Advances in Agriculture

Advances in Agriculture / 2014 / Article

Review Article | Open Access

Volume 2014 |Article ID 587070 | 7 pages |

Genes Acting on Transcriptional Control during Abiotic Stress Responses

Academic Editor: Mahmut Tör
Received30 Apr 2014
Revised17 Jul 2014
Accepted22 Jul 2014
Published25 Aug 2014


Abiotic stresses are the major cause of yield loss in crops around the world. Greater genetic gains are possible by combining the classical genetic improvement with advanced molecular biology techniques. The understanding of mechanisms triggered by plants to meet conditions of stress is of fundamental importance for the elucidation of these processes. Current genetically modified crops help to mitigate the effects of these stresses, increasing genetic gains in order to supply the agricultural market and the demand for better quality food throughout the world. To obtain safe genetic modified organisms for planting and consumption, a thorough grasp of the routes and genes that act in response to these stresses is necessary. This work was developed in order to collect important information about essential TF gene families for transcriptional control under abiotic stress responses.

1. Introduction

Plant breeding is “the art and science of changing the characteristics of the plant in order to produce desired characteristics” and has been successfully practiced since of the beginning of civilization [1, 2]. Currently, their priorities and focus are the increase of yield in the same area. With population growth, the demand for food is increasing. However, large and small crop yields oscillate annually, because of several abiotic stresses, causing the increase in world food prices and food deficit.

In some developmental stage, a stress or a combination of abiotic stresses can cause irreversible damage to plants. In rice, for example, cold can be drastically harmful during grain filling, depending on the temperature and time of exposure [3]. Also, water restriction at flowering can significantly reduce grain production in wheat cultivars [4]. Salinity, at higher concentrations, can inhibit germination and reduce the production of biomass, whereas low soil pH can lead to accumulation and mineral imbalance, all greatly affecting yield [5].

Abiotic stresses lead to a series of morphological and physiological, biochemical, and molecular changes that dramatically affect plant productivity [6]. In field conditions, a stress is always associated with other stress. For example, aluminum toxicity is always associated with other mineral imbalance [7, 8] and drought in most cases is associated with heat or salinity [9]. When plants receive any sign of stress, signaling is activated in the membrane, which will awake different intermediate stress genes. These genes could be members of the MAP Kinase cascade, or calcium-dependent, which has the function to activate transcription factors that will bind to different types of protective genes [10, 11]. These protective genes will drive the accumulation of macromolecular and damage repair proteins, cellular protection protein, osmotic homeostasis, and/or ionic homeostasis proteins. Many of these will be performing excretion of metals to the apoplast or reallocation of ions that can be found in excess; others will modulate proteins that lose their function in stress without the aid of these modulators. Other genes will provide the accumulation of osmoprotectants to prevent the loss of water; finally, we can see that a very large number of genes will act against abiotic stresses. Drought, salinity, high temperature, and oxidative stress are often interconnected and may induce cell damage and even, in this case, denaturation of structural and functional proteins [12]. Similarly, genes that act against these stresses have a specific regulation; however, they usually induce the same defense response [1214].

Genes linked to the processes of abiotic stresses tolerance are divided into three classes: genes involved in signaling cascades and transcriptional control, the genes that have direct roles in the protection of membranes and proteins, and genes involved in ion uptake and transport [12, 13].

Many reports involving genetic expression and transformation have been conducted mainly with model plants, in order to obtain better tolerance to abiotic stresses. These are of great importance, because it is possible to have a better understanding of the defense mechanisms that plants may have facing a stressful condition and thus increase crop productivity, avoiding losses to farmers and consumers.

Thus, this review will report the main families of transcription factors that act against abiotic stresses, covering a paramount process of mechanism defense that is responsible for the activation of pretranscription protection responses.

2. Transcription Factors

Transcription factors (TFs) are commonly defined as proteins that recognize and bind, alone or with the interaction of other proteins, DNA sequences of promoters, to regulate transcription, by activating or inhibiting the expression of particular genes [15]. They interact with cis-acting elements in the promoter region of genes, activating or disabling the transcription, therefore regulating gene expression. TFs are ranked and grouped into families according to their DNA binding conserved domain. However, those TFs who do not own conserved domains but interact with TFs with domains to form transcriptional complexes are also described as transcription factors [15].

With the sequencing of the A. thaliana genome [16], nearly 2000 TFs divided into ca. 30 families could be identified, half of them being unique to plants [17, 18]. This number is much higher than in animals [19] supporting the idea that transcriptional regulation in plants is much more significant than in animals and humans. There is about 1500 TF involved in stress response, corroborating with the idea that the transcriptional regulation involved in abiotic stress in plants is extremely complex [20]. It is known that there are several pathways that respond independently to environmental stresses, suggesting an intricate gene regulatory network [21]. But it is known that a large number of TFs that are involved in abiotic stress responses function independently. Thus, this review will focus on these TF families, as well as their use in crop improvement programs, through engineering stress technology.

2.1. Zinc-Finger (ZFPs)

In A. thaliana, 600 ZFP genes were identified [22]. These belong to zinc-finger family TFs that have a sequence motif of cysteine ​​and/or histidine that coordinates zinc atoms to form specific peptide structures. They have an EAR repressor domain that is important in the regulation of genes against biotic and abiotic stresses [23].

