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2014 | 36 | 07 |

Tytuł artykułu

NAC transcription factor expression, amino acid concentration and growth of elite rice cultivars upon stress

Warianty tytułu

Języki publikacji



NAC transcription factors (TF) play important roles in regulating osmotic stress tolerance in plants. We tested the expression of 57 NAC genes in the presence of NaCl in young leaves of two elite rice cultivars, Cotaxtla and Tres Ríos, which display contrasting responses to salinity at the biochemical and physiological levels. Using qRT-PCR, the expression of 41 out of 57 NAC genes was validated, of which 23 showed regulation by NaCl. We identified two NAC genes (Os02g56600 and Os12g07790) induced in Cotaxtla, but repressed in Tres Ríos when plants were exposed to 100 mM NaCl in nutrient solution. In both elite cultivars, treated plants showed higher concentrations of total amino acids and proline in comparison to the controls; in all cases, Cotaxtla plants accumulated more free amino acids and proline than Tres Ríos plants. Furthermore, shoot growth was more affected in both cultivars, while root length was not reduced in treated plants in comparison to the controls. We conclude that both elite rice cultivars exhibit different expression patterns of NAC transcription factors as well as biochemical and physiological responses to salt stress, giving rise to better performance of Cotaxtla plants in comparison to Tres Ríos plants under our experimental conditions.

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Opis fizyczny



  • Colegio de Postgraduados, Campus Montecillo, Carretera Mexico-Texcoco km. 36.5, CP 56230 Montecillo, Estado de Mexico, Mexico
  • Colegio de Postgraduados, Campos Cordoba, Carretera Cordoba-Veracruz km. 348, CP 94961 Amatlan de los Reyes, Veracruz, Mexico
  • Colegio de Postgraduados, Campus Montecillo, Carretera Mexico-Texcoco km. 36.5, CP 56230 Montecillo, Estado de Mexico, Mexico


