Journal of Plant Biotechnology

The Korean Society of Plant Biotechnology (한국식물생명공학회)
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Drought and salinity stress response in wheat: physiological and TaNAC gene expression analysis in contrasting Egyptian wheat genotypes

  • El-Moneim, D. Abd (Department of Plant Production (Genetic branch), Faculty of Agricultural and Environmental sciences, Arish University) ;
  • Alqahtani, Mesfer M. (Department of Biological Sciences, Faculty of Science and Humanities, Shaqra University) ;
  • Abdein, Mohamed A. (Biology Department, Faculty of Arts and Science, Northern Border University) ;
  • Germoush, Mousa O. (Biology Department, College of Science, Jouf University)
  • Received : 2019.12.16
  • Accepted : 2020.01.27
  • Published : 2020.03.31
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Abstract

Drought and salinity are significant stressors for crop plants, including wheat. The relationship between physiological mechanisms and gene expression is important for stress tolerance. NAC transcription factors (TFs) play vital roles in abiotic stress. In this study, we assessed the expression of four TaNAC genes with some physiological traits of nine Egyptian wheat genotypes under different concentrations of PEG and NaCl. All the physiological traits that we assessed declined under both stress conditions in all genotypes. In addition, all the genes that we measured were induced under both stress conditions in young leaves. Shandaweel 1, Bani Seuf 7, Sakha 95, and Misr 2 genotypes showed higher gene expression and were linked with a better genotypic performance in physiological traits under both stress conditions. In addition, we found an association between the expression of NAC genes and physiological traits. Overall, NAC genes may act as beneficial markers for selecting for genotypic tolerance to these stress conditions in wheat.

Keywords

References

  1. Abbas Z K, Mobin M (2015) Comparative growth and physiological responses of two wheat (Triticum aestivum L.) cultivars differing in salt tolerance to salinity and cyclic drought stress. Archives of Agronomy and Soil Science, DOI: 10.1080/03650340.2015.108355
  2. Agarwal PK, and Jha B (2010) Transcription factors in plants and ABA dependent and independent abiotic stress signaling. Biol. Plant. 54:201-212. doi: 10.1007/s10535-010-0038-7
  3. Aida M, Ishida T, Fukaki H, Fujisawa H and Tasaka M (1997) Genes involved in organ separation in Arabidopsis: an analysis of the cupshaped cotyledon mutant. Plant Cell 9:841-857. https://doi.org/10.1105/tpc.9.6.841
  4. Aida M, Ishida T, and Tasaka M (1999) Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: interaction among the CUP-SHAPED COTYLEDON and SHOOT MERISTEMLESS genes. Development 126:1563-1570 https://doi.org/10.1242/dev.126.8.1563
  5. Anjum SA, Jian-hang N, Ran W, Jin-huan L, Mei-ru L, Ji-xuan S, Jun L, Zohaib A, San-gen W, Xue-feng Z (2016) Regulation mechanism of exogenous 5-aminolevulinic acid on growth and physiological characters of Leymus chinensis (Trin.) under high temperature stress. The Philippine Agricultural Scientist 99(3):253-259
  6. Bayoumi TY, Eid MH and Metwali EM (2008) Application of physiological and biochemical indices as a screening technique for drought tolerance in wheat genotypes. African J. Biotechnol 7:2341-2352
  7. Baloglu MC, Oz MT, Oktem HA, Yucel M (2012) Expression analysis of TaNAC69-1 and TtNAMB-2, wheat NAC family transcription factor genes under abiotic stress conditions in durum wheat (Triticum turgidum). Plant Mol Biol Rep 30:1246-1252 https://doi.org/10.1007/s11105-012-0445-3
  8. Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: Regulation mechanisms from whole plant to cell. Annals of Botany 103:551-560 https://doi.org/10.1093/aob/mcn125
  9. Christianson JA, Wilson IW, Llewellyn DJ, Dennis ES (2009) The low-oxygen induced NAC domain transcription factor ANAC102 affects viability of Arabidopsis seeds following low-oxygen treatment. Plant Physiol 149:1724-1738 https://doi.org/10.1104/pp.108.131912
