Plant vascular meristems are sets of pluripotent cells that enable radial growth by giving rise to vascular tissues and are therefore crucial to plant development. However, the overall dynamics of cellular determination and patterning in and around vascular meristems is still unexplored. We study this process in the shoot vascular tissue of Arabidopsis thaliana, which is organized in vascular bundles that contain three basic cell types (procambium, xylem and phloem). A set of molecules involved in this process has now been identified and partially characterized, but it is not yet clear how the regulatory interactions among them, in conjunction with cellular communication processes, give rise to the steady patterns that accompany cell-fate determination and arrangement within vascular bundles. We put forward a dynamic model factoring in the interactions between molecules (genes, peptides, mRNA and hormones) that have been reported to be central in this process, as well as the relevant communication mechanisms. When a few proposed interactions (unverified, but based on related data) are postulated, the model reproduces the hormonal and molecular patterns expected for the three regions within vascular bundles. In order to test the model, we simulated mutant and hormone-depleted systems and compared the results with experimentally reported phenotypes. The proposed model provides a formal framework integrating a set of growing experimental data and renders a dynamic account of how the collective action of hormones, genes, and other molecules may result in the specification of the three main cell types within shoot vascular bundles. It also offers a tool to test the necessity and sufficiency of particular interactions and conditions for vascular patterning and yields novel predictions that may be experimentally tested. Finally, this model provides a reference for further studies comparing the overall dynamics of tissue organization and formation by meristems in other plant organs and species.

Functional Genomics and Proteomics of Plants Central European Institute of Technology Masaryk University Brno Czech Republic

Zobrazit více v PubMed

Azpeitia E, Benítez M, Vega I, Villarreal C, Alvarez-Buylla ER (2010) Single-cell and coupled GRN models of cell patterning in the Arabidopsis thaliana root stem cell niche. BMC Syst Biol 4: 134. PubMed PMC

Fujita H, Toyokura K, Okada K, Kawaguchi M (2011) Reaction-diffusion pattern in shoot apical meristem of plants. PloS One 6: e18243. PubMed PMC

Vernoux T, Brunoud G, Farcot E, Morin V, Van den Daele H, et al. (2011) The auxin signalling network translates dynamic input into robust patterning at the shoot apex. Mol Syst Biol 7: 508. PubMed PMC

Turner S, Sieburth LE (2003) Vascular patterning. In: The Arabidopsis Book. American Society of Plant Biologists 2: e0073. PubMed PMC

Esau K (1977) Anatomy Of Seed Plants. John Wiley & Sons. 576 p.

Altamura MM, Possenti M, Matteucci A, Baima S, Ruberti I, et al. (2001) Development of the vascular system in the inflorescence stem of Arabidopsis . New Phytol 151: 381–389.

Lehesranta SJ, Lichtenberger R, Helariutta Y (2010) Cell-to-cell communication in vascular morphogenesis. Curr Op Plant Biol 13: 59–65. PubMed

Fukuda H (2004) Signals that control plant vascular cell differentiation. Nat Rev Mol Cell Biol 5: 379–391. PubMed

Elo A, Immanen J, Nieminen K, Helariutta Y (2009) Stem cell function during plant vascular development.Semin Cell Dev Biol. 20: 1097–1106. PubMed

Caño-Delgado A, Lee JY, Demura T (2010) Regulatory mechanisms for specification and patterning of plant vascular tissues. Ann Rev Cell Dev Biol 26: 605–637. PubMed

Ibañes M, Fàbregas N, Chory J, Caño-Delgado AI (2009) Brassinosteroid signaling and auxin transport are required to establish the periodic pattern of Arabidopsis shoot vascular bundles. Proc Nat Acad Sci USA 106: 13630–13635. PubMed PMC

De Smet I, Tetsumura T, De Rybel B, Frey NFD, Laplaze L, et al. (2007) Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis. Development 134: 681–690. PubMed

Bishopp A, Help H, El-Showk S, Weijers D, Scheres B, et al. (2011) A mutually inhibitory interaction between auxin and cytokinin specifies vascular pattern in roots. Curr Biol 21: 917–926. PubMed

Matsumoto-Kitano M, Kusumoto T, Tarkowski P, Kinoshita-Tsujimura K, Václavíková K, et al. (2008) Cytokinins are central regulators of cambial activity. Proc Nat Acad Sci USA 105: 20027–20031. PubMed PMC

Hejátko J, Ryu H, Kim GT, Dobesová R, Choi S, et al. (2009) The histidine kinases CYTOKININ-INDEPENDENT1 and ARABIDOPSIS HISTIDINE KINASE2 and 3 regulate vascular tissue development in Arabidopsis shoots. Plant Cell 21: 2008–2021. PubMed PMC

Bishopp A, Lehesranta S, Vatén A, Help H, El-Showk S, et al. (2011) Phloem-transported cytokinin regulates polar auxin transport and maintains vascular pattern in the root meristem. Curr Biol 21: 927–932. PubMed

