Signals that control plant vascular cell differentiation

Nature Reviews Molecular Cell Biology

Volumn 5, Issue 5, 2004, Pages 379-391

  Fukuda, Hiroo ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AUXIN; BRASSINOSTEROID; CYTOKININ; GENE PRODUCT; UNCLASSIFIED DRUG; XYLOGEN;

APOPTOSIS; ARABIDOPSIS; CELL CULTURE; CELL DIFFERENTIATION; CELL MATURATION; CELL POLARITY; GENE EXPRESSION; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; NONHUMAN; PLANT CELL; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; TRANSPORT KINETICS; VASCULAR TISSUE; ZINNIA ELEGANS;

ARABIDOPSIS; BIOLOGICAL TRANSPORT; BODY PATTERNING; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL POLARITY; INDOLEACETIC ACIDS; PLANT LEAVES; PLANT PHYSIOLOGY;

ARABIDOPSIS; ARABIDOPSIS THALIANA; ZINNIA; ZINNIA ELEGANS;

EID: 2342539842     PISSN: 14710072     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrm1364     Document Type: Review

References (120)

1. Ye, Z.-H. Vascular tissue differentiation and pattern formation in plants. Annu. Rev. Plant Biol. 53, 183-202 (2002).
2. Dengler, N. & Kang, J. Vascular patterning and leaf shape. Curr. Opin. Plant Biol. 4. 50-56 (2001).
3. Jacobs, W. P. The role of auxin in differentiation of xylem around a wound. Am. J. Bot. 39, 301-309 (1952).
4. Sachs, T. The control of the patterned differentiation of vascular tissues. Adv. Bot. Res. 9, 152-262 (1981).
5. Sachs, T. Integrating cellular and organismic aspects of vascular differentiation. Plant Cell Physiol. 41, 649-656 (2000).
6. Mattsson, J., Sung, Z. R. & Berieth, T. Responses of plant vascular systems to auxin transport inhibition. Development 126, 2979-2991 (1999).
7. Sieburth, L. E. Auxin is required for leaf vein pattern in Arabidopsis. Plant Physiol. 121, 1179-1190 (1999).
8. Berleth, T., Mattsson, K. & Hardtke, C. S. Vascular continuity and auxin signals. Trends Plant Sci. 5, 387-393 (2000). This review summarizes the role of polar auxin flow in vascular continuity on the basis of results with mutants and inhibitors of auxin transport.
9. Okada, K., Ueda, J., Komaki, M. K., Bell, C. J. & Shimura, Y. Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell 3, 677-684 (1991).
10. Gälweller, L. et al. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282, 2226-2230 (1998). This paper shows evidence that AtPIN1 is located on the base of vascular cells and functions in polar auxin transport.
11. Uggla, C., Moritz, T., Sandberg, G. & Sundberg, B. Auxin as a positional signal in pattern formation in plants. Proc. Natl Acad. Sci. USA 93, 9282-9286 (1996). This paper shows that cambial cells have the highest concentration of IAA among vascular cells.
12. Steinmann, T. et al. Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science 286, 316-318 (1999).
13. Geldner, N. et al. The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112, 219-230 (2003). This paper presents a model in which endosomal recycling that is regulated by GNOM ADP-ribosylation-factor-guanine-nucleotide-exchange factor functions in the asymmetrical transport of AtPIN1, leading to polar auxin transport.
14. Koizumi, K., Sugiyama, M. & Fukuda, H. 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 (2000).
15. Bennett, S. R. M., Alvarez, J., Bossinger, G. & Smyth, D. R. Morphogenesis in pinoid mutants of Arabidopsis thaliana. Plant J. 8, 505-520 (1995).
16. Benjamins, R., Quint, A., Weijers, D., Hooykaas, P. & Offringa, R. The PINOID protein kinase regulates organ development in Arabidopsis by enhancing polar auxin transport. Development 128, 4057-4067 (2001).
17. Muday, G. K. & Murphy, A. S. An emerging model of auxin transport regulation. Plant Cell 14, 293-299 (2002).
18. Baumann, C. A. & Saltiel, A. R. Spatial compartmentalization of signal transduction in insulin action. Bioessays 23, 215-222 (2001).