  10. Dalirie, MS, Sharif, RS, Farzaneh, S (2010) Evaluation of yield, dry matter accumulation and leaf area index in wheat genotypes as affected by terminal drought stress. Not. Bot. Horti Agrobotanici Cluj-Napoca 38(1):182-186
  11. Dencic S, Kastori R, Kobiljski B, and Duggan B (2000) Evaluation of grain yield and its components in wheat cultivars and landraces under near optimal and drought conditions, Euphytica 113(1):43-52 https://doi.org/10.1023/A:1003997700865
  12. Eftekhari A, Baghizadeh A, Yaghoobi MM and Abdolshahi R (2017) Differences in the drought stress response of DREB2 and CAT1 genes and evaluation of related physiological parameters in some bread wheat cultivars, Biotechnology & Biotechnological Equipment, 31(4):709-716, DOI: 10.1080/13102818.2017.1316214
  13. El-Hendawy SE, Ruan Y, Hu YC, Schmidhalter U (2009) A comparison of screening criteria for salt tolerance in wheat under field and environment controlled conditions. J Agron Crop Sci 195:356-367 https://doi.org/10.1111/j.1439-037X.2009.00372.x
  14. Farooq S and Azam F (2006) The Use of Cell Membrane Stability (CMS) Technique to Screen for Salt Tolerant Wheat Varieties. J. Plant Physiol 163:629-637 https://doi.org/10.1016/j.jplph.2005.06.006
  15. Franco JA, Fernandez JA, Banon S and Gonzalez A (1997) Relationship between the effects of salinity on seedling growth and yield of six muskmelon cultivars. Hort Science 32, 642-644 https://doi.org/10.21273/HORTSCI.32.4.642
  16. Fujita M, Fujita Y, Maruyama K, Seki M, Hiratsu K, Ohme-Takagi M, Tran L SP, Yamaguchi-Shinozaki K, and Shinozaki K (2004) A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant J. 39:863-876 https://doi.org/10.1111/j.1365-313X.2004.02171.x
  17. Ghaderi N, Normohammadi S, Javadi T (2015) Morpho-physiological Responses of Strawberry (Fragaria${\times}$ananassa) to Exogenous Salicylic Acid Application under Drought Stress. J. Agr. Sci. Tech. 17:167-178167
  18. Ghogdi EA, Darbandi AI and Borzouei A (2012) Effects of salinity on some physiological traits in wheat (Triticum aestivum L.) cultivars. Ind. J. Sci. Technol 5(1):1906-1906
  19. Jeong JS, Kim YS, Baek KH, Jung H, Ha SH, Do Choi Y, et al. (2010) Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiol 153(1):185-97 https://doi.org/10.1104/pp.110.154773
  20. Jeong JS, Kim YS, Redillas MC, Jang G, Jung H, Bang SW, et al. (2013) OsNAC5 overexpression enlarges root diameter in rice plants leading to enhanced drought tolerance and increased grain yield in the field. Plant Biotechnol. J. 11(1):101-14 https://doi.org/10.1111/pbi.12011
  21. Hamama KA, Negim O (2014) Evaluation of wheat genotypes and some soil properties under saline water irrigation. Annals of Agricultural Science 59(2):165-176 https://doi.org/10.1016/j.aoas.2014.11.002
  22. Hao Y, Wei W, Song Q, Chen H, Zhang Y, et al. (2011) Soybean NAC transcription factors promote abiotic stress tolerance and lateral root formation in transgenic plants. Plant J. 68:302-313 https://doi.org/10.1111/j.1365-313X.2011.04687.x
  23. He, XJ, Mu RL, Cao WH, Zhang ZG, Zhang JS, and Chen, SY (2005) AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. Plant J. 44:903-916 https://doi.org/10.1111/j.1365-313X.2005.02575.x
  24. Hu, H, Dai M, Yao J, Xiao B, Li X, Zhang Q, and Xiong L (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 https://doi.org/10.1073/pnas.0604882103
  25. Hu H, You J, Fang Y, Zhu X, Qi Z, and Xiong L (2008) Characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice. Plant Mol. Biol. 67:169-181 https://doi.org/10.1007/s11103-008-9309-5
  26. Hu Y, Schmidhalter U (2000) Reduced cellular cross-sectional area in the leaf elongation zone of wheat causes a decrease in dry weight deposition under saline conditions. Aust. J. Plant Physiol. 28:165-170
  27. Hu Y, Schmidhalter U (2001) Effects of salinity and macronutrient levels on micronutrients in wheat. J. Plant Nutr. 24:273-281 https://doi.org/10.1081/PLN-100001387