  • Ahmed CB, Rouina BB, Sensoy S, Boukhriss M, Abdullah FB (2010) Exogenous proline effects on photosynthetic performance and antioxidant defense system of young olive tree. J Agric Food Chem 58:4216–4222
  • Albacete A, Ghanem ME, Martínez-Andújar C, Acosta M, Sánchez-Bravo J, Martínez V, Lutts S, Dodd IC, Pérez-Alfocea F (2008) Hormonal changes in relation to biomass partitioning and shoot growth impairment in salized tomato (Solanum lycopersicum L.) plants. J Exp Bot 69:4118–4131
  • Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216
  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:2005–2007
  • Bernstein N, Kafkafi U (2002) Root growth under salinity stress. In: Weisel Y, Eshel A, Kafkafi U (eds) Plant root: the hidden half. Marcel Dekker, New York, pp 787–819
  • Bernstein N, Meiri A, Zilberstaine M (2004) Root growth of avocado is more sensitive to salinity than shoot growth. J Amer Hort Sci 129:188–192
  • Caldana C, Scheible WR, Mueller-Roeber B, Ruzicic S (2007) A quantitative RT-PCR platform for high-throughput expression profiling of 2500 rice transcription factors. Plant Meth 3(7). doi:10.1186/1746-4811-3-7
  • Cenci A, Guignon V, Roux N, Rouard M (2014) Genomic analysis of NAC transcription factors in banana (Musa acuminata) and definition of NAC orthologous groups for monocots and dicots. Plant Mol Biol 85(1–2):63–80. doi:10.1007/s11103-013-0169-2
  • Chang B, Yang L, Cong W, Zu Y, Tang Z (2014) The improved resistance to high salinity induced by trehalose is associated with ionic regulation and osmotic adjustment in Catharanthus roseus. Plant Physiol Biochem 77C:140–148. doi:10.1016/j.plaphy.2014.02.001
  • Chen X, Wang Y, Lv B, Li J, Luo L, Lu S, Zhang X, Ma H, Ming F (2014) The NAC family of transcription factor OSNAP confers abiotic stress response through the ABA pathway. Plant Cell Physiol. doi:10.1093/pcp/pct2014
  • Chiou TJ, Aung K, Lin SI, Wu CC, Chiang SF, Su CL (2006) Regulation of phosphate homeostasis by microRNA in Arabidopsis. Plant Cell 18:412–421
  • Czechowski T, Bari RP, Stitt M, Scheible WR, Udvardi M (2004) Real-time RT-PCR profiling of over 1400 Arabidopsis transcription factors: unprecedented sensitivity reveals novel rootand shoot-specific genes. Plant J 38:366–379
  • Díaz-Martín J, Almoguera C, Prieto-Dapena P, Espinosa JM, Jordano J (2005) Functional interaction between two transcription factors involved in the developmental regulation of a small heat stress protein gene promoter. Plant Physiol 139:1483–1494
  • Fang J, You J, Xie K, Xie W, Xiong L (2008) Systematic sequence analysis and identification of tissue-specific or stress-responsive genes of NAC transcription factor family in rice. Mol Genet Genomics 280:547–563. doi:10.1007/s00438-008-0386-6
  • Friedman M (2004) Applications of the ninhydrin reaction for analysis of amino acids, peptides, and proteins to agricultural biomedical sciences. J Amer Food Chem 52:385–406
  • García-Morales S, Trejo-Téllez LI, Gómez-Merino FC, Caldana C, Espinosa-Victoria D, Herrera-Cabrera E (2012) Growth, photosynthetic activity and potassium and sodium concentration in rice plants under salt stress. Acta Sci 34:317–324
  • Hameed M, Nawaz T, Ashraf M, Naz N, Batool R, Sajid M, Ahmad A, Riaz A (2013) Physioanatomical adaptations in response to salt stress in Sporobolus arabicus (Poaceae) from the Salt Range, Pakistan. Turk J Bot 37:715–724. doi:10.3906/bot-1208-1
  • Hamilton EW, Heckathorn SA (2001) Mitochondrial adaptation to NaCl. Complex I is protected by antioxidants and small heat shock proteins, whereas complex II is protected by proline and betaine. Plant Physiol 126:1266–1274
  • Hasanuzzaman M, Nahar K, Fujita M (2013) Plant response to salt stress and role of exogenous protectants to mitigate salt-induced damages. In: Ahmad P, Azooz MN, Prasad MNV (eds) Ecophysiology and responses of plant under salt stress. Springer, New York, pp 25–87
  • Hasegawa P, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499
  • Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments: a review. Plant Signal Behav 7:1–11
  • Hoque MA, Okuma E, Nakamara Y, Shimoishi Y, Murata Y (2008) Proline and glycine betaine enhance antioxidant defense and methylglyoxal detoxification systems and reduce NaCl induced damage in cultured tobacco cells. J Plant Physiol 165:813–824
  • Hu H, Dai M, Yao J, Xiao B, Li X, Zhang Q, Xiong L (2006) Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Nat Acad Sci USA 103:12987–12992. doi:10.1073/pnas.0604882103
  • Jeong JS, Kim YS, Baek KH, Jung H, Ha SH, Choi YD, Kim M, Reuzeau C, Kim JK (2010) Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiol 153:185–197
  • Khedr AHA, Abbas MA, Wahid AAA, Quick WP, Abogadallah GM (2003) Proline induces the expression of salt-stress-responsive proteins and may improve the adaptation of Pancratium maritimum L. to salt-stress. J Exp Bot 54:2553–2562
  • Le DT, Nishiyama R, Watanabe Y, Mochida K, Yamaguchi-Shinozaki K, Shinozaki K, Tran LSP (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
