Advances in the Research of Transcription Factors Involved in Plant Salt Stress Regulation

CHEN Na, CHENG Guo, WANG Mian, YANG Zhen, WANG Tong,CHEN Ming-na, PAN Li-juan, CHI Xiao-yuan, YU Shan-lin*

(1. Shandong Peanut Research Institute, Qingdao 266100, China;2. Qingdao Entry-Exit Inspection and Quarantine Bureau, Qingdao 266001, China)



Advances in the Research of Transcription Factors Involved in Plant Salt Stress Regulation

CHEN Na1, CHENG Guo2, WANG Mian1, YANG Zhen1, WANG Tong1,CHEN Ming-na1, PAN Li-juan1, CHI Xiao-yuan1, YU Shan-lin1*

(1. Shandong Peanut Research Institute, Qingdao 266100, China;2.QingdaoEntry-ExitInspectionandQuarantineBureau,Qingdao266001,China)

Salt stress is a major environmental factor that adversely affects plant growth, development and crop yields. During the process of response and adaptation to salt stress, there are many changes in biochemical and physiological reaction, and many genes are activated, leading to accumulation of numerous proteins involved in resistance to salt stress. The expression of stress-induced genes is mainly regulated by specific transcription factors (TFs). Typically, the TFs are capable of activating or repressing the transcription of multiple target genes. So far, various TFs and cis-acting elements contained in stress-responsive promoters have been described. These TFs and cis-motifs function not only as molecular switches for gene expression, but also as terminal points of signal transduction in the signaling processes. In this article, we summarize the research progress of several TFs families, including transcription factors of NAC, bZIP and bHLH, which involved in plant salt stress regulation.

transcription factors; salt stress; regulation mechanism; research advances

Salt stress afflicts plant culture in many parts of the world, particularly on irrigated land[1]. Crop growth and productivity are often accompanied by salt stress, which results in a range of morphological, physiological, biochemical and molecular changes in the plant[2-3].

The perception of salt stress operates through various sensors, which initiate a cascade of transcription, and consequently leading to the production of protective proteins and metabolites[4]. Transcription factors (TFs) are important components for regulating salt-responsive genes[5]. Large numbers of transcription factors that include activators, co-activators and suppressor have already been identified. Among them, transcription factors play critical roles in plant responses to salt stress via transcriptional regulation of the downstream genes responsible for plant tolerance to salt challenges. They constitute a redundant family of transcriptional regulators in plants with 134 members in theArabidopsisgenome, 94 for indica rice genome and 113 injaponica[6]. Many transcription factors are related proteins that share the homologous DNA binding domain and are classified in families based on their DNA-binding domains, such as the MYB-like proteins (containing helix-turn-helix motifs), the MADS domain proteins, the homeobox proteins, the bZIP (basic region leucine zipper) proteins or the zinc finger proteins (ZFPs)[7].

Previous studies have revealed some key components that control and modulate salt stress adaptive pathways include transcription factors ranging from AP2/ERF, WRKY, and MYB proteins to general TFs[8-10]. In this review, we focus on recent advances in salt stress related NAC, bZIP and bHLH transcription factors and transcription factor -based engineering of increased salt adaptation. We hope to indicate the study direction of transcription factors involved in peanut salt stress regulation.

1 NAC TAF1, UC2) transcription factors and plant salt stress

The major NAC pathway is active in response to abiotic stress which has been identified and well elucidated inArabidopsisand rice[5, 11-12]. The NAC TF family is widely distributed in plants, but so far has not been found in other eukaryotes[13].

Large-scale abiotic stress responsive expression analysis indicated that NAC family proteins may have important functions in plant salt stress acclimation. For example, out of 88 NAC transcription members in genome ofMedicagotruncatula, 36 members were up-regulated in roots during salt stress treatment[14]. A microarray analysis of the root transcriptome following NaCl exposure detected that 23 ANAC genes was induced and 7 genes was reduced, respectively, by a two-fold threshold[15]. In crops, such as rice, Fang et al. systematically analyzed the NAC family and identified 140 putative ONAC or ONAC-like TFs, among which 19 genes were up-regulated by salt stress[16]. Computational prediction assumed that there are at least 205 NAC or NAC-like TFs members in soybean, among which 8 genes were characterized to be induced by high salinity[17-19].

Functional analysis revealed potentials of NAC in improvement of plant salt stress tolerance. NAC TFs enhance stress tolerance in the model plantArabidopsis. The expression ofArabidopsisAtNAC2 was induced by salt stress and this induction required ethylene and auxin signaling pathway. Overexpression ofAtNAC2 could maintain the number of lateral roots in transgenic lines during salt stress, which indicate that AtNAC2/ANAC092 may be a transcription factor incorporating the environmental and endogenous stimuli into the process of plant lateral root development[20]. Recently, ANAC092 gene also demonstrated an intricate overlap of ANAC092- mediated gene regulatory networks during salt-promoted senescence and seed maturation[21]. TransgenicArabidopsisoverexpressing a salt inducible rice NAC gene, theONAC063, showed enhanced tolerance to high salinity and osmotic pressure by similar mechanisms because ONAC063-upregulated genes were almost similar to those up-regulated by ANAC019, ANAC055 or ANAC072[22]. Overexpression ofTaNAC2 andTaNAC67 resulted in pronounced enhanced tolerances to salt stress inArabidopsisthrough enhancing expression of multiple abiotic stress responsive genes and improving physiological traits, including strengthened cell membrane stability, retention of higher chlorophyll contents, and so on[23-24]. In addition, many NAC transcription factors isolated from other plants were also involved in salt resistance regulation in transgenic lines. These members includedEcNAC1 of finger millet,GmNAC11 andGmNAC20 of soybean,DgNAC1 of chrysanthemum[25-27].

