The Arabidopsis thaliana hypocotyl, a model to identify and study control mechanisms of cellular expansion

Plant Cell Reports

Volumn 33, Issue 5, 2014, Pages 697-706

  Boron, Agnieszka Karolina ^a   Vissenberg, Kris ^a  

^a UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

Arabidopsis thaliana; Cell wall; Cellulose; Hypocotyl development; Light regulation; Microtubules

Indexed keywords

ARABIDOPSIS PROTEIN; CELLULOSE; PHYTOHORMONE;

ARABIDOPSIS; BIOLOGICAL MODEL; CELL WALL; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIGHT; METABOLISM; MICROTUBULE; PHYSIOLOGY; PLANT EPIDERMIS; PLANT GROWTH; PLANT ROOT; RADIATION RESPONSE; SIGNAL TRANSDUCTION; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL WALL; CELLULOSE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; HYPOCOTYL; LIGHT; MICROTUBULES; MODELS, BIOLOGICAL; PLANT EPIDERMIS; PLANT GROWTH REGULATORS; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; SIGNAL TRANSDUCTION;

EID: 84914676854     PISSN: 07217714     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00299-014-1591-x     Document Type: Review

References (103)

1. Ang LH, Chattopadhyay S, Wei N, Oyama T, Okada K, Batschauer A, Deng XW (1998) Molecular interaction between COP1 and HY5 defines a regulatory switch for light control of Arabidopsis development. Mol Cell 1:213–222
2. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815
3. Bai MY, Fan M, Wang ZY (2012) A triple helix-loop-helix/basic helix-loop-helix cascade controls cell elongation downstream of multiple hormonal and environmental signaling pathways in Arabidopsis. Plant Cell 24:4917–4929
4. Ballesteros ML, Bolle C, Lois LM, Moore JM, Vielle-Calzada JP, Grossniklaus U, Chua NH (2001) LAF1, a MYB transcription activator for phytochrome A signaling. Genes Dev 15:2613–2625
5. Beeckman T, Przemeck GK, Stamatiou G, Lau R, Terryn N, De Rycke R, Inzé D, Berleth T (2002) Genetic complexity of cellulose synthase a gene function in Arabidopsis embryogenesis. Plant Physiol 130:1883–1893
6. Bernhardt A, Lechner E, Hano P, Schade V, Dieterle M, Anders M, Dubin MJ, Benvenuto G, Bowler C, Genschik P, Hellmann H (2006) CUL4 associates with DDB1 and DET1 and its downregulation affects diverse aspects of development in Arabidopsis thaliana. Plant J 47:591–603
7. Briggs WR, Olney MA (2001) Photoreceptors in plant photomorphogenesis to date. Five phytochromes, two cryptochromes, one phototropin, and one superchrome. Plant Physiol 125:85–88
8. Bringmann M, Li E, Sampathkumar A, Kocabek T, Hauser MT, Persson S (2012) POM-POM2/cellulose synthase interacting1 is essential for the functional association of cellulose synthase and microtubules in Arabidopsis. Plant Cell 24:163–177
9. Cao L, Wang L, Zheng M, Cao H, Ding L, Zhang X, Fu Y (2013) Arabidopsis AUGMIN subunit 8 is a microtubule plus-end binding protein that promotes microtubule reorientation in hypocotyls. Plant Cell 25:2187–2201
10. Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3:1–30
11. Casal JJ (2013) Photoreceptor signaling networks in plant responses to shade. Annu Rev Plant Biol 64:403–427
12. Catalá R, Medina J, Salinas J (2011) Integration of low temperature and light signaling during cold acclimation response in Arabidopsis. Proc Natl Acad Sci USA 108:16475–16480
