Research Advances in the Molecular Mechanisms of Plant Microtubules in Regulating Hypocotyl Elongation

doi:10.11983/CBB20170

Abstract

Abstract: As one of the major members of cytoskeleton, microtubules play important roles in plant growth and deve- lopment. Hypocotyl has become a model system to study cell elongation, which is regulated by multiple internal and ex- ternal signalings. Here, we reviewed the recent research progress for the roles of microtubules in regulating the hypocotyl elongation in response to diversed environmental and developmental cues, which will extend our understanding on how microtubules response to the upstream signal and play roles in the elongation of plant hypocotyls.

Key words: microtubule, hypocotyl, elongation, environmental signals, growth and developmental cues

Jianru Yue, Yunjian He, Tianqi Qiu, Nannan Guo, Xueping Han, Xianling Wang. Research Advances in the Molecular Mechanisms of Plant Microtubules in Regulating Hypocotyl Elongation[J]. Chinese Bulletin of Botany, 2021, 56(3): 363-371.

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URL: https://www.chinbullbotany.com/EN/10.11983/CBB20170

https://www.chinbullbotany.com/EN/Y2021/V56/I3/363

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References 68

1	何群, 尤瑞麟 (2004). 应用Steedman’s wax切片法观察植物细胞微管骨架. 植物学通报 21, 547-555.
2	李志刚, 张新成, 林丽, 李素丽, 杨丽涛, 李杨瑞 (2008). 甘蔗茎尖细胞有丝分裂过程中微管骨架的变化. 植物学通报 25, 276-283.
3	Achard P, Liao LL, Jiang CF, Desnos T, Bartlett J, Fu XD, Harberd NP (2007). DELLAs contribute to plant photomorphogenesis. Plant Physiol 143, 1163-1172. DOI URL
4	Adamowski M, Li LX, Friml J (2019). Reorientation of cortical microtubule arrays in the hypocotyl of Arabidopsis thaliana is induced by the cell growth process and independent of auxin signaling. Int J Mol Sci 20, 3337. DOI URL
5	Alabadí D, Gallego-Bartolomé J, Orlando L, García- Cárcel L, Rubio V, Martínez C, Frigerio M, Iglesias-Pedraz JM, Espinosa A, Deng XW, Blázquez MA (2008). Gibberellins modulate light signaling pathways to prevent Arabidopsis seedling de-etiolation in darkness. Plant J 53, 324-335. PMID
6	Ambrose JC, Shoji T, Kotzer AM, Pighin JA, Wasteneys GO (2007). The Arabidopsis CLASP gene encodes a microtubule-associated protein involved in cell expansion and division. Plant Cell 19, 2763-2775. DOI URL
7	Baskin TI, Beemster GTS, Judy-March JE, Marga F (2004). Disorganization of cortical microtubules stimulates tangential expansion and reduces the uniformity of cellulose microfibril alignment among cells in the root of Ara- bidopsis. Plant Physiol 135, 2279-2290. DOI URL
8	Bleecker AB, Estelle MA, Somerville C, Kende H (1988). Insensitivity to ethylene conferred by a dominant mutation in Arabidopsis thaliana. Science 241, 1086-1089. DOI URL
9	Chen X, Grandont L, Li HJ, Hauschild R, Paque S, Abuzeineh A, Rakusová H, Benkova E, Perrot-Re- chenmann C, Friml J (2014). Inhibition of cell expansion by rapid ABP1-mediated auxin effect on microtubules. Na- ture 516, 90-93.
10	Chory J, Nagpal P, Peto CA (1991). Phenotypic and genetic analysis of det2, a new mutant that affects light- regulated seedling development in Arabidopsis. Plant Cell 3, 445-459. DOI URL
11	Clouse SD (2011). Brassinosteroid signal transduction: from receptor kinase activation to transcriptional networks regulating plant development. Plant Cell 23, 1219-1230. DOI URL
12	Cowling RJ, Harberd NP (1999). Gibberellins control Arabidopsis hypocotyl growth via regulation of cellular elongation. J Exp Bot 50, 1351-1357. DOI URL
13	de Grauwe L, Vandenbussche F, Tietz O, Palme K, van der Straeten D (2005). Auxin, ethylene and brassinos-teroids: tripartite control of growth in theArabidopsis hy- pocotyl. Plant Cell Physiol 46, 827-836. DOI URL
14	De Lucas M, Davière JM, Rodríguez-Falcón M, Pontin M, Iglesias-Pedraz JM, Lorrain S, Fankhauser C, Blázquez MA, Titarenko E, Prat S (2008). A molecular framework for light and gibberellin control of cell elongation. Nature 451, 480-484. DOI URL
15	Duek PD, Fankhauser C (2005). bHLH class transcription factors take centre stage in phytochrome signaling. Trends Plant Sci 10, 51-54. DOI URL
16	Ehrhardt DW, Shaw SL (2006). Microtubule dynamics and organization in the plant cortical array. Annu Rev Plant Biol 57, 859-875. PMID
17	Feng SH, Martinez C, Gusmaroli G, Wang Y, Zhou JL, Wang F, Chen LY, Yu L, Iglesias-Pedraz JM, Kircher S, Schäfer E, Fu XD, Fan LM, Deng XW (2008). Coordi-nated regulation ofArabidopsis thaliana development by light and gibberellins. Nature 451, 475-479. DOI URL