Following the discovery of potential use of NAC TFs to improve stress tolerance inArabidopsis, a number of important successes were reported on the application of NAC TFs in genetic engineering of important crops, such as cultivated rice for enhanced tolerance against various environmental stresses. Transgenic rice overexpressing the stress inducibleSNAC1 orSNAC2/OsNAC6 gene both displayed salt tolerance[28-30]. TheSNAC1 transgenic rice was more sensitive to abscisic acid[28]. More recently, Liu et al. proved that overexpression ofSNAC1 improves salt tolerance by enhancing root development and reducing transpiration rate in transgenic cotton[31]. Overexpression ofSNAC2/OsNAC6 could enhance expression of a large number of genes encoding proteins with predicted stress tolerance functions such as detoxification, redox homeostasis and proteolytic degradation as well[29-30]. Overexpression of another rice NAC gene, theONAC045 gene, whose expression is induced by high salinity and ABA treatment, showed significantly enhanced tolerance to salt at the seedling stage. At least, expression levels of two stress-responsive genes,OsLEA3-1 andOsPM1, were up-regulated inONAC045 transgenic lines[32]. However, expressions ofOsLEA3-1 andOsPM1 were not affected in eitherSNAC1 orSNAC2 transgenic rice, suggesting that ONAC045 TF improves stress tolerance of transgenic plants in different pathway than SNAC1 and SNAC2/OsNAC6[32]. Moreover, the potential transcriptional target genes of SNAC1 and SNAC2 are also different. There is no overlapping between the two sets of genes up or down-regulated in the two overexpression plants, respectively[29]. The core DNA binding sites for the putative SNAC1 and SNAC2 target genes are the same, but comparison of the flanking sequences of the core DNA binding sites in the putative SNAC1 and SNAC2 target genes revealed different conserved flanking sequences of the core binding sites of genes targeted by SNAC1 and SNAC2. Together, these results may suggest that different stress-responsive NAC TFs may activate the transcription of a different set of target genes, thus conferring diverse functions that jointly lead to stress tolerance.

As we know, most transcription factors are localized in cell nucleus to exercise their transcription regulation functions. However, some membrane-bound transcription factors (MTTFs) were identified in recent years[33]. Six of the NAC factors - NTM1, NTL8, NTL6, NTL9, ANAC013 and ANAC017 -had been demonstrated to be membrane-bounded[33-40]. NAC-MTTFs appear to be localized to different membranes, including the nuclear/endoplasmic reticulum or the plasma membrane[34-35,37,39-40]. Among these MTTFs, NTL6 and NTL8 had been found to regulate salt-stress signaling impinging on flowering or seed germination pathways[35-36]. Under salt stress, the repression of FT (Flowering locus T) was attenuated, albeit mildly, in anntl8 mutant[35]. In addition, the germination rate under salt stress in seeds overexpressing the truncated form of NTL8 was decreased and that of anntl8 mutant was increased, suggesting that NTL8 regulates salt responses in seed germination[36]. Similarly to NTL8, transformants constitutively expressing an active form of NTL6 exhibited a hypersensitive response to ABA and high salinity in seed germination[38].

As a whole, strong evidence indicated that transgenic rice plants harboring NAC genes have enhanced stress tolerance even in field trials, suggesting that NAC TFs are promising candidate genes for genetic engineering of different crops aimed at improving their productivity under adverse conditions.

2 bZIP TFs and their role in conferring salt stress tolerance to plants

bZIPs organize a large family which have been described inArabidopsis(75), rice (89), sorghum (92), soybean (131), and recently in maize (125)[41]. All the members of this family contain a basic region/leucine zipper (bZIP) domain. The bZIP family was subdivided into 10 groups named A to I, plus S inArabidopsisaccording to their sequence similarities and functional features[41-43]. While many bZIPs can form homodimers, bZIP members classified in different groups can be combined through heterodimerization to form specific bZIP pairs with distinct functionalities.

Previous studies have indicated that bZIP proteins are key regulators involved in salt stress adaption. A lot of bZIP proteins isolated from diverse species includingArabidopsis, rice, tomato, soybean, maize and wheat, etc., enhanced the salt tolerance of the transgenic plants[44-56].

The function mechanisms of bZIPs have been studied thoroughly. Some members of the basic region/leucine zipper (bZIP)-type protein family are ABA-responsive element binding protein (AREB) and ABA-responsive element binding factor (ABF), which act as major transcription factors in ABA-responsive gene expression under salt stress conditions inArabidopsis. For example, bZIP factors SlAREB1, ScAREB1, SpAREB1, AtABI5, OsABI5, and ABF2-4 inArabidopsisall have a key regulatory role in ABA signaling under salt stress[50,54, 57-58]. A key regulator of salt stress adaptation, the group F bZIP TF bZIP24, was identified by differential screening of salt-inducible transcripts inA.thalianaand a halophyticArabidopsis-relative model species[59]. In addition, AtbZIP24 shows salt inducible subcellular re-targeting to the nucleus and formation of homodimers, suggesting that molecular dynamics of bZIP factors could mediate new signaling connections within the complex cellular signaling network[59]. RNAi-mediated repression of the factor conferred increased salt tolerance toArabidopsis. The improved tolerance was mediated by stimulated transcription of a wide range of stress-inducible genes involved in cytoplasmic ion homeostasis, osmotic adjustment, as well as in plant growth and development, which demonstrated a pivotal function of bZIP24 in salt tolerance by regulating multiple mechanisms that are essential for stress adaptation[59].

