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A novel Ap2/ERF transcription factor from Stipa purpurea leads to enhanced drought tolerance in Arabidopsis thaliana

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SpERF1 acts as a positive regulator, contributing to drought stress tolerance in A. thaliana through activating DRE/CRT elements in the promoters of abiotic stress-responsive genes.

Abstract

Stipa purpurea is an endemic perennial grass species in alpine arid and semi-arid meadows on the Qinghai-Xizang Plateau, which is highly tolerant against drought and cold. ERF transcription factors are known to regulate gene expression under abiotic and biotic treatments. Herein, we isolated a full-length ERF gene CDS from S. purpurea named SpERF1, which was induced by drought, cold, and jasmonic acid stresses. Subcellular localization revealed that SpERF1 is a nuclear protein, consistent with its roles as a transcription factor. Overexpression of SpERF1 enhanced drought tolerance of transgenic Arabidopsis thaliana via the activation of DRE/CRT elements in the promoters of abiotic stress-responsive genes. Furthermore, increased accumulation of proline indicated that SpERF1 might be involved in proline synthesis in the transgenic lines, allowing them to have a better buffering capacity and membrane protection under drought stress. This study indicated that SpERF1 might be an attractive target in the genetic engineering for improving stress tolerance in other crops. Moreover, SpERF1 protein function analysis increased our understanding of S. purpurea’s ability to adapt to the adverse conditions of the Qinghai-Xizang Plateau.

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References

  • Ayarpadikannan S, Chung E, Kim K, So H-A, Schraufnagle KR, Lee J-H (2014) RsERF1 derived from wild radish (Raphanus sativus) confers salt stress tolerance in Arabidopsis. Acta Physiol Plant 36:993–1008

    Article  CAS  Google Scholar 

  • Bennett J, Hondred D, Register JC III (2015) Keeping qRT-PCR rigorous and biologically relevant. Plant Cell Rep 34:1

    Article  CAS  PubMed  Google Scholar 

  • Bowman JL, Smyth DR (1999) CRABS CLAW, a gene that regulates carpel and nectary development in Arabidopsis, encodes a novel protein with zinc finger and helix-loop-helix domains. Development 126:2387–2396

    CAS  PubMed  Google Scholar 

  • Budar F, Thia-Toong L, Van Montagu M, Hernalsteens JP (1986) Agrobacterium-mediated gene transfer results mainly in transgenic plants transmitting as a single Mendelian factor. Genetics 114:303–313

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng M-C, Liao P-M, Kuo W-W, Lin T-P (2013) The Arabidopsis ETHYLENE RESPONSE FACTOR1 regulates abiotic stress-responsive gene expression by binding to different cis-acting elements in response to different stress signals. Plant Physiol 162:1566–1582

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Demiral T, Türkan I (2005) Comparative lipid peroxidation, antioxidant defense systems and proline content in roots of two rice cultivars differing in salt tolerance. Environ Exp Bot 53:247–257

    Article  CAS  Google Scholar 

  • Epron D, Dreyer E (1992) Effects of severe dehydration on leaf photosynthesis in Quercus petraea (Matt.) Liebl.: photosystem II efficiency, photochemical and nonphotochemical fluorescence quenching and electrolyte leakage. Tree Physiol 10:273–284

    Article  CAS  PubMed  Google Scholar 

  • Fujimoto SY, Ohta M, Usui A, Shinshi H, Ohme-Takagi M (2000) Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box–mediated gene expression. Plant Cell 12:393–404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao S, Zhang H, Tian Y, Li F, Zhang Z, Lu X, Chen X, Huang R (2008) Expression of TERF1 in rice regulates expression of stress-responsive genes and enhances tolerance to drought and high-salinity. Plant Cell Rep 27:1787–1795

    Article  CAS  PubMed  Google Scholar 

  • Gou X, Chen F, Jacoby G, Cook E, Yang M, Peng J, Zhang Y (2007) Rapid tree growth with respect to the last 400 years in response to climate warming, northeastern Tibetan Plateau. Int J Climatol 27:1497–1504

    Article  Google Scholar 

  • Grigorova B, Vaseva I, Demirevska K, Feller U (2011) Combined drought and heat stress in wheat: changes in some heat shock proteins. Biol Plantarum 55:105–111

    Article  CAS  Google Scholar 

  • Gullì M, Corradi M, Rampino P, Marmiroli N, Perrotta C (2007) Four members of the HSP101 gene family are differently regulated in Triticum durum Desf. FEBS Lett 581:4841–4849

    Article  PubMed  Google Scholar 

  • Hao D, Ohme-Takagi M, Sarai A (1998) Unique mode of GCC box recognition by the DNA-binding domain of ethylene-responsive element-binding factor (ERF domain) in plant. J Biol Chem 273:26857–26861

