Role and Function of Eethylene Response Factor in Different Plants under Multiple Biotic and Abiotic Stresses

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Bibliographic Information
Journal Pakistan Journal of Biochemistry and Biotechnology
Title Role and Function of Eethylene Response Factor in Different Plants under Multiple Biotic and Abiotic Stresses
Author(s) Akram, Rabia, Farah Deeba, Maryam Zain, Nadia Iqbal
Volume 1
Issue 1
Year 2020
Pages 1-19
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URL Link
Chicago 16th Akram, Rabia, Farah Deeba, Maryam Zain, Nadia Iqbal. "Role and Function of Eethylene Response Factor in Different Plants under Multiple Biotic and Abiotic Stresses." Pakistan Journal of Biochemistry and Biotechnology 1, no. 1 (2020).
APA 6th Akram, R., Deeba, F., Zain, M., Iqbal, N. (2020). Role and Function of Eethylene Response Factor in Different Plants under Multiple Biotic and Abiotic Stresses. Pakistan Journal of Biochemistry and Biotechnology, 1(1).
MHRA Akram, Rabia, Farah Deeba, Maryam Zain, Nadia Iqbal. 2020. 'Role and Function of Eethylene Response Factor in Different Plants under Multiple Biotic and Abiotic Stresses', Pakistan Journal of Biochemistry and Biotechnology, 1.
MLA Akram, Rabia, Farah Deeba, Maryam Zain, Nadia Iqbal. "Role and Function of Eethylene Response Factor in Different Plants under Multiple Biotic and Abiotic Stresses." Pakistan Journal of Biochemistry and Biotechnology 1.1 (2020). Print.
Harvard AKRAM, R., DEEBA, F., ZAIN, M., IQBAL, N. 2020. Role and Function of Eethylene Response Factor in Different Plants under Multiple Biotic and Abiotic Stresses. Pakistan Journal of Biochemistry and Biotechnology, 1.


These stresses effect crop production and quality, thus result is in economic lose and food insecurity. Many factors play vital role in regulating growth of plants along with developmental pathways during biotic and abiotic stresses. Transcription factors are proteins that control physiological, developmental and stress responses in plants. Ethylene response factors belong to the biggest family of transcription factors, known to participate in various stress tolerance like drought, heat, salt and cold. They are significant regulators of plant gene expression. The objective of this review is to present how ethylene response factor family proteins became the focus of stress tolerance as well as the development and growth of plants.


Role and function of Ethylene Response Factor in different plants under multiple biotic and abiotic Stresses

Rabia Akram1, Farah Deeba1, Maryam zain1, Nadia Iqbal1*

1Department of Biochemistry and Biotechnology, The Women University, Multan, Pakistan

*Corresponding Author:

Dr. Nadia Iqbal

Department of Biochemistry and Biotechnology, The Women University, Multan, Pakistan


Abiotic and biotic stresses are the causes of drastic changes in plants growth and development.

These stresses effect crop production and quality, thus result is in economic lose and food insecurity. Many factors play vital role in regulating growth of plants along with developmental pathways during biotic and abiotic stresses. Transcription factors are proteins that control physiological, developmental and stress responses in plants. Ethylene response factors belong to the biggest family of transcription factors, known to participate in various stress tolerance like drought, heat, salt and cold. They are significant regulators of plant gene expression. The objective of this review is to present how ethylene response factor family proteins became the focus of stress tolerance as well as the development and growth of plants.

Introduction of ethylene response factor gene

Plants are susceptible to several types of environmental stresses throughout their life cycle. Theseadverse environmental conditions, specifically high salt concentration, temperature, soil moisture affect the growth, development, yield and geological distribution of cultivated crops across the world and decrease possible crop productivity approximately to 70% (1).

Biotic stresses for example weeds, diseases and insects occur at variable extent which may not be relevant in a particular developmental stage but decrease plant productivity (2).One of the main objective of cop breeding program is development of stress tolerant crop (3). Several widespread abiotic stresses reported to take place around the world are salinity (4), drought (5), water logging, extreme temperatures (6), also nutrient deficiency (7).

A variety of defense mechanism like maintenance of membrane integrity, generation of antioxidants, hormone regulation, stimulation of stress proteins and carbon fixation rate have been found to work in plant. Various mechanisms in plant are governed involving particular genes for these stresses(8) and help plants to protect against a series of outside stresses during morphological adaptation (9). A large number of genes with diverse functions are induced or repressed when a plant is undergo to abiotic stresses. These genes encode for proteins which could be divided into two groups. One of them is primary group comprises functional proteins that is key enzymes for osmolytes biosynthesis like proline and sugar alcohols, molecular chaperones, and membrane transporters which are directly related to defense of plants from abiotic stress. The other groupcontains proteins that are regulatory in nature and control signal transduction and stress receptive gene expression and consists of a variety of transcription factors and protein kinases (10).

Transcription factors (TFs) that are regulatory proteins have a central part in initiatingdefense gene expression (11). They interact throughcis-acting components present in promoter region of various stress regulated genes and consequently start cascades or entire system of genes that perform together increased tolerance to various stresses at a time. Stress responsive transcription factors are strongtools for genetic engineering because their overexpression can result in either upregulation or downregulation of entire collection of genes under their control.A large number of transcription factors participate in plant stress tolerance and regulate plant responses to diverse stresses.InArabidopsis more than 1500 genes have reported to encode a various transcription factors(12). Some of the transcription factorsrelated to plant stress response are categorized into numerous large families for example AP2/ERF, NAC, bZIP, zinc-finger,MYB, MYC and WRKY (13).Eethylene responsive factoris the member of large gene family the APETALA2/Ethylene-Responsive Factor superfamily. This superfamily also include AP2as well as RAV family(12). This superfamily has characteristic AP2/ERF domain, which contains near about sixty to seventy amino acids. The families of AP2/ERF superfamily defined like, proteins of AP2 family have AP2/ERF domains which are two repeated domains, and proteins of ERF family consist of one domain that is AP2/ERF, whereasproteins of RAV family have a B3 domain. The ethylene response factor family isfurther divided into two distinctive subfamilies, one is CBF/DREB subfamily, second is ERF subfamily (14). The ERF region initially identified as conserved element in four proteins characterized in Nicotiana tabacum. These proteins are distinctive ethylene responsive element binding proteins, named ERF 1, 2, 3, 4 also found to interact with consensus promoter sequence GCC box which play role in ethylene responsive transcription of genes (15). The ERF subfamily proteins were classified into six sets, B-1 to B-6. Nakano et al., (16) studied the expression of various genes of ERF subfamily in various plants and their biological roles.

