Mercury (Hg) is a serious environmental pollution threat to the planet. The accumulation of Hg in plants disrupts many cellular-level functions and inhibits growth and development, but the mechanism is not fully understood. To gain more insight into the cellular response to Hg, we performed a large-scale analysis of the rice transcriptome during Hg stress. Genes induced with short-term exposure represented functional categories of cell-wall formation, chemical detoxification, secondary metabolism, signal transduction and abiotic stress response. Moreover, Hg stress upregulated several genes involved in aromatic amino acids (Phe and Trp) and increased the level of free Phe and Trp content. Exogenous application of Phe and Trp to rice roots enhanced tolerance to Hg and effectively reduced Hg-induced production of reactive oxygen species. Hg induced calcium accumulation and activated mitogen-activated protein kinase. Further characterization of the Hg-responsive genes we identified may be helpful for better understanding the mechanisms of Hg in plants.
References
[1]
Zabihi M, Haghighi Asl A, Ahmadpour A (2010) Studies on adsorption of mercury from aqueous solution on activated carbons prepared from walnut shell. J Hazard Mater 174: 251–256.
[2]
Li P, Feng XB, Qiu GL, Shang LH, Li ZG (2009) Mercury pollution in Asia: a review of the contaminated sites. J Hazard Mater 168: 591–601.
[3]
Zhou ZS, Huang SQ, Guo K, Mehta SK, Zhang PC, et al. (2007) Metabolic adaptations to mercury-induced oxidative stress in roots of Medicago sativa L. J Inorg Biochem. 101: 1–9.
[4]
Beauford W, Barber J, Barringer AR (1977) Uptake and distribution of mercury within higher plants. Physiol Plant 39: 261–265.
[5]
Cobbett CS (2000) Phytochelatins and their roles in heavy metal detoxification. Plant Physiol 123: 825–832.
[6]
Chen YA, Chi WC, Huang TL, Lin CY, Quynh Nguyeh TT, et al. (2012) Mercury-induced biochemical and proteomic changes in rice roots. Plant Physiol Biochem 55: 23–32.
[7]
Heidenreich B, Mayer K, Sandermann HJR, Ernst D (2001) Mercury-induced genes in Arabidopsis thaliana: identification of induced genes upon long-term mercuric ion exposure. Plant Cell Environ 24: 1227–1234.
[8]
Lopes MS, Iglesia-Turi？o S, Cabrera-Bosquet L, Serret MD, Bort J, et al. (2013) Molecular and physiological mechanisms associated with root exposure to mercury in barley. Metallomics 5: 1305–1315.
[9]
Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: An overview. Arch Biochem Biophys 444: 139–158.
[10]
Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S (2002) The protein kinase complement of the human genome. Science 298: 1912–1934.
[11]
Gao LL, Xue HW (2011) Global analysis of expression profiles of rice receptor-like kinase genes. Mol Plant 5: 143–153.
[12]
Yeh CM, Chien PS, Huang HJ (2007) Distinct signalling pathways for induction of MAP kinase activities by cadmium and copper in rice roots. J Exp Bot 58: 659–671.
[13]
Trinh NN, Huang TL, Chi WC, Fu SF, Chen CC, et al. (2014) Chromium stress response effect on signal transduction and expression of signaling genes in rice. Physiol Plant 150: 205–224.
[14]
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402–408.
[15]
Chi WC, Fu SF, Huang TL, Chen YA, Chen CC, et al. (2011) Identification of transcriptome profiles and signaling pathways for the allelochemical juglone in rice roots. Plant Mol Biol 77: 591–607.
[16]
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.
[17]
Thimm O, Bl？sing O, Gibon Y, Nagel A, Meyer S, et al. (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37: 914–939.
[18]
Werner T (2008) Bioinformatics applications for pathway analysis of microarray data. Curr Opin Biotechnol 19: 50–54.