  28. Hu Y, Camp KH, Schmidhalter U (2000) Kinetics and spatial distribution of leaf elongation of wheat (Triticum aestivum L.) under saline soil conditions. Int J Plant Sci. 161:575-582 https://doi.org/10.1086/314280
  29. Huang Q, Yan W, Bin L, Junli C, Mingjie C, Kexiu L, Guangxiao Y and Guangyuan H (2015) TaNAC29, a NAC transcription factor from wheat, enhances salt and drought tolerance in transgenic Arabidopsis. BMC Plant Biology. 15:268. DOI 10.1186/s12870-015-0644-9
  30. Kamoshita A, Wade LJ, Yamauchi A (2000) Genotypic variation in response of rainfed lowland rice to drought and rewatering. III. Water extraction during drought period. Plant Production Science 3:189-196 https://doi.org/10.1626/pps.3.189
  31. Keyvan S (2010) The effects of drought stress on yield, relative water content, proline, soluble carbohydrates and chlorophyll of bread wheat cultivars. J Anim Plant Sci. 8:1051-1060
  32. Kim SY, Kim SG, Kim YS, Seo PJ, Bae M, Yoon HK, Park CM (2007) Exploring membrane-associated NAC transcription factors in Arabidopsis: implications for membrane biology in genome regulation. Nucleic Acids Res 35:203-213 https://doi.org/10.1093/nar/gkl1068
  33. 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(4):402-408 https://doi.org/10.1006/meth.2001.1262
  34. Lonbani M and Arzani A (2011) Morpho-physiological traits associated with terminal drought stress tolerance in triticale and wheat. Agronomy Research 9(1-2):315-329
  35. Lu M, Sheng Y. Deng-Feng Z. Yun-Su S. Yan-Chun S. Tian-Yu W.Yu L (2012) A maize stress-responsive NAC transcription factor, ZmSNAC1, confers enhanced tolerance to dehydration in transgenic Arabidopsis. Plant Cell Rep 31:1701-1711 https://doi.org/10.1007/s00299-012-1284-2
  36. Meng C, Cai C, Zhang T, Guo W (2009) Characterization of six novel NAC genes and their responses to abiotic stresses in Gossypium hirsutum L. Plant Sci 176:352-359 https://doi.org/10.1016/j.plantsci.2008.12.003
  37. Mao X, Zhang H, Qian X, Li A, Zhao G, Jing R (2012) TaNAC2, a NAC-type wheat transcription factor conferring enhanced multiple abiotic stress tolerances in Arabidopsis. J Exp Bot. 63(8):2933-46 https://doi.org/10.1093/jxb/err462
  38. Mao X, Chen S, Li A, Zhai C, Jing R (2014) Novel NAC transcription factor TaNAC67 confers enhanced multi-abiotic stress tolerances in Arabidopsis. PLoS ONE. 9(1):e84359 https://doi.org/10.1371/journal.pone.0084359
  39. Moumeni A, Satoh K, Kondoh H, Asano T, Hosaka A, Venuprasa R, Serraj R, Kumar A, Leung H, Kikuchi S (2011) Comparative analysis of root transcriptome profiles of two pairs of drought tolerant and susceptible rice near-isogenic lines under different drought stress. BMC Plant Biol 11:174 https://doi.org/10.1186/1471-2229-11-174
  40. Mickky BM, Aldesuquy HS (2017) Impact of osmotic stress on seedling growth observations, membrane characteristics and antioxidant defense system of different wheat genotypes. Egyptian Journal of Basic and Applied Sciences, 4:1, 47-54, DOI: 10.1016/j.ejbas.2016.10.001
  41. Mitsuda N, Iwase A, Yamamoto H, Yoshida M, Seki M, Shinozaki K, Ohme-Takagi M (2007) NAC transcription factors, NST1 and NST3 are key regulators of the formation of secondary walls in woody tissues of Arabidopsis. Plant Cell 19:270-280 https://doi.org/10.1105/tpc.106.047043
  42. Nayer M K, R Heidari, N Abbaspour and F Rahmani (2012) Growth responses and aquaporin expression in grape genotypes under salinity. Iranian Journal of Plant Physiology 2(4):497-507
  43. Nakashima, K, Tran L-SP, Van Nguyen, D, Fujita M, Maruyama K, Todaka D, Ito Y, Hayashi N, Shinozaki K, and Yamaguchi-Shinozaki K (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 https://doi.org/10.1111/j.1365-313X.2007.03168.x
  44. Nakashima K, Takasaki H, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2011) NAC transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819:97-103