13. Chan J, Eder M, Crowell EF, Hampson J, Calder G, Lloyd C (2011) Microtubules and CESA tracks at the inner epidermal wall align independently of those on the outer wall of light-grown Arabidopsis hypocotyls. J Cell Sci 124:1088–1094
14. Chang CS, Li Y-H, Chen L-T, Chen W-C, Hsieh W-P, Shin J, Jane W-N, Chou S-J, Choi G, Hu J-M, Somerville S, Wu S-H (2008) LZF1, a HY5-regulated transcriptional factor, functions in Arabidopsis de-etiolation. Plant J 54:205–219
15. Chapman EJ, Greenham K, Castillejo C, Sartor R, Bialy A, Sun TP, Estelle M (2012) Hypocotyl transcriptome reveals auxin regulation of growth-promoting genes through GA-dependent and -independent pathways. PLoS One 7:e36210
16. Chattopadhyay S, Ang LH, Puente P, Deng XW, Wei N (1998) Arabidopsis bZIP protein HY5 directly interacts with light-responsive promoters in mediating light control of gene expression. Plant Cell 10:673–683
17. Chen M, Chory J, Fankhauser C (2004) Light signal transduction in higher plants. Annu Rev Genet 38:87–117
18. Chen H, Shen Y, Tang X, Yu L, Wang J, Guo L, Zhang Y, Zhang H, Feng S, Strickland E, Zheng N, Deng XW (2006) Arabidopsis CULLIN4 forms an E3 ubiquitin ligase with RBX1 and the CDD complex in mediating light control of development. Plant Cell 18:1991–2004
19. Chen D, Xu G, Tang W, Jing Y, Ji Q, Fei Z, Lin R (2013) Antagonistic basic helix-loop-helix/bZIP transcription factors form transcriptional modules that integrate light and reactive oxygen species signaling in Arabidopsis. Plant Cell 25:1657–1673
20. Cluis CP, Mouchel CF, Hardtke CS (2004) The Arabidopsis transcription factor HY5 integrates light and hormone signaling pathways. Plant J 38:332–347
21. Collett CE, Harberd NP, Leyser O (2000) Hormonal interactions in the control of Arabidopsis hypocotyl elongation. Plant Physiol 124:553–561
22. Cosgrove DJ (2000) Loosening of plant cell walls by expansin. Nature 407:321–326
23. Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861
24. Cowling RJ, Harberd NP (1999) Gibberellins control Arabidopsis hypocotyl growth via regulation of cellular elongation. J Exp Bot 50:1351–1357
25. Crowell EF, Timpano H, Desprez T, Franssen-Verheijen T, Emons AM, Höfte H, Vernhettes S (2011) Differential regulation of cellulose orientation at the inner and outer face of epidermal cells in the Arabidopsis hypocotyl. Plant Cell 23:2592–2605
26. De Grauwe L, Vandenbussche F, Tietz O, Palme K, Van Der Straeten D (2005) Auxin, ethylene and brassinosteroids: tripartite control of growth in the Arabidopsis hypocotyl. Plant Cell Physiol 46:827–836
27. De Grauwe L, Vandenbussche F, Van Der Straeten D (2006) Signal crosstalk in the control of hypocotyl elongation in Arabidopsis. In: Verbelen J-P, Vissenberg K (eds) The expanding cell. Plant cell monographs, vol 5. Springer, Berlin, pp 271–293
28. Derbyshire P, Findlay K, McCann MC, Roberts K (2007a) Cell elongation in Arabidopsis hypocotyls involves dynamic changes in cell wall thickness. J Exp Bot 58:2079–2089
29. Derbyshire P, McCann MC, Roberts K (2007b) Restricted cell elongation in Arabidopsis hypocotyls is associated with a reduced average pectin esterification level. BMC Plant Biol 7:31
30. Dieterle M, Zhou YC, Schafer E, Funk M, Kretsch T (2001) EID1, an F-box protein involved in phytochrome A-specific light signaling. Genes Dev 15:939–944