[19]
Usadel B, Nagel A, Thimm O, Redestig H, Blaesing OE, et al. (2005) Extension of the visualization tool mapman to allow statistical analysis of arrays, display of coresponding genes, and comparison with known responses. Plant Physiol 138: 1195–1204.
[20]
Potters G, Pasternak TP, Guisez Y, Palme KJ, Jansen MAK (2007) Stress-induced morphogenic responses: growing out of trouble? Trends Plant Sci 12: 98–105.
[21]
Massot N, Nicander B, Barceló J, Poschenrieder C, Tillberg E (2002) A rapid increase in cytokinin levels and enhanced ethylene evolution precede Al3+-induced inhibition of root growth in bean seedlings (Phaseolus vulgaris L.). Plant Growth Regul 37: 105–112.
[22]
Christensen JH, Bauw G, Welinder KG, Van Montagu M, Boerjan W (1998) Purification and characterization of peroxidases correlated with lignification in poplar xylem. Plant Physiol 118: 125–135.
[23]
Bohm PAF, Zanardo FML, Ferrarese MLL, Ferrarese-Filho O (2006) Peroxidase activity and lignification in soybean root growth-inhibition by juglone. Biol Plant 50: 315–317.
[24]
Baerson SR, Sánchez-Moreiras A, Pedrol-Bonjoch N, Schulz M, Kagan IA, et al. (2005) Detoxification and transcriptome response in Arabidopsis seedlings exposed to the allelochemical benzoxazolin-2(3H)-one. J Biol Chem 280: 21867–21881.
[25]
Soranzo N, Sari Gorla M, Mizzi L, De Toma G, Frova C (2004) Organisation and structural evolution of the rice glutathione S-transferase gene family. Mol Genet Genomics 271: 511–521.
[26]
Marrs KA (1996) The functions and regulation of plant glutathione S-transferases. Annu Rev Plant Physiol Plant Mol Biol 47: 127–158.
[27]
Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53: 159–182.
[28]
Ruiz ON, Alvarez D, Torres C, Roman L, Daniell H (2011) Metallothionein expression in chloroplasts enhances mercury accumulation and phytoremediation capability. Plant Biotechnol J 9: 609–617.
[29]
Herrmann KM, Weaver LM (1999) The shikimate pathway. Annu Rev Plant Physiol Plant Mol Biol 50: 473–503.
[30]
Sharma SS, Dietz KJ (2006) The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot 57: 711–726.
[31]
Jo WJ, Loguinov A, Chang M, Wintz H, Nislow C, et al. (2008) Identification of genes involved in the toxic response of Saccharomyces cerevisiae against iron and copper overload by parallel analysis of deletion mutants. Toxicol Sci 101: 140–151.
[32]
Sanjaya, Hsiao PY, Su RC, Ko SS, Tong CG, et al. (2008) Overexpression of Arabidopsis thaliana tryptophan synthase beta 1 (AtTSB1) in Arabidopsis and tomato confers tolerance to cadmium stress. Plant Cell Environ 31: 1074–1085.
[33]
Kang K, Park S, Natsagdorj U, Kim YS, Back K (2011) Methanol is an endogenous elicitor molecule for the synthesis of tryptophan and tryptophan-derived secondary metabolites upon senescence of detached rice leaves. Plant J 66: 247–57.
[34]
Rea PA (1999) MRP subfamily ABC transporters from plants and yeast. J Exp Bot 50 (Special Issue): 895–913.
[35]
Ouyang J, Cai Z, Xia K, Wang Y, Duan J, et al. (2010) Identification and analysis of eight peptide transporter homologs in rice. Plant Sci 179: 374–382.
[36]
Song W, Koh S, Czako M, Marton L, Drenkard E, et al. (1997) Antisense expression of the peptide transport gene AtPTR2-B delays flowering and arrests seed development in transgenic Arabidopsis plants. Plant Physiol 114: 927–935.
