Genome-wide transcriptome analysis reveals that cadmium stress signaling controls the expression of genes in drought stress signal pathways in rice

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Oono, Youko ^a   Yazawa, Takayuki ^a,b   Kawahara, Yoshihiro ^a   Kanamori, Hiroyuki ^a   Kobayashi, Fuminori ^a   Sasaki, Harumi ^a   Mori, Satomi ^a   Wu, Jianzhong ^a   Handa, Hirokazu ^a   Itoh, Takeshi ^a   Matsumoto, Takashi ^a  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^b HITACHI LTD   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CADMIUM; CHELATING AGENT; SCAVENGER; CATION TRANSPORT PROTEIN;

ARTICLE; CELLULAR STRESS SIGNAL; DREB GENE; DROUGHT STRESS; GENE ACTIVATION; GENE CONTROL; GENE EXPRESSION; GENE ONTOLOGY; GENETIC ANALYSIS; GENOME WIDE TRANSCRIPTOME ANALYSIS; MICROARRAY ANALYSIS; NONHUMAN; PLANT GENE; PLANT GENETICS; PLANT STRUCTURES; PROTEIN EXPRESSION; QUALITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RICE; RNA SEQUENCE; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; TRANSCRIPTOMICS; UPREGULATION; CYTOLOGY; DROUGHT; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GENOMICS; METABOLISM; MULTIGENE FAMILY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; TOXICITY;

CADMIUM; CATION TRANSPORT PROTEINS; DROUGHTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENOMICS; MULTIGENE FAMILY; ORYZA SATIVA; SEQUENCE ANALYSIS, RNA; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; UP-REGULATION;

EID: 84901240811     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0096946     Document Type: Article

References (90)

1. Clemens S, Palmgren MG, Krämer U (2002) A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci 7: 309-315. (Pubitemid 36726515)
2. Roth U, von Roepenack-Lahaye E, Clemens S (2006) Proteome changes in Arabidopsis thaliana roots upon exposure to Cd2+. J Exp Bot 57: 4003-4013. (Pubitemid 44950400)
3. Zhang M, Liu X, Yuan L, Wu K, Duan J, et al. (2012) Transcriptional profiling in cadmium-treated rice seedling roots using suppressive subtractive hybridization. Plant Physiol Biochem 50: 79-86.
4. Halliwell B, Gutteridge JM (1984) Oxygen-toxicity, oxygen radicals, transition-metals and disease. Biochem J 219: 1-14. (Pubitemid 14171443)
5. Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, et al. (2011) ROS signaling: the new wave? Trends Plant Sci 16: 300-309.
6. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9: 490-498. (Pubitemid 39301187)
7. Frova C (2003) The plant glutathione transferase gene family: genomic structure, functions, expression and evolution. Physiol Plant 119: 469-479.
8. Cosio C, Dunand C (2009) Specific functions of individual class III peroxidase genes. J Exp Bot 60: 391-408.
9. Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53: 159-182. (Pubitemid 36257491)
10. Kramer U, Talke IN, Hanikenne M (2007) Transition metal transport. FEBS Lett 581: 2263-2272. (Pubitemid 46726303)
11. Moons A (2003) Ospdr9, which encodes a PDR-type ABC transporter, is induced by heavy metals, hypoxic stress and redox perturbations in rice roots. FEBS Lett 553: 370-376.
12. Uraguchi S, Kamiya T, Sakamoto T, Kasai K, Sato Y, et al. (2011) Low-affinity cation transporter (OsLCT1) regulates cadmium transport into rice grains. Proc Natl Acad Sci USA 108: 20959-20964.
13. Ueno D, Yamaji N, Kono I, Huang CF, Ando T, et al. (2010) Gene limiting cadmium accumulation in rice. Proc Natl Acad Sci USA 107: 16500-16505.
14. Korshunova YO, Eide D, Clark WG, Guerinot ML, Pakrasi HB (1999) The IRT1 protein from Arabidopsis thaliana is a metal transporter with a broad substrate range. Plant Mol Biol 40: 37-44.
15. Grossoehme NE, Akilesh S, Guerinot ML, Wilcox DE (2006) Metal-binding thermodynamics of the histidine-rich sequence from the metal-transport protein IRT1 of Arabidopsis thaliana. Inorg Chem 45: 8500-8508.
16. Pedas P, Ytting CK, Fuglsang AT, Jahn TP, Schjoerring JK, et al. (2008) Manganese efficiency in barley: identification and characterization of the metal ion transporter HvIRT1. Plant Physiol 148: 455-466. (Pubitemid 352847619)
17. Lee S, An G (2009) Over-expression of OsIRT1 leads to increased iron and zinc accumulations in rice. Plant Cell Environ 32: 408-416.
