Understanding the development of vascular tissues in plants is crucial because the evolution of vasculature enabled plants to thrive on land. Various systems and approaches have been used to advance our knowledge about the genetic regulation of vasculature development, from the scale of single genes to networks. In this review, we provide a perspective on the major approaches used in studying plant vascular development, and we cover the mechanisms and genetic networks underlying vascular tissue specification, patterning, and differentiation.


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Literature Cited

  1. Agusti J, Lichtenberger R, Schwarz M, Nehlin L, Greb T. 1.  2011. Characterization of transcriptome remodeling during cambium formation identifies MOL1 and RUL1 as opposing regulators of secondary growth. PLOS Genet 7:e1001312 [Google Scholar]
  2. Anne P, Azzopardi M, Gissot L, Beaubiat S, Hématy K. 2.  Palauqui J-C; 2015. OCTOPUS negatively regulates BIN2 to control phloem differentiation in Arabidopsis thaliana. Curr. Biol. 25:2584–90 [Google Scholar]
  3. Asano T, Masumura T, Kusano H, Kikuchi S, Kurita A. 3.  et al. 2002. Construction of a specialized cDNA library from plant cells isolated by laser capture microdissection: toward comprehensive analysis of the genes expressed in the rice phloem. Plant J 32:401–8 [Google Scholar]
  4. Baima S, Forte V, Possenti M, Peñalosa A, Leoni G. 4.  et al. 2014. Negative feedback regulation of auxin signaling by ATHB8/ACL5–BUD2 transcription module. Mol. Plant 7:1006–25 [Google Scholar]
  5. Baima S, Nobili F, Sessa G, Lucchetti S, Ruberti I, Morelli G. 5.  1995. The expression of the Athb-8 homeobox gene is restricted to provascular cells in Arabidopsis thaliana. Development 121:4171–82 [Google Scholar]
  6. Bartrina I, Otto E, Strnad M, Werner T, Schmülling T. 6.  2011. Cytokinin regulates the activity of reproductive meristems, flower organ size, ovule formation, and thus seed yield in Arabidopsis thaliana. Plant Cell 23:69–80 [Google Scholar]
  7. Bauby H, Divol F, Truernit E, Grandjean O, Palauqui J-C. 7.  2007. Protophloem differentiation in early Arabidopsis thaliana development. Plant Cell Physiol 48:97–109 [Google Scholar]
  8. Benfey PN, Linstead PJ, Roberts K, Schiefelbein JW, Hauser M-T, Aeschbacher RA. 8.  1993. Root development in Arabidopsis: four mutants with dramatically altered root morphogenesis. Development 119:57–70 [Google Scholar]
  9. Berleth T, Jurgens G. 9.  1993. The role of the monopteros gene in organising the basal body region of the Arabidopsis embryo. Development 118:575–87 [Google Scholar]
  10. Bhalerao RP, Fischer U. 10.  2014. Auxin gradients across wood—instructive or incidental?. Physiol. Plant. 151:43–51 [Google Scholar]
  11. Birnbaum K, Shasha DE, Wang JY, Jung JW, Lambert GM. 11.  et al. 2003. A gene expression map of the Arabidopsis root. Science 302:1956–60 [Google Scholar]
  12. Bishopp A, Help H, el-Showk S, Weijers D, Scheres B. 12.  et al. 2011. A mutually inhibitory interaction between auxin and cytokinin specifies vascular pattern in roots. Curr. Biol. 21:917–26 [Google Scholar]
  13. Bonke M, Thitamadee S, Mähönen AP, Hauser M-T, Helariutta Y. 13.  2003. APL regulates vascular tissue identity in Arabidopsis. Nature 426:181–86 [Google Scholar]
  14. Brady SM, Orlando DA, Lee J-Y, Wang JY, Koch J. 14.  et al. 2007. A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318:801–6 [Google Scholar]
  15. Brown DM, Zeef LAH, Ellis J, Goodacre R, Turner SR. 15.  2005. Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 17:2281–95 [Google Scholar]
  16. Campbell L, Turner S. 16.  2017. Regulation of vascular cell division. J. Exp. Bot. 68:27–43 [Google Scholar]
  17. Caño-Delgado A, Yin Y, Yu C, Vafeados D, Mora-García S. 17.  et al. 2004. BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development 131:5341 [Google Scholar]
  18. Carland FM, Berg BL, FitzGerald JN, Jinamornphongs S, Nelson T, Keith B. 18.  1999. Genetic regulation of vascular tissue patterning in Arabidopsis. Plant Cell 11:2123–37 [Google Scholar]
