Abstract
Drought is a major abiotic stress that restricts plant growth and development. The AP2/ERF transcription factors (TFs) have been proven to play a unique role in plant growth and drought responses. In this study, the transgenic 84K poplar with ERF016 overexpression (OX) or inhibition (RNA interference, RNAi) was used to examine the function of ERF016 in plant growth, development and drought tolerance. Morphological and physiological methods were used to analyse plant growth, water content, malondialdehyde (MDA) content, proline content, antioxidant enzyme activity, soluble sugar content, soluble starch content and non-structural carbohydrate (NSC) content. Under drought stress conditions, leaf water content and relative water content, aboveground part fresh weight and underground part fresh weight of OX was significantly increased compared with RNAi and the non-transgenic wild-type (WT) plants. In terms of substance synthesis and antioxidant enzyme activity, OX had the highest contents of soluble sugar, soluble starch and NSC, and the highest activity of catalase (CAT) enzyme, which was significantly different from RNAi, but not from WT under drought treatment. Under drought conditions, proline content and peroxidase (POD) enzyme activity of OX were the lowest, which were significantly different from WT and RNAi. Compared with the RNAi and WT, OX showed obvious changes in vascular structure, yielding smaller vessels and thicker vessel walls. In addition, the number of lateral roots of OX was increased compared to WT and RNAi under drought treatment. These results provide new evidence that ERF016 regulates poplar growth and drought tolerance.
Similar content being viewed by others
Data availability
All data generated in this study are included in this article and its supplementary information files. Any additional information required to reanalyze the data is available from the corresponding author upon request.
References
Agarwal PK, Jha B (2010) Transcription factors in plants and ABA dependent and independent abiotic stress signalling. Biol Plant 54(2):201–212. https://doi.org/10.1007/s10535-010-0038-7
An JP, Zhang XW, Bi SQ, You CX, Wang XF, Hao YJ (2020) The ERF transcription factor MdERF38 promotes drought stress-induced anthocyanin biosynthesis in apple. Plant J 101(3):573–589. https://doi.org/10.1111/tpj.14555
Awad H, Barigah T, Badel E, Cochard H, Herbette S (2010) Poplar vulnerability to xylem cavitation acclimates to drier soil conditions. Physiol Plant 139(3):280–288. https://doi.org/10.1111/j.1399-3054.2010.01367.x
Barchet GL, Dauwe R, Guy RD, Schroeder WR, Soolanayakanahally RY, Campbell MM, Mansfield SD (2014) Investigating the drought-stress response of hybrid poplar genotypes by metabolite profiling. Tree Physiol 34(11):1203–1219. https://doi.org/10.1093/treephys/tpt080
Bijalwan P, Sharma M, Kaushik P (2022) Review of the effects of drought stress on plants: a systematic approach.https://doi.org/10.20944/preprints202202.0014.v1
Brunner I, Herzog C, Dawes MA, Arend M, Sperisen C (2015) How tree roots respond to drought. Front Plant Sci 6:547. https://doi.org/10.3389/fpls.2015.00547
Chambers-Ostler A, Gloor E, Galbraith D, Groenendijk P, Brienen R (2022) Vessel tapering is conserved along a precipitation gradient in tropical trees of the genus Cedrela. Trees. https://doi.org/10.1007/s00468-022-02345-6
Chen Y, Yao Z, Sun Y, Wang E, Tian C, Sun Y, Liu J, Sun C, Tian L (2022) Current studies of the effects of drought stress on root exudates and rhizosphere microbiomes of crop plant species. Int J Mol Sci 23(4):2374. https://doi.org/10.3390/ijms23042374
