp061 PubMedGoogle Scholar
  23. De Smet I, Vassileva V, De Rybel B, Levesque MP, Grunewald W, Van Damme D, Van Noorden G, Naudts M, Van Isterdael G, De Clercq R, Wang JY, Meuli N, Vanneste S, Friml J, Hilson P, Jurgens G, Ingram GC, Inze D, Benfey PN, Beeckman T (2008) Receptor-like kinase acr4 restricts formative cell divisions in the Arabidopsis root. Science 322(5901):594–597. doi: 10.1126/science.1160158 PubMedGoogle Scholar
  24. Digby J, Wareing PF (1966) Effect of applied growth hormones on cambial division and differentiation of cambial derivatives. Ann Bot 30(119):539Google Scholar
  25. Dolan L, Roberts K (1995) Secondary thickening in roots of Arabidopsis thaliana anatomy and cell-surface changes. New Phytol 131(1):121–128Google Scholar
  26. Dolan L, Janmaat K, Willemsen V, Linstead P, Poethig S, Roberts K, Scheres B (1993) Cellular organisation of the Arabidopsis thaliana root. Development 119(1):71–84PubMedGoogle Scholar
  27. Donner TJ, Sherr I, Scarpella E (2009) Regulation of preprocambial cell state acquisition by auxin signaling in Arabidopsis leaves. Development 136(19):3235–3246. doi: 10.1242/dev.037028 PubMedGoogle Scholar
  28. Donner TJ, Sherr I, Scarpella E (2010) Auxin signal transduction in Arabidopsis vein formation. Plant Signal Behav 5(1):70–72PubMedGoogle Scholar
  29. Emery JF, Floyd SK, Alvarez J, Eshed Y, Hawker NP, Izhaki A, Baum SF, Bowman JL (2003) Radial patterning of Arabidopsis shoots by class iii hd-zip and kanadi genes. Curr Biol 13(20):1768–1774. doi: S0960982203007188 PubMedGoogle Scholar
  30. Esau K (1943) Origin and development of primary vascular tissues in seed plants. Bot Rev 9(3):125–206Google Scholar
  31. Eshed Y, Baum SF, Perea JV, Bowman JL (2001) Establishment of polarity in lateral organs of plants. Curr Biol 11(16):1251–1260. doi: S0960-9822(01)00392-X PubMedGoogle Scholar
  32. Eshed Y, Izhaki A, Baum SF, Floyd SK, Bowman JL (2004) Asymmetric leaf development and blade expansion in Arabidopsis are mediated by kanadi and yabby activities. Development 131(12):2997–3006. doi: 10.1242/dev.01186 PubMedGoogle Scholar
  33. Etchells JP, Turner SR (2010) The pxy-cle41 receptor ligand pair defines a multifunctional pathway that controls the rate and orientation of vascular cell division. Development 137(5):767–774. doi: 10.1242/dev.044941 PubMedGoogle Scholar
  34. Fahn A, Waisel Y, Benjamin L (1968) Cambial activity in Acacia raddiana Savi. Ann Bot 32(127):677Google Scholar
  35. Feraru E, Friml J (2008) Pin polar targeting. Plant Physiol 147(4):1553–1559. doi: 10.1104/pp.108.121756 PubMedGoogle Scholar
  36. Fisher K, Turner S (2007) Pxy, a receptor-like kinase essential for maintaining polarity during plant vascular-tissue development. Curr Biol 17(12):1061–1066. doi: 10.1016/j.cub.2007.05.049 PubMedGoogle Scholar
  37. Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM (1999) Signaling of cell fate decisions by clavata3 in Arabidopsis shoot meristems. Science 283(5409):1911–1914PubMedGoogle Scholar
  38. Fuchs M, van Bel AJE, Ehlers K (2010) Season-associated modifications in symplasmic organization of the cambium in Populus nigra. Ann Bot 105(3):375–387. doi: 10.1093/aob/mcp300 PubMedGoogle Scholar