18. Satoh-Nagasawa N, Mori M, Nakazawa N, Kawamoto T, Nagato Y, et al. (2012) Mutations in rice (Oryza sativa) heavy metal ATPase 2 (OsHMA2) restrict the translocation of zinc and cadmium. Plant Cell Physiol 53: 213-224.
19. Sasaki A, Yamaji N, Yokosho K, Ma JF (2012) Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell 24: 2155-67.
20. Ogawa I, Nakanishi H, Mori S, Nishizawa N (2009) Time course analysis of gene regulation under cadmium stress in rice. Plant and Soil 325: 97-108.
21. Oono Y, Kawahara Y, Kanamori H, Mizuno H, Yamagata H, et al. (2011) mRNA-seq reveals a comprehensive transcriptome profile of rice under phosphate stress. Rice 4: 50-65.
22. Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10: 57-63.
23. Yoshida S, Forno AD, Cock HJ, Gomez AK (1976) Laboratory Manual for Physiological Studies of Rice, 3rd edn. Manila, The Philippines.
24. Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17: 10-12.
25. Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
26. Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111.
27. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, et al. (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511-515.
28. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
29. Mortazavi A, Williams BA, Mccue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621-628. (Pubitemid 351911867)
30. Lee K, Bae DW, Kim SH, Han HJ, Liu X, et al. (2010) Comparative proteomic analysis of the short-term responses of rice roots and leaves to cadmium. J Plant Physiol 167: 161-168.
31. Shah K, Kumar RG, Verma S, Dubey RS (2001) Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings. Plant Sci 161: 1135-1144. (Pubitemid 34003149)
32. Perfus-Barbeoch L, Leonhardt N, Vavasseur A, Forestier C (2002) Heavy metal toxicity: cadmium permeates through calcium channels and disturbs the plant water status. Plant J 32: 539-548. (Pubitemid 36814961)
33. Lu TT, Lu GJ, Fan DL, Zhu CR, Li W, et al. (2010) Function annotation of the rice transcriptome at single-nucleotide resolution by RNA-seq. Genome Res 20: 1238-1249.
34. Jang IC, Oh SJ, Seo JS, Choi WB, Song SI, et al. (2003) Expression of a bifunctional fusion of the Escherichia coli genes for trehalose-6-phosphate synthase and trehalose-6-phosphate phosphatase in transgenic rice plants increases trehalose accumulation and abiotic stress tolerance without stunting growth. Plant Physiol 131: 516-524. (Pubitemid 36219514)
35. Mundy J, Chua NH (1988) Abscisic-acid and water-stress induce the expression of a novel rice gene. Embo J 7: 2279-2286.
36. Yamaguchi-Shinozaki K, Mundy J, Chua NH (1990) 4 tightly linked Rab genes are differentially expressed in rice. Plant Mol Biol 14: 29-39.
37. Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57: 781-803. (Pubitemid 44061045)
38. Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG, et al. (2003) OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. Plant J 33: 751-763. (Pubitemid 36325917)
39. Ito Y, Katsura K, Maruyama K, Taji T, Kobayashi M, et al. (2006) Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant Cell Physiol 47: 141-153. (Pubitemid 43278254)
40. Chen JQ, Meng XP, Zhang Y, Xia M, Wang XP (2008) Over-expression of OsDREB genes lead to enhanced drought tolerance in rice. Biotechnol Lett 30: 2191-2198.
41. Xiang Y, Tang N, Du H, Ye HY, Xiong LZ (2008) Characterization of OsbZIP23 as a key player of the basic leucine zipper transcription factor family for conferring abscisic acid sensitivity and salinity and drought tolerance in rice. Plant Physiol 148: 1938-1952. (Pubitemid 352847471)
42. Zou MJ, Guan YC, Ren HB, Zhang F, Chen F (2008) A bZIP transcription factor, OsABI5, is involved in rice fertility and stress tolerance. Plant Mol Biol 66: 675-683.
43. Iuchi S, Kobayashi M, Taji T, Naramoto M, Seki M, et al. (2001) Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J 27: 325-333. (Pubitemid 32817925)
44. Lefebvre V, North H, Frey A, Sotta B, Seo M, et al. (2006) Functional analysis of Arabidopsis NCED6 and NCED9 genes indicates that ABA synthesized in the endosperm is involved in the induction of seed dormancy. Plant J 45: 309-319. (Pubitemid 43373716)
45. Qin XQ, Zeevaart JAD (2002) Overexpression of a 9-cis-epoxycarotenoid dioxygenase gene in Nicotiana plumbaginifolia increases abscisic acid and phaseic acid levels and enhances drought tolerance. Plant Physiol 128: 544-551.
