A meta-analysis of the overexpression of AP2/ERF genes in response to drought stress in plants

Abstract

The APETALA2/ethylene-responsive element-binding factor (AP2/ERF) family is primarily known for regulating plant development; however, it also participates in abiotic stress responses. Ethylene response factor (ERF) and dehydration responsive element-binding (DREB) transcription factors (TFs), the subgroups of this superfamily, are especially active in drought response. A thorough meta-analysis has yet to be performed despite the numerous studies conducted on the overexpression of the AP2/ERF superfamily in various plant species. In the present study, a comprehensive meta-analysis was performed to investigate the effects of AP2/ERF overexpression on drought stress. The analysis was conducted using 35 studies on 20 different species. A total of ten moderator analyses were performed, and summary effect analysis demonstrated that AP2/ERF members, namely ERF and DREB overexpression, notably enhanced the survival rate (P = 0.0275) and proline content (P = 0.0000) under drought conditions. Overexpression also resulted in elevated levels of catalase and peroxidase activity, hydrogen peroxide, photosynthesis rate, plant dry weight, plant fresh weight, root length, shoot dry weight, stomatal conductance, and transpiration rate under drought conditions compared to the control group; however, a negative effect on malondialdehyde level, relative water content, ion leakage, and singlet oxygen. The primary conclusion of this meta-analysis research is that AP2/ERF overexpression leads to an increase in proline levels and a rise in the survival rate of plants under drought stress. The results of this study are expected to provide valuable insights for future research in the AP2/ERF superfamily

Keywords

• AP2
• ERF
• DREB
• proline
• drought
• Meta-analysis

References

1. N. Figueroa, A. F. Lodeyro, N. Carrillo and R. Gómez, “Meta-analysis reveals key features of the improved drought tolerance of plants overexpressing NAC transcription factors,” Environmental and Experimental Botany, vol. 186, pp. 104449, 2021. https://doi:10.1016/J.ENVEXPBOT.2021.104449.
2. M. Chieb and E. W. Gachomo, “The role of plant growth promoting rhizobacteria in plant drought stress responses,” BMC Plant Biology, vol. 23, no. 1, pp. 407, 2023. https://doi:10.1186/s12870-023-04403-8.
3. S. Toscano and D. Romano, “Morphological, Physiological, and Biochemical Responses of Zinnia to Drought Stress,” Horticulture, vol. 7, no. 10, pp. 362, 2021. https://doi:10.3390/HORTICULTURAE7100362.
4. M. Naeem, C. Yavuz and M. E. Çalışkan, “Allele Mining for Molecular Breeding in Potato,” in Allele Mining for Genomic Designing of Vegetable Crops, 1st ed., C. Kole, T. K. Behera, and P. Kaushik, Eds., Boca Raton: CRC Press, 2024.
5. M. Manna, T. Thakur, O. Chirom, R. Mandlik, R. Deshmukh and P. Salvi, “Transcription factors as key molecular target to strengthen the drought stress tolerance in plants,” Physiologia Plantarum, vol. 172, no. 2, pp. 847–868, 2021. https://doi:10.1111/PPL.13268.
6. K. D. Jofuku, B. G. den Boer, M. Van Montagu and J. K. Okamuro, “Control of Arabidopsis flower and seed development by the homeotic gene APETALA2.,” Plant Cell, vol. 6, no. 9, pp. 1211–1225, 1994. https://doi:10.1105/tpc.6.9.1211.
7. E. Magnani, K. Sjölander and S. Hake, “From Endonucleases to Transcription Factors: Evolution of the AP2 DNA Binding Domain in Plants,” Plant Cell, vol. 16, no. 9, pp. 2265, 2004. https://doi:10.1105/TPC.104.023135.
8. K. Feng et al., “Advances in AP2/ERF super-family transcription factors in plant,” Critical Reviews in Biotechnology, vol. 40, no. 6, pp. 750–776, 2020. https://doi:10.1080/07388551.2020.1768509.