  39. Galweiler L, Guan C, Muller A, Wisman E, Mendgen K, Yephremov A, Palme K (1998) Regulation of polar auxin transport by atpin1 in Arabidopsis vascular tissue. Science 282(5397):2226–2230PubMedGoogle Scholar
  40. Geier F, Lohmann JU, Gerstung M, Maier AT, Timmer J, Fleck C (2008) A quantitative and dynamic model for plant stem cell regulation. PLoS ONE 3(10):e3553. doi: 10.1371/journal.pone.0003553 PubMedGoogle Scholar
  41. Gendreau E, Traas J, Desnos T, Grandjean O, Caboche M, Hofte H (1997) Cellular basis of hypocotyl growth in Arabidopsis thaliana. Plant Physiol 114(1):295–305. doi: 114/1/295 PubMedGoogle Scholar
  42. Ghouse AKM, Hashmi S (1979) Cambium periodicity in Polyalthia longifolia. Phytomorphology 29(1):64–67Google Scholar
  43. Gonzali S, Novi G, Loreti E, Paolicchi F, Poggi A, Alpi A, Perata P (2005) A turanose-insensitive mutant suggests a role for wox5 in auxin homeostasis in Arabidopsis thaliana. Plant J 44(4):633–645. doi: 10.1111/j.1365-313X.2005.02555.x PubMedGoogle Scholar
  44. Grandjean O, Vernoux T, Laufs P, Belcram K, Mizukami Y, Traas J (2004) In vivo analysis of cell division, cell growth, and differentiation at the shoot apical meristem in Arabidopsis. Plant Cell 16(1):74–87. doi: 10.1105/tpc.017962 PubMedGoogle Scholar
  45. Grieneisen VA, Xu J, Maree AFM, Hogeweg P, Scheres B (2007) Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature 449:1008–1013. doi: 10.1038/nature06215 PubMedGoogle Scholar
  46. Groover AT (2005) What genes make a tree a tree? Trends Plant Sci 10(5):210–214PubMedGoogle Scholar
  47. Grunewald W, Friml J (2010) The march of the pins: developmental plasticity by dynamic polar targeting in plant cells. EMBO J 29(16):2700–2714PubMedGoogle Scholar
  48. Ha CM, Jun JH, Fletcher JC (2010) Shoot apical meristem form and function. Curr Top Dev Biol 91:103–140. doi: S0070-2153(10)91004-1 PubMedGoogle Scholar
  49. Haecker A, Gross-Hardt R, Geiges B, Sarkar A, Breuninger H, Herrmann M, Laux T (2004) Expression dynamics of wox genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development 131(3):657–668. doi: 10.1242/dev.0096310.1016/S0070-2153(10)91004-1 PubMedGoogle Scholar
  50. Hauser MT, Morikami A, Benfey PN (1995) Conditional root expansion mutants of Arabidopsis. Development 121(4):1237–1252PubMedGoogle Scholar
  51. Heisler MG, Ohno C, Das P, Sieber P, Reddy GV, Long JA, Meyerowitz EM (2005) Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr Biol 15(21):1899–1911. doi: 10.1016/j.cub.2005.09.052 PubMedGoogle Scholar
  52. Helariutta Y, Bhalerao R (2003) Between xylem and phloem: the genetic control of cambial activity in plants. Plant Biol 5(5):465–472Google Scholar
  53. Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Jung J, Sena G, Hauser MT, Benfey PN (2000) The short-root gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101(5):555–567. doi: S0092-8674(00)80865-X PubMedGoogle Scholar
  54. 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(39):15208–15213. doi: 10.1073/pnas.0808444105 PubMedGoogle Scholar
  55. Hirakawa Y, Kondo Y, Fukuda H (2010a) Regulation of vascular development by cle peptide-receptor systems. J Integr Plant Biol 52(1):8–16. doi: 10.1111/j.1744-7909.2010.00904.x PubMedGoogle Scholar
