Signaling and gene regulatory programs in plant vascular stem cells

Genesis

Volumn 49, Issue 12, 2011, Pages 885-904

  Zhou, Jing ^a,b   Sebastian, Jose ^a   Lee, Ji Young ^a,b  

^a United States Department of Agriculture   (United States)

^b Department of Molecular Biology and Genetics   (United States)

Author keywords

Cambium; Cell cell communication; Gene regulatory network; Phloem; Procambium; Vascular tissues; Xylem

Indexed keywords

ARABINOGALACTAN; AUXIN; BRASSINOSTEROID; CYTOKININ; ETHYLENE; GIBBERELLIN; MICRORNA;

CELL COMMUNICATION; CELL DIFFERENTIATION; CELL POPULATION; CELL TYPE; GENE CONTROL; INTRACELLULAR SIGNALING; NONHUMAN; PHLOEM; PHOTOMORPHOGENESIS; PLANT CELL; PLANT GENE; PLANT LIFE CYCLE STAGE; PLANT TISSUE; PRIORITY JOURNAL; REVIEW; SOMATIC CELL GENETICS; STEM CELL; TRANSCRIPTION REGULATION; VASCULAR TISSUE; XYLEM;

CAMBIUM; CELL COMMUNICATION; CELL DIFFERENTIATION; CYTOKININS; GENE EXPRESSION REGULATION, PLANT; GENE REGULATORY NETWORKS; GIBBERELLINS; INDOLEACETIC ACIDS; MICRORNAS; MORPHOGENESIS; PLANT CELLS; PLANT VASCULAR BUNDLE; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; XYLEM;

EID: 83055181099     PISSN: 1526954X     EISSN: 1526968X     Source Type: Journal    
DOI: 10.1002/dvg.20795     Document Type: Review

References (182)

1. Agusti J, Lichtenberger R, Schwarz M, Nehlin L, Greb T. 2011. Characterization of transcriptome remodeling during cambium formation identifies MOL1 and RUL1 as opposing regulators of secondary growth. PLoS Genet 7: e1001312.
2. Aloni R, Langhans M, Aloni E, Dreieicher E, Ullrich CI. 2005. Root-synthesized cytokinin in arabidopsis is distributed in the shoot by the transpiration stream. J Exp Bot 56: 1535-1544.
3. Aloni R, Langhans M, Aloni E, Ullrich CI. 2004. Role of cytokinin in the regulation of root gravitropism. Planta 220: 177-182.
4. Argyros RD, Mathews DE, Chiang YH, Palmer CM, Thibault DM, Etheridge N, Argyros DA, Mason MG, Kieber JJ, Schaller GE. 2008. Type B response regulators of arabidopsis play key roles in cytokinin signaling and plant development. Plant Cell 20: 2102-2116.
5. Asami T, Min YK, Nagata N, Yamagishi K, Takatsuto S, Fujioka S, Murofushi N, Yamaguchi I, Yoshida S. 2000. Characterization of brassinazole, a triazole-type brassinosteroid biosynthesis inhibitor. Plant Physiol 123: 93-100.
6. Bartel DP. 2004. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 116: 281-297.
7. Baucher M, El Jaziri M, Vandeputte O. 2007. From primary to secondary growth: Origin and development of the vascular system. J Exp Bot 58: 3485-3501.
8. Benfey PN, Scheres B. 2000. Root development. Curr Biol 10: R813-R815.
9. Benjamins R, Quint A, Weijers D, Hooykaas P, Offringa R. 2001. The PINOID protein kinase regulates organ development in Arabidopsis by enhancing polar auxin transport. Development 128: 4057-4067.
10. Benkova E, Michniewicz M, Sauer M, Teichmann T, Seifertova D, Jurgens G, Friml J. 2003. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115: 591-602.
11. Berleth T, Mattsson J. 2000. Vascular development: Tracing signals along veins. Curr Opin Plant Biol 3: 406-411.
12. Bishopp A, Help H, El-Showk S, Weijers D, Scheres B, Friml J, Benkova E, Mahonen AP, Helariutta Y. 2011a. A mutually inhibitory interaction between auxin and cytokinin specifies vascular pattern in roots. Curr Biol 21: 917-926.
13. Bishopp A, Lehesranta S, Vaten A, Help H, El-Showk S, Scheres B, Helariutta K, Mahonen AP, Sakakibara H, Helariutta Y. 2011b. Phloem-transported cytokinin regulates polar auxin transport and maintains vascular pattern in the root meristem. Curr Biol 21: 927-932.
