Differential Expression Analysis of a Subset of Drought-Responsive GmNAC Genes in Two Soybean Cultivars Differing in Drought Tolerance

International Journal of Molecular Sciences

Volumn 14, Issue 12, 2013, Pages 23828-23841

  Thao, Nguyen Phuong ^a   Thu, Nguyen Binh Anh ^a   Hoang, Xuan Lan Thi ^a   Van Ha, Chien ^b,c   Tran, Lam Son Phan ^b  

^a INTERNATIONAL UNIVERSITY   (Viet Nam)

^b RIKEN Center for Sustainable Resource Science   (Japan)

^c Vietnamese Academy of Agricultural Science   (Viet Nam)

Author keywords

Comparative expression analysis; Drought stress; NAC transcription factor; Real time quantitative PCR; Soybean

Indexed keywords

ARTICLE; CONTROLLED STUDY; CULTIVAR; DOWN REGULATION; DROUGHT STRESS; DROUGHT TOLERANCE; GENE; GENE EXPRESSION; GENE SILENCING; GENETIC ENGINEERING; GENOTYPING TECHNIQUE; GMNAC GENE; NONHUMAN; PHENOTYPE; PHYLOGENY; PHYSIOLOGICAL PROCESS; PLANT GROWTH; PLANT ROOT; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; SOYBEAN; UPREGULATION; DROUGHT; GENE EXPRESSION REGULATION; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PLANT GENE;

TRANSCRIPTION FACTOR; VEGETABLE PROTEIN;

DROUGHTS; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENETIC ENGINEERING; GENOTYPE; PLANT PROTEINS; PLANT ROOTS; SOYBEANS; TRANSCRIPTION FACTORS;

EID: 84889817892     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms141223828     Document Type: Article

References (58)