  19. Carland FM, Nelson T. 19.  2009. CVP2- and CVL1-mediated phosphoinositide signaling as a regulator of the ARF GAP SFC/VAN3 in establishment of foliar vein patterns. Plant J 59:895–907 [Google Scholar]
  20. Carlsbecker A, Lee J-Y, Roberts CJ, Dettmer J, Lehesranta S. 20.  et al. 2010. Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465:316–21 [Google Scholar]
  21. Collins C, Maruthi NM, Jahn CE. 21.  2015. CYCD3 D-type cyclins regulate cambial cell proliferation and secondary growth in Arabidopsis. J. Exp. Bot. 66:4595–606 [Google Scholar]
  22. de Lucas M, Pu L, Turco GM, Gaudinier A, Morao AK. 22.  et al. 2016. Transcriptional regulation of Arabidopsis Polycomb Repressive Complex 2 coordinates cell type proliferation and differentiation. Plant Cell 28:2616–31 [Google Scholar]
  23. De Rybel B, Adibi M, Breda AS, Wendrich JR, Smit ME. 23.  et al. 2014. Integration of growth and patterning during vascular tissue formation in Arabidopsis. Science 345:1255215 [Google Scholar]
  24. De Rybel B, Breda AS, Weijers D. 24.  2014. Prenatal plumbing—vascular tissue formation in the plant embryo. Physiol. Plant. 151:126–33 [Google Scholar]
  25. De Rybel B, Mähönen AP, Helariutta Y, Weijers D. 25.  2016. Plant vascular development: from early specification to differentiation. Nat. Rev. Mol. Cell Biol. 17:30–40 [Google Scholar]
  26. De Rybel B, Möller B, Yoshida S, Grabowicz I, de Reuille PB. 26.  et al. 2013. A bHLH complex controls embryonic vascular tissue establishment and indeterminate growth in Arabidopsis. Dev. Cell 24:426–37 [Google Scholar]
  27. Deeken R, Ache P, Kajahn I, Klinkenberg J, Bringmann G, Hedrich R. 27.  2008. Identification of Arabidopsis thaliana phloem RNAs provides a search criterion for phloem‐based transcripts hidden in complex datasets of microarray experiments. Plant J 55:746–59 [Google Scholar]
  28. del Pozo JC, Diaz-Trivino S, Cisneros N, Gutierrez C. 28.  2006. The balance between cell division and endoreplication depends on E2FC–DPB, transcription factors regulated by the ubiquitin–SCFSKP2A pathway in Arabidopsis. Plant Cell 18:2224–35 [Google Scholar]
  29. Demura T, Tashiro G, Horiguchi G, Kishimoto N, Kubo M. 29.  et al. 2002. Visualization by comprehensive microarray analysis of gene expression programs during transdifferentiation of mesophyll cells into xylem cells. PNAS 99:15794–99 [Google Scholar]
  30. Depuydt S, Rodriguez-Villalon A, Santuari L, Wyser-Rmili C, Ragni L, Hardtke CS. 30.  2013. Suppression of Arabidopsis protophloem differentiation and root meristem growth by CLE45 requires the receptor-like kinase BAM3. PNAS 110:7074–79 [Google Scholar]
  31. Donner TJ, Sherr I, Scarpella E. 31.  2009. Regulation of preprocambial cell state acquisition by auxin signaling in Arabidopsis leaves. Development 136:3235–46 [Google Scholar]
  32. Drainas D, Kalpaxis DL. 32.  1994. Bimodal action of spermine on ribosomal peptidyltransferase at low concentration of magnesium ions. Biochim Biophys Acta 1208:55–64 [Google Scholar]
  33. Du J, Miura E, Robischon M, Martinez C, Groover A. 33.  2011. The Populus Class III HD ZIP transcription factor POPCORONA affects cell differentiation during secondary growth of woody stems. PLOS ONE 6:e17458 [Google Scholar]
  34. el-Showk S, Blomster T, Siligato R, Marée AFM, Mähönen AP, Grieneisen VA. 34.  2015. Parsimonious model of vascular patterning links transverse hormone fluxes to lateral root initiation: auxin leads the way, while cytokinin levels out. PLOS Comput. Biol. 11:e1004450 [Google Scholar]
  35. Emery JF, Floyd SK, Alvarez J, Eshed Y, Hawker NP. 35.  et al. 2003. Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr. Biol. 13:1768–74 [Google Scholar]
  36. Eriksson ME, Israelsson M, Olsson O, Moritz T. 36.  2000. Increased gibberellin biosynthesis in transgenic trees promotes growth, biomass production and xylem fiber length. Nat. Biotechnol. 18:784–88 [Google Scholar]
  37. Eshed Y, Baum SF, Perea JV, Bowman JL. 37.  2001. Establishment of polarity in lateral organs of plants. Curr. Biol. 11:1251–60 [Google Scholar]
  38. Etchells JP, Mishra LS, Kumar M, Campbell L, Turner SR. 38.  2015. Wood formation in trees is increased by manipulating PXY-regulated cell division. Curr. Biol. 25:1050–55 [Google Scholar]