Research with mutants in several plant species shows the importance of this family of transcription factors against various abiotic stresses. In rice, OsISAP1 gene, which has a zinc-finger domain, was isolated and it was identified that it has a high rate of transcription after stress by cold, salinity, dehydration, and heavy metals. Overexpression in tobacco led to an increased tolerance to cold, salinity, and dehydration [24]. In A. thaliana, the expression of Zat12 indicated that it produces transcripts during oxidative, osmotic, saline, and heat stress. When the same gene had its constitutive expression by genetic transformation, a high number of transcripts of genes responsive to oxidative and light stress were affected [25].

Also in A. thaliana, when the gene rhl41 was placed in front of a constitutive promoter, it showed efficiency in tolerating high rates of brightness and increased the leaf anthocyanin and chlorophyll contents, playing a key role in acclimatizing plants under intense change in light intensity [26]. AZF1, AZF2, AZF3, and STZ proteins, possessing a repressor domain, were effective in repressing the expression of other TFs. AZF2 and STZ were strongly induced when plants were subjected to dehydration, salinity, cold, and ABA stress [27].

2.2. MYB and MYC

This TFs family is abundant in plants, with about 200 members. Phylogenetic analyses indicated a clear division between monocots and dicots [20]. The MYB domain is composed of one to three imperfect repeats, with 52 amino acid residues that adopt three α-helices [28]. The third helix of each repeat is the helix that makes direct contact with DNA [29]. Members of the MYB family are involved in processes including primary and secondary metabolism; cell fate and identity; developmental processes; and responses to biotic and abiotic stresses [30]. MYBs participate in the ABA-dependent signaling stress pathway and are activated only after ABA accumulation. AtMYB60, AtMYB96, and AtMYB44 act in the ABA signaling cascade regulating stomata movement in response to abiotic stresses, the first two being also activated in drought stress and disease resistance [3133]. AtMYB13, AtMYB15, AtMYB33, and AtMYB101 are all involved in ABA-mediated responses to environmental stresses [34].

Recently, it was demonstrated that overexpression of a member of the MYB family in O. sativa and A. thaliana, OsMYB2P-1, gave an excellent tolerance to low levels of Pi, and a better reallocation of Pi when it is found in high concentrations on the soil, showing the importance of this TF in combating this stress [35]. AtMYB102 is involved in routes of osmotic dehydration, injuries, and salt stress [36]. AtMYB15 is upregulated by salt and cold and, in freezing conditions, it acts as a repressor of the expression of CBF genes [37]. It was also demonstrated that overexpression of the same gene resulted in increased tolerance to salt and drought [38].

2.3. NAC

The NAC family of TFs is largely described in plants, with about 150 members identified in rice [39]. They contain a diversified C-terminal domain and a highly conserved N-terminal [40] and were firstly characterized from petunia (NAM protein) and A. thaliana (AtaF1, Ataf2, and Cuc2 proteins) [41]. NAC TFs recognize the cis- element NACRS [42] that is a drought responsive element.

It is known that the rice genes ONAC19, ONAC55, ONAC72, and ONAC045 are induced by drought [43], and ONAC045 also by high salt, low temperature, and ABA treatment [44]. In Brassicas, the gene BnNAC is induced in response to wounding, insect feeding, cold shock, and dehydration [45]. In soybean, some NAC genes that act against stresses were identified. GmNAC2, GmNAC3, and GmNAC4 are induced by osmotic, ABA, JA, and salinity stresses [46]. In wheat, the gene TaNAC4 is induced by cold, salt, ABA, MeJa, ethylene, and wounding stresses, suggesting a cross talk between pathogen and abiotic stresses [47].

2.4. bZIP

The bZIP family of TFs is extremely abundant, having homologues in several species, including 17 in yeast, 56 in humans, 75 in Arabidopsis, 89 in rice, 92 in sorghum, 125 in maize, and 131 in soybean [48, 49]. The bZIP domain, fairly conserved, consists of a double structure, forming a α-helix, the same as the one providing the name of the family [50]. It has a hydrophobic portion at the C-terminus, creating an amphipathic helix. The DNA adherence occurs through two subunits that attach via hydrophobic interaction of the helix, creating a structure called zipper [51]. The preferred binding sites are the cis-elements A-box (TACGTA), C-box (GACGTC), and G-box (CACGTG) [52]. The family is subdivided into ten groups, according to their genetic similarity and not to the function of each protein [48, 49].

The role of bZIP proteins in response to biotic stress is widely known. Several proteins bZIP, of the type TGA, act as regulators of SA signaling. Members of this family bind to NPR1 genes that are key components in the SA defense signaling pathway [53, 54].

Another bZIP protein, from A. thaliana, is coded by AtbZIP10, which interacts with LSD1. This gene is a negative regulator of cell death and protects plant cells from oxidative stress [55]. Studies report that bZIP proteins act in abiotic stress. The rice gene OsISAP1, a bZIP family, when overexpressed in tobacco, conferred tolerance to cold, dehydration, and salt stress at the seed germination [24]. Another rice TF, OsbZIP71, was strongly induced by drought, PEG, and ABA treatments and repressed by salt treatment, suggesting that this gene may play an important role in ABA mediated drought and salt tolerance [56].

