TAA1-regulated local auxin biosynthesis in the root-apex transition zone mediates the aluminum-induced inhibition of root growth in Arabidopsis

Plant Cell

Volumn 26, Issue 7, 2014, Pages 2889-2904

  Yang, Zhong Bao ^a   Geng, Xiaoyu ^a   He, Chunmei ^a   Zhang, Feng ^a   Wang, Rong ^a   Horst, Walter J ^b   Ding, Zhaojun ^a  

^a SHANDONG UNIVERSITY   (China)

^b LEIBNIZ UNIVERSITY HANNOVER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

1-AMINOCYCLOPROPANE-1-CARBOXYLIC ACID; ALUMINUM; AMINO ACID; ARABIDOPSIS PROTEIN; ARF10 PROTEIN, ARABIDOPSIS; ARF16 PROTEIN, ARABIDOPSIS; ETHYLENE; ETHYLENE DERIVATIVE; INDOLEACETIC ACID DERIVATIVE; PHYTOHORMONE; TRANSCRIPTION FACTOR; TRYPTOPHAN AMINOTRANSFERASE;

ARABIDOPSIS; CELL WALL; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY; PLANT ROOT; REPORTER GENE; SIGNAL TRANSDUCTION; TRANSPORT AT THE CELLULAR LEVEL; UPREGULATION;

ALUMINUM; AMINO ACIDS, CYCLIC; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOLOGICAL TRANSPORT; CELL WALL; ETHYLENES; GENE EXPRESSION REGULATION, PLANT; GENES, REPORTER; INDOLEACETIC ACIDS; PLANT GROWTH REGULATORS; PLANT ROOTS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRYPTOPHAN TRANSAMINASE; UP-REGULATION;

EID: 84907308741     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.114.127993     Document Type: Article

References (89)