  39. Etchells JP, Provost CM, Mishra L, Turner SR. 39.  2013. WOX4 and WOX14 act downstream of the PXY receptor kinase to regulate plant vascular proliferation independently of any role in vascular organisation. Development 140:2224 [Google Scholar]
  40. Etchells JP, Provost CM, Turner SR. 40.  2012. Plant vascular cell division is maintained by an interaction between PXY and ethylene signalling. PLOS Genet 8:e1002997 [Google Scholar]
  41. Fisher K, Turner S. 41.  2007. PXY, a receptor-like kinase essential for maintaining polarity during plant vascular-tissue development. Curr. Biol. 17:1061–66 [Google Scholar]
  42. Foster AS. 42.  1952. Foliar venation in angiosperms from an ontogenetic standpoint. Am. J. Bot 39:752–66 [Google Scholar]
  43. Friml J, Vieten A, Sauer M, Weijers D, Schwarz H. 43.  et al. 2003. Efflux-dependent auxin gradients establish the apical–basal axis of Arabidopsis. Nature 426:147–53 [Google Scholar]
  44. Fukuda H, Komamine A. 44.  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 [Google Scholar]
  45. Fukuda H, Komamine A. 45.  1982. Lignin synthesis and its related enzymes as markers of tracheary-element differentiation in single cells isolated from the mesophyll of Zinnia elegans. Planta 155:423–30 [Google Scholar]
  46. Furuta KM, Hellmann E, Helariutta Y. 46.  2014. Molecular control of cell specification and cell differentiation during procambial development. Annu. Rev. Plant Biol. 65:607–38 [Google Scholar]
  47. Furuta KM, Yadav SR, Lehesranta S, Belevich I, Miyashima S. 47.  et al. 2014. Arabidopsis NAC45/86 direct sieve element morphogenesis culminating in enucleation. Science 345:933 [Google Scholar]
  48. Gälweiler L, Guan C, Müller A, Wisman E, Mendgen K. 48.  et al. 1998. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282:2226–30 [Google Scholar]
  49. Ge C, Cui X, Wang Y, Hu Y, Fu Z. 49.  et al. 2006. BUD2, encoding an S-adenosylmethionine decarboxylase, is required for Arabidopsis growth and development. Cell Res 16:446–56 [Google Scholar]
  50. Goué N, Noël-Boizot N, Vallance M, Magel E, Label P. 50.  2012. Microdissection to isolate vascular cambium cells in poplar. Silva Fenn 46:5–16 [Google Scholar]
  51. Gursanscky NR, Jouannet V, Grünwald K, Sanchez P, Laaber‐Schwarz M, Greb T. 51.  2016. MOL1. is required for cambium homeostasis in Arabidopsis. Plant J. 86:210–20 [Google Scholar]
  52. Hamann T, Benkova E, Bäurle I, Kientz M, Jürgens G. 52.  2002. The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. Genes Dev 16:1610–15 [Google Scholar]
  53. Hamann T, Mayer U, Jurgens G. 53.  1999. The auxin-insensitive bodenlos mutation affects primary root formation and apical-basal patterning in the Arabidopsis embryo. Development 126:1387–95 [Google Scholar]
  54. Hanzawa Y, Takahashi T, Komeda Y. 54.  1997. ACL5: an Arabidopsis gene required for internodal elongation after flowering. Plant J 12:863–74 [Google Scholar]
  55. Hardtke CS, Berleth T. 55.  1998. The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J 17:1405–11 [Google Scholar]
  56. Hawker NP, Bowman JL. 56.  2004. Roles for Class III HD-Zip and KANADI genes in Arabidopsis root development. Plant Physiol 135:2261–70 [Google Scholar]
  57. Heo JO, Blob B, Helariutta Y. 57.  2017. Differentiation of conductive cells: a matter of life and death. Curr. Opin. Plant Biol. 35:23–29 [Google Scholar]
  58. Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Jung J. 58.  et al. 2000. The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101:555–67 [Google Scholar]
  59. Hertzberg M, Aspeborg H, Schrader J, Andersson A, Erlandsson R. 59.  et al. 2001. A transcriptional roadmap to wood formation. PNAS 98:14732–37 [Google Scholar]
  60. Hirakawa Y, Kondo Y, Fukuda H. 60.  2010. TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in Arabidopsis. Plant Cell 22:2618–29 [Google Scholar]
  61. Hirakawa Y, Shinohara H, Kondo Y, Inoue A, Nakanomyo I. 61.  et al. 2008. Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system. PNAS 105:15208–13 [Google Scholar]
