Correlation between differential drought tolerability of two contrasting drought-responsive chickpea cultivars and differential expression of a subset of CaNAC genes under normal and dehydration conditions

Frontiers in Plant Science

Volumn 6, Issue JUNE, 2015, Pages 1-12

  Nguyen, Kien Huu ^a,b   Van Ha, Chien ^a,b   Watanabe, Yasuko ^a   Tran, Uyen Thi ^a   Esfahani, Maryam Nasr ^c   Van Nguyen, Dong ^b   Tran, Lam Son Phan ^a  

^a RIKEN Center for Sustainable Resource Science   (Japan)

^b Institute of Agricultural Genetic   (Viet Nam)

^c LORESTAN UNIVERSITY   (Iran)

Author keywords

Chickpea; Differential drought tolerability; Differential expression; NAC transcription factors; RT qPCR

Indexed keywords

CICER ARIETINUM;

EID: 84934998825     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00449     Document Type: Article

References (51)

1. Albacete, A. A., Martinez-Andujar, C., and Perez-Alfocea, F. (2014). Hormonal and metabolic regulation of source-sink relations under salinity and drought: from plant survival to crop yield stability. Biotechnol. Adv. 32, 12–30. doi: 10.1016/j.biotechadv.2013.10.005
2. Bampidis, V. A., and Christodoulou, V. (2011). Chickpeas (Cicer arietinum L.) in animal nutrition: a review. Anim. Feed Sci. Technol. 168, 1–20. doi: 10.1016/j.anifeedsci.2011.04.098
3. Garg, R., Sahoo, A., Tyagi, A. K., and Jain, M. (2010). Validation of internal control genes for quantitative gene expression studies in chickpea (Cicer arietinum L.). Biochem. Biophys. Res. Commun. 396, 283–288. doi: 10.1016/j.bbrc.2010.04.079
4. Guttikonda, S. K., Valliyodan, B., Neelakandan, A. K., Tran, L. S., Kumar, R., Quach, T. N., et al. (2014). Overexpression of AtDREB1D transcription factor improves drought tolerance in soybean. Mol. Biol. Rep. 41, 7995–8008. doi: 10.1007/s11033-014-3695-3
5. Ha, C. V., Le, D. T., Nishiyama, R., Watanabe, Y., Tran, U. T., Dong, N. V., et al. (2013). Characterization of the newly developed soybean cultivar DT2008 in relation to the model variety W82 reveals a new genetic resource for comparative and functional genomics for improved drought tolerance. Biomed. Res. Int. 2013, 1–8. doi: 10.1155/2013/759657
6. Ha, C. V., Leyva-Gonzalez, M. A., Osakabe, Y., Tran, U. T., Nishiyama, R., Watanabe, Y., et al. (2014). Positive regulatory role of strigolactone in plant responses to drought and salt stress. Proc. Natl. Acad. Sci. U.S.A. 111, 851–856. doi: 10.1073/pnas.1322135111
7. Hadiarto, T., and Tran, L. S. (2011). Progress studies of drought-responsive genes in rice. Plant Cell Rep. 30, 297–310. doi: 10.1007/s00299-010-0956-z
8. Hu, H., Dai, M., Yao, J., Xiao, B., Li, X., Zhang, Q., et al. (2006). Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc. Natl. Acad. Sci. U.S.A. 103, 12987–12992. doi: 10.1073/pnas.0604882103
9. Jain, D., and Chattopadhyay, D. (2010). Analysis of gene experession in response to water deficit of chickpea (Cicer arietinum L.) varieties differing in drought tolerance. BMC Plant Biol. 10:24. doi: 10.1186/1471-2229-10-24
10. Jain, M., Misra, G., Patel, R. K., Priya, P., Jhanwar, S., Khan, A. W., et al. (2013). A draft genome sequence of the pulse crop chickpea (Cicer arietinum L.). Plant J. 74, 715–729. doi: 10.1111/tpj.12173