19. Simpson, F. Whitehead, J. P. & James, D. E. GLUT4: at the cross roads between membrane trafficking and signal transduction. Traffic 2, 2-11 (2001).
20. Swarup, R. et al. Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. Genes Dev. 15, 2648-2653 (2001).
21. Demura, T. et al. 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 (2002). This paper, together with reference 96, provides a comprehensive analysis of gene expression during xylem cell differentiation.
22. Hobbie, L. et al. The axr6 mutants of Arabidopsis thaliana define a gene involved in auxin response and early development. Development 127, 23-32 (2000).
23. Hamann, T., Mayer, U. & Jürgens, G. The auxin-insensitive bodenlos mutation affects primary root formation and apical-basal patterning in the Arabidopsis embryo. Development 126, 1387-1395 (1999).
24. Hardtke, C. S. & Berleth, T. The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J. 17, 1405-1411 (1998).
25. Ulmasov, T., Hagen, G. & Guilfoyle, T. J. Activation and repression of transcription by auxin-response factors. Proc. Natl Acad. Sci. USA 96, 5844-5849 (1999).
26. Berleth, T. & Jürgens, G. The role of the monopteros gene in organising the basal body region of the Arabidopsis embryo. Development 118, 575-587 (1993).
27. Przemeck, G. K., Mattsson, J., Hardtke, C. S., Sung, Z. R. & Berleth, T. Studies on the role of the Arabidopsis gene MONOPTEROS in vascular development and plant cell axialization. Planta 200, 229-237 (1996).
28. Hellmann, H. & Estelle, M. Plant development regulation by protein degradation. Science 297, 793-797 (2002).
29. Groover, A. T., Pattishall, A. & Jones, A. M. IAA8 expression during vascular cell differentiation. Plant Mol. Biol. 51, 427-435 (2003).
30. Carland, F. M. & McHale, N. A. LOP1: a gene involved in auxin transport and vascular patterning in Arabidopsis. Development 122, 1811-1819 (1996).
31. Carland, F. M., Berg, B. L., FitzGerald, J. N. & Jinamomphongs, S. Genetic regulation of vascular tissue patterning in Arabidopsis. Plant Cell 11, 2123-2137 (1999).
32. Deyholos, M. K., Cordner, G., Beebe, D. & Sieburth, L. E. The SCARFACE gene is required for cotyledon and leaf vein patterning. Development 127, 3205-3213 (2000).
33. Aloni, R. Foliar and axial aspects of vascular differentiation: hypotheses and evidence. J. Plant Growth Reg. 20, 22-34 (2001).
34. Meinhardt, H. Models of biological pattern formation: common mechanism in plant and animal development. Int. J. Dev. Biol. 40, 123-134 (1996).
35. Nelson, T. & Dengler, N. Leaf vascular pattern formation. Plant Cell 9, 1121-1135 (1997).
36. Asai, R., Taguchi, E., Kume, Y., Saito, M. & Kondo, S. Zebrafish Leopard gene as a component of tha putative reaction-diffusion system. Mech. Dev. 89, 87-92 (1999).
37. Parker, G., Schofield, R., Sundberg, B. & Turner, S. Isolation of COV1, a gene involved in the regulation of vascular patterning in the stem of Arabidopsis. Development 130, 2139-2148 (2003).
38. Waites, R., Selvadurai, H. R. N., Oliver, I. R. & Hudson, A. The PHANTASTICA gene encodes a MYB transcription factor involved in growth and dorsoventrality of lateral organs in Antirrhinum. Cell 93, 779-789 (1998).
39. Waites, R. & Hudson, A. phantastica: a gene required for dorsoventrality of leaves in Antirrhinum majus. Development 121, 2143-2154 (1995).
40. McConnell, J. R. et al. Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411, 709-713 (2001).
41. McConnell, J. R. & Barton, M. K. Leaf polarity and meristem formation in Arabidopsis. Development 125, 2935-2942 (1998).
