Evaluation of Candidate Reference Genes for Normalization of Quantitative RT-PCR in Soybean Tissues under Various Abiotic Stress Conditions

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Le, Dung Tien ^a   Aldrich, Donavan L ^b   Valliyodan, Babu ^b   Watanabe, Yasuko ^a   van Ha, Chien ^a   Nishiyama, Rie ^a   Guttikonda, Satish K ^b,c   Quach, Truyen N ^b,d   Gutierrez Gonzalez, Juan J ^b,e   Tran, Lam Son Phan ^a   Nguyen, Henry T ^b  

^a RIKEN   (Japan)

^b UNIVERSITY OF MISSOURI   (United States)

^c Dow AgroSciences   (United States)

^d UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^e UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ABSCISIC ACID; ALPHA TUBULIN; BETA TUBULIN; ELONGATION FACTOR 1ALPHA; ELONGATION FACTOR 1BETA; F BOX PROTEIN; INSULINASE;

60S GENE; ABC GENE; ABIOTIC STRESS; ACT11 GENE; ACT27 GENE; ARTICLE; CDPK GENE; COLD STRESS; CONTROLLED STUDY; CYP2 GENE; DROUGHT STRESS; ELF1A GENE; ELF1B GENE; FBOX GENE; GENE; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC STABILITY; IDE GENE; NONHUMAN; PLANT GENE; PLANT GENETICS; PLANT ROOT; PLANT TISSUE; QUANTITATIVE ANALYSIS; REFERENCE GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SALINITY; SALT STRESS; SEEDLING; SHOOT; SOYBEAN; SUBI2 GENE; TISSUE SPECIFICITY; TUBA GENE; TUBB GENE; VALIDATION PROCESS;

ABSCISIC ACID; BASE SEQUENCE; COLD-SHOCK RESPONSE; DEHYDRATION; DNA PRIMERS; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; PLANT GROWTH REGULATORS; PLANT ROOTS; REAL-TIME POLYMERASE CHAIN REACTION; REFERENCE STANDARDS; SALT-TOLERANCE; SOYBEANS; STRESS, PHYSIOLOGICAL; TRANSCRIPTION, GENETIC;

GLYCINE MAX;

EID: 84867012974     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0046487     Document Type: Article

References (64)