[37]
Zhang WH, Tyerman SD (1999) Inhibition of water channels by HgCl2 in intact wheat root cells. Plant Physiol 120: 849–858.
[38]
Daniels MJ, Mirkov TE, Chrispeels MJ (1994) The plasma membrane of Arabidopsis thaliana contains a mercury-insensitive aquaporin that is a homolog of the tonoplast water channel protein TIP. Plant Physiol 106: 1325–1333.
[39]
Biela A, Grote K, Otto B, Hoth S, Hedrich R, et al. (1999) The Nicotiana tabacum plasma membrane aquaporin NtAQP1 is mercury-insensitive and permeable for glycerol. Plant J 18: 565–570.
[40]
Becraft PW (2002) Receptor kinase signaling in plant development. Annu Rev Cell Dev Biol 18: 163–192.
[41]
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.
[42]
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.
[43]
Shiu SH, Karlowski WM, Pan R, Tzeng YH, Mayer KF, et al. (2004) Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16: 1220–1234.
[44]
Pitorre D, Llauro C, Jobet E, Guilleminot J, Brizard JP, et al. (2010) RLK7, a leucine-rich repeat receptor-like kinase, is required for proper germination speed and tolerance to oxidative stress in Arabidopsis thaliana. Planta 232: 1339–1353.
[45]
Rodriguez M, Petersen M, Mundy J (2010) Mitogen-activated protein kinase signaling in plants. Annu Rev Plant Biol 61: 621–649.
[46]
Fu SF, Chou WC, Huang DD, Huang HJ (2002) Transcriptional regulation of a rice mitogen-activated protein kinase gene, OsMAPK4, in response to environmental stresses. Plant Cell Physiol 43: 958–963.
[47]
Kim JA, Agrawal GK, Rakwal R, Han KS, Kim KN, et al. (2003) Molecular cloning and mRNA expression analysis of a novel rice (Oryza sativa L.) MAPK kinase kinase, OsEDR1, an ortholog of Arabidopsis AtEDR1, reveal its role in defense/stress signalling pathways and development. Biochem Biophys Res Commun 300: 868–876.
[48]
Agarwal PK, Gupta K, Jha B (2010) Molecular characterization of the Salicornia brachiata SbMAPKK gene and its expression by abiotic stress. Mol Biol Rep 37: 981–986.
[49]
Agarwal PK, Agarwal P, Reddy MK, Sopory SK (2006) Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep 25: 1263–1274.
[50]
Katiyar-Agarwal S, Agarwal M, Grover A (2003) Heat-tolerant basmati rice engineered by over-expression of hsp101. Plant Mol Biol 51: 677–686.
[51]
Yokotani N, Ichikawa T, Kondou Y, Matsui M, Hirochika H, et al. (2008) Expression of rice heat stress transcription factor OsHsfA2e enhances tolerance to environmental stresses in transgenic Arabidopsis. Planta 227: 957–967.
[52]
Ishihama N, Yamada R, Yoshioka M, Katou S, Yoshioka H (2011) Phosphorylation of the Nicotiana benthamiana WRKY8 transcription factor by MAPK functions in the defense response. Plant Cell 23: 1153–1170.
[53]
Chen L, Song Y, Li S, Zhang L, Zou C, et al. (2012) The role of WRKY transcription factors in plant abiotic stresses. Biochim Biophys Acta 1819: 120–128.
[54]
Fridborg I, Kuusk S, Moritz T, Sundberg E (1999) The Arabidopsis dwarf mutant shi exhibits reduced gibberellin responses conferred by overexpression of a new putative zinc finger protein. Plant Cell 11: 1019–1031.
[55]
Lin CY, Trinh NN, Fu SF, Hsiung YC, Chia LC, et al. (2013) Comparison of early transcriptome responses to copper and cadmium in rice roots. Plant Mol Biol 81: 507–22.
[56]
Hirayama T, Shinozaki K (2010) Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J 61: 1041–1052.