The ethylene responsive factors also governed by feedback mechanism and may be ethylene dependent or ethylene independent. Apart from regulation mechanism, ERFs expressions are regulated post-transcriptionally via micro RNAs, while expressions of miRNA are also regulated through ERFs. Ethylene responsive factors have found to involve as activator or various genes while it may act as repressor of various genes during of plants defense response averse to biotic stress condition (17). Ethylene responsive factors also defense role in fungal and bacterial diseases responses as well as during viral infection in plants (18). SERF1 overexpression enhanced tolerance of salinity through ROS stimulated MAPK indicating flow (19). TaERF1 in wheat was appeared in the direction of improve easiness to abiotic, also biotic stress conditions (20). AP2/EREBP family which are plant-specific TFs exposed by Arabidopsis mutational analysis, that were liable for enhance wax substance, decline stomatal density, changed cuticle premises in addition to the connected important raise in tolerance of drought Arabidopsis modified shine (21).

Ethylene response factors (ERF) are associated in stress tolerance in a number of species of plants(22), it was revealed that GhERF2, GhERF3 and GhERF6 can proceed as significant frequent components of various signaling pathways receptive to abiotic and biotic stresses. To advance identify with their activity, the development of transgenic plants overexpressing these genes is ongoing (23).


ERFs previously named ethylene response binding proteins denoted by ERE binding proteins. The ethylene responsive element proteins earliest extracted from plant Nicotiana tabacum(15). ERFs consist of a domain, AP2 DNA-binding region, as of a plant-definite fabulous family of 122 TFs in Arabidopsis. In genome of tomato, near 85 gene of ethylene responsive factors family protein stay uncharacterized (24). It is described that in various plants ERF domains product be present within several regulatory genes (25, 26) but is not present in fungi, yeast or mammalian (27). In the most recent decade, to a large extent, consideration have been accentuated on AP2/ERF large family. The hypothesis elucidates as the lateral gene movement of HNH-AP2 endonuclease originated from bacteria or virus into the host plant might bring about regenerate the AP2/ERF great family (28).

Functional diversity in plants

Up to now, Ethylene responsive TFs have been recognized as well as distinguished from numerous species of plants for example Arabidopsis (16), poplar (29), cotton (30), soybean (31), barley (32), maize (33), cucumber (34), apple, wheat (35), rice (36),sorghum (37), Medicago truncatula (38), also potato (39). Overall 147 genes in Arabidopsis, encoding AP2/ERF TFs, transcription factors named ERF encoded by 122 of these 147. ERF TFs of Arabidopsis may be divided into 12 groups different from each other, found on phylogenetic analysis, these groups named as I to X, VI-L,Xb-L (16).Functional diversity of ethylene response factor in different plants is given in table 1.


The ERF TFs take part in plants development procedures, in response to environmental stresses and hormone signaling (39). The ethylene response factor family has been comprehensively studied in recent times. In AP2/ERF domain b-sheet, 2 conserved amino acid residues distinguished ERF transcription factors, residues are 14th Ala as well as 19thAsp (14).ERF TFs allocate a conserved 58–59 amino acid domain (the ethylene response factor domain) and encompass sturdy capability to bind an extensive s rt of CREs within promoter of mark genes. From the cis-regulatory elements, DRE/CRT and GCC-box are the two chief DNA-binding elements (40). Most stimulatingly, numerous studies expose ERF proteins interconnect by DRE/CRT motif, a cis-acting element which acts in response to osmotic stress or cold (41), they build up defense by inter relating among stress-regulated genes (42).

The α-helix as well as β-sheet of ERF region identify the GCC box (called core cis-acting element AGCCGCC) of objective DNA on the ER promoter region (43). Pathogenesis-related (PR) genes are expressed by these GCC box elements (44). Additionally, the minority conservative elements of other than AP2 region grant transcriptional repression or activation in favor of particular gene, for example ERF connected amphiphilic oppression element that is EAR:DLNxxP (45), LWSY element (30)in addition to B3 oppression domain motif that is BRD:RLFGV (46). ERF protein either has homology resemblance with identified DNA joining proteins nor has fundamental zinc finger or leucine zipper elements, which propose ERF is a set of novel DNA binding proteins (43).Figure 1 gives classification and highlights functional association among AP2/ERFs in a variety of abiotic stress responses plants.

Role of ethylene response factor

Ethylene responsive factors take part essential regulatory tasks in various developmental processes and stress responses in plants. Genes of ERF family in an extensive array of plant types, were categorized into 8groups and 14 subgroups on the base of gene structures, conserved motifs, phylogenetic relationships, and biological functions. ERF genes, particularly in groups II as well as VII, may be utilized like contenders to develop crop resistance, for the reason that overexpression of ERF genes increases various disease resistance along with progresseasiness to drought, salt, freezing also in transgenic plant. The inclusive testing of phylogenetic correlations, conserved pattern, moreover physiological functions is beneficial in illuminating the biological roles of genes of ERF family in signal transduction, gene regulation along with defense response below stress environments (11).