1. Tran LS, Mochida K, (2010) Functional genomics of soybean for improvement of productivity in adverse conditions. Funct Integr Genomics 10: 447-462.
2. Tran LS, Nguyen HT (2009) Future biotechnology of legumes. In: Emerich WD, Krishnan H, editors. Nitrogen fixation in crop production. Madison, WI: ASA-CSA-SSSA. pp. 265-308.
3. Thao NP, Tran LS, (2011) Potentials toward genetic engineering of drought-tolerant soybean. Crit Rev Biotechnol doi:10.3109/07388551.2011.643463.
4. Gutierrez-Gonzalez JJ, Guttikonda SK, Tran LS, Aldrich DL, Zhong R, et al. (2010) Differential expression of isoflavone biosynthetic genes in soybean during water deficits. Plant Cell Physiol 51: 936-948.
5. Neelakandan AK, Nguyen HT, Kumar R, Tran LS, Guttikonda SK, et al. (2010) Molecular characterization and functional analysis of Glycine max sterol methyl transferase 2 genes involved in plant membrane sterol biosynthesis. Plant Mol Biol 74: 503-518.
6. Hadiarto T, Tran LS, (2011) Progress studies of drought-responsive genes in rice. Plant Cell Rep 30: 297-310.
7. Manavalan LP, Guttikonda SK, Tran LS, Nguyen HT, (2009) Physiological and molecular approaches to improve drought resistance in soybean. Plant Cell Physiol 50: 1260-1276.
8. Tran LS, Nakashima K, Shinozaki K, Yamaguchi-Shinozaki K, (2007) Plant gene networks in osmotic stress response: from genes to regulatory networks. Methods Enzymol 428: 109-128.
9. Nakashima K, Ito Y, Yamaguchi-Shinozaki K, (2009) Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol 149: 88-95.
10. Jogaiah S, Ramsandra Govind S, Tran LS, (2012) System biology-based approaches towards understanding drought tolerance in food crops. Crit Rev Biotechnol doi: 10.3109/07388551.2012.659174.
11. Tran LS, Nishiyama R, Yamaguchi-Shinozaki K, Shinozaki K, (2010) Potential utilization of NAC transcription factors to enhance abiotic stress tolerance in plants by biotechnological approach. GM Crops 1: 32-39.
12. Valliyodan B, Nguyen HT, (2006) Understanding regulatory networks and engineering for enhanced drought tolerance in plants. Curr Opin Plant Biol 9: 189-195.
13. Xin H, Qin F, Tran LS (2012) Transcription factors involved in environmental stress responses in plants. In: Ahmad P, Prasad MNV, editors. Environmental Adaptations and Stress Tolerance of Plants in the Era of Climate Change. New York: Springer. pp. 279-295.
14. Choudhary SP, Volkan Oral H, Bhardwaj R, Yu JQ, Tran LS, (2012) Interaction of Brassinosteroids and Polyamines Enhances Copper Stress Tolerance in Raphanus Sativus. J Exp Bot doi: 10.1093/jxb/ers219.
15. Ma Y, Qin F, Tran LS, (2012) Contribution of Genomics to Gene Discovery in Plant Abiotic Stress Responses. Molecular Plant doi: 10.1093/mp/sss085.
16. Choudhary SP, Yu JQ, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS, (2012) Benefits of brassinosteroid crosstalk. Trends Plant Sci Available: http://dx.doi.org/10.1016/j.tplants.2012.05.012.
17. Ha S, Vankova R, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS, (2012) Cytokinins: metabolism and function in plant adaptation to environmental stresses. Trends Plant Sci 17: 172-179.
18. Le DT, Choi JD, Tran LS, (2010) Amino acids conferring herbicide resistance in tobacco acetohydroxyacid synthase. GM Crops 1: 62-67.
19. Mochida K, Shinozaki K, (2011) Advances in omics and bioinformatics tools for systems analyses of plant functions. Plant Cell Physiol 52: 2017-2038.
20. Alwine JC, Kemp DJ, Stark GR, (1977) Method for detection of specific RNAs in agarose gels by transfer to diazobenzyloxymethyl-paper and hybridization with DNA probes. Proc Natl Acad Sci U S A 74: 5350-5354.
21. Tran LS, 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.
22. Tran LS, Urao T, Qin F, Maruyama K, Kakimoto T, et al. (2007) Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc Natl Acad Sci U S A 104: 20623-20628.
23. Stolf-Moreira R, Lemos EGM, Carareto-Alves L, Marcondes J, Pereira SS, et al. (2011) Transcriptional Profiles of Roots of Different Soybean Genotypes Subjected to Drought Stress. Plant Molecular Biology Reporter 29: 19-34.
24. Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, et al. (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31: 279-292.
25. Kreps JA, Wu Y, Chang HS, Zhu T, Wang X, et al. (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130: 2129-2141.
26. Tran LS, Nakashima K, Sakuma Y, Osakabe Y, Qin F, et al. (2007) Co-expression of the stress-inducible zinc finger homeodomain ZFHD1 and NAC transcription factors enhances expression of the ERD1 gene in Arabidopsis. Plant J 49: 46-63.
27. Nishiyama R, Le DT, Watanabe Y, Matsui A, Tanaka M, et al. (2012) Transcriptome analyses of a salt-tolerant cytokinin-deficient mutant reveal differential regulation of salt stress response by cytokinin deficiency. PLoS One 7: e32124.
28. Qin F, Kodaira KS, Maruyama K, Mizoi J, Tran LS, et al. (2011) SPINDLY, a negative regulator of gibberellic acid signaling, is involved in the plant abiotic stress response. Plant Physiol 157: 1900-1913.
29. Kodaira KS, Qin F, Tran LS, Maruyama K, Kidokoro S, et al. (2011) Arabidopsis Cys2/His2 zinc-finger proteins AZF1 and AZF2 negatively regulate abscisic acid-repressive and auxin-inducible genes under abiotic stress conditions. Plant Physiol 157: 742-756.
30. Ballman KV, (2008) Genetics and genomics: gene expression microarrays. Circulation 118: 1593-1597.
31. Tang T, Francois N, Glatigny A, Agier N, Mucchielli MH, et al. (2007) Expression ratio evaluation in two-colour microarray experiments is significantly improved by correcting image misalignment. Bioinformatics 23: 2686-2691.
32. To TK, Nakaminami K, Kim JM, Morosawa T, Ishida J, et al. (2011) Arabidopsis HDA6 is required for freezing tolerance. Biochemical and Biophysical Research Communications 406: 414-419.
33. Matsui A, Ishida J, Morosawa T, Mochizuki Y, Kaminuma E, et al. (2008) Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tiling array. Plant Cell Physiol 49: 1135-1149.
34. Matsui A, Ishida J, Morosawa T, Okamoto M, Kim JM, et al. (2010) Arabidopsis tiling array analysis to identify the stress-responsive genes. Methods Mol Biol 639: 141-155.
35. Czechowski T, Bari RP, Stitt M, Scheible WR, Udvardi MK, (2004) Real-time RT-PCR profiling of over 1400 Arabidopsis transcription factors: unprecedented sensitivity reveals novel root- and shoot-specific genes. Plant Journal 38: 366-379.
36. Nolan T, Hands RE, Bustin SA, (2006) Quantification of mRNA using real-time RT-PCR. Nature Protocols 1: 1559-1582.
37. Ginzinger DG, (2002) Gene quantification using real-time quantitative PCR: An emerging technology hits the mainstream. Experimental Hematology 30: 503-512.
38. Udvardi MK, Czechowski T, Scheible WR, (2008) Eleven golden rules of quantitative RT-PCR. Plant Cell 20: 1736-1737.
39. Tran LS, Quach TN, Guttikonda SK, Aldrich DL, Kumar R, et al. (2009) Molecular characterization of stress-inducible GmNAC genes in soybean. Mol Genet Genomics 281: 647-664.
40. Le DT, Nishiyama R, Watanabe Y, Mochida K, Yamaguchi-Shinozaki K, et al. (2011) Genome-wide expression profiling of soybean two-component system genes in soybean root and shoot tissues under dehydration stress. DNA Res 18: 17-29.
41. Le DT, Nishiyama R, Watanabe Y, Mochida K, Yamaguchi-Shinozaki K, et al. (2011) Genome-wide survey and expression analysis of the plant-specific NAC transcription factor family in soybean during development and dehydration stress. DNA Res 18: 263-276.
42. Pereira SS, Guimaraes FC, Carvalho JF, Stolf-Moreira R, Oliveira MC, et al. (2011) Transcription factors expressed in soybean roots under drought stress. Genet Mol Res 10doi: 10.4238/2011.October.4221.4235.
43. Gutierrez L, Mauriat M, Guenin S, Pelloux J, Lefebvre JF, et al. (2008) The lack of a systematic validation of reference genes: a serious pitfall undervalued in reverse transcription-polymerase chain reaction (RT-PCR) analysis in plants. Plant Biotechnol J 6: 609-618.
