Abstract
Homeodomain-leucine zipper (HD-Zip) IV transcription factors are integral in the plant response to abiotic stressors. In maize, few HD-Zip IV proteins have yet been reported, and the functions are not well understood. In the current study, we isolated ZmHDZIV14 from the HD-Zip IV transcription factor family from maize and characterized its role in the stress response. We conducted a phylogenetic analysis showing that there was high homology and thus likely similar functions between ZmHDZIV14 and AtHDG11. Heterologous overexpression of ZmHDZIV14 in Arabidopsis caused increased sensitivity to abscisic acid (ABA), tolerance of salt and mannitol at germination stage, and drought tolerance of seedlings. ZmHDZIV14 transgenic Arabidopsis lines placed under drought stress additionally displayed lower levels of malondialdehyde, higher proline, and relative water content, compared to the wild-type. Further, modified tobacco plants (35S::ZmHDZIV14) responded to drought conditions with appropriate stomatal changes. After drought was relieved, expression of P5CS1, RD22, RD29B, RAB18, NCED3, and ERD1 were upregulated in transgenic Arabidopsis. It can be seen ZmHDZIV14 expression resulted in physiological and molecular changes in the transgenic lines, which improved overall drought tolerance. In summary, our results indicate that ZmHDZIV14 is a transcriptional regulator that modifies an ABA-dependent signaling pathway to regulate the drought response in plants.
Similar content being viewed by others
Abbreviations
- HD-Zip:
-
homeodomain-leucine zippe
- ABA:
-
abscisic acid
- START:
-
steroidogenic acute regulatory protein-related lipid transfer
- Pro:
-
proline
- SOD:
-
superoxide dismutas
- MDA:
-
malondialdehyde
- NaCl:
-
salt
- WT:
-
wild-type
- MS:
-
Murashige and Skoog
- RWC:
-
relative water content
- WUE:
-
water use efficiency
- P :
-
photosynthetic
- T :
-
transpiration
- ROS:
-
reactive oxygen species
References
Agalou A et al (2008) A genome-wide survey of HD-zip genes in rice and analysis of drought-responsive family members. Plant Mol Biol 66:87–103. https://doi.org/10.1007/s11103-007-9255-7
Ariel FD, Manavella PA, Dezar CA, Chan RL (2007) The true story of the HD-Zip family. Trends Plant Sci 12:419–426. https://doi.org/10.1016/j.tplants.2007.08.003
Aso K, Kato M, Banks JA, Hasebe M (1999) Characterization of homeodomain-leucine zipper genes in the fern Ceratopteris richardii and the evolution of the homeodomain-leucine zipper gene family in vascular plants. Mol Biol Evol 16:544–552. https://doi.org/10.1093/oxfordjournals.molbev.a026135
Badis G et al (2009) Diversity and complexity in DNA recognition by transcription factors. Science 324:1720–1723. https://doi.org/10.1126/science.1162327
Cai W, Yang Y, Wang W, Guo G, Liu W, Bi C (2018) Overexpression of a wheat (Triticum aestivum L.) bZIP transcription factor gene, TabZIP6, decreased the freezing tolerance of transgenic Arabidopsis seedlings by down-regulating the expression of CBFs. Plant Physiol Biochem 124:100–111. https://doi.org/10.1016/j.plaphy.2018.01.008
Cao YJ, Wei Q, Liao Y, Song HL, Li X, Xiang CB, Kuai BK (2009) Ectopic overexpression of AtHDG11 in tall fescue resulted in enhanced tolerance to drought and salt stress. Plant Cell Rep 28:579–588. https://doi.org/10.1007/s00299-008-0659-x
Chen E et al (2017) Genome-wide analysis of the HD-ZIP IV transcription factor family in Gossypium arboreum and GaHDG11 involved in osmotic tolerance in transgenic Arabidopsis. Mol Gen Genomics 292:593–609. https://doi.org/10.1007/s00438-017-1293-5