ERF TFs have been revealed to be concerned in the regulation of expression of lipids, cell wall constituents, pathogenesis related genes, biosynthesis genes, basic type defense related genes, chitinase, osmotin, moreover b-1,3-glucanase encoding genes (28). Few of them are exposed to be concerned with in the control of plant reactions to biotic, also abiotic pressures by either activating or repressing abscisic acid responsive genes (47). Such as AtERF4 over-expression plant was a smaller amount of responsive to ABA suppressed root enlargement that entails negative control of ABA also ethylene reactions (48). The expression of ABA-responsive genes are repressed by AtERF7 that binds to the GCC box (49).ERF111 or ABR1 takes part as a negative controller of ABA reactions throughout seed germination, ABA and stress regulated gene expression (50) wherever as in Arabidopsis ABA hypersensitivity is conferred by transgenic plant, overexpressing AtERF13 (51). AtERF15 exposed on the way to proceed as a activist controller of ABA reactions (52). In contrast, ABA may also bring about the few ERF genes expression such as the expression of tomato ERF gene JERF1/3, cotton ERF gene GbERF in addition to tobacco ERF gene NtCEF1 has been revealed to be evoked by ABA (53).Sub group IX in IXERF subfamily accommodates 4 tiny ERFs through amino acids, varied as of 131-139. These tiny ethylene response fators named ERF95, ERF96, ERF97,ERF98. Additionally toward AP2/ERF area, these ethylene response factor have unfamiliarrole pattern termedCMIX-1 (16). In the group of these, ERF95 in addition called ethylene and salt inducible1 (ESE1), furthermore ERF98 have been exposed to concerned with the control of salt acceptance (54). In the past ERF97termed AtERF14, it has been revealed to control plants protection retort (55). In recent times ERF96 also has been revealed to regulate plant defense response (56).

Role of ERF during Stress

ERFs are concerned during the parameter of plant growth, expansion, metabolism as well as plant reactions to ecological stimulus like abiotic and biotic stresses (57). The ERF transcription factors are participated in the ethylene signaling pathway as well as directing in the direction of the expression of a variety of protection-associated genes, for example pathogenesis-related genes (40), abiotic stress receptive genes (58). The existence of a GCC-box or a dehydration responsive element/C-repeat element (DRE/CRT, CCGAC) situated in the promoter sequences of defense-related genes are involved in characterization of these genes (14). Figure 2 shows stress related genes expression, their role under stresses

Table 1: Examples of ERF family proteins involved in regulation of multiple abiotic stress responses in different plants.

Figure 1: AP2/ERF transcription factors in plants, their classification and their functions has also been reported.

Role of ERF during Stress

ERFs are concerned during the parameter of plant growth, expansion, metabolism as well as plant reactions to ecological stimulus likeabiotic and biotic stresses (57). The ERF transcription factors are participated in the ethylene signaling pathway as well as directing in the direction of the expression of a variety of protection-associated genes, for example pathogenesis-related genes (40), abiotic stress receptive genes (58). The existence of a GCC-box or a dehydration responsive element/C-repeat element (DRE/CRT, CCGAC) situated in the promoter sequences ofdefense-related genes are involved in characterization of these genes (14). Figure 2 shows stress related genes expression, their role under stresses.

Abiotic stress

Environmental stresses that are nutrient deficiency, drought, salinity, extreme temperatures and chemical toxicity, leads to a chain of physiological,morphological, molecular, and biochemical changes which negatively have an effect on plant development, yield and survival all-inclusive (59); (60), in responseto those stressesplants develop mechanisms. Plant feedbacks are multifarious, including extensivemetabolic and transcriptional events (61). The molecular and physiological studies of environmental stresses have proposed a familiar network of several signaling tracks that mediate salt, extreme temperatures and drought stress responses in plants (62). In abiotic stress responses the DREBs proteins are most extremelyconsidered ethylene response factor. Elements of the subfamily DREB1/CBFs are quickly induced in retort to chilly stress andget better tolerance to freezing when expressed ectopically, (63). Whereas,RNAi lines of Arabidopsis for CBF1 or CBF3 have decreased cold tolerance (64). The very fact, for freezing tolerance CBF2associated by quantitative trait locus (65), point out that DREB1/CBF genes are cold activated and in Arabidopsis are liable to be mainmonitor of reaction to wintry stress. Furthermorein Arabidopsis CBF2 abnormal gene communication has been revealed to retard leaf senescence, indicating that CBFs prop upchillysurvivalthrough deceleration down growth moreover delaying blossoming in coldnesstill temperatures raise in spring (66).

Figure 2: A representive model of process of abiotic or biotic stress tolerance in plants.

The subgroup of DREB2 contains eight elements in Arabidopsis, moreoverhomologs in the genetic material of numerous angiosperm families. Along with the components of the DREB2 subdivison, Arabidopsis DREB2A as well as DREB2B were induced in loss of water, heat and elevated saltiness in an ABA independent way (67). The abnormal gene expression of a constitutively dynamicstructure of DREB2A demonstrates developed forbearance to famine, heat and elevated salt stresses (67);(68) whereas DREB2A are furthersusceptible to temperature Shock (67). From rice or Arabidopsis several ERF-VII genes areexposed to be participated with in response to hypoxia as well assubmergence (69).In Arabidopsis RAP2.12 are constitutive ERF-VII factors, they arerecommended to proceed as prime triggers for the molecular feedback to insufficiency of oxygen (70); (71), that is then comforted at the oxygen deprivation activated ethylene response factors HRE1 also HRE2 (72). In submerged deepwater rice, SK1and SK2 motivate internodes elongation to effect clearance of the water level (73), whereas Sub1A promotes a quiescent strategy that allows carbohydrate saving and improves tolerance after flash-flood (74). A number of ERF genes from various plants have been exposed to confer various stress tolerance when expressed ectopically (75). This ‘unspecific’ effect may be explained by the activation of tolerance pathways whichreduce a generic stress statusfor example oxidative bursts generated as results of the primary stresses. Otherwise constitutive ERF expression could set the plant in a common alert state that fasten or expand the response when a specific stress is applied (28).