  62. Hussey S, Mizrachi E, Creux N, Myburg A. 62.  2013. Navigating the transcriptional roadmap regulating plant secondary cell wall deposition. Front. Plant Sci. 4:325 [Google Scholar]
  63. Hwang I, Sheen J, Müller B. 63.  2012. Cytokinin signaling networks. Annu. Rev. Plant Biol. 63:353–80 [Google Scholar]
  64. Imai A, Hanzawa Y, Komura M, Yamamoto KT, Komeda Y, Takahashi T. 64.  2006. The dwarf phenotype of the Arabidopsis acl5 mutant is suppressed by a mutation in an upstream ORF of a bHLH gene. Development 133:3575–85 [Google Scholar]
  65. Immanen J, Nieminen K, Smolander OP, Kojima M, Alonso Serra J. 65.  et al. 2016. Cytokinin and auxin display distinct but interconnected distribution and signaling profiles to stimulate cambial activity. Curr. Biol. 26:1990–97 [Google Scholar]
  66. Inoue T, Higuchi M, Hashimoto Y, Seki M, Kobayashi M. 66.  et al. 2001. Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature 409:1060–63 [Google Scholar]
  67. Ito Y, Nakanomyo I, Motose H, Iwamoto K, Sawa S. 67.  et al. 2006. Dodeca-CLE peptides as suppressors of plant stem cell differentiation. Science 313:842 [Google Scholar]
  68. Jacobs WP. 68.  1952. The role of auxin in differentiation of xylem around a wound. Am. J. Bot. 39:301–9 [Google Scholar]
  69. Jouannet V, Brackmann K, Greb T. 69.  2015. (Pro)cambium formation and proliferation: two sides of the same coin?. Curr. Opin. Plant Biol. 23:54–60 [Google Scholar]
  70. Kang YH, Hardtke CS. 70.  2016. Arabidopsis MAKR5 is a positive effector of BAM3‐dependent CLE45 signaling. EMBO Rep 17:1145–54 [Google Scholar]
  71. Katayama H, Iwamoto K, Kariya Y, Asakawa T, Kan T. 71.  et al. 2015. A negative feedback loop controlling bHLH complexes is involved in vascular cell division and differentiation in the root apical meristem. Curr. Biol. 25:3144–50 [Google Scholar]
  72. Kerstetter RA, Bollman K, Taylor RA, Bomblies K, Poethig RS. 72.  2001. KANADI. regulates organ polarity in Arabidopsis. Nature 411:706–9 [Google Scholar]
  73. Knott JM, Römer P, Sumper M. 73.  2007. Putative spermine synthases from Thalassiosira pseudonana and Arabidopsis thaliana synthesize thermospermine rather than spermine. FEBS Lett 581:3081–86 [Google Scholar]
  74. Ko D, Kang J, Kiba T, Park J, Kojima M. 74.  et al. 2014. Arabidopsis ABCG14 is essential for the root-to-shoot translocation of cytokinin. PNAS 111:7150–55 [Google Scholar]
  75. Ko J-H, Han K-H, Park S, Yang J. 75.  2004. Plant body weight–induced secondary growth in Arabidopsis and its transcription phenotype revealed by whole-transcriptome profiling. Plant Physiol 135:1069–83 [Google Scholar]
  76. Kondo Y, Fujita T, Sugiyama M, Fukuda H. 76.  2015. A novel system for xylem cell differentiation in Arabidopsis thaliana. Mol. Plant 8:612–21 [Google Scholar]
  77. Kondo Y, Ito T, Nakagami H, Hirakawa Y, Saito M. 77.  et al. 2014. Plant GSK3 proteins regulate xylem cell differentiation downstream of TDIF–TDR signalling. Nat. Commun. 5:3504 [Google Scholar]
  78. Kondo Y, Nurani AM, Saito C, Ichihashi Y, Saito M. 78.  et al. 2016. Vascular cell induction culture system using Arabidopsis leaves (VISUAL) reveals the sequential differentiation of sieve element–like cells. Plant Cell 28:1250–62 [Google Scholar]
  79. Kubo M, Udagawa M, Nishikubo N, Horiguchi G, Yamaguchi M. 79.  et al. 2005. Transcription switches for protoxylem and metaxylem vessel formation. Genes Dev 19:1855–60 [Google Scholar]
  80. Kumar M, Campbell L, Turner S. 80.  2015. Secondary cell walls: biosynthesis and manipulation. J. Exp. Bot. 67:515–31 [Google Scholar]
  81. Liebsch D, Sunaryo W, Holmlund M, Norberg M, Zhang J. 81.  et al. 2014. Class I KNOX transcription factors promote differentiation of cambial derivatives into xylem fibers in the Arabidopsis hypocotyl. Development 141:4311–19 [Google Scholar]
  82. Little CHA, MacDonald JE, Olsson O. 82.  2002. Involvement of indole-3-acetic acid in fascicular and interfascicular cambial growth and interfascicular extraxylary fiber differentiation in Arabidopsis thaliana inflorescence stems. Int. J. Plant Sci. 163:519–29 [Google Scholar]