Mahönen AP, Bishopp A, Higuchi M, Nieminen KM, Kinoshita K, et al. (2006) Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development. Science 311: 94–98. PubMed

Hwang I, Sheen J, Müller B (2012) Cytokinin signaling networks. Ann Rev Plant Biol 63: 353–380. PubMed

Baima S, Nobili F, Sessa G, Lucchetti S, Ruberti I, et al. (1995) The expression of the Athb-8 homeobox gene is restricted to provascular cells in Arabidopsis thaliana. Development 121: 4171–4182. PubMed

Baima S, Possenti M, Matteucci A, Wisman E, Altamura MM, et al. (2001) The Arabidopsis ATHB-8 HD-zip protein acts as a differentiation-promoting transcription factor of the vascular meristems. Plant Physiol 126: 643–655. PubMed PMC

Kubo M, Udagawa M, Nishikubo N, Horiguchi G, Yamaguchi M, et al. (2005) Transcription switches for protoxylem and metaxylem vessel formation. Genes Dev 19: 1855–1860. PubMed PMC

Yamaguchi M, Kubo M, Fukuda H, Demura T (2008) Vascular-related NAC-DOMAIN7 is involved in the differentiation of all types of xylem vessels in Arabidopsis roots and shoots. Plant J 55: 652–664. PubMed

Bonke M, Thitamadee S, Mähönen AP, Hauser M, Helariutta Y (2003) APL regulates vascular tissue identity in Arabidopsis. Nature 426: 181–186. PubMed

Ji J, Shimizu R, Sinha N, Scanlon MJ (2010) Analyses of WOX4 transgenics provide further evidence for the evolution of the WOX gene family during the regulation of diverse stem cell functions. Plant Signal Behav 5: 916–920. PubMed PMC

Fisher K, Turner S (2007) PXY, a receptor-like kinase essential for maintaining polarity during plant vascular-tissue development. Curr Biol 17: 1061–1066. PubMed

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: 767–774. PubMed

Ohashi-Ito K, Fukuda H (2010) Transcriptional regulation of vascular cell fates. Curr Op Plant Biol 13: 670–676. PubMed

La Rota C, Chopard J, Das P, Paindavoine S, Rozier F, et al. (2011) A Data-Driven Integrative Model of Sepal Primordium Polarity in Arabidopsis. Plant Cell 23: 1–17. PubMed PMC

Hernández-Hernández V, Niklas KJ, Newman SA, Benítez M (2012) Dynamical patterning modules in plant development and evolution. Int J Dev Biol 56: 661–74. PubMed

Kauffman SA (1969) Metabolic stability and epigenesis in randomly constructed genetic nets. J Theor Biol 22: 437–467. PubMed

Sankar M, Osmont KS, Rolcik J, Gujas B, Tarkowska D, et al. (2011) A qualitative continuous model of cellular auxin and brassinosteroid signaling and their crosstalk. Bioinformatics 27: 1404–1412. PubMed

Okadalat K, Uedalb J, Komaki MK, Bell CJ (1991) Requirement of the Auxin Polar Transport System in Early Stages of Arabídopsis Floral Bud Formation. Plant Cell 3: 677–684. PubMed PMC

Mähönen AP, Bonke M, Kauppinen L, Riikonen M, Benfey PN, et al. (2000) A novel two-component hybrid molecule regulates vascular morphogenesis of the Arabidopsis root. Genes Dev 14: 2938–43. PubMed PMC

Mattsson J, Sung ZR, Berleth T (1999) Responses of plant vascular systems to auxin transport inhibition. Development 126: 2979–2991. PubMed

Turner S, Sieburth LE (2002) Vascular Patterning. In The Arabidopsis Book. American Society of Plant Biologists 5: 1. PubMed PMC

Mähönen AP, Higuchi M, Törmäkangas K, Miyawaki K, Pischke MS, et al. (2006) Cytokinins regulate a bidirectional phosphorelay network in Arabidopsis. Curr Biol 1611: 1116–22. PubMed

Ohashi-Ito K, Fukuda H (2003) HD-zip III homeobox genes that include a novel member, ZeHB-13 (Zinnia)/ATHB-15 (Arabidopsis), are involved in procambium and xylem cell differentiation. Plant Cell Physiol 44: 1350–1358. PubMed

Gardiner J, Donner TJ, Scarpella E (2011) Simultaneous activation of SHR and ATHB8 expression defines switch to preprocambial cell state in Arabidopsis leaf development. Dev Dyn 240: 261–270. PubMed

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 Nat Acad Sci USA 105: 18625–18630. PubMed PMC

Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27: 297–300. PubMed PMC

Emery JF, Floyd SK, Alvarez J, Eshed Y, Hawker NP, et al. (2003) Radial Patterning of Arabidopsis Shoots by Class III HD-ZIP and KANADI Genes. Curr Biol 13: 1768–1774. PubMed

Ilegems M, Douet V, Meylan-Bettex M, Uyttewaal M, Brand L, et al. (2010) Interplay of auxin, KANADI and Class III HD-ZIP transcription factors in vascular tissue formation. Development 137: 975–984. PubMed