  56. Hirakawa Y, Kondo Y, Fukuda H (2010b) Tdif peptide signaling regulates vascular stem cell proliferation via the wox4 homeobox gene in Arabidopsis. Plant Cell. doi: 10.1105/tpc.110.076083 PubMedGoogle Scholar
  57. Hohm T, Zitzler E, Simon R (2010) A dynamic model for stem cell homeostasis and patterning in Arabidopsis meristems. PLoS ONE 5(2):e9189. doi: 10.1371/journal.pone.0009189 PubMedGoogle Scholar
  58. Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, Widmayer P, Gruissem W, Zimmermann P (2008) Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Adv Bioinformatics 2008:420747PubMedGoogle Scholar
  59. Ikeda M, Mitsuda N, Ohme-Takagi M (2009) Arabidopsis wuschel is a bifunctional transcription factor that acts as a repressor in stem cell regulation and as an activator in floral patterning. Plant Cell 21(11):3493–3505. doi: 10.1105/tpc.109.069997 PubMedGoogle Scholar
  60. Ilegems M, Douet V, Meylan-Bettex M, Uyttewaal M, Brand L, Bowman JL, Stieger PA (2010) Interplay of auxin, kanadi and class iii hd-zip transcription factors in vascular tissue formation. Development 137(6):975–984. doi: 10.1242/dev.047662 PubMedGoogle Scholar
  61. Iqbal M (1990) The vascular cambium. Research studies in botany and related applied fields, vol 7. Research Studies Press Ltd, TauntonGoogle Scholar
  62. 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(5788):842–845. doi: 10.1126/science.1128436 PubMedGoogle Scholar
  63. Izhaki A, Bowman JL (2007) Kanadi and class iii hd-zip gene families regulate embryo patterning and modulate auxin flow during embryogenesis in Arabidopsis. Plant Cell 19(2):495–508. doi: 10.1105/tpc.106.047472 PubMedGoogle Scholar
  64. Jaillais Y, Chory J (2010) Unraveling the paradoxes of plant hormone signaling integration. Nat Struct Mol Biol 17(6):642–645PubMedGoogle Scholar
  65. Ji J, Strable J, Shimizu R, Koenig D, Sinha N, Scanlon MJ (2010) Wox4 promotes procambial development. Plant Physiol 152(3):1346–1356. doi: 10.1104/pp.109.149641 PubMedGoogle Scholar
  66. Kado CI (1976) Tumor-inducing substance of Agrobacterium tumefaciens. Annu Rev Phytopathol 14:265–308Google Scholar
  67. Kanehisa M, Goto S (2000) Kegg: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28(1):27–30PubMedGoogle Scholar
  68. Kang J, Dengler N (2004) Vein pattern development in adult leaves of Arabidopsis thaliana. Int J Plant Sci 165(2):231–242Google Scholar
  69. Kayes JM, Clark SE (1998) Clavata2, a regulator of meristem and organ development in Arabidopsis. Development 125(19):3843–3851PubMedGoogle Scholar
  70. Kerstetter RA, Bollman K, Taylor RA, Bomblies K, Poethig RS (2001) Kanadi regulates organ polarity in Arabidopsis. Nature 411(6838):706–709. doi: 10.1038/35079629 PubMedGoogle Scholar
  71. Ko JH, Han KH (2004) Arabidopsis whole-transcriptome profiling defines the features of coordinated regulations that occur during secondary growth. Plant Mol Biol 55(3):433–453. doi: 10.1007/s11103-004-1051-z PubMedGoogle Scholar