1. Thao, N.P.; Tran, L.-S.P. Potentials toward genetic engineering of drought-tolerant soybean. Crit. Rev. Biotechnol. 2012, 32, 349-362.
2. Shinozaki, K.; Yamaguchi-Shinozaki, K. Gene networks involved in drought stress response and tolerance. J. Exp. Bot. 2007, 58, 221-227.
3. Nishiyama, R.; Watanabe, Y.; Leyva-Gonzalez, M.A.; van Ha, C.; Fujita, Y.; Tanaka, M.; Seki, M.; Yamaguchi-Shinozaki, K.; Shinozaki, K.; Herrera-Estrella, L.; Arabidopsis AHP2, AHP3, and AHP5 histidine phosphotransfer proteins function as redundant negative regulators of drought stress response. Proc. Natl. Acad. Sci. USA 2013, 110, 4840-4845.
4. Yang, S.; Vanderbeld, B.; Wan, J.; Huang, Y. Narrowing down the targets: Towards successful genetic engineering of drought-tolerant crops. Mol. Plant 2010, 3, 469-490.
5. Yamaguchi-Shinozaki, K.; Shinozaki, K. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu. Rev. Plant Biol. 2006, 57, 781-803.
6. Zhang, G.; Chen, M.; Li, L.; Xu, Z.; Chen, X.; Guo, J.; Ma, Y. Overexpression of the soybean GmERF3 gene, an AP2/ERF type transcription factor for increased tolerances to salt, drought, and diseases in transgenic tobacco. J. Exp. Bot. 2009, 60, 3781-3796.
7. Lu, G.; Gao, C.; Zheng, X.; Han, B. Identification of OsbZIP72 as a positive regulator of ABA response and drought tolerance in rice. Planta 2009, 229, 605-615.
8. Abe, H.; Urao, T.; Ito, T.; Seki, M.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 2003, 15, 63-78.
9. Luo, X.; Bai, X.; Sun, X.; Zhu, D.; Liu, B.; Ji, W.; Cai, H.; Cao, L.; Wu, J.; Hu, M. Expression of wild soybean WRKY20 in Arabidopsis enhances drought tolerance and regulates ABA signalling. J. Exp. Bot. 2013, 64, 2155-2169.
10. Tran, L.-S.P.; Nakashima, K.; Sakuma, Y.; Simpson, S.D.; Fujita, Y.; Maruyama, K.; Fujita, M.; Seki, M.; Shinozaki, K.; Yamaguchi-Shinozaki, K. 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 2004, 16, 2481-2498.
11. Souer, E.; van Houwelingen, A.; Kloos, D.; Mol, J.; Koes, R. The no apical meristem gene of petunia is required for pattern formation in embryos and flowers and is expressed at meristem and primordia boundaries. Cell 1996, 85, 159-170.
12. Nuruzzaman, M.; Manimekalai, R.; Sharoni, A.M.; Satoh, K.; Kondoh, H.; Ooka, H.; Kikuchi, S. Genome-wide analysis of NAC transcription factor family in rice. Gene 2010, 465, 30-44.
13. Hu, R.; Qi, G.; Kong, Y.; Kong, D.; Gao, Q.; Zhou, G. Comprehensive analysis of NAC domain transcription factor gene family in Populus trichocarpa. BMC Plant Biol. 2010, 10, 145.
14. Rushton, P.J.; Bokowiec, M.T.; Han, S.; Zhang, H.; Brannock, J.F.; Chen, X.; Laudeman, T.W.; Timko, M.P. Tobacco transcription factors: Novel insights into transcriptional regulation in the Solanaceae. Plant Physiol. 2008, 147, 280-295.
15. Mochida, K.; Yoshida, T.; Sakurai, T.; Yamaguchi-Shinozaki, K.; Shinozaki, K.; Tran, L.S.P. In silico analysis of transcription factor repertoire and prediction of stress responsive transcription factors in soybean. DNA Res. 2009, 16, 353-369.
16. Xie, Q.; Frugis, G.; Colgan, D.; Chua, N.-H. Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev. 2000, 14, 3024-3036.
17. Duval, M.; Hsieh, T.-F.; Kim, S.Y.; Thomas, T.L. Molecular characterization of AtNAM: A member of the Arabidopsis NAC domain superfamily. Plant Mol. Biol. 2002, 50, 237-248.
18. Yoo, S.Y.; Kim, Y.; Kim, S.Y.; Lee, J.S.; Ahn, J.H. Control of flowering time and cold response by a NAC-domain protein in Arabidopsis. PLoS One 2007, 2, e642.
19. Zhong, R.; Richardson, E.A.; Ye, Z.-H. Two NAC domain transcription factors, SND1 and NST1, function redundantly in regulation of secondary wall synthesis in fibers of Arabidopsis. Planta 2007, 225, 1603-1611.
20. Olsen, A.N.; Ernst, H.A.; Leggio, L.L.; Skriver, K. NAC transcription factors: Structurally distinct, functionally diverse. Trends Plant Sci. 2005, 10, 79-87.
21. Puranik, S.; Sahu, P.P.; Srivastava, P.S.; Prasad, M. NAC proteins: Regulation and role in stress tolerance. Trends Plant Sci. 2012, 17, 369-381.
22. Hao, Y.J.; Wei, W.; Song, Q.X.; Chen, H.W.; Zhang, Y.Q.; Wang, F.; Zou, H.F.; Lei, G.; Tian, A.G.; Zhang, W.K. Soybean NAC transcription factors promote abiotic stress tolerance and lateral root formation in transgenic plants. Plant J. 2011, 68, 302-313.
