EXPANSINA17 Up-Regulated by LBD18/ASL20 promotes lateral root formation during the auxin response

Plant and Cell Physiology

Volumn 54, Issue 10, 2013, Pages 1600-1611

  Lee, Han Woo ^a   Kim, Jungmook ^a  

^a Chonnam National University   (South Korea)

Author keywords

Arabidopsis thaliana; Auxin; Cell wall loosening factor; EXP17; Lateral root formation; LBD18

Indexed keywords

ARABIDOPSIS PROTEIN; AUXIN; BETA GLUCURONIDASE; EXPANSIN A7 PROTEIN, ARABIDOPSIS; GREEN FLUORESCENT PROTEIN; INDOLEACETIC ACID DERIVATIVE; LBD18 PROTEIN, ARABIDOPSIS; PHYTOHORMONE; TRANSCRIPTION FACTOR;

ARABIDOPSIS; ARABIDOPSIS THALIANA; ARTICLE; CELL WALL LOOSENING FACTOR; DRUG EFFECT; EXP17; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LATERAL ROOT FORMATION; LBD18; METABOLISM; MUTATION; PLANT ROOT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TIME; TRANSGENIC PLANT; UPREGULATION;

ARABIDOPSIS THALIANA; AUXIN; CELL WALL LOOSENING FACTOR; EXP17; LATERAL ROOT FORMATION; LBD18;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GLUCURONIDASE; GREEN FLUORESCENT PROTEINS; INDOLEACETIC ACIDS; MUTATION; PLANT GROWTH REGULATORS; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TIME FACTORS; TRANSCRIPTION FACTORS; UP-REGULATION;

EID: 84885928841     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pct105     Document Type: Article

References (59)

