The root cap determines ethylene-dependent growth and development in maize roots

Molecular Plant

Volumn 1, Issue 2, 2008, Pages 359-367

  Hahn, Achim ^a,b   Zimmermann, Roman ^a,b   Wanke, Dierk ^b   Harter, Klaus ^b   Edelmann, Hans G ^a,c  

^a UNIVERSITY OF COLOGNE   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c UNIVERSITY OF SIEGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ZEA MAYS;

1 AMINOCYCLOPROPANECARBOXYLIC ACID; 1-AMINOCYCLOPROPANE-1-CARBOXYLIC ACID; AMINO ACID; CYTOKININ; ETHYLENE; ETHYLENE DERIVATIVE; INDOLEACETIC ACID DERIVATIVE; STARCH;

ARTICLE; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MAIZE; METABOLISM; PHYSIOLOGY; PLANT ROOT; PLANT ROOT CAP; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEEDLING;

AMINO ACIDS, CYCLIC; CYTOKININS; ETHYLENES; GENE EXPRESSION REGULATION, PLANT; INDOLEACETIC ACIDS; PLANT ROOT CAP; PLANT ROOTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEEDLING; STARCH; TRANSCRIPTION, GENETIC; ZEA MAYS;

EID: 56049121788     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/ssm027     Document Type: Article

References (58)

