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Genomic profiling of rice roots with short- and long-term chromium stress

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Abstract

Cr(VI) is the most toxic valency form of Cr, but its toxicity targets and the cellular systems contributing to acquisition of tolerance remain to be resolved at the molecular level in plants. We used microarray assay to analyze the transcriptomic profiles of rice roots in response to Cr(VI) stress. Gene ontology analysis revealed that the 2,688 Cr-responsive genes were involved in binding activity, metabolic process, biological regulation, cellular process and catalytic activity. More transcripts were responsive to Cr(VI) during long-term exposure (24 h, 2,097 genes), than short-term exposure (1- and 3-h results pooled, 1,181 genes). Long-term Cr(VI)-regulated genes are involved in cytokinin signaling, the ubiquitin–proteasome system pathway, DNA repair and Cu transportation. The expression of AS2 transcription factors was specifically modulated by long-term Cr(VI) stress. The protein kinases receptor-like cytoplasmic kinase and receptor-like kinase in flowers 3 were significantly upregulated with only short-term Cr(VI) exposure. In addition, 4 mitogen-activated protein kinase kinase kinases, 1 mitogen-activated protein kinase (MAPK) and 1 calcium-dependent protein kinase (CDPK) were upregulated with short-term Cr(VI) treatment. Expression of reactive oxygen species and calcium and activity of MAPKs and CDPK-like kinases were induced with increasing Cr(VI) concentration. These results may provide new insights into understanding the mechanisms of Cr toxicity and tolerance during different stages in rice roots.

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References

  • Bartlett RJ (1991) Chromium cycling in soil and water: links, gaps, and methods. Environ Health Perspect 92:17–24

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Becraft PW (2002) Receptor kinase signaling in plant development. Annu Rev Cell Dev Biol 18:163–192

    Article  CAS  PubMed  Google Scholar 

  • Bogatek R, Gniazdowska A (2007) ROS and phytohormones in plant–plant allelopathic interaction. Plant Signal Behav 2:317–318

    Article  PubMed Central  PubMed  Google Scholar 

  • Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379–406

    Article  CAS  PubMed  Google Scholar 

  • Bridgewater LC, Manning FC, Woo ES, Patierno SR (1994) DNA polymerase arrest by adducted trivalent chromium. Mol Carcinog 9:122–133

    Article  CAS  PubMed  Google Scholar 

  • Cervantes C, Campos-Garcia J, Devars S, Gutiérrez-Corona FG, Loza-Tavera H, Carlos J, Torres-Guzmán JC, Moreno-Sánchez R (2001) Interactions of chromium with microorganisms and plants. FEMS Microbiol Rev 25:335–347

    Article  CAS  PubMed  Google Scholar 

  • Chandra P, Sinha S, Rai UN (1997) Bioremediation of chromium from water and soil by vascular aquatic plants. In: Kruger EL, Anderson TA, Coats JR (eds) Phytoremediation of soil and water contaminants, ACS symposium series 664. American Chemical Society, Washington, DC, pp 274–282

    Chapter  Google Scholar 

  • Choudhary SP, Kanwar M, Bhardwaj R, Yu JQ, Tran LS (2012) Chromium stress mitigation by polyamine-brassinosteroid application involves phytohormonal and physiological strategies in Raphanus sativus L. PLoS ONE 7:e33210

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dardick C, Chen J, Richter T, Ouyang S, Ronald P (2007) The rice kinase database. A phylogenomic database for the rice kinome. Plant Physiol 143:579–586

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Davies FT, Puryear JD, Newton RJ, Egilla JN, Grossi JAS (2002) Mycorrhizal fungi increase chromium uptake by sunflower plants: influence on tissue mineral concentration, growth, and gas exchange. J Plant Nutr 25:2389–2407

    Article  CAS  Google Scholar 

  • De Flora S (2000) Treshold mechanisms and site specificity in chromium (VI) carcinogenesis. Carcinogenesis 21:533–541

    Article  PubMed  Google Scholar 

  • Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38(suppl 2):W64–W70

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dube BK, Tewari K, Chatterjee J, Chatterjee C (2003) Excess chromium alters uptake and translocation of certain nutrients in citrullus. Chemosphere 53:1147–1153

    Article  CAS  PubMed  Google Scholar 

  • Dubey S, Misra P, Dwivedi S, Chatterjee S, Bag SK, Mantri S, Asif MH, Rai A, Kumar S, Shri M, Tripathi P, Tripathi RD, Trivedi PK, Chakrabarty D, Tuli R (2010) Transcriptomic and metabolomic shifts in rice roots in response to Cr(VI) stress. BMC Genom 11:648

    Article  Google Scholar 

  • Edgar R, Domrachev M, Lash AE (2002) Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30:207–210