18	Fischer K, Schopfer P (1997). Interaction of auxin, light, and mechanical stress in orienting microtubules in relation to tropic curvature in the epidermis of maize coleoptiles. Protoplasma 196, 108-116. DOI URL
19	Friml J, Wiśniewska J, Benková E, Mendgen K, Palme K (2002). Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415, 806-809. PMID
20	Furutani I, Watanabe Y, Prieto R, Masukawa M, Suzuki K, Naoi K, Thitamadee S, Shikanai T, Hashimoto T (2000). The SPIRAL genes are required for directional control of cell elongation in Arabidopsis thaliana. Deve- lopment 127, 4443-4453.
21	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. PMID
22	Gray WM, Ostin A, Sandberg G, Romano CP, Estelle M (1998). High temperature promotes auxin-mediated hy-pocotyl elongation in Arabidopsis. Proc Natl Acad Sci USA 95, 7197-7202. DOI URL
23	Gudesblat GE, Russinova E (2011). Plants grow on bras-sinosteroids. Curr Opin Plant Biol 14, 530-537. DOI URL
24	Harberd NP, Belﬁeld E, Yasumura Y (2009). The angio- sperm gibberellin-GID1-DELLA growth regulatory mecha-nism: how an “inhibitor of an inhibitor” enables flexible response to fluctuating environments. Plant Cell 21, 1328-1339. DOI URL
26	Hashimoto T (2003). Dynamics and regulation of plant interphase microtubules: a comparative view. Curr Opin Plant Biol 6, 568-576. PMID
27	Hashimoto T, Kato T (2006). Cortical control of plant microtubules. Curr Opin Plant Biol 9, 5-11. PMID
28	Jensen PJ, Hangarter RP, Estelle M (1998). Auxin transport is required for hypocotyl elongation in light-grown but not dark-grownArabidopsis. Plant Physiol 116, 455-462. PMID
29	Kim SY, Kim BH, Lim CJ, Lim CO, Nam KH (2010). Constitutive activation of stress-inducible genes in a brassinosteroid-insensitive 1(bri1) mutant results in higher tolerance to cold. Physiol Plant 138, 191-204.
30	Kim TW, Wang ZY (2010). Brassinosteroid signal transduc-tion from receptor kinases to transcription factors. Annu Rev Plant Biol 61, 681-704. DOI URL
31	Kost B, Chua NH (2002). The plant cytoskeleton: vacuoles and cell walls make the difference. Cell 108, 9-12. DOI URL
32	Le J, Vandenbussche F, de Cnodder T, van der Straeten D, Verbelen JP (2005). Cell elongation and microtubule behavior in the Arabidopsis hypocotyl: responses to ethy- lene and auxin. J Plant Growth Regul 24, 166-178. DOI URL
33	Li JJ, Wang XL, Qin T, Zhang Y, Liu XM, Sun JB, Zhou Y, Zhu L, Zhang ZD, Yuan M, Mao TL (2011). MDP25, a novel calcium regulatory protein, mediates hypocotyl cell elongation by destabilizing cortical microtubules in Ara- bidopsis. Plant Cell 23, 4411-4427. DOI URL
34	Li L, Ye HX, Guo HQ, Yin YH (2010). Arabidopsis IWS1 interacts with transcription factor BES1 and is involved in plant steroid hormone brassinosteroid regulated gene expression. Proc Natl Acad Sci USA 107, 3918-3923. DOI URL
35	Lian N, Liu XM, Wang XH, Zhou YY, Li H, Li JG, Mao TL (2017). COP1 mediates dark-specific degradation of micro- tubule-associated protein WDL3 in regulating Arabidopsis hypocotyl elongation. Proc Natl Acad Sci USA 114, 12321-12326. DOI URL
36	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 seve- ring. Science 342, 1245533. DOI URL
37	Lindeboom JJ, Nakamura M, Saltini M, Hibbel A, Walia A, Ketelaar T, Emons AMC, Sedbrook JC, Kirik V, Mulder BM, Ehrhardt DW (2019). CLASP stabilization of plus ends created by severing promotes microtubule creation and reorientation. J Cell Biol 218, 190-205. DOI
38	Liu XM, Qin T, Ma QQ, Sun JB, Liu ZQ, Yuan M, Mao TL (2013). Light-regulated hypocotyl elongation involves proteasome-dependent degradation of the microtubule regulatory protein WDL3 in Arabidopsis. Plant Cell 25, 1740-1755. DOI URL
39	Lloyd C, Chan J (2004). Microtubules and the shape of plants to come. Nat Rev Mol Cell Biol 5, 13-23.
40	Ma QQ, Wang XH, Sun JB, Mao TL (2018). Coordinated regulation of hypocotyl cell elongation by light and ethy- lene through a microtubule destabilizing protein. Plant Phy- siol 176, 678-690.
41	Margolis RL, Wilson L (1981). Microtubule treadmills— possible molecular machinery. Nature 293, 705-711. PMID
42	Mitchison T, Kirschner M (1984). Dynamic instability of microtubule growth. Nature 312, 237-242. PMID
43	Nakajima K, Furutani I, Tachimoto H, Matsubara H, Hashimoto T (2004). SPIRAL1 encodes a plant-specific microtubule-localized protein required for directional control of rapidly expanding Arabidopsis cells. Plant Cell 16, 1178-1190. PMID
44	Nakajima K, Kawamura T, Hashimoto T (2006). Role of the SPIRAL1 gene family in anisotropic growth of Arabi-dopsis thaliana. Plant Cell Physiol 47, 513-522. PMID