1. Alonso, J.M., Stepanova, A.N., Solano, R., Wisman, E., Ferrari, S., Ausubel, F.M., and Ecker, J.R. (2003). Five components of the ethyleneresponse pathway identified in a screen for weak ethylene-insensitive mutants in Arabidopsis. Proc. Natl. Acad. Sci. USA 100: 2992-2997.
2. Audic, S., and Claverie, J.M. (1997). The significance of digital gene expression profiles. Genome Res. 7: 986-995.
3. Baluška, F., Mancuso, S., Volkmann, D., and Barlow, P.W. (2010). Root apex transition zone: A signalling-response nexus in the root. Trends Plant Sci. 15: 402-408.
4. Baster, P., Robert, S., Kleine-Vehn, J., Vanneste, S., Kania, U., Grunewald, W., De Rybel, B., Beeckman, T., and Friml, J. (2013). SCF(TIR1/AFB)-auxin signalling regulates PIN vacuolar trafficking and auxin fluxes during root gravitropism. EMBO J. 32: 260-274.
5. Benjamini, Y., and Yekutieli, D. (2001). The control of the false discovery rate in multiple testing under dependency. Ann. Stat. 29: 1165-1188.
6. Benková, E., and Hejátko, J. (2009). Hormone interactions at the root apical meristem. Plant Mol. Biol. 69: 383-396.
7. Bielach, A., Duclercq, J., Marhavý, P., and Benková, E. (2012). Genetic approach towards the identification of auxin-cytokinin crosstalk components involved in root development. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367: 1469-1478.
8. Chen, L., Wang, T., Zhao, M., Tian, Q., and Zhang, W.H. (2012). Identification of aluminum-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. Planta 235: 375-386.
9. Delhaize, E., and Ryan, P.R. (1995). Aluminum toxicity and tolerance in plants. Plant Physiol. 107: 315-321.
10. Ding, Z., and De Smet, I. (2013). Localised ABA signalling mediates root growth plasticity. Trends Plant Sci. 18: 533-535.
11. Ding, Z., and Friml, J. (2010). Auxin regulates distal stem cell differentiation in Arabidopsis roots. Proc. Natl. Acad. Sci. USA 107: 12046-12051.
12. Ding, Z., et al. (2012). ER-localized auxin transporter PIN8 regulates auxin homeostasis and male gametophyte development in Arabidopsis. Nat. Commun. 3: 941-949.
13. Doncheva, S., Amenós, M., Poschenrieder, C., and Barceló, J. (2005). Root cell patterning: A primary target for aluminium toxicity in maize. J. Exp. Bot. 56: 1213-1220.
14. Duan, L., Dietrich, D., Ng, C.H., Chan, P.M., Bhalerao, R., Bennett, M.J., and Dinneny, J.R. (2013). Endodermal ABA signaling promotes lateral root quiescence during salt stress in Arabidopsis seedlings. Plant Cell 25: 324-341.
15. Eticha, D., Zahn, M., Bremer, M., Yang, Z., Rangel, A.F., Rao, I.M., and Horst, W.J. (2010). Transcriptomic analysis reveals differential gene expression in response to aluminium in common bean (Phaseolus vulgaris) genotypes. Ann. Bot. (Lond.) 105: 1119-1128.
16. Farrokhi, N., Burton, R.A., Brownfield, L., Hrmova, M., Wilson, S.M., Bacic, A., and Fincher, G.B. (2006). Plant cell wall biosynthesis: Genetic, biochemical and functional genomics approaches to the identification of key genes. Plant Biotechnol. J. 4: 145-167.
17. Fujiwara, T., Hirai, M.Y., Chino, M., Komeda, Y., and Naito, S. (1992). Effects of sulfur nutrition on expression of the soybean seed storage protein genes in transgenic petunia. Plant Physiol. 99: 263-268.
18. Fukaki, H., Nakao, Y., Okushima, Y., Theologis, A., and Tasaka, M. (2005). Tissue-specific expression of stabilized SOLITARY-ROOT/IAA14 alters lateral root development in Arabidopsis. Plant J. 44: 382-395.
19. 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.
20. Gifford, M.L., Dean, A., Gutierrez, R.A., Coruzzi, G.M., and Birnbaum, K.D. (2008). Cell-specific nitrogen responses mediate developmental plasticity. Proc. Natl. Acad. Sci. USA 105: 803-808.
21. Gribaa, A., Dardelle, F., Lehner, A., Rihouey, C., Burel, C., Ferchichi, A., Driouich, A., and Mollet, J.C. (2013). Effect of water deficit on the cell wall of the date palm (Phoenix dactylifera 'Deglet nour', Arecales) fruit during development. Plant Cell Environ. 36: 1056-1070.
22. Guilfoyle, T.J., and Hagen, G. (2007). Auxin response factors. Curr. Opin. Plant Biol. 10: 453-460.
23. Hayashi, K. (2012). The interaction and integration of auxin signaling components. Plant Cell Physiol. 53: 965-975.
24. Hayashi, K., Tan, X., Zheng, N., Hatate, T., Kimura, Y., Kepinski, S., and Nozaki, H. (2008). Small-molecule agonists and antagonists of F-box protein-substrate interactions in auxin perception and signaling. Proc. Natl. Acad. Sci. USA 105: 5632-5637.