14. Bjorklund S, Antti H, Uddestrand I, Moritz T, Sundberg B. 2007. Cross-talk between gibberellin and auxin in development of Populus wood: Gibberellin stimulates polar auxin transport and has a common transcriptome with auxin. Plant J 52: 499-511.
15. Blakeslee JJ, Peer WA, Murphy AS. 2005. Auxin transport. Curr Opin Plant Biol 8: 494-500.
16. Bleckmann A, Weidtkamp-Peters S, Seidel CAM, Simon R. 2010. Stem cell signaling in arabidopsis requires CRN to localize CLV2 to the plasma membrane. Plant Physiol 152: 166-176.
17. Bonan GB. 2008. Forests and climate change: Forcings, feedbacks, and the climate benefits of forests. Science 320: 1444-1449.
18. Bonke M, Thitamadee S, Mahonen AP, Hauser MT, Helariutta Y. 2003. APL regulates vascular tissue identity in arabidopsis. Nature 426: 181-186.
19. Bowman JL, Eshed Y, Baum SF. 2002. Establishment of polarity in angiosperm lateral organs. Trends Genet 18: 134-141.
20. 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: 617-619.
21. Cano-Delgado A, Lee JY, Demura T. 2010. Regulatory mechanisms for specification and patterning of plant vascular tissues. Annu Rev Cell Dev Biol 26: 605-637.
22. Cano-Delgado A, Yin Y, Yu C, Vafeados D, Mora-Garcia S, Cheng JC, Nam KH, Li J, Chory J. 2004. BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development 131: 5341-5351.
23. Carland FM, Fujioka S, Nelson T. 2010. The sterol methyltransferases SMT1, SMT2, and SMT3 influence Arabidopsis development through nonbrassinosteroid products. Plant Physiol 153: 741-756.
24. Carland FM, Fujioka S, Takatsuto S, Yoshida S, Nelson T. 2002. The identification of CVP1 reveals a role for sterols in vascular patterning. Plant Cell 14: 2045-2058.
25. Carland FM, McHale NA. 1996. LOP1: A gene involved in auxin transport and vascular patterning in arabidopsis. Development 122: 1811-1819.
26. Carland FM, Nelson T. 2004. Cotyledon vascular pattern2-mediated inositol (1, 4, 5) triphosphate signal transduction is essential for closed venation patterns of arabidopsis foliar organs. Plant Cell 16: 1263-1275.
27. Carland FM, Nelson T. 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.
28. 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: 316-321.
29. Cheng Y, Dai X, Zhao Y. 2006. Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Genes Dev 20: 1790-1799.
30. Choe S, Noguchi T, Fujioka S, Takatsuto S, Tissier CP, Gregory BD, Ross AS, Tanaka A, Yoshida S, Tax FE, Feldmann KA. 1999. The Arabidopsis dwf7/ste1 mutant is defective in the delta7 sterol C-5 desaturation step leading to brassinosteroid biosynthesis. Plant Cell 11: 207-221.
31. Christensen SK, Dagenais N, Chory J, Weigel D. 2000. Regulation of auxin response by the protein kinase PINOID. Cell 100: 469-478.
32. Clark SE, Running MP, Meyerowitz EM. 1993. Clavata1, a regulator of meristem and flower development in arabidopsis. Development 119: 397-418.
33. 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: 575-585.
34. Clay NK, Nelson T. 2002. VH1, a provascular cell-specific receptor kinase that influences leaf cell patterns in arabidopsis. Plant Cell 14: 2707-2722.
35. Clay NK, Nelson T. 2005. Arabidopsis thickvein mutation affects vein thickness and organ vascularization, and resides in a provascular cell-specific spermine synthase involved in vein definition and in polar auxin transport. Plant Physiol 138: 767-777.
36. Clouse SD. 1996. Molecular genetic studies confirm the role of brassinosteroids in plant growth and development. Plant J 10: 1-8.
37. Cnops G, Neyt P, Raes J, Petrarulo M, Nelissen H, Malenica N, Luschnig C, Tietz O, Ditengou F, Palme K, Azmi A, Prinsen E, Van Lijsebettens M. 2006. The TORNADO1 and TORNADO2 genes function in several patterning processes during early leaf development in Arabidopsis thaliana. Plant Cell 18: 852-866.
38. Dalessan G. 1973. Hormonal-control of xylogenesis in pith parenchyma explants of lactuca. Ann Bot 37: 375-382.
39. 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: 594-597.
40. Demura T, Tashiro G, Horiguchi G, Kishimoto N, Kubo M, Matsuoka N, Minami A, Nagata-Hiwatashi M, Nakamura K, Okamura Y, Sassa N, Suzuki S, Yazaki J, Kikuchi S, Fukuda H. 2002. Visualization by comprehensive microarray analysis of gene expression programs during transdifferentiation of mesophyll cells into xylem cells. Proc Natl Acad Sci USA 99: 15794-15799.