31. Dolan L, Janmaat K, Willemsen V, Linstead P, Poethig S, Roberts K, Scheres B (1993) Cellular organisation of the Arabidopsis thaliana root. Development 119:71–84
32. Effendi Y, Jones AM, Scherer GFE (2013) AUXIN-BINDING-PROTEIN1 (ABP1) in phytochrome-B-controlled responses. J Exp Bot 64:5065–5074
33. Ehrhardt DW, Shaw SL (2006) Microtubule dynamics and organization in the plant cortical array. Annu Rev Plant Biol 57:859–875
34. Fairchild CD, Schumaker MA, Quail PH (2000) HFR1 encodes an atypical bHLH protein that acts in phytochrome A signal transduction. Genes Dev 14:2377–2391
35. Gangappa SN, Crocco CD, Johansson H, Datta S, Hettiarachchi C, Holm M, Botto JF (2013) The Arabidopsis B-BOX protein BBX25 interacts with HY5, negatively regulating BBX22 expression to suppress seedling photomorphogenesis. Plant Cell 25:1243–1257
36. Gendreau E, Traas J, Desnos T, Grandjean O, Caboche M, Höfte H (1997) Cellular basis of hypocotyl growth in Arabidopsis thaliana. Plant Physiol 114:295–305
37. Gu Y, Kaplinsky N, Bringmann M, Cobb A, Carroll A, Sampathkumar A, Baskin TI, Persson S, Somerville CR (2010) Identification of a cellulose synthase-associated protein required for cellulose biosynthesis. Proc Natl Acad Sci USA 107:12866–12871
38. Guénin S, Mareck A, Rayon C, Lamour R, Assoumou Ndong Y, Domon JM, Sénéchal F, Fournet F, Jamet E, Canut H, Percoco G, Mouille G, Rolland A, Rustérucci C, Guerineau F, Van Wuytswinkel O, Gillet F, Driouich A, Lerouge P, Gutierrez L, Pelloux J (2011) Identification of pectin methylesterase 3 as a basic pectin methylesterase isoform involved in adventitious rooting in Arabidopsis thaliana. New Phytol 192:114–126
39. Gutierrez R, Lindeboom JJ, Paredez AR, Emons AMC, Ehrhardt DW (2009) Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments. Nat Cell Biol 11:797–806
40. Hamada T, Nagasaki-Takeuchi N, Kato T, Fujiwara M, Sonobe S, Fukao Y, Hashimoto T (2013) Purification and characterization of novel microtubule-associated proteins from Arabidopsis cell suspension cultures. Plant Physiol 163:1804–1816
41. Hoecker U, Tepperman JM, Quail PH (1999) SPA1, a WDrepeat protein specific to phytochrome A signal transduction. Science 284:496–499
42. Holm M, Ma LG, Qu LJ, Deng XW (2002) Two interacting bZIP proteins are direct targets of COP1-mediated control of light-dependent gene expression in Arabidopsis. Genes Dev 16:1247–1259
43. Hudson M, Ringli C, Boylan MT, Quail PH (1999) The FAR1 locus encodes a novel nuclear protein specific to phytochrome A signaling. Genes Dev 13:2017–2027
44. Huq E, Quail PH (2002) PIF4, a phytochrome-interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis. EMBO J 21:2441–2450
45. Huq E, Tepperman JM, Quail PH (2000) GIGANTEA is a nuclear protein involved in phytochrome signaling in Arabidopsis. Proc Natl Acad Sci USA 97:9789–9794
46. Huq E, Al-Sady B, Hudson M, Kim CH, Apel K, Quail PH (2004) Phytochrome-interacting factor 1 is a critical bHLH regulator of chlorophyll biosynthesis. Science 305:1937–1941
47. Jensen PJ, Hangarter RP, Estelle M (1998) Auxin transport is required for hypocotyl elongation in light-grown but not dark-grown Arabidopsis. Plant Physiol 116:455–462
48. Jing Y, Lin R (2013) PICKLE is a repressor in seedling de-etiolation pathway. Plant Signal Behav 8:e25026