  72. Ko JH, Prassinos C, Han KH (2006) Developmental and seasonal expression of ptahb1, a Populus gene encoding a class iiihd-zip protein, is closely associated with secondary growth and inversely correlated with the level of microrna (mir166). New Phytol 169(3):469–478. doi: 10.1111/j.1469-8137.2005.01623.x PubMedGoogle Scholar
  73. Kramer EM (2004) Pin and aux/lax proteins: their role in auxin accumulation. Trends Plant Sci 9(12):578–582. doi: 10.1016/j.tplants.2004.10.010 PubMedGoogle Scholar
  74. Larson PR (1994) The vascular cambium: development and structure, Springer series in wood science. Springer, BerlinGoogle Scholar
  75. Lehesranta SJ, Lichtenberger R, Helariutta Y (2009) Cell-to-cell communication in vascular morphogenesis. Curr Opin Plant Biol. doi: 10.1016/j.pbi.2009.09.004 PubMedGoogle Scholar
  76. Lev-Yadun S (1994) Induction of sclereid differentiation in the pith of Arabidopsis thaliana (L.) Heynh. J Exp Bot 45(281):1845–1849Google Scholar
  77. Lev-Yadun S, Wyatt SE, Flaishman MA (2004) The inflorescence stem fibers of Arabidopsis thaliana revoluta (ifl1) mutant. J Plant Growth Regul 23(4):301–306Google Scholar
  78. Li LG, Lu SF, Chiang V (2006) A genomic and molecular view of wood formation. Crit Rev Plant Sci 25(3):215–233. doi: 10.1080/07352680600611519 Google Scholar
  79. Li W-F, Cui K-M, He X-Q (2009) Regulation of cell cycle regulators by environmental signals during growth-dormancy cycle of trees. Plant Signal Behav 4(10):959–961PubMedGoogle Scholar
  80. Liphschitz N, Levyadun S, Waisel Y (1981) The annual rhythm of activity of the lateral meristems (cambium and phellogen) in Cupressus sempervirens L. Ann Bot 47(4):485–496Google Scholar
  81. Liu Z, Duguay J, Ma F, Wang TW, Tshin R, Hopkins MT, McNamara L, Thompson JE (2008) Modulation of eif5a1 expression alters xylem abundance in Arabidopsis thaliana. J Exp Bot 59(4):939–950. doi: 10.1093/jxb/ern017 PubMedGoogle Scholar
  82. Mattsson J, Ckurshumova W, Berleth T (2003) Auxin signaling in Arabidopsis leaf vascular development. Plant Physiol 131(3):1327–1339. doi: 10.1104/pp.013623 PubMedGoogle Scholar
  83. Maughan SC, Murray JA, Bogre L (2006) A greenprint for growth: signalling the pattern of proliferation. Curr Opin Plant Biol 9(5):490–495. doi: 10.1016/j.pbi.2006.07.010 PubMedGoogle Scholar
  84. Mayer KF, Schoof H, Haecker A, Lenhard M, Jurgens G, Laux T (1998) Role of wuschel in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95(6):805–815. doi: S0092-8674(00)81703-1 PubMedGoogle Scholar
  85. McHale NA, Koning RE (2004) Microrna-directed cleavage of nicoltiana sylvestris phavoluta mRNA regulates the vascular cambium and structure of apical meristems. Plant Cell 16(7):1730–1740. doi: 10.1105/tpc.021816 PubMedGoogle Scholar
  86. Mizukami Y, Fischer RL (2000) Plant organ size control: aintegumenta regulates growth and cell numbers during organogenesis. Proc Natl Acad Sci USA 97(2):942–947PubMedGoogle Scholar
  87. Moller B, Weijers D (2009) Auxin control of embryo patterning. Cold Spring Harb Perspect Biol 1(5). doi: 10.1101/cshperspect.a001545
  88. Moubayidin L, Perilli S, Dello Ioio R, Di Mambro R, Costantino P, Sabatini S (2010) The rate of cell differentiation controls the Arabidopsis root meristem growth phase. Curr Biol 20(12):1138–1143. doi: 10.1016/j.cub.2010.05.035 PubMedGoogle Scholar