41. Dettmer J, Elo A, Helariutta Y. 2009. Hormone interactions during vascular development. Plant Mol Biol 69: 347-360.
42. Dimitrov P, Zucker SW. 2006. A constant production hypothesis guides leaf venation patterning. Proc Natl Acad Sci USA 103: 9363-9368.
43. Donner TJ, Sherr I, Scarpella E. 2009. Regulation of preprocambial cell state acquisition by auxin signaling in arabidopsis leaves. Development 136: 3235-3246.
44. Elo A, Immanen J, Nieminen K, Helariutta Y. 2009. Stem cell function during plant vascular development. Semin Cell Dev Biol 20: 1097-1106.
45. 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: 1768-1774.
46. Esau K. 1977. Membranous modifications in sieve element plasids of spinach affected by the aster yellows disease. J Ultrastruct Res 59: 87-100.
47. 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.
48. Feugier FG, Mochizuki A, Iwasa Y. 2005. Self-organization of the vascular system in plant leaves: Inter-dependent dynamics of auxin flux and carrier proteins. J Theor Biol 236: 366-375.
49. Fiers M, Golemiec E, Xu J, van der Geest L, Heidstra R, Stiekema W, Liu CM. 2005. The 14-amino acid CLV3, CLE19, and CLE40 peptides trigger consumption of the root meristem in arabidopsis through a CLAVATA2-dependent pathway. Plant Cell 17: 2542-2553.
50. Fisher K, Turner S. 2007. PXY, a receptor-like kinase essential for maintaining polarity during plant vascular-tissue development. Curr Biol 17: 1061-1066.
51. Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM. 1999. Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283: 1911-1914.
52. Fosket DE, Torrey JG. 1969. Hormonal control of cell proliferation and xylem differentiation in cultured tissues of Glycine max var, Biloxi. Plant Physiol 44: 871-880.
53. Fukuda H. 2004. Signals that control plant vascular cell differentiation. Nat Rev Mol Cell Biol 5: 379-391.
54. Fukuda H, Higashiyama T. 2011. Diverse functions of plant peptides: Entering a new phase. Plant Cell Physiol 52: 1-4.
55. Fukuda H, Hirakawa Y, Sawa S. 2007. Peptide signaling in vascular development. Curr Opin Plant Biol 10: 477-482.
56. 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.
57. 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: 2226-2230.
58. Geldner N, Anders N, Wolters H, Keicher J, Kornberger W, Muller P, Delbarre A, Ueda T, Nakano A, Jurgens G. 2003. The arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112: 219-230.
59. Goldberg RB, de Paiva G, Yadegari R. 1994. Plant embryogenesis: Zygote to seed. Science 266: 605-614.
60. Grunewald W, Friml J. 2010. The march of the PINs: Developmental plasticity by dynamic polar targeting in plant cells. EMBO J 29: 2700-2714.
61. Hamann T, Benkova E, Baurle I, Kientz M, Jurgens G. 2002. The arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. Genes Dev 16: 1610-1615.
62. Hamann T, Mayer U, Jurgens G. 1999. The auxin-insensitive bodenlos mutation affects primary root formation and apical-basal patterning in the arabidopsis embryo. Development 126: 1387-1395.
63. Hanzawa Y, Takahashi T, Komeda Y. 1997. ACL5: An Arabidopsis gene required for internodal elongation after flowering. Plant J 12: 863-874.
64. Hanzawa Y, Takahashi T, Michael AJ, Burtin D, Long D, Pineiro M, Coupland G, Komeda Y. 2000. ACAULIS5, an arabidopsis gene required for stem elongation, encodes a spermine synthase. EMBO J 19: 4248-4256.
65. Hardtke CS, Berleth T. 1998. The arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J 17: 1405-1411.
66. Henmi K, Tsuboi S, Demura T, Fukuda H, Iwabuchi M, Ogawa KI. 2001. A possible role of glutathione and glutathione disulfide in tracheary element differentiation in the cultured mesophyll cells of Zinnia elegans. Plant Cell Physiol 42: 673-676.
67. Higuchi M, Pischke MS, Mahonen AP, Miyawaki K, Hashimoto Y, Seki M, Kobayashi M, Shinozaki K, Kato T, Tabata S, Helariutta Y, Sussman MR, Kakimoto T. 2004. In planta functions of the arabidopsis cytokinin receptor family. Proc Natl Acad Sci USA 101: 8821-8826.
68. Hirakawa Y, Kondo Y, Fukuda H. 2010. TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in arabidopsis. Plant Cell 22: 2618-2629.
69. 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: 15208-15213.
