Coordination between apoplastic and symplastic detoxification confers plant aluminum resistance

Plant Physiology

Volumn 162, Issue 4, 2013, Pages 1947-1955

  Zhu, Xiao Fang ^a   Lei, Gui Jie ^a   Wang, Zhi Wei ^a   Shi, Yuan Zhi ^c   Braam, Janet ^d   Li, Gui Xin ^b   Zheng, Shao Jian ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b ZHEJIANG UNIVERSITY   (China)

^c BEIJING HOSPITAL   (China)

^d RICE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 NAPHTHYLACETIC ACID; 1-NAPHTHALENEACETIC ACID; ABC TRANSPORTER; ALS1 PROTEIN, ARABIDOPSIS; ALUMINUM; ARABIDOPSIS PROTEIN; ARYLACETIC ACID DERIVATIVE; INDOLEACETIC ACID; INDOLEACETIC ACID DERIVATIVE;

ARABIDOPSIS; ARTICLE; CYTOSOL; DRUG DETOXIFICATION; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MERISTEM; METABOLISM; MUTATION; PHYSIOLOGY; PLANT ROOT;

ALUMINUM; ARABIDOPSIS; ARABIDOPSIS PROTEINS; ATP-BINDING CASSETTE TRANSPORTERS; CYTOSOL; GENE EXPRESSION REGULATION, PLANT; INDOLEACETIC ACIDS; MERISTEM; METABOLIC DETOXICATION, DRUG; MUTATION; NAPHTHALENEACETIC ACIDS; PLANT ROOTS;

EID: 84880988822     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.219147     Document Type: Article

References (55)