  89. Nieminen KM, Kauppinen L, Helariutta Y (2004) A weed for wood? Arabidopsis as a genetic model for xylem development. Plant Physiol 135(2):653–659PubMedGoogle Scholar
  90. Nilsson J, Karlberg A, Antti H, Lopez-Vernaza M, Mellerowicz E, Perrot-Rechenmann C, Sandberg G, Bhalerao RP (2008) Dissecting the molecular basis of the regulation of wood formation by auxin in hybrid aspen. Plant Cell 20(4):843–855. doi: 10.1105/tpc.107.055798 PubMedGoogle Scholar
  91. Oelkers K, Goffard N, Weiller GF, Gresshoff PM, Mathesius U, Frickey T (2008) Bioinformatic analysis of the cle signaling peptide family. BMC Plant Biol 8:1. doi: 10.1186/1471-2229-8-1 PubMedGoogle Scholar
  92. Ogawa M, Shinohara H, Sakagami Y, Matsubayashi Y (2008) Arabidopsis clv3 peptide directly binds clv1 ectodomain. Science 319(5861):294. doi: 10.1126/science.1150083 PubMedGoogle Scholar
  93. Oh S, Park S, Han KH (2003) Transcriptional regulation of secondary growth in Arabidopsis thaliana. J Exp Bot 54(393):2709–2722. doi: 10.1093/jxb/erg304 PubMedGoogle Scholar
  94. Ohashi-Ito K, Kubo M, Demura T, Fukuda H (2005) Class iii homeodomain leucine-zipper proteins regulate xylem cell differentiation. Plant Cell Physiol 46(10):1646–1656. doi: 10.1093/pcp/pci180 PubMedGoogle Scholar
  95. Ohyama K, Shinohara H, Ogawa-Ohnishi M, Matsubayashi Y (2009) A glycopeptide regulating stem cell fate in Arabidopsis thaliana. Nat Chem Biol 5(8):578–580. doi: 10.1038/nchembio.182 PubMedGoogle Scholar
  96. Pesquet E, Korolev AV, Calder G, Lloyd CW (2010) The microtubule-associated protein AtMAP70-5 regulates secondary wall patterning in Arabidopsis wood cells. Curr Biol 20(8):744–749Google Scholar
  97. Petersson SV, Johansson AI, Kowalczyk M, Makoveychuk A, Wang JY, Moritz T, Grebe M, Benfey PN, Sandberg G, Ljung K (2009) An auxin gradient and maximum in the Arabidopsis root apex shown by high-resolution cell-specific analysis of iaa distribution and synthesis. Plant Cell 21(6):1659–1668. doi: 10.1105/tpc.109.066480 PubMedGoogle Scholar
  98. Petrasek J, Friml J (2009) Auxin transport routes in plant development. Development 136(16):2675–2688. doi: 10.1242/dev.030353 PubMedGoogle Scholar
  99. Petrasek J, Mravec J, Bouchard R, Blakeslee JJ, Abas M, Seifertova D, Wisniewska J, Tadele Z, Kubes M, Covanova M, Dhonukshe P, Skupa P, Benkova E, Perry L, Krecek P, Lee OR, Fink GR, Geisler M, Murphy AS, Luschnig C, Zazimalova E, Friml J (2006) Pin proteins perform a rate-limiting function in cellular auxin efflux. Science 312(5775):914–918. doi: 10.1126/science.1123542 PubMedGoogle Scholar
  100. Pineau C, Freydier A, Ranocha P, Jauneau A, Turner S, Lemonnier G, Renou JP, Tarkowski P, Sandberg G, Jouanin L, Sundberg B, Boudet AM, Goffner D, Pichon M (2005) Hca: an Arabidopsis mutant exhibiting unusual cambial activity and altered vascular patterning. Plant J 44(2):271–289. doi: 10.1111/j.1365-313X.2005.02526.x PubMedGoogle Scholar
  101. Plomion C, Leprovost G, Stokes A (2001) Wood formation in trees. Plant Physiol 127(4):1513–1523PubMedGoogle Scholar
  102. Prigge MJ, Otsuga D, Alonso JM, Ecker JR, Drews GN, Clark SE (2005) Class iii homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell 17(1):61–76. doi: 10.1105/tpc.104.026161 PubMedGoogle Scholar