Biotic stress

ERFs are entailed inbiotic stress responses, ethylene response factor proteins initiallyextracted the same as transcription factors (TFs) whichconnect to promoter regions of stress-responsive genes. ERF genes assessed to date, are provoked through biotic stresses, consist of wounding, germ contagionstresses, such as transcription of basic type pathogenesis-related (PR) genes, defense-related genes,chitinase, osmotin, and b-1,3-glucanase activated by numerous ERFs. On the other hand, the group of target genes regulated by each ERF has not been entirelyrevealed. ERF1 as well as its homologs be associated to ERF-IX group, are possibly the ERF transcription factors whose participation in pathogen reaction in Arabidopsis has been most widely distinguished (76), as wella number ofproteins of ERF adjust ethylene biogenesis (77). Tobacco OPBP1 when expressed ectopically in transgenic rice increases resistance to pathogens (78).

Figure 3: Hormonal signalling and expression of genes in biotic stresses.


The existing information about various roles ofAP2/ERFs recommends that the members of this large superfamilycan be utilized for improving stress tolerancefor better crop yields. The members of this family can be employed in improving nutritional quality of grown varieties. Up to now extensiveadvancement has been done to know the functions ofAP2/ERFs,in response to various stresses. To develop multiple stress tolerant crops the members of this superfamily have been used.The plants genome sequencing projects have facilitated for recognition of ethylene response factors in different plants. It is stated that the proteins of ERF family has ability to confer resistance against numerous stresses in crop plant.


1. Agarwal, P. K.; Agarwal, P.; Reddy, M.; Sopory, S. K., Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant cell reports 2006, 25 (12), 1263-1274.

2. Yang, C.; Guo, W.; Li, G.; Gao, F.; Lin, S.; Zhang, T., QTLs mapping for Verticillium wilt resistance at seedling and maturity stages in Gossypium barbadense L. Plant Science 2008, 174 (3), 290-298.

3. Fritsche-Neto, R.; Borém, A. Plant breeding for biotic stress resistance; Springer: 2012.

4. Shrivastava, P.; Kumar, R., Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi journal of biological sciences 2015, 22 (2), 123-131.

5. Aroca, R.; Ruiz-Lozano, J. M., Regulation of root water uptake under drought stress conditions. In Plant responses to drought stress, Springer: 2012; pp 113-127.

6. Theocharis, A.; Clément, C.; Barka, E. A., Physiological and molecular changes in plants grown at low temperatures. Planta 2012, 235 (6), 1091-1105.

7. Liang, C.; Tian, J.; Liao, H., Proteomics dissection of plant responses to mineral nutrient deficiency. Proteomics 2013, 13 (3-4), 624-636.

8. Khan, A.; Pan, X.; Najeeb, U.; Tan, D. K. Y.; Fahad, S.; Zahoor, R.; Luo, H., Coping with drought: stress and adaptive mechanisms, and management through cultural and molecular alternatives in cotton as vital constituents for plant stress resilience and fitness. Biological research 2018, 51 (1), 47.

9. Boudsocq, M.; Laurière, C., Osmotic signaling in plants. Multiple pathways mediated by emerging kinase families. Plant physiology 2005, 138 (3), 1185-1194.

10. Lata, C.; Prasad, M., Role of DREBs in regulation of abiotic stress responses in plants. Journal of experimental botany 2011, 62 (14), 4731-4748.

11. Xu, Z.-S.; Chen, M.; Li, L.-C.; Ma, Y.-Z., Functions of the ERF transcription factor family in plants. Botany 2008, 86 (9), 969-977.

12. Riechmann, J. L.; Heard, J.; Martin, G.; Reuber, L.; Jiang, C.-Z.; Keddie, J.; Adam, L.; Pineda, O.; Ratcliffe, O.; Samaha, R., Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 2000, 290 (5499), 2105-2110.

13. Umezawa, T.; Fujita, M.; Fujita, Y.; Yamaguchi-Shinozaki, K.; Shinozaki, K., Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. Current opinion in biotechnology 2006, 17 (2), 113-122.

14. Sakuma, Y.; Liu, Q.; Dubouzet, J. G.; Abe, H.; Shinozaki, K.; Yamaguchi-Shinozaki, K., DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration-and cold-inducible gene expression. Biochemical and biophysical research communications 2002, 290 (3), 998-1009.

15. Ohme-Takagi, M.; Shinshi, H., Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. The Plant Cell 1995, 7 (2), 173-182.

16. Nakano, T.; Suzuki, K.; Fujimura, T.; Shinshi, H., Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant physiology 2006, 140 (2), 411-432.

17. Maruyama, Y.; Yamoto, N.; Suzuki, Y.; Chiba, Y.; Yamazaki, K.-i.; Sato, T.; Yamaguchi, J., The Arabidopsis transcriptional repressor ERF9 participates in resistance against necrotrophic fungi. Plant science 2013, 213, 79-87.

18. Chen, T.; Lv, Y.; Zhao, T.; Li, N.; Yang, Y.; Yu, W.; He, X.; Liu, T.; Zhang, B., Comparative transcriptome profiling of a resistant vs. susceptible tomato (Solanum lycopersicum) cultivar in response to infection by tomato yellow leaf curl virus. PloS one 2013, 8 (11).