46. Tan BC, Joseph LM, Deng WT, Liu LJ, Li QB, et al. (2003) Molecular characterization of the Arabidopsis 9-cis epoxycarotenoid dioxygenase gene family. Plant J 35: 44-56. (Pubitemid 36821104)
47. Parcy F, Valon C, Raynal M, Gaubier-Comella P, Delseny M, et al. (1994) Regulation of gene expression programs during Arabidopsis seed development: roles of the ABI3 locus and of endogenous abscisic acid. Plant Cell 6: 1567-1582. (Pubitemid 24986211)
48. Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 47: 377-403.
49. Xiao BZ, Huang YM, Tang N, Xiong LZ (2007) Over-expression of a LEA gene in rice improves drought resistance under the field conditions. Theor Appl Genet 115: 35-46. (Pubitemid 46980424)
50. Takasaki H, Maruyama K, Kidokoro S, Ito Y, Fujita Y, et al. (2010) The abiotic stress-responsive NAC-type transcription factor OsNAC5 regulates stress-inducible genes and stress tolerance in rice. Mol Genet Genomics 284: 173-183.
51. Hu HH, Dai MQ, Yao JL, Xiao BZ, Li XH, et al. (2006) Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci USA 103: 12987-12992.
52. Sperotto RA, Ricachenevsky FK, Duarte GL, Boff T, Lopes KL, et al. (2009) Identification of up-regulated genes in flag leaves during rice grain filling and characterization of OsNAC5, a new ABA-dependent transcription factor. Planta 230: 985-1002.
53. Song SY, Chen Y, Chen J, Dai XY, Zhang WH (2011) Physiological mechanisms underlying OsNAC5-dependent tolerance of rice plants to abiotic stress. Planta 234: 331-345.
54. Tran LSP, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, et al. (2004) Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell 16: 2481-2498. (Pubitemid 39247086)
55. Oh SJ, Kim YS, Kwon CW, Park HK, Jeong JS, et al. (2009) Overexpression of the transcription factor AP37 in rice improves grain yield under drought conditions. Plant Physiol 150: 1368-1379.
56. Xu DQ, Huang J, Guo SQ, Yang X, Bao YM, et al. (2008) Overexpression of a TFIIIA-type zinc finger protein gene ZFP252 enhances drought and salt tolerance in rice (Oryza sativa L.). FEBS Lett 582: 1037-1043.
57. Taji T, Ohsumi C, Seki M, Iuchi S, Yamaguchi-Shinozaki K, et al. (2002) Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 29: 417-426. (Pubitemid 34196954)
58. Sun XM, Zhang JX, Zhang HJ, Ni YW, Zhang Q, et al. (2010) The responses of Arabidopsis thaliana to cadmium exposure explored via metabolite profiling. Chemosphere 78: 840-845.
59. Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14: 1675-1690. (Pubitemid 35002928)
60. Chen SL, Kao CH (1995) Cd induced changes in proline level and peroxidase-activity in roots of rice seedlings. Plant Growth Regul 17: 67-71.
61. Shah K, Dubey RS (1997) Effect of cadmium on proline accumulation and ribonuclease activity in rice seedlings: role of proline as a possible enzyme protectant. Biol Plant 40: 121-130.
62. Ye HY, Du H, Tang N, Li XH, Xiong LZ (2009) Identification and expression profiling analysis of TIFY family genes involved in stress and phytohormone responses in rice. Plant Mol Biol 71: 291-305.
63. Park MR, Yun KY, Mohanty B, Herath V, Xu FY, et al. (2010) Supra-optimal expression of the cold-regulated OsMyb4 transcription factor in transgenic rice changes the complexity of transcriptional network with major effects on stress tolerance and panicle development. Plant Cell Environ 33: 2209-2230.
64. Oh SJ, Song SI, Kim YS, Jang HJ, Kim SY, et al. (2005) Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiol 138: 341-351.
65. Soranzo N, Gorla MS, 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. (Pubitemid 38916394)
66. Passardi F, Longet D, Penel C, Dunand C (2004) The class III peroxidase multigenic in land plants family in rice and its evolution. Phytochemistry 65: 1879-1893. (Pubitemid 38981677)
67. Huang TL, Quynh TTN, Fu SF, Lin CY, Chen YC, et al. (2012) Transcriptomic changes and signalling pathways induced by arsenic stress in rice roots. Plant Mol Biol 80: 587-608.
68. Roxas VP, Lodhi SA, Garrett DK, Mahan JR, Allen RD (2000) Stress tolerance in transgenic tobacco seedlings that overexpress glutathione S-transferase/glutathione peroxidase. Plant Cell Physiol 41: 1229-1234. (Pubitemid 32003660)
69. Hiraga S, Sasaki K, Ito H, Ohashi Y, Matsui H (2001) A large family of class III plant peroxidases. Plant Cell Physiol 42: 462-468. (Pubitemid 32526170)
70. Passardi F, Penel C, Dunand C (2004) Performing the paradoxical: how plant peroxidases modify the cell wall. Trends Plant Sci 9: 534-540. (Pubitemid 39408748)
71. Liu X, Williams CE, Nemacheck JA, Wang H, Subramanyam S, et al. (2010) Reactive oxygen species are involved in plant defense against a gall midge. Plant Physiol 152: 985-999.