25. He, W., et al. (2011). A small-molecule screen identifies L-kynurenine as a competitive inhibitor of TAA1/TAR activity in ethylene-directed auxin biosynthesis and root growth in Arabidopsis. Plant Cell 23: 3944-3960.
26. Horst, W.J., Wang, Y., and Eticha, D. (2010). The role of the root apoplast in aluminium-induced inhibition of root elongation and in aluminium resistance of plants: A review. Ann. Bot. (Lond.) 106: 185-197.
27. Illés, P., Schlicht, M., Pavlovkin, J., Lichtscheidl, I., Baluška, F., and Ovecka, M. (2006). Aluminium toxicity in plants: Internalization of aluminium into cells of the transition zone in Arabidopsis root apices related to changes in plasma membrane potential, endosomal behaviour, and nitric oxide production. J. Exp. Bot. 57: 4201-4213.
28. Iuchi, S., Koyama, H., Iuchi, A., Kobayashi, Y., Kitabayashi, S., Kobayashi, Y., Ikka, T., Hirayama, T., Shinozaki, K., and Kobayashi, M. (2007). Zinc finger protein STOP1 is critical for proton tolerance in Arabidopsis and coregulates a key gene in aluminum tolerance. Proc. Natl. Acad. Sci. USA 104: 9900-9905.
29. Jansen, L., Roberts, I., De Rycke, R., and Beeckman, T. (2012). Phloemassociated auxin response maxima determine radial positioning of lateral roots in maize. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367: 1525-1533.
30. Kobayashi, Y., Hoekenga, O.A., Itoh, H., Nakashima, M., Saito, S., Shaff, J.E., Maron, L.G., Piñeros, M.A., Kochian, L.V., and Koyama, H. (2007). Characterization of AtALMT1 expression in aluminum-inducible malate release and its role for rhizotoxic stress tolerance in Arabidopsis. Plant Physiol. 145: 843-852.
31. Kobayashi, Y., Kobayashi, Y., Sugimoto, M., Lakshmanan, V., Iuchi, S., Kobayashi, M., Bais, H.P., and Koyama, H. (2013). Characterization of the complex regulation of AtALMT1 expression in response to phytohormones and other inducers. Plant Physiol. 162: 732-740.
32. Kochian, L.V., Hoekenga, O.A., and Pineros, M.A. (2004). How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annu. Rev. Plant Biol. 55: 459-493.
33. Kollmeier, M., Felle, H.H., and Horst, W.J. (2000). Genotypical differences in aluminum resistance of maize are expressed in the distal part of the transition zone. Is reduced basipetal auxin flow involved in inhibition of root elongation by aluminum? Plant Physiol. 122: 945-956.
34. Kumari, M., Taylor, G.J., and Deyholos, M.K. (2008). Transcriptomic responses to aluminum stress in roots of Arabidopsis thaliana. Mol. Genet. Genomics 279: 339-357.
35. Lavenus, J., Goh, T., Roberts, I., Guyomarc'h, S., Lucas, M., De Smet, I., Fukaki, H., Beeckman, T., Bennett, M., and Laplaze, L. (2013). Lateral root development in Arabidopsis: Fifty shades of auxin. Trends Plant Sci. 18: 450-458.
36. Li, R., Yu, C., Li, Y., Lam, T.W., Yiu, S.M., Kristiansen, K., and Wang, J. (2009). SOAP2: An improved ultrafast tool for short read alignment. Bioinformatics 25: 1966-1967.
37. Liu, J., Magalhaes, J.V., Shaff, J., and Kochian, L.V. (2009). Aluminumactivated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminum tolerance. Plant J. 57: 389-399.
38. Liu, P.P., Montgomery, T.A., Fahlgren, N., Kasschau, K.D., Nonogaki, H., and Carrington, J.C. (2007). Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. Plant J. 52: 133-146.
39. Liu, X., Huang, J., Wang, Y., Khanna, K., Xie, Z., Owen, H.A., and Zhao, D. (2010). The role of floral organs in carpels, an Arabidopsis loss-of-function mutation in microRNA160a, in organogenesis and the mechanism regulating its expression. Plant J. 62: 416-428.
40. Ma, J.F., Shen, R., Nagao, S., and Tanimoto, E. (2004). Aluminum targets elongating cells by reducing cell wall extensibility in wheat roots. Plant Cell Physiol. 45: 583-589.
41. Mai, Y.X., Wang, L., and Yang, H.Q. (2011). A gain-of-function mutation in IAA7/AXR2 confers late flowering under short-day light in Arabidopsis. J. Integr. Plant Biol. 53: 480-492.
42. Maron, L.G., Kirst, M., Mao, C., Milner, M.J., Menossi, M., and Kochian, L.V. (2008). Transcriptional profiling of aluminum toxicity and tolerance responses in maize roots. New Phytol. 179: 116-128.
43. Massot, N., Nicander, B., Barceló, J., Poschenrieder, C., and Tillberg, E. (2002). A rapid increase in cytokinin levels and enhanced ethylene evolution precede Al3+-induced inhibition of root growth in bean seedlings (Phaseolus vulgaris L.). Plant Growth Regul. 37: 105-112.