2.5. WRKY

Members of the WRKY family of TFs act as transcriptional regulators in biotic and abiotic stresses, specific to plants and protists [37]. This family has a conserved domain of 60 amino acids with the WRKYGWK sequence at the N-terminus. They possess cysteine and histidine residues binding a zinc atom, which forms a finger type structure [37, 57]. Reports on WRKY family genes in diverse plant species showed that they respond to various abiotic stresses. In rice, OsWRKY89 increased tolerance to UV irradiation and fungal infection [58], and OsWRKY45 is upregulated by cold, heat, salt, and dehydration [59]. The overexpression of OsWRKY11 enhanced heat and drought tolerance [60]. Soybean genes GmWRKY21 and GmWRKY54, when cloned in A. thaliana, conferred salt and drought tolerance [61]. AtWRKY25 and AtWRKY33 showed importance in salt tolerance in A. thaliana while AtWRKY45 is involved in ABA synthesis and tolerance to drought [58, 62]. In tobacco, the knockout of NbWRKY produced chlorosis and senescing phenotypes [63]. These results demonstrate that WRKY family genes play a role against abiotic stresses in different metabolic pathways.

2.6. HSPs

The last family of TFs to be discussed in the “fight” against abiotic stress is the HSF family (heat shock factor) in which members bind to the promoter region of some chaperones, also known as heat shock proteins (HSPs) [64]. These TFs are located in the cytoplasm when in their inactive state [65, 66] and have a C-terminal portion and 3 N-terminal portions, besides the amino acid leucine [67].

The overall structure and recognition of HSFs are conserved in both kingdoms, even with different size and sequences. Near to the N-terminal binding domain (DBD) DNA is formed by a set of three helices (H1, H2, and H3) and a segment of four antiparallel β sheets. The inner portion of the β-sheet is highly conserved and hydrophobic. On the other hand, the outer portion is composed of nonconserved and hydrophilic domains [68, 69]. The hydrophobic portion ensures perfect placement of H2-T-H3 portions, which are responsible for recognizing the promoters of HSPs, the HSE (heat stress promoter element) [70].

In the HSFs structure, one can still find the oligomerizing domain (OD or region HR-A/B), which is connected to the DBD by a region of variable length of amino acids. A pattern of hydrophobic amino acids in the region HR-A/B leads to forming a helical filament. Their description is based on the conservation of the oligomerizing domain: HsfA, HsfB, and HsfC [71].

There are several differences among the structures of HSFs: class B has a more compact HR-A/B region, while the classes A and C are elongated [71]. Class A is characterized by the presence of an AHA transactivator domain in the C-terminal domain, while classes B and C do not. This suggests a role for transcriptional activation of class A, while classes B and C act as coactivators or repressors [7274]. An exception is the HSFs of the A3 and HsfA8 class that do not have AHA domain. The first has a pattern of tryptophan residues, which also act as activators and class that do not have the AHA domain [71]. An exception to class B HSFs was identified in HSFb5 that does not have the tetrapeptide repressor [75]. The DO differences confer distinct patterns of heterooligomerization [71]. The HSFs structures still have nuclear localization signal (NLS) and nuclear export signal (NES).

In mammals, only 4 HSFs were characterized [75, 76], and in D. melanogaster and S. cerevisiae only one has been described [77]. This strongly contrasts with plants, where surveys report at least 21 HSFs in A. thaliana [78], 30 in corn, 24 in Brachypodium, 25 in rice, 27 in tomato, and 52 in soybeans [71], supporting the idea that, in plants, there were several duplications, which make HSFs extremely complex. Each class has its own regulatory network; however, all cooperate in the regulation of various functions and stages of stress [65, 79].

The interaction of these HSFs with HSPs involved with environmental stresses is widely studied. Several studies with mutants (mainly A. thaliana) are helping to elucidate the specific functions of these HSFs. These studies usually employ the techniques of silencing the domain by merging it with a repressor or making use of constitutive promoters when overexpression is needed. HsfA1 mutants in tomato, which had gene expression regulated by the 35S promoter (cauliflower mosaic virus, CAMV), display a 10-fold increase in expression when compared to the control, and the mutants that were cosuppressed by RNAi demonstrated the need of HsfA1 for the control of heat stress [80].

HsfA2 A. thaliana mutant, also with constitutive expression, resulted in a thermotolerance, osmotic, and salt tolerant stresses, suggesting the involvement of this gene in various stress regulatory networks [81]. Aiming at clarifying the influence of genes in class B in A. thaliana, the knockout of AtHsfB1 and AtHsfB2b resulted in plant resistance when exposed to the fungus Alternaria brassicicola. [82].

Studies with rice mutants also demonstrate the performance of HSFs as the response to abiotic stresses. Overexpression of OsHsfA7 mutant in rice and A. thaliana promoted a tolerance of 42°C, resulting in the survival of more than 50% of the mutants when stressed, twice the value of the results obtained by the control WT [83]. Another report confirmed the higher expression of HSPs and HSFs under heat stress in rice, showing that the regulation of abiotic stress induces a very large range of genes and several HSPs act together in different cascades to combat the problems of abiotic stress [84].