70. Hobbie L, McGovern M, Hurwitz LR, Pierro A, Liu NY, Bandyopadhyay A, Estelle M. 2000. The axr6 mutants of Arabidopsis thaliana define a gene involved in auxin response and early development. Development 127: 23-32.
71. Hosokawa M, Suzuki S, Umezawa T, Sato Y. 2001. Progress of lignification mediated by intercellular transportation of monolignols during tracheary element differentiation of isolated Zinnia mesophyll cells. Plant Cell Physiol 42: 959-968.
72. Hou H, Erickson J, Meservy J, Schultz EA. 2010. FORKED1 encodes a PH domain protein that is required for PIN1 localization in developing leaf veins. Plant J 63: 960-973.
73. Ibanes M, Fabregas N, Chory J, Cano-Delgado AI. 2009. Brassinosteroid signaling and auxin transport are required to establish the periodic pattern of Arabidopsis shoot vascular bundles. Proc Natl Acad Sci USA 106: 13630-13635.
74. 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: 975-984.
75. Imai A, Hanzawa Y, Komura M, Yamamoto KT, Komeda Y, Takahashi T. 2006. The dwarf phenotype of the Arabidopsis acl5 mutant is suppressed by a mutation in an upstream ORF of a bHLH gene. Development 133: 3575-3585.
76. Inoue T, Higuchi M, Hashimoto Y, Seki M, Kobayashi M, Kato T, Tabata S, Shinozaki K, Kakimoto T. 2001. Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature 409: 1060-1063.
77. Ishida K, Yamashino T, Yokoyama A, Mizuno T. 2008. Three type-B response regulators, ARR1, ARR10 and ARR12, play essential but redundant roles in cytokinin signal transduction throughout the life cycle of Arabidopsis thaliana. Plant Cell Physiol 49: 47-57.
78. Jacobs WP. 1952. The role of auxin in differentiation of xylem around a wound. Am J Bot 39: 301-309.
79. Jenik PD, Barton MK. 2005. Surge and destroy: The role of auxin in plant embryogenesis. Development 132: 3577-3585.
80. Jeong S, Trotochaud AE, Clark SE. 1999. The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase. Plant Cell 11: 1925-1934.
81. Junghans U, Langenfeld-Heyser R, Polle A, Teichmann T. 2004. Effect of auxin transport inhibitors and ethylene on the wood anatomy of poplar. Plant Biol (Stuttg) 6: 22-29.
82. Kakehi J-I, Kuwashiro Y, Motose H, Igarashi K, Takahashi T. 2010. Norspermine substitutes for thermospermine in the control of stem elongation in Arabidopsis thaliana. FEBS Lett 584: 3042-3046.
83. Kakehi J-I, Kuwashiro Y, Niitsu M, Takahashi T. 2008. Thermospermine is required for stem elongation in Arabidopsis thaliana. Plant Cell Physiol 49: 1342-1349.
84. Kaplan DR, Cooke TJ. 1997. Fundamental concepts in the embryogenesis of dicotyledons: A morphological interpretation of embryo mutants. Plant Cell 9: 1903-1919.
85. Kim J, Jung JH, Reyes JL, Kim YS, Kim SY, Chung KS, Kim JA, Lee M, Lee Y, Narry Kim V, Chua NH, Park CM. 2005. microRNA-directed cleavage of ATHB15 mRNA regulates vascular development in Arabidopsis inflorescence stems. Plant J 42: 84-94.
86. Kleine-Vehn J, Huang F, Naramoto S, Zhang J, Michniewicz M, Offringa R, Friml J. 2009. PIN auxin efflux carrier polarity is regulated by PINOID kinase-mediated recruitment into GNOM-independent trafficking in Arabidopsis. Plant Cell 21: 3839-3849.
87. Knott JM, Romer P, Sumper M. 2007. Putative spermine synthases from Thalassiosira pseudonana and Arabidopsis thaliana synthesize thermospermine rather than spermine. FEBS Lett 581: 3081-3086.
88. Koizumi K, Naramoto S, Sawa S, Yahara N, Ueda T, Nakano A, Sugiyama M, Fukuda H. 2005. VAN3 ARF-GAP-mediated vesicle transport is involved in leaf vascular network formation. Development 132: 1699-1711.
89. Koizumi K, Sugiyama M, Fukuda H. 2000. A series of novel mutants of Arabidopsis thaliana that are defective in the formation of continuous vascular network: Calling the auxin signal flow canalization hypothesis into question. Development 127: 3197-3204.
90. Kondo Y, Hirakawa Y, Kieber JJ, Fukuda H. 2011. CLE peptides can negatively regulate protoxylem vessel formation via cytokinin signaling. Plant Cell Physiol 52: 37-48.