19. Schmidt, R.; Mieulet, D.; Hubberten, H.-M.; Obata, T.; Hoefgen, R.; Fernie, A. R.; Fisahn, J.; San Segundo, B.; Guiderdoni, E.; Schippers, J. H., SALT-RESPONSIVE ERF1 regulates reactive oxygen species–dependent signaling during the initial response to salt stress in rice. The Plant Cell 2013, 25 (6), 2115-2131.

20. Xu, Z.-S.; Xia, L.-Q.; Chen, M.; Cheng, X.-G.; Zhang, R.-Y.; Li, L.-C.; Zhao, Y.-X.; Lu, Y.; Ni, Z.-Y.; Liu, L., Isolation and molecular characterization of the Triticum aestivum L. ethylene-responsive factor 1 (TaERF1) that increases multiple stress tolerance. Plant molecular biology 2007, 65 (6), 719-732.

21. Aharoni, A.; Dixit, S.; Jetter, R.; Thoenes, E.; van Arkel, G.; Pereira, A., The SHINE clade of AP2 domain transcription factors activates wax biosynthesis, alters cuticle properties, and confers drought tolerance when overexpressed in Arabidopsis. The Plant Cell 2004, 16 (9), 2463-2480.

22. Ashraf, J.; Zuo, D.; Wang, Q.; Malik, W.; Zhang, Y.; Abid, M. A.; Cheng, H.; Yang, Q.; Song, G., Recent insights into cotton functional genomics: progress and future perspectives. Plant biotechnology journal 2018, 16 (3), 699-713.

23. Zhou, J.; Tang, X.; Martin, G. B., The Pto kinase conferring resistance to tomato bacterial speck disease interacts with proteins that bind a cis‐element of pathogenesis‐related genes. The EMBO Journal 1997, 16 (11), 3207-3218.

24. Jin, L. G.; Li, H.; Liu, J. Y., Molecular characterization of three ethylene responsive element binding factor genes from cotton. Journal of integrative plant biology 2010, 52 (5), 485-495.

25. Sharma, M. K.; Kumar, R.; Solanke, A. U.; Sharma, R.; Tyagi, A. K.; Sharma, A. K., Identification, phylogeny, and transcript profiling of ERF family genes during development and abiotic stress treatments in tomato. Molecular Genetics and Genomics 2010, 284 (6), 455-475.

26. Okamuro, J. K.; Caster, B.; Villarroel, R.; Van Montagu, M.; Jofuku, K. D., The AP2 domain of APETALA2 defines a large new family of DNA binding proteins in Arabidopsis. Proceedings of the National Academy of Sciences 1997, 94 (13), 7076-7081.

27. Weigel, D., The APETALA2 domain is related to a novel type of DNA binding domain. The Plant Cell 1995, 7 (4), 388.

28. Licausi, F.; Ohme‐Takagi, M.; Perata, P., APETALA 2/Ethylene Responsive Factor (AP 2/ERF) transcription factors: Mediators of stress responses and developmental programs. New Phytologist 2013, 199 (3), 639-649.

29. Zhuang, J.; Cai, B.; Peng, R.-H.; Zhu, B.; Jin, X.-F.; Xue, Y.; Gao, F.; Fu, X.-Y.; Tian, Y.-S.; Zhao, W., Genome-wide analysis of the AP2/ERF gene family in Populus trichocarpa. Biochemical and biophysical research communications 2008, 371 (3), 468-474.

30. Jin, L.-G.; Liu, J.-Y., Molecular cloning, expression profile and promoter analysis of a novel ethylene responsive transcription factor gene GhERF4 from cotton (Gossypium hirstum). Plant Physiology and Biochemistry 2008, 46 (1), 46-53.

31. Zhang, G.; Chen, M.; Chen, X.; Xu, Z.; Guan, S.; Li, L.-C.; Li, A.; Guo, J.; Mao, L.; Ma, Y., Phylogeny, gene structures, and expression patterns of the ERF gene family in soybean (Glycine max L.). Journal of experimental botany 2008, 59 (15), 4095-4107.

32. Gil-Humanes, J.; Pistón, F.; Martín, A.; Barro, F., Comparative genomic analysis and expression of the APETALA2-like genes from barley, wheat, and barley-wheat amphiploids. BMC plant biology 2009, 9 (1), 66.

33. Zhuang, J.; Deng, D.-X.; Yao, Q.-H.; Zhang, J.; Xiong, F.; Chen, J.-M.; Xiong, A.-S., Discovery, phylogeny and expression patterns of AP2-like genes in maize. Plant Growth Regulation 2010, 62 (1), 51-58.

34. Hu, L.; Liu, S., Genome-wide identification and phylogenetic analysis of the ERF gene family in cucumbers. Genetics and Molecular Biology 2011, 34 (4), 624-634.

35. Zhuang, J.; Chen, J.-M.; Yao, Q.-H.; Xiong, F.; Sun, C.-C.; Zhou, X.-R.; Zhang, J.; Xiong, A.-S., Discovery and expression profile analysis of AP2/ERF family genes from Triticum aestivum. Molecular biology reports 2011, 38 (2), 745-753.

36. Rashid, M.; Guangyuan, H.; Guangxiao, Y.; Hussain, J.; Xu, Y., AP2/ERF transcription factor in rice: genome-wide canvas and syntenic relationships between monocots and eudicots. Evolutionary Bioinformatics 2012, 8, EBO. S9369.

37. Yan, H.; Hong, L.; Zhou, Y.; Jiang, H.; Zhu, S.; Fan, J.; Cheng, B., A genome-wide analysis of the ERF gene family in sorghum. Genet Mol Res 2013, 12 (2), 2038-2055.

38. Zhang, H.; Zhang, J.; Quan, R.; Pan, X.; Wan, L.; Huang, R., EAR motif mutation of rice OsERF3 alters the regulation of ethylene biosynthesis and drought tolerance. Planta 2013, 237 (6), 1443-1451.