In addition, numerous bZIPs were proved to control signal transduction pathways by molecular re-organization and by posttranslational mechanisms[60-61]. Specific homodimerizations and heterodimerizations within the class of bZIP TFs as well as modular flexibility of the interacting proteins and posttranslational modifications might determine the functional specificity of bZIP factors in cellular transcription networks[44, 51-52,62]. The phosphorylation of bZIP proteins seems also important for their function. For example, potato StABF1 is phosphorylated in response to ABA and salt stress in a calcium-dependent manner, and a potato CDPK isoform (StCDPK2) had been identified to phosphorylate StABF1 in vitro[63]. The three factors AREB1, AREB2, and ABF3 can form homodimers and heterodimers as well as interact with a SnRK2 protein kinase suggesting ABA-dependent phosphorylation of the proteins[64].

Similar to NAC transcription factors, one bZIP transcription factors involved in salt stress were also demonstrated to be membrane-bounded. Most bZIP MTTFs are anchored in the membrane of endoplasmic reticulum. In response to stress, cytosolic components of the transcription factors are released by proteolysis and move to the nucleus where they promote the up-regulation of stress response genes[65-66]. One such stress sensor/transducer isArabidopsisAtbZIP17, which is activated in response to salt stress. Under salt stress conditions, the stress-inducible expression of the activated AtbZIP17 enhanced salt tolerance as demonstrated by chlorophyll bleaching and seedling survival assays[65].

3 bHLH TFs and their role in conferring salt stress tolerance to plants

The bHLH family transcription factors have been intensively studied in plants and animals[66-67]. With the genome-wide analysis of the bHLH transcription factor family in plants, 162 bHLH genes inArabidopsisand 167 in rice were identified[68]. This family is defined by the bHLH signature domain, which is evolutionarily conserved[69-70]. Plant bHLH proteins bind to the E-box (CANNTG) motif in gene promoters; a consensus core element called G-box (CACGTG) is the most common form[68].

Although numerous bHLH members were identified inArabidopsisand rice, only a few of them had been revealed to be involved in plant salt stress regulation.ChrysanthemumdichrumCdICE1 and tomatoSlICE1aboth contain conserved bHLH domain and overexpression of these two genes could both improve the tolerance of transgenic plants to salinity[71-72]. Jiang et al. identified three salt-inducible bHLH proteins: bHLH41, bHLH42/TT8 and bHLH92. Among which,bHLH92 was highly induced at the transcript level by a wide range of abiotic stresses and the response to NaCl was quantitatively the highest[73]. Overexpression ofbHLH92 moderately increased the tolerance to NaCl and osmotic stresses. However, knock-out mutants of this gene failed to show significant differences from WT plants in the root elongation assay under NaCl stress, suggesting that bHLH92 function is not required for full tolerance to NaCl, and may therefore be redundant with other bHLH proteins.OrbHLH001 andOrbHLH2 were cloned from Dongxiang wild rice[74-75]. Overexpression ofOrbHLH001 andOrbHLH2 enhances tolerance to salt stress inArabidopsis[74-75]. Examination of the expression of cold-responsive genes in transgenicArabidopsisshowed that the function of OrbHLH001 differs from that of ICE1 and is independent of a CBF/DREB1 cold-response pathway[75]. However, overexpression ofOrbHLH2 inArabidopsisimproved salt tolerance by enhancing the expression level of DREB1A/CBF3 and its down stream target genes, but the ABA signal pathway was not affected in transgenicArabidopsis, which suggest that OrbHLH2 probably function in salt response through an ABA-independent pathway[74]. These results suggest that different homologs of ICE1 may mediate the regulation of salt tolerance in a different signal response process. And what's more, Chen et al. indicated that overexpression ofOrbHLH001 could also confer salt tolerance in transgenic rice plants[76]. OrbHLH001 protein exercise its function by inducing the expression ofOsAKT1, another quantitative trait loci (QTLs) controlling K+uptake into the root and the Na+/K+ratio in salt-stress, to regulate the Na+/K+ratio inOrbHLH001-overexpressed plants[76].

Guan et al. found a nuclear-localized calcium-binding protein, RSA1 (Short Root in Salt Medium 1), which is required for salt tolerance, and identified its interacting partner, RITF1, a bHLH transcription factor. They show that RSA1 and RITF1 regulate the transcription of several genes involved in the detoxification of reactive oxygen species generated by salt stress and that they also regulate the SOS1 gene that encodes a plasma membrane Na+/H+antiporter essential for salt tolerance[77]. This study discovered a novel nuclear calcium-sensing and -signaling pathway that is important for gene regulation and salt stress tolerance.

As more members in the complex systems in stress response are reported, the function of bHLH transcription factors will be better understood.

