biologia plantarum

International journal on Plant Life established by Bohumil Němec in 1959

Biologia plantarum 53:85-99, 2009 | DOI: 10.1007/s10535-009-0012-4

Microarray analysis of Arabidopsis genome response to aluminum stress

S. B. Goodwin1,*, T. R. Sutter1
1 W. Harry Feinstone Center for Genomic Research, Department of Biology, University of Memphis, Memphis, USA

To better understand the mechanisms involved in aluminum toxicity and tolerance in plants, microarray technology was used to evaluate changes in gene expression in Arabidopsis thaliana under Al stress. With the use of Affymetrix Arabidopsis ATH1 Genechip, a comparison of RNA expression profiles was made between control and Al-treated Arabidopsis seedlings. A total of 256 genes were identified as Al-responsive. Ninety-four genes were shown to be up-regulated and 162 were down-regulated; comprising 1.1 % of the 24 000 Arabidopsis genes. Real-time RT-PCR was used to confirm the microarray data. The analysis showed that a large number of transcription factors and several putative signaling components were up-regulated by aluminum. Chloroplast structural and photosynthetic genes were, in general, down-regulated. A number of previously identified Al-responsive genes, e.g. GST, Auxin-regulated, Peroxidase, and Chitinase, were up-regulated by Al-stress, whereas Wali 3 and Wali 4 were down-regulated. We also identified several up-regulated genes involved in vacuolar signaling, sorting and docking. Three genes were also up-regulated by Al-stress, Ras GTP-binding protein, ABC-cassette binding, and the AtELP1 receptor genes, have previously been documented as responsive to drought and/or oxidative stress and may play important roles the detoxification of Al ions by transportation and storage into root vacuoles. Ultrastructural changes in the roots tips cells of Arabidopsis were evaluated using transmission electron microscopy and energy-dispersive X-ray analysis with scanning electron microscopy and results showed Al accumulation in the root tips of Arabidopsis.

Keywords: gene expression; microarray gene chip
Subjects: aluminum; Arabidopsis thaliana; gene expression; microarray analysis; polymerase chain reaction (PCR); signalling; transcription factors; transmission electrom microscopy; X-ray analysis

Received: March 23, 2007; Accepted: November 30, 2007; Published: March 1, 2009  Show citation

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Goodwin, S.B., & Sutter, T.R. (2009). Microarray analysis of Arabidopsis genome response to aluminum stress. Biologia plantarum, 53(1), 85-99. doi: 10.1007/s10535-009-0012-4
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    References