45	Peng JR, Carol P, Richards DE, King KE, Cowling RJ, Murphy GP, Harberd NP (1997). The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes Dev 11, 3194-3205. DOI URL
46	Reid JB, Botwright NA, Smith JJ, O’Neill DP, Kerckhoffs LHJ (2002). Control of gibberellin levels and gene expres- sion during de-etiolation in pea. Plant Physiol 128, 734-741. DOI URL
47	Romano CP, Robson PRH, Smith H, Estelle M, Klee H (1995). Transgene-mediated auxin overproduction in Ara- bidopsis: hypocotyl elongation phenotype and interactions with the hy6-1 hypocotyl elongation and axr1 auxin-resis tant mutants. Plant Mol Biol 27, 1071-1083. PMID
48	Sambade A, Pratap A, Buschmann H, Morris RJ, Lloyd C (2012). The influence of light on microtubule dynamics and alignment in the Arabidopsis hypocotyl. Plant Cell 24, 192-201. DOI URL
49	Sauret-Güeto S, Calder G, Harberd NP (2012). Transient gibberellin application promotes Arabidopsis thaliana hypocotyl cell elongation without maintaining transverse o- rientation of microtubules on the outer tangential wall of epidermal cells. Plant J 69, 628-639. DOI URL
50	Shibaoka H (1974). Involvement of wall microtubules in gibberellin promotion and kinetin inhibition of stem elongation. Plant Cell Physiol 15, 255-263.
51	Shibaoka H (1993). Regulation by gibberellins of the orientation of cortical microtubules in plant cells. Aust J Plant Physiol 20, 461-470.
52	Silverstone AL, Ciampaglio CN, Sun TP (1998). The Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway. Plant Cell 10, 155-169. PMID
53	Smalle J, Haegman M, Kurepa J, van Montagu M, Straeten DVD (1997). Ethylene can stimulate Arabidopsis hypocotyl elongation in the light. Proc Natl Acad Sci USA 94, 2756-2761. DOI URL
54	Soga K, Yamaguchi A, Kotake T, Wakabayashi K, Hoson T (2010). Transient increase in the levels of γ-tubulin complex and katanin are responsible for reorientation by ethylene and hypergravity of cortical microtubules. Plant Signal Behav 5, 1480-1482. DOI URL
55	Sun JB, Ma QQ, Mao TL (2015). Ethylene regulates the Arabidopsis microtubule-associated protein WAVE-DAM- PENED2-LIKE5 in etiolated hypocotyl elongation. Plant Physiol 169, 325-337.
56	Tang WQ, Kim TW, Oses-Prieto JA, Sun Y, Deng ZP, Zhu SW, Wang RJ, Burlingame AL, Wang ZY (2008). BSKs mediate signal transduction from the receptor kinase BRI1 in Arabidopsis. Science 321, 557-560. DOI URL
57	Thitamadee S, Tuchihara K, Hashimoto T (2002). Microtubule basis for left-handed helical growth inArabidopsis. Nature 417, 193-196. PMID
58	True JH, Shaw SL (2020). Exogenous auxin induces trans- verse microtubule arrays through TRANSPORT INHIBI-TOR RESPONSE1/AUXIN SIGNALING F-BOX receptors. Plant Physiol 182, 892-907. DOI URL
59	van der Graaff E, Nussbaumer C, Keller B (2003). The Arabidopsis thaliana rlp mutations revert the ectopic leaf blade formation conferred by activation tagging of the LEP gene. Mol Genet Genomics 270, 243-252. PMID
60	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.
61	Wang CF, Liu WW, Wang GD, Li J, Dong L, Han LB, Wang Q, Tian J, Yu YJ, Gao CX, Kong ZS (2017). KTN80 confers precision to microtubule severing by specific targeting of Katanin complexes in plant cells. EMBO J 36, 3435-3447. DOI URL
62	Wang XF, Mao TL (2019). Understanding the functions and mechanisms of plant cytoskeleton in response to environmental signals. Curr Opin Plant Biol 52, 86-96. DOI URL
63	Wang XL, Zhang J, Yuan M, Ehrhardt DW, Wang ZY, Mao TL (2012). Arabidopsis microtubule destabilizing protein40 is involved in brassinosteroid regulation of hypocotyl elongation. Plant Cell 24, 4012-4025. DOI URL
64	Wang ZY, Seto H, Fujioka S, Yoshida S, Chory J (2001). BRI1 is a critical component of a plasma-membrane receptor for plant steroids. Nature 410, 380-383. PMID
65	Ye HX, Li L, Yin YH (2011). Recent advances in the regulation of brassinosteroid signaling and biosynthesis pathways. J Integr Plant Biol 53, 455-468. DOI URL
66	Yu YW, Wang J, Zhang ZJ, Quan RD, Zhang HW, Deng XW, Ma LG, Huang RF (2013). Ethylene promotes hypocotyl growth and HY5 degradation by enhancing the movement of COP1 to the nucleus in the light. PLoS Ge- net 9, e1004025.
67	Zhao YD, Christensen SK, Fankhauser C, Cashman JR, Cohen JD, Weigel D, Chory J (2001). A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science 291, 306-309. DOI URL
68	Zhong SW, Shi H, Xue C, Wang L, Xi YP, Li JG, Quail PH, Deng XW, Guo HW (2012). A molecular framework of light-controlled phytohormone action in Arabidopsis. Curr Biol 22, 1530-1535. DOI URL