  83. Love J, Björklund S, Vahala J, Hertzberg M, Kangasjärvi J, Sundberg B. 83.  2009. Ethylene is an endogenous stimulator of cell division in the cambial meristem of Populus. PNAS 106:5984–89 [Google Scholar]
  84. Lucas WJ, Groover A, Lichtenberger R, Furuta K, Yadav S-R. 84.  et al. 2013. The plant vascular system: evolution, development and functions. J. Integr. Plant Biol. 55:294–388 [Google Scholar]
  85. Mähönen AP, Bishopp A, Higuchi M, Nieminen KM, Kinoshita K. 85.  et al. 2006. Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development. Science 311:94–98 [Google Scholar]
  86. Mähönen AP, Bonke M, Kauppinen L, Riikonen M, Benfey PN, Helariutta Y. 86.  2000. A novel two-component hybrid molecule regulates vascular morphogenesis of the Arabidopsis root. Genes Dev 14:2938–43 [Google Scholar]
  87. Mähönen AP, Higuchi M, Törmäkangas K, Miyawaki K, Pischke MS. 87.  et al. 2006. Cytokinins regulate a bidirectional phosphorelay network in Arabidopsis. Curr. Biol. 16:1116–22 [Google Scholar]
  88. Marhavý P, Bielach A, Abas L, Abuzeineh A, Duclercq J. 88.  et al. 2011. Cytokinin modulates endocytic trafficking of PIN1 auxin efflux carrier to control plant organogenesis. Dev. Cell 21:796–804 [Google Scholar]
  89. Marhavý P, Duclercq J, Weller B, Feraru E, Bielach A. 89.  et al. 2014. Cytokinin controls polarity of PIN1-dependent auxin transport during lateral root organogenesis. Curr. Biol. 24:1031–37 [Google Scholar]
  90. Mariconti L, Pellegrini B, Cantoni R, Stevens R, Bergounioux C. 90.  et al. 2002. The E2F family of transcription factors from Arabidopsis thaliana. J. Biol. Chem. 277:9911–19 [Google Scholar]
  91. Matsumoto-Kitano M, Kusumoto T, Tarkowski P, Kinoshita-Tsujimura K, Václavíková K. 91.  et al. 2008. Cytokinins are central regulators of cambial activity. PNAS 105:20027–31 [Google Scholar]
  92. Mattsson J, Ckurshumova W, Berleth T. 92.  2003. Auxin signaling in Arabidopsis leaf vascular development. Plant Physiol 131:1327–39 [Google Scholar]
  93. Mattsson J, Sung ZR, Berleth T. 93.  1999. Responses of plant vascular systems to auxin transport inhibition. Development 126:2979–91 [Google Scholar]
  94. Mauriat M, Sandberg LG, Moritz T. 94.  2011. Proper gibberellin localization in vascular tissue is required to control auxin-dependent leaf development and bud outgrowth in hybrid aspen. Plant J 67:805–16 [Google Scholar]
  95. Mayer U, Ruiz RAT, Berleth T, Miseéra S, Juürgens G. 95.  1991. Mutations affecting body organization in the Arabidopsis embryo. Nature 353:402–7 [Google Scholar]
  96. Mazur E, Kurczyńska EU, Friml J. 96.  2014. Cellular events during interfascicular cambium ontogenesis in inflorescence stems of Arabidopsis. Protoplasma 251:1125–39 [Google Scholar]
  97. McConnell JR, Emery J, Eshed Y, Bao N, Bowman J, Barton MK. 97.  2001. Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411:709–13 [Google Scholar]
  98. Mellor N, Adibi M, el-Showk S, De Rybel B, King J. 98.  et al. 2017. Theoretical approaches to understanding root vascular patterning: a consensus between recent models. J. Exp. Bot. 68:5–16 [Google Scholar]
  99. Milhinhos A, Prestele J, Bollhöner B, Matos A, Vera‐Sirera F. 99.  et al. 2013. Thermospermine levels are controlled by an auxin‐dependent feedback loop mechanism in Populus xylem. Plant J 75:685–98 [Google Scholar]
  100. Mitsuda N, Seki M, Shinozaki K, Ohme-Takagi M. 100.  2005. The NAC transcription factors NST1 and NST2 of Arabidopsis regulate secondary wall thickenings and are required for anther dehiscence. Plant Cell 17:2993–3006 [Google Scholar]
  101. Motose H, Sugiyama M, Fukuda H. 101.  2004. A proteoglycan mediates inductive interaction during plant vascular development. Nature 429:873–78 [Google Scholar]
  102. Mou Z, Wang X, Fu Z, Dai Y, Han C. 102.  et al. 2002. Silencing of phosphoethanolamine N-methyltransferase results in temperature-sensitive male sterility and salt hypersensitivity in Arabidopsis. Plant Cell 14:2031–43 [Google Scholar]
  103. Mouchel CF, Briggs GC, Hardtke CS. 103.  2004. Natural genetic variation in Arabidopsis identifies BREVIS RADIX, a novel regulator of cell proliferation and elongation in the root. Genes Dev 18:700–14 [Google Scholar]
