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Microarray analysis of Arabidopsis genome response to aluminum stress

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Biologia Plantarum

Abstract

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.

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Abbreviations

CW:

cell wall

EDXMA:

energy-dispersive X-ray analysis

EM:

electron microscopy

IS:

interstitial space

MS:

Murashige and Skoog

PCR:

polymerize chain reaction

PD:

plasmodesmata

SEM:

scanning electron microscopy

TEM:

transmission electron microscopy

V:

vacuole

References

  • Bowles, D.: A multigene family of glycosyltransferases in a model plant, Arabidopsis thaliana.-Biochem. Soc. Trans. 30: 301–306, 2002.

    Article  PubMed  CAS  Google Scholar 

  • Bray, E.A.: Genes commonly regulated by water-deficit stress in Arabidopsis thaliana.-J. exp. Bot 55: 2331–2341, 2004.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Cosgrove, D.J.: Loosening of plant cell walls by expansins.-Nature 407: 321–326, 2000.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Ebel, J., Cosio, E.G.: Elicitors of plant defense responses.-Int. Rev. Cytol. 148: 1–36, 1994.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Foy, C.D.: Plant adaptation to acid, aluminum toxic soils.-Commun. Soc. Sci. Plant Anal. 19: 959–987, 1988.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Javot, H., Maurel, C.: The role of aquaporins in root water uptake.-Ann. Bot. 90: 3001–3013, 2002.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Keller, B.: Structural cell wall proteins.-Plant Physiol. 101: 1127–1130, 1993.

    PubMed  CAS  Google Scholar 

  • Kochian, L.V.: Cellular mechanisms of aluminum toxicity and resistance in plants.-Annu. Rev. Plant Physiol. Plant mol. Biol. 46: 237–260, 1995.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Ma, J.F., Hiradate, S.: Form of aluminum for uptake and translocation in buckwheat (Fagopyrum esculentum Moench).-Planta 211: 355–360, 2000.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Mittler, R., Vanderauwera, S., Gollery, M., Van Breusegem, F.: Reactive oxygen gene network in plants.-Trends Plant Sci. 9: 490–498, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Moffat, A.S.: Engineering plants to cope with metals.-Science 285: 369–370, 1999.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Osawa, H., Matsumoto, H.: Possible involement of protein phosphorylation in aluminum-responsive malate efflux from wheat root apex.-Plant Physiol. 126: 411–420, 2001.

    Article  PubMed  CAS  Google Scholar 

  • Passardi, F., Cosio, C., Penel, C., Dunand, C.: Peroxidases have more functions than a Swiss army knife.-Plant Cell Rep. 24: 255–265, 2005.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • PfaffI, M.W.: A new mathematical model for relative quantification in real-time RT-PCR.-Nucl. Acids Res. 29: 2002–2007, 2001.

    Google Scholar 

  • Ragland, M., Soliman, K.M.: Sali5-4a and Sali3-2: two genes induced by Al in soybean roots.-Plant Physiol. 114: 395–395, 1997.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Sampedro, J., Cosgrove, D.J.: The expansin superfamily.-Genome Biol. 6: 242.1–242.11, 2005.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Šimonovičová, 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Sivaguru, M., Fujiwara, T., Šámaj, J., Baluška, 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Snowen, K.C., Gardner, R.C.: Five genes induced by aluminum in wheat (Triticum aestivum L.) roots.-Plant Physiol. 103: 855–861, 1993.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Tamás, L., Huttová, J., Mistrík, I., Šimonovičová, M., Široká, B.: Aluminum-induced drought and oxidative stress in barley roots.-J. Plant Physiol. 163: 781–784, 2006.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Vernoud, V., Horton, A.C., Yang, Z., Nielsen, E.: Analysis of the small GTPase gene superfamily of Arabidopsis.-Plant Physiol. 131: 1191–1208, 2003.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Von Uexkull, H.R., Mutert, E.: Global extent, development and economic impact of acid soils.-Plant Soil 171:1–15, 1995.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • Wisman, E., Ohlrogge, J.: Arabidopsis microarray service facilities.-Plant Physiol. 124: 1468–1471, 2000.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Zheng, S.J., Yang, J.L.: Target sites of aluminum phytotoxicity.-Biol. Plant. 49: 321–331, 2005.

    Article  CAS  Google Scholar 

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  1. W. Harry Feinstone Center for Genomic Research, Department of Biology, University of Memphis, Memphis, TN, 38152, USA

    S. B. Goodwin & T. R. Sutter

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  1. S. B. Goodwin
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  2. T. R. Sutter
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Goodwin, S.B., Sutter, T.R. Microarray analysis of Arabidopsis genome response to aluminum stress. Biol Plant 53, 85–99 (2009). https://doi.org/10.1007/s10535-009-0012-4

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