    Article  CAS  PubMed  Google Scholar 

  • Hong S-W, Lee U, Vierling E (2003) Arabidopsis hot mutants define multiple functions required for acclimation to high temperatures. Plant Physiol 132:757–767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang Z, Zhang Z, Zhang X, Zhang H, Huang D, Huang R (2004) Tomato TERF1 modulates ethylene response and enhances osmotic stress tolerance by activating expression of downstream genes. FBBS Lett 573:110–116

    Article  CAS  Google Scholar 

  • Huang L, Liu J, Shao Q, Liu R (2011) Changing inland lakes responding to climate warming in Northeastern Tibetan Plateau. Clim Change 109:479–502

    Article  Google Scholar 

  • Iyer LM, Kumpatla SP, Chandrasekharan MB, Hall TC (2000) Transgene silencing in monocots. Springer, Netherlands, pp 203–226

    Google Scholar 

  • Kasuga M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2004) A combination of the Arabidopsis DREB1A gene and stress-inducible rd29A promoter improved drought-and low-temperature stress tolerance in tobacco by gene transfer. Plant Cell Physiol 45:346–350

    Article  CAS  PubMed  Google Scholar 

  • Kishor PK, Hong Z, Miao G-H, Hu C-AA, Verma DPS (1995) Overexpression of [delta]-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol 108:1387–1394

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lindemose S, O’Shea C, Jensen MK, Skriver K (2013) Structure, function and networks of transcription factors involved in abiotic stress responses. Int J Mol Sci 14:5842–5878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Makhloufi E, Yousfi F-E, Marande W, Mila I, Hanana M, Bergès H, Mzid R, Bouzayen M (2014) Isolation and molecular characterization of ERF1, an ethylene response factor gene from durum wheat (Triticum turgidum L. subsp. durum), potentially involved in salt-stress responses. J Exp Bot 65:6359–6371

    Article  CAS  PubMed  Google Scholar 

  • Matysik J, Bhalu B, Mohanty P (2002) Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. Curr Sci India 82:525–532

    CAS  Google Scholar 

  • Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) AP2/ERF family transcription factors in plant abiotic stress responses. BBA-Gene Regul Mec. 1819:86–96

    CAS  Google Scholar 

  • Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140:411–432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olvera-Carrillo Y, Campos F, Reyes JL, Garciarrubio A, Covarrubias AA (2010) Functional analysis of the group 4 late embryogenesis abundant proteins reveals their relevance in the adaptive response during water deficit in Arabidopsis. Plant Physiol 154:373–390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oñate-Sánchez L, Anderson JP, Young J, Singh KB (2007) AtERF14, a member of the ERF family of transcription factors, plays a nonredundant role in plant defense. Plant Physiol 143:400–409

    Article  PubMed  PubMed Central  Google Scholar 

  • Premachandra G, Saneoka H, Ogata S (1990) Cell membrane stability, an indicator of drought tolerance, as affected by applied nitrogen in soyabean. J Agr Sci. 115:63–66

    Article  CAS  Google Scholar 

  • Quan R, Hu S, Zhang Z, Zhang H, Zhang Z, Huang R (2010) Overexpression of an ERF transcription factor TSRF1 improves rice drought tolerance. Plant Biotechnol J 8:476–488

    Article  CAS  PubMed  Google Scholar 

  • Rong W, Qi L, Wang A, Ye X, Du L, Liang H, Xin Z, Zhang Z (2014) The ERF transcription factor TaERF3 promotes tolerance to salt and drought stresses in wheat. Plant Biotechnol J 12:468–479

    Article  CAS  PubMed  Google Scholar 

  • Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration-and cold-inducible gene expression. Bioch Bioph Res Co 290:998–1009

    Article  CAS  Google Scholar 

  • Sayar R, Khemira H, Kameli A, Mosbahi M (2008) Physiological tests as predictive appreciation for drought tolerance in durum wheat (Triticum durum Desf.). Agron Res 6:79–90

    Google Scholar 

  • Sharma MK, Kumar R, Solanke AU, Sharma R, Tyagi AK, Sharma AK (2010) Identification, phylogeny, and transcript profiling of ERF family genes during development and abiotic stress treatments in tomato. Mol Genet Genom 284:455–475

    Article  CAS  Google Scholar 

  • Sharoni AM, Nuruzzaman M, Satoh K, Shimizu T, Kondoh H, Sasaya T, Choi I-R, Omura T, Kikuchi S (2011) Gene structures, classification and expression models of the AP2/EREBP transcription factor family in rice. Plant Cell Physiol 52:344–360

    Article  CAS  PubMed  Google Scholar 

  • Silva-Ortega CO, Ochoa-Alfaro AE, Reyes-Agüero JA, Aguado-Santacruz GA, Jiménez-Bremont JF (2008) Salt stress increases the expression of p5cs gene and induces proline accumulation in cactus pear. Plant Physiol Bioch 46:82–92

    Article  CAS  Google Scholar 

  • Solano R, Stepanova A, Chao Q, Ecker JR (1998) Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. Gene Dev 12:3703–3714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun XD, Feng ZH, Meng LS (2012) Ectopic expression of the Arabidopsis ASYMMETRIC LEAVES2-LIKE5 (ASL5) gene in cockscomb (Celosia cristata) generates vascular-pattern modifications in lateral organs. Plant Cell Tiss Organ Cult 110:163–169