  104. Mouchel CF, Osmont KS, Hardtke CS. 104.  2006. BRX mediates feedback between brassinosteroid levels and auxin signalling in root growth. Nature 443:458–61 [Google Scholar]
  105. Müller CJ, Valdés AE, Guodong W, Ramachandran P, Beste L. 105.  et al. 2016. PHABULOSA mediates an auxin signaling loop to regulate vascular patterning in Arabidopsis. Plant Physiol 170:956–70 [Google Scholar]
  106. Muñiz L, Minguet EG, Singh SK, Pesquet E, Vera-Sirera F. 106.  et al. 2008. ACAULIS5 controls Arabidopsis xylem specification through the prevention of premature cell death. Development 135:2573–82 [Google Scholar]
  107. Muraro D, Mellor N, Pound MP, Lucas M, Chopard J. 107.  et al. 2014. Integration of hormonal signaling networks and mobile microRNAs is required for vascular patterning in Arabidopsis roots. PNAS 111:857–62 [Google Scholar]
  108. Nagawa S, Sawa S, Sato S, Kato T, Tabata S, Fukuda H. 108.  2006. Gene trapping in Arabidopsis reveals genes involved in vascular development. Plant Cell Physiol 47:1394–405 [Google Scholar]
  109. Nakajima K, Sena G, Nawy T, Benfey PN. 109.  2001. Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413:307–11 [Google Scholar]
  110. Nieminen K, Blomster T, Helariutta Y, Mähönen AP. 110.  2015. Vascular cambium development. Arabidopsis Book 13:e0177 [Google Scholar]
  111. Nieminen K, Immanen J, Laxell M, Kauppinen L, Tarkowski P. 111.  et al. 2008. Cytokinin signaling regulates cambial development in poplar. PNAS 105:20032–37 [Google Scholar]
  112. Nilsson J, Karlberg A, Antti H, Lopez-Vernaza M, Mellerowicz E. 112.  et al. 2008. Dissecting the molecular basis of the regulation of wood formation by auxin in hybrid aspen. Plant Cell 20:843–55 [Google Scholar]
  113. Obara K, Kuriyama H, Fukuda H. 113.  2001. Direct evidence of active and rapid nuclear degradation triggered by vacuole rupture during programmed cell death in Zinnia. Plant Physiol 125:615–26 [Google Scholar]
  114. Oda Y, Mimura T, Hasezawa S. 114.  2005. Regulation of secondary cell wall development by cortical microtubules during tracheary element differentiation in Arabidopsis cell suspensions. Plant Physiol 137:1027–36 [Google Scholar]
  115. Ohashi-Ito K, Fukuda H. 115.  2010. Transcriptional regulation of vascular cell fates. Curr. Opin. Plant Biol. 13:670–76 [Google Scholar]
  116. Ohashi-Ito K, Matsukawa M, Fukuda H. 116.  2013. An atypical bHLH transcription factor regulates early xylem development downstream of auxin. Plant Cell Physiol 54:398–405 [Google Scholar]
  117. Ohashi-Ito K, Saegusa M, Iwamoto K, Oda Y, Katayama H. 117.  et al. 2014. A bHLH complex activates vascular cell division via cytokinin action in root apical meristem. Curr. Biol. 24:2053–58 [Google Scholar]
  118. Okada K, Ueda J, Komaki MK, Bell CJ, Shimura Y. 118.  1991. Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell 3:677–84 [Google Scholar]
  119. Péret B, Swarup K, Ferguson A, Seth M, Yang Y. 119.  et al. 2012. AUX/LAX genes encode a family of auxin influx transporters that perform distinct functions during Arabidopsis development. Plant Cell 24:2874–85 [Google Scholar]
  120. Pesquet E, Tuominen H. 120.  2011. Ethylene stimulates tracheary element differentiation in Zinnia elegans cell cultures. N. Phytologist 190:138–49 [Google Scholar]
  121. Provart NJ, Alonso J, Assmann SM, Bergmann D, Brady SM. 121.  et al. 2016. 50 years of Arabidopsis research: Highlights and future directions. New Phytol 209:921–44 [Google Scholar]
  122. Przemeck GKH, Mattsson J, Hardtke CS, Sung ZR, Berleth T. 122.  1996. Studies on the role of the Arabidopsis gene MONOPTEROS in vascular development and plant cell axialization. Planta 200:229–37 [Google Scholar]
  123. Randall RS, Miyashima S, Blomster T, Zhang J, Elo A. 123.  et al. 2015. AINTEGUMENTA and the D-type cyclin CYCD3;1 regulate root secondary growth and respond to cytokinins. Biol. Open 4:1229–36 [Google Scholar]
  124. Rashotte AM, Mason MG, Hutchison CE, Ferreira FJ, Schaller GE, Kieber JJ. 124.  2006. A subset of Arabidopsis AP2 transcription factors mediates cytokinin responses in concert with a two-component pathway. PNAS 103:11081–85 [Google Scholar]