These studies emphasize the importance of transcription factors, indicating HSFs in the regulation of metabolic pathways responsive to abiotic stresses. One can observe that TFs can regulate multiple defense mechanisms, thus being considered of great importance in breeding programs that aim mechanisms of tolerance to abiotic stresses.

3. Conclusion and Perspectives

Around 70% of yield losses in major crops occur due to abiotic stresses. There has been a tremendous effort to clarify the stress response pathways, such as the elucidation of the function and characterization of various genes and gene families, directly or indirectly responsible for fighting stresses.

The combination of genetic engineering techniques, together with the understanding of the mechanisms developed by plants to supply a certain kind of aggression, will provide advanced strategies in order to fight with the various types of stress and thereby obtain genetic gains sufficient to meet world demand for food.

The diversity and specificity of TFs make key components for triggering signaling cascades and the understanding and knowledge of the field are fundamental to the generation of new technologies that may be useful in breeding programs, such as overexpression of TFs that can bind specific promoter of genes that interact directly in a stress response, or the manipulation of specific transcription factors to increase the tolerance to determinate stress.

So, one must consider transcription factors as important candidates in breeding and crop improvement programs, since they are the keys to unlock the needed variability that will lead to the next generation of plants and push yield plateaus beyond the critical points needed by our growing population.

Conflict of Interests

The authors declare that there is no conflict of interests regarding the publication of this paper.


