iBet uBet web content aggregator. Adding the entire web to your favor.
iBet uBet web content aggregator. Adding the entire web to your favor.



Link to original content: https://doi.org/10.1007/s00709-010-0211-z
The vascular cambium: molecular control of cellular structure | Protoplasma Skip to main content
Log in

The vascular cambium: molecular control of cellular structure

  • Review Article
  • Published:
Protoplasma Aims and scope Submit manuscript

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.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aggarwal P, Yadav RK, Reddy GV (2010) Identification of novel markers for stem-cell niche of Arabidopsis shoot apex. Gene Expr Patterns 10(6):259–264

    CAS  PubMed  Google Scholar 

  • 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):381–389

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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):51–58

    CAS  Google Scholar 

  • 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):4171–4182

    CAS  PubMed  Google Scholar 

  • 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):643–655

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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):3485–3501

    CAS  PubMed  Google Scholar 

  • 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):615–619

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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):1–13

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Chaffey N, Cholewa E, Regan S, Sundberg B (2002) Secondary xylem development in Arabidopsis: a model for wood formation. Physiol Plant 114(4):594–600

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Clark SE, Running MP, Meyerowitz EM (1993) Clavata1, a regulator of meristem and flower development in Arabidopsis. Development 119(2):397–418

    CAS  PubMed  Google Scholar 

  • 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):575–585

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Davis JD, Evert RF (1968) Seasonal development of secondary phloem in Populus tremuloides. Bot Gaz 129(1):1

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Digby J, Wareing PF (1966) Effect of applied growth hormones on cambial division and differentiation of cambial derivatives. Ann Bot 30(119):539

    CAS  Google Scholar 

  • Dolan L, Roberts K (1995) Secondary thickening in roots of Arabidopsis thaliana anatomy and cell-surface changes. New Phytol 131(1):121–128

    Google Scholar 

  • 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):71–84

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Donner TJ, Sherr I, Scarpella E (2010) Auxin signal transduction in Arabidopsis vein formation. Plant Signal Behav 5(1):70–72

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Esau K (1943) Origin and development of primary vascular tissues in seed plants. Bot Rev 9(3):125–206

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Fahn A, Waisel Y, Benjamin L (1968) Cambial activity in Acacia raddiana Savi. Ann Bot 32(127):677

    Google Scholar 

  • Feraru E, Friml J (2008) Pin polar targeting. Plant Physiol 147(4):1553–1559. doi:10.1104/pp.108.121756

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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):1911–1914

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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):2226–2230

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Ghouse AKM, Hashmi S (1979) Cambium periodicity in Polyalthia longifolia. Phytomorphology 29(1):64–67

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Groover AT (2005) What genes make a tree a tree? Trends Plant Sci 10(5):210–214

    CAS  PubMed  Google Scholar 

  • Grunewald W, Friml J (2010) The march of the pins: developmental plasticity by dynamic polar targeting in plant cells. EMBO J 29(16):2700–2714

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Hauser MT, Morikami A, Benfey PN (1995) Conditional root expansion mutants of Arabidopsis. Development 121(4):1237–1252

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Helariutta Y, Bhalerao R (2003) Between xylem and phloem: the genetic control of cambial activity in plants. Plant Biol 5(5):465–472

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Hirakawa Y, Shinohara H, Kondo Y, Inoue A, Nakanomyo I, Ogawa M, Sawa S, Ohashi-Ito K, Matsubayashi Y, Fukuda H (2008) Non-cell-autonomous control of vascular stem cell fate by a cle peptide/receptor system. Proc Natl Acad Sci USA 105(39):15208–15213. doi:10.1073/pnas.0808444105

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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 2008:420747

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Iqbal M (1990) The vascular cambium. Research studies in botany and related applied fields, vol 7. Research Studies Press Ltd, Taunton

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Jaillais Y, Chory J (2010) Unraveling the paradoxes of plant hormone signaling integration. Nat Struct Mol Biol 17(6):642–645

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Kado CI (1976) Tumor-inducing substance of Agrobacterium tumefaciens. Annu Rev Phytopathol 14:265–308

    CAS  Google Scholar 

  • Kanehisa M, Goto S (2000) Kegg: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28(1):27–30

    CAS  PubMed  Google Scholar 

  • Kang J, Dengler N (2004) Vein pattern development in adult leaves of Arabidopsis thaliana. Int J Plant Sci 165(2):231–242

    Google Scholar 

  • Kayes JM, Clark SE (1998) Clavata2, a regulator of meristem and organ development in Arabidopsis. Development 125(19):3843–3851

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Larson PR (1994) The vascular cambium: development and structure, Springer series in wood science. Springer, Berlin

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Lev-Yadun S (1994) Induction of sclereid differentiation in the pith of Arabidopsis thaliana (L.) Heynh. J Exp Bot 45(281):1845–1849

    CAS  Google Scholar 

  • Lev-Yadun S, Wyatt SE, Flaishman MA (2004) The inflorescence stem fibers of Arabidopsis thaliana revoluta (ifl1) mutant. J Plant Growth Regul 23(4):301–306

