Salinity stress limits plant growth and has a major impact on agricultural productivity. Here, we identify NAC transcription factor SlTAF1 as a regulator of salt tolerance in cultivated tomato (Solanum lycopersicum). While overexpression of SlTAF1 improves salinity tolerance compared with wild-type, lowering SlTAF1 expression causes stronger salinity-induced damage. Under salt stress, shoots of SlTAF1 knockdown plants accumulate more toxic Na+ ions, while SlTAF1 overexpressors accumulate less ions, in accordance with an altered expression of the Na+ transporter genes SlHKT1;1 and SlHKT1;2. Furthermore, stomatal conductance and pore area are increased in SlTAF1 knockdown plants during salinity stress, but decreased in SlTAF1 overexpressors. We identified stress-related transcription factor, abscisic acid metabolism and defence-related genes as potential direct targets of SlTAF1, correlating it with reactive oxygen species scavenging capacity and changes in hormonal response. Salinity-induced changes in tricarboxylic acid cycle intermediates and amino acids are more pronounced in SlTAF1 knockdown than wild-type plants, but less so in SlTAF1 overexpressors. The osmoprotectant proline accumulates more in SlTAF1 overexpressors than knockdown plants. In summary, SlTAF1 controls the tomato's response to salinity stress by combating both osmotic stress and ion toxicity, highlighting this gene as a promising candidate for the future breeding of stress-tolerant crops.

CSIRO Agriculture and Food St Lucia Qld 4067 Australia

Institute of Biochemistry and Biology University of Potsdam Karl Liebknecht Straße 24 25 Haus 20 14476 Potsdam Golm Germany

Institute of Biology Leiden University Sylviusweg 72 2333 BE Leiden the Netherlands

Laboratory of Growth Regulators The Czech Academy of Sciences Institute of Experimental Botany Palacký University Šlechtitelů 27 CZ 78371 Olomouc Czech Republic

Max Planck Institute of Molecular Plant Physiology Am Mühlenberg 1 14476 Potsdam Golm Germany

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Asins MJ, Villalta I, Aly MM, Olias R, Alvarez DEMP, Huertas R, Li J, Jaime-Perez N, Haro R, Raga V et al. 2013. Two closely linked tomato HKT coding genes are positional candidates for the major tomato QTL involved in Na+/K+ homeostasis. Plant, Cell & Environment 36: 1171-1191.

Balazadeh S, Siddiqui H, Allu AD, Matallana-Ramirez LP, Caldana C, Mehrnia M, Zanor MI, Kohler B, Mueller-Roeber B. 2010. A gene regulatory network controlled by the NAC transcription factor ANAC092/AtNAC2/ORE1 during salt-promoted senescence. The Plant Journal 62: 250-264.

Belhaj K, Chaparro-Garcia A, Kamoun S, Nekrasov V. 2013. Plant genome editing made easy: targeted mutagenesis in model and crop plants using the CRISPR/Cas system. Plant Methods 9: 39.

Belver A, Olias R, Huertas R, Rodriguez-Rosales MP. 2012. Involvement of SlSOS2 in tomato salt tolerance. Bioengineered 3: 298-302.

Brooks C, Nekrasov V, Lippman ZB, Van Eck J. 2014. Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-associated9 system. Plant Physiology 166: 1292-1297.

Campos JF, Cara B, Perez-Martin F, Pineda B, Egea I, Flores FB, Fernandez-Garcia N, Capel J, Moreno V, Angosto T et al. 2016. The tomato mutant ars1 (altered response to salt stress 1) identifies an R1-type MYB transcription factor involved in stomatal closure under salt acclimation. Plant Biotechnology Journal 14: 1345-1356.

Chen JQ, Meng XP, Zhang Y, Xia M, Wang XP. 2008. Over-expression of OsDREB genes lead to enhanced drought tolerance in rice. Biotechnology Letters 30: 2191-2198.

Davenport RJ, Munoz-Mayor A, Jha D, Essah PA, Rus A, Tester M. 2007. The Na+ transporter AtHKT1;1 controls retrieval of Na+ from the xylem in Arabidopsis. Plant, Cell & Environment 30: 497-507.

Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI. 2014. Plant salt-tolerance mechanisms. Trends in Plant Science 19: 371-379.

Du M, Zhai Q, Deng L, Li S, Li H, Yan L, Huang Z, Wang B, Jiang H, Huang T et al. 2014. Closely related NAC transcription factors of tomato differentially regulate stomatal closure and reopening during pathogen attack. Plant Cell 26: 3167-3184.

Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG, Miura S, Seki M, Shinozaki K, Yamaguchi-Shinozaki K. 2003. OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. The Plant Journal 33: 751-763.

Ebrahimian-Motlagh S, Ribone PA, Thirumalaikumar VP, Allu AD, Chan RL, Mueller-Roeber B, Balazadeh S. 2017. JUNGBRUNNEN1 confers drought tolerance downstream of the HD-Zip I transcription factor AtHB13. Frontiers in Plant Science 8: 2118.

Ernst HA, Olsen AN, Larsen S, Lo Leggio L. 2004. Structure of the conserved domain of ANAC, a member of the NAC family of transcription factors. EMBO Reports 5: 297-303.

Frusciante L, Carli P, Ercolano MR, Pernice R, Di Matteo A, Fogliano V, Pellegrini N. 2007. Antioxidant nutritional quality of tomato. Molecular Nutrition and Food Research 51: 609-617.

Fujita M, Fujita Y, Maruyama K, Seki M, Hiratsu K, Ohme-Takagi M, Tran LS, Yamaguchi-Shinozaki K, Shinozaki K. 2004. A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. The Plant Journal 39: 863-876.

Gálvez FJ, Baghour M, Hao G, Cagnac O, Rodríguez-Rosales MP, Venema K. 2012. Expression of LeNHX isoforms in response to salt stress in salt-sensitive and salt-tolerant tomato species. Plant Physiology and Biochemistry 51: 109-115.

Garapati P, Xue GP, Munne-Bosch S, Balazadeh S. 2015. Transcription factor ATAF1 in Arabidopsis promotes senescence by direct regulation of key chloroplast maintenance and senescence transcriptional cascades. Plant Physiology 168: 1122-1139.

Gharsallah C, Fakhfakh H, Grubb D, Gorsane F. 2016. Effect of salt stress on ion concentration, proline content, antioxidant enzyme activities and gene expression in tomato cultivars. AOB Plants 8: plw055.

Golldack D, Lüking I, Yang O. 2011. Plant tolerance to drought and salinity: stress regulating transcription factors and their functional significance in the cellular transcriptional network. Plant Cell Reports 30: 1383-1391.

Gong Q, Li P, Ma S, Indu Rupassara S, Bohnert HJ. 2005. Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana. The Plant Journal 44: 826-839.

Gonzalez-Guzman M, Apostolova N, Belles JM, Barrero JM, Piqueras P, Ponce MR, Micol JL, Serrano R, Rodriguez PL. 2002. The short-chain alcohol dehydrogenase ABA2 catalyzes the conversion of xanthoxin to abscisic aldehyde. Plant Cell 14: 1833-1846.

Graether SP, Boddington KF. 2014. Disorder and function: a review of the dehydrin protein family. Frontiers in Plant Science 5: 576.

Hichri I, Muhovski Y, Clippe A, Zizkova E, Dobrev PI, Motyka V, Lutts S. 2016. SlDREB2, a tomato dehydration-responsive element-binding 2 transcription factor, mediates salt stress tolerance in tomato and Arabidopsis. Plant, Cell & Environment 39: 62-79.

Hong Y, Zhang H, Huang L, Li D, Song F. 2016. Overexpression of a stress-responsive NAC transcription factor gene ONAC022 improves drought and salt tolerance in Rice. Frontiers in Plant Science 7: 4.

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. Proceedings of the National Academy of Sciences, USA 103: 12987-12992.

Hu WH, Yan XH, He Y, Ye XL. 2018. Role of alternative oxidase pathway in protection against drought-induced photoinhibition in pepper leaves. Photosynthetica 56: 1297-1303.

Huertas R, Olias R, Eljakaoui Z, Galvez FJ, Li J, De Morales PA, Belver A, Rodriguez-Rosales MP. 2012. Overexpression of SlSOS2 (SlCIPK24) confers salt tolerance to transgenic tomato. Plant, Cell & Environment 35: 1467-1482.