49. Jing Y, Zhang D, Wang X, Tang W, Wang W, Huai J, Xu G, Chen D, Li Y, Lin R (2013) Arabidopsis chromatin remodeling factor PICKLE interacts with transcription factor HY5 to regulate hypocotyl cell elongation. Plant Cell 25:242–256
50. Koornneef M, Rolff E, Spruitt CJP (1980) Genetic control of light inhibited hypocotyl elongation in Arabidopsis thaliana L. Heynh. Z Pflanzenphysiol 100:147–160
51. Lau OS, Deng XW (2010) Plant hormone signaling lightens up: integrators of light and hormones. Curr Opin Plant Biol 13:571–577
52. Lau OS, Deng XW (2012) The photomorphogenic repressors COP1 and DET1: 20 years later. Trends Plant Sci 17:584–593
53. Lee J, He K, Stolc V, Lee H, Figueroa P, Gao Y, Tongprasit W, Zhao HY, Lee I, Deng XW (2007) Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development. Plant Cell 19:731–749
54. Lei L, Li S, Gu Y (2012) Cellulose synthase interactive protein 1 (CSI1) mediates the intimate relationship between cellulose microfibrils and cortical microtubules. Plant Signal Behav 7:714–718
55. Li J, Li G, Gao S, Martinez C, He G, Zhou Z, Huang X, Lee JH, Zhang H, Shen Y, Wang H, Deng XW (2010) Arabidopsis transcription factor ELONGATED HYPOCOTYL5 plays a role in the feedback regulation of phytochrome A signaling. Plant Cell 22:3634–3649
56. Li S, Lei L, Somerville CR, Gu Y (2012) Cellulose synthase interactive protein 1 (CSI1) links microtubules and cellulose synthase complexes. Proc Natl Acad Sci USA 109:185–190
57. Liang X, Wang H, Mao L, Hu Y, Dong T, Zhang Y, Wang X, Bi Y (2012) Involvement of COP1 in ethylene- and light-regulated hypocotyl elongation. Planta 236:1791–1802
58. Lin R, Wang H (2004) Arabidopsis FHY3/FAR1 gene family and distinct roles of its members in light control of Arabidopsis development. Plant Physiol 136:4010–4022
59. Lindeboom JJ, Nakamura M, Hibbel A, Shundyak K, Gutierrez R, Ketelaar T, Emons AMC, Mulder BM, Kirik V, Ehrhardt DW (2013) A mechanism for reorientation of cortical microtubule arrays driven by microtubule severing. Science 342:1245533. doi:10.1126/science.1245533
60. Liu XL, Covington MF, Fankhauser C, Chory J, Wagner DR (2001) ELF3 encodes a circadian clock-regulated nuclear protein that functions in an Arabidopsis PHYB signal transduction pathway. Plant Cell 13:1293–1304
61. Liu X, Qin T, Ma Q, Sun J, Liu Z, Yuan M, Mao T (2013) Light-regulated hypocotyl elongation involves proteasome-dependent degradation of the microtubule regulatory protein WDL3 in Arabidopsis. Plant Cell 25:1740–1755
62. Lloyd C, Chan J (2008) The parallel lives of microtubules and cellulose microfibrils. Curr Opin Plant Biol 11:641–646
63. Ma L, Li J, Qu L, Hager J, Chen Z, Zhao H, Deng XW (2001) Light control of Arabidopsis development entails coordinated regulation of genome expression and cellular pathways. Plant Cell 13:2589–2607
64. Martínez-García JF, Huq E, Quail PH (2000) Direct targeting of light signals to a promoter element-bound transcription factor. Science 288:859–863
65. Miedes E, Suslov D, Vandenbussche F, Kenobi K, Ivakov A, Van Der Straeten D, Lorences EP, Mellerowicz EJ, Verbelen JP, Vissenberg K (2013) Xyloglucan endotransglucosylase/hydrolase (XTH) overexpression affects growth and cell wall mechanics in etiolated Arabidopsis hypocotyls. J Exp Bot 64:2481–2497
66. Mohnen D (2008) Pectin structure and biosynthesis. Curr Opin Plant Biol 11:266–277