91. Kubo M, Udagawa M, Nishikubo N, Horiguchi G, Yamaguchi M, Ito J, Mimura T, Fukuda H, Demura T. 2005. Transcription switches for protoxylem and metaxylem vessel formation. Genes Dev 19: 1855-1860.
92. Kuroha T, Tokunaga H, Kojima M, Ueda N, Ishida T, Nagawa S, Fukuda H, Sugimoto K, Sakakibara H. 2009. Functional analyses of LONELY GUY cytokinin-activating enzymes reveal the importance of the direct activation pathway in Arabidopsis. Plant Cell 21: 3152-3169.
93. Laux T. 2003. The stem cell concept in plants: A matter of debate. Cell 113: 281-283.
94. Laux T, Mayer KF, Berger J, Jurgens G. 1996. The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122: 87-96.
95. Love J, Bjorklund S, Vahala J, Hertzberg M, Kangasjarvi J, Sundberg B. 2009. Ethylene is an endogenous stimulator of cell division in the cambial meristem of Populus. Proc Natl Acad Sci USA 106: 5984-5989.
96. Mahonen AP, Bishopp A, Higuchi M, Nieminen KM, Kinoshita K, Tormakangas K, Ikeda Y, Oka A, Kakimoto T, Helariutta Y. 2006. Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development. Science 311: 94-98.
97. Mahonen AP, Bonke M, Kauppinen L, Riikonen M, Benfey PN, Helariutta Y. 2000. A novel two-component hybrid molecule regulates vascular morphogenesis of the Arabidopsis root. Genes Dev 14: 2938-2943.
98. Mallory AC, Reinhart BJ, Jones-Rhoades MW, Tang G, Zamore PD, Barton MK, Bartel DP. 2004. MicroRNA control of PHABULOSA in leaf development: Importance of pairing to the microRNA 5' region. EMBO J 23: 3356-3364.
99. Mallory AC, Vaucheret H. 2006. Functions of microRNAs and related small RNAs in plants. Nat Genet 38 Suppl: S31-S36.
100. Matsumoto-Kitano M, Kusumoto T, Tarkowski P, Kinoshita-Tsujimura K, Vaclavikova K, Miyawaki K, Kakimoto T. 2008. Cytokinins are central regulators of cambial activity. Proc Natl Acad Sci USA 105: 20027-20031.
101. Mattsson J, Sung ZR, Berleth T. 1999. Responses of plant vascular systems to auxin transport inhibition. Development 126: 2979-2991.
102. 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: 805-815.
103. McCarthy RL, Zhong R, Ye Z-H. 2009. MYB83 is a direct target of SND1 and acts redundantly with MYB46 in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell Physiol 50: 1950-1964.
104. McHale NA, Koning RE. 2004. MicroRNA-directed cleavage of Nicotiana sylvestris PHAVOLUTA mRNA regulates the vascular cambium and structure of apical meristems. Plant Cell 16: 1730-1740.
105. Men S, Boutte Y, Ikeda Y, Li X, Palme K, Stierhof Y-D, Hartmann M-A, Moritz T, Grebe M. 2008. Sterol-dependent endocytosis mediates post-cytokinetic acquisition of PIN2 auxin efflux carrier polarity. Nat Cell Biol 10: 237-244.
106. Michniewicz M, Zago MK, Abas L, Weijers D, Schweighofer A, Meskiene I, Heisler MG, Ohno C, Zhang J, Huang F, Schwab R, Weigel D, Meyerowitz EM, Luschnig C, Offringa R, Friml J. 2007. Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell 130: 1044-1056.
107. Mitchison GJ. 1980. A model for vein formation in higher plants. Proc R Soc Lond B 207: 79-109.
108. Mitchison GJ. 1981. The polar transport of auxin and vein patterns in plants. Phil Trans R Soc Lond B 295: 461-471.
109. Mittler R, Lam E. 1995. In situ detection of nDNA fragmentation during the differentiation of tracheary elements in higher plants. Plant Physiol 108: 489-493.
110. Miyashima S, Koi S, Hashimoto T, Nakajima K. 2011. Non-cell-autonomous microRNA165 acts in a dose-dependent manner to regulate multiple differentiation status in the Arabidopsis root. Development 138: 2303-2313.
111. Miyawaki K, Tarkowski P, Matsumoto-Kitano M, Kato T, Sato S, Tarkowska D, Tabata S, Sandberg G, Kakimoto T. 2006. Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis. Proc Natl Acad Sci USA 103: 16598-16603.
112. Mockaitis K, Estelle M. 2008. Auxin receptors and plant development: A new signaling paradigm. Annu Rev Cell Dev Biol 24: 55-80.