1. Barlier I, Kowalczyk M, Marchant A, Ljung K, Bhalerao R, Bennett M, Sandberg G, Bellini C (2000) The SUR2 gene of Arabidopsis thaliana encodes the cytochrome P450 CYP83B1, a modulator of auxin homeostasis. Proc Natl Acad Sci USA 97: 14819-14824
2. Becnel J, Natarajan M, Kipp A, Braam J (2006) Developmental expression patterns of Arabidopsis XTH genes reported by transgenes and Genevestigator. Plant Mol Biol 61: 451-467
3. Boerjan W, Cervera M-T, Delarue M, Beeckman T, Dewitte W, Bellini C, Caboche M, Van Onckelen H, Van Montagu M, Inzé D (1995) Superroot, a recessive mutation in Arabidopsis, confers auxin overproduction. Plant Cell 7: 1405-1419
4. Chang YC, Yamamoto Y, Matsumoto H (1999) Accumulation of aluminium in the cell wall pectin in cultured tobacco (Nicotiana tabacum L.) cells treated with a combination of aluminium and iron. Plant Cell Environ 22: 1009-1017
5. Clarkson DT (1967) Interactions between aluminum and phosphorus on root surfaces and cell wall material. Plant Soil 27: 347-356
6. Delarue M, Prinsen E, Onckelen HV, Caboche M, Bellini C (1998) Sur2 mutations of Arabidopsis thaliana define a new locus involved in the control of auxin homeostasis. Plant J 14: 603-611
7. Doncheva S, Amenós M, Poschenrieder C, Barceló J (2005) Root cell patterning: a primary target for aluminium toxicity in maize. J Exp Bot 56: 1213-1220
8. Eticha D, Stass A, Horst WJ (2005a) Cell-wall pectin and its degree of methylation in the maize root-apex: significance for genotypic differences in aluminium resistance. Plant Cell Environ 28: 1410-1420
9. Eticha D, Stass A, Horst WJ (2005b) Localization of aluminium in the maize root apex: can morin detect cell wall-bound aluminium? J Exp Bot 56: 1351-1357
10. Ezaki B, Kiyohara H, Matsumoto H, Nakashima S (2007) Overexpression of an auxilin-like gene (F9E10.5) can suppress Al uptake in roots of Arabidopsis. J Exp Bot 58: 497-506
11. Foy CD (1988) Plant adaptation to acid, aluminum-toxic soils. Commun Soil Sci Plant 19: 959-987
12. Fry SC, Smith RC, Renwick KF, Martin DJ, Hodge SK, Matthews KJ (1992) Xyloglucan endotransglycosylase, a new wall-loosening enzyme activity from plants. Biochem J 282: 821-828
13. Hagen G, Guilfoyle T (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol Biol 49: 373-385
14. Hoekenga OA, Maron LG, Piñeros MA, Cançado GMA, Shaff J, Kobayashi Y, Ryan PR, Dong B, Delhaize E, Sasaki T, et al (2006) AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. Proc Natl Acad Sci USA 103: 9738-9743
15. Horst WJ (1995) The role of the apoplast in aluminium toxicity and resistance of higher plants: a review. Z Pflanzenernähr Bodenkd 158: 419-428
16. Horst WJ, Wang Y, 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
17. Huang CF, Yamaji N, Chen Z, Ma JF (2012) A tonoplast-localized half-size ABC transporter is required for internal detoxification of aluminum in rice. Plant J 69: 857-867
18. Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annu Rev Plant Physiol Plant Mol Biol 46: 237-260
19. Kochian LV, Hoekenga OA, Piñeros MA (2004) How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annu Rev Plant Biol 55: 459-493
20. Kollmeier M, Felle HH, Horst WJ (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
21. Larsen PB, Cancel J, Rounds M, Ochoa V (2007) Arabidopsis ALS1 encodes a root tip and stele localized half type ABC transporter required for root growth in an aluminum toxic environment. Planta 225: 1447-1458
22. Larsen PB, Degenhardt J, Tai CY, Stenzler LM, Howell SH, Kochian LV (1998) Aluminum-resistant Arabidopsis mutants that exhibit altered patterns of aluminum accumulation and organic acid release from roots. Plant Physiol 117: 9-18
23. Larsen PB, Geisler MJ, Jones CA, Williams KM, Cancel JD (2005) ALS3 encodes a phloem-localized ABC transporter-like protein that is required for aluminum tolerance in Arabidopsis. Plant J 41: 353-363
24. Larsen PB, Tai CY, Kochian LV, Howell SH (1996) Arabidopsis mutants with increased sensitivity to aluminum. Plant Physiol 110: 743-751
25. Liu Q, Yang JL, He LS, Li YY, Zheng SJ (2008) Effect of aluminum on cell wall, plasma membrane, antioxidants and root elongation in triticale. Biol Plant 52: 87-92
26. Ljung K, Hull AK, Celenza J, Yamada M, Estelle M, Normanly J, Sandberg G (2005) Sites and regulation of auxin biosynthesis in Arabidopsis roots. Plant Cell 17: 1090-1104
27. Ma JF (2000) Role of organic acids in detoxification of aluminum in higher plants. Plant Cell Physiol 41: 383-390
28. Ma JF, Furukawa J (2003) Recent progress in the research of external Al detoxification in higher plants: a minireview. J Inorg Biochem 97: 46-51