  125. Robischon M, Du J, Miura E, Groover A. 125.  2011. The Populus Class III HD ZIP, popREVOLUTA, influences cambium initiation and patterning of woody stems. Plant Physiol 155:1214–25 [Google Scholar]
  126. Rodriguez-Villalon A, Gujas B, Kang YH, Breda AS, Cattaneo P. 126.  et al. 2014. Molecular genetic framework for protophloem formation. PNAS 111:11551–56 [Google Scholar]
  127. Rodriguez-Villalon A, Gujas B, van Wijk R, Munnik T, Hardtke CS. 127.  2015. Primary root protophloem differentiation requires balanced phosphatidylinositol-4,5-biphosphate levels and systemically affects root branching. Development 142:1437 [Google Scholar]
  128. Sachs T. 128.  1981. The control of the patterned differentiation of vascular tissues. Adv. Bot. Res. 9:151–262 [Google Scholar]
  129. Salazar-Henao JE, Lehner R, Betegón-Putze I, Vilarrasa-Blasi J, Caño-Delgado AI. 129.  2016. BES1 regulates the localization of the brassinosteroid receptor BRL3 within the provascular tissue of the Arabidopsis primary root. J. Exp. Bot. 67:4951–61 [Google Scholar]
  130. Salehin M, Bagchi R, Estelle M. 130.  2015. SCFTIR1/AFB-based auxin perception: mechanism and role in plant growth and development. Plant Cell 27:9–19 [Google Scholar]
  131. Sawchuk MG, Edgar A, Scarpella E. 131.  2013. Patterning of leaf vein networks by convergent auxin transport pathways. PLOS Genet 9:e1003294 [Google Scholar]
  132. Sawchuk MG, Head P, Donner TJ, Scarpella E. 132.  2007. Time‐lapse imaging of Arabidopsis leaf development shows dynamic patterns of procambium formation. New Phytol 176:560–71 [Google Scholar]
  133. Scarpella E, Marcos D, Friml J, Berleth T. 133.  2006. Control of leaf vascular patterning by polar auxin transport. Genes Dev 20:1015–27 [Google Scholar]
  134. Scheres BJG, Di Laurenzio L, Willemsen V, Hauser M-T, Janmaat K. 134.  et al. 1995. Mutations affecting the radial organisation of the Arabidopsis root display specific defects throughout the embryonic axis. Development 121:53–62 [Google Scholar]
  135. Scheres BJG, Wolkenfelt H, Willemsen V, Terlouw M, Lawson E. 135.  et al. 1994. Embryonic origin of the Arabidopsis primary root and root meristem initials. Development 120:2475–87 [Google Scholar]
  136. Schlereth A, Moller B, Liu W, Kientz M, Flipse J. 136.  et al. 2010. MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 464:913–16 [Google Scholar]
  137. Shininger TL. 137.  1979. The control of vascular development. Annu. Rev. Plant Physiol. 30:313–37 [Google Scholar]
  138. Smet W, De Rybel B. 138.  2016. Genetic and hormonal control of vascular tissue proliferation. Curr. Opin. Plant Biol. 29:50–56 [Google Scholar]
  139. Snow R. 139.  1935. Activation of cambial growth by pure hormones. New Phytol 34:347–60 [Google Scholar]
  140. Sorokin HP, Mathur SN, Thimann KV. 140.  1962. The effects of auxins and kinetin on xylem differentiation in the pea epicotyl. Am. J. Bot. 49:444–54 [Google Scholar]
  141. Steinmann T, Geldner N, Grebe M, Mangold S, Jackson CL. 141.  et al. 1999. Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science 286:316–18 [Google Scholar]
  142. Sterky F, Regan S, Karlsson J, Hertzberg M, Rohde A. 142.  et al. 1998. Gene discovery in the wood-forming tissues of poplar: analysis of 5,692 expressed sequence tags. PNAS 95:13330–35 [Google Scholar]
  143. Suer S, Agusti J, Sanchez P, Schwarz M, Greb T. 143.  2011. WOX4. imparts auxin responsiveness to cambium cells in Arabidopsis. Plant Cell 23:3247–59 [Google Scholar]
  144. Takano A, Kakehi JI, Takahashi T. 144.  2012. Thermospermine is not a minor polyamine in the plant kingdom. Plant Cell Physiol 53:606–16 [Google Scholar]
  145. Taylor-Teeples M, Lin L, de Lucas M, Turco G, Toal TW. 145.  et al. 2015. An Arabidopsis gene regulatory network for secondary cell wall synthesis. Nature 517:571–75 [Google Scholar]
  146. Torrey JG. 146.  1965. Physiological bases of organization and development in the root. Encyclopedia of Plant Physiology, Vol. 15 Differentiation and Development FT Addicott, A Lang, W Ruhland 1256–327 Berlin: Springer [Google Scholar]