  1. J. M. Poehlmann and D. A. Sleper, “Breeding wheat,” in Breeding Field Crops, pp. 259–277, Iowa State University Press, Ames, Iowa, USA, 1995. View at: Google Scholar
  2. M. E. Ferreira and D. Grattapaglia, “Introdução ao uso de marcadores moleculares em análise genética,” EMBRAPA/CENARGEN, 1996. View at: Google Scholar
  3. E. Ruelland and A. Zachowski, “How plants sense temperature,” Environmental and Experimental Botany, vol. 69, no. 3, pp. 225–232, 2010. View at: Publisher Site | Google Scholar
  4. D. Santos, V. F. Guimarães, J. Klein et al., “Cultivares de trigo submetidas a déficit hídrico no início do florescimento, em casa de vegetação,” Revista Brasileira de Engenharia Agrícola e Ambiental, vol. 8, pp. 836–842, 2012. View at: Google Scholar
  5. S. Nagarajan, “Abiotic tolerance and crop improvement,” in Abiotic Stress Adaptation in Plants Physiological, Molecular and Genomic Foundation, A. Pareek, S. K. Sopory, and H. J. Bohnert, Eds., Springer, 2010. View at: Google Scholar
  6. W. Wang, B. Vinocur, O. Shoseyov, and A. Altman, “Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response,” Trends in Plant Science, vol. 9, no. 5, pp. 244–252, 2004. View at: Publisher Site | Google Scholar
  7. N. Thawornwong and A. van Diest, “Influences of high acidity and aluminum on the growth of lowland rice,” Plant and Soil, vol. 41, no. 1, pp. 141–159, 1974. View at: Publisher Site | Google Scholar
  8. C. D. Foy and A. L. Fleming, “Aluminium tolerance of two wheat cultivars related to nitrate reductase activities,” Journal of Plant Nutrition, vol. 5, pp. 1313–1333, 1982. View at: Google Scholar
  9. A. S. Moffat, “Finding new ways to protect drought-stricken plants,” Science, vol. 296, no. 5571, pp. 1226–1229, 2002. View at: Publisher Site | Google Scholar
  10. A. K. Singh, S. K. Sopory, R. Wu, and S. L. Singla-Pareek, “Transgenics aproaches,” in Abiotic Stress Adaptation in Plants, A. Pareek, S. K. Sopory, and H. J. Bohnert, Eds., pp. 417–450, Springer, Amsterdam, The Netherlands, 2010. View at: Publisher Site | Google Scholar
  11. P. Bhatnagar-Mathur, V. Vadez, and K. K. Sharma, “Transgenic approaches for abiotic stress tolerance in plants: retrospect and prospects,” Plant Cell Reports, vol. 27, no. 3, pp. 411–424, 2008. View at: Publisher Site | Google Scholar
  12. B. Vinocur and A. Altman, “Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations,” Current Opinion in Biotechnology, vol. 16, no. 2, pp. 123–132, 2005. View at: Publisher Site | Google Scholar
  13. Z. N. Ozturk, V. Talamé, M. Deyholos et al., “Monitoring large-scale changes in transcript abundance in drought- and salt-stressed barley,” Plant Molecular Biology, vol. 48, no. 5-6, pp. 551–573, 2002. View at: Publisher Site | Google Scholar
  14. A. Schrank, “Transcrição,” in Biologia Molecular Básica, A. Zaha, H. B. Ferreira, and L. M. P. Passaglia, Eds., vol. 4, pp. 401–406, 2012. View at: Google Scholar
  15. N. Mitsuda and M. Ohme-Takagi, “Functional analysis of transcription factors in arabidopsis,” Plant and Cell Physiology, vol. 50, no. 7, pp. 1232–1248, 2009. View at: Publisher Site | Google Scholar
  16. Arabidopsis Genome Initiative, “Analysis of the genome sequence of the flowering plant Arabidopsis thaliana,” Nature, vol. 408, pp. 796–815, 2000. View at: Google Scholar
  17. K. Iida, M. Seki, T. Sakurai et al., “RARTF: database and tools for complete sets of Arabidopsis transcription factors,” DNA Research, vol. 12, no. 4, pp. 247–256, 2005. View at: Publisher Site | Google Scholar
  18. D. M. Riaño-Pachón, S. Ruzicic, I. Dreyer, and B. Mueller-Roeber, “PlnTFDB: an integrative plant transcription factor database,” BMC Bioinformatics, vol. 8, article 42, 2007. View at: Publisher Site | Google Scholar
  19. J. L. Riechmann, J. Heard, G. Martin et al., “Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes,” Science, vol. 290, no. 5499, pp. 2105–2110, 2000. View at: Publisher Site | Google Scholar
  20. J. L. Riechmann and O. J. Ratcliffe, “A genomic perspective on plant transcription factors,” Current Opinion in Plant Biology, vol. 3, no. 5, pp. 423–434, 2000. View at: Publisher Site | Google Scholar
  21. T. Umezawa, M. Fujita, Y. Fujita, and K. Yamaguchi-Shinozaki, “Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future,” Current Opinion in Biotechnology, vol. 17, no. 2, pp. 113–122, 2006. View at: Publisher Site | Google Scholar
  22. T. Eulgem, P. J. Rushton, S. Robatzek, and I. E. Somssich, “The WRKY superfamily of plant transcription factors,” Trends in Plant Science, vol. 5, no. 5, pp. 199–206, 2000. View at: Publisher Site | Google Scholar
  23. I. Winicov and D. R. Bastola, “Transgenic overexpression of the transcription factor Alfin1 enhances expression of the endogenous MsPRP2 gene in alfalfa and improves salinity tolerance of the plants,” Plant Physiology, vol. 120, no. 2, pp. 473–480, 1999. View at: Publisher Site | Google Scholar
  24. A. Mukhopadhyay, S. Vij, and A. K. Tyagi, “Overexpression of a zinc-finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 16, pp. 6309–6314, 2004. View at: Publisher Site | Google Scholar
  25. S. Davletova, K. Schlauch, J. Coutu, and R. Mittler, “The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis,” Plant Physiology, vol. 139, no. 2, pp. 847–856, 2005. View at: Publisher Site | Google Scholar