9. N. Ma et al., “Plant disease resistance outputs regulated by AP2/ERF transcription factor family,” Stress Biology, vol. 4, no. 1, 2024. https://doi:10.1007/S44154-023-00140-Y.
10. C. Dong, Y. Xi, X. Chen and Z. M. Cheng, “Genome-wide identification of AP2/EREBP in Fragaria vesca and expression pattern analysis of the FvDREB subfamily under drought stress,” BMC Plant Biology, vol. 21, no. 1, pp. 295, 2021. https://doi:10.1186/S12870-021-03095-2.
11. K. Yamaguchi-Shinozaki and K. Shinozaki, “A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress,” Plant Cell, vol. 6, no. 2, pp. 251–264, 1994. https://doi:10.1105/TPC.6.2.251.
12. J. Mizoi, K. Shinozaki and K. Yamaguchi-Shinozaki, “AP2/ERF family transcription factors in plant abiotic stress responses,” Biochimica et Biophysica Acta, vol. 1819, no. 2, pp. 86–96, 2012. https://doi:10.1016/J.BBAGRM.2011.08.004.
13. D. Bouaziz et al., “Identification and functional characterization of ten AP2/ERF genes in potato,” Plant Cell, Tissue and Organ Culture, vol. 123, no. 1, pp. 155–172, 2015. https://doi:10.1007/s11240-015-0823-2.
14. Q. Liu et al., “Two Transcription Factors, DREB1 and DREB2, with an EREBP/AP2 DNA Binding Domain Separate Two Cellular Signal Transduction Pathways in Drought- and Low-Temperature-Responsive Gene Expression, Respectively, in Arabidopsis,” Plant Cell, vol. 10, no. 8, pp. 1391–1406, 1998. https://doi:10.1105/TPC.10.8.1391.
15. L. Erpen, H. S. Devi, J. W. Grosser and M. Dutt, “Potential use of the DREB/ERF, MYB, NAC and WRKY transcription factors to improve abiotic and biotic stress in transgenic plants,” Plant Cell, Tissue and Organ Culture, vol. 132, no. 1, pp. 1–25, 2017. https://doi:10.1007/S11240-017-1320-6.
16. P. K. Agarwal, P. Agarwal, M. K. Reddy and S. K. Sopory, “Role of DREB transcription factors in abiotic and biotic stress tolerance in plants,” Plant Cell Reports, vol. 25, no. 12, pp. 1263–1274, 2006. https://doi:10.1007/S00299-006-0204-8.
17. X. Jin et al., “Transcription factor OsAP21 gene increases salt/drought tolerance in transgenic Arabidopsis thaliana,” Molecular Biology Reports, vol. 40, no. 2, pp. 1743–1752, 2013. https://doi:10.1007/s11033-012-2228-1.
18. C. Gu, Z.-H. Guo, P.-P. Hao, G.-M. Wang, Z.-M. Jin and S.-L. Zhang, “Multiple regulatory roles of AP2/ERF transcription factor in angiosperm,” Botanical Studies, vol. 58, no. 1, pp. 6, 2017. https://doi:10.1186/s40529-016-0159-1.
19. X. Zhu et al., “Genome-wide analysis of AP2/ERF gene and functional analysis of CqERF24 gene in drought stress in quinoa,” International Journal of Biological Macromolecules, vol. 253, pp. 127582, 2023. https://doi:10.1016/j.ijbiomac.2023.127582.
20. R. R. Reis et al., “Induced over-expression of AtDREB2A CA improves drought tolerance in sugarcane,” Plant Science, vol. 221–222, pp. 59–68, 2014. https://doi:10.1016/j.plantsci.2014.02.003.
21. Y. Wang et al., “Overexpression of a tomato AP2/ERF transcription factor SlERF.B1 increases sensitivity to salt and drought stresses,” Scientia Horticulturae, vol. 304, pp. 111332, 2022. https://doi:10.1016/j.scienta.2022.111332.
22. M.-L. Zhou, J.-T. Ma, Y.-M. Zhao, Y.-H. Wei, Y.-X. Tang and Y.-M. Wu, “Improvement of drought and salt tolerance in Arabidopsis and Lotus corniculatus by overexpression of a novel DREB transcription factor from Populus euphratica,” Gene, vol. 506, no. 1, pp. 10–17, 2012. https://doi: 10.1016/j.gene.2012.06.089.
23. K. Chen et al., “AP2/ERF transcription factor GmDREB1 confers drought tolerance in transgenic soybean by interacting with GmERFs,” Plant Physiology and Biochemistry, vol. 170, pp. 287–295, 2022. https://doi:10.1016/j.plaphy.2021.12.014.