39. Charfeddine, M.; Saïdi, M. N.; Charfeddine, S.; Hammami, A.; Bouzid, R. G., Genome-wide analysis and expression profiling of the ERF transcription factor family in potato (Solanum tuberosum L.). Molecular biotechnology 2015, 57 (4), 348-358.

40. Zarei, A.; Körbes, A. P.; Younessi, P.; Montiel, G.; Champion, A.; Memelink, J., Two GCC boxes and AP2/ERF-domain transcription factor ORA59 in jasmonate/ethylene-mediated activation of the PDF1. 2 promoter in Arabidopsis. Plant molecular biology 2011, 75 (4-5), 321-331.

41. Lee, J.-H.; Hong, J.-P.; Oh, S.-K.; Lee, S.; Choi, D.; Kim, W., The ethylene-responsive factor like protein 1 (CaERFLP1) of hot pepper (Capsicum annuum L.) interacts in vitro with both GCC and DRE/CRT sequences with different binding affinities: possible biological roles of CaERFLP1 in response to pathogen infection and high salinity conditions in transgenic tobacco plants. Plant molecular biology 2004, 55 (1), 61-81.

42. Shoji, T.; Mishima, M.; Hashimoto, T., Divergent DNA-binding specificities of a group of ETHYLENE RESPONSE FACTOR transcription factors involved in plant defense. Plant physiology 2013, 162 (2), 977-990.

43. Hao, D.; Ohme-Takagi, M.; Sarai, A., Unique mode of GCC box recognition by the DNA-binding domain of ethylene-responsive element-binding factor (ERF domain) in plant. Journal of Biological Chemistry 1998, 273 (41), 26857-26861.

44. Wan, L.; Wu, Y.; Huang, J.; Dai, X.; Lei, Y.; Yan, L.; Jiang, H.; Zhang, J.; Varshney, R. K.; Liao, B., Identification of ERF genes in peanuts and functional analysis of AhERF008 and AhERF019 in abiotic stress response. Functional & integrative genomics 2014, 14 (3), 467-477.

45. Hiratsu, K.; Matsui, K.; Koyama, T.; Ohme‐Takagi, M., Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis. The Plant Journal 2003, 34 (5), 733-739.

46. Ikeda, M.; Ohme-Takagi, M., A novel group of transcriptional repressors in Arabidopsis. Plant and cell physiology 2009, 50 (5), 970-975.

47. Mizoi, J.; Ohori, T.; Moriwaki, T.; Kidokoro, S.; Todaka, D.; Maruyama, K.; Kusakabe, K.; Osakabe, Y.; Shinozaki, K.; Yamaguchi-Shinozaki, K., GmDREB2A; 2, a canonical DEHYDRATION-RESPONSIVE ELEMENT-BINDING PROTEIN2-type transcription factor in soybean, is posttranslationally regulated and mediates dehydration-responsive element-dependent gene expression. Plant physiology 2013, 161 (1), 346-361.

48. Yang, Z.; Tian, L.; Latoszek-Green, M.; Brown, D.; Wu, K., Arabidopsis ERF4 is a transcriptional repressor capable of modulating ethylene and abscisic acid responses. Plant molecular biology 2005, 58 (4), 585-596.

49. Zhang, H.; Li, W.; Chen, J.; Yang, Y.; Zhang, Z.; Zhang, H.; Wang, X.-C.; Huang, R., Transcriptional activator TSRF1 reversely regulates pathogen resistance and osmotic stress tolerance in tobacco. Plant molecular biology 2007, 63 (1), 63-71.

50. Pandey, G. K.; Grant, J. J.; Cheong, Y. H.; Kim, B. G.; Li, L.; Luan, S., ABR1, an APETALA2-domain transcription factor that functions as a repressor of ABA response in Arabidopsis. Plant Physiology 2005, 139 (3), 1185-1193.

51. Lee, S.-j.; Park, J. H.; Lee, M. H.; Yu, J.-h.; Kim, S. Y., Isolation and functional characterization of CE1 binding proteins. BMC plant biology 2010, 10 (1), 277.

52. Lee, S.-b.; Lee, S.-j.; Kim, S. Y., AtERF15 is a positive regulator of ABA response. Plant cell reports 2015, 34 (1), 71-81.

53. Lee, J.-H.; Kim, D.-M.; Lee, J. H.; Kim, J.; Bang, J. W.; Kim, W. T.; Pai, H.-S., Functional characterization of NtCEF1, an AP2/EREBP-type transcriptional activator highly expressed in tobacco callus. Planta 2005, 222 (2), 211-224.

54. Zhang, Z.; Wang, J.; Zhang, R.; Huang, R., The ethylene response factor AtERF98 enhances tolerance to salt through the transcriptional activation of ascorbic acid synthesis in Arabidopsis. The Plant Journal 2012, 71 (2), 273-287.

55. Oñate-Sánchez, L.; Anderson, J. P.; Young, J.; Singh, K. B., AtERF14, a member of the ERF family of transcription factors, plays a nonredundant role in plant defense. Plant Physiology 2007, 143 (1), 400-409.

56. Catinot, J.; Huang, J. B.; Huang, P. Y.; Tseng, M. Y.; Chen, Y. L.; Gu, S. Y.; Lo, W. S.; Wang, L. C.; Chen, Y. R.; Zimmerli, L., ETHYLENE RESPONSE FACTOR 96 positively regulates A rabidopsis resistance to necrotrophic pathogens by direct binding to GCC elements of jasmonate–and ethylene‐responsive defence genes. Plant, cell & environment 2015, 38 (12), 2721-2734.

57. Müller, M.; Munné-Bosch, S., Ethylene response factors: a key regulatory hub in hormone and stress signaling. Plant physiology 2015, 169 (1), 32-41.