  26. A. Iida, T. Kazuoka, S. Torikai, H. Kikuchi, and K. Oeda, “A zinc finger protein RHL41 mediates the light acclimatization response in Arabidopsis,” Plant Journal, vol. 24, no. 2, pp. 191–203, 2000. View at: Publisher Site | Google Scholar
  27. H. Sakamoto, K. Maruyama, Y. Sakuma et al., “Arabidopsis Cys2/His2-type zinc-finger proteins function as transcription repressors under drought, cold, and high-salinity stress conditions,” Plant Physiology, vol. 136, no. 1, pp. 2734–2746, 2004. View at: Publisher Site | Google Scholar
  28. C. Yanhui, Y. Xiaoyuan, H. Kun et al., “The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family,” Plant Molecular Biology, vol. 60, no. 1, pp. 107–124, 2006. View at: Publisher Site | Google Scholar
  29. L. Jia, M. T. Clegg, and T. Jiang, “Evolutionary dynamics of the DNA-binding domains in putative R2R3-MYB genes identified from rice subspecies indica and japonica genomes,” Plant Physiology, vol. 134, no. 2, pp. 575–585, 2004. View at: Publisher Site | Google Scholar
  30. C. Dubos, R. Stracke, E. Grotewold, B. Weisshaar, C. Martin, and L. Lepiniec, “MYB transcription factors in Arabidopsis,” Trends in Plant Science, vol. 15, no. 10, pp. 573–581, 2010. View at: Publisher Site | Google Scholar
  31. E. Cominelli, M. Galbiati, A. Vavasseur et al., “A guard-cell-specific MYB transcription factor regulates stomatal movements and plant drought tolerance,” Current Biology, vol. 15, no. 13, pp. 1196–1200, 2005. View at: Publisher Site | Google Scholar
  32. P. J. Seo, F. Xiang, M. Qiao et al., “The MYB96 transcription factor mediates abscisic acid signaling during drought stress response in Arabidopsis,” Plant Physiology, vol. 151, no. 1, pp. 275–289, 2009. View at: Publisher Site | Google Scholar
  33. P. J. Seo and C. Park, “MYB96-mediated abscisic acid signals induce pathogen resistance response by promoting salicylic acid biosynthesis in Arabidopsis,” New Phytologist, vol. 186, no. 2, pp. 471–483, 2010. View at: Publisher Site | Google Scholar
  34. J. L. Reyes and N. Chua, “ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination,” Plant Journal, vol. 49, no. 4, pp. 592–606, 2007. View at: Publisher Site | Google Scholar
  35. X. Dai, Y. Wang, A. Yang, and W. Zhang, “OsMYB2P-1, an R2R3 MYB transcription factor, is involved in the regulation of phosphate-starvation responses and root architecture in rice,” Plant Physiology, vol. 159, no. 1, pp. 169–183, 2012. View at: Publisher Site | Google Scholar
  36. H. C. Yong, H. Chang, R. Gupta, X. Wang, T. Zhu, and S. Luan, “Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis,” Plant Physiology, vol. 129, no. 2, pp. 661–677, 2002. View at: Publisher Site | Google Scholar
  37. P. Agarwal, M. P. Reddy, and J. Chikara, “WRKY: its structure, evolutionary relationship, DNA-binding selectivity, role in stress tolerance and development of plants,” Molecular Biology Reports, vol. 38, no. 6, pp. 3883–3896, 2011. View at: Publisher Site | Google Scholar
  38. Z. Ding, S. Li, X. An, X. Liu, H. Qin, and D. Wang, “Transgenic expression of MYB15 confers enhanced sensitivity to abscisic acid and improved drought tolerance in Arabidopsis thaliana,” Journal of Genetics and Genomics, vol. 36, no. 1, pp. 17–29, 2009. View at: Publisher Site | Google Scholar
  39. Y. Xiong, T. Liu, C. Tian, S. Sun, J. Li, and M. Chen, “Transcription factors in rice: a genome-wide comparative analysis between monocots and eudicots,” Plant Molecular Biology, vol. 59, no. 1, pp. 191–203, 2005. View at: Publisher Site | Google Scholar
  40. H. Hu, J. You, Y. Fang, X. Zhu, Z. Qi, and L. Xiong, “Characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice,” Plant Molecular Biology, vol. 67, no. 1-2, pp. 169–181, 2008. View at: Publisher Site | Google Scholar
  41. M. Aida, T. Ishida, H. Fukaki, H. Fujisawa, and M. Tasaka, “Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant,” The Plant Cell, vol. 9, no. 6, pp. 841–857, 1997. View at: Publisher Site | Google Scholar
  42. L. P. Tran, K. Nakashima, Y. Sakuma et al., “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, vol. 16, no. 9, pp. 2481–2498, 2004. View at: Publisher Site | Google Scholar
  43. H. Hu, M. Dai, J. Yao et al., “Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 35, pp. 12987–12992, 2006. View at: Publisher Site | Google Scholar
  44. X. Zheng, B. Chen, G. Lu, and B. Han, “Overexpression of a NAC transcription factor enhances rice drought and salt tolerance,” Biochemical and Biophysical Research Communications, vol. 379, no. 4, pp. 985–989, 2009. View at: Publisher Site | Google Scholar
  45. D. Hegedus, M. Yu, D. Baldwin et al., “Molecular characterization of Brassica napus NAC domain transcriptional activators induced in response to biotic and abiotic stress,” Plant Molecular Biology, vol. 53, no. 3, pp. 383–397, 2003. View at: Publisher Site | Google Scholar
  46. G. L. Pinheiro, C. S. Marques, M. D. B. L. Costa et al., “Complete inventory of soybean NAC transcription factors: Sequence conservation and expression analysis uncover their distinct roles in stress response,” Gene, vol. 444, no. 1-2, pp. 10–23, 2009. View at: Publisher Site | Google Scholar