    1. Bowles, D.: A multigene family of glycosyltransferases in a model plant, Arabidopsis thaliana.-Biochem. Soc. Trans. 30: 301-306, 2002. Go to original source...
    2. Bray, E.A.: Genes commonly regulated by water-deficit stress in Arabidopsis thaliana.-J. exp. Bot 55: 2331-2341, 2004. Go to original source...
    3. Brinker, M., Van Zyl, L., Liu, W., Craig, D., Sederoff, R., Clapham, D.H., Von Arnold, S.: Microarray analysis of gene expression during adventitious root development in Pinus contorta.-Plant Physiol. 135: 1526-1539, 2004. Go to original source...
    4. Chaumont, F., Barrieu, F., Herman, E.M., Chrispeels, M.J.: Characterization of a maize tonoplast aquaporins expressed in zones of cell division and elongation.-Plant Physiol. 117: 1143-1152, 1998. Go to original source...
    5. Cheong, Y.H., Kim, K.N., Pandey, G.K., Gupta, R., Grant, J.J., Luan, S.: CBL1, a calcium sensor that differentially regulates salt, drought, and cold responses in Arabidopsis.-Plant Cell 15: 1833-1845, 2003. Go to original source...
    6. Cosgrove, D.J.: Loosening of plant cell walls by expansins.-Nature 407: 321-326, 2000. Go to original source...
    7. Cruz-Ortega, R., Cushman, J.C., Ownby, J.D.: cDNA clones encoding 1,3-beta-glucanase and a fimbrin-like cytoskeletal protein are induced by Al toxicity in wheat roots.-Plant Physiol. 114: 1453-1460, 1997. Go to original source...
    8. Ebel, J., Cosio, E.G.: Elicitors of plant defense responses.-Int. Rev. Cytol. 148: 1-36, 1994. Go to original source...
    9. Ekman, D.R., Lorenz, W.W., Przybyla, A.E., Wolfe, N.L., Dean, J.F.D.: SAGE analysis of transcriptome responses in Arabidopsis roots exposed to 2,4,6-trinitrotoluene.-Plant Physiol. 133: 1397-1406, 2003. Go to original source...
    10. Ezaki, B., Katsuhara, M., Kawamura, M., Matsumoto, H.: Different mechanisms of four aluminum (Al)-resistant transgenes for Al toxicity in Arabidopsis.-Plant Physiol. 127: 918-927, 2001. Go to original source...
    11. Ferguson, D.L., Turley, R.B., Kloth, R.H.: Identification of a δ-TIP cDNA clones and determination of related A and D genome subfamilies in Gossypium species.-Plant mol. Biol. 34: 111-118, 1997. Go to original source...
    12. Foy, C.D.: Plant adaptation to acid, aluminum toxic soils.-Commun. Soc. Sci. Plant Anal. 19: 959-987, 1988. Go to original source...
    13. Gaedeke, N., Klein, M., Kolukisaoglu, U., Forestier, C., Muller, A., Ansorge, M., Becker, D., Mamnun, Y., Kuchler, K., Schulz, B., Mueller-Roeber, B., Martinoia, E.: The Arabidopsis thaliana ABC transporter AtMRP5 controls root development and stomata movement.-EMBO J. 20: 1875-1887, 2001. Go to original source...
    14. Hamel, F., Breton, C.., Houde, M.: Isolation and characterization of wheat aluminum-regulated genes: possible involvement of aluminum as a pathogenesis response elictor.-Planta 205: 531-538, 1998. Go to original source...
    15. Hamilton, C.A., Good, A.G., Taylor, G.J.: Induction of vacuolar ATPase and mitochondrial ATP synthase by aluminum in an aluminum-resistant cultivar of wheat.-Plant Physiol. 125: 2068-2077, 2001. Go to original source...
    16. Hayes, J., Ma, J.: Al-induced efflux of organic acid anions is poorly associated with internal organic acid metabolism in triticale roots.-J. exp. Bot. 54: 1753-1759, 2003. Go to original source...
    17. Hoekenga, O.A.., Maron, L.G., Pineros, M.A., Cancado, G.M., Shaff, J., Kobayashi, Y., Ryan P.R., Dong, B., Delhaze, E., Sasaki, T., Matsumoto, H., Yamamoto, Y., Koyama, H., Kochian, L.V.: AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis.-Proc. nat. Acad. Sci. USA 103: 9749-9750, 2006. Go to original source...
    18. Hoekenga, O.A.., Vision, T.J., Shaff, J.E., Monfone, A.J., Lee, G.P.: Idenification and characterization of aluminum tolerance loci in Arabidopsis (Landberg erecta × Columbia) by quantitative trait locus mapping. A physiologically simple but genetically complex trait.-Plant Physiol. 132: 936-948, 2003. Go to original source...
    19. Hossain, M., Zhou, M.X., Mendham, N.J.: A reliable screening system for aluminum tolerance in barley cultivars.-Aust. J. agr. Res. 56: 475-482, 2005. Go to original source...