4 Other transcription factors related to salt stress in plants

Numerous transcription factors were found to be invovled in plant salt tolerance regulation using large scale screening methods such as microarray hybridization. Besides the TFs referred above, a lot of other transcription factors may be involved in plant salt stress regulation. These transcription factors usually contain the conserved domain such as C2C2-DOF, GARP, GRAS, MADS, PHD, SBP, C3HC4-type RING finger, HSF, MYC, ZIM, LBD, and so on[15, 78-81].

Several members of above mentioned family transcription factors were indicated to confer plant salt stress tolerance. For example, a poplar GRAS gene, PeSCL7, enhanced tolerance to salt treatments in transgenicArabidopsis[82]. Corrales et al. reported a group of five tomato DOF (DNA binding with One Finger) genes,SlCDF1-5.SlCDF1-5 genes exhibited distinct diurnal expression patterns and were differentially induced in response to osmotic, salt, heat, and low-temperature stresses[83].Arabidopsisplants overexpressingSlCDF1 orSlCDF3 showed increased salt tolerance. In addition, the expression of various stress-responsive genes, such asCOR15,RD29A, andRD10, were differentially activated in the overexpressing lines[83].

However, most of the transcription factors were screened by microarray lack function analysis in salt stress regulation processes of plant. Therefore, more and more transcription factors will be proved to be involved in salt stress regulation in the future.

5 Research advances of transcription factors involved in peanut salt stress regulation

The cultivated peanut (ArachishypogaeaL.) is an important oil crop and play an important role in the economy of many countries[84]. Like many other crop species, peanut is relatively sensitive to salinity[84-85]. Some studies indicated that salinity could decrease seed germination, seedling development and dry matter accumulation[86-90]. Other proofs also indicated that salinity could induce damage to the photosynthetic apparatus or cause deficiencies of nutrient elements such as Ca, K and Mg[91-92], and lead to severe yield losses[90,93-94]. Based on gene expression response to abiotic stress, some transcription factor families, such as NAC, ERF and MYB, have been proved to be involved in peanut abiotic stress egulation[95-98]. AhNAC3 improves water stress tolerance by increasing superoxide scavenging and promoting the accumulation of various protective molecules in tobacco[96]. The overexpression ofAhERF019 enhances tolerance to drought, heat, and salt stresses inArabidopsis, but its regulation mechanism has not been studied[98].FourArabidopsistranscription factors,AtDREB1A,AtDREB2A,AtHB7 andAtABF3, enhance salt and drought tolerance by activating multiple cellular tolerance pathways in transgenic peanut[99-100]. Due to the complexity of the peanut genome and the difficulties of genetic transformation, there are limited studies on the molecular mechanisms of abiotic stress regulation in peanut. More studies are needed to clarify the signaling pathway involved in abiotic stress regulation in peanut.

[1] Epstein E, Norlyn D, Rush, D W, et al. Saline culture of crops: a genetic approach [J]. Science, 1980, 210: 399-404.

[2] Bhatnagar-Mathur P, Vadez V, Sharma K. Transgenic approaches for abiotic stress tolerance in plants: retrospect and prospects [J]. Plant Cell Reports, 2008, 27: 411-424.

[3] Sakamoto H, Maruyama K, Sakuma Y, et al.ArabidopsisCys2/His2-type zinc-finger proteins functions transcription repressors under drought, cold, and high-salinity stress conditions [J]. Plant Physiology, 2004, 136: 2734-2746.

[4] Bartels D, Sunkar R. Drought and salt tolerance in plants [J]. Critical Reviews in Plant Sciences, 2005, 24: 23-58.

[5] Nakashima K, Ito Y, Yamaguchi-Shinozaki K. Transcriptional regulatory networks in response to abiotic stresses inArabidopsisand grasses [J]. Plant Physiology, 2009, 149: 88-95.

[6] Kielbowicz-Matuk A. Involvement of plant C2H2-type zinc finger transcription factors in stress responses [J]. Plant Science, 2012, 185-186: 78-85.

[7] Fujimoto S Y, Ohta M, Usui A, et al.Arabidopsisethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression [J]. Plant Cell, 2000, 12: 393-404.

[8] Dubos C, Stracke R, Grotewold E, et al. MYB transcription factors inArabidopsis[J]. Trends in Plant Science, 2010, 15: 573-581.

[9] Chen L, Song Y, Li S, et al. The role of WRKY transcription factors in plant abiotic stresses [J]. Biochimica et Biophysica Acta, 2012, 1819: 120-128.

[10] Li X P, Tian A G, Luo G Z, et al. Soybean DRE-binding transcription factors that are responsive to abiotic stresses [J]. Theorrtical and Applied Genetics, 2005, 110: 1355-1362.

[11] Yamaguchi-Shinozaki K, Shinozaki K. Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters [J]. Trends in Plant Science, 2005, 10: 88-94.

[12] Yamaguchi-Shinozaki K, Shinozaki K. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses [J]. Annual Review of Plant Biology, 2006, 57: 781-803.

[13] Olsen A N, Ernst H A, Leggio L L, et al. NAC transcription factors: structurally distinct, functionally diverse [J]. Trends in Plant Science, 2005, 10: 79-87.

[14] Li D F, Su Z, Dong J L, et al. An expression database for roots of the model legumeMedicagotruncatulaunder salt stress [J]. BMC Genomics, 2009, 10: 517.

[15] Jiang Y, Deyholos M K. Comprehensive transcriptional profiling of NaCl-stressedArabidopsisroots reveals novel classes of responsive genes [J]. BMC Plant Biology, 2006, 6: 25.