1. Berckmans, B., Vassileva, V., Schmid, S.P., Maes, S., Parizot, B., Naramoto, S. et al. (2011) Auxin-dependent cell cycle reactivation through transcriptional regulation of Arabidopsis E2Fa by Lateral Organ Boundary proteins. Plant Cell 23: 3671-3683.
2. Borghi, L., Bureau, M. and Simon, R. (2007) Arabidopsis JAGGED LATERAL ORGANS is expressed in boundaries and coordinates KNOX and PIN activity. Plant Cell 19: 1795-1808. (Pubitemid 47218841)
3. Bortiri, E., Chuck, G., Vollbrecht, E., Rocheford, T., Martienssen, R. and Hake, S. (2006) ramosa2 encodes a LATERAL ORGAN BOUNDARY domain protein that determines the fate of stem cells in branch meristems of maize. Plant Cell 18: 574-585. (Pubitemid 43956162)
4. Brummell, D.A., Harpster, M.H., Civello, P.M., Palys, J.M., Bennett, A.B. and Dunsmuir, P. (1999) Modification of expansin protein abundance in tomato fruit alters softening and cell wall polymer metabolism during ripening. Plant Cell 11: 2203-2216.
5. Bureau, M., Rast, M.I., Illmer, J. and Simon, R. (2010) JAGGED LATERAL ORGAN (JLO) controls auxin dependent patterning during development of the Arabidopsis embryo and root. Plant Mol. Biol. 74: 479-491.
6. Cho, H.T. and Cosgrove, D.J. (2000) Altered expression of expansion modulates leaf growth and pedicel abscission in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 97: 9783-9788. (Pubitemid 30650853)
7. Cho, H.T. and Cosgrove, D.J. (2002) Regulation of root hair initiation and expansin gene expression in Arabidopsis. Plant Cell 14: 3237-3253. (Pubitemid 36029144)
8. Choi, D., Lee, Y., Cho, H.T. and Kende, H. (2003) Regulation of expansin gene expression affects growth and development in transgenic rice plants. Plant Cell 15: 1386-1398. (Pubitemid 36715180)
9. Cosgrove, D.J. (2000a) Loosening of plant cell walls by expansins. Nature 407: 321-326.
10. Cosgrove, D.J. (2000b) Expansive growth of plant cell walls. Plant Physiol. Biochem. 38: 109-124. (Pubitemid 30170278)
11. De Smet, I., Lau, S., Voss, U., Vanneste, S., Benjamins, R., Rademacher, E.H. et al. (2010) Bimodular auxin response controls organogenesis in Arabidopsis. Proc. Natl Acad. Sci. USA 107: 2705-2710.
12. Ditengou, F.A., Teale, W.D., Kochersperger, P., Flittner, K.A., Kneuper, I., van der Graaff, E. et al. (2008) Mechanical induction of lateral root initiation in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 105: 18818-18823.
13. Evans, M.M. (2007) The indeterminate gametophyte1 gene of maize encodes a LOB domain protein required for embryo sac and leaf development. Plant Cell 19: 46-62. (Pubitemid 46852700)
14. Fukaki, H., Tameda, S., Masuda, H. and Tasaka, M. (2002) Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J. 29: 153-168. (Pubitemid 34134693)
15. Goh, H.H., Sloan, J., Dorca-Fornell, C. and Fleming, A. (2012) Inducible repression of multiple expansin genes leads to growth suppression during leaf development. Plant Physiol. 159: 1759-1770.
16. Gray-Mitsumune, M., Blomquist, K., McQueen-Mason, S., Teeri, T.T., Sundberg, B. and Mellerowicz, E.J. (2008) Ectopic expression of a wood-abundant expansin PttEXPA1 promotes cell expansion in primary and secondary tissues in aspen. Plant Biotechnol J. 6: 62-72. (Pubitemid 350233584)
17. Guo, W., Zhao, J., Li, X., Qin, L., Yan, X. and Liao, H. (2011) A soybean b-expansin gene GmEXPB2 intrinsically involved in root system architecture responses to abiotic stresses. Plant J. 66: 541-552.
18. Hochholdinger, F. and Zimmermann, R. (2008) Conserved and diverse mechanisms in root development. Curr. Biol. 11: 70-74. (Pubitemid 351172872)
19. Inukai, Y., Sakamoto, T., Ueguchi-Tanaka, M., Shibata, Y., Gomi, K., Umemura, I. et al. (2005) Crown rootless1, which is essential for crown root formation in rice, is a target of an AUXIN RESPONSE FACTOR in auxin signaling. Plant Cell 17: 1387-1396. (Pubitemid 43138192)
20. Iwakawa, H., Ueno, Y., Semiarti, E., Onouchi, H., Kojima, S., Tsukaya, H. et al. (2002) The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana, required for formation of symmetric flat leaf lamina, encodes a member of a novel family of proteins characterized by cysteine repeats and a leucine zipper. Plant Cell Physiol. 43: 467-478. (Pubitemid 34604593)