  • Liu G, Li X, Jin S, Liu X, Zhu L, Nie X, Zhang X (2014) Overexpression of rice NAC gene SNAC1 improves drought and salt tolerance by enhancing root development and reducing transpiration rate in transgenic cotton. PLoS One 9(1):e86895. doi:10.1371/journal.pone.0086895
  • 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 63:2933–2946
  • Mao X, Chen S, Li A, Zhai C, Jing R (2014) Novel NAC transcription factor TaNAC67 confers enhanced multi-abiotic stress tolerance in Arabidopsis. PLoS One 9(1):e84359. doi:10.1371/journal.pone.0084359
  • Matysik J, Alia, Bhalu B, Mohanty P (2002) Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. Curr Sci 82:525–532
  • Momayezi MR, Zaharah AR, Hanafi MM (2012) The effects of cation ratios on root lamella suberization in rice (Oryza sativa L.) with contrasting salt tolerance. Int J Agron. doi:10.1155/2012/76919
  • Moradi F, Ismail AM (2007) Responses of photosynthesis, chlorophyll fluorescence and ROS-scavenging systems to salt stress during seedling and reproductive stages in rice. Ann Bot 99:1161–1173
  • Munns R (2002) Salinity, growth and phytohormones. In: Lauchli A, Luttge U (eds) Salinity: environment—plants-molecules. Kluwer, Dordrecht, pp 271–290
  • Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167:645–663
  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681
  • Nakashima K, Tran LS, Van Nguyen D, Fujita M, Maruyama K, Todaka D, Ito Y, Hayashi N, Shinozaki K, 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
  • Nakashima K, Takasaki H, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) NAC transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819:97–103
  • Nounjan N, Nghia PT, Theerakulpisut P (2012) Exogenous proline and trehalose promote recovery of rice seedlings from salt-stress and differentially modulate antioxidant enzymes and expression of related genes. J Plant Physiol 169:59–604
  • Nuruzzaman M, Manimekalai R, Sharoni AM, Satoh K, Kondoh H, Ooka H, Kikuchi S (2010) Genome-wide analysis of NAC transcription factor family in rice. Gene 465:30–44
  • Nuruzzaman M, Sharoni AM, Kikuchi S (2013) Roles of NAC transcription factors in the regulation of biotic and abiotic stress responses in plants. Front Microbiol 4:248. doi:10.3389/fmicb.2013.00248
  • Puranik S, Sahu PP, Srivastava PS, Prasad M (2012) NAC proteins: regulation and role in stress tolerance. Trend Plant Sci 17:369–381
  • Ramegowda V, Senthil-Kumar M, Nataraja KN, Reddy MK, Mysore KS, Udayakumar M (2012) Expression of a finger millet transcription factor, EcNAC1, in tobacco confers abiotic stress-tolerance. PLoS One 7:e40397. doi:10.1371/journal.pone.0040397
  • Saad AS, Li X, Li HP, Huang T, Gao CS, Guo MW, Cheng W, Zhao GY, Liao YC (2013) A rice stress-responsive NAC gene enhances tolerance of transgenic wheat to drought and salt stresses. Plant Sci 203–204:33–40. doi:10.1016/j.plantsci.2012.12.016
  • SAS (2012) SAS/STAT® 9.3 User’s Guide. SAS Institute. Cary, NC, USA
  • Smirnoff N, Cumbes QJ (1989) Hydroxyl radical scavenging activity of compatible solutes. Phytochem 28:1057–1060
  • Sneha S, Rishi A, Dadhich A, Chandra S (2013) Effect of salinity on seed germination, accumulation of proline and free amino acids in Pennisetum glaucum (L.) R. Br. Pak J Biol Sci 16:877–881
  • Sobahan MA, Arias CR, Okuma E, Shimoishi Y, Nakamura Y, Hirai Y, Mori IC, Murata Y (2009) Exogenousproline and glycinebetaine suppress apoplastic flow to reduce Na+ uptake in rice seedlings. Biosci Biotechnol Biochem 73:2037–2042
  • Sobhanian H, Aghaei K, Komatsu S (2011) Changes in the plant proteome resulting from salt stress: toward the creation of salttolerant crops? J Proteomics 74:1323–1337
  • Sperotto RA, Ricachenevsky FK, Duarte GL, Boff T, Lopes KL, Sperb ER, Grusak MA, Fett JP (2009) Identification of upregulated genes in flag leaves during rice grain filling and characterization of OsNAC5, a new ABA-dependent transcription factor. Planta 230:985–1002. doi:10.1007/s00425-009-1000-9
  • Szabados L, Svouré A (2009) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97
  • 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 early responsive to dehydration stress 1 promoter. Plant Cell 16:2481–2498. doi:10.1105/tpc.104.022699
  • Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3. doi:10.1186/gb-2002-3-7-research0034
  • Wankhade SD, Cornejo MJ, Mateu-Andrés I, Sanz A (2013) Morphophysiological variations in response to NaCl stress during vegetative and reproductive development of rice. Acta Physiol Plant 35:323–333
  • Zhang B, Pan X, Cobb GP, Anderson TA (2006) Plant microRNA: a small regulatory molecule with big impact. Dev Biol 289:3–16
  • Zhang ZH, Liu Q, Song HX, Rong XM, Abdelbagi MI (2012) Responses of different rice (Oryza sativa L.) genotypes to salt stress and relation to carbohydrate metabolism and chlorophyll content. Afr J Agric Res 7:19–27
  • Zhong H, Guo QQ, Chen L, Ren F, Wang QQ, Zheng Y, Li XB (2012) Two Brassica napus genes encoding NAC transcription factors are involved in response to high-salinity stress. Plant Cell Rep 31:1991–2003. doi:10.1007/s00299-012-1311-3

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