1. Aloni, R., Langhans, M., Aloni, E., and Ullrich, C.I. (2004). Role of cytokinin in the regulation of root gravitropism. Planta 220, 177-182. (Pubitemid 40033013)
2. Aloni, R., Langhans, M., Aloni, E., Dreieicher, E., and Ullrich, C.I. (2005). Root-synthesized cytokinin in Arabidopsis is distributed in the shoot by the transpiration stream. J. Exp. Bot. 56, 1535-1544. (Pubitemid 40764442)
3. Aloni, R., Aloni, E., Langhans, M., and Ullrich, C. (2006). Role of cytokinin and auxin in shaping root architecture: regulating vasculature differentiation, lateral root initiation, root apical dominance and root gravitropism. Ann. Bot 97, 883-893.
4. Alonso, J.M., Stepanova, A.N., Solano, R., Wisman, E., Ferrari, S., Ausubel, F.M., and Ecker, J.R. (2003). Five components of the ethylene-response pathway identified in a screen for weak ethylene-insensitive mutants in Arabidopsis. Proc. Natl Acad. Sci. U S A 100, 2992-2997. (Pubitemid 36297611)
5. Barlow, P.W. (2003). The root cap: cell dynamics, cell differentiation and cap function. J. Plant Growth Regul. 21, 261-286.
6. Barlow, P.W. (1974a). Regeneration of the cap of Zea mays. New Phytol. 73, 937-954.
7. Barlow, P.W. (1974b). Recovery of geotropism after removal of the root cap. J. Exp. Bot. 25, 1137-1148.
8. Beyer, E.M. (1976). A potent inhibitor of ethylene action in plants. Plant Physiol. 58, 268-271.
9. Blancaflor, E.B., Fasano, J.M., and Gilroy, S. (1998). Mapping the functional roles of cap cells in the response of Arabidopsis primary roots to gravity. Plant Physiol. 116, 213-222. (Pubitemid 28503856)
10. Bleecker, A.B., Estelle, M.A., Somerville, C., and Kende, H. (1988). Insensitivity to ethylene conferred by a dominant mutation in Arabidopsis thaliana. Science 241, 1086-1089.
11. Blilou, I., Xu, J., Wildwater, M., Willemsen, V., Paponov, I., Friml, J., Heidstra, R., Aida, M., Palme, K., and Scheres, B. (2005). The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433, 39-44. (Pubitemid 40101136)
12. Bradley, D., Carpenter, R., Sommer, H., Hartley, N., and Coen, E. (1993). Complementary floral homeotic phenotypes result from opposite orientations of a transposon at the plena locus of Antirrhinum. Cell 72, 85-95. (Pubitemid 23029695)
13. Buer, C.S., Sukumar, P., and Muday, G.K. (2006). Ethylene modulates flavonoid accumulation and gravitropic responses in roots of Arabidopsis. Plant Physiol. 140, 1384-1396. (Pubitemid 43956223)
14. Cary, A.J., Liu, W., and Howell, S.H. (1995). Cytokinin action is coupled to ethylene in its effects on the inhibition of root and hypocotyl elongation in Arabidopsis thaliana seedlings. Plant Physiol. 107, 1075-1082.
15. Chadwick, A.V., and Burg, S.P. (1967). An explanation of the inhibition of root growth caused by indole-3-acetic acid. Plant Physiol. 42, 415-420.
16. Chae, H.S., Faure, F., and Kieber, J.J. (2003). The eto1, eto2, and eto3 mutations and cytokinin treatment increase ethylene biosynthesis in Arabidopsis by increasing the stability of ACS protein. Plant Cell 15, 545-559. (Pubitemid 36230004)
17. Cholodny, N. (1926). Beiträge zur Analyse der geotropischen Reaktion. Jahrb. Wiss. Bot. 65, 447-459.
18. Clark, D.G., Gubrium, E.K., Barrett, J.E., Nell, T.A., and Klee, H.J. (1999). Root formation in ethylene-insensitive plants. Plant Physiol. 121, 53-60.
19. Dharmasiri, S., Swarup, R., Mockaitis, K., Dharmasiri, N., Singh, S.K., Kowalchyk, M., Marchant, A., Mills, S., Sandberg, G., Bennett, M.J., and Estelle, M. (2006). AXR4 is required for localization of the auxin influx facilitator AUX1. Science 312, 1218-20. (Pubitemid 43801148)
20. Edelmann, H.G., and Roth, U. (2006). Gravitropic plant growth regulation and ethylene: an unsought cardinal coordinate for a disused model. Protoplasma 229, 183-191. (Pubitemid 44974254)
21. Gallie, D.R., and Young, T.E. (2004). The ethylene biosynthetic and perception machinery is differentially expressed during endosperm and embryo development in maize. Mol. Gen. Genomics 271, 267-281. (Pubitemid 38591174)
22. Hahn, A., Firn, R.D., and Edelmann, H.G. (2006). Interacting signal transduction chains in gravity-stimulated maize roots. Signal Trans. 6, 449-455. (Pubitemid 46032220)
23. Hasenstein, K.H., and Evans, M.L. (1988). Effects of cations on hormone transport in primary roots of Zea mays. Plant Physiol. 86, 890-894.
24. Hussain, A., Black, C.R., Taylor, I.B., and Roberts, J.A. (1999). Soil compaction: a role for ethylene in regulating leaf expansion and shoot growth in tomato? Plant Physiol. 212, 1227-1238.
25. Iijima, M., Higuchi, T., and Barlow, P.W. (2004). Contribution of root cap mucilage and presence of an intact root cap in maize (Zea mays) to the reduction of soil mechanical impedance. Ann. Bot. 94, 473-477. (Pubitemid 41301666)
26. Jackson, D.P. (1991). In situ hybridization in plants. In Molecular Plant Pathology: A Practical Approach, D.J. Bowles, Gurr, S.J. and M. McPerson, eds : (Oxford University Press), pp. 163-174.
27. Jiang, K., Zhang, S., Lee, S., Tsai, G., Kim, K., Huang, H., Chilcott, C., Zhu, T., and Feldman, L.J. (2006). Transcription profile analyses identify genes and pathways central to root cap functions in maize. Plant Mol. Biol. 60, 343-363. (Pubitemid 43327573)
28. Juniper, B.E., Groves, S., Landau-Schachar, B., and Audus, L.J. (1966). Root cap and the perception of gravity. Nature 209, 93-94.
29. Kramer, S., Piotrowski, M., Kühnemann, F., and Edelmann, H.G. (2003). Physiological and biochemical characterization of ethylene-generated gravicompetence in primary shoots of coleoptile-less gravi-incompetent rye seedlings. J. Exp. Bot. 54, 2723-2732. (Pubitemid 37537863)