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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):959–961

    CAS  PubMed  Google Scholar 

  • 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):485–496

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Mizukami Y, Fischer RL (2000) Plant organ size control: aintegumenta regulates growth and cell numbers during organogenesis. Proc Natl Acad Sci USA 97(2):942–947

    CAS  PubMed  Google Scholar 

  • Moller B, Weijers D (2009) Auxin control of embryo patterning. Cold Spring Harb Perspect Biol 1(5). doi:10.1101/cshperspect.a001545

  • 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

    CAS  PubMed  Google Scholar 

  • Nieminen KM, Kauppinen L, Helariutta Y (2004) A weed for wood? Arabidopsis as a genetic model for xylem development. Plant Physiol 135(2):653–659

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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):744–749

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Petrasek J, Friml J (2009) Auxin transport routes in plant development. Development 136(16):2675–2688. doi:10.1242/dev.030353

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Plomion C, Leprovost G, Stokes A (2001) Wood formation in trees. Plant Physiol 127(4):1513–1523

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Reinders-Gouwentak CA (1965) Physiology of the cambium and other secondary meristems of the shoot, vol 15 (i), Encyclopedia of plant physiology. Springer, Berlin

    Google Scholar 

  • Reinhardt D, Mandel T, Kuhlemeier C (2000) Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell 12(4):507–518

    CAS  PubMed  Google Scholar 

  • Sachs T (1981) The control of the patterned differentiation of vascular tissues. Adv Bot Res Incorp Adv Plant Pathol 9:151–262

    Google Scholar 

  • Sachs T (1991) Cell polarity and tissue patterning in plants. Development: 83–93

  • 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

    CAS  PubMed  Google Scholar 

  • Savidge RA (1988) Auxin and ethylene regulation of diameter growth in trees. Tree Physiol 4(4):401–414

    CAS  PubMed  Google Scholar 

  • Savidge RA (2001) Intrinsic regulation of cambial growth. J Plant Growth Regul 20(1):52–77

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Scheres B (2007) Stem-cell niches: nursery rhymes across kingdoms. Nat Rev Mol Cell Biol 8(5):345–354. doi:10.1038/nrm2164

    CAS  PubMed  Google Scholar 

  • 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):635–644

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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):609–622

    CAS  PubMed  Google Scholar 

  • Sibout R, Plantegenet S, Hardtke CS (2008) Flowering as a condition for xylem expansion in Arabidopsis hypocotyl and root. Curr Biol 18(6):458–463

    CAS  PubMed  Google Scholar 

  • 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 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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 169

    Google Scholar 

  • 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):2723–2735

    CAS  PubMed  Google Scholar 

  • Tax FE, Durbak A (2006) Meristems in the movies: live imaging as a tool for decoding intercellular signaling in shoot apical meristems. Plant Cell 18:1331–1337

    CAS  PubMed  Google Scholar 

  • 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):577–585

    CAS  PubMed  Google Scholar 

  • 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):9282–9286

    CAS  PubMed  Google Scholar 

  • Uggla C, Mellerowicz EJ, Sundberg B (1998) Indole-3-acetic acid controls cambial growth in scots pine by positional signaling. Plant Physiol 117(1):113–121

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Vanbel AJE (1990) Xylem-phloem exchange via the rays—the undervalued route of transport. J Exp Bot 41(227):631–644

    Google Scholar 

  • 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):287–289

    PubMed  Google Scholar 

  • 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):5157–5165

    CAS  PubMed  Google Scholar 

  • 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

  • Waisel Y, Liphschi N, Fahn A (1970) Cambial activity in Zygophyllum dumosum Boiss. Ann Bot 34(135):409

    Google Scholar 

  • Wang G, Fiers M (2010) Cle peptide signaling during plant development. Protoplasma 240(1–4):33–43. doi:10.1007/s00709-009-0095-y

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Xia Q, Steeves TA (1999) Initial differentiation of vascular tissue in the shoot apex of carrot (Daucus carota L.). Ann Bot 83(2):157–166

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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):1185–1196

    CAS  PubMed  Google Scholar 

  • 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):803–818

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Zhong RQ, Ye ZH (1999) Ifl1, a gene regulating interfascicular fiber differentiation in Arabidopsis, encodes a homeodomain-leucine zipper protein. Plant Cell 11(11):2139–2152

    CAS  PubMed  Google Scholar 

  • Zhong RQ, Ye ZH (2001) Alteration of auxin polar transport in the Arabidopsis ifl1 mutants. Plant Physiol 126(2):549–563

    CAS  PubMed  Google Scholar 

  • 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):369–385

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Brian Joseph Jones.

Additional information

Handling Editor: David Robinson

Electronic supplementary materials

Below is the link to the electronic supplementary material.

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)

High resolution image file (EPS 493 kb)

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)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Matte Risopatron, J.P., Sun, Y. & Jones, B.J. The vascular cambium: molecular control of cellular structure. Protoplasma 247, 145–161 (2010). https://doi.org/10.1007/s00709-010-0211-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-010-0211-z

Keywords

Navigation