Demura T, Tashiro G, Horiguchi G, Kishimoto N, Kubo M, et al. (2002) Visualization by comprehensive microarray analysis of gene expression programs during transdifferentiation of mesophyll cells into xylem cells. Proc Nat Acad Sci USA 99: 15794–15799. PubMed PMC

Yoshida S, Iwamoto K, Demura T, Fukuda H (2009) Comprehensive analysis of the regulatory roles of auxin in early transdifferentiation into xylem cells. Plant Mol Biol 70: 457–469. PubMed

Sawa S, Demura T, Horiguchi G, Kubo M, Fukuda H (2005) The ATE Genes Are Responsible for Repression of Transdifferentiation into Xylem Cells in Arabidopsis. Plant Physiol 137: 141–148. PubMed PMC

Caño-Delgado A, Yin Y, Yu C, Vafeados D, Mora-García S, et al. (2004) BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development 131: 5341–5351. PubMed

Yoshida S, Kuriyama H, Fukuda H (2005) Inhibition of transdifferentiation into tracheary elements by polar auxin transport inhibitors through intracellular auxin depletion. Plant Cell Physiol 46: 2019–2028. PubMed

Gälweiler L, Guan C, Müller A, Wisman E, Mendgen K, et al. (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282: 2226–30. PubMed

Prigge MJ, Otsuga D (2005) Class III Homeodomain-Leucine Zipper Gene Family Members Have Overlapping, Antagonistic, and Distinct Roles in Arabidopsis Development. 17: 61–76. PubMed PMC

Carlsbecker A, Helariutta Y (2005) Phloem and xylem specification: pieces of the puzzle emerge. Curr Op Plant Biol 8: 512–517. PubMed

Fukuda H, Komamine A (1980) Direct Evidence for Cytodifferentiation to Tracheary Elements without Intervening Mitosis in a Culture of Single Cells Isolated from the Mesophyll of Zinnia elegans. Plant Physiol 65: 61–64. PubMed PMC

Fukuda H, Komamine A (1980) Establishment of an Experimental System for the Study of Tracheary Element Differentiation from Single Cells Isolated from the Mesophyll of Zinnia elegans. Plant Physiol 65: 57–60. PubMed PMC

Suer S, Agusti J, Sanchez P, Schwarz M, Greb T (2011) WOX4 Imparts Auxin Responsiveness to Cambium Cells in Arabidopsis. Plant Cell 23: 3247–3259. PubMed PMC

Riefler M, Novak O, Strnad M, Schmülling T (2006) Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell 18(1): 40–54. PubMed PMC

Hass C, Lohrmann J, Albrecht V, Sweere U, Hummel F, et al. (2004) The response regulator 2 mediates ethylene signalling and hormone signal integration in Arabidopsis. EMBO J 23: 3290–3302. PubMed PMC

Kushwah S, Jones AM, Laxmi A (2011) Cytokinin interplay with ethylene, auxin and glucose signaling controls Arabidopsis seedling root directional growth. Plant Physiol 156: 1851–1866. PubMed PMC

Argueso CT, Ferreira FJ, Epple P, To JPC, Hutchison CE, et al. (2012) Two-component elements mediate interactions between cytokinin and salicylic acid in plant immunity. PLoS Genet 8: e1002448. PubMed PMC

Sweere U, Eichenberg K, Lohrmann J, Mira-Rodado V, Bäurle I, et al. (2001) Interaction of the response regulator ARR4 with phytochrome B in modulating red light signaling. Science 294: 1108–1111. PubMed

Mira-Rodado V, Sweere U, Grefen C, Kunkel T, Fejes E, et al. (2007) Functional cross-talk between two-component and phytochrome B signal transduction in Arabidopsis. J Exp Bot 58: 2595–2607. PubMed

Yoshida S, Mandel T, Kuhlemeier C (2011) Stem cell activation by light guides plant organogenesis. Genes Dev 25: 1439–1450. PubMed PMC

Horák J, Janda L, Pekárová B, Hejátko J (2011) Molecular mechanisms of signalling specificity via phosphorelay pathways in Arabidopsis. Curr Protein Pept Sci 12: 126–36. PubMed

Carlsbecker A, Lee JY, Roberts CJ, Dettmer J, Lehesranta S, et al. (2010) Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465: 316–321. PubMed PMC

Müller GB (2007) Evo-devo: extending the evolutionary synthesis. Nat Rev Genet 8: 943–949. PubMed

Finet C, Jaillais Y (2012) Auxology: when auxin meets plant evo-devo. Dev Biol 369: 19–31. PubMed

Meyerowitz EM (2002) Plants compared to animals: The broadest comparative study of development. Science 295: 1482–1485. PubMed

Nakata M, Matsumoto N, Tsugeki R, Rikirsch E, Laux T, et al. (2012) Roles of the Middle Domain – Specific WUSCHEL-RERELATED HOMEOBOX genes in early development of leaves in Arabidopsis. Plant Cell 24: 519–35. PubMed PMC