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • EPA, USA (Environmental Protection Agency, United States of America) (1984)

  • Gao G, Zhong Y, Guo A, Zhu Q, Tang W, Zheng W, Gu X, Wei L, Luo J (2006) DRTF: a database of rice transcription factors. Bioinformatics 22:1286–1287

    Article  CAS  PubMed  Google Scholar 

  • Gidalevitz T, Prahlad V, Morimoto RI (2011) The stress of protein misfolding: from single cells to multicellular organisms. Cold Spring Harb Perspect Biol 3:3

    Article  Google Scholar 

  • Gish LA, Clark SE (2011) The RLK/Pelle family of kinases. Plant J 66:117–127

    Article  CAS  PubMed  Google Scholar 

  • Grennan AK (2006) Abiotic stress in rice. An “Omic” approach. Plant Physiol 140:1139–1141

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Huang TL, Huang HJ (2008) ROS and CDPK-like kinase-mediated activation of MAP kinase in rice roots exposed to lead. Chemosphere 71:1377–1385

    Article  CAS  PubMed  Google Scholar 

  • Huang TL, Nguyen QTT, Fu SF, Lin CY, Chen YC, Huang HJ (2012) Transcriptomic changes and signaling pathways induced by arsenic stress in rice roots. Plant Mol Biol 80:587–608

    Article  CAS  PubMed  Google Scholar 

  • Huffman EWD Jr, Allaway HW (1973a) Chromium in plants: distribution in tissues, organelles, and extracts and availability of bean leaf Cr to animals. J Agric Food Chem 21:982–986

    Article  PubMed  Google Scholar 

  • Huffman EWD Jr, Allaway WH (1973b) Growth of plants in solution culture containing low levels of chromium. Plant Physiol 52:72–75

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • IARC (International Agency for Research on Cancer) (1980) Chromium and chromium compounds. IARC monographs on the evaluation of carcinogenic risk of chemicals to humans, vol 23. International Agency for Research on Cancer Lyon, France. pp 205–323

  • Kende H, Zeevaart JAD (1997) The five “classical” plant hormones. Plant Cell 9:1197–1210

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Keramat B, Manouchehri KK, Arvin MJ (2010) Effect of methyl jasmonate treatment on alleviation of cadmium damages in soybean. J Plant Nutr 33(7):1016–1025

    Article  CAS  Google Scholar 

  • Khan AG (2001) Relationships between chromium biomagnification ratio, accumulation factor, and mycorrhizae in plants growing on tannery effluent-polluted soil. Environ Int 26:417–423

    Article  CAS  PubMed  Google Scholar 

  • Kimbrough DE, Cohen Y, Winer AM, Creelman L, Mabuni C (1999) A critical assessment of chromium in the environment. Crit Rev Environ Sci Technol 29:1–46

    Article  CAS  Google Scholar 

  • Klaumann S, Nickolaus SD, Furst SH, Starck S, Schneider S, Neuhaus HE, Trentmann O (2011) The tonoplast copper transporter COPT5 acts as an exporter and is required for interorgan allocation of copper in Arabidopsis thaliana. New Phytol 192:393–404

    Article  CAS  PubMed  Google Scholar 

  • Kortenkamp A, O’Brien P, Beyersmann D (1991) The reduction of chromate is a prerequisite of chromium binding to cell nuclei. Carcinogenesis 12:1143–1144

    Article  CAS  PubMed  Google Scholar 

  • Kotas J, Stasicka Z (2000) Commentary chromium occurrence in the environment and methods of its speciation. Environ Pollut 107:263–283

    Article  CAS  PubMed  Google Scholar 

  • Krishnamurthy S, Wilkens MM (1994) Environmental chemistry of chromium. Northeast Geol 16:14–17

    Google Scholar 

  • Labra M, Grassi F, Imazio S, Di Fabio T, Citterio S, Sgorbati S, Agradi E (2004) Genetic and DNA-methylation changes induced by potassium dichromate in Brassica napus L. Chemosphere 54:1049–1058

    Article  CAS  PubMed  Google Scholar 

  • Lehti-Shiu MD, Zou C, Hanada K, Shiu SH (2009) Evolutionary history and stress regulation of plant receptor-like kinase/pelle genes. Plant Physiol 150:12–26

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Levis AG, Bianchi V (1982) Mutagenic and cytogenetic effects of chromium compounds. In: Langard S (ed) Biological and environmental aspects of chromium. Elsevier, Amsterdam, pp 171–208

    Chapter  Google Scholar 

  • Li WX, Chen TB, Huang ZC, Lei M, Liao XY (2006) Effect of arsenic on chloroplast ultrastructure and calcium distribution in arsenic hyperaccumulator Pteris vittata L. Chemosphere 62:803–809