113. Mori M, Nomura T, Ooka H, Ishizaka M, Yokota T, Sugimoto K, Okabe K, Kajiwara H, Satoh K, Yamamoto K, Hirochika H, Kikuchi S. 2002. Isolation and characterization of a rice dwarf mutant with a defect in brassinosteroid biosynthesis. Plant Physiol 130: 1152-1161.
114. Motose H, Sugiyama M, Fukuda H. 2004. A proteoglycan mediates inductive interaction during plant vascular development. Nature 429: 873-878.
115. Moyle R, Schrader J, Stenberg A, Olsson O, Saxena S, Sandberg G, Bhalerao RP. 2002. Environmental and auxin regulation of wood formation involves members of the Aux/IAA gene family in hybrid aspen. Plant J 31: 675-685.
116. Muday GK, DeLong A. 2001. Polar auxin transport: Controlling where and how much. Trends Plant Sci 6: 535-542.
117. Muller B, Sheen J. 2007a. Advances in cytokinin signaling. Science 318: 68-69.
118. Muller B, Sheen J. 2007b. Arabidopsis cytokinin signaling pathway. Sci STKE 2007: cm5.
119. Muller R, Bleckmann A, Simon R. 2008. The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell 20: 934-946.
120. Muniz L, Minguet EG, Singh SK, Pesquet E, Vera-Sirera F, Moreau-Courtois CL, Carbonell J, Blazquez MA, Tuominen H. 2008. ACAULIS5 controls Arabidopsis xylem specification through the prevention of premature cell death. Development 135: 2573-2582.
121. Nakajima K, Sena G, Nawy T, Benfey PN. 2001. Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413: 307-311.
122. Naramoto S, Sawa S, Koizumi K, Uemura T, Ueda T, Friml J, Nakano A, Fukuda H. 2009. Phosphoinositide-dependent regulation of VAN3 ARF-GAP localization and activity essential for vascular tissue continuity in plants. Development 136: 1529-1538.
123. Nemhauser JL, Mockler TC, Chory J. 2004. Interdependency of brassinosteroid and auxin signaling in Arabidopsis. PLoS Biol 2: E258.
124. Nieminen K, Immanen J, Laxell M, Kauppinen L, Tarkowski P, Dolezal K, Tahtiharju S, Elo A, Decourteix M, Ljung K, Bhalerao R, Keinonen K, Albert VA, Helariutta Y. 2008. Cytokinin signaling regulates cambial development in poplar. Proc Natl Acad Sci USA 105: 20032-20037.
125. Niklas KJ, Tiffney BH, Knoll AH. 1985. Patterns in vascular land plant diversification: An analysis at the species level. In: Valentine JW, editor. Phanerozoic diversity patterns: Patterns in macroevolution. Princeton, NJ: Princeton University Press. pp 97-128.
126. 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: 843-855.
127. Nishimura C, Ohashi Y, Sato S, Kato T, Tabata S, Ueguchi C. 2004. Histidine kinase homologs that act as cytokinin receptors possess overlapping functions in the regulation of shoot and root growth in Arabidopsis. Plant Cell 16: 1365-1377.
128. Ogawa M, Shinohara H, Sakagami Y, Matsubayashi Y. 2008. Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319: 294.
129. Ohashi-Ito K, Fukuda H. 2010. Transcriptional regulation of vascular cell fates. Curr Opin Plant Biol 13: 670-676.
130. Oparka KJ, Turgeon R. 1999. Sieve elements and companion cells-traffic control centers of the phloem. Plant Cell 11: 739-750.
131. Ponting CP, Aravind L. 1999. START: A lipid-binding domain in StAR, HD-ZIP and signalling proteins. Trends Biochem Sci 24: 130-132.
132. Pullen M, Clark N, Zarinkamar F, Topping J, Lindsey K. 2010. Analysis of vascular development in the hydra sterol biosynthetic mutants of Arabidopsis. PLoS ONE 5: e12227.
133. Pyo H, Demura T, Fukuda H. 2007. TERE: A novel cis-element responsible for a coordinated expression of genes related to programmed cell death and secondary wall formation during differentiation of tracheary elements. Plant J 51: 955-965.
134. Ragni L, Nieminen K, Pacheco-Villalobos D, Sibout R, Schwechheimer C, Hardtke CS. 2011. Mobile gibberellin directly stimulates arabidopsis hypocotyl xylem expansion. Plant Cell 23: 1322-1336.
135. Replogle A, Wang J, Bleckmann A, Hussey RS, Baum TJ, Sawa S, Davis EL, Wang X, Simon R, Mitchum MG. 2011. Nematode CLE signaling in Arabidopsis requires CLAVATA2 and CORYNE. Plant J 65: 430-440.