  103. Reinders-Gouwentak CA (1965) Physiology of the cambium and other secondary meristems of the shoot, vol 15 (i), Encyclopedia of plant physiology. Springer, BerlinGoogle Scholar
  104. Reinhardt D, Mandel T, Kuhlemeier C (2000) Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell 12(4):507–518PubMedGoogle Scholar
  105. Sachs T (1981) The control of the patterned differentiation of vascular tissues. Adv Bot Res Incorp Adv Plant Pathol 9:151–262Google Scholar
  106. Sachs T (1991) Cell polarity and tissue patterning in plants. Development: 83–93Google Scholar
  107. Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T, Nakajima K, Scheres B, Heidstra R, Laux T (2007) Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446(7137):811–814. doi: 10.1038/nature05703 PubMedGoogle Scholar
  108. Savidge RA (1988) Auxin and ethylene regulation of diameter growth in trees. Tree Physiol 4(4):401–414PubMedGoogle Scholar
  109. Savidge RA (2001) Intrinsic regulation of cambial growth. J Plant Growth Regul 20(1):52–77Google Scholar
  110. Sawchuk MG, Head P, Donner TJ, Scarpella E (2007) Time-lapse imaging of Arabidopsis leaf development shows dynamic patterns of procambium formation. New Phytol 176:560–571. doi: 10.1111/j.1469-8137.2007.02193.x PubMedGoogle Scholar
  111. Scarpella E, Francis P, Berleth T (2004) Stage-specific markers define early steps of procambium development in Arabidopsis leaves and correlate termination of vein formation with mesophyll differentiation. Development 131(14):3445–3455. doi: 10.1242/dev.01182 PubMedGoogle Scholar
  112. Scarpella E, Marcos D, Friml J, Berleth T (2006) Control of leaf vascular patterning by polar auxin transport. Genes Dev 20(8):1015–1027. doi: 10.1101/gaf.1402406 PubMedGoogle Scholar
  113. Scheres B (2007) Stem-cell niches: nursery rhymes across kingdoms. Nat Rev Mol Cell Biol 8(5):345–354. doi: 10.1038/nrm2164 PubMedGoogle Scholar
  114. Schoof H, Lenhard M, Haecker A, Mayer KFX, Jurgens G, Laux T (2000) The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the clavata and wuschel genes. Cell 100(6):635–644PubMedGoogle Scholar
  115. Schrader J, Nilsson J, Mellerowicz E, Berglund A, Nilsson P, Hertzberg M, Sandberg G (2004) A high-resolution transcript profile across the wood-forming meristem of poplar identifies potential regulators of cambial stem cell identity. Plant Cell 16(9):2278–2292. doi: 10.1105/tpc.104.024190 PubMedGoogle Scholar
  116. Sessa G, Steindler C, Morelli G, Ruberti I (1998) The Arabidopsis athb-8, -9 and -14 genes are members of a small gene family coding for highly related hd-zip proteins. Plant Mol Biol 38(4):609–622PubMedGoogle Scholar
  117. Sibout R, Plantegenet S, Hardtke CS (2008) Flowering as a condition for xylem expansion in Arabidopsis hypocotyl and root. Curr Biol 18(6):458–463PubMedGoogle Scholar
  118. Sjödin A, Street NR, Sandberg G, Gustafsson P, Jansson S (2009) The Populus genome integrative explorer (popgenie): a new resource for exploring the Populus genome. New Phytol 182(4):1013–1025. doi: 10.1111/j.1469-8137.2009.02807.x Google Scholar
