GSA-1/ARG1 protects root gravitropism in Arabidopsis under ammonium stress

New Phytologist

Volumn 200, Issue 1, 2013, Pages 97-111

  Zou, Na ^a,b   Li, Baohai ^b   Chen, Hao ^c   Su, Yanhua ^b   Kronzucker, Herbert J ^d   Xiong, Liming ^c   Baluška, František ^e   Shi, Weiming ^b  

^a JIANGXI AGRICULTURAL UNIVERSITY   (China)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^c DONALD DANFORTH PLANT SCIENCE CENTER   (United States)

^d UNIVERSITY OF TORONTO   (Canada)

^e UNIVERSITY OF BONN   (Germany)

Author keywords

Ammonium; AUX1; Auxin transport; GSA 1 ARG1; PIN2; Root gravitropism

Indexed keywords

ACCLIMATION; AGAR; AMMONIUM; ANGIOSPERM; BIOASSAY; GENE EXPRESSION; INHIBITION; MUTATION; NUTRIENT AVAILABILITY; PLANT; ROOT ARCHITECTURE; WATER AVAILABILITY;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

AMMONIA; AMMONIUM DERIVATIVE; ARABIDOPSIS PROTEIN; ARG1 PROTEIN, ARABIDOPSIS; AUX1 PROTEIN, ARABIDOPSIS; GSA 1 PROTEIN, ARABIDOPSIS; GSA-1 PROTEIN, ARABIDOPSIS; PIN2 PROTEIN, ARABIDOPSIS;

ADAPTATION; ARABIDOPSIS; ARTICLE; AUX1; AUXIN TRANSPORT; GENETICS; GRAVITROPISM; GRAVITY; GSA-1/ARG1; METABOLISM; MUTATION; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PIN2; PLANT GENE; PLANT ROOT; ROOT GRAVITROPISM;

AMMONIUM; AUX1; AUXIN TRANSPORT; GSA-1/ARG1; PIN2; ROOT GRAVITROPISM;

ADAPTATION, PHYSIOLOGICAL; AMMONIUM COMPOUNDS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENES, PLANT; GRAVITATION; GRAVITROPISM; MUTATION; PLANT ROOTS; STRESS, PHYSIOLOGICAL;

EID: 84883050837     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12365     Document Type: Article

References (58)