[16] Fang Y, You J, Xie K, et al. Systematic sequence analysis and identification of tissue-specific or stress-responsive genes of NAC transcription factor family in rice [J]. Molecular Genetics and Genomics, 2008, 280: 535-546.

[17] Tran L S, Quach T N, Guttikonda S K, et al. Molecular characterization of stress-inducible GmNAC genes in soybean [J]. Molecular Genetics and Genomics, 2009, 281: 647-664.

[18] Mochida K, Yoshida T, Sakurai T, et al. In silico analysis of transcription factor repertoire and prediction of stress responsive transcription factors in soybean [J]. DNA Research, 2009, 16: 353-369.

[19] Pinheiro G L, Marques C S, Costa M D, et al. Complete inventory of soybean NAC transcription factors: sequence conservation and expression analysis uncover their distinct roles in stress response [J]. Gene, 2009, 444: 10-23.

[20] He X J, Mu R L, Cao W H, et al. AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development [J]. Plant Journal, 2005, 44: 903-916.

[21] Balazadeh S, Wu A, Mueller-Roeber B. Salt-triggered expression of the ANAC092-dependent senescence regulon inArabidopsisthaliana[J]. Plant Signaling & Behavior, 2010, 5: 733-735.

[22] Yokotani N, Ichikawa T, Kondou Y, et al. Tolerance to various environmental stresses conferred by the salt-responsive rice geneONAC063 in transgenicArabidopsis[J]. Planta, 2009, 229: 1065-1075.

[23] Mao X G, Chen S S, Li A, et al. Novel NAC transcription factor TaNAC67 confers enhanced multi-abiotic stress tolerances inArabidopsis[J]. PLoS One, 2014, 9: e84359.

[24] Mao X G, Zhang H Y, Qian X Y, et al. TaNAC2, a NAC-type wheat transcription factor conferring enhanced multiple abiotic stress tolerances inArabidopsis[J]. Journal of Experimental Botany, 2012, 63: 2933-2946.

[25] Ramegowda V, Senthil-Kumar M, Nataraja K N, et al. Expression of a finger millet transcription factor, EcNAC1, in tobacco confers abiotic stress-tolerance [J]. PLoS One, 2012, 7: e40397.

[26] Hao Y J, Wei W, Song Q X, et al. Soybean NAC transcription factors promote abiotic stress tolerance and lateral root formation in transgenic plants [J]. Plant Journal, 2011, 68: 302-313.

[27] Liu Q L, Xu K D, Zhao L J, et al. Overexpression of a novel chrysanthemum NAC transcription factor gene enhances salt tolerance in tobacco [J]. Biotechnology Letters, 2011, 33: 2073-2082.

[28] Hu H H, Dai M Q, Yao J L, et al. Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice [J]. Proceedings of the National Academy of Sciences of the United States of America, 2006, 103: 12987-12992.

[29] Hu H, You J, Fang Y, et al. Characterization of transcription factor geneSNAC2 conferring cold and salt tolerance in rice [J]. Plant Molecular Biology, 2008, 67: 169-181.

[30] Nakashima K, Tran L S, Van Nguyen D, et al. Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress- responsive gene expression in rice [J]. Plant Journal, 2007, 51: 617-630.

[31] Liu G, Li X, Jin S, et al. Overexpression of rice NAC geneSNAC1 improves drought and salt tolerance by enhancing root development and reducing transpiration rate in transgenic cotton [J]. PLoS One, 2014, 9: e86895.

[32] Zheng X N, Chen B, Lu G J, et al. Overexpression of a NAC transcription factor enhances rice drought and salt tolerance [J]. Biochemical and Biophysical Research Communications, 2009, 379: 985-989.

[33] Chen Y N, Slabaugh E, anf Brandizzi F. Membrane-tethered transcription factors inArabidopsisthaliana: novel regulators in stress response and development [J]. Current Opinion in Plant Biology, 2008, 11: 695-701.

[34] Kim Y S, Kim S G, Park J E, et al. A membrane-bound NAC transcription factor regulates cell division inArabidopsis[J]. Plant Cell, 2006, 18: 3132-3144.

[35] Kim S G, Kim S Y, Park C M. A membrane-associated NAC transcription factor regulates salt-responsive flowering via Flowering Locus T inArabidopsis[J]. Planta, 2007, 226: 647-654.

[36] Kim S G, Lee A K, Yoon H K, et al. A membrane-bound NAC transcription factor NTL8 regulates gibberellic acid-mediated salt signaling inArabidopsisseed germination [J]. Plant Journal, 2008, 55: 77-88.

[37] Yoon H K, Kim S G, Kim S Y, et al. Regulation of leaf senescence by NTL9-mediated osmotic stress signaling inArabidopsis[J]. Molecules and Cells, 2008, 25: 438-445.

[38] Seo P J, Park C M. A membrane-bound NAC transcription factor as an integrator of biotic and abiotic stress signals [J]. Plant Signaling & Behavior, 2010, 5: 481-483.

[39] De Clercq I, Vermeirssen V, Van Aken O, et al. The membrane-bound NAC transcription factor ANAC013 functions in mitochondrial retrograde regulation of the oxidative stress response inArabidopsis[J]. Plant Cell, 2013, 25: 3472-3490.