11. Jogaiah, S., Govind, S. R., and Tran, L. S. (2013). Systems biology-based approaches toward understanding drought tolerance in food crops. Crit. Rev. Biotechnol. 33, 23–39. doi: 10.3109/07388551.2012.659174
12. Jukantil, A. K., Gaur, P. M., Gowda, C. L. L., and Chibbar, R. N. (2012). Nutritional quality and health benefits of chickpea (Cicer arietinum L.): a review. Br. J. Nutr. 108, 11–26. doi: 10.1017/S0007114512000797
13. Kaiser, H. (2009). The relation between stomatal aperture and gas exchange under consideration of pore geometry and diffusional resistance in the mesophyll. Plant Cell Environ. 32, 1091–1098. doi: 10.1111/j.1365-3040.2009.01990.x
14. Le, D. T., Aldrich, D. L., Valliyodan, B., Watanabe, Y., Van Ha, C., Nishiyama, R., et al. (2012). Evaluation of candidate reference genes for normalization of quantitative RT-PCR in soybean tissues under various abiotic stress conditions. PLoS ONE 7:e46487. doi: 10.1371/journal.pone.0046487
15. Le, D. T., Nishiyama, R., Watanabe, Y., Mochida, K., Yamaguchi-Shinozaki, K., Shinozaki, K., et al. (2011a). Genome-wide expression profiling of soybean two-component system genes in soybean root and shoot tissues under dehydration stress. DNA Res. 18, 17–29. doi: 10.1093/dnares/dsq032
16. Le, D. T., Nishiyama, R., Watanabe, Y., Mochida, K., Yamaguchi-Shinozaki, K., Shinozaki, K., et al. (2011b). 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. doi: 10.1093/dnares/dsr015
17. Manavalan, L. P., Guttikonda, S. K., Tran, L.-S. P., and Nguyen, H. T. (2009). Physiological and molecular approaches to improve drought resistance in soybean. Plant Cell Physiol. 50, 1260–1276. doi: 10.1093/pcp/pcp082
18. Molina, C., Rotter, B., Horres, R., Udupa, S. M., Besser, B., Bellarmino, L., et al. (2008). SuperSAGE: the drought stress-responsive transcriptome of chickpea roots. BMC Genomics 9:553. doi: 10.1186/1471-2164-9-553
19. Nakashima, K., Takasaki, H., Mizoi, J., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2012). NAC transcription factors in plant abiotic stress responses. Biochim. Biophys. Acta 1819, 97–103. doi: 10.1016/j.bbagrm.2011.10.005
20. Nakashima, K., Tran, L. S., Van Nguyen, D., Fujita, M., Maruyama, K., Todaka, D., et al. (2007). Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J. 51, 617–630. doi: 10.1111/j.1365-313X.2007.03168.x
21. Nasr Esfahani, M., Sulieman, S., Schulze, J., Yamaguchi-Shinozaki, K., Shinozaki, K., and Tran, L. S. (2014). Mechanisms of physiological adjustment of N2 fixation in Cicer arietinum L. (chickpea) during early stages of water deficit: single or multi-factor controls. Plant J. 79, 964–980. doi: 10.1111/tpj.12599
22. Ngwe, T., Nukui, Y., Oyaizu, S., Takamoto, G., Koike, S., Ueda, K., et al. (2012). Bean husks as a supplemental fiber for ruminants: potential use for activation of fibrolytic rumen bacteria to improve main forage digestion. Anim. Sci. J. 83, 43–49. doi: 10.1111/j.1740-0929.2011.00916.x
23. Ni, F. T., Chu, L. Y., Shao, H. B., and Liu, Z. H. (2009). Gene expression and regulation of higher plants under soil water stress. Curr. Genomics 10, 269–280. doi: 10.2174/138920209788488535
24. Nishiyama, R., Watanabe, Y., Fujita, Y., Le, D. T., Kojima, M., Werner, T., 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. doi: 10.1105/tpc.111.087395