    20. Irizarry, R.A., Bolstad, B.M., Collin, F., Cope, L.M., Hobbs, B., Speed, T.P.: Summaries of Affymetrix GeneChip probe level data.-Nucl. Acids Res. 31: 1-8, 2003. Go to original source...
    21. Javot, H., Maurel, C.: The role of aquaporins in root water uptake.-Ann. Bot. 90: 3001-3013, 2002. Go to original source...
    22. Karlsson, M., Johansson, I., Bush, M., McCann, M.C., Maurel, C., Larsson, C., Kjellbom, W.G.: An abundant TIP expressed in mature highly vacuolated cells.-Plant J. 21: 83-90, 2000. Go to original source...
    23. Keller, B.: Structural cell wall proteins.-Plant Physiol. 101: 1127-1130, 1993. Go to original source...
    24. Kochian, L.V.: Cellular mechanisms of aluminum toxicity and resistance in plants.-Annu. Rev. Plant Physiol. Plant mol. Biol. 46: 237-260, 1995. Go to original source...
    25. Kochian, L.V., Hoekenga, O.A., Pineros, M.A.: How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency.-Annu. Rev. Plant Biol. 55: 459-493, 2004. Go to original source...
    26. Kochian, L.V., Pineros, M.A., Hoekenga, O.A.: The physiology, genetics and molecular biology of plant aluminum resistance and toxicity.-Plant Soil 274: 175-195, 2005. Go to original source...
    27. Larsen, P.B., Cancel, J., Rounds, M., Ochoa, V.: 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, 2006. Go to original source...
    28. Larsen, P.B., Geister, M.J.B., Jones, C.A., Kelly, M.W., Cancel, J.D.: ALS3 encodes a phloem-localized ABC transporter-like protein that is required for aluminum tolerance in Arabidopsis.-Plant J. 41:353-363, 2005. Go to original source...
    29. Lazof, D.B., Goldsmith, J.G., Ruffy, T.W., Linton, R.W.: The early entry of Al into cells of intact soybean roots. A comparison of three developmental root regions using secondary ion mass spectrometry imaging.-Plant Physiol. 112: 1289-1300, 1996. Go to original source...
    30. Leonhardt, N., Kwak, J.M., Robert, N., Waner, D., Leonhardt, G., Schroeder, J.I.: Microarray expression analyses of Arabidopsis guard cells and isolation of a recessive abscisic acid hypersensitive protein phosphatase 2C mutant.-Plant Cell 17: 1330-1333, 2004. Go to original source...
    31. Le Van, H., Kuraishi, S., Sakurai, N.: Aluminum-induced rapid root inhibition and changes in cell-wall components of squash seedlings.-Plant Physiol. 106: 1107-1114, 1994. Go to original source...
    32. Li, C., Wong W.H.: Model-based analysis of oligonucleotide arrays: Expression index computation and outlier detection.-Proc. nat. Acad. Sci. USA 98: 31-36, 2001. Go to original source...
    33. Ma, J.F., Hiradate, S.: Form of aluminum for uptake and translocation in buckwheat (Fagopyrum esculentum Moench).-Planta 211: 355-360, 2000. Go to original source...
    34. Ma, J.F., Hiradate, S., Nomoto, K., Iwashita, T., Matsumoto, H..: Internal detoxification mechanism of Al in hydrangea: Identification of Al form in the leaves.-Plant Physiol. 113: 1033-39, 1997. Go to original source...
    35. Mao, C., Yi, K., Yang, L., Zheng, B., Wu, Y., Liu, F., Wu, P.: Identification of aluminum-regulated genes by cDNA-AFLP in rice (Oryza sativa L): aluminum-regulated genes for the metabolism of cell wall components.-J. exp. Bot. 55: 137-143, 2006. Go to original source...
    36. Milla, M.A., Bulter, E.D., Rodriguez, H., Wilson, C.F., Anderson, O., Gustafson, J.P.: Expressed sequence tagbased gene expression analysis under aluminum stress in rye.-Plant Physiol. 130: 1706-1716, 2002. Go to original source...
    37. Mittler, R., Vanderauwera, S., Gollery, M., Van Breusegem, F.: Reactive oxygen gene network in plants.-Trends Plant Sci. 9: 490-498, 2004. Go to original source...
    38. Moffat, A.S.: Engineering plants to cope with metals.-Science 285: 369-370, 1999. Go to original source...
    39. Nahm, MY., Kim, S.W., Yun, D., Lee, S.Y., Cho, M.J., Bahk, J.D.: Molecular and biochemical analysis of OsRab7, a rice Rab7 homolog.-Plant Cell Physiol. 44: 1341-1349, 2003. Go to original source...