42. Emery, J. F. et al. Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr. Biol. 13, 1768-1774 (2003). Based on complementary vascular phenotypes of HD-ZIP-III and KANADI mutants, this paper proposes that a genetic programme that is dependent on miRNA controls the radial patterning of vascular bundles as well as shoots.
43. Sawa, S. et al. FILAMENTOUS FLOWER, a meristem and organ identity gene of Arabidopsis, encodes a protein with a zinc finger and HMG-related domains. Genes Dev. 13, 1079-1088 (1999).
44. Siegfried, K. R. et al. Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development 126, 4117-4128 (1999).
45. Eshed, Y., Baum, S. F., Perea, J. V. & Bowman, J. L. Establishment of polarity in lateral organs of plants. Curr. Biol. 11, 1251-1260 (2001).
46. Kerstetter, R. A., Bollman, K., Taylor, R. A., Bomblies, K. & Poethig, R. S. KANADI regulates organ polarity in Arabidopsis. Nature 411, 706-709 (2001).
47. Eshed, Y., Baum, S. F. & Bowman, J. L. Distinct mechanisms promote polarity establishment in carpels of Arabidopsis. Cell 99, 199-209 (1999).
48. Bonke, M., Thitamadee, S., Mähönen, A. P., Hauser, M.-T. & Helariutta, Y. APL regulates vascular tissue identity in Arabidopsis. Nature 426, 181-186 (2003).
49. Scheres, B. et al. Mutants affecting the radial organisation of the Arabidoposis root display specific defects throughout the embryonic axis. Development 121, 53-62 (1995).
50. Mähönen, A. P. et al. A novel two-component hybrid molecule regulates vascular marphogenesis of the Arabidopsis root. Genes Dev. 14, 2938-2943 (2000). This paper shows the involvement of cytokinin in the formation and maintenance of the procambium.
51. Yamada, H. et al. The Arabidopsis AHK4 histidine kinase is a cytokinin-binding receptor that transduces cytokinin signals across the membrane. Plant Cell Physiol. 42, 1017-1023 (2001).
52. Suzuki, T., Ishikawa, K., Yamashino, T. & Mizuno, T. An Arabidopsis histidine-containing phosphotransfer (HPt) factor implicated in phosphorelay signal transduction: overexpression of AHP2 in plants results in hypersensitiveness to cytokinin. Plant Cell Physiol. 43, 123-129 (2002).
53. Hwang, I. & Sheen, J. Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature 413, 383-389 (2001).
54. Sakai, H. et al. ARR1, a transcription factor for genes immediately responsive to cytokinins. Science 294, 1519-1521 (2001).
55. Kiba, T. et al. The type-A response regulator, ARR15, acts as a negative regulator in the cytokinin-mediated signal transduction in Arabidopsis thaliana. Plant Cell Physiol. 44, 868-874 (2003).
56. Kakimoto, T. Identification of plant cytokinin biosynthetic enzymes as dimethylallyl diphosphate:ATP/ADP isopentenyltransferases. Plant Cell Physiol. 42, 677-685 (2001).
57. Takei, K., Sakakibara, H. & Sugiyama, T. Identification of genes encoding adenylate isopentenyltransferase, a cytokinin biosynthesis enzyme, in Arabidopsis thaliana. J. Biol. Chem. 276, 26405-26410 (2001).
58. Miyawaki, K., Matsumoto-Kitano, M. & Kakimoto, T. Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin, cytokinin, and nitrate. Plant J. 37, 128-138 (2004).
59. Fukuda, H. Tracheary element differentiation. Plant Cell 9, 1147-1156 (1997). This review summarizes the process of transdifferentiation from mesophyll cells into xylem cells.
60. Baima, S. et al. The expression of the Athb-8 homeobox gene is restricted to provascular cells in Arabidopsis thaliana. Development 121, 4171-4182 (1995). This is the first paper to show vascular-precursor-cell-specific expression of a member of the HD-ZIP-III gene family.
61. Ohashi-Ito, K. & Fukuda, H. HD-Zip III homeobox genes that include a novel member, ZeHB-13 (Zinnia)/AtHB-15 (Arabidopsis), are involved in xylem pattern formation. Plant Cell Physiol. 44, 1350-1358 (2003).