[40] Ng S, Ivanova A, Duncan O, et al. Membrane-bound NAC transcription factor, ANAC017, mediates mitochondrial retrograde signaling inArabidopsis[J]. Plant Cell, 2013, 25: 3450-3471.

[41] Wei K, Chen J, Wang Y, et al. Genome-wide analysis of bZIP- encoding genes in maize [J]. DNA Research, 2012, 19: 463-476.

[42] Jakoby M, Weisshaar B, Droge-Laser W, et al. bZIP transcription factors inArabidopsis[J]. Trends in Plant Science, 2002, 7: 106-111.

[43] Nijhawan A, Jain M, Tyagi A K, et al. Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice [J]. Plant Physiology, 2007, 146: 333-350.

[44] Liu C, Mao B, Ou S, et al. OsbZIP71, a bZIP transcription factor, confers salinity and drought tolerance in rice [J]. Plant Molecular Biology, 2014, 84: 19-36.

[45] Hsieh T H, Li C W, Su R C, et al. A tomato bZIP transcription factor, SlAREB, is involved in water deficit and salt stress response [J]. Planta, 2010, 231: 1459-1473.

[46] Cheng L, Li S, Hussain J, et al. Isolation and functional characterization of a salt responsive transcriptional factor, LrbZIP from lotus root (NelumbonuciferaGaertn) [J]. Molecular Biology Reports, 2013, 40: 4033-4045.

[47] Li Y, Sun Y, Yang Q, et al. Isolation and characterization of a gene fromMedicagosativaL., encoding a bZIP transcription factor [J]. Molecular Biology Reports, 2013, 40: 1227-1239.

[48] Ying S, Zhang D F, Fu J, et al. Cloning and characterization of a maize bZIP transcription factor, ZmbZIP72, confers drought and salt tolerance in transgenicArabidopsis[J]. Planta, 2012, 235: 253-266.

[49] Gao S Q, Chen M, Xu Z S, et al. The soybean GmbZIP1 transcription factor enhances multiple abiotic stress tolerances in transgenic plants [J]. Plant Molecular Biology, 2011, 75: 537-553.

[50] Yanez M, Caceres S, Orellana S, et al. An abiotic stress-responsive bZIP transcription factor from wild and cultivated tomatoes regulates stress-related genes [J]. Plant Cell Reports, 2009, 28: 1497-1507.

[51] Liao Y, Zhang J S, Chen S Y, et al. Role of soybean GmbZIP132 under abscisic acid and salt stresses [J]. Journal of Integrative Plant Biology, 2008, 50: 221-230.

[52] Liao Y, Zou H F, Wei W, et al. SoybeanGmbZIP44,GmbZIP62 andGmbZIP78 genes function as negative regulator of ABA signaling and confer salt and freezing tolerance in transgenicArabidopsis[J]. Planta, 2008, 228: 225-240.

[53] Kobayashi F, Maeta E, Terashima A, et al. Positive role of a wheat HvABI5 ortholog in abiotic stress response of seedlings [J]. Physiologia Plantarum, 2008, 134: 74-86.

[54] Zou M, Guan Y, Ren H, et al. A bZIP transcription factor, OsABI5, is involved in rice fertility and stress tolerance [J]. Plant Molecular Biology, 2008, 66: 675-683.

[55] Xiang Y, Tang N, Du H, et al. Characterization of OsbZIP23 as a key player of the basic leucine zipper transcription factor family for conferring abscisic acid sensitivity and salinity and drought tolerance in rice [J]. Plant Physiology, 2008, 148: 1938-1952.

[56] Zhang X, Wang L, Meng H, et al. Maize ABP9 enhances tolerance to multiple stresses in transgenicArabidopsisby modulating ABA signaling and cellular levels of reactive oxygen species [J]. Plant Molecular Biology, 2011, 75: 365-378.

[57] Tezuka K, Taji T, Hayashi T, et al. A novel abi5 allele reveals the importance of the conserved Ala in the C3 domain for regulation of downstream genes and salt tolerance during germination inArabidopsis[J]. Plant Signaling & Behavior, 2013, 8: e23455.

[58] Kim S, Kang J Y, Cho D I, et al. ABF2, an ABRE-binding bZIP factor, is an essential component of glucose signaling and its overexpression affects multiple stress tolerance [J]. Plant Journal, 2004, 40: 75-87.

[59] Yang O, Popova O V, Süthoff U, et al. TheArabidopsisbasic leucine zipper transcription factor AtbZIP24 regulates complex transcriptional networks involved in abiotic stress resistance [J]. Gene, 2009, 436: 45-55.

[60] Jindra M, Gaziova I, Uhlirova M, et al. Coactivator MBF1 preserves the redox-dependent AP-1 activity during oxidative stress inDrosophila[J]. EMBO Journal, 2004, 23: 3538-3547.

[61] Schütze K, Harter K, Chaban C. Post-translational regulation of plant bZIP factors [J]. Trends in Plant Science, 2008, 13: 247-255.

[62] Miller M. The importance of being flexible: the case of basic region leucine zipper transcriptional regulators [J]. Current Protein & Peptide Science, 2009, 10: 244-269.

[63] Muniz Garcia M N, Giammaria V, Grandellis C, et al. Characterization of StABF1, a stress-responsive bZIP transcription factor fromSolanumtuberosumL. that is phosphorylated by StCDPK2 in vitro [J].Planta, 2012, 235: 761-778.