Cheng Z, Zhang X, Zhao K, Yao W, Li R, Zhou B, Jiang T (2019) Over-expression of ERF38 gene enhances salt and osmotic tolerance in transgenic poplar. Front Plant Sci 10:1375. https://doi.org/10.3389/fpls.2019.01375
Chinnusamy V, Schumaker K, Zhu JK (2004) Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot 55(395):225–236. https://doi.org/10.1093/jxb/erh005
Cochard H, Barigah ST, Kleinhentz M, Eshel A (2008) Is xylem cavitation resistance a relevant criterion for screening drought resistance among Prunus species? J Plant Physiol 165(9):976–982. https://doi.org/10.1016/j.jplph.2007.07.020
Damour G, Simonneau T, Cochard H, Urban L (2010) An overview of models of stomatal conductance at the leaf level. Plant Cell Environ 33(9):1419–1438. https://doi.org/10.1111/j.1365-3040.2010.02181.x
de Jong SM, Addink EA, Doelman JC (2014) Detecting leaf-water content in Mediterranean trees using high-resolution spectrometry. Int J Appl Earth Obs Geoinf 27:128–136. https://doi.org/10.1016/j.jag.2013.09.011
De Micco V, Aronne G (2012) Morpho-anatomical traits for plant adaptation to drought. In: Plant responses to drought stress. Springer, pp 37–61. https://doi.org/10.1007/978-3-642-32653-0_2
Du C, Sun P, Cheng X, Zhang L, Wang L, Hu J (2022) QTL mapping of drought-related traits in the hybrids of Populus deltoides ’Danhong’xPopulus simonii “Tongliao1.” BMC Plant Biol 22(1):238. https://doi.org/10.1186/s12870-022-03613-w
Echeverria A, Petrone-Mendoza E, Segovia-Rivas A, Figueroa-Abundiz VA, Olson ME (2022) The vessel wall thickness-vessel diameter relationship across woody angiosperms. Am J Bot 109(6):856–873. https://doi.org/10.1002/ajb2.1854
Fonta JE, Giri J, Vejchasarn P, Lynch JP, Brown KM (2022) Spatiotemporal responses of rice root architecture and anatomy to drought. Plant Soil 479(1–2):443–464. https://doi.org/10.1007/s11104-022-05527-w
Gao J (2006) Experimental guidance for plant physiology. China Higher Education Press, Beijing
Gill SS, Anjum NA, Gill R, Yadav S, Hasanuzzaman M, Fujita M, Mishra P, Sabat SC, Tuteja N (2015) Superoxide dismutase–mentor of abiotic stress tolerance in crop plants. Environ Sci Pollut Res Int 22(14):10375–10394. https://doi.org/10.1007/s11356-015-4532-5
Gupta A, Rico-Medina A, Cano-Delgado AI (2020) The physiology of plant responses to drought. Science 368(6488):266–269. https://doi.org/10.1126/science.aaz7614
Javed T, Shabbir R, Ali A, Afzal I, Zaheer U, Gao SJ (2020) Transcription factors in plant stress responses: challenges and potential for sugarcane improvement. Plants 9(4):491. https://doi.org/10.3390/plants9040491
Junttila S, Hölttä T, Salmon Y, Filella I, Peñuelas J (2022) A novel method to simultaneously measure leaf gas exchange and water content. Remote Sens 14(15):3693. https://doi.org/10.3390/rs14153693
Kim HK, Verpoorte R (2010) Sample preparation for plant metabolomics. Phytochem Anal 21(1):4–13. https://doi.org/10.1002/pca.1188
Labbo AM, Mehmood M, Akhtar MN, Khan MJ, Tariq A, Sadiq I (2018) Genome-wide identification of AP2/ERF transcription factors in mungbean (Vigna radiata) and expression profiling of the VrDREB subfamily under drought stress. Crop Pasture Sci 69(10):1009–1019. https://doi.org/10.1071/cp18180
Lehmann S, Funck D, Szabados L, Rentsch D (2010) Proline metabolism and transport in plant development. Amino Acids 39(4):949–962. https://doi.org/10.1007/s00726-010-0525-3