  119. Stahl Y, Wink RH, Ingram GC, Simon R (2009) A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr Biol 19(11):909–914. doi: 10.1016/j.cub.2009.03.060 PubMedGoogle Scholar
  120. Strabala TJ, O'Donnell PJ, Smit AM, 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(4):1331–1344. doi: 10.1104/pp.105.075515 PubMedGoogle Scholar
  121. Sundberg B, Uggla C, Tuominen H (2000) Cambial growth and auxin gradients. In: Savidge R, Barnett J, Napier R (eds) Cell and molecular biology of wood formation. BIOS Scientific Publishers, Oxford, p 169Google Scholar
  122. Talbert PB, Adler HT, Parks DW, Comai L (1995) The revoluta gene is necessary for apical meristem development and for limiting cell divisions in the leaves and stems of Arabidopsis thaliana. Development 121(9):2723–2735PubMedGoogle Scholar
  123. Tax FE, Durbak A (2006) Meristems in the movies: live imaging as a tool for decoding intercellular signaling in shoot apical meristems. Plant Cell 18:1331–1337PubMedGoogle Scholar
  124. Tuominen H, Puech L, Fink S, Sundberg B (1997) A radial concentration gradient of indole-3-acetic acid is related to secondary xylem development in hybrid aspen. Plant Physiol 115(2):577–585PubMedGoogle Scholar
  125. Uggla C, Moritz T, Sandberg G, Sundberg B (1996) Auxin as a positional signal in pattern formation in plants. Proc Natl Acad Sci USA 93(17):9282–9286PubMedGoogle Scholar
  126. Uggla C, Mellerowicz EJ, Sundberg B (1998) Indole-3-acetic acid controls cambial growth in scots pine by positional signaling. Plant Physiol 117(1):113–121PubMedGoogle Scholar
  127. Uyttewaal M, Traas J, Hamant O (2010) Integrating physical stress, growth, and development. Curr Opin Plant Biol 13(1):46–52. doi: 10.1016/j.pbi.2009.10.004 PubMedGoogle Scholar
  128. Vanbel AJE (1990) Xylem-phloem exchange via the rays—the undervalued route of transport. J Exp Bot 41(227):631–644Google Scholar
  129. van den Berg C, Willemsen V, Hendriks G, Weisbeek P, Scheres B (1997) Short-range control of cell differentiation in the Arabidopsis root meristem. Nature 390(6657):287–289PubMedGoogle Scholar
  130. Vernoux T, Kronenberger J, Grandjean O, Laufs P, Traas J (2000) Pin-formed 1 regulates cell fate at the periphery of the shoot apical meristem. Development 127(23):5157–5165PubMedGoogle Scholar
  131. Vernoux T, Besnard F, Traas J (2010) Auxin at the shoot apical meristem. Cold Spring Harb Perspect Biol 2(4). doi: 10.1101/cshperspect.a001487
  132. Waisel Y, Liphschi N, Fahn A (1970) Cambial activity in Zygophyllum dumosum Boiss. Ann Bot 34(135):409Google Scholar
  133. Wang G, Fiers M (2010) Cle peptide signaling during plant development. Protoplasma 240(1–4):33–43. doi: 10.1007/s00709-009-0095-y PubMedGoogle Scholar
  134. Wenzel CL, Schuetz M, Yu Q, Mattsson J (2007) Dynamics of monopteros and pin-formed1 expression during leaf vein pattern formation in Arabidopsis thaliana. Plant J 49(3):387–398. doi: 10.1111/j.1365-313X.2006.02977.x PubMedGoogle Scholar
  135. Werner T, Schmulling T (2009) Cytokinin action in plant development. Curr Opin Plant Biol 12(5):527–538. doi: 10.1016/j.pbi.2009.07.002 PubMedGoogle Scholar