  47. N. Xia, G. Zhang, X. Liu et al., “Characterization of a novel wheat NAC transcription factor gene involved in defense response against stripe rust pathogen infection and abiotic stresses,” Molecular Biology Reports, vol. 37, no. 8, pp. 3703–3712, 2010. View at: Publisher Site | Google Scholar
  48. M. Jakoby, B. Weisshaar, W. Dröge-Laser et al., “bZIP transcription factors in Arabidopsis,” Trends in Plant Science, vol. 7, no. 3, pp. 106–111, 2002. View at: Publisher Site | Google Scholar
  49. K. Wei, J. Chen, Y. Wang et al., “Genome-wide analysis of bZIP-encoding genes in maize,” DNAResearch, vol. 19, no. 6, pp. 463–476, 2012. View at: Publisher Site | Google Scholar
  50. M. A. Schumacher, R. H. Goodman, and R. G. Brennan, “The structure of a CREB bZIP·somatostatin CRE complex reveals the basis for selective dimerization and divalent cation-enhanced DNA binding,” Journal of Biological Chemistry, vol. 275, no. 45, pp. 35242–35247, 2000. View at: Publisher Site | Google Scholar
  51. H. C. Hurst, “Transcription factors 1: bZIP proteins,” Protein Profile, vol. 2, no. 2, pp. 101–168, 1995. View at: Google Scholar
  52. T. Izawa, R. Foster, and N. Chua, “Plant bZIP protein DNA binding specificity,” Journal of Molecular Biology, vol. 230, no. 4, pp. 1131–1144, 1993. View at: Publisher Site | Google Scholar
  53. C. M. J. Pieterse, D. Van Der Does, C. Zamioudis, A. Leon-Reyes, and S. C. M. Van Wees, “Hormonal modulation of plant immunity,” Annual Review of Cell and Developmental Biology, vol. 28, pp. 489–521, 2012. View at: Publisher Site | Google Scholar
  54. K. B. Singh, R. C. Foley, and L. Oñate-Sánchez, “Transcription factors in plant defense and stress responses,” Current Opinion in Plant Biology, vol. 5, no. 5, pp. 430–436, 2002. View at: Publisher Site | Google Scholar
  55. A. Mateo, P. Mühlenbock, C. Rustérucci et al., “LESION SIMULATING DISEASE 1 is required for acclimation to conditions that promote excess excitation energy,” Plant Physiology, vol. 136, no. 1, pp. 2818–2830, 2004. View at: Publisher Site | Google Scholar
  56. C. Liu, B. Mao, S. Ou et al., “OsbZIP71, a bZIP transcription factor, confers salinity and drought tolerance in rice,” Plant Molecular Biology, vol. 84, pp. 19–36, 2014. View at: Google Scholar
  57. K. Yamasaki, T. Kigawa, M. Seki, K. Shinozaki, and S. Yokoyama, “DNA-binding domains of plant-specific transcription factors: structure, function, and evolution,” Trends in Plant Science, vol. 18, no. 5, pp. 3883–3896, 2013. View at: Publisher Site | Google Scholar
  58. H. Wang, J. Hao, X. Chen et al., “Overexpression of rice WRKY89 enhances ultraviolet B tolerance and disease resistance in rice plants,” Plant Molecular Biology, vol. 65, no. 6, pp. 799–815, 2007. View at: Publisher Site | Google Scholar
  59. Y. Qiu and D. Yu, “Over-expression of the stress-induced OsWRKY45 enhances disease resistance and drought tolerance in Arabidopsis,” Environmental and Experimental Botany, vol. 65, no. 1, pp. 35–47, 2009. View at: Publisher Site | Google Scholar
  60. X. Wu, Y. Shiroto, S. Kishitani, Y. Ito, and K. Toriyama, “Enhanced heat and drought tolerance in transgenic rice seedlings overexpressing OsWRKY11 under the control of HSP101 promoter,” Plant Cell Reports, vol. 28, no. 1, pp. 21–30, 2009. View at: Publisher Site | Google Scholar
  61. Q. Zhou, A. Tian, H. Zou et al., “Soybean WRKY-type transcription factor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants,” Plant Biotechnology Journal, vol. 6, no. 5, pp. 486–503, 2008. View at: Publisher Site | Google Scholar
  62. Y. Jiang and M. K. Deyholos, “Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes,” BMC Plant Biology, vol. 6, article 25, 2006. View at: Publisher Site | Google Scholar
  63. K. Archana, N. Rama, H. M. Mamrutha, and K. N. Nataraja, “Down-regulation of an abiotic stress related Nicotiana benthamiana WRKY transcription factor induces physiological abnormalities,” Indian Journal of Biotechnology, vol. 8, no. 1, pp. 53–60, 2009. View at: Google Scholar
  64. H. R. B. Pelham, “A regulatory upstream promoter element in the Drosophila Hsp70 heat-shock gene,” Cell, vol. 30, no. 2, pp. 517–528, 1982. View at: Publisher Site | Google Scholar
  65. S. K. Baniwal, K. Bharti, K. Y. Chan et al., “Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors,” Journal of Biosciences, vol. 29, no. 4, pp. 471–487, 2004. View at: Publisher Site | Google Scholar
  66. W. Hu, G. Hu, and B. Han, “Genome-wide survey and expression profiling of heat shock proteins and heat shock factors revealed overlapped and stress specific response under abiotic stresses in rice,” Plant Science, vol. 176, no. 4, pp. 583–590, 2009. View at: Publisher Site | Google Scholar
  67. T. J. Schuetz, G. J. Gallo, L. Sheldon, P. Tempst, and R. E. Kingston, “Isolation of a cDNA for HSF2: Evidence for two heat shock factor genes in humans,” Proceedings of the National Academy of Sciences of the United States of America, vol. 88, no. 16, pp. 6911–6915, 1991. View at: Google Scholar
  68. F. F. Damberger, J. G. Pelton, C. J. Harrison, H. C. M. Nelson, and D. E. Wemmer, “Solution structure of the DNA-binding domain of the heat shock transcription factor determined by multidimensional heteronuclear magnetic resonance spectroscopy,” Protein Science, vol. 3, no. 10, pp. 1806–1821, 1994. View at: Publisher Site | Google Scholar