23. Riechmann, J.L.; Ratcliffe, O.J. A genomic perspective on plant transcription factors. Curr. Opin. Plant Biol. 2000, 3, 423-434.
24. Fang, Y.; You, J.; Xie, K.; Xie, W.; Xiong, L. Systematic sequence analysis and identification of tissue-specific or stress-responsive genes of NAC transcription factor family in rice. Mol. Genet. Genomics 2008, 280, 547-563.
25. Nakashima, K.; Tran, L.S.P.; van Nguyen, D.; Fujita, M.; Maruyama, K.; Todaka, D.; Ito, Y.; Hayashi, N.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J. 2007, 51, 617-630.
26. Hu, H.; Dai, M.; Yao, J.; Xiao, B.; Li, X.; Zhang, Q.; Xiong, L. Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc. Natl. Acad. Sci. USA 2006, 103, 12987-12992.
27. Zheng, X.; Chen, B.; Lu, G.; Han, B. Overexpression of a NAC transcription factor enhances rice drought and salt tolerance. Biochem. Bioph. Res. Commun. 2009, 379, 985-989.
28. Xue, G.-P.; Way, H.M.; Richardson, T.; Drenth, J.; Joyce, P.A.; McIntyre, C.L. Overexpression of TaNAC69 leads to enhanced transcript levels of stress up-regulated genes and dehydration tolerance in bread wheat. Mol. Plant 2011, 4, 697-712.
29. Tang, Y.; Liu, M.; Gao, S.; Zhang, Z.; Zhao, X.; Zhao, C.; Zhang, F.; Chen, X. Molecular characterization of novel TaNAC genes in wheat and overexpression of TaNAC2a confers drought tolerance in tobacco. Physiol. Plant. 2012, 144, 210-224.
30. Liu, X.; Liu, S.; Wu, J.; Zhang, B.; Li, X.; Yan, Y.; Li, L. Overexpression of Arachis hypogaea NAC3 in tobacco enhances dehydration and drought tolerance by increasing superoxide scavenging. Plant Physiol. Bioch. 2013, 70, 354-359.
31. Tran, L.S.P.; Quach, T.N.; Guttikonda, S.K.; Aldrich, D.L.; Kumar, R.; Neelakandan, A.; Valliyodan, B.; Nguyen, H.T. Molecular characterization of stress-inducible GmNAC genes in soybean. Mol. Genet. Genomics 2009, 281, 647-664.
32. Soybean Production (Food and Agriculture Organization of the United Nations-FAO). Available online: http://faostat3.fao.org/faostat-gateway/go/to/download/Q/QC/E (accessed on 15 October 2013).
33. Sadeghipour, O.; Abbasi, S. Soybean response to drought and seed inoculation. World Appl. Sci. J. 2012, 17, 55-60.
34. Ku, Y.-S.; Au-Yeung, W.-K.; Yung, Y.-L.; Li, M.-W.; Wen, C.-Q.; Liu, X.; Lam, H.-M. Drought Stress and Tolerance in Soybean. In A Comprehensive Survey of Internaitonal Soybean Research-Genetics, Physiology, Agronomy and Nitrogen Relationships; Board, J.E., Ed.; InTech: New York, NY, USA, 2013; pp. 209-237.
35. Stolf-Moreira, R.; Lemos, E.G.M.; Carareto-Alves, L.; Marcondes, J.; Pereira, S.S.; Rolla, A.A.P.; Pereira, R.M.; Neumaier, N.; Binneck, E.; Abdelnoor, R.V. Transcriptional profiles of roots of different soybean genotypes subjected to drought stress. Plant Mol. Biol. Rep. 2011, 29, 19-34.
36. Le, D.T.; Tarrago, L.; Watanabe, Y.; Kaya, A.; Lee, B.C.; Tran, U.; Nishiyama, R.; Fomenko, D.E.; Gladyshev, V.N.; Tran, L.-S.P. Diversity of plant methionine sulfoxide reductases b and evolution of a form specific for free methionine sulfoxide. PLoS One 2013, 8, e65637.
37. Van Ha, C.; Le, D.T.; Nishiyama, R.; Watanabe, Y.; Sulieman, S.; Tran, U.T.; Mochida, K.; van Dong, N.; Yamaguchi-Shinozaki, K.; Shinozaki, K. The auxin response factor transcription factor family in soybean: Genome-wide identification and expression analyses during development and water stress. DNA Res. 2013, 20, 511-524.
38. Hossain, Z.; Khatoon, A.; Komatsu, S. Soybean proteomics for unraveling abiotic stress response mechanism. J. Proteome Res. 2013, 12, 4670-4684.
39. Wang, Z.; Libault, M.; Joshi, T.; Valliyodan, B.; Nguyen, H.; Xu, D.; Stacey, G.; Cheng, J. Soydb: A knowledge database of soybean transcription factors. BMC Plant Biol. 2010, 10, 14.
40. Schmutz, J.; Cannon, S.B.; Schlueter, J.; Ma, J.; Mitros, T.; Nelson, W.; Hyten, D.L.; Song, Q.; Thelen, J.J.; Cheng, J. Genome sequence of the palaeopolyploid soybean. Nature 2010, 463, 178-183.
41. Meng, Q.; Zhang, C.; Gai, J.; Yu, D. Molecular cloning, sequence characterization and tissue-specific expression of six NAC-like genes in soybean (Glycine max (L.) Merr.). J. Plant Physiol. 2007, 164, 1002-1012.