25. Olsen, A. N., Ernst, H. A., Leggio, L. L., and Skriver, K. (2005). NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci. 10, 79–87. doi: 10.1016/j.tplants.2004.12.010
26. Osakabe, Y., Yamaguchi-Shinozaki, K., Shinozaki, K., and Tran, L.-S. P. (2013). Sensing the environment: key roles of membrane-localized kinases in plant perception and response to abiotic stress. J. Exp. Bot. 64, 445–458. doi: 10.1093/jxb/ers354
27. Puranik, S., Sahu, P. P., Srivastava, P. S., and Prasad, M. (2012). NAC proteins: regulation and role in stress tolerance. Trends Plant Sci. 17, 369–381. doi: 10.1016/j.tplants.2012.02.004
28. Rozrokh, M., Sabaghpour, S. H., and Armin, M. (2013). Determining the best indices of drought tolerance in chickpea genotypes. Plant Ecophysiol. 4, 25–36.
29. Rozrokh, M., Sabaghpour, S. H., Armin, M., and Asgharipour, M. (2012). The effects of drought stress on some biochemical traits in twenty genotypes of chickpea. Eur. J. Exp. Biol. 2, 1980–1987.
30. Rubio, L. A. (2005). Ileal digestibility of defatted soybean, lupin and chickpea seed meals in cannulated Iberian pigs: I. Proteins. J. Sci. Food Agric. 85, 1313–1321. doi: 10.1002/Jsfa.1963
31. Sabaghpour, S. H., Malhotra, R. S., and Banai, T. (2005). Registration of ‘Hashem’ Kabuli chickpea. Crop Sci. 45:2651. doi: 10.2135/cropsci2004.0772
32. Shanker, A. K., Maheswari, M., Yadav, S. K., Desai, S., Bhanu, D., Attal, N. B., et al. (2014). Drought stress responses in crops. Funct. Integr. Genomics 14, 11–22. doi: 10.1007/s10142-013-0356-x
33. Shao, H. B., Chu, L. Y., Jaleel, C. A., Manivannan, P., Panneerselvam, R., and Shao, M. A. (2009). Understanding water deficit stress-induced changes in the basic metabolism of higher plants – biotechnologically and sustainably improving agriculture and the ecoenvironment in arid regions of the globe. Crit. Rev. Biotechnol. 29, 131–151. doi: 10.1080/07388550902869792
34. Shao, H. B., Chu, L. Y., Shao, M. A., Jaleel, C. A., and Mi, H. M. (2008). Higher plant antioxidants and redox signaling under environmental stresses. C. R. Biol. 331, 433–441. doi: 10.1016/j.crvi.2008.03.011
35. Sharp, R. E., Poroyko, V., Hejlek, L. G., Spollen, W. G., Springer, G. K., Bohnert, H. J., et al. (2004). Root growth maintenance during water deficits: physiology to functional genomics. J. Exp. Bot. 55, 2343–2351. doi: 10.1093/jxb/erh276
36. Singh, K. B., Malhotra, R. S., and Saxena, M. C. (1992). Registration of ‘ILC 482’ chickpea. Crop Sci. 32:826. doi: 10.2135/cropsci1992.0011183X003200030051x
37. Stolf-Moreira, R., Lemos, E. G. M., Carareto-Alves, L., Marcondes, J., Pereira, S. S., Rolla, A. A. P., et al. (2011). Transcriptional profiles of roots of different soybean genotypes subjected to drought stress. Plant Mol. Biol. Rep. 29, 19–34. doi: 10.1007/s11105-010-0203-3
38. Thao, N. P., Thu, N. B., Hoang, X. L., Van Ha, C., and Tran, L. S. (2013). Differential expression analysis of a subset of drought-responsive GmNAC genes in two soybean cultivars differing in drought tolerance. Int. J. Mol. Sci. 14, 23828–23841. doi: 10.3390/ijms141223828