Huertas R, Rubio L, Cagnac O, Garcia-Sanchez MJ, Alche Jde D, Venema K, Fernandez JA, Rodriguez-Rosales MP. 2013. The K+/H+ antiporter LeNHX2 increases salt tolerance by improving K+ homeostasis in transgenic tomato. Plant, Cell & Environment 36: 2135-2149.

Jaime-Perez N, Pineda B, Garcia-Sogo B, Atares A, Athman A, Byrt CS, Olias R, Asins MJ, Gilliham M, Moreno V et al. 2017. The sodium transporter encoded by the HKT1;2 gene modulates sodium/potassium homeostasis in tomato shoots under salinity. Plant, Cell & Environment 40: 658-671.

Jensen MK, Hagedorn PH, de Torres-Zabala M, Grant MR, Rung JH, Collinge DB, Lyngkjaer MF. 2008. Transcriptional regulation by an NAC (NAM-ATAF1,2-CUC2) transcription factor attenuates ABA signalling for efficient basal defence towards Blumeria graminis f. sp. hordei in Arabidopsis. The Plant Journal 56: 867-880.

Jensen MK, Kjaersgaard T, Nielsen MM, Galberg P, Petersen K, O'Shea C, Skriver K. 2010. The Arabidopsis thaliana NAC transcription factor family: structure-function relationships and determinants of ANAC019 stress signalling. Biochemical Journal 426: 183-196.

Jensen MK, Rung JH, Gregersen PL, Gjetting T, Fuglsang AT, Hansen M, Joehnk N, Lyngkjaer MF, Collinge DB. 2007. The HvNAC6 transcription factor: a positive regulator of penetration resistance in barley and Arabidopsis. Plant Molecular Biology 65: 137-150.

Jin J, Tian F, Yang DC, Meng YQ, Kong L, Luo J, Gao G. 2017. PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Research 45: D1040-D1045.

Kim YS, Sakuraba Y, Han SH, Yoo SC, Paek NC. 2013. Mutation of the Arabidopsis NAC016 transcription factor delays leaf senescence. Plant, Cell & Physiology 54: 1660-1672.

Klaring HP, Zude M. 2009. Sensing of tomato plant response to hypoxia in the root environment. Scientia Horticulturae 122: 17-25.

Kopka J, Schauer N, Krueger S, Birkemeyer C, Usadel B, Bergmuller E, Dormann P, Weckwerth W, Gibon Y, Stitt M et al. 2005. GMD@CSB.DB: the golm metabolome database. Bioinformatics 21: 1635-1638.

Koenig D, Jimenez-Gomez JM, Kimura S, Fulop D, Chitwood DH, Headland LR, Kumara R et al. 2013. Comparative transcriptomics reveals patterns of selection in domesticated and wild tomato. Proceeding of the National Academy of Sciences, USA 110: 2655-2662.

Lata C, Prasad M. 2011. Role of DREBs in regulation of abiotic stress responses in plants. Journal of Experimental Botany 62: 4731-4748.

Li XD, Zhuang KY, Liu ZM, Yang DY, Ma NN, Meng QW. 2016. Overexpression of a novel NAC-type tomato transcription factor, SlNAM1, enhances the chilling stress tolerance of transgenic tobacco. Journal of Plant Physiology 204: 54-65.

Li XY, Li L, Liu X, Zhang B, Zheng WL, Ma WL. 2014. Analysis of physiological characteristics of abscisic acid sensitivity and salt resistance in Arabidopsis ANAC mutants (ANAC019, ANAC072 and ANAC055). Biotechnology and Biotechnological Equipments 26: 2966-2970.

Lin PC, Hwang SG, Endo A, Okamoto M, Koshiba T, Cheng WH. 2007. Ectopic expression of ABSCISIC ACID 2/GLUCOSE INSENSITIVE 1 in Arabidopsis promotes seed dormancy and stress tolerance. Plant Physiology 143: 745-758.