44. Jian B, Liu B, Bi Y, Hou W, Wu C, et al. (2008) Validation of internal control for gene expression study in soybean by quantitative real-time PCR. BMC Mol Biol 9: 59.
45. Hu R, Fan C, Li H, Zhang Q, Fu YF, (2009) Evaluation of putative reference genes for gene expression normalization in soybean by quantitative real-time RT-PCR. BMC Mol Biol 10: 93.
46. Libault M, Thibivilliers S, Bilgin DD, Radwan O, Benitez M, et al. (2008) Identification of four soybean reference genes for gene expression normalization. The Plant Genome 1: 44-54.
47. Stolf-Moreira R, Lemos EGM, Abdelnoor RV, Beneventi MA, Rolla AAP, et al. (2011) Identification of reference genes for expression analysis by real-time quantitative PCR in drought-stressed soybean. Pesquisa Agropecuária Brasileira 46: 58-65.
48. Ramakers C, Ruijter JM, Deprez RH, Moorman AF, (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339: 62-66.
49. Ruijter JM, Ramakers C, Hoogaars WM, Karlen Y, Bakker O, et al. (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res 37: e45.
50. Silver N, Best S, Jiang J, Thein SL, (2006) Selection of housekeeping genes for gene expression studies in human reticulocytes using real-time PCR. BMC Mol Biol 7: 33.
51. Gao SQ, Chen M, Xu ZS, Zhao CP, Li L, et al. (2011) The soybean GmbZIP1 transcription factor enhances multiple abiotic stress tolerances in transgenic plants. Plant Mol Biol 75: 537-553.
52. Nishiyama R, Watanabe Y, Fujita Y, Le DT, Kojima M, et al. (2011) Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought, salt and abscisic acid responses, and abscisic acid biosynthesis. Plant Cell 23: 2169-2183.
53. Aslam M, Grover A, Sinha VB, Fakher B, Pande V, et al. (2012) Isolation and characterization of cold responsive NAC gene from Lepidium latifolium. Mol Biol Rep DOI: 10.1007/s11033-012-1828-0.
54. Irsigler AS, Costa MD, Zhang P, Reis PA, Dewey RE, et al. (2007) Expression profiling on soybean leaves reveals integration of ER- and osmotic-stress pathways. BMC Genomics 8: 431.
55. Stolf-Moreira R, Medri ME, Neumaier N, Lemos NG, Brogin RL, et al. (2010) Cloning and quantitative expression analysis of drought-induced genes in soybean. Genet Mol Res 9: 858-867.
56. Nouri MZ, Hiraga S, Yanagawa Y, Sunohara Y, Matsumoto H, et al. (2012) Characterization of calnexin in soybean roots and hypocotyls under osmotic stress. Phytochemistry 74: 20-29.
57. Xie ZM, Zou HF, Lei G, Wei W, Zhou QY, et al. (2009) Soybean Trihelix transcription factors GmGT-2A and GmGT-2B improve plant tolerance to abiotic stresses in transgenic Arabidopsis. PLoS One 4: e6898.
58. Wei W, Huang J, Hao YJ, Zou HF, Wang HW, et al. (2009) Soybean GmPHD-type transcription regulators improve stress tolerance in transgenic Arabidopsis plants. PLoS One 4: e7209.
59. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: RESEARCH0034.
60. Toda K, Takahashi R, Iwashina T, Hajika M, (2011) Difference in chilling-induced flavonoid profiles, antioxidant activity and chilling tolerance between soybean near-isogenic lines for the pubescence color gene. J Plant Res 124: 173-182.
61. Maruyama K, Todaka D, Mizoi J, Yoshida T, Kidokoro S, et al. (2012) Identification of cis-acting promoter elements in cold- and dehydration-induced transcriptional pathways in Arabidopsis, rice, and soybean. DNA Res 19: 37-49.
62. Fujita Y, Fujita M, Shinozaki K, Yamaguchi-Shinozaki K, (2011) ABA-mediated transcriptional regulation in response to osmotic stress in plants. J Plant Res 124: 509-525.
63. Kortner TM, Valen EC, Kortner H, Marjara IS, Krogdahl A, et al. (2011) Candidate reference genes for quantitative real-time PCR (qPCR) assays during development of a diet-related enteropathy in Atlantic salmon (Salmo salar L.) and the potential pitfalls of uncritical use of normalization software tools. Aquaculture 318: 355-363.
64. Mehdi Khanlou K, Van Bockstaele E, (2012) A critique of widely used normalization software tools and an alternative method to identify reliable reference genes in red clover (Trifolium pratense L.). Planta doi:.