蛋白名称	对微管的调节	在下胚轴伸长中的作用	参考文献
Katanin	依赖ATP切割微管	通过蓝光刺激诱导, 在微管交叉部位切断微管, 产生新末端并迅速由横向变为纵向生长, 从而导致下胚轴细胞的生长方向改变	Lindeboom et al., 2013; Wang et al., 2017
CLASP	稳定微管正端	维持下胚轴正常生长, CLASP缺失突变体clasp-1下胚轴明显短于野生型	Ambrose et al., 2007
MDP25	解聚微管	作为下胚轴伸长的负调节因子, MDP25可直接与微管结合, 促进微管解聚, mdp25突变体的黄化下胚轴更长, 而MDP25过表达植株下胚轴较短	Li et al., 2011
WDL3	稳定并重排微管	黑暗下, WDL3被26S蛋白酶体降解, 促进下胚轴伸长; 光调节微管重排过程中, WDL3通过调节下胚轴细胞中微管成束抑制下胚轴伸长	Liu et al., 2013
MDP60	去稳定并重排微管	通过PIF3介导光和乙烯信号, 协同调控微管去稳定蛋白, 促进下胚轴伸长	Ma et al., 2018
SPR1	稳定微管	下胚轴伸长的正向调节因子SPR1在快速生长的下胚轴中高表达, 通过调节微管动态促进黑暗下下胚轴伸长	Nakajima et al., 2004, 2006
WDL5	稳定并重排微管	乙烯激活EIN3, EIN3直接调控WDL5上调表达, WDL5通过维持微管纵向排列抑制黄化下胚轴伸长	Sun et al., 2015
MDP40	去稳定并重排微管	油菜素甾醇激活BZR1, BZR1直接结合到MDP40的启动子上并上调其表达, MDP40解聚微管使其变为横向排列, 从而促进黄化下胚轴伸长	Wang et al., 2012