42. Pinheiro, G.L.; Marques, C.S.; Costa, M.D.B.L.; Reis, P.A.B.; Alves, M.S.; Carvalho, C.M.; Fietto, L.G.; Fontes, E.P.B. Complete inventory of soybean NAC transcription factors: Sequence conservation and expression analysis uncover their distinct roles in stress response. Gene 2009, 444, 10-23.
43. Le, D.T.; Nishiyama, R.; Watanabe, Y.; Mochida, K.; Yamaguchi-Shinozaki, K.; Shinozaki, K.; Tran, L.S.P. Genome-wide survey and expression analysis of the plant-specific NAC transcription factor family in soybean during development and dehydration stress. DNA Res. 2011, 18, 263-276.
44. Le, D.T.; Nishiyama, R.; Watanabe, Y.; Tanaka, M.; Seki, M.; Yamaguchi-Shinozaki, K.; Shinozaki, K.; Tran, L.-S.P. Differential gene expression in soybean leaf tissues at late developmental stages under drought stress revealed by genome-wide transcriptome analysis. PLoS One 2012, 7, e49522.
45. Manavalan, L.P.; Guttikonda, S.K.; Tran, L.S.P.; Nguyen, H.T. Physiological and molecular approaches to improve drought resistance in soybean. Plant Cell Physiol. 2009, 50, 1260-1276.
46. Gowda, V.R.; Henry, A.; Yamauchi, A.; Shashidhar, H.; Serraj, R. Root biology and genetic improvement for drought avoidance in rice. Field Crop. Res. 2011, 122, 1-13.
47. Abd Allah, A.; Shimaa, A.; Zayed, B.; Gohary, A.E. The role of root system traits in the drought tolerance of rice (Oryza sativa L.). Int. J. Agric. Biol. Sci. 2010, 1, 83-87.
48. Guo, P.; Baum, M.; Grando, S.; Ceccarelli, S.; Bai, G.; Li, R.; von Korff, M.; Varshney, R.K.; Graner, A.; Valkoun, J. Differentially expressed genes between drought-tolerant and drought-sensitive barley genotypes in response to drought stress during the reproductive stage. J. Exp. Bot. 2009, 60, 3531-3544.
49. Kasuga, M.; Liu, Q.; Miura, S.; Yamaguchi-Shinozaki, K.; Shinozaki, K. Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat. Biotechnol. 1999, 17, 287-291.
50. Rivero, R.M.; Kojima, M.; Gepstein, A.; Sakakibara, H.; Mittler, R.; Gepstein, S.; Blumwald, E. Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proc. Natl. Acad. Sci. USA 2007, 104, 19631-19636.
51. Yamaguchi-Shinozaki, K.; Shinozaki, K. Organization of cis-acting regulatory elements in osmotic-and cold-stress-responsive promoters. Trends Plant Sci. 2005, 10, 88-94.
52. Behnam, B.; Iuchi, S.; Fujita, M.; Fujita, Y.; Takasaki, H.; Osakabe, Y.; Yamaguchi-Shinozaki, K.; Kobayashi, M.; Shinozaki, K. Characterization of the promoter region of an Arabidopsis gene for 9-cis-epoxycarotenoid dioxygenase involved in dehydration-inducible transcription. DNA Res. 2013, 20, 315-324.
53. Ramya, M.; Raveendran, M.; Ramalingam, S.J. In silico analysis of drought tolerant genes in rice. Int. J. Biol. Med. Res. 2010, 3, 110-114.
54. Maruyama, K.; Todaka, D.; Mizoi, J.; Yoshida, T.; Kidokoro, S.; Matsukura, S.; Takasaki, H.; Sakurai, T.; Yamamoto, Y.Y.; Yoshiwara, K. Identification of cis-acting promoter elements in cold-and dehydration-induced transcriptional pathways in Arabidopsis, rice, and soybean. DNA Res. 2012, 19, 37-49.
55. Tran, L.S.P.; Nakashima, K.; Sakuma, Y.; Osakabe, Y.; Qin, F.; Simpson, S.D.; Maruyama, K.; Fujita, Y.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Co-expression of the stress-inducible zinc finger homeodomain ZFHD1 and NAC transcription factors enhances expression of the ERD1 gene in Arabidopsis. Plant J. 2007, 49, 46-63.
56. Thu, N.B. A; Nguyen, Q. T; Hoang, X.L. T; Thao, N. P; Tran, L.S.P. Evaluation of drought tolerance of the Vietnamese soybean cultivars provides potential resources for soybean production and genetic engineering. Unpublished Observation, 2013.
57. Le, D.T.; Aldrich, D.L.; Valliyodan, B.; Watanabe, Y.; van Ha, C.; Nishiyama, R.; Guttikonda, S.K.; Quach, T.N.; Gutierrez-Gonzalez, J.J.; Tran, L.-S.P. Evaluation of candidate reference genes for normalization of quantitative RT-PCR in soybean tissues under various abiotic stress conditions. PLoS One 2012, 7, e46487.
58. Le, D.T.; Nishiyama, R.; Watanabe, Y.; Mochida, K.; Yamaguchi-Shinozaki, K.; Shinozaki, K.; Tran, L.S.P. Genome-wide expression profiling of soybean two-component system genes in soybean root and shoot tissues under dehydration stress. DNA Res. 2011, 18, 17-29.