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743. https://doi.org/10.1046/j.1365-313x.1998.00343.x
Depège-Fargeix N et al (2011) Functional characterization of the HD-ZIP IV transcription factor OCL1 from maize. J Exp Bot 62:293–305. https://doi.org/10.1093/jxb/erq267
Dezar CA, Gago GM, Gonzalez DH, Chan RL (2005) Hahb-4, a sunflower homeobox-leucine zipper gene, is a developmental regulator and confers drought tolerance to Arabidopsis thaliana plants. Transgenic Res 14:429–440. https://doi.org/10.1007/s11248-005-5076-0
Di Cristina M, Sessa G, Dolan L, Linstead P, Baima S, Ruberti I, Morelli G (1996) The Arabidopsis Athb-10 (GLABRA2) is an HD-Zip protein required for regulation of root hair development. Plant J 10:393–402. https://doi.org/10.1046/j.1365-313x.1996.10030393.x
Gago G, Almoguera C, Jordano J, Gonzalez D, Chan R (2002) Hahb-4, a Homeobox-Leucine zipper gene potentially involved in abscisic acid-dependent responses to water stress in sunflower plant. Cell Environ 25:633–640. https://doi.org/10.1046/j.1365-3040.2002.00853.x
Hobert O (2008) Gene regulation by transcription factors and microRNAs. Science 319:1785–1786. https://doi.org/10.1126/science.1151651
Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 47:377–403. https://doi.org/10.1146/annurev.arplant.47.1.377
Javelle M, Vernoud V, Rogowsky PM, Ingram GC (2011) Epidermis: the formation and functions of a fundamental plant tissue. New Phytol 189:17–39. https://doi.org/10.1111/j.1469-8137.2010.03514.x
Khosla A, Paper JM, Boehler AP, Bradley AM, Neumann TR, Schrick K (2014) HD-Zip proteins GL2 and HDG11 have redundant functions in Arabidopsis trichomes, and GL2 activates a positive feedback loop via MYB23. Plant Cell 26:2184–2200. https://doi.org/10.1105/tpc.113.120360
Mao H, Yu L, Li Z, Liu H, Han R (2016) Molecular evolution and gene expression differences within the HD-Zip transcription factor family of Zea mays L. Genetica 144:243–257. https://doi.org/10.1007/s10709-016-9896-z
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410. https://doi.org/10.1016/s1360-1385(02)02312-9
Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498. https://doi.org/10.1016/j.tplants.2004.08.009
Nakamura M, Katsumata H, Abe M, Yabe N, Komeda Y, Yamamoto KT, Takahashi T (2006) Characterization of the class IV homeodomain-Leucine Zipper gene family in Arabidopsis. Plant Physiol 141:1363–1375. https://doi.org/10.1104/pp.106.077388
Nauš J, Šmecko S, Špundová M (2016) Chloroplast avoidance movement as a sensitive indicator of relative water content during leaf desiccation in the dark. Photosynth Res 129:217–225. https://doi.org/10.1007/s11120-016-0291-5
Rerie WG, Feldmann KA, Marks MD (1994) The GLABRA2 gene encodes a homeo domain protein required for normal trichome development in Arabidopsis. Genes Dev 8:1388–1399. https://doi.org/10.1101/gad.8.12.1388
Schrick K, Nguyen D, Karlowski WM, Mayer KF (2004) START lipid/sterol-binding domains are amplified in plants and are predominantly associated with homeodomain transcription factors. Genome Biol 5:R41. https://doi.org/10.1186/gb-2004-5-6-r41
Sessa G, Steindler C, Morelli G, Ruberti I (1998) The Arabidopsis Athb-8, -9 and -14 genes are members of a small gene family coding for highly related HD-ZIP proteins. Plant Mol Biol 38:609–622. https://doi.org/10.1023/a:1006016319613
Sharma P, Jha A, Dubey R, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012:1–26. https://doi.org/10.1155/2012/217037
Shinozaki K, Yamaguchi-Shinozaki K (1997) Gene expression and signal transduction in water-stress response. Plant Physiol 115:327–334. https://doi.org/10.1104/pp.115.2