24. Z. Ren et al., “Analysis of the molecular mechanisms regulating how ZmEREB24 improves drought tolerance in maize (Zea mays) seedlings,” Plant Physiology and Biochemistry, vol. 207, pp. 108292, 2024. https://doi:10.1016/j.plaphy.2023.108292.
25. Y. Guo et al., “Meta-analysis of the effects of overexpression of WRKY transcription factors on plant responses to drought stress,” BMC Genetics, vol. 20, no. 1, pp. 1–14, 2019. https://doi:10.1186/S12863-019-0766-4/FIGURES/9.
26. C. Dong, Y. Ma, M. Wisniewski and Z. M. Cheng, “Meta-analysis of the effect of overexpression of CBF/DREB family genes on drought stress response,” Environmental and Experimental Botany, vol. 142, pp. 1–14, 2017. https://doi:10.1016/J.ENVEXPBOT.2017.07.014.
27. W. Liu et al., “Meta-Analysis of the Effect of Overexpression of MYB Transcription Factors on the Regulatory Mechanisms of Anthocyanin Biosynthesis,” Frontiers in Plant Science, vol. 12, pp. 781343, 2021. https://doi:10.3389/FPLS.2021.781343/BIBTEX.
28. J. Ren, X. Yang, C. Ma, Y. Wang, J. Zhao and L. Kang, “Meta-analysis of the effect of the overexpression of aquaporin family genes on the drought stress response,” Plant Biotechnology Reports, vol. 15, no. 2, pp. 139–150, 2021. https://doi:10.1007/S11816-021-006665/FIGURES/8.
29. R. Tao, Y. Liu, S. Chen and S. Shityakov, “Meta-Analysis of the Effects of Overexpressed bZIP Transcription Factors in Plants under Drought Stress,” Plants, vol. 13, no. 3, pp. 337, 2024. https://doi:10.3390/plants13030337.
30. M. Borenstein, “Effect sizes for continuous data.,” in The handbook of research synthesis and meta-analysis, Russell Sage Foundation, 2009, pp. 221–235. Accessed: Jun. 10, 2024. [Online]. Available: https://psycnet.apa.org/record/2009-05060-012.
31. M. S. Rosenberg, “MetaWin 3: open-source software for meta-analysis,” Frontiers in Bioinformatics, vol. 4, 2024. https://doi:10.3389/fbinf.2024.1305969.
32. J. P. T. Higgins and S. G. Thompson, “Quantifying heterogeneity in a meta‐analysis,” Statistics in Medicine, vol. 21, no. 11, pp. 1539–1558, 2002. https://doi:10.1002/sim.1186.
33. T. B. Huedo-Medina, J. Sánchez-Meca, F. Marín-Martínez and J. Botella, “Assessing heterogeneity in meta-analysis: Q statistic or I2 index?,” Psychological Methods, vol. 11, no. 2, pp. 193–206, 2006. https://doi:10.1037/1082-989X.11.2.193.
34. J. L. Peters, A. J. Sutton, D. R. Jones, K. R. Abrams and L. Rushton, “Contour-enhanced meta-analysis funnel plots help distinguish publication bias from other causes of asymmetry,” Journal of Clinical Epidemiology, vol. 61, no. 10, pp. 991–996, 2008. https://doi:10.1016/j.jclinepi.2007.11.010.
35. J. A. Sterne and M. Egger, “Funnel plots for detecting bias in meta-analysis,” Journal of Clinical Epidemiology, vol. 54, no. 10, pp. 1046–1055, 2001. https://doi:10.1016/S0895-4356(01)00377-8.
36. G. Zhang et al., “Overexpression of the soybean GmERF3 gene, an AP2/ERF type transcription factor for increased tolerances to salt, drought, and diseases in transgenic tobacco,” Journal of Experimental Botany, vol. 60, no. 13, pp. 3781–3796, 2009. https://doi:10.1093/jxb/erp214.
37. Y. Zhai et al., “Overexpression of soybean GmERF9 enhances the tolerance to drought and cold in the transgenic tobacco,” Plant Cell, Tissue and Organ Culture, vol. 128, no. 3, pp. 607–618, 2017. https://doi:10.1007/s11240-016-1137-8.
38. Q. Zhao et al., “The AP2 transcription factor NtERF172 confers drought resistance by modifying NtCAT,” Plant Biotechnology Journal, vol. 18, no. 12, pp. 2444–2455, 2020. https://doi:10.1111/pbi.13419.
39. P. N. de Oliveira et al., “Overexpression of TgERF1, a Transcription Factor from Tectona grandis, Increases Tolerance to Drought and Salt Stress in Tobacco,” International Journal of Molecular Sciences, vol. 24, no. 4, p. 4149, 2023. https://doi:10.3390/ijms24044149.