67. Mouille G, Robin S, Lecomte M, Pagant S, Höfte H (2003) Classification and identification of Arabidopsis cell wall mutants using Fourier transform infrared (FT-IR) microspectroscopy. Plant J 35:393–404
68. Nemhauser J, Chory J (2002) Photomorphogenesis. In: Meyerowitz E, Somerville C (eds) The Arabidopsis book. American Society of Plant Biologists, Rockville, pp 1–12
69. Ni M, Tepperman JM, Quail PH (1998) PIF3, a phytochrome-interacting factor necessary for normal photoinduced signal transduction, is a novel basic helix-loop-helix protein. Cell 95:657–667
70. Osterlund MT, Hardtke CS, Wei N, Deng XW (2000) Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature 405:462–466
71. Oyama T, Shimura Y, Okada K (1997) The Arabidopsis HY5 gene encodes a bZIP protein that regulates stimulus-induced development of root and hypocotyl. Genes Dev 11:2983–2995
72. Paredez AR, Somerville CR, Ehrhardt DW (2006) Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312:1491–1495
73. Pelletier S, Van Orden J, Vissenberg K, Delacourt J, Urbain A, Mouille G, Lemonnier G, Renou J-P, Höfte H (2010) Transcript profiling reveals a role for pectin de-methylesterification in the growth acceleration in dark-grown Arabidopsis hypocotyls. Plant J 188:726–739
74. Petricka JJ, Winter CM, Benfey PN (2012) Control of Arabidopsis root development. Annu Rev Plant Biol 63:563–590
75. Prasad BR, Kumar SV, Nandi A, Chattopadhyay S (2012) Functional interconnections of HY1 with MYC2 and HY5 in Arabidopsis seedling development. BMC Plant Biol 12:37
76. Raz V, Koornneef M (2001) Cell division activity during apical hook development. Plant Physiol 125:219–226
77. Refrégier G, Pelletier S, Jaillard D, Höfte H (2004) Interaction between wall deposition and cell elongation in dark-grown hypocotyl cells in Arabidopsis. Plant Physiol 135:959–968
78. Richmond PA, Métraux JP, Taiz L (1980) Cell expansion patterns and directionality of wall mechanical properties in nitella. Plant Physiol 65:211–217
79. Saibo NJM, Vriezen WH, Beemster GTS, Van Der Straeten D (2003) Growth and stomata development of Arabidopsis hypocotyls are controlled by gibberellins and modulated by ethylene and auxins. Plant J 33:989–1000
80. Sambade A, Pratap A, Buschmann H, Morris R, Lloyd C (2012) The influence of light on microtubule dynamics and alignment in the Arabidopsis hypocotyl. Plant Cell 24:192–201
81. Scheres B, Wolkenfelt H, Willemsen V, Terlouw M, Lawson E, Dean C, Weisbeek P (1994) Embryonic origin of the Arabidopsis root and root meristem initials. Development 120:2475–2487
82. Shin J, Park E, Choi G (2007) PIF3 regulates anthocyanin biosynthesis in an HY5-dependent manner with both factors directly binding anthocyanin biosynthetic gene promoters in Arabidopsis. Plant J 49:981–994
83. Staub JM, Wei N, Deng XW (1996) Evidence for FUS6 as a component of the nuclear-localized COP9 complex in Arabidopsis. Plant Cell 8:2047–2056
84. Sun XD, Ni M (2011) HYPOSENSITIVE TO LIGHT, an alpha/beta fold protein, acts downstream of ELONGATED HYPOCOTYL 5 to regulate seedling de-etiolation. Mol Plant 4:116–126
85. Suslov D, Verbelen J-P (2006) Cellulose orientation determines mechanical anisotropy in onion epidermis cell walls. J Exp Bot 57:2183–2192