Li J, Guo X, Zhang M, Wang X, Zhao Y, Yin Z, Zhang Z, Wang Y, Xiong H, Zhang H, Todorovska E, Li Z (2018) OsERF71 confers drought tolerance via modulating ABA signaling and proline biosynthesis. Plant Sci 270:131–139. https://doi.org/10.1016/j.plantsci.2018.01.017
Li Q, Shen C, Zhang Y, Zhou Y, Niu M, Wang HL, Lian C, Tian Q, Mao W, Wang X, Liu C, Yin W, Xia X (2022) PePYL4 enhances drought tolerance by modulating water use efficiency and ROS scavenging in Populus. Tree Physiol. https://doi.org/10.1093/treephys/tpac106
Liang X, Zhang L, Natarajan SK, Becker DF (2013) Proline mechanisms of stress survival. Antioxid Redox Signal 19(9):998–1011. https://doi.org/10.1089/ars.2012.5074
Liang Y, Ma F, Li B, Guo C, Hu T, Zhang M, Liang Y, Zhu J, Zhan X (2022) A bHLH transcription factor SlbHLH96 promotes drought tolerance in tomato. Hortic Res. https://doi.org/10.1093/hr/uhac198
Liu L, Cheng Z, Yao W, Wang X, Jia F, Zhou B, Jiang T (2021) Ectopic expression of poplar gene <i>PsnERF138</i> in tobacco confers salt stress tolerance and growth advantages. Forestry Res 1(1):1–9. https://doi.org/10.48130/fr-2021-0013
Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444(2):139–158. https://doi.org/10.1016/j.abb.2005.10.018
Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) AP2/ERF family transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819(2):86–96. https://doi.org/10.1016/j.bbagrm.2011.08.004
Nardini A, Casolo V, Dal Borgo A, Savi T, Stenni B, Bertoncin P, Zini L, McDowell NG (2016) Rooting depth, water relations and non-structural carbohydrate dynamics in three woody angiosperms differentially affected by an extreme summer drought. Plant Cell Environ 39(3):618–627. https://doi.org/10.1111/pce.12646
Rao RCN, Williams JH, Wadia KDR, Hubick KT, Farquhar GD (1993) Crop growth, water-use efficiency and carbon isotope discrimination in groundnut (Arachis hypogaea L.) genotypes under end-of season drought conditions. Ann Appl Biol 122(2):357–367. https://doi.org/10.1111/j.1744-7348.1993.tb04041.x
Rao S, Tian Y, Zhang C, Qin Y, Liu M, Niu S, Li Y, Chen J (2022) The JASMONATE ZIM-domain-OPEN STOMATA1 cascade integrates jasmonic acid and abscisic acid signaling to regulate drought tolerance by mediating stomatal closure in poplar. J Exp Bot. https://doi.org/10.1093/jxb/erac418
Ren Y, Jing Y, Kang X (2021) In vitro induction of tetraploid and resulting trait variation in Populus alba × Populus glandulosa clone 84K. Plant Cell Tissue Organ Cult 146(2):285–296. https://doi.org/10.1007/s11240-021-02068-5
Rosell JA, Olson ME, Anfodillo T (2017) Scaling of xylem vessel diameter with plant size: causes, predictions, and outstanding questions. Curr Forestry Rep 3(1):46–59. https://doi.org/10.1007/s40725-017-0049-0
Shao HB, Chu LY, Jaleel CA, Zhao CX (2008) Water-deficit stress-induced anatomical changes in higher plants. C R Biol 331(3):215–225. https://doi.org/10.1016/j.crvi.2008.01.002
Siemens JA, Zwiazek JJ (2003) Effects of water deficit stress and recovery on the root water relations of trembling aspen (Populus tremuloides) seedlings. Plant Sci 165(1):113–120. https://doi.org/10.1016/s0168-9452(03)00149-3
W GV, Scharwies JD, Dinneny JR (2022) Deconstructing the root system of grasses through an exploration of development, anatomy and function. Plant Cell Environ 45(3):602–619.https://doi.org/10.1111/pce.14270
Wang S, Huang J, Wang X, Fan Y, Liu Q, Han Y (2021) PagERF16 of populus promotes lateral root proliferation and sensitizes to salt stress. Front Plant Sci 12:669143. https://doi.org/10.3389/fpls.2021.669143