39. Thu, N. B., Hoang, X. L., Doan, H., Nguyen, T. H., Bui, D., Thao, N. P., et al. (2014a). Differential expression analysis of a subset of GmNAC genes in shoots of two contrasting drought-responsive soybean cultivars DT51 and MTD720 under normal and drought conditions. Mol. Biol. Rep. 41, 5563–5569. doi: 10.1007/s11033-014-3507-9
40. Thu, N. B., Hoang, X. L., Nguyen, T. D. H., Thao, N. P., and Tran, L. S. (2014b). Differential expression of two-component system-related drought-responsive genes in two contrasting drought-tolerant soybean cultivars DT51 and MTD720 under well-watered and drought conditions. Plant Mol. Biol. Rep. doi:10.1007/s11105-014-0825-y
41. Thu, N. B., Nguyen, Q. T., Hoang, X. L., Thao, N. P., and Tran, L. S. (2014c). Evaluation of drought tolerance of the Vietnamese soybean cultivars provides potential resources for soybean production and genetic engineering. Biomed. Res. Int. 2014:809736. doi: 10.1155/2014/809736
42. Tran, L. S., Nakashima, K., Sakuma, Y., Simpson, S. D., Fujita, Y., Maruyama, K., 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. doi: 10.1105/tpc.104.022699
43. Tran, L. S., Nakashima, K., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2007). Plant gene networks in osmotic stress response: from genes to regulatory networks. Methods Enzymol. 428, 109–128. doi: 10.1016/S0076-6879(07)28006-1
44. Tran, L. S., Nishiyama, R., Yamaguchi-Shinozaki, K., and Shinozaki, K. (2010). Potential utilization of NAC transcription factors to enhance abiotic stress tolerance in plants by biotechnological approach. GM Crops 1, 32–39. doi: 10.4161/gmcr.1.1.10569
45. Tran, L. S., Quach, T. N., Guttikonda, S. K., Aldrich, D. L., Kumar, R., Neelakandan, A., et al. (2009). Molecular characterization of stress-inducible GmNAC genes in soybean. Mol. Genet. Genomics 281, 647–664. doi: 10.1007/s00438-009-0436-8
46. Varshney, R. K., Song, C., Saxena, R. K., Azam, S., Yu, S., Sharpe, A. G., et al. (2013). Draft genome sequence of chickpea (Cicer arietinum) provides a resource for trait improvement. Nat. Biotechnol. 31, 240–246. doi: 10.1038/nbt.2491
47. Xue, G. P., Way, H. M., Richardson, T., Drenth, J., Joyce, P. A., and Mcintyre, C. L. (2011). Overexpression of Ta N A C 6 9 leads to enhanced transcript levels of stress up-regulated genes and dehydration tolerance in bread wheat. Mol. Plant 4, 697–712. doi: 10.1093/mp/ssr013
48. Yamaguchi-Shinozaki, K., and Shinozaki, K. (2006). Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu. Rev. Plant Biol. 57, 781–803. doi: 10.1146/annurev.arplant.57.032905.105444
49. Yang, X., Wang, X., Ji, L., Yi, Z., Fu, C., Ran, J., et al. (2015). Overexpression of a Miscanthus lutarioriparius NAC gene MlNAC5 confers enhanced drought and cold tolerance in Arabidopsis. Plant Cell Rep. 34, 943–958. doi: 10.1007/s00299-015-1756-2
50. Zheng, X., Chen, B., Lu, G., and Han, B. (2009). Overexpression of a NAC transcription factor enhances rice drought and salt tolerance. Biochem. Biophys. Res. Commun. 379, 985–989. doi: 10.1016/j.bbrc.2008.12.163
51. Zhu, M., Chen, G., Zhang, J., Zhang, Y., Xie, Q., Zhao, Z., et al. (2014). The abiotic stress-responsive NAC-type transcription factor SlNAC4 regulates salt and drought tolerance and stress-related genes in tomato (Solanum lycopersicum). Plant Cell Rep. 33, 1851–1863. doi: 10.1007/s00299-014-1662-z