    40. Osawa, H., Matsumoto, H.: Possible involement of protein phosphorylation in aluminum-responsive malate efflux from wheat root apex.-Plant Physiol. 126: 411-420, 2001. Go to original source...
    41. Passardi, F., Cosio, C., Penel, C., Dunand, C.: Peroxidases have more functions than a Swiss army knife.-Plant Cell Rep. 24: 255-265, 2005. Go to original source...
    42. Peixoto, P.H.P., Cambraia, J., Sant'Anna, R., Mosquim, P.R., Moreira, M.A.: Aluminum effects in lipid peroxidation and on activities of enzymes of oxidative metabolism in Sorghum.-Braz. J. Plant Physiol. 11: 137-143. 1999.
    43. PfaffI, M.W.: A new mathematical model for relative quantification in real-time RT-PCR.-Nucl. Acids Res. 29: 2002-2007, 2001. Go to original source...
    44. Ragland, M., Soliman, K.M.: Sali5-4a and Sali3-2: two genes induced by Al in soybean roots.-Plant Physiol. 114: 395-395, 1997.
    45. Rental, M.C., Lecourieux, D., Ouaked, F., Usher, S.L., Petersen, L., Okamoto, H., Knight, H., Peck, S.C., Grierson, C.S., Hirt, H., Knight, M.C.: OXI1 kinase is necessary for oxidative burst-mediated signaling in Arabidopsis.-Nature 427: 558-861, 2004. Go to original source...
    46. Richards, K.D., Schott, E., Sharma, Y.K., Davis, K.R., Gardner, R.C.: Aluminum induces oxidative stress genes in Arabidopsis thaliana.-Plant Physiol. 116: 409-418, 1998. Go to original source...
    47. Richards, K.D., Snowden, K.C., Gardner, R.C.: Wali6 and wali7. Genes induced by aluminum in wheat (Triticum aestivum L.) roots.-Plant Physiol. 105:1455-1456, 1994. Go to original source...
    48. Sampedro, J., Cosgrove, D.J.: The expansin superfamily.-Genome Biol. 6: 242.1-242.11, 2005. Go to original source...
    49. Sanderfoot, A.A., Ahmed, S.U., Marty-Mazars, D., Rapoport, I., Kirchhausen, T., Marty, F., Raikhel, N.V.: A putative vacuolar cargo receptor partially colocalizes with AtPEP12p on a prevacuolar compartment in Arabidopsis roots.-Proc. nat. Acad. Sci. USA 95: 9920-9925, 1998. Go to original source...
    50. Sasaki, T., Eunichi, B., Matsumoto, H.: A gene encoding multidrug resistance (MDR)-like protein is induced by aluminum and inhibitors of calcium flux in wheat.-Plant Cell. Physiol. 43: 177-185, 2002. Go to original source...
    51. Savenstrand, H., Brosche, M., Angehagen, M., Strid, A.: Molecular markers for ozone stress isolated by suppression subtractive hybridization: specificity of gene expression and identification of a novel stress-regulated gene.-Plant Cell Environ. 23: 689-700, 2000. Go to original source...
    52. Shen, R., Ma, J.F., Kyo, M., Iwashita, T.: Compartmentation of aluminum in leaves of an Al-accumulor, Fagopyrum esculentum Moench.-Planta 215: 394-398, 2002. Go to original source...
    53. Shen, R., Iwashita, T., Ma, J.F.: Form of Al changes with Al concentration in leaves of buckwheat.-J. exp. Bot. 55: 131-136, 2004. Go to original source...
    54. Silva, I.R., Smyth, T.J., Moxley, D.F., Carter, T.E., Allen, N.S., Rufty, T.W.: Aluminum accumulation at nuclei of cells in the root tip. Fluorescence detection using lumogallion and confocal laser scanning microscopy.-Plant Physiol. 123: 543-552, 2000. Go to original source...
    55. ©imonovičová, M., Tamás, L., Huttová, J., Mistrík, I.: Effect of aluminum on oxidative stress related enzymes activities in barley roots.-Biol. Plant. 48: 261-266, 2004. Go to original source...
    56. Shin, Y.K., Yum, H., Kim, E.S., Cho, H., Gothandam, K.M., Hyun, J., Chung, Y.Y.: BcXTH1, a Brassica campestris homologue of Arabidopsis XTH9, is associated with cell expansion.-Planta 224: 32-41, 2006. Go to original source...
    57. Sivaguru, M., Fujiwara, T., ©ámaj, J., Baluąka, F., Yang, Z., Osawa, H., Maeda, T., Mori, T., Volkmann, D., Matsumoto, H.: Aluminum-induced 1→3-β-D-glucan inhibits cell-to-cell trafficking of molecules through plasodesmata. A new mechanism of aluminum toxicity in plants.-Plant Physiol. 124: 991-1005, 2000. Go to original source...
    58. Smart, L.B., Moskal, W.A., Cameron, K.D., Bennett, A.B.: MIP genes are down-regulated under drought stress in Nicotiana glauca.-Plant Cell Physiol. 42: 686-693, 2001. Go to original source...