1. Bainbridge K, Guyomarc'h S, Bayer E, Swarup R, Bennett M, Mandel T, Kuhlemeier C. 2008. Auxin influx carriers stabilize phyllotactic patterning. Genes & Development 22: 810-823.
2. Baluška F, Mancuso S, Volkmann D, Barlow PW. 2010. Root apex transition zone: a signalling-response nexus in the root. Trends in Plant Science 15: 402-408.
3. Blancaflor EB, Fasano JM, Gilroy S. 1998. Mapping the functional roles of cap cells in the response of Arabidopsis primary roots to gravity. Plant Physiology 116: 213-222.
4. Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B. 2005. The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433: 39-44.
5. Bonser AM, Lynch J, Snapp S. 1996. Effect of phosphorus deficiency on growth angle of basal roots in Phaseolus vulgaris. New Phytologist 132: 281-288.
6. Boonsirichai K, Sedbrook JC, Chen R, Gilroy S, Masson PH. 2003. ALTERED RESPONSE TO GRAVITY is a peripheral membrane protein that modulates gravity-induced cytoplasmic alkalinization and lateral auxin transport in plant statocytes. Plant Cell 15: 2612-2625.
7. + toxicity in higher plants: a critical review. Journal of Plant Physiology 159: 567-584.
8. Caspar T, Pickard BG. 1989. Gravitropism in a starchless mutant of Arabidopsis. Planta 177: 185-197.
9. Chavarría-Krauser A, Nagel KA, Palme K, Schurr U, Walter A, Scharr H. 2008. Spatio-temporal quantification of differential growth processes in root growth zones based on a novel combination of image sequence processing and refined concepts describing curvature production. New Phytologist 177: 811-821.
10. Chen R, Guan C, Boonsirichai K, Masson PH. 2002. Complex physiological and molecular processes underlying root gravitropism. Plant Molecular Biology 49: 305-317.
11. Clough SJ, Bent AF. 1998. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant Journal 16: 735-743.
12. Forde B, Lorenzo H. 2001. The nutritional control of root development. Plant and Soil 232: 51-68.
13. Friml J. 2003. Auxin transport - shaping the plant. Current Opinion in Plant Biology 6: 7-12.
14. 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.
15. Ge L, Peer W, Robert S, Swarup R, Ye S, Prigge M, Cohen J, Friml J, Murphy A, Tang D. 2010. Arabidopsis ROOT UVB SENSITIVE2/WEAK AUXIN RESPONSE1 is required for polar auxin transport. Plant Cell 22: 1749-1761.
16. Gerendás J, Zhu Z, Bendixen R, Ratcliffe RG, Sattelmacher B. 1997. Physiological and biochemical processes related to ammonium toxicity in higher plants. Zeitschrift für Pflanzenernaehrung und Bodenkunde 160: 239-251.
17. Harrison BR, Masson PH. 2008. ARL2, ARG1 and PIN3 define a gravity signal transduction pathway in root statocytes. Plant Journal 53: 380-392.
18. + sensitivity mediated by Arabidopsis GDP-mannose pyrophosphorylase. Plant, Cell & Environment 34: 847-858.
19. Kiss JZ, Hertel R, Sack FD. 1989. Amyloplasts are necessary for full gravitropic sensitivity in roots of Arabidopsis thaliana. Planta 177: 198-206.
20. Kronzucker HJ, Siddiqi MY, Glass ADM. 1997. Conifer root discrimination against soil nitrate and the ecology of forest succession. Nature 385: 59-61.
21. Laxmi A, Pan J, Morsy M, Chen R. 2008. Light plays an essential role in intracellular distribution of auxin efflux carrier PIN2 in Arabidopsis thaliana. PLoS ONE 3: e1510.
22. Lewis DR, Muday GK. 2009. Measurement of auxin transport in Arabidopsis thaliana. Nature Protocols 4: 437-451.
23. Li BH, Li Q, Kronzucker HJ, Shi W. 2011b. Roles of abscisic acid and auxin in shoot-supplied ammonium inhibition of root system development. Plant Signaling & Behavior 6: 1451-1453.
24. Li BH, Li Q, Su YH, Chen H, Xiong LM, Mi GH, Kronzucker HJ, Shi WM. 2011a. Shoot-supplied ammonium targets the root auxin influx carrier AUX1 and inhibits lateral root emergence in Arabidopsis. Plant, Cell & Environment 34: 933-946.
25. Li BH, Li Q, Xiong LM, Kronzucker HJ, Krämer U, Shi WM. 2012. Arabidopsis plastid AMOS1/EGY1 integrates abscisic acid signaling to regulate global gene expression response to ammonium stress. Plant Physiology 160: 2040-2051.
26. Li GJ, Li BH, Dong GQ, Feng XY, Kronzucker HJ, Shi WM. 2013. Ammonium-induced shoot ethylene production is associated with the inhibition of lateral root formation in Arabidopsis. Journal of Experimental Botany 64: 1413-1425.
27. + efflux and GMPase activity. Plant, Cell & Environment 33: 1529-1542.
28. Li X, Zhang W. 2008. Salt-avoidance tropism in Arabidopsis thaliana. Plant Signaling & Behavior 3: 351-353.
29. Liao H, Rubio G, Yan X, Cao A, Brown KM, Lynch JP. 2001. Effect of phosphorus availability on basal root shallowness in common bean. Plant and Soil 232: 69-79.
30. Luschnig C, Gaxiola RA, Grisafi P, Fink GR. 1998. EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes & Development 12: 2175-2187.
31. Marchant A, Bennett MJ. 1998. The Arabidopsis AUX1 gene: a model system to study mRNA processing in plants. Plant Molecular Biology 36: 463-471.
32. Marchant A, Kargul J, May ST, Muller P, Delbarre A, Perrot-Rechenmann C, Bennett MJ. 1999. AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues. EMBO Journal 18: 2066-2073.