    Article  CAS  PubMed  Google Scholar 

  • Lin WC, Shuai B, Springer PS (2003) The Arabidopsis LATERAL ORGAN BOUNDARIES-domain gene ASYMMETRIC LEAVES2 functions in the repression of KNOX gene expression and in adaxial-abaxial patterning. Plant Cell 15:2241–2252

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lin TC, Yang CR, Chang FH (2007) Burning characteristics and emission products related to metallic content in incense. J Hazard Mater 140:165–172

    Article  CAS  PubMed  Google Scholar 

  • Liu F, Ni W, Griffith ME, Huang Z, Chang C, Peng W, Ma H, Xie D (2004) The ASK1 and ASK2 genes are essential for Arabidopsis early development. Plant Cell 16:5–20

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Liu D, Zou J, Wang M, Jiang W (2008) Hexavalent chromium uptake and its effects on mineral uptake, antioxidant defence system and photosynthesis in Amaranthus viridis L. Bioresour Technol 99:2628–2636

    Article  CAS  PubMed  Google Scholar 

  • Manning FC, Xu F, Patierno SR (1992) Transcriptional inhibition by carcinogenic chromate: relationship to DNA damage. Mol Carcinog 6:270–279

    Article  CAS  PubMed  Google Scholar 

  • Manning FC, Blankenship LJ, Wise JP, Xu J, Bridgewater LC, Patierno SR (1994) Induction of internucleosomal DNA fragmentation by carcinogenic chromate: relationship to DNA damage, genotoxicity, and inhibition of macromolecular synthesis. Environ Health Perspect 102(Suppl 3):159–167

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mazzucotelli E (2006) The E3 ubiquitin ligase gene family in plants: regulation by degradation. Curr Genomics 7:509–522

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Miller G, Shulaev V, Mittler R (2008) Reactive oxygen signaling and abiotic stress. Physiol Plant 13:481–489

    Article  Google Scholar 

  • Moral R, Pedreno JN, Gomez I, Mataix J (1995) Effects of chromium on the nutrient content and morphology of tomato. J Plant Nutr 18:815–822

    Article  CAS  Google Scholar 

  • Nakagami H, Pitzschke A, Hirt H (2005) Emerging MAP kinase pathways in plant stress signaling. Trends Plant Sci 10:339–346

    Article  CAS  PubMed  Google Scholar 

  • Neill SJ, Desikan R, Hancock JT (2002) Hydrogen peroxide signaling. Curr Opin Plant Biol 5:388–395

    Article  CAS  PubMed  Google Scholar 

  • Ouyang B, Yang T, Li H, Zhang L, Zhang Y, Zhang J, Fei Z, Ye Z (2007) Identification of early salt stress response genes in tomato root by suppression subtractive hybridization and microarray analysis. J Exp Bot 58:507–520

    Article  CAS  PubMed  Google Scholar 

  • Padmalatha KV, Dhandapani G, Kanakachari M, Kumar S (2012) Genome-wide transcriptomic analysis of cotton under drought stress reveal significant down-regulation of genes and pathways involved in fibre elongation and up-regulation of defense responsive genes. Plant Mol Biol 78:223–246

    Article  CAS  PubMed  Google Scholar 

  • Panda SK (2007) Chromium-mediated oxidative stress and ultrastructural changes in root cells of developing rice seedlings. J Plant Physiol 164:1419–1428

    Article  CAS  PubMed  Google Scholar 

  • Patterson C (2002) A new gun in town: the U box is a ubiquitin ligase domain. Sci STKE 2002(116):pe4

  • Plaper A, Jenko-Brinovec S, Premzl A, Kos J, Raspor P (2002) Genotoxicity of trivalent chromium in bacterial cells. Possible effects on DNA topology. Chem Res Toxicol 15:943–949

    Article  CAS  PubMed  Google Scholar 

  • Price AH, Taylor A, Ripley SJ, Griffiths A, Trewavas AJ, Knight MR (1994) Oxidative signals in tobacco increase cytosolic calcium. Plant Cell 12:1387–1398

    Google Scholar 

  • Ren Q, Kang KH, Paulsen IT (2004) TransportDB: a relational database of cellular membrane transport systems. Nucleic Acids Res 32:D284–D288

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Riveros-Rosas H, Pfeifer GD, Lynam DR, Pedroza JL, Julián-Sánchez A, Canales O, Garfias J (1997) Personal exposure to elements in Mexico City air. Sci Total Environ 198:79–96

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez M, Petersen M, Mundy J (2010) Mitogen-activated protein kinase signaling in plants. Annu Rev Plant Biol 61:621–649