    59. Snowen, K.C., Gardner, R.C.: Five genes induced by aluminum in wheat (Triticum aestivum L.) roots.-Plant Physiol. 103: 855-861, 1993. Go to original source...
    60. Sohn, E.J., Kim, E.S., Zhao, M., Kim, S.J., Kim, H., Kim, Y.W., Lee, Y.J., Hillmer, S., Sohn, U., Jiang, L., Hwang, I.: Rha1, an Arabidopsis Rab5 homolog, plays a critical role in the vacuolar trafficking of soluble cargo proteins.-Plant Cell 15: 1057-1070, 2003. Go to original source...
    61. Sormo, C.G., Leiro, I., Brembu, T., Winge, P., Os, V., Bones, A.M.: the crystal structure of Arabidopsis thaliana RAC7/ROP9: The first RAS superfamily GTPase from the plant kingdom.-Phytochemistry 67: 2332-2340, 2006. Go to original source...
    62. Sugiyama, A., Shitan, N., Sato, S., Nakamura, Y., Tabata, S., Yazaki, K.: Genome-wide analysis of ATP-binding cassette (ABC) proteins in a model legume plant, Lotus japonicus: comparison with Arabidopsis ABC protein family.-DNA Res. 13: 205-228, 2006. Go to original source...
    63. Tamás, L., Huttová, J., Mistrík, I., ©imonovičová, M., ©iroká, B.: Aluminum-induced drought and oxidative stress in barley roots.-J. Plant Physiol. 163: 781-784, 2006. Go to original source...
    64. Taylor, G.J., McDonald-Stephens, J.L., Hunter, D.B., Bertsch, P.M., Elmore, D.: Direct measurement of aluminum uptake and distribution in single cells of Chara corallina.-Plant Physiol. 123: 987-996, 2000. Go to original source...
    65. Tchieu, J.H., Fana, F., Fink, J.L., Harper, J., Nair, T.M., Niedner, R.H., Smith, D.W., Steube, K., Tam, T.M., Veretnik, S., Wang, D., Gribskov.: The plantsP and plantsT functional genomics databases.-Nucl. Acids Res. 31: 342-344, 2003. Go to original source...
    66. Tesfaye, M., Temple, S.J., Allen, D.L., Vance, C.P., Samac, D.A.: Overexpression of malate dehydrogenase in trangenic alfalfa enhances organic acid synthesis and confers tolerance to aluminum.-Plant Physiol. 127: 1836-1844, 2001. Go to original source...
    67. Vazquez, M.D., Poschenrieder, C., Corrales, I., Barceló, J.: Change in apoplastic aluminum during the initial growth reponse to aluminum by roots of a tolerant maize variety.-Plant Physiol. 119: 435-444, 1999. Go to original source...
    68. Vernoud, V., Horton, A.C., Yang, Z., Nielsen, E.: Analysis of the small GTPase gene superfamily of Arabidopsis.-Plant Physiol. 131: 1191-1208, 2003. Go to original source...
    69. Vissenberg, K., Oyama, M., Osato, Y., Yokoyama, R., Verbelen, J.P., Nishitant, K.: Differential expression of AtXTH17, AtXTH18, AtXTH19 and AtXTH20 genes in Arabidopsis roots. Physiological roles in specification in cell wall construction.-Plant Cell Physiol. 46: 192-200, 2005. Go to original source...
    70. Von Rad, U., Mueller, M.J., Durner, J.: Evaluation of natural and synthetic stimulants of plant immunity by microarray technology.-New Phytol. 165: 191-202, 2005. Go to original source...
    71. Von Uexkull, H.R., Mutert, E.: Global extent, development and economic impact of acid soils.-Plant Soil 171:1-15, 1995. Go to original source...
    72. Wang, J.-W., Kao, C.H.: Protective effect of ascorbic acid and glutathione on AlCl3-inhibited growth of rice roots.-Biol. Plant. 51: 493-500, 2007. Go to original source...
    73. Werck-Reichhart, D., Bak, S., Paquette, S..: Cytochromes P450.-In: Somerville, C.R., Meyerowitz, E.M. (ed.): The Arabidopsis Book. Pp. 1-28. American Society of Plant Biologists, Rockville 2002. Go to original source...
    74. Wisman, E., Ohlrogge, J.: Arabidopsis microarray service facilities.-Plant Physiol. 124: 1468-1471, 2000. Go to original source...
    75. Wildermuth, M.C., Dewdney, J., Wu, G., Ausubel, F.M.: Isochorismate synthase is required to synthesize salicylic acid for plant defense.-Nature 417: 562-565, 2002. Go to original source...
    76. Yang, Z.M., Wang, J., Wang, S.H., Xu, L.L.: Salicylic acid-induced aluminum tolerance by modulation of citrate efflux from roots of Cassia tora L.-Planta 217: 168-174, 2003. Go to original source...
    77. Zheng, S.J., Yang, J.L.: Target sites of aluminum phytotoxicity.-Biol. Plant. 49: 321-331, 2005. Go to original source...

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