  69. J. Schultheiss, O. Kunert, U. Gase, K. Scharf, L. Nover, and H. Rüterjans, “Solution structure of the DNA-binding domain of the tomato heat-stress transcription factor HSF24,” European Journal of Biochemistry, vol. 236, no. 3, pp. 911–921, 1996. View at: Publisher Site | Google Scholar
  70. M. P. Cicero, S. T. Hubl, C. J. Harrison, O. Littlefield, J. A. Hardy, and H. C. M. Nelson, “The wing in yeast heat shock transcription factor (HSF) DNA-binding domain is required for full activity,” Nucleic Acids Research, vol. 29, no. 8, pp. 1715–1723, 2001. View at: Publisher Site | Google Scholar
  71. K. Scharf, T. Berberich, I. Ebersberger, and L. Nover, “The plant heat stress transcription factor (Hsf) family: structure, function and evolution,” Biochimica et Biophysica Acta—Gene Regulatory Mechanisms, vol. 1819, no. 2, pp. 104–119, 2012. View at: Publisher Site | Google Scholar
  72. S. Kotak, M. Port, A. Ganguli, F. Bicker, and P. Von Koskull-Döring, “Characterization of C-terminal domains of Arabidopsis heat stress transcription factors (Hsfs) and identification of a new signature combination of plant class a Hsfs with AHA and NES motifs essential for activator function and intracellular localization,” The Plant Journal, vol. 39, no. 1, pp. 98–112, 2004. View at: Publisher Site | Google Scholar
  73. E. Czarnecka-Verner, S. Pan, T. Salem, and W. B. Gurley, “Plant class B HSFs inhibit transcription and exhibit affinity for TFIIB and TBP,” Plant Molecular Biology, vol. 56, no. 1, pp. 57–75, 2004. View at: Publisher Site | Google Scholar
  74. D. Mittal, S. Chakrabarti, A. Sarkar, A. Singh, and A. Grover, “Heat shock factor gene family in rice: genomic organization and transcript expression profiling in response to high temperature, low temperature and oxidative stresses,” Plant Physiology and Biochemistry, vol. 47, no. 9, pp. 785–795, 2009. View at: Publisher Site | Google Scholar
  75. L. Pirkkala, P. Nykänen, and L. Sistonen, “Roles of the heat shock transcription factors in regulation of the heat shock response and beyond,” FASEB Journal, vol. 15, no. 7, pp. 1118–1131, 2001. View at: Publisher Site | Google Scholar
  76. A. Tessari, E. Salata, A. Ferlin, L. Bartoloni, M. L. Slongo, and C. Foresta, “Characterization of HSFY, a novel AZFb gene on the Y chromosome with a possible role in human spermatogenesis,” Molecular Human Reproduction, vol. 10, no. 4, pp. 253–258, 2004. View at: Publisher Site | Google Scholar
  77. A. Nakai, “New aspects in the vertebrate heat stress factor system: HsfA3 and HsfA4,” Cell Stress Chaperones, vol. 4, pp. 86–93, 1999. View at: Google Scholar
  78. L. Nover and S. K. Baniwal, “Multiplicity of heat stress transcription factors controlling the complex heat stress response of plants,” in Proceedings of the International Symposium on Environmental Factors. Cellular Stress and Evolution, p. 15, 2006. View at: Google Scholar
  79. J. Tripp, S. K. Mishra, and K. Scharf, “Functional dissection of the cytosolic chaperone network in tomato mesophyll protoplasts,” Plant, Cell and Environment, vol. 32, no. 2, pp. 123–133, 2009. View at: Publisher Site | Google Scholar
  80. S. K. Mishra, J. Tripp, S. Winkelhaus et al., “In the complex family of heat stress transcription factors, HsfA1 has a unique role as master regulator of thermotolerance in tomato,” Genes and Development, vol. 16, no. 12, pp. 1555–1567, 2002. View at: Publisher Site | Google Scholar
  81. D. Ogawa, K. Yamaguchi, and T. Nishiuchi, “High-level overexpression of the Arabidopsis HsfA2 gene confers not only increased themotolerance but also salt/osmotic stress tolerance and enhanced callus growth,” Journal of Experimental Botany, vol. 58, no. 12, pp. 3373–3383, 2007. View at: Publisher Site | Google Scholar
  82. M. Kumar, W. Busch, H. Birke, B. Kemmerling, T. Nürnberger, and F. Schöffl, “Heat shock factors HsfB1 and HsfB2b are involved in the regulation of Pdf1.2 expression and pathogen resistance in Arabidopsis,” Molecular Plant, vol. 2, no. 1, pp. 152–165, 2009. View at: Publisher Site | Google Scholar
  83. J. Liu, Q. Qin, Z. Zhang et al., “OsHSF7 gene in rice, Oryza sativa L., encodes a transcription factor that functions as a high temperature receptive and responsive factor,” BMB Reports, vol. 42, no. 1, pp. 16–21, 2009. View at: Publisher Site | Google Scholar
  84. G. Chandel, M. Dubey, and R. Meena, “Differential expression of heat shock proteins and heat stress transcription factor genes in rice exposed to different levels of heat stress,” Journal of Plant Biochemistry and Biotechnology, vol. 22, no. 3, pp. 277–285, 2013. View at: Publisher Site | Google Scholar

Copyright © 2014 Glacy Jaqueline da Silva and Antonio Costa de Oliveira. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

1482 Views | 734 Downloads | 2 Citations
 PDF  Download Citation  Citation
 Download other formatsMore
 Order printed copiesOrder

We are committed to sharing findings related to COVID-19 as quickly and safely as possible. Any author submitting a COVID-19 paper should notify us at to ensure their research is fast-tracked and made available on a preprint server as soon as possible. We will be providing unlimited waivers of publication charges for accepted articles related to COVID-19.