Liu Y, Sun J, Wu Y. 2016. Arabidopsis ATAF1 enhances the tolerance to salt stress and ABA in transgenic rice. Journal of Plant Research 129: 955-962.

Lu PL, Chen NZ, An R, Su Z, Qi BS, Ren F, Chen J, Wang XC. 2007. A novel drought-inducible gene, ATAF1, encodes a NAC family protein that negatively regulates the expression of stress-responsive genes in Arabidopsis. Plant Molecular Biology 63: 289-305.

Luedemann A, Strassburg K, Erban A, Kopka J. 2008. TagFinder for the quantitative analysis of gas chromatography-mass spectrometry (GC-MS)-based metabolite profiling experiments. Bioinformatics 24: 732-737.

Mao C, Ding J, Zhang B, Xi D, Ming F. 2018. OsNAC2 positively affects salt-induced cell death and binds to the OsAP37 and OsCOX11 promoters. The Plant Journal 94: 454-468.

Massaretto IL, Albaladejo I, Purgatto E, Flores FB, Plasencia F, Egea-Fernandez JM, Bolarin MC, Egea I. 2018. Recovering tomato landraces to simultaneously improve fruit yield and nutritional quality against salt stress. Frontiers in Plant Science 9: 1778.

Maathuis FJM. 2014. Sodium in plants: perception, signaling, and regulation of sodium fluxes. Journal of Experimental Botany 65: 849-858.

Mishra KB, Iannacone R, Petrozza A, Mishra A, Armentano N, La Vecchia G, Trtilek M, Cellini F, Nedbal L. 2012. Engineered drought tolerance in tomato plants is reflected in chlorophyll fluorescence emission. Plant Science 182: 79-86.

Mittler R, Vanderauwera S, Gollery M, Van Breusegem F. 2004. Reactive oxygen gene network of plants. Trends in Plant Science 9: 490-498.

Moller IS, Gilliham M, Jha D, Mayo GM, Roy SJ, Coates JC, Haseloff J, Tester M. 2009. Shoot Na+ exclusion and increased salinity tolerance engineered by cell type-specific alteration of Na+ transport in Arabidopsis. Plant Cell 21: 2163-2178.

Munns R, Tester M. 2008. Mechanisms of salinity tolerance. Annual Reviews in Plant Biology 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. The Plant Journal 51: 617-630.

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.

Olias R, Eljakaoui Z, Li J, De Morales PA, Marin-Manzano MC, Pardo JM, Belver A. 2009. The plasma membrane Na+/H+ antiporter SOS1 is essential for salt tolerance in tomato and affects the partitioning of Na+ between plant organs. Plant, Cell & Environment 32: 904-916.

Olsen AN, Ernst HA, Leggio LL, Skriver K. 2005. NAC transcription factors: structurally distinct, functionally diverse. Trends in Plant Science 10: 79-87.

Ooka H, Satoh K, Doi K, Nagata T, Otomo Y, Murakami K, Matsubara K, Osato N, Kawai J, Carninci P et al. 2003. Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Research 10: 239-247.

Orellana S, Yanez M, Espinoza A, Verdugo I, Gonzalez E, Ruiz-Lara S, Casaretto JA. 2010. The transcription factor SlAREB1 confers drought, salt stress tolerance and regulates biotic and abiotic stress-related genes in tomato. Plant, Cell & Environment 33: 2191-2208.

Osorio S, Do PT, Fernie AR. 2012. Profiling primary metabolites of tomato fruit with gas chromatography/mass spectrometry. Methods in Molecular Biology 860: 101-109.

Pérez-Rodríguez P, Riaño-Pachón DM, Corrêa LG, Rensing SA, Kersten B, Mueller-Roeber B. 2010. PlnTFDB: updated content and new features of the plant transcription factor database. Nucleic Acids Research 38: D822-827.

Petrov V, Hille J, Mueller-Roeber B, Gechev TS. 2015. ROS-mediated abiotic stress-induced programmed cell death in plants. Frontiers in Plant Science 6: 69.

Puranik S, Sahu PP, Srivastava PS, Prasad M. 2012. NAC proteins: regulation and role in stress tolerance. Trends in Plant Science 17: 369-381.