30. Le, J., Vandenbussche, F., Van Der Straeten, D., and Verbelen, J.P. (2001). In the early response of Arabidopsis roots to ethylene, cell elongation is up-and down-regulated and uncoupled from differentiation. Plant Physiol. 125, 519-522. (Pubitemid 32169858)
31. Lee, J.S., Chang, K.W., and Evans, M.L. (1990). Effects of ethylene on the kinetics of curvature and auxin redistribution in gravistimulated roots of Zea mays. Plant Physiol. 94, 1770-1775. (Pubitemid 120030102)
32. Ljung, K., Hull, A.K., Celenza, J., Yamada, M., Estelle, M., Normanly, J., and Sandberg, G. (2005). Sites and regulation of auxin biosynthesis in Arabidopsis roots. Plant Cell 17, 1090-1104. (Pubitemid 43142128)
33. Luschnig, C., Gaxiola, R.A., Grisafi, P., and Fink, G.R. (1998). EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev. 12, 2175-2187. (Pubitemid 28348041)
34. Mähönen, A.P., Bonke, M., Kauppinen, L., Riikonen, M., Benfey, P.N., and Helariutta, Y. (2000). A novel two-component hybrid molecule regulates vascular morphogenesis of the Arabidopsis root. Genes Dev. 14, 2938-2943.
35. Mähönen, A.P., Bishopp, A., Higuchi, M., Nieminen, K.M., Kinoshita, K., Törmänkangas, K., Ikeda, Y., Atsushiro, O., Kakimoto, T., and Helariutta, Y. (2006). Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development. Science 311, 94-98. (Pubitemid 43063066)
36. Masucci, J.D., and Schiefelbein, J.W. (1996). Hormones act downstream of TTG and GL2 to promote root hair outgrowth during epidermis development in the Arabidopsis root. Plant Cell 8, 1505-1517. (Pubitemid 26380824)
37. Miyawaki, K., Matsumoto-Kitano, M., and Kakimoto, T. (2004). Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin, cytokinin, and nitrate. Plant J. 37, 128-138. (Pubitemid 38078271)
38. Ottenschläger, I., Wolff, P., Wolverton, C., Bhalerao, R.P., Sandberg, G., Ishikawa, H., Evans, M., and Palme, K. (2003). Gravity-regulated differential auxin transport from columella to lateral root cap cells. Proc. Natl Acad. Sci. U S A 100, 2987-2991. (Pubitemid 36297610)
39. Pickett, F.B., Wilson, A.K., and Estelle, M. (1990). The aux1 mutation of Arabidopsis confers both auxin and ethylene resistance. Plant Physiol. 94, 1462-1466. (Pubitemid 120015716)
40. Rodriguez, F.I., Esch, J.J., Hall, A.E., Binder, B.M., Schaller, G.E., and Bleecker, A.B. (1999). A copper cofactor for the ethylene receptor ETR1 from Arabidopsis. Science 283, 996-998.
41. Růžička, K., Ljung, K., Vanneste, S., Podhorská, R., Beeckman, T., Friml, J., and Benková, E. (2007). Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell 19, 2197-2212. (Pubitemid 47347462)
42. Saltveit, M.E., and Dilley, D.R. (1978). Rapidly induced wound ethylene from excised segments of etiolated Pisum sativum L., cv. Alaska I: characterization of the response. Plant Physiol. 61, 447-450.
43. Smalle, J., and Van Der Straeten, D. (1997). Ethylene and vegetative growth. Physiol. Plant 100, 593-605.
44. Smith, K.A., and Robertson, P.D. (1971). Effect of ethylene on root extension of cereals. Nature 234, 148-149.
45. Solano, R., Stepanova, A., Chao, Q., and Ecker, J.R. (1998). Nuclear events in ethylene signalling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. Genes Dev. 12, 3703-3714. (Pubitemid 29019651)
46. Stepanova, A.N., Hoyt, J.M., Hamilton, A.A., and Alonso, J.M. (2005). A link between ethylene and auxin uncovered by the characterization of two root-specific ethylene-insensitive mutants in Arabidopsis. Plant Cell 17, 2230-2242. (Pubitemid 41672943)
47. Stepanova, A.N., Yun, J., Likhacheva, A.V., and Alonso, J.M. (2007). Multilevel interactions between ethylene and auxin in Arabidopsis roots. Plant Cell 19, 2169-2185. (Pubitemid 47347460)
48. Swarup, R., Perry, P., Hagenbeek, D., Van Der Straeten, D., Beemster, G.T.S., Sandberg, G., Bhalerao, R., Ljung, K., and Bennett, M.J. (2007). Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell 19, 2186-2196. (Pubitemid 47347461)
49. Tanimoto, M., Roberts, K., and Dolan, L. (1995). Ethylene is a positive regulator of root hair development in Arabidopsis thaliana. Plant J. 8, 943-948. (Pubitemid 3009654)
50. Vogel, J.P., Woeste, K.E., Theologis, A., and Kieber, J.J. (1998). Recessive and dominant mutations in the ethylene biosynthetic gene ACS5 of Arabidopsis confer cytokinin insensitivity and ethylene overproduction, respectively. Proc. Natl Acad. Sci. U S A 95, 4766-4771. (Pubitemid 28207988)
51. Went, F.W., and Thiemann, K.V. (1937). Phytohormones (New York: (Macmillan).
52. Whalen, M.C., and Feldman, L.J. (1988). The effect of ethylene on root growth of Zea mays seedlings. Can. J. Bot. 66, 719-723.
53. Wiśniewska, J., Xu, J., Seifertova, D., Brewer, B.P., Ruzicka, K., Blilou, I., Rouquie, D., Benkova, E., Scheres, B., and Friml, J. (2006). Polar PIN localization directs auxin flow in plants. Science 312, 883. (Pubitemid 43727314)
54. Yang, S.F., and Hofman, N.E. (1984). Ethylene biosynthesis and its regulation in higher plants. Annu. Rev. Plant Physiol. 35, 155-189.
55. Yang, Y., Hammes, U.Z., Taylor, C.G., Schachtmann, D.P., and Nielsen, E. (2006). High-affinity auxin transport by the AUX1 influx carrier protein. Curr. Biol. 16, 1123-1127. (Pubitemid 43815747)
56. Young, T.E., Meeley, R.B., and Gallie, D.R. (2004). ACC synthase expression regulates leaf performance and drought tolerance in maize. Plant J. 40, 813-825. (Pubitemid 39623254)
57. Yu, Y.B., and Yang, S.F. (1980). Biosynthesis of wound ethylene. Plant Physiol. 66, 281-285.
58. Zimmermann, R., and Werr, W. (2005). Pattern formation in the monocot embryo as revealed by NAM and CUC3 orthologues from Zea mays L.. Plant Mol. Biol. 58, 669-685. (Pubitemid 41297947)