29. Ma JF, Hiradate S (2000) Form of aluminium for uptake and translocation in buckwheat (Fagopyrum esculentum Moench). Planta 211: 355-360
30. Ma JF, Hiradate S, Nomoto K, Iwashita T, Matsumoto H (1997a) Internal detoxification mechanism of Al in hydrangea. Identification of Al form in the leaves. Plant Physiol 113: 1033-1039
31. Ma JF, Hiradate S, Nomoto K, Iwashita T, Matsumoto H (1997b) Internal detoxification mechanism of Al in hydrangea (identification of Al form in the leaves). Plant Physiol 113: 1033-1039
32. Ma JF, Shen RF, Nagao S, Tanimoto E (2004) Aluminum targets elongating cells by reducing cell wall extensibility in wheat roots. Plant Cell Physiol 45: 583-589
33. Ma JF, Zheng SJ, Hiradate S, Matsumoto H (1997c) Detoxifying aluminium with buckwheat. Nature 390: 569-570
34. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plant 15: 473-496
35. Nezames CD, Sjogren CA, Barajas JF, Larsen PB (2012) The Arabidopsis cell cycle checkpoint regulators TANMEI/ALT2 and ATR mediate the active process of aluminum-dependent root growth inhibition. Plant Cell 24: 608-621
36. Nishitani K, Tominaga R (1992) Endo-xyloglucan transferase, a novel class of glycosyltransferase that catalyzes transfer of a segment of xyloglucan molecule to another xyloglucan molecule. J Biol Chem 267: 21058-21064
37. Pan JW, Zhu MY, Chen H (2001) Aluminum-induced cell death in root-tip cells of barley. Environ Exp Bot 46: 71-79
38. Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Physiol Plant Mol Biol 52: 527-560
39. Schmohl N, Horst WJ (2000) Cell wall pectin content modulates aluminium sensitivity of Zea mays (L.) cells grown in suspension culture. Plant Cell Environ 23: 735-742
40. Shen H, Hou NY, Schlicht M, Wan YL, Baluska F (2008) Aluminum toxicity targets PIN2 in Arabidopsis root apices: effects on PIN2 endocytosis vesicular recycling, and polar auxin transport. Chin Sci Bull 53: 2480-2487
41. Shen RF, Ma JF, Kyo M, Iwashita T (2002) Compartmentation of aluminium in leaves of an Al-accumulator, Fagopyrum esculentum Moench. Planta 215: 394-398
42. Sun P, Tian QY, Chen J, Zhang WH (2010) Aluminium-induced inhibition of root elongation in Arabidopsis is mediated by ethylene and auxin. J Exp Bot 61: 347-356
43. Tabuchi A, Matsumoto H (2001) Changes in cell-wall properties of wheat (Triticum aestivum) roots during aluminum-induced growth inhibition. Physiol Plant 112: 353-358
44. Taylor GJ (1991) Current views of the aluminum stress response: the physiological basis of tolerance. Curr Top Plant Biochem Physiol 10: 57-93
45. Thompson JE, Fry SC (2001) Restructuring of wall-bound xyloglucan by transglycosylation in living plant cells. Plant J 26: 23-34
46. von Uexküll HR, Mutert E (1995) Global extent, development and economic impact of acid soils. In RA Date, NJ Grundon, GE Raymet, ME Probert, eds, Plant-Soil Interactions at Low pH: Principles and Management. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 5-19
47. Xia JX, Yamaji N, Kasai T, Ma JF (2010) Plasma membrane-localized transporter for aluminum in rice. Proc Natl Acad Sci USA 107: 18381-18385
48. Yamaji N, Huang CF, Nagao S, Yano M, Sato Y, Nagamura Y, Ma JF (2009) A zinc finger transcription factor ART1 regulates multiple genes implicated in aluminum tolerance in rice. Plant Cell 21: 3339-3349
49. Yang JL, Li YY, Zhang YJ, Zhang SS, Wu YR, Wu P, Zheng SJ (2008) Cell wall polysaccharides are specifically involved in the exclusion of aluminum from the rice root apex. Plant Physiol 146: 602-611
50. Yang JL, Zhu XF, Peng YX, Zheng C, Li GX, Liu Y, Shi YZ, Zheng SJ (2011b) Cell wall hemicellulose contributes significantly to aluminum adsorption and root growth in Arabidopsis. Plant Physiol 155: 1885-1892
51. Yang JL, Zhu XF, Zheng C, Zhang YJ, Zheng SJ (2011a) Genotypic differences in Al resistance and the role of cell-wall pectin in Al exclusion from the root apex in Fagopyrum tataricum. Ann Bot (Lond) 107: 371-378
52. Zhao Y, 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
53. Zheng SJ, Lin XY, Yang JL, Liu Q, Tang CX (2004) The kinetics of aluminum adsorption and desorptiion by root cell walls of an aluminum resistant wheat (Triticum aestivum L.) cultivar. Plant Soil 261: 85-90
54. Zhou Y, Xu XY, Chen LQ, Yang JL, Zheng SJ (2012) Nitric oxide exacerbates Al-induced inhibition of root elongation in rice bean by affecting cell wall and plasma membrane properties. Phytochemistry 76: 46-51
55. Zhu XF, Shi YZ, Lei GJ, Fry SC, Zhang BC, Zhou YH, Braam J, Jiang T, Xu XY, Mao CZ, et al (2012) XTH31, encoding an in-vitro XEH/XET-active enzyme, controls Al sensitivity by modulating in-vivo XET action, cell wall xyloglucan content and Al binding capacity in Arabidopsis. Plant Cell 24: 4731-4747