Raghavendra AS, Gonugunta VK, Christmann A, Grill E. 2010. ABA perception and signaling. Trends in Plant Science 15: 395-401.

Richter JA, Behr JH, Erban A, Kopka J, Zörb C. 2019. Ion-dependent metabolic responses of Vicia faba L. to salt stress. Plant, Cell, & Environment 42: 295-309.

Rohrmann J, Tohge T, Alba R, Osorio S, Caldana C, McQuinn R, Arvidsson S, van der Merwe MJ, Riaño-Pachón DM, Mueller-Roeber B et al. 2011. Combined transcription factor profiling, microarray analysis and metabolite profiling reveals the transcriptional control of metabolic shifts occurring during tomato fruit development. The Plant Journal 68: 999-1013.

Romani F, Ribone PA, Capella M, Miguel VN, Chan RL. 2016. A matter of quantity: Common features in the drought response of transgenic plants overexpressing HD-Zip I transcription factors. Plant Science 251: 139-154.

Sakuma Y, Maruyama K, Osakabe Y, Qin F, Seki M, Shinozaki K, Yamaguchi-Shinozaki K. 2006. Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18: 1292-1309.

Sakuraba Y, Piao W, Lim JH, Han SH, Kim YS, An G, Paek NC. 2015. Rice ONAC106 inhibits leaf senescence and increases salt tolerance and tiller angle. Plant and Cell Physiology 56: 2325-2339.

Sanchez DH, Siahpoosh MR, Roessner U, Udvardi M, Kopka J. 2008. Plant metabolomics reveals conserved and divergent metabolic responses to salinity. Physiologia Plantarum 132: 209-219.

Schwarz D, Thompson AJ, Klaring HP. 2014. Guidelines to use tomato in experiments with a controlled environment. Frontiers in Plant Science 5: 625.

Shabala S. 2009. Salinity and programmed cell death: unravelling mechanisms for ion specific signalling. Journal of Experimental Botany 60: 709-712.

Shabala S. 2013. Learning from halophytes: physiological basis and strategies to improve abiotic stress tolerance in crops. Annals of Botany 112: 1209-1221.

Shinozaki Y, Nicolas P, Fernandez-Pozo N, Ma Q, Evanich DJ, Shi Y, Xu Y, Zheng Y, Snyder SI, Martin LBB et al. 2018. High-resolution spatiotemporal transcriptome mapping of tomato fruit development and ripening. Nature Communications 9: 364.

Shkolnik D, Finkler A, Pasmanik-Chor M, Fromm H. 2019. CALMODULIN-BINDING TRANSCRIPTION ACTIVATOR 6: a key regulator of Na+ homeostasis during germination. Plant Physiology 180: 1101-1118.

Sholi NJY. 2012. Effect of salt stress on seed germination, plant growth, photosynthesis and ion accumulation of four tomato cultivars. American Journal of Plant Physiology 7: 269-275.

Smith CA, Melino VJ, Sweetman C, Soole KL. 2009. Manipulation of alternative oxidase can influence salt tolerance in Arabidopsis thaliana. Physiologia Plantarum 137: 459-472.

Szabados L, Savouré A. 2010. Proline: a multifunctional amino acid. Trends in Plant Science 15: 89-97.

Tak H, Negi S, Ganapathi TR. 2017. Banana NAC transcription factor MusaNAC042 is positively associated with drought and salinity tolerance. Protoplasma 254: 803-816.

Takahashi F, Suzuki T, Osakabe Y, Betsuyaku S, Kondo Y, Dohmae N, Fukuda H, Yamaguchi-Shinozaki K, Shinozaki K. 2018. A small peptide modulates stomatal control via abscisic acid in long-distance signalling. Nature 556: 235-238.

Takasaki H, Maruyama K, Kidokoro S, Ito Y, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K, Nakashima K. 2010. The abiotic stress-responsive NAC-type transcription factor OsNAC5 regulates stress-inducible genes and stress tolerance in rice. Molecular Genetics and Genomics 284: 173-183.

Thirumalaikumar VP, Devkar V, Mehterov N, Ali S, Ozgur R, Turkan I, Mueller-Roeber B, Balazadeh S. 2018. NAC transcription factor JUNGBRUNNEN1 enhances drought tolerance in tomato. Plant Biotechnology Journal 16: 354-366.