40. X. Wang, H. Han, J. Yan, F. Chen and W. Wei, “A New AP2/ERF Transcription Factor from the Oil Plant Jatropha curcas Confers Salt and Drought Tolerance to Transgenic Tobacco,” Applied Biochemistry and Biotechnology, vol. 176, no. 2, pp. 582–597, 2015. https://doi: 10.1007/s12010-015-1597-z.
41. Y. Guo, R. Huang, L. Duan and J. Wang, “The APETALA2/ethylene-responsive factor transcription factor OsDERF2 negatively modulates drought stress in rice by repressing abscisic acid responsive genes,” The Journal of Agricultural Science, vol. 155, no. 6, pp. 966–977, 2017. https://doi:10.1017/S0021859617000041.
42. Y. Jin et al., “OsERF101, an ERF family transcription factor, regulates drought stress response in reproductive tissues,” Plant Molecular Biology, vol. 98, no. 1–2, pp. 51–65, 2018. https://doi:10.1007/s11103-018-0762-5.
43. Y. Pan, G. B. Seymour, C. Lu, Z. Hu, X. Chen and G. Chen, “An ethylene response factor (ERF5) promoting adaptation to drought and salt tolerance in tomato,” Plant Cell Reports, vol. 31, no. 2, pp. 349–360, 2012. https://doi:10.1007/s00299-011-1170-3.
44. M. A. El-Esawi and A. A. Alayafi, “Overexpression of StDREB2 Transcription Factor Enhances Drought Stress Tolerance in Cotton (Gossypium barbadense L.),” Genes (Basel)., vol. 10, no. 2, p. 142, 2019. https://doi:10.3390/genes10020142.
45. D. Bouaziz et al., “Overexpression of StDREB1 Transcription Factor Increases Tolerance to Salt in Transgenic Potato Plants,” Molecular Biotechnology, vol. 54, no. 3, pp. 803–817, 2013. https://doi:10.1007/s12033-012-9628-2.
46. X. Liao et al., “Overexpression of MsDREB6.2 results in cytokinin‐deficient developmental phenotypes and enhances drought tolerance in transgenic apple plants,” Plant Journal, vol. 89, no. 3, pp. 510–526, 2017. https://doi:10.1111/tpj.13401.
47. M. Cui et al., “Induced over-expression of the transcription factor OsDREB2A improves drought tolerance in rice,” Plant Physiology and Biochemistry, vol. 49, no. 12, pp. 1384–1391, 2011. https://doi:10.1016/j.plaphy.2011.09.012.
48. J. Li et al., “OsERF71 confers drought tolerance via modulating ABA signaling and proline biosynthesis,” Plant Science, vol. 270, pp. 131–139, 2018. https://doi:10.1016/j.plantsci.2018.01.017.
49. Y. Gao et al., “NtRAV4 negatively regulates drought tolerance in Nicotiana tabacum by enhancing antioxidant capacity and defence system,” Plant Cell Reports, vol. 41, no. 8, pp. 1775–1788, 2022. https://doi:10.1007/s00299-022-02896-5.
50. Y. Zhang et al., “An APETALA2/ethylene responsive factor, OsEBP89 knockout enhances adaptation to direct-seeding on wet land and tolerance to drought stress in rice,” Molecular Genetics and Genomics, vol. 295, no. 4, pp. 941–956, 2020. https://doi:10.1007/s00438-020-01669-7.
51. M. A. B. Saddique, Z. Ali, M. A. Sher, B. Farid, R. M. Ikram and M. S. Ahmad, “Proline, Total Antioxidant Capacity, and OsP5CS Gene Activity in Radical and Plumule of Rice are Efficient Drought Tolerance Indicator Traits,” International Journal of Agronomy, vol. 2020, pp. 1–9, 2020. https://doi:10.1155/2020/8862792.
52. M. Wang, J. Zhuang, Z. Zou, Q. Li, H. Xin and X. Li, “Overexpression of a Camellia sinensis DREB transcription factor gene (CsDREB) increases salt and drought tolerance in transgenic Arabidopsis thaliana,” Journal of Plant Biology, vol. 60, no. 5, pp. 452–461, 2017. https://doi:10.1007/s12374-016-0547-9.
53. Z. Xie, T. M. Nolan, H. Jiang and Y. Yin, “AP2/ERF Transcription Factor Regulatory Networks in Hormone and Abiotic Stress Responses in Arabidopsis,” Frontiers in Plant Science, vol. 10, 2019. https://doi:10.3389/fpls.2019.00228.