44. Moore, A., Donahue, C.J., Bauer, K.D., and Mather, J.P. (1998). Simultaneous measurement of cell cycle and apoptotic cell death. Methods Cell Biol. 57: 265-278.
45. Mortazavi, A., Williams, B.A., McCue, K., Schaeffer, L., and Wold, B. (2008). Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5: 621-628.
46. Muday, G.K., Rahman, A., and Binder, B.M. (2012). Auxin and ethylene: Collaborators or competitors? Trends Plant Sci. 17: 181-195.
47. Nishimura, T., Nakano, H., Hayashi, K., Niwa, C., and Koshiba, T. (2009). Differential downward stream of auxin synthesized at the tip has a key role in gravitropic curvature via TIR1/AFBs-mediated auxin signaling pathways. Plant Cell Physiol. 50: 1874-1885.
48. 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.
49. Overvoorde, P., Fukaki, H., and Beeckman, T. (2010). Auxin control of root development. Cold Spring Harb. Perspect. Biol. 2: a001537.
50. Pan, W., Shou, S., Zhou, X., Guo, T., Zhu, M., and Pan, J. (2011). Alinduced cell wall hydroxyproline-rich glycoprotein accumulation is involved in alleviating Al toxicity in rice. Acta Physiol. Plant. 33: 601-608.
51. 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.
52. Rademacher, E.H., Möller, B., Lokerse, A.S., Llavata-Peris, C.I., van den Berg, W., and Weijers, D. (2011). A cellular expression map of the Arabidopsis AUXIN RESPONSE FACTOR gene family. Plant J. 68: 597-606.
53. Rangel, A.F., Rao, I.M., and Horst, W.J. (2007). Spatial aluminium sensitivity of root apices of two common bean (Phaseolus vulgaris L.) genotypes with contrasting aluminium resistance. J. Exp. Bot. 58: 3895-3904.
54. Rosquete, M.R., von Wangenheim, D., Marhavý, P., Barbez, E., Stelzer, E.H., Benková, E., Maizel, A., and Kleine-Vehn, J. (2013). An auxin transport mechanism restricts positive orthogravitropism in lateral roots. Curr. Biol. 23: 817-822.
55. Ruzicka, 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.
56. Ryan, P.R., and Kochian, L.V. (1993). Interaction between aluminum toxicity and calcium uptake at the root apex in near-isogenic lines of wheat (Triticum aestivum L.) differing in aluminum tolerance. Plant Physiol. 102: 975-982.
57. Ryan, P.R., Ditomaso, J.M., and Kochian, L.V. (1993). Aluminum toxicity in roots: An investigation of spatial sensitivity and the role of the root cap. J. Exp. Bot. 44: 437-446.
58. Schlicht, M., Strnad, M., Scanlon, M.J., Mancuso, S., Hochholdinger, F., Palme, K., Volkmann, D., Menzel, D., and Baluška, F. (2006). Auxin immunolocalization implicates vesicular neurotransmitter-like mode of polar auxin transport in root apices. Plant Signal. Behav. 1: 122-133.
59. Sivaguru, M., and Horst, W.J. (1998). The distal part of the transition zone is the most aluminum-sensitive apical root zone of maize. Plant Physiol. 116: 155-163.
60. Sivaguru, M., Baluška, F., Volkmann, D., Felle, H.H., and Horst, W.J. (1999). Impacts of aluminum on the cytoskeleton of the maize root apex. Short-term effects on the distal part of the transition zone. Plant Physiol. 119: 1073-1082.
61. Sivaguru, M., Liu, J., and Kochian, L.V. (2013). Targeted expression of SbMATE in the root distal transition zone is responsible for sorghum aluminum resistance. Plant J. 76: 297-307.
62. Stepanova, A.N., Robertson-Hoyt, J., Yun, J., Benavente, L.M., Xie, D.Y., Dolezal, K., Schlereth, A., Jürgens, G., and Alonso, J.M. (2008). TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133: 177-191.
63. 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.
64. Stepanova, A.N., Yun, J., Robles, L.M., Novak, O., He, W., Guo, H., Ljung, K., and Alonso, J.M. (2011). The Arabidopsis YUCCA1 flavin monooxygenase functions in the indole-3-pyruvic acid branch of auxin biosynthesis. Plant Cell 23: 3961-3973.
65. Steward, N., Martin, R., Engasser, J.M., and Goergen, J.L. (1999). A new methodology for plant cell viability assessment using intracellular esterase activity. Plant Cell Rep. 19: 171-176.
66. Sun, P., Tian, Q.Y., Chen, J., and Zhang, W.H. (2010). Aluminiuminduced inhibition of root elongation in Arabidopsis is mediated by ethylene and auxin. J. Exp. Bot. 61: 347-356.
67. Sun, P., Tian, Q.Y., Zhao, M.G., Dai, X.Y., Huang, J.H., Li, L.H., and Zhang, W.H. (2007). Aluminum-induced ethylene production is associated with inhibition of root elongation in Lotus japonicus L. Plant Cell Physiol. 48: 1229-1235.
68. Swarup, R., Perry, P., Hagenbeek, D., Van Der Straeten, D., Beemster, G.T., 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.