62. Ohashi-Ito, K., Demura, T. & Fukura, H. Promotion of transcript accumulation of novel Zinnia immature xylem-specific HD-ZIP III homeobox genes by brassinosteroids. Plant Cell Physiol. 43, 1146-1153 (2002).
63. Zhong, R., Taylor, J. J. & Ye, Z.-H. Disruption of interfascicular fiber differentiation in an Arabidopsis mutant. Plant Cell 9, 2159-2170 (1997).
64. Zhong, R. & Ye, Z.-H. IFL1, a gene regulating interfascicular fiber differentiation in Arabidopsis, encodes a homeodomain-leucine zipper protein. Plant Cell 11, 2139-2152 (1999).
65. Otsuga, D., DeGuzman, B., Prigge, M. J., Drews, G. N. & Clark, S. E. REVOLUTA regulates meristem initiation at lateral positions. Plant J. 25, 223-236 (2001).
66. Baima, S. et al. The Arabidopsis ATHB-8 HD-Zip protein acts as a differentiation-promoting transcription factor of the vascular meristems. Plant Physiol. 126, 643-655 (2001).
67. Rhoades, M. W. et al. Prediction of plant microRNA targets. Cell 110, 513-520 (2002).
68. Tang, G., Reinhart, B. J., Bartel, D. P. & Zamore, P. D. A biochemical framework for RNA silencing in plants. Genes Dev. 17, 49-63 (2003).
69. Reinhart, B. J., Weinstein, E. G., Rhoades, M. W., Bartel, B. & Bartel, D. P. MicroRNAs in plants. Genes Dev. 16, 1616-1626 (2002).
70. Bohmert, K. et al. AGO1 defines a novel locus of Arabidopsis controlling leaf development. EMBO J. 17, 170-180 (1998).
71. Lynn, K. et al. The PINHEAD/ZWILLE gene acts pleiotropically in Arabidopsis development and has overlapping functions with the ARGONAUTE1 gene. Development 126, 469-481 (1999).
72. Choe, S. et al. The Arabidopsis dwf7/ste1 mutant is defective in the δ7 sterol C-5 desaturation step leading to brassinosteroid biosynthesis. Plant Cell 11, 207-221 (1999).
73. Szekeres, M. et al. Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis. Cell 85, 171-182 (1996).
74. Asami, T. & Yoshida, S. Brassinosteroid biosynthesis inhibitors. Trends Plant Sci. 4, 348-353 (1999).
75. Nagata, N., Asami, T. & Yoshida, S. Brassinazole, an inhibitor of brassinosteroid biosynthesis, inhibits development of secondary xylem in cress plants (Lepidium sativum). Plant Cell Physiol. 42, 1006-1011 (2001).
76. Iwasaki, T. & Shibaoka, H. Brassinosteroids act as regulators of tracheary-element differentiation in isolated Zinnia mesophyll cells. Plant Cell Physiol. 32, 1007-1014 (1991).
77. Yamamoto, R. et al. Brassinosteroid levels increase drastically prior to morphogenesis of tracheary elements. Plant Physiol. 125, 556-563 (2001).
78. Yamamoto, R., Demura, T. & Fukuda, H. Brassinosteroids induce entry into the final stage of tracheary element differentiation in cultured Zinnia cells. Plant Cell Physiol. 38, 980-983 (1997). This paper shows that endogenous BRs are involved in the initiation of the last step of xylem cell differentiation.
79. Wang, Z.-Y., Seto, H., Fujioka, S., Yoshida, S. & Chory, J. BRI1 is a cntica critical component of a plasma-membrane receptor for plant steroids. Nature 410, 380-383 (2001).
80. Li, J. & Chory, J. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signaling transduction. Cell 90, 929-938 (1997).
81. Friedrichsen, D. M., Joazeiro, C. A., Li, J., Hunter, T. & Chory, J. Brassinosteroid-insensitive-1 is a ubiquitously expressed leucine-rich repeat receptor serine/threonine kinase. Plant Physiol. 123, 1247-1256 (2000).