72. Ahn IP, Kim S, Kang S, Suh SC, Lee YH (2005) Rice defense mechanisms against Cochliobolus miyabeanus and Magnaporthe grisea are distinct. Phytopathology 95: 1248-1255. (Pubitemid 41541496)
73. Valerio L, De Meyer M, Penel C, Dunand C (2004) Expression analysis of the Arabidopsis peroxidase multigenic family. Phytochemistry 65: 1331-1342. (Pubitemid 38844717)
74. Rouhier N, Couturier J, Jacquot JP (2006) Genome-wide analysis of plant glutaredoxin systems. J Exp Bot 57: 1685-1696. (Pubitemid 43992218)
75. Nuruzzaman M, Gupta M, Zhang CJ, Wang L, Xie WB, et al. (2008) Sequence and expression analysis of the thioredoxin protein gene family in rice. Mol Genet Genomics 280: 139-151.
76. Lee KO, Jang HH, Jung BG, Chi YH, Lee JY, et al. (2000) Rice 1Cys-peroxiredoxin over-expressed in transgenic tobacco does not maintain dormancy but enhances antioxidant activity. FEBS Lett 486: 103-106.
77. Obara K, Sumi K, Fukuda H (2002) The use of multiple transcription starts causes the dual targeting of Arabidopsis putative monodehydroascorbate reductase to both mitochondria and chloroplasts. Plant Cell Physiol 43: 697-705. (Pubitemid 34877884)
78. Considine MJ, Holtzapffel RC, Day DA, Whelan J, Millar AH (2002) Molecular distinction between alternative oxidase from monocots and dicots. Plant Physiol 129: 949-953. (Pubitemid 34801069)
79. Koeduka T, Matsui K, Akakabe Y, Kajiwara T (2002) Catalytic properties of rice alpha-oxygenase - A comparison with mammalian prostaglandin H synthases. J Biol Chem 277: 22648-22655. (Pubitemid 34967242)
80. Koeduka T, Matsui K, Hasegawa M, Akakabe Y, Kajiwara T (2005) Rice fatty acid alpha-dioxygenase is induced by pathogen attack and heavy metal stress: activation through jasmonate signaling. J Plant Physiol 162: 912-920. (Pubitemid 41059480)
81. Tirajoh A, Aung TST, McKay AB, Plant AL (2005) Stress-responsive alpha-dioxygenase expression in tomato roots. J Exp Bot 56: 713-723. (Pubitemid 40295158)
82. Grill E, Loffler S, Winnacker EL, Zenk MH (1989) Phytochelatins, the heavy-metal-binding peptides of plants, are synthesized from glutathione by a specific gamma-glutamylcysteine dipeptidyl transpeptidase (Phytochelatin Synthase). Proc Natl Acad Sci USA 86: 6838-6842.
83. Ha SB, Smith AP, Howden R, Dietrich WM, Bugg S, et al. (1999) Phytochelatin synthase genes from Arabidopsis and the yeast Schizosaccharomyces pombe. Plant Cell 11: 1153-1163.
84. Gautam N, Verma PK, Verma S, Tripathi RD, Trivedi PK, et al. (2012) Genome-wide identification of rice class I metallothionein gene: tissue expression patterns and induction in response to heavy metal stress. Funct Integr Genomics 12: 635-647.
85. Zhou GK, Xu YF, Li J, Yang LY, Liu JY (2006) Molecular analyses of the metallothionein gene family in rice (Oryza sativa L.). J Biochem Mol Biol 39: 595-606. (Pubitemid 44714541)
86. Palmiter RD (1998) The elusive function of metallothioneins. Proc Natl Acad Sci USA 95: 8428-8430.
87. Huang XH, Kurata N, Wei XH, Wang ZX, Wang A, et al. (2012) A map of rice genome variation reveals the origin of cultivated rice. Nature 490: 497-501.
88. Wittkopp PJ, Kalay G (2012) Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nat Rev Genet 13: 59-69.
89. Li LG, He ZY, Pandey GK, Tsuchiya T, Luan S (2002) Functional cloning and characterization of a plant efflux carrier for multidrug and heavy metal detoxification. J Biol Chem 277: 5360-5368. (Pubitemid 34968582)
90. Mizuno T, Usui K, Horie K, Nosaka S, Mizuno N, et al. (2005) Cloning of three ZIP/NRAMP transporter genes from a Ni hyperaccumulator plant Thlaspi japonicum and their Ni2+-transport abilities. Plant Physiol Biochem 43: 793-801. (Pubitemid 41454854)