33. Ottenschläger I, Wolff P, Wolverton C, Bhalerao RP, Sandberg G, Ishikawa H, Evans M, Palme K. 2003. Gravity-regulated differential auxin transport from columella to lateral root cap cells. Proceedings of the National Academy of Sciences, USA 100: 2987-2991.
34. Perrin RM, Young LS, Murthy UMN, Harrison BR, Wang Y, Will JL, Masson PH. 2005. Gravity signal transduction in primary roots. Annals of Botany (London) 96: 737-743.
35. Qin C, Qian W, Wang W, Wu Y, Yu C, Jiang X, Wang D, Wu P. 2008. GDP-mannose pyrophosphorylase is a genetic determinant of ammonium sensitivity in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 105: 18308-18313.
36. Rashotte AM, Brady SR, Reed RC, Ante SJ, Muday GK. 2000. Basipetal auxin transport is required for gravitropism in roots of Arabidopsis. Plant Physiology 122: 481-490.
37. Rigas S, Ditengou FA, Ljung K, Daras G, Tietz O, Palme K, Hatzopoulos P. 2012. Root gravitropism and root hair development constitute coupled developmental responses regulated by auxin homeostasis in the Arabidopsis root apex. New Phytologist 197: 1130-1141.
38. Roman G, Lubarsky B, Kieber JJ, Rothenberg M, Ecker JR. 1995. Genetic analysis of ethylene signal transduction in Arabidopsis thaliana: five novel mutant loci integrated into a stress response pathway. Genetics 139: 1393-1409.
39. Salathia N, Lee HN, Sangster TA, Morneau K, Landry CR, Schellenberg K, Behere AS, Gunderson KL, Cavalieri D, Jander G et al. 2007. Indel arrays: an affordable alternative for genotyping. Plant Journal 51: 727-737.
40. Sedbrook JC, Chen R, Masson PH. 1999. ARG1 (altered response to gravity) encodes a DnaJ-like protein that potentially interacts with the cytoskeleton. Proceedings of the National Academy of Sciences, USA 96: 1140-1145.
41. Shin H, Shin HS, Guo Z, Blancaflor EB, Masson PH, Chen R. 2005. Complex regulation of Arabidopsis AGR1/PIN2-mediated root gravitropic response and basipetal auxin transport by cantharidin-sensitive protein phosphatases. Plant Journal 42: 188-200.
42. Sun F, Zhang W, Hu H, Li B, Wang Y, Zhao Y, Li K, Liu M, Li X. 2008. Salt modulates gravity signaling pathway to regulate growth direction of primary roots in Arabidopsis. Plant Physiology 146: 178-188.
43. Swarup R, Friml J, Marchant A, Ljung K, Sandberg G, Palme K, Bennett M. 2001. Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. Genes & Development 15: 2648-2653.
44. Swarup R, Kargul J, Marchant A, Zadika D, Rahman A, Mills R, Yemm A, May S, Williams L, Millner P et al. 2004. Structure-function analysis of the presumptive Arabidopsis auxin permease AUX1. Plant Cell 16: 3069-3083.
45. Swarup R, Kramer EM, Perry P, Knox K, Leyser HMO, Haseloff J, Beemster GTS, Bhalerao R, Bennett MJ. 2005. Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal. Nature Cell Biology 7: 1057-1065.
46. Takahashi N, Yamazaki Y, Kobayashi A, Higashitani A, Takahashi H. 2003. Hydrotropism interacts with gravitropism by degrading amyloplasts in seedling roots of Arabidopsis and radish. Plant Physiology 132: 805-810.
47. Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ. 1997. Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9: 1963-1971.
48. Verbelen J-P, De Cnodder T, Le J, Vissenberg K, Baluška F. 2006. The root apex of Arabidopsis thaliana consists of four distinct zones of cellular activities: meristematic zone, transition zone, fast elongation zone, and growth terminating zone. Plant Signaling & Behavior 1: 296-304.
49. Vicente-Agullo F, Rigas S, Desbrosses G, Dolan L, Hatzopoulos P, Grabov A. 2004. Potassium carrier TRH1 is required for auxin transport in Arabidopsis roots. Plant Journal 40: 523-535.
50. Wan Y, Jasik J, Wang L, Hao H, Volkmann D, Menzel D, Mancuso S, Baluška F, Lin J. 2012. The signal transducer NPH3 integrates the phototropin1 photosensor with PIN2-based polar auxin transport in Arabidopsis root phototropism. Plant Cell 24: 551-565.
51. Weigel D, Glazebrook J. 2002. Arabidopsis: a laboratory manual. New York, NY, USA: Cold Spring Harbor Laboratory Press, 243-245.
52. Wisniewska J, Xu J, Seifertová D, Brewer PB, Ruzicka K, Blilou I, Benková E, Scheres B, Friml J. 2006. Polar PIN localization directs auxin flow in plants. Science 312: 883.
53. Wolverton C, Mullen JL, Ishikawa H, Evans ML. 2002. Root gravitropism in response to a signal originating outside of the cap. Planta 215: 153-157.
54. Yokawa K, Kagenishi T, Baluška F. 2013. Root photomorphogenesis in laboratory-maintained Arabidopsis seedlings. Trends in Plant Science 18: 117-119.
55. Yokawa K, Kagenishi T, Kawano T, Mancuso S, Baluška F. 2011. Illumination of Arabidopsis roots induces immediate burst of ROS production. Plant Signaling & Behavior 6: 1460-1464.
56. Zhang J, Xu JX, Kong YZ, Ji ZD, Wang XC, An FY, Li C, Sun JQ, Zhang SZ, Yang XH et al. 2005. Generation of chemical-inducible activation tagging T-DNA insertion lines of Arabidopsis thaliana. Acta Genetica Sinica 32: 1082-1088.
57. Zou N, Li BH, Dong GQ, Kronzucker HJ, Shi WM. 2012. Ammonium-induced loss of root gravitropism is related to auxin distribution and TRH1 function, and is uncoupled from the inhibition of root elongation in Arabidopsis. Journal of Experimental Botany 63: 3777-3788.
58. Zuo J, Niu QW, Chua NH. 2000. An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. Plant Journal 24: 265-273.