[64] Yoshida T, Fujita Y, Sayama H, et al. AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation [J]. Plant Journal, 2010, 61: 672-685.

[65] Liu J X, Srivastava R, Howell S H. Stress-induced expression of an activated form of AtbZIP17 provides protection from salt stress inArabidopsis[J]. Plant Cell Environment, 2008, 31: 1735-1743.

[66] Srivastava R, Deng Y, Howell S H. Stress sensing in plants by an ER stress sensor/transducer, bZIP28 [J]. Frontiers in Plant Science, 2014, 5: 59.

[66] Toledo-Ortiz G, Huq E, Quail P H. TheArabidopsisbasic/helix-loop-helix transcription factor family [J]. Plant Cell, 2003, 15: 1749-1770.

[67] Sonnenfeld M J, Delvecchio C, Sun X. Analysis of the transcriptional activation domain of the Drosophila tango bHLH-PAS transcription factor [J]. Development Genes and Evolution, 2005, 215:221-229.

[68] Li X X, Duan X P, Jiang H X, et al. Genome-wide analysis of basic/helix-loop-helix transcription factor family in rice andArabidopsis[J]. Plant Physiology, 2006, 141: 1167-1184.

[69] Murre C, McCaw P S, Baltimore D. A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins [J]. Cell, 1989, 56: 777-783.

[70] Ferre-D'Amare A R, Pognonec P, Roeder R G, et al. Structure and function of the b/HLH/Z domain of USF [J]. EMBO Journal, 1994, 13:180-189.

[71] Chen L, Chen Y, Jiang J F, et al. The constitutive expression ofChrysanthemumdichrumICE1 inChrysanthemumgrandiflorumimproves the level of low temperature, salinity and drought tolerance [J]. Plant Cell Reports, 2012, 31: 1747-1758.

[72] Feng H L, Ma N N, Meng X, et al. A novel tomato MYC-type ICE1-like transcription factor, SlICE1a, confers cold, osmotic and salt tolerance in transgenic tobacco [J]. Plant Physiology and Biochemistry, 2013, 73: 309-320.

[73] Jiang Y, Yang B, Deyholos M K. Functional characterization of theArabidopsisbHLH92 transcription factor in abiotic stress [J]. Molecular Genetics and Genomics, 2009, 282: 503-516.

[74] Zhou J, Li F, Wang J L, et al. Basic helix-loop-helix transcription factor from wild rice (OrbHLH2) improves tolerance to salt- and osmotic stress inArabidopsis[J]. Journal of Plant Physiology, 2009, 166: 1296-1306.

[75] Li F, Guo S, Zhao Y, et al. Overexpression of a homopeptide repeat-containing bHLH protein gene (OrbHLH001) from Dongxiang Wild Rice confers freezing and salt tolerance in transgenicArabidopsis[J]. Plant Cell Reports, 2010, 29: 977-986.

[76] Chen Y, Li F, Ma Y, et al. Overexpression of OrbHLH001, a putative helix-loop-helix transcription factor, causes increased expression of AKT1 and maintains ionic balance under salt stress in rice [J]. Journal of Plant Physiology, 2013, 170: 93-100.

[77] Guan Q, Wu J, Yue X, et al. A nuclear calcium-sensing pathway is critical for gene regulation and salt stress tolerance inArabidopsis[J]. PLoS Genetics, 2013, 9: e1003755.

[78] Srivastava A K, Ramaswamy N K, Suprasanna P, et al. Genome- wide analysis of thiourea- modulated salinity stress-responsive transcripts in seeds ofBrassicajuncea: identification of signalling and effector components of stress tolerance [J]. Annals of Botany, 2010, 106: 663-674.

[79] Gruber V, Blanchet S, Diet A, et al. Identification of transcription factors involved in root apex responses to salt stress inMedicagotruncatula[J]. Molecular Genetics and Genomics, 2009, 281: 55-66.

[80] Wei B, Zhang R Z, Guo J J, et al. Genome-wide analysis of the MADS-box gene family inBrachypodiumdistachyon[J]. PLoS One, 2014, 9: e84781.

[81] Ji X Y, Wang Y C, Liu G F. Expression analysis of MYC genes fromTamarixhispidain response to different abiotic stresses [J]. International Journal of Molecular Sciences, 2012, 13: 1300-1313.

[82] Ma H S, Liang D, Shuai P, et al. The salt- and drought-inducible poplar GRAS protein SCL7 confers salt and drought tolerance inArabidopsisthaliana[J]. Journal of Experimental Botany, 2010, 61: 4011-4019.

[83] Corrales A R, Nebauer S G, Carrillo L, et al. Characterization of tomato cycling Dof factors reveals conserved and new functions in the control of flowering time and abiotic stress responses [J]. Journal of Experimental Botany, 2014, 65: 995-1012.

[84] El-Akhal M R, Rincón A, Coba de la Pena T, et al. Effects of salt stress and rhizobial inoculation on growth and nitrogen fixation of three peanut cultivars [J]. Plant Biolology, 2013, 15: 415-421.

[85] Greenway H, Munns R. Mechanisms of salt tolerance in nonhalophytes [J]. Annual Review of Plant Physiology, 1980, 31: 149-190.

[86] Nautiyal P C, Ravindra V, Joshi Y C. Germination and early seedling growth of some groundnut cultivars under salt stress [J]. Indian Journal of Plant Physiology, 1989, 32: 251-253.