  45. Nakashima K, Takasaki H, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) NAC transcription factors in plant abiotic stress responses. Biochim Biophys Acta. 1819(2):97-103 https://doi.org/10.1016/j.bbagrm.2011.10.005
  46. Neumann PM (1993) Rapid and reversible modifications of extension capacity of cell walls in elongating maize leaf tissues responding to root addition and removal of NaCl. Plant Cell Environ. 16:1107-1114 https://doi.org/10.1111/j.1365-3040.1996.tb02068.x
  47. Niaz A, Amin R, Ali D (2014) GSTF1 Gene Expression Analysis in Cultivated Wheat Plants under Salinity and ABA Treatments. Molecular Biology Research Communications 3(1):9-19
  48. Nuruzzaman M, Manimekalai R, Sharoni AM, Satoh K, Kondoh H, Ooka H, et al (2010) Genome-wide analysis of NAC transcription factor family in rice. Gene 465:30-44. doi: 10.1016/j.gene.2010.06.008
  49. Ouhaddach M, H ElYacoubi, A Douaik, A Rochdi (2018) Morpho-Physiological and Biochemical Responses to Salt Stress in Wheat (Triticum aestivum L.) at the Heading Stage J. Mater. Environ. Sci. 9(6):1899-1907
  50. Ozhuner E, Eldem V, Ipek A, Okay S, Sakcali S, et al. (2013) Boron stress responsive microRNAs and their targets in barley. PLoS One 8:e59543 https://doi.org/10.1371/journal.pone.0059543
  51. Pandurangaiah M, Lokanadha R G, Sudhakarbabu O, Nareshkumar A, Kiranmai K, Lokesh U, Thapa G, Sudhakar C (2014) Overexpression of horsegram (Macrotyloma uniflorum Lam. Verdc.) NAC transcriptional factor (MuNAC4) in groundnut confers enhanced drought tolerance. Molecular Biotechnology 56:758-769 https://doi.org/10.1007/s12033-014-9754-0
  52. Passioura J B (1996) Drought and drought tolerance, "in Drought Tolerance in Higher Plants: Genetical, Physiological and Molecular Biological Analysis, E. Belhassen, Ed., pp. 3-12, Kluwer Academic, Dordrecht, The Netherlands
  53. Puranik S, Sahu PP, Srivastava PS, Prasad M (2012) NAC proteins: regulation and role in stress tolerance. Trends Plant Sci. 17(6):369-81 https://doi.org/10.1016/j.tplants.2012.02.004
  54. Quach TN, Tran L-SP, Valliyodan B, Nguyen HT, Kumar R, et al. (2014) Functional Analysis of Water Stress-Responsive Soybean GmNAC003 and GmNAC004 Transcription Factors in Lateral Root Development in Arabidopsis. PLoS ONE 9(1):e84886. doi: 10.1371/journal.pone.0084886
  55. Rizza F, Badeck FW, Cattivelli L, Lidestri O, di Fonzo N, and Stanca AM (2004) Use of a water stress index to identify barley genotypes adapted to rainfed and irrigated conditions. Crop Science 44(6):2127-2137 https://doi.org/10.2135/cropsci2004.2127
  56. Rucker KS, Kevin CK, Holbrook CC, and Hook JE (1995) Identification of peanut genotypes with improved drought avoidance traits. Peanut Science 22:14-18, 1995 https://doi.org/10.3146/pnut.22.1.0003
  57. Sairam, R. K., Rao, K. V. and Srivastava, G. C (2002) Differential Response of Wheat Genotypes to Long Term Salinity Stress in Relation to Oxidative Stress, Antioxidant Activity and Osmolyte Concentration. Plant Sci. 163:1037-1046 https://doi.org/10.1016/S0168-9452(02)00278-9
  58. Schonfeld MA, Johnson RC, Carwer BF, Mornhinweg DW (1988) Water relations in winter wheat as drought resistance indicators. Crop. Sci. 28: 526-531 https://doi.org/10.2135/cropsci1988.0011183X002800030021x
  59. Shao HB, Chu LY, Jaleel CA, and Zhao CX (2008) Water-deficit stress-induced anatomical changes in higher plants. Comptes Rendus 331(3):215-225 https://doi.org/10.1016/j.crvi.2008.01.002
  60. Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot. 58:221-227 https://doi.org/10.1093/jxb/erl164
  61. Souer, E, Van Houwelingen A, Kloos D, Mol J and Koes R (1996) 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 85, 159-170 https://doi.org/10.1016/S0092-8674(00)81093-4
  62. Sinclair TR and Ludlow MM (1985) Who taught plants thermo-dynamics? The unfulfilled potential of water potential. Aust. J. Plant Physiol. 12:213-217 https://doi.org/10.1071/PP9850213
  63. Tambussi EA, Nogues S, Araus JL (2005) Ear of durum wheat under water stress: water relations and photosynthetic metabolism. Planta. 221:446-458 https://doi.org/10.1007/s00425-004-1455-7