    Article  CAS  Google Scholar 

  • Sung DY, Guy CL (2003) Physiological and molecular assessment of altered expression of Hsc70-1 in Arabidopsis. Evidence for pleiotropic consequences. Plant Physiol 132:979–987

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97

    Article  CAS  PubMed  Google Scholar 

  • Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Yang L, Zheng Z, Grumet R, Loescher W, Zhu J-K, Yang P, Hu IY, Chan Z (2013) Transcriptomic and physiological variations of three Arabidopsis ecotypes in response to salt stress. PLoS One 8:e69036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weising K, Schell J, Kahl G (1988) Foreign genes in plants: transfer, structure, expression, and applications. Annu Rev Genet 22:421–477

    Article  CAS  PubMed  Google Scholar 

  • Welin BV, Olson Å, Nylander M, Palva ET (1994) Characterization and differential expression of dhn/lea/rab-like genes during cold acclimation and drought stress in Arabidopsis thaliana. Plant Mol Biol 26:131–144

    Article  CAS  PubMed  Google Scholar 

  • 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 (2007) Isolation and molecular characterization of the Triticum aestivum L. ethylene-responsive factor 1 (TaERF1) that increases multiple stress tolerance. Plant Mol Biol 65:719–732

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Dong C, Yang S, Li X, Sun X, Yang Y (2015a) Physiological and proteomic adaptation of the alpine grass Stipa purpurea to a drought gradient. PLoS One 10:e0117475

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang Y, Li X, Kong X, Ma L, Hu X, Yang Y (2015b) Transcriptome analysis reveals diversified adaptation of Stipa purpurea along a drought gradient on the Tibetan Plateau. Func Integr Genomic 15:295–307

    Article  CAS  Google Scholar 

  • Yue P, Lu X, Ye R, Zhang C, Yang S, Zhou Y, Peng M (2011) Distribution of Stipa purpurea steppe in the Northeastern Qinghai-Xizang Plateau (China). Russ J Ecol 42:50–56

    Article  CAS  Google Scholar 

  • Zhang Z, Yao W, Dong N, Liang H, Liu H, Huang R (2007) A novel ERF transcription activator in wheat and its induction kinetics after pathogen and hormone treatments. J Exp Bot 58:2993–3003

    Article  CAS  PubMed  Google Scholar 

  • Zhang G, Chen M, Chen X, Xu Z, Guan S, Li L-C, Li A, Guo J, Mao L, Ma Y (2008) Phylogeny, gene structures, and expression patterns of the ERF gene family in soybean (Glycine max L.). J Exp Bot 59:4095–4107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang G, Chen M, Li L, Xu Z, Chen X, Guo J, Ma Y (2009) Overexpression of the soybean GmERF3 gene, an AP2/ERF type transcription factor for increased tolerances to salt, drought, and diseases in transgenic tobacco. J Exp Bot 60:3781–3796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Li F, Li D, Zhang H, Huang R (2010) Expression of ethylene response factor JERF1 in rice improves tolerance to drought. Planta 232:765–774

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Zhuang J, Cai B, Peng R-H, Zhu B, Jin X-F, Xue Y, Gao F, Fu X-Y, Tian Y-S, Zhao W (2008) Genome-wide analysis of the AP2/ERF gene family in Populus trichocarpa. Biochem Bioph Res Co 371:468–474

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported financially by the National Natural Science Foundation of China (No. 41271058), the Major State Basic Research Development Program of China (No. 2010CB951704), and the Major Projects of National Natural Science Foundation of China (No. 31590823).

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    Authors and Affiliations

    1. Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Science, Kunming, 650204, China

      Yunqiang Yang, Chao Dong, Xiong Li, Jiancan Du, Min Qian, Xudong Sun & Yongping Yang

    2. Plant Germplasm and Genomics Center, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650201, China

      Yunqiang Yang, Chao Dong, Xiong Li, Jiancan Du, Min Qian, Xudong Sun & Yongping Yang

    3. Institute of Tibetan Plateau Research at Kunming, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650201, China

      Yunqiang Yang, Chao Dong, Xiong Li, Jiancan Du, Min Qian, Xudong Sun & Yongping Yang

    4. University of Chinese Academy of Sciences, Beijing, 100049, China

      Chao Dong & Jiancan Du

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    1. Yunqiang Yang
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    2. Chao Dong
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    Correspondence to Xudong Sun or Yongping Yang.

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    Communicated by I. Hwang.

    Y. Yang, C. Dong contributed equally to this work.

    A novel ERF transcription factor from Stipa purpurea.

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    Yang, Y., Dong, C., Li, X. et al. A novel Ap2/ERF transcription factor from Stipa purpurea leads to enhanced drought tolerance in Arabidopsis thaliana . Plant Cell Rep 35, 2227–2239 (2016). https://doi.org/10.1007/s00299-016-2030-y

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