    Article  CAS  PubMed  Google Scholar 

  • Sancenon V, Puig S, Mateu-Andres I, Dorcey E, Thiele DJ, Penarrubia L (2004) The Arabidopsis copper transporter COPT1 functions in root elongation and pollen development. J Biol Chem 279:15348–15355

    Article  CAS  PubMed  Google Scholar 

  • Sangwan V, Örvar BL, Beyerly J, Hirt H, Dhindsa RS (2002) Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant MAP kinase pathways. Plant J 31:629–638

    Article  CAS  PubMed  Google Scholar 

  • Shanker AK, Cervantes C, Loza-Tavera H, Avudainayagam S (2005) Chromium toxicity in plants. Environ Int 31:739–753

    Article  CAS  PubMed  Google Scholar 

  • Shringarpure R, Grune T, Mehlhase J, Davies KJ (2003) Ubiquitin conjugation is not required for the degradation of oxidized proteins by proteasome. J Biol Chem 278:311–318

    Article  CAS  PubMed  Google Scholar 

  • Sinha S, Saxena R, Singh S (2002) Comparative study on accumulation of Cr from metal solution and tannery effluent under repeated metal exposure by aquatic plants: its toxic effects. Chemosphere 80:17–31

    CAS  Google Scholar 

  • Usadel B, Nagel A, Thimm O, Redestig H, Blaesing OE, Palacios-Rojas N, Selbig J, Hannemann J, Piques MC, Steinhauser D, Scheible WR, Gibon Y, Morcuende R, Weicht D, Meyer S, Stitt M (2005) Extension of the visualization tool MapMan to allow statistical analysis of arrays, display of corresponding genes, and comparison with known responses. Plant Physiol 138:1195–1204

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vij S, Giri J, Dansana PK, Kapoor S, Tyagi AK (2008) The receptor-like cytoplasmic kinase (OsRLCK) gene family in rice: organization, phylogenetic relationship, and expression during development and stress. Mol Plant 1:732–750

    Article  CAS  PubMed  Google Scholar 

  • WHO (World Health Organization) (1988) Chromium. Environmental health criteria 61. World Health Organisation, Geneva

    Google Scholar 

  • Winter D, Vinegar B, Nahal H, Ammar R, Wilson G, Provart N (2007) An “electronic fluorescent pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2:e718

    Article  PubMed Central  PubMed  Google Scholar 

  • Yamamoto A, Wada O, Ono T (1981) A low-molecular-weight, chromium-binding substance in mammals. Toxicol Appl Pharmacol 59:515–523

    Article  CAS  PubMed  Google Scholar 

  • Yeh CM, Chien PS, Huang HJ (2007) Distinct signaling pathways for induction of MAP kinase activities by cadmium and copper in rice roots. J Exp Bot 58:659–671

    Article  CAS  PubMed  Google Scholar 

  • Yuan M, Chu Z, Li X, Xu C, Wang S (2010) The bacterial pathogen Xanthomonas oryzae overcomes rice defenses by regulating host copper redistribution. Plant Cell 22:3164–3176

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zeng LR, Park CH, Venu RC, Gough J, Wang GL (2008) Classification, expression pattern, and E3 ligase activity assay of rice U-box-containing proteins. Mol Plant 1:800–815

    Article  CAS  PubMed  Google Scholar 

  • Zhao D, Ni W, Feng B, Han T, Petrasek MG, Ma H (2003) Members of the ASK gene family exhibit a variety of expression patterns and may play diverse roles in Arabidopsis. Plant Physiol 133:203–217

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

This work was supported by research grants from the National Science Council (NSC) and Ministry of Education, Taiwan. Microarray assays were performed by the DNA Microarray Core Laboratory at the Institute of Plant and Microbial Biology, Academia Sinica. Data mining performed at the Bioinformatics Core for Genomic Medicine and Biotechnology Development at NCKU was supported by the NSC (97-3112-B-006 -011). Furthermore, we thank Ms. Laura Smales (Canada) for English editing.

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  1. Department of Life Sciences, National Cheng Kung University, No. 1 University Road, Tainan City, 701, Taiwan

    Tsai-Lien Huang, Li-Yao Huang, Ngoc-Nam Trinh & Hao-Jen Huang

  2. Department of Biology, National Changhua University of Education, No. 1, Jin-De Road, Changhua City, 500, Taiwan

    Shih-Feng Fu

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  1. Tsai-Lien Huang
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Huang, TL., Huang, LY., Fu, SF. et al. Genomic profiling of rice roots with short- and long-term chromium stress. Plant Mol Biol 86, 157–170 (2014). https://doi.org/10.1007/s11103-014-0219-4

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