  64. Tang Y, Liu M, Gao S, Zhang Z, Zhao X, Zhao C, et al. (2012) Molecular characterization of novel TaNAC genes in wheat and overexpression of TaNAC2a confers drought tolerance in tobacco. Physiol Plant 144(3):210-24 https://doi.org/10.1111/j.1399-3054.2011.01539.x
  65. Teulat B, Zoumarou-Wallis N, Rotter B, Ben Salem M, Bahri H and This D (2003) QTL for relative water content in field-grown barley and their stability across Mediterranean environments. Theoretical and Applied Genetics 108:181-188 https://doi.org/10.1007/s00122-003-1417-7
  66. Tran LS, Quach TN, Guttikonda SK, Aldrich DL, Kumar R, Neelakandan A, Valliyodan B, Nguyen HT (2009) Molecular characterization of stress-inducible GmNAC genes in soybean. Mol Genet Genomics 281:647-664 https://doi.org/10.1007/s00438-009-0436-8
  67. Redillas MC, Jeong JS, Kim YS, Jung H, Bang SW, Choi YD, et al. (2012) The overexpression of OsNAC9 alters the root architecture of rice plants enhancing drought resistance and grain yield under field conditions. Plant Biotechnol J. 10(7):792-805 https://doi.org/10.1111/j.1467-7652.2012.00697.x
  68. Richards RA (1992) Increasing salinity tolerance of grain crops: is it worthwhile? Plant Soil 146:89-98 https://doi.org/10.1007/BF00012000
  69. Wang C, Deng P, Chen L, Wang X, Ma H, Hu W, et al. (2013) A Wheat WRKY Transcription Factor TaWRKY10 Confers Tolerance to Multiple Abiotic Stresses in Transgenic Tobacco. PLoS ONE 8(6):e65120 https://doi.org/10.1371/journal.pone.0065120
  70. Xia N, Zhang G, Sun Y, Zhu L, Xu L, et al. (2010a) TaNAC8, a novel NAC transcription factor gene in wheat, responds to stripe rust pathogen infection and abiotic stresses. Physiol Mol Plant Pathol 74:394-402 https://doi.org/10.1016/j.pmpp.2010.06.005
  71. Xia N, Zhang G, Liu X, Deng L, Cai G, et al. (2010b) Characterization of a novel wheat NAC transcription factor gene involved in defense response against stripe rust pathogen infection and abiotic stresses. Mol Biol Rep 37:3703-3712 https://doi.org/10.1007/s11033-010-0023-4
  72. Xue G, Neil IB, McIntyre CL, Riding GA, Kemal Kazan K, et al. (2006) TaNAC69 from the NAC superfamily of transcription factors is up-regulated by abiotic stresses in wheat and recognizes two consensus DNA-binding sequences. Funct Plant Biol 33:43-57 https://doi.org/10.1071/FP05161
  73. Xue G, Way H, Richardson T, Drenth J, Joyce P, et al. (2011) Overexpression of TaNAC69 leads to enhanced transcript levels of stress up-regulated genes and dehydration tolerance in bread wheat. Mol Plant 4:697-712 https://doi.org/10.1093/mp/ssr013
  74. Xue GP, Loveridge CW (2004) HvDRF1 is involved in abscisic acid-mediated gene regulation in barley and produces two forms of AP2 transcriptional activators, interacting preferably with a CT-rich element. Plant J 37:326-339 https://doi.org/10.1046/j.1365-313X.2003.01963.x
  75. Yamaguchi-Shinozaki K, Koizumi M, Urao S and Shinozaki K (1992) Molecular cloning and Characterization of 9 cDNAs for genes that are responsive to desiccation in Arabidopsis thaliana, sequence analysis of one cDNA clone that encodes a putative transmembrane channel protein. Plant Cell Physiol 33:217-224 https://doi.org/10.1093/oxfordjournals.pcp.a078243
  76. Yousfi S, Marquez AJ, Betti M, Araus JL, Serret MD (2016) Gene expression and physiological responses to salinity and water stress of contrasting durum wheat genotypes. J Integr Plant Biol. 2016 (1):48-66. doi: 10.1111/jipb.12359
  77. Zheng X, Chen B, Lu G, Han B (2009) Overexpression of a NAC transcription factor enhances rice drought and salt tolerance. Biochem Biophys Res Commun. 379(4):985-9 https://doi.org/10.1016/j.bbrc.2008.12.163
  78. Zhou QY, Tian AG, Zou HF, Xie ZM, Lei G, Huang J, Wang CM, Wang HW, Zhang JS, Chen SY (2008) Soybean WRKY-type transcription factor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants. Plant Biotechnol J 6:486-503 https://doi.org/10.1111/j.1467-7652.2008.00336.x