58. Park, J. M.; Park, C.-J.; Lee, S.-B.; Ham, B.-K.; Shin, R.; Paek, K.-H., Overexpression of the tobacco Tsi1 gene encoding an EREBP/AP2–type transcription factor enhances resistance against pathogen attack and osmotic stress in tobacco. The Plant Cell 2001, 13 (5), 1035-1046.

59. Huang, G.-T.; Ma, S.-L.; Bai, L.-P.; Zhang, L.; Ma, H.; Jia, P.; Liu, J.; Zhong, M.; Guo, Z.-F., Signal transduction during cold, salt, and drought stresses in plants. Molecular biology reports 2012, 39 (2), 969-987.

60. Sharma, R.; De Vleesschauwer, D.; Sharma, M. K.; Ronald, P. C., Recent advances in dissecting stress-regulatory crosstalk in rice. Molecular Plant 2013, 6 (2), 250-260.

61. Zhu, J.-K., Cell signaling under salt, water and cold stresses. Current opinion in plant biology 2001, 4 (5), 401-406.

62. Kang, Y.; Khan, S.; Ma, X., Climate change impacts on crop yield, crop water productivity and food security–A review. Progress in natural Science 2009, 19 (12), 1665-1674.

63. Kasuga, M.; Liu, Q.; Miura, S.; Yamaguchi-Shinozaki, K.; Shinozaki, K., Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nature biotechnology 1999, 17 (3), 287-291.

64. Maruyama, K.; Takeda, M.; Kidokoro, S.; Yamada, K.; Sakuma, Y.; Urano, K.; Fujita, M.; Yoshiwara, K.; Matsukura, S.; Morishita, Y., Metabolic pathways involved in cold acclimation identified by integrated analysis of metabolites and transcripts regulated by DREB1A and DREB2A. Plant physiology 2009, 150 (4), 1972-1980.

65. Alonso-Blanco, C.; Gomez-Mena, C.; Llorente, F.; Koornneef, M.; Salinas, J.; Martínez-Zapater, J. M., Genetic and molecular analyses of natural variation indicate CBF2 as a candidate gene for underlying a freezing tolerance quantitative trait locus in Arabidopsis. Plant Physiology 2005, 139 (3), 1304-1312.

66. Sharabi-Schwager, M.; Lers, A.; Samach, A.; Guy, C. L.; Porat, R., Overexpression of the CBF2 transcriptional activator in Arabidopsis delays leaf senescence and extends plant longevity. Journal of experimental botany 2010, 61 (1), 261-273.

67. Sakuma, Y.; Maruyama, K.; Osakabe, Y.; Qin, F.; Seki, M.; Shinozaki, K.; Yamaguchi-Shinozaki, K., Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. The Plant Cell 2006, 18 (5), 1292-1309.

68. Sakuma, Y.; Maruyama, K.; Qin, F.; Osakabe, Y.; Shinozaki, K.; Yamaguchi-Shinozaki, K., Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proceedings of the National Academy of Sciences 2006, 103 (49), 18822-18827.

69. Hinz, M.; Wilson, I. W.; Yang, J.; Buerstenbinder, K.; Llewellyn, D.; Dennis, E. S.; Sauter, M.; Dolferus, R., Arabidopsis RAP2. 2: an ethylene response transcription factor that is important for hypoxia survival. Plant physiology 2010, 153 (2), 757-772.

70. Gibbs, D. J.; Lee, S. C.; Isa, N. M.; Gramuglia, S.; Fukao, T.; Bassel, G. W.; Correia, C. S.; Corbineau, F.; Theodoulou, F. L.; Bailey-Serres, J., Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants. Nature 2011, 479 (7373), 415-418.

71. Licausi, F.; Kosmacz, M.; Weits, D. A.; Giuntoli, B.; Giorgi, F. M.; Voesenek, L. A.; Perata, P.; van Dongen, J. T., Oxygen sensing in plants is mediated by an N-end rule pathway for protein destabilization. Nature 2011, 479 (7373), 419-422.

72. Licausi, F.; Van Dongen, J. T.; Giuntoli, B.; Novi, G.; Santaniello, A.; Geigenberger, P.; Perata, P., HRE1 and HRE2, two hypoxia‐inducible ethylene response factors, affect anaerobic responses in Arabidopsis thaliana. The Plant Journal 2010, 62 (2), 302-315.

73. Hattori, Y.; Nagai, K.; Furukawa, S.; Song, X.-J.; Kawano, R.; Sakakibara, H.; Wu, J.; Matsumoto, T.; Yoshimura, A.; Kitano, H., The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature 2009, 460 (7258), 1026-1030.

74. Xu, K.; Xu, X.; Fukao, T.; Canlas, P.; Maghirang-Rodriguez, R.; Heuer, S.; Ismail, A. M.; Bailey-Serres, J.; Ronald, P. C.; Mackill, D. J., Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 2006, 442 (7103), 705-708.

75. Mito, T.; Seki, M.; Shinozaki, K.; Ohme‐Takagi, M.; Matsui, K., Generation of chimeric repressors that confer salt tolerance in Arabidopsis and rice. Plant Biotechnology Journal 2011, 9 (7), 736-746.

76. Moffat, C. S.; Ingle, R. A.; Wathugala, D. L.; Saunders, N. J.; Knight, H.; Knight, M. R., ERF5 and ERF6 play redundant roles as positive regulators of JA/Et-mediated defense against Botrytis cinerea in Arabidopsis. PloS one 2012, 7 (4).

77. Li, Z.; Zhang, L.; Yu, Y.; Quan, R.; Zhang, Z.; Zhang, H.; Huang, R., The ethylene response factor AtERF11 that is transcriptionally modulated by the bZIP transcription factor HY5 is a crucial repressor for ethylene biosynthesis in Arabidopsis. The Plant Journal 2011, 68 (1), 88-99.