136. Robles P, Fleury D, Candela H, Cnops G, Alonso-Peral MM, Anami S, Falcone A, Caldana C, Willmitzer L, Ponce MR, Van Lijsebettens M, Micol JL. 2010. The RON1/FRY1/SAL1 gene is required for leaf morphogenesis and venation patterning in Arabidopsis. Plant Physiol 152: 1357-1372.
137. Rolland-Lagan AG, Prusinkiewicz P. 2005. Reviewing models of auxin canalization in the context of leaf vein pattern formation in Arabidopsis. Plant J 44: 854-865.
138. Sachs T. 1981. The control of the patterned differentiation of vascular tissues. In: Woolhouse HW, editor. Advances in botanical research. London: Academic Press. pp 151-262.
139. Sachs T. 1991. Cell polarity and tissue patterning in plants. Development 113: 83-93.
140. Scarpella E, Helariutta Y. 2010. Vascular pattern formation in plants. Curr Top Dev Biol 91: 221-265.
141. Scarpella E, Marcos D, Friml J, Berleth T. 2006. Control of leaf vascular patterning by polar auxin transport. Genes Dev 20: 1015-1027.
142. Scheres B, DiLaurenzio L, Willemsen V, Hauser MT, Janmaat K, Weisbeek P, Benfey PN. 1995. Mutations affecting the radial organization of the Arabidopsis root display specific defects throughout the radial axis. Development 121: 53-62.
143. Scheres B, McKhann H, van den Berg C, Willemsen V, Wolkenfelt H, de Vrieze G, Weisbeek P. 1996. Experimental and genetic analysis of root development in Arabidopsis thaliana. Plant Soil 111: 959-964.
144. Schlereth A, Moller B, Liu W, Kientz M, Flipse J, Rademacher EH, Schmid M, Jurgens G, Weijers D. 2010. MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 464: 913-916.
145. 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: 635-644.
146. Schrader J, Baba K, May ST, Palme K, Bennett M, Bhalerao RP, Sandberg G. 2003. Polar auxin transport in the wood-forming tissues of hybrid aspen is under simultaneous control of developmental and environmental signals. Proc Natl Acad Sci USA 100: 10096-10101.
147. Schrick K, Fujioka S, Takatsuto S, Stierhof YD, Stransky H, Yoshida S, Jurgens G. 2004. A link between sterol biosynthesis, the cell wall, and cellulose in Arabidopsis. Plant J 38: 227-243.
148. Sieburth LE, Deyholos MK. 2006. Vascular development: The long and winding road. Curr Opin Plant Biol 9: 48-54.
149. Sieburth LE, Muday GK, King EJ, Benton G, Kim S, Metcalf KE, Meyers L, Seamen E, Van Norman JM. 2006. SCARFACE encodes an ARF-GAP that is required for normal auxin efflux and vein patterning in Arabidopsis. Plant Cell 18: 1396-1411.
150. Sorefan K, Girin T, Liljegren SJ, Ljung K, Robles P, Galvan-Ampudia CS, Offringa R, Friml J, Yanofsky MF, Ostergaard L. 2009. A regulated auxin minimum is required for seed dispersal in Arabidopsis. Nature 459: 583-586.
151. Soyano T, Thitamadee S, Machida Y, Chua NH. 2008. Asymmetric leaves2-like19/lateral organ boundaries domain30 and ASL20/LBD18 regulate tracheary element differentiation in Arabidopsis. Plant Cell 20: 3359-3373.
152. Spicer R, Groover A. 2010. Evolution of development of vascular cambia and secondary growth. New Phytol 186: 577-592.
153. Stahl Y, Wink RH, Ingram GC, Simon R. 2009. A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr Biol 19: 909-914.
154. Stewart JL, Nemhauser JL. 2010. Do trees grow on money? Auxin as the currency of the cellular economy. Cold Spring Harb Perspect Biol 2: a001420.
155. Stewart RN, Dermen H. 1975. Flexibility in ontogeny as shown by the contribution of the shoot apical layers to the leaves of periclinal chimaeras. Am J Bot 62: 935-947.
156. Steynen QJ, Schultz EA. 2003. The FORKED genes are essential for distal vein meeting in Arabidopsis. Development 130: 4695-4708.
157. Szekeres M, Nemeth K, Koncz-Kalman Z, Mathur J, Kauschmann A, Altmann T, Redei GP, Nagy F, Schell J, Koncz C. 1996. Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis. Cell 85: 171-182.
158. Takahashi T, Kakehi J. 2010. Polyamines: Ubiquitous polycations with unique roles in growth and stress responses. Ann Bot 105: 1-6.
159. Teale WD, Paponov IA, Palme K. 2006. Auxin in action: signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 7: 847-859.