  136. Whitford R, Fernandez A, De Groodt R, Ortega E, Hilson P (2008) Plant cle peptides from two distinct functional classes synergistically induce division of vascular cells. Proc Natl Acad Sci USA 105(47):18625–18630. doi: 10.1073/pnas.0809395105 PubMedGoogle Scholar
  137. Williams L, Fletcher JC (2005) Stem cell regulation in the Arabidopsis shoot apical meristem. Curr Opin Plant Biol 8(6):582–586. doi: 10.1016/j.pbi.2005.09.010 PubMedGoogle Scholar
  138. Xia Q, Steeves TA (1999) Initial differentiation of vascular tissue in the shoot apex of carrot (Daucus carota L.). Ann Bot 83(2):157–166Google Scholar
  139. Yao X, Wang H, Li H, Yuan Z, Li F, Yang L, Huang H (2009) Two types of cis-acting elements control the abaxial epidermis-specific transcription of the mir165a and mir166a genes. FEBS Lett 583(22):3711–3717. doi: 10.1016/j.febslet.2009.10.076 PubMedGoogle Scholar
  140. Zhao C, Johnson BJ, Kositsup B, Beers EP (2000) Exploiting secondary growth in Arabidopsis. Construction of xylem and bark cDNA libraries and cloning of three xylem endopeptidases. Plant Physiol 123(3):1185–1196PubMedGoogle Scholar
  141. Zhao C, Craig JC, Petzold HE, Dickerman AW, Beers EP (2005) The xylem and phloem transcriptomes from secondary tissues of the Arabidopsis root-hypocotyl. Plant Physiol 138(2):803–818PubMedGoogle Scholar
  142. Zhao CS, Avci U, Grant EH, Haigler CH, Beers EP (2008) Xnd1, a member of the nac domain family in Arabidopsis thaliana, negatively regulates lignocellulose synthesis and programmed cell death in xylem. Plant J 53(3):425–436. doi: 10.1111/j.1365-313X.2007.03350.x PubMedGoogle Scholar
  143. Zhao Z, Andersen SU, Ljung K, Dolezal K, Miotk A, Schultheiss SJ, Lohmann JU (2010) Hormonal control of the shoot stem-cell niche. Nature 465(7301):1089–1092. doi: 10.1038/nature09126 PubMedGoogle Scholar
  144. Zhong RQ, Ye ZH (1999) Ifl1, a gene regulating interfascicular fiber differentiation in Arabidopsis, encodes a homeodomain-leucine zipper protein. Plant Cell 11(11):2139–2152PubMedGoogle Scholar
  145. Zhong RQ, Ye ZH (2001) Alteration of auxin polar transport in the Arabidopsis ifl1 mutants. Plant Physiol 126(2):549–563PubMedGoogle Scholar
  146. Zhong RQ, Ye ZH (2004) Amphivasal vascular bundle 1, a gain-of-function mutation of the ifl1/rev gene, is associated with alterations in the polarity of leaves, stems and carpels. Plant Cell Physiol 45(4):369–385PubMedGoogle Scholar
  147. Zhong RQ, Taylor JJ, Ye ZH (1997) Disruption of interfascicular fiber differentiation in an Arabidopsis mutant. Plant Cell 9(12):2159–2170. doi: 10.1105/tpc.9.12.2159 PubMedGoogle Scholar
  148. Zhou GK, Kubo M, Zhong R, Demura T, Ye ZH (2007) Overexpression of mir165 affects apical meristem formation, organ polarity establishment and vascular development in Arabidopsis. Plant Cell Physiol 48(3):391–404. doi: 10.1093/pcp/pcm008 PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Juan Pablo Matte Risopatron
    • 1
  • Yuqiang Sun
    • 2
    • 3
  • Brian Joseph Jones
    • 1
    • 2
  1. 1.FAFNRUniversity of SydneySydneyAustralia
  2. 2.Umeå Plant Science Centre, Department of Plant PhysiologyUmeå UniversitetUmeåSweden
  3. 3.Hangzhou Normal UniversityCollege of Life and Environmental UniversityHangzhouChina

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