78. Chen, X.; Guo, Z., Tobacco OPBP1 enhances salt tolerance and disease resistance of transgenic rice. International journal of molecular sciences 2008, 9 (12), 2601-2613.

79. Rong, W.; Qi, L.; Wang, A.; Ye, X.; Du, L.; Liang, H.; Xin, Z.; Zhang, Z., The ERF transcription factor Ta ERF 3 promotes tolerance to salt and drought stresses in wheat. Plant biotechnology journal 2014, 12 (4), 468-479.

80. Scarpeci, T. E.; Frea, V. S.; Zanor, M. I.; Valle, E. M., Overexpression of AtERF019 delays plant growth and senescence, and improves drought tolerance in Arabidopsis. Journal of experimental botany 2017, 68 (3), 673-685.

81. Pellegrineschi, A.; Reynolds, M.; Pacheco, M.; Brito, R. M.; Almeraya, R.; Yamaguchi-Shinozaki, K.; Hoisington, D., Stress-induced expression in wheat of the Arabidopsis thaliana DREB1A gene delays water stress symptoms under greenhouse conditions. Genome 2004, 47 (3), 493-500.

82. Trujillo, L. E.; Menéndez, C.; Ochogavía, M. E.; Hernández, I.; Borrás, O.; Rodríguez, R.; Coll, Y.; Arrieta, J. G.; Banguela, A.; Ramírez, R., Engineering drought and salt tolerance in plants using SodERF3, a novel sugarcane ethylene responsive factor. Biotecnología Aplicada 2009, 26 (2), 168-171.

83. Joo, J.; Choi, H. J.; Lee, Y. H.; Kim, Y.-K.; Song, S. I., A transcriptional repressor of the ERF family confers drought tolerance to rice and regulates genes preferentially located on chromosome 11. Planta 2013, 238 (1), 155-170.

84. Song, C.-P.; Agarwal, M.; Ohta, M.; Guo, Y.; Halfter, U.; Wang, P.; Zhu, J.-K., Role of an Arabidopsis AP2/EREBP-type transcriptional repressor in abscisic acid and drought stress responses. The Plant Cell 2005, 17 (8), 2384-2396.

85. Zhai, Y.; Li, J.-W.; Li, X.-W.; Lei, T.-T.; Yan, F.; Zhao, Y.; Li, Y.-J.; Su, L.-T.; Wang, Y.; Wang, Q.-Y., Isolation and characterization of a novel transcriptional repressor GmERF6 from soybean. Biologia plantarum 2013, 57 (1), 26-32.

86. Upadhyay, R. K.; Gupta, A.; Ranjan, S.; Singh, R.; Pathre, U. V.; Nath, P.; Sane, A. P., The EAR motif controls the early flowering and senescence phenotype mediated by over-expression of SlERF36 and is partly responsible for changes in stomatal density and photosynthesis. PloS one 2014, 9 (7).

87. Bi, H.; Yang, B., Gene editing with TALEN and CRISPR/Cas in rice. In Progress in molecular biology and translational science, Elsevier: 2017; Vol. 149, pp 81-98.

88. Li, J.; Meng, X.; Zong, Y.; Chen, K.; Zhang, H.; Liu, J.; Li, J.; Gao, C., Gene replacements and insertions in rice by intron targeting using CRISPR–Cas9. Nature plants 2016, 2 (10), 1-6.

89. Hoang, T. M. L.; Tran, T. N.; Nguyen, T. K. T.; Williams, B.; Wurm, P.; Bellairs, S.; Mundree, S., Improvement of salinity stress tolerance in rice: challenges and opportunities. Agronomy 2016, 6 (4), 54.

90. Shen, C.; Que, Z.; Xia, Y.; Tang, N.; Li, D.; He, R.; Cao, M., Knock out of the annexin gene OsAnn3 via CRISPR/Cas9-mediated genome editing decreased cold tolerance in rice. Journal of Plant Biology 2017, 60 (6), 539-547.

91. Mao, Y.; Zhang, Z.; Feng, Z.; Wei, P.; Zhang, H.; Botella, J. R.; Zhu, J. K., Development of germ‐line‐specific CRISPR‐Cas9 systems to improve the production of heritable gene modifications in Arabidopsis. Plant biotechnology journal 2016, 14 (2), 519-532.

92. Fan, W.; Hai, M.; Guo, Y.; Ding, Z.; Tie, W.; Ding, X.; Yan, Y.; Wei, Y.; Liu, Y.; Wu, C., The ERF transcription factor family in cassava: genome-wide characterization and expression analyses against drought stress. Scientific reports 2016, 6, 37379.

93. Liu, J.; Wang, F.; Yu, G.; Zhang, X.; Jia, C.; Qin, J.; Pan, H., Functional analysis of the maize C-repeat/DRE motif-binding transcription factor CBF3 promoter in response to abiotic stress. International journal of molecular sciences 2015, 16 (6), 12131-12146.

94. Wang, Z.; Zhang, N.; Zhou, X.; Fan, Q.; Si, H.; Wang, D., Isolation and characterization of StERF transcription factor genes from potato (Solanum tuberosum L.). Comptes rendus biologies 2015, 338 (4), 219-226.

95. Klay, I.; Pirrello, J.; Riahi, L.; Bernadac, A.; Cherif, A.; Bouzayen, M.; Bouzid, S., Ethylene response factor Sl-ERF. B. 3 is responsive to abiotic stresses and mediates salt and cold stress response regulation in tomato. The Scientific World Journal 2014, 2014.

96. Li, R.; Zhang, L.; Wang, L.; Chen, L.; Zhao, R.; Sheng, J.; Shen, L., Reduction of tomato-plant chilling tolerance by CRISPR–Cas9-mediated SlCBF1 mutagenesis. Journal of agricultural and food chemistry 2018, 66 (34), 9042-9051.