82. Clouse, S. D., Langford, M. & McMorris, T. C. A brassinosteroid-insensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development. Plant Physiol. 111, 671-678 (1996).
83. Li, J. et al. BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110, 213-222 (2002).
84. Nam, K. H. & Li, J. BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110, 203-212 (2002).
85. Yin, Y., Wu, D. & Chory, J. Plant receptor kinases: systemin receptor identified. Proc. Natl Acad. Sci. USA 99, 9090-9092 (2002).
86. Clay, N. K. & Nelson, T. VH1, a provascular cell-specific receptor kinase that influences leaf cell patterns in Arabidopsis. Plant Cell 14, 2707-2722 (2002).
87. Clouse, S. D. Brassinosteroid signal transduction: clarifying the pathway from ligand perception to gene expression. Mol. Cell 10, 973-982 (2002).
88. Willemsen, V. et al. Cell polarity and PIN protein positioning in Arabidopsis require STEROL METHYL TRANSFERASE1 function. Plant Cell 15, 612-625 (2003).
89. Jang, J. C. et al. A critical role of sterols in embryonic patterning and meristem programming revealed by the fackel mutants of Arabidopsis thaliana. Genes Dev. 14, 1485-1497 (2000).
90. Carland, F. M., Fujioka, S., Takatsuto, S., Yoshida, S. & Nelson, T. The identification of CVP1 reveals a role for sterols in vascular patterning. Plant Cell 14, 2045-2058 (2002). This paper shows a crucial role for steroids in the continuity of vascular bundles.
91. Motose, H., Fukuda, H. & Sugiyama, M. Involvement of local intercellular communication in the differentiation of Zinnia mesophyll cells into tracheary elements. Planta 213, 121-131 (2001).
92. Motose, H., Sugiyama, M. & Fukuda, H. An arabinogalactan protein(s) is a key component of a fraction that mediates local intercellular communication involved in tracheary element differentiation of Zinnia mesophyll cells. Plant Cell Physiol. 42, 129-137 (2001). These two papers show that a secreted arabinogalactan protein, xylogen, mediates local intercellular communication that initiates xylem cell differentiation.
93. Fukuda, H. & Kobayashi, H. Dynamic organization of the cytoskeleton during tracheary-element differentiation. Dev. Growth Differ. 31, 9-16 (1989).
94. Doblin, M. S., Kurek, I., Jacob-Wilk, D. & Delmer, D. P. Cellulose biosynthesis in plants: from genes to rosettes. Plant Cell Physiol. 43, 1407-1420 (2002).
95. Taylor, N. G., Howells, R. M., Huttly, A. K., Vickers, K. & Turner, S. R. Interactions among three distinct CesA proteins essential for cellulose synthesis. Proc. Natl Acad. Sci. USA 100, 1450-1455 (2003).
96. Gardiner, J. C., Taylor, N. G. & Tumer, S. R. Control of cellulose synthase complex localization in developing xylem. Plant Cell 15, 1740-1748 (2003).
97. Desprez, T. et al. Resistance against herbicide isoxaben and cellulose deficiency caused by distinct mutations in same cellulose synthase isoform CESA6. Plant Physiol. 128, 482-490 (2002).
98. Milioni, D., Sado, P.-E., Stacey, N. J., Roberts, K. & McCann, C. M. Early gene expression associated with the commitment and differentiation of a plant tracheary element is revealed by cDNA-amplified fragment length polymorphism analysis. Plant Cell 14, 2813-2824 (2002).
99. Hertzberg, M. et al. A transcriptional roadmap to wood formation. Proc. Natl Acad. Sci. USA 98, 14732-14737 (2001).
100. Whetten, R., Sun, Y.-H., Zhang, Y. & Sederoff, R. Functional genomics and cell wall biosynthesis in loblolly pine. Plant Mol. Biol. 47, 275-291 (2001).
101. Kawaoka, A. et al. Functional analysis of tobacco LIM protein Ntlim1 involved in lignin biosynthesis. Plant J. 22, 289-301 (2000).