Wang S, Fan Y, Du S, Zhao K, Liu Q, Yao W, Zheng T, Han Y (2022) PtaERF194 inhibits plant growth and enhances drought tolerance in poplar. Tree Physiol. https://doi.org/10.1093/treephys/tpac026
Wei N, Zhai Q, Li H, Zheng S, Zhang J, Liu W (2022) Genome-wide identification of ERF transcription factor family and functional analysis of the drought stress-responsive genes in Melilotus albus. Int J Mol Sci 23(19):12023. https://doi.org/10.3390/ijms231912023
Wu C, Lin M, Chen F, Chen J, Liu S, Yan H, Xiang Y (2022) Homologous drought-induced 19 proteins, PtDi19-2 and PtDi19-7, enhance drought tolerance in transgenic plants. Int J Mol Sci 23(6):3371. https://doi.org/10.3390/ijms23063371
Xu P, Ma W, Hu J, Cai W (2022) The nitrate-inducible NAC transcription factor NAC056 controls nitrate assimilation and promotes lateral root growth in Arabidopsis thaliana. PLoS Genet 18(3):e1010090. https://doi.org/10.1371/journal.pgen.1010090
Yang F, Miao L-F (2010) Adaptive responses to progressive drought stress in two poplar species originating from different altitudes. Silva Fennica 44(1):23–37
Yang X, Lu M, Wang Y, Wang Y, Liu Z, Chen S (2021) Response mechanism of plants to drought stress. Horticulturae 7(3):50. https://doi.org/10.3390/horticulturae7030050
Yao C, Li X, Li Y, Yang G, Liu W, Shao B, Zhong J, Huang P, Han D (2022) Overexpression of a Malus baccata MYB transcription factor gene MbMYB4 increases cold and drought tolerance in Arabidopsis thaliana. Int J Mol Sci 23(3):1794. https://doi.org/10.3390/ijms23031794
Zandi P, Schnug E (2022) Reactive oxygen species, antioxidant responses and implications from a microbial modulation perspective. Biology 11(2):155. https://doi.org/10.3390/biology11020155
Zhang Z, Qu W-j, Li X-f (2004) Plant physiology experiment guidance. China Agricultural Science and Technology Press, Beijing (in Chinese)
Zhang Y, Zhu J, Khan M, Wang Y, Xiao W, Fang T, Qu J, Xiao P, Li C, Liu JH (2022) Transcription factors ABF4 and ABR1 synergistically regulate amylase-mediated starch catabolism in drought tolerance. Plant Physiol. https://doi.org/10.1093/plphys/kiac428
Zhao MJ, Yin LJ, Liu Y, Ma J, Zheng JC, Lan JH, Fu JD, Chen M, Xu ZS, Ma YZ (2019) The ABA-induced soybean ERF transcription factor gene GmERF75 plays a role in enhancing osmotic stress tolerance in Arabidopsis and soybean. BMC Plant Biol 19(1):506. https://doi.org/10.1186/s12870-019-2066-6
Acknowledgements
Many thanks to Lin Wang, Changhong Yu, Siyuan Nan and Yajing Li of Shanxi Agricultural University for their great help in this study.
Funding
This work was supported by the Opening Project of State Key Laboratory of Tree Genetics and Breeding (K2021104), the Natural Science Foundation of Shanxi Province (20210302123425, 202103021223150), the Biobreeding Project of Shanxi Agricultural University (YZGC140), the Scientific and Technologial Innovation Programs of Higher Education Institutions in Shanxi (2021L099) and the National Natural Science Foundation of China (31800564).
Author information
Authors and Affiliations
Contributions
SJW, YZH and KZ planned and designed the research. SQZ, ZZX, XHH, JH, LDZ and XJ performed experiments. SQZ and ZZX analysed data. SQZ wrote the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Bo Ouyang.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zou, S., Xu, Z., Huan, X. et al. Transcription factor ERF016 regulates vascular structure and water metabolism to enhance drought tolerance in poplar. Plant Growth Regul 100, 619–632 (2023). https://doi.org/10.1007/s10725-022-00956-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-022-00956-0