69. Tabuchi, A., and Matsumoto, H. (2001). Changes in cell-wall properties of wheat (Triticum aestivum) roots during aluminum-induced growth inhibition. Physiol. Plant. 112: 353-358.
70. Tao, Y., et al. (2008). Rapid synthesis of auxin via a new tryptophandependent pathway is required for shade avoidance in plants. Cell 133: 164-176.
71. Teale, W.D., Paponov, I.A., Ditengou, F., and Palme, K. (2005). Auxin and the developing root of Arabidopsis thaliana. Physiol. Plant. 123: 130-138.
72. Teale, W.D., Paponov, I.A., and Palme, K. (2006). Auxin in action: Signalling, transport and the control of plant growth and development. Nat. Rev. Mol. Cell Biol. 7: 847-859.
73. Tian, H., Niu, T., Yu, Q., Quan, T., and Ding, Z. (2013). Auxin gradient is crucial for the maintenance of root distal stem cell identity in Arabidopsis. Plant Signal. Behav. 8: e26429.
74. Tian, H., Wabnik, K., Niu, T., Li, H., Yu, Q., Pollmann, S., Vanneste, S., Govaerts, W., Rolcík, J., Geisler, M., Friml, J., and Ding, Z. (2014a). WOX5-IAA17 feedback circuit-mediated cellular auxin response is crucial for the patterning of root stem cell niches in Arabidopsis. Mol. Plant 7: 277-289.
75. Tian, Q., Zhang, X., Ramesh, S., Gilliham, M., Tyerman, S.D., and Zhang, W.H. (2014b). Ethylene negatively regulates aluminiuminduced malate efflux from wheat roots and tobacco cells transformed with TaALMT1. J. Exp. Bot. 65: 2415-2426.
76. Tsutsui, T., Yamaji, N., Huang, C.F., Motoyama, R., Nagamura, Y., and Ma, J.F. (2012). Comparative genome-wide transcriptional analysis of Al-responsive genes reveals novel Al tolerance mechanisms in rice. PLoS ONE 7: e48197-e48205.
77. Vanneste, S., et al. (2005). Cell cycle progression in the pericycle is not sufficient for SOLITARY ROOT/IAA14-mediated lateral root initiation in Arabidopsis thaliana. Plant Cell 17: 3035-3050.
78. Verbelen, J.P., De Cnodder, T., Le, J., Vissenberg, K., and Baluška, F. (2006). The 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.
79. Von Uexküll, H.R., and Mutert, E. (1995). Global extent, development and economic impact of acid soils. Plant Soil 171: 1-15.
80. Wang, J.W., Wang, L.J., Mao, Y.B., Cai, W.J., Xue, H.W., and Chen, X.Y. (2005). Control of root cap formation by microRNA-targeted auxin response factors in Arabidopsis. Plant Cell 17: 2204-2216.
81. Yang, J.L., Zhu, X.F., Peng, Y.X., Zheng, C., Li, G.X., Liu, Y., Shi, Y.Z., and Zheng, S.J. (2011a). Cell wall hemicellulose contributes significantly to aluminum adsorption and root growth in Arabidopsis. Plant Physiol. 155: 1885-1892.
82. Yang, Z.B., Eticha, D., Albacete, A., Rao, I.M., Roitsch, T., and Horst, W.J. (2012). Physiological and molecular analysis of the interaction between aluminium toxicity and drought stress in common bean (Phaseolus vulgaris). J. Exp. Bot. 63: 3109-3125.
83. Yang, Z.B., Eticha, D., Rotter, B., Rao, I.M., and Horst, W.J. (2011b). Physiological and molecular analysis of polyethylene glycol-induced reduction of aluminium accumulation in the root tips of common bean (Phaseolus vulgaris). New Phytol. 192: 99-113.
84. Yang, Z.B., Rao, I.M., and Horst, W.J. (2013). Interaction of aluminium and drought stress on root growth and crop yield on acid soils. Plant Soil 372: 3-25.
85. Zeng, Q.Y., Yang, C.Y., Ma, Q.B., Li, X.P., Dong, W.W., and Nian, H. (2012). Identification of wild soybean miRNAs and their target genes responsive to aluminum stress. BMC Plant Biol. 12: 182.
86. Zhao, Y., Christensen, S.K., Fankhauser, C., Cashman, J.R., Cohen, J.D., Weigel, D., and Chory, J. (2001). A role for flavin monooxygenaselike enzymes in auxin biosynthesis. Science 291: 306-309.
87. Zhou, W., Wei, L., Xu, J., Zhai, Q., Jiang, H., Chen, R., Chen, Q., Sun, J., Chu, J., Zhu, L., Liu, C.M., and Li, C. (2010). Arabidopsis tyrosylprotein sulfotransferase acts in the auxin/PLETHORA pathway in regulating postembryonic maintenance of the root stem cell niche. Plant Cell 22: 3692-3709.
88. Zhu, X.F., Lei, G.J., Wang, Z.W., Shi, Y.Z., Braam, J., Li, G.X., and Zheng, S.J. (2013). Coordination between apoplastic and symplastic detoxification confers plant aluminum resistance. Plant Physiol. 162: 1947-1955.
89. Zhu, X.F., et al. (2012). XTH31, encoding an in vitro XEH/XET-active enzyme, regulates aluminum sensitivity by modulating in vivo XET action, cell wall xyloglucan content, and aluminum binding capacity in Arabidopsis. Plant Cell 24: 4731-4747.