蛋白名称	对微管的调节	在下胚轴伸长中的作用	参考文献
Katanin	依赖ATP切割微管	通过蓝光刺激诱导, 在微管交叉部位切断微管, 产生新末端并迅速由横向变为纵向生长, 从而导致下胚轴细胞的生长方向改变	Lindeboom et al., 2013; Wang et al., 2017
CLASP	稳定微管正端	维持下胚轴正常生长, CLASP缺失突变体clasp-1下胚轴明显短于野生型	Ambrose et al., 2007
MDP25	解聚微管	作为下胚轴伸长的负调节因子, MDP25可直接与微管结合, 促进微管解聚, mdp25突变体的黄化下胚轴更长, 而MDP25过表达植株下胚轴较短	Li et al., 2011
WDL3	稳定并重排微管	黑暗下, WDL3被26S蛋白酶体降解, 促进下胚轴伸长; 光调节微管重排过程中, WDL3通过调节下胚轴细胞中微管成束抑制下胚轴伸长	Liu et al., 2013
MDP60	去稳定并重排微管	通过PIF3介导光和乙烯信号, 协同调控微管去稳定蛋白, 促进下胚轴伸长	Ma et al., 2018
SPR1	稳定微管	下胚轴伸长的正向调节因子SPR1在快速生长的下胚轴中高表达, 通过调节微管动态促进黑暗下下胚轴伸长	Nakajima et al., 2004, 2006
WDL5	稳定并重排微管	乙烯激活EIN3, EIN3直接调控WDL5上调表达, WDL5通过维持微管纵向排列抑制黄化下胚轴伸长	Sun et al., 2015
MDP40	去稳定并重排微管	油菜素甾醇激活BZR1, BZR1直接结合到MDP40的启动子上并上调其表达, MDP40解聚微管使其变为横向排列, 从而促进黄化下胚轴伸长	Wang et al., 2012

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