102. Borevitz, J. O., Xia, Y., Blount, J., Dixon, R. A. & Lamb, C. Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12, 2383-2394 (2000).
103. Milioni, D. et al. Differential expression of cell-wall-related genes during the formation of tracheary elements in the Zinnia mesophyll cell system. Plant Mol. Biol. 47, 221-238 (2001).
104. Burgess, J. & Linstead, P. In vitro tracheary element formation: structural studies and the effect of triiodobenzoic acid. Planta 160, 481-489 (1984).
105. Nakashima, J., Takabe, K., Fujita, M. & Fukuda, H. Autolysis during in vitro tracheary element differentiation: formation and location of the perforation. Plant Cell Physiol. 41, 1267-1271 (2000).
106. Shinohara, N., Demura, T. & Fukuda, H. Isolation of a vascular cell wall-specific monoclonal antibody recognizing a cell polarity by using a phage display subtraction method. Proc. Natl Acad. Sci. USA 97, 2585-2590 (2000).
107. Nakanomyo, I., Kost, B., Chua, N.-H. & Fukuda, H. Preferential and asymmetrical accumulation of a Rac small GTPase mRNA in differentiating xylem cells of Zinnia elegans. Plant Cell Physiol. 43, 1484-1492 (2002).
108. Im, K.-H., Cosgrove, D. J. & Jones, A. M. Subcellular localization of expansin mRNA in xylem cells. Plant Physiol. 123, 463-470 (2000).
109. Jones, A. M. Programmed cell death in development and defense. Plant Physiol. 125, 94-97 (2001).
110. Obara, K. & Fukuda, H. in Programmed Cell Death in Plants (ed. Gray, J.) 131-154 (Sheffield Academic Press, UK, 2003).
111. Funk, V., Kositsup, B., Zhao, C. & Beers, E. P. The Arabidopsis xylem peptidase XCP1 is a tracheary element vacuolar protein that may be a papain orthology. Plant Physiol. 128, 84-94 (2002).
112. Ito, J. & Fukuda, H. ZEN1 is a key enzyme in degradation of nuclear DNA during programmed cell death of tracheary elements. Plant Cell 14, 3201-3211 (2002). This paper shows that a distinct S1 nuclease functions in nuclear-DNA degradation in programmed cell death of TEs.
113. Groover, A., DeWitt, N., Heidel, A. & Jones, A. Programmed cell death of plant tracheary elements differentiating in vitro. Protoplasma 196, 197-211 (1997).
114. Kuriyama, H. Loss of tonoplast integrity programmed in tracheary element differentiation. Plant Physiol. 121, 763-774 (1999).
115. Obara, K., Kuriyama, H. & Fukuda, H. Direct evidence of active and rapid nuclear degradation triggered by vacuole rupture during programmed cell death in Zinnia. Plant Physiol. 125, 615-626 (2001).
116. Vercher, Y., Molowny, A. & Carbonell, J. Gibberellic acid effects on the ultrastructure of endocarp cells of unpollinated ovaries of Pisum sativum. Physiol. Plant 71, 302-308 (1987).
117. Kuo, A., Cappelluti, S., Cervantes-Cervantes, M., Rodriguez, M. & Bush, D. S. Okadaic acid, a protein phosphatase inhibitor, blocks calcium changes, gene expression, and cell death induced by gibberellin in wheat aleurone cells. Plant Cell 8, 259-269 (1996).
118. Scarpella, E., Rueb, S., Boot, K. J. M., Hoge, J. H. C. & Meijer, A. H. A role for the rice homeobox gene Oshox1 in provascular cell fate commitment. Development 127, 3655-3669 (2000). This paper shows that the use of a homeobox gene as a molecular marker allows us to distinguish developmental stages of procambium in rice roots.
119. Fukuda, H., Koizumi, K. & Demura, T. Vascular differentiation. Shokubutsusaiboukougaku 12, 212-222 (2000).
120. Weier, T. E., Stocking, C. R., Barbour M. G. & Rost, T. L. Botany 6th edn 118 (John Wiley & Sons, New Jersey, USA, 1982).