86. Suslov D, Verbelen J-P, Vissenberg K (2009) Onion epidermis as a new model to study the control of growth anisotropy in higher plants. J Exp Bot 60:4175–4187
87. Tang W, Ji Q, Huang Y, Jiang Z, Bao M, Wang H, Lin R (2012) FAR-RED ELONGATED HYPOCOTYL3 and FAR-RED IMPAIRED RESPONSE1 transcription factors integrate light and abscisic acid signaling in Arabidopsis. Plant Physiol 163:857–866
88. Tsukagoshi H, Busch W, Benfey PN (2010) Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143:606–616
89. Ulm R, Baumann A, Oravecz A, Máté Z, Adám E, Oakeley EJ, Schäfer E, Nagy F (2004) Genome-wide analysis of gene expression reveals function of the bZIP transcription factor HY5 in the UV-B response of Arabidopsis. Proc Natl Acad Sci USA 101:1397–1402
90. Van Sandt V, Suslov D, Verbelen J-P, Vissenberg K (2007) Xyloglucan endotransglucosylase activity loosens a plant cell wall. Ann Bot 100:1467–1473
91. Vandenbussche F, Verbelen JP, Van Der Straeten D (2005) Of light and length: regulation of hypocotyl growth in Arabidopsis. Bioessay 27:375–384
92. Vandenbussche F, Habricot Y, Condiff AS, Maldiney R, Van der Straeten D, Ahmad M (2007) HY5 is a point of convergence between cryptochrome and cytokinin signalling pathways in Arabidopsis thaliana. Plant J 49:428–441
93. Vandenbussche F, Suslov D, De Grauwe L, Vissenberg K, Van Der Straeten D (2011) The role of brassinosteroids in shoot gravitropism. Plant Physiol 156:1331–1336
94. Vandenbussche F, Vaseva I, Vissenberg K, Van Der Straeten D (2012) Ethylene in vegetative development: a tale with a riddle. New Phytol 194:895–909
95. Verbelen J-P, De Cnodder T, Le J, Vissenberg K, Baluska F (2006) Root apex of Arabidopsis thaliana consists of four distinct zones of growth activities: meristematic zone, transition zone, fast elongation zone, and growth terminating zone. Plant Signal Behav 1:296–304
96. Vineyard L, Elliott A, Dhingra S, Lucas JR, Shaw SL (2013) Progressive transverse microtubule array organization in hormone-induced Arabidopsis hypocotyl cells. Plant Cell 25:662–676
97. von Arnim AG, Deng XW (1994) Light inactivation of Arabidopsis photomorphogenic repressor COP1 involves a cell-specific regulation of its nucleocytoplasmic partitioning. Cell 79:1035–1045
98. Wang H, Deng XW (2003) Dissecting the phytochrome A-dependent signaling network in higher plants. Trends Plant Sci 8:172–178
99. Wei N, Deng XW (1996) The role of the COP/DET/FUS genes in light control of Arabidopsis seedling development. Plant Physiol 112:871–878
100. Yu Y, Wang J, Zhang Z, Quan R, Zhang H, Deng XW, Ma L, Huang R (2013) Ethylene promotes hypocotyl growth and HY5 degradation by enhancing the movement of COP1 to the nucleus in the light. PLoS Genet 9:e1004025
101. Zeidler M, Zhou Q, Sarda X, Yau CP, Chua NH (2004) The nuclear localization signal and the C-terminal region of FHY1 are required for transmission of phytochrome A signals. Plant J 40:355–365
102. Zhang H, He H, Wang X, Wang X, Yang X, Li L, Deng XW (2011) Genome-wide mapping of the HY5-mediated gene networks in Arabidopsis that involve both transcriptional and post-transcriptional regulation. Plant J 65:346–358
103. Zheng X, Wu S, Zhai H, Zhou P, Song M, Su L, Xi Y, Li Z, Cai Y, Meng F, Yang L, Wang H, Yang J (2013) Arabidopsis phytochrome B promotes SPA1 nuclear accumulation to repress photomorphogenesis under far-red light. Plant Cell 25:115–133