[87] Janila P, Rao T N, Kumar A A. Germination and early seedling growth of groundnut (ArachishypogaeaL.) varieties under salt stress [J]. Annual Agriculture Research, 1999, 20: 180-182.

[88] Mensah J K, Akomeah P A, Ikhajiagbe B, et al. Effects of salinity on germination, growth and yield of five groundnut genotypes [J]. African Journal of Biotechnology, 2006, 5: 1973-1979.

[89] Singh A, Prasad R. Salt stress effects growth and cell wall bound enzymes inArachishypogaeaL. seedlings [J]. International Journal of Integrative Biology, 2009, 7: 118-123.

[90] Hammad S A R, Shaban K A, Tantawy M F. Studies on salinity tolerance of two peanut cultivars in relation to growth, leaf water content some chemical aspects and yield [J]. Journal of Applied Sciences Research, 2010, 6: 1517-1526.

[91] Taffouo V D, Meguekam T L, Ngueleumeni M L P, et al. Mineral nutrient status, some quality and morphological characteristic changes in peanut (ArachishypogaeaL.) cultivars under salt stress [J]. African Journal of Environmental Science and Technology, 2010, 4: 471-479.

[92] Qin L Q, Li L, Bi C, et al. Damaging mechanisms of chilling and salt stress toArachishypogaeaL. leaves [J]. Photosynthetica, 2011, 49: 37-42.

[93] Lauter D J, Meiri A. Peanut pod development in pegging and root zone salinized with sodium chloride [J]. Crop Science, 1990, 30: 660-664.

[94] Girdhar I K, Bhalodia P K, Misra J B, et al. Performance of groundnut,ArachishypogaeaL. as influenced by soil salinity and saline water irrigation in black clay soils [J]. Journal of Oilseeds Research, 2005, 22: 183-187.

[95] Chen N, Yang Q L, Su M W, et al. Cloning of six ERF family transcription factor genes from peanut and analysis of their expression during abiotic stress [J]. Plant Molecular Biology Reporter, 2012, 30: 1415-1425.

[96] Liu X, Liu S, Wu J, et al. Overexpression ofArachishypogaeaNAC3 in tobacco enhances dehydration and drought tolerance by increasing superoxide scavenging [J]. Plant Physiology and Biochemistry, 2013, 70: 354-359.

[97] Chen N, Yang Q L, Pan L J, et al. Identification of 30 MYB transcription factor genes and analysis of their expression during abiotic stress in peanut (ArachishypogaeaL.) [J]. Gene, 2014, 533: 332-345.

[98] Wan L, Wu Y, Huang J, et al. Identification of ERF genes in peanuts and functional analysis ofAhERF008 andAhERF019 in abiotic stress response [J]. Functional and Integrative Genomics, 2014, 14: 467-477.

[99] Pruthvi V, Narasimhan R, Nataraja K N. Simultaneous expression of abiotic stress responsive transcription factors,AtDREB2A,AtHB7 andAtABF3 improves salinity and drought tolerance in peanut [J]. PLoS One, 2014, 9: e111152.

[100] Sarkar T, Thankappan R, Kumar A, et al. Heterologous expression of theAtDREB1Agene in transgenic peanut conferred tolerance to drought and salinity stresses [J]. PloS One, 2014, 9: e110507.

2016-06-13

2014年国家“万人计划”青年拔尖人才；国家花生产业技术体系项目(CARS-14)；山东省自然科学基金项目(ZR2011CQ036；ZR2012CQ031；ZR2014YL011；ZR2014YL012)；国家自然科学基金项目(31000728; 31200211)；青岛市科技计划应用基础研究项目(11-2-4-9-(3)-jch; 12-1-4-11-(2)-jch)；青岛市民生计划项目(14-2-3-34-nsh)；山东省农业科学院青年科研基金项目(2016YQN14)；山东省农业科学院青年英才培养计划

陈娜(1979-)，女，山东蓬莱人，山东省花生研究所副研究员，博士，主要从事花生遗传育种研究。

参与植物盐胁迫调控的转录因子研究进展

陈 娜1，程 果2，王 冕1，杨 珍1，王 通1，陈明娜1，潘丽娟1，迟晓元1，禹山林1*

(1. 山东省花生研究所，山东 青岛 266100； 2. 青岛市出入境检验检疫局，山东 青岛 266001)

盐胁迫是影响植物生长、发育和作物产量的主要环境因子。在盐胁迫的响应和适应过程中，植物会产生许多生理生化反应，许多基因被激活，导致大量参与盐胁迫的蛋白质的积累。胁迫响应基因的表达主要由特定的转录因子(TF)调控，转录因子通常可以激活或抑制多个靶基因的转录。目前已发现多个胁迫响应的转录因子，对它们调控的基因启动子区的顺式作用元件也有很多研究。转录因子及其顺式作用元件不仅是基因表达的分子开关，而且在信号传导过程中是信号转导通路的终端。在这篇文章中，我们重点总结了参与植物盐胁迫调控的几类转录因子，包括NAC、bZIP和bHLH的研究进展。

转录因子；盐胁迫；调控机理；研究进展

S332.6；Q789

A

10.14001/j.issn.1002-4093.2016.03.008

*通讯作者：禹山林(1956-)，男，研究员，主要从事花生遗传育种研究。E-mail: yshanlin1956@163.com