Tran LS, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama K, Fujita M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K. 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.

Verbruggen N, Hermans C. 2008. Proline accumulation in plants: a review. Amino Acids 35: 753-759.

Wang G, Zhang S, Ma X, Wang Y, Kong F, Meng Q. 2016. A stress-associated NAC transcription factor (SlNAC35) from tomato plays a positive role in biotic and abiotic stresses. Physiologia Plantarum 158: 45-64.

Wang LL, Hu ZL, Zhu MK, Zhu ZG, Hu JT, Qanmber G, Chen GP. 2017. The abiotic stress-responsive NAC transcription factor SlNAC11 is involved in drought and salt response in tomato (Solanum lycopersicum L.). Plant Cell, Tissue and Organ Culture 129: 161-174.

Wang X, Basnayake BM, Zhang H, Li G, Li W, Virk N, Mengiste T, Song F. 2009. The Arabidopsis ATAF1, a NAC transcription factor, is a negative regulator of defense responses against necrotrophic fungal and bacterial pathogens. Molecular Plant-Microbe Interactions 22: 1227-1238.

Wu A, Allu AD, Garapati P, Siddiqui H, Dortay H, Zanor MI, Asensi-Fabado MA, Munne-Bosch S, Antonio C, Tohge T et al. 2012. JUNGBRUNNEN1, a reactive oxygen species-responsive NAC transcription factor, regulates longevity in Arabidopsis. Plant Cell 24: 482-506.

Wu HJ, Zhang Z, Wang JY, Oh DH, Dassanayake M, Liu B, Huang Q, Sun HX, Xia R, Wu Y et al. 2012. Insights into salt tolerance from the genome of Thellungiella salsuginea. Proceeding of the National Academy of Sciences, USA 109: 12219-12224.

Xue GP, Bower NI, McIntyre CL, Riding GA, Kazan K, Shorter R. 2006. TaNAC69 from the NAC superfamily of transcription factors is up-regulated by abiotic stresses in wheat and recognises two consensus DNA-binding sequences. Functional Plant Biology 33: 43-57.

Yamaguchi T, Blumwald E. 2005. Developing salt-tolerant crop plants: challenges and opportunities. Trends in Plant Science 10: 615-620.

Ye H, Liu S, Tang B, Chen J, Xie Z, Nolan TM, Jiang H, Guo H, Lin HY, Li L et al. 2017. RD26 mediates crosstalk between drought and brassinosteroid signalling pathways. Nature Communications 8: 14573.

Zhang P, Senge M, Dai Y. 2016. Effects of salinity stress on growth, yield, fruit quality and water use efficiency of tomato under hydroponics system. Reviews in Agricultural Science 4: 46-55.

Zhang XX, Tang YJ, Ma QB, Yang CY, Mu YH, Suo HC, Luo LH, Nian H. 2016. OsDREB2A, a rice transcription factor, significantly affects salt tolerance in transgenic soybean. PLoS ONE 8: e83011.

Zhao X, Wang W, Zhang F, Deng J, Li Z, Fu B. 2014. Comparative metabolite profiling of two rice genotypes with contrasting salt stress tolerance at the seedling stage. PLoS ONE 9: e108020.

Zheng X, Chen B, Lu G, Han B. 2009. Overexpression of a NAC transcription factor enhances rice drought and salt tolerance. Biochemical and Biophysical Research Communications 379: 985-989.

Zhu M, Chen G, Zhang J, Zhang Y, Xie Q, Zhao Z, Pan Y, Hu Z. 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 Reports 33: 1851-1863.

Zhu M, Meng X, Cai J, Li G, Dong T, Li Z. 2018. Basic leucine zipper transcription factor SlbZIP1 mediates salt and drought stress tolerance in tomato. BMC Plant Biology 18: 83.

Zhu T, Zou L, Li Y, Yao X, Xu F, Deng X, Zhang D, Lin H. 2018. Mitochondrial alternative oxidase-dependent autophagy involved in ethylene-mediated drought tolerance in Solanum lycopersicum. Plant Biotechnology Journal 16: 2063-2076.