160. Telewski FW, Jaffe MJ. 1986. Thigmomorphogenesis: The role of ethylene in the response of Pinus taeda and Abies fraseri to mechanical perturbation. Plant Physiol 66: 227-233.
161. Tor M, Lotze MT, Holton N. 2009. Receptor-mediated signalling in plants: Molecular patterns and programmes. J Exp Bot 60: 3645-3654.
162. Trotochaud AE, Jeong S, Clark SE. 2000. CLAVATA3, a multimeric ligand for the CLAVATA1 receptor-kinase. Science 289: 613-617.
163. Turner S, Gallois P, Brown D. 2007. Tracheary element differentiation. Annu Rev Plant Biol 58: 407-433.
164. Vera-Sirera F, Minguet EG, Singh SK, Ljung K, Tuominen H, Blazquez MA, Carbonell J. 2010. Role of polyamines in plant vascular development. Plant Physiol Biochem 48: 534-539.
165. Wang Q, Little CH, Oden PC. 1997. Control of longitudinal and cambial growth by gibberellins and indole-3-acetic acid in current-year shoots of Pinus sylvestris. Tree Physiol 17: 715-721.
166. Werner T, Motyka V, Strnad M, Schmulling T. 2001. Regulation of plant growth by cytokinin. Proc Natl Acad Sci USA 98: 10487-10492.
167. West AH, Stock AM. 2001. Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem Sci 26: 369-376.
168. Willemsen V, Friml J, Grebe M, van den Toorn A, Palme K, Scheres B. 2003. Cell polarity and PIN protein positioning in Arabidopsis require sterol methyltransferase 1 function. Plant Cell 15: 612-625.
169. Willmann MR, Poethig RS. 2007. Conservation and evolution of miRNA regulatory programs in plant development. Curr Opin Plant Biol 10: 503-511.
170. Wilson K, White DJB. 1986. The anatomy of wood: Its diversity and variability. London: Stobart & Son.
171. Yamaguchi M, Goue N, Igarashi H, Ohtani M, Nakano Y, Mortimer JC, Nishikubo N, Kubo M, Katayama Y, Kakegawa K, Dupree P, Demura T. 2010a. vascular-related nac-domain6 and vascular-related nac-domain7 effectively induce transdifferentiation into xylem vessel elements under control of an induction system. Plant Physiol 153: 906-914.
172. Yamaguchi M, Ohtani M, Mitsuda N, Kubo M, Ohme-Takagi M, Fukuda H, Demura T. 2010b. VND-INTERACTING2, a NAC domain transcription factor, negatively regulates xylem vessel formation in Arabidopsis. Plant Cell 22: 1249-1263.
173. Yamamoto R, Demura T, Fukuda H. 1997. Brassinosteroids induce entry into the final stage of tracheary element differentiation in cultured Zinnia cells. Plant Cell Physiol 38: 980-983.
174. Yamamoto R, Fujioka S, Iwamoto K, Demura T, Takatsuto S, Yoshida S, Fukuda H. 2007. Co-regulation of brassinosteroid biosynthesis-related genes during xylem cell differentiation. Plant Cell Physiol 48: 74-83.
175. Ye ZH, Varner JE. 1993. Gene expression patterns associated with in vitro tracheary element formation in isolated single mesophyll cells of Zinnia elegans. Plant Physiol 103: 805-813.
176. Yordanov YS, Regan S, Busov V. 2010. Members of the lateral organ boundaries domain transcription factor family are involved in the regulation of secondary growth in populus. Plant Cell 22: 3662-3677.
177. Zhao Y. 2010. Auxin biosynthesis and its role in plant development. Annu Rev Plant Biol 61: 49-64.
178. Zhong R, Lee C, Zhou J, McCarthy RL, Ye Z-H. 2008. A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell 20: 2763-2782.
179. Zhong R, Richardson EA, Ye ZH. 2007. The MYB46 transcription factor is a direct target of SND1 and regulates secondary wall biosynthesis in Arabidopsis. Plant Cell 19: 2776-2792.
180. Zhong R, Ye ZH. 1999. IFL1, a gene regulating interfascicular fiber differentiation in Arabidopsis, encodes a homeodomain-leucine zipper protein. Plant Cell 11: 2139-2152.
181. Zhong R, Ye ZH. 2001. Alteration of auxin polar transport in the Arabidopsis ifl1 mutants. Plant Physiol 126: 549-563.
182. Zhou J, Lee C, Zhong R, Ye ZH. 2009. MYB58 and MYB63 are transcriptional activators of the lignin biosynthetic pathway during secondary cell wall formation in Arabidopsis. Plant Cell 21: 248-266.