  147. Truernit E, Bauby H, Belcram K, Barthélémy J, Palauqui J-C. 147.  2012. OCTOPUS, a polarly localised membrane-associated protein, regulates phloem differentiation entry in Arabidopsis thaliana. Development 139:1306 [Google Scholar]
  148. Truernit E, Bauby H, Dubreucq B, Grandjean O, Runions J. 148.  et al. 2008. High-resolution whole-mount imaging of three-dimensional tissue organization and gene expression enables the study of phloem development and structure in Arabidopsis. Plant Cell 20:1494–503 [Google Scholar]
  149. Ueguchi C, Koizumi H, Suzuki T, Mizuno T. 149.  2001. Novel family of sensor histidine kinase genes in Arabidopsis thaliana. Plant Cell Physiol 42:231–35 [Google Scholar]
  150. Uggla C, Mellerowicz EJ, Sundberg B. 150.  1998. Indole-3-acetic acid controls cambial growth in Scots pine by positional signaling. Plant Physiol 117:113–21 [Google Scholar]
  151. Uggla C, Moritz T, Sandberg G, Sundberg B. 151.  1996. Auxin as a positional signal in pattern formation in plants. PNAS 93:9282–86 [Google Scholar]
  152. Vera-Sirera F, De Rybel B, Urbez C, Kouklas E, Pesquera M. 152.  et al. 2015. A bHLH-based feedback loop restricts vascular cell proliferation in plants. Dev. Cell 35:432–43 [Google Scholar]
  153. Weijers D, Schlereth A, Ehrismann JS, Schwank G, Kientz M, Jürgens G. 153.  2006. Auxin triggers transient local signaling for cell specification in Arabidopsis embryogenesis. Dev. Cell 10:265–70 [Google Scholar]
  154. Wenzel CL, Schuetz M, Yu Q, Mattsson J. 154.  2007. Dynamics of MONOPTEROS and PIN‐FORMED1 expression during leaf vein pattern formation in Arabidopsis thaliana. Plant J 49:387–98 [Google Scholar]
  155. Werner T, Motyka V, Strnad M, Schmülling T. 155.  2001. Regulation of plant growth by cytokinin. PNAS 98:10487–92 [Google Scholar]
  156. Wisman E, Cardon GH, Fransz P, Saedler H. 156.  1998. The behaviour of the autonomous maize transposable element En/Spm in Arabidopsis thaliana allows efficient mutagenesis. Plant Mol. Biol. 37:989–99 [Google Scholar]
  157. Xaplanteri MA, Petropoulos AD, Dinos GP, Kalpaxis DL. 157.  2005. Localization of spermine binding sites in 23S rRNA by photoaffinity labeling: parsing the spermine contribution to ribosomal 50S subunit functions. Nucleic Acids Res 33:2792–805 [Google Scholar]
  158. Xu B, Ohtani M, Yamaguchi M, Toyooka K, Wakazaki M. 158.  et al. 2014. Contribution of NAC transcription factors to plant adaptation to land. Science 343:1505–8 [Google Scholar]
  159. Yamamoto R, Demura T, Fukuda H. 159.  1997. Brassinosteroids induce entry into the final stage of tracheary element differentiation in cultured Zinnia cells. Plant Cell Physiol 38:980–83 [Google Scholar]
  160. Ye Z-H, Zhong R. 160.  2015. Molecular control of wood formation in trees. J. Exp. Bot. 66:4119–31 [Google Scholar]
  161. Yoshimoto K, Noutoshi Y, Hayashi K-I, Shirasu K, Takahashi T, Motose H. 161.  2012. A chemical biology approach reveals an opposite action between thermospermine and auxin in xylem development in Arabidopsis thaliana. Plant Cell Physiol 53:635–45 [Google Scholar]
  162. Young BS. 162.  1954. The effects of leaf primordia on differentiation in the stem. New Phytol 53:445–60 [Google Scholar]
  163. Zhang K, Novak O, Wei Z, Gou M, Zhang X. 163.  et al. 2014. Arabidopsis ABCG14 protein controls the acropetal translocation of root-synthesized cytokinins. Nat. Commun. 5:3274 [Google Scholar]
  164. Zhong R, Demura T, Ye Z-H. 164.  2006. SND1, a NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of Arabidopsis. Plant Cell 18:3158–70 [Google Scholar]
  165. Zhong R, Lee C, Zhou J, McCarthy RL, Ye Z-H. 165.  2008. A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell 20:2763–82 [Google Scholar]
  166. Zhu Y, Song D, Sun J, Wang X, Li L. 166.  2013. PtrHB7, a class III HD-Zip gene, plays a critical role in regulation of vascular cambium differentiation in Populus. Mol. Plant 6:1331–43 [Google Scholar]
  167. Zürcher E, Liu J, di Donato M, Geisler M, Müller B. 167.  2016. Plant development regulated by cytokinin sinks. Science 353:1027–30 [Google Scholar]

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