21. Jefferson, R.A. and Wilson, K.J. (1991) The GUS gene fusion system. Plant Mol. Biol. Manual B14: 1-33.
22. Jeon, J., Kim, N.Y., Kim, S., Kang, N.Y., Novák, O., Ku, S.J. et al. (2010) A subset of cytokinin two-component signaling system plays a role in cold temperature stress response in Arabidopsis. J. Biol. Chem. 285: 23371-23386.
23. Laskowski, M., Biller, S., Stanley, K., Kajstura, T. and Prusty, R. (2006) Expression profiling of auxin-treated Arabidopsis roots: toward a molecular analysis of lateral root emergence. Plant Cell Physiol. 47: 788-792. (Pubitemid 43946309)
24. Lee, D.J., Park, J.W., Lee, H.W. and Kim, J. (2009a) Genome-wide analysis of the transcriptome downstream of iaa1 during early auxin response and expression analysis of iaa1-regulated auxin-response genes. J. Exp. Bot. 60: 3935-3957.
25. Lee, D.K., Ahn, J.H., Song, S.K., Choi, Y.D. and Lee, J.S. (2003) Expression of an expansin gene is correlated with root elongation in soybean. Plant Physiol. 131: 985-997. (Pubitemid 36400338)
26. Lee, H.W., Kim, M.J., Kim, N.Y., Lee, S.H. and Kim, J. (2013) LBD18 acts as a transcriptional activator that directly binds to the EXPANSIN14 promoter in promoting lateral root emergence of Arabidopsis. Plant J. 73: 212-224.
27. Lee, H.W., Kim, N.Y., Lee, D.J. and Kim, J. (2009b) LBD18/ASL20 regulates lateral root formation in combination with LBD16/ASL18 downstream of ARF7 and ARF19 in Arabidopsis. Plant Physiol. 151: 1377-1389.
28. Lin, C., Choi, H.S. and Cho, H.T. (2011) Root hair-specific EXPANSIN A7 is required for root hair elongation in Arabidopsis. Mol. Cells 31: 393-397.
29. Lin, W.C., Shuai, B. and Springer, P.S. (2003) The Arabidopsis lateral organ boundaries-domain gene asymmetric leaves2 functions in the repression of KNOX gene expression and in adaxial-abaxial patterning. Plant Cell 15: 2241-2252. (Pubitemid 37261797)
30. Liu, H., Wang, S., Yu, X., Yu, J., He, X., Zhang, S. et al. (2005) ARL1, a LOB-domain protein required for adventitious root formation in rice. Plant J. 43: 47-56. (Pubitemid 40962734)
31. Lucas, M., Godin, C., Jay-Allemand, C. and Laplaze, L. (2008) Auxin fluxes in the root apex co-regulate gravitropism and lateral root initiation. J. Exp. Bot. 59: 55-66. (Pubitemid 351598964)
32. Malamy, J.E. and Benfey, P.N. (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124: 33-44. (Pubitemid 27053004)
33. McQueen-Mason, S.J. and Cosgrove, D.J. (1995) Expansin mode of action on cell walls: analysis of wall hydrolysis, stress-relaxation, and binding. Plant Physiol. 107: 87-100.
34. McQueen-Mason, S.J. and Cosgrove, D.J. (2000) Disruption of hydrogen-bonding between plant-cell wall polymers by proteins that induce wall extension. Proc. Natl Acad. Sci. USA 91: 6574-6578.
35. McQueen-Mason, S.J., Durachko, D.M. and Cosgrove, D.J. (1992) Two endogenous proteins that induce cell-wall extension in plants. Plant Cell 4: 1425-1433.
36. Neuteboom, L.W., Veth-Tello, L.M., Clijdesdale, O.R., Hooykaas, P.J. and van der Zaal, B.J. (1999) A novel subtilisin-like protease gene from Arabidopsis thaliana is expressed at sites of lateral root emergence. DNA Res. 6: 13-19. (Pubitemid 129705125)
37. Noh, S.A., Lee, H.S., Kim, Y.S., Paek, K.H., Shin, J.S. and Bae, J.M. (2013) Down-regulation of the IbEXP1 gene enhanced storage root development in sweetpotato. J. Exp. Bot. 64: 129-142.
38. Oh, S.A., Park, K.S., Twell, D. and Park, S.K. (2010) The SIDECAR POLLEN gene encodes a microspore-specific LOB/AS2 domain protein required for the correct timing and orientation of asymmetric cell division. Plant J. 64: 839-850.
39. Okushima, Y., Fukaki, H., Onoda, M., Theologis, A. and Tasaka, M. (2007) ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell 19: 118-130. (Pubitemid 46852706)
40. Okushima, Y., Overvoorde, P.J., Arima, K., Alonso, J.M., Chan, A., Chang, C. et al. (2005) Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19. Plant Cell 17: 444-463. (Pubitemid 41672967)
41. Parizot, B., Laplaze, L., Ricaud, L., Boucheron-Dubuisson, E., Bayle, V., Bonke, M. et al. (2008) Diarch symmetry of the vascular bundle in Arabidopsis root encompasses the pericycle and is reflected in distich lateral root initiation. Plant Physiol. 146: 140-148. (Pubitemid 351380044)
42. Park, J.Y., Kim, H.J. and Kim, J. (2002) Mutation in domain II of IAA1 confers diverse auxin-related phenotypes and represses auxinactivated expression of Aux/IAA genes in steroid regulatorinducible system. Plant J. 32: 669-683. (Pubitemid 36010873)
43. Péret, B., De Rybel, B., Casimiro, I., Benková, E., Swarup, R., Laplaze, L. et al. (2009a) Arabidopsis lateral root development: an emerging story. Trends Plant Sci. 14: 399-408.
44. Péret, B., Larrieu, A. and Bennett, M.J. (2009b) Lateral root emergence: a difficult birth. J. Exp. Bot. 60: 3637-3643.
45. Péret, B., Li, G., Zhao, J., Band, L.R., Voß, U., Postaire, O. et al. (2012) Auxin regulates aquaporin function to facilitate lateral root emergence. Nat. Cell Biol. 14: 991-998.
46. Reinhardt D., Wittwer, F., Mandel, T. and Kuhlemeier, C.(1998) Localized upregulation of a new expansin gene predicts the site of leaf formation in the tomato meristem. Plant Cell 10, 1427-1437. (Pubitemid 28542148)
47. Richter, G.L., Monshausen, G.B., Krol, A. and Gilroy, S. (2009) Mechanical stimuli modulate lateral root organogenesis. Plant Physiol. 151: 1855-1866.
48. Sampedro, J. and Cosgrove, D.J. (2005) The expansin superfamily. Genome Biol. 6: 242.
49. Shuai, B., Reynaga-Peña, C.G. and Springer, P.S. (2002) The LATERAL ORGAN BOUNDARIES gene defines a novel, plant-specific gene family. Plant Physiol. 129: 747-761. (Pubitemid 34695944)
50. Soyano, T., Thitamadee, S., Machida, Y. and Chua, N.H. (2008) ASYMMETRIC LEAVES2-LIKE19/LATERAL ORGAN BOUNDARIES DOMAIN30 and ASL20/LBD18 regulate tracheary element differentiation in Arabidopsis. Plant Cell 20: 3359-3373.
51. Swarup, K., Benková, E., Swarup, R., Casimiro, I., Péret, B., Yang, Y. et al. (2008) The auxin influx carrier LAX3 promotes lateral root emergence. Nat. Cell Biol. 10: 946-954.
52. Taramino, G., Sauer, M., Stauffer, J.L. Jr., Multani, D., Niu, X., Sakai, H. et al. (2007) The maize (Zea mays L.) RTCS gene encodes a LOB domain protein that is a key regulator of embryonic seminal and post-embryonic shoot-borne root initiation. Plant J. 50: 649-659. (Pubitemid 46733753)
53. Wielopolska, A., Townley, H., Moore, I., Waterhouse, P. and Helliwell, C. (2005) A high-throughput inducible RNAi vector for plants. Plant Biotechnol J. 3: 583-590. (Pubitemid 44944497)
54. Xu, B., Gou, J.Y., Li, F.G., Shangguan, X.X., Zhao, B., Yang, C.Q. et al. (2012) A cotton BURP domain protein interacts with a-expansin and their co-expression promotes plant growth and fruit production. Mol. Plant 6: 945-958.
55. Xu, L., Xu, Y., Dong, A., Sun, Y., Pi, L., Xu, Y. et al. (2003) Novel as1 and as2 defects in leaf adaxial-abaxial polarity reveal the requirement for ASYMMETRIC LEAVES1 and 2 and ERECTA functions in specifying leaf adaxial identity. Development 130: 4097-4107. (Pubitemid 37063427)
56. Zenoni, S., Fasoli, M., Tornielli, G.B., Dal Santo, S., Sanson, A., de Groot, P. et al. (2011) Overexpression of PhEXPA1 increases cell size, modifies cell wall polymer composition and affects the timing of axillary meristem development in Petunia hybrida. New Phytol. 191: 662-677.
57. Zenoni, S., Reale, L., Tornielli, G.B., Lanfaloni, L., Porceddu, A., Ferrarini, A. et al. (2004) Downregulation of the Petunia hybrida a-expansin gene PhEXP1 reduces the amount of crystalline cellulose in cell walls and leads to phenotypic changes in petal limbs. Plant Cell 16: 295-308. (Pubitemid 38192690)
58. Zhang, X.Q., Wei, P.C., Xiong, Y.M., Yang, Y., Chen, J. and Wang, X.C. (2011) Overexpression of the Arabidopsis a-expansin gene AtEXPA1 accelerates stomatal opening by decreasing the volumetric elastic modulus. Plant Cell Rep. 30: 27-36.
59. ZhiMing, Y., Bo, K., XiaoWei, H., ShaoLei, L., YouHuang, B., WoNa, D. et al. (2011) Root hair-specific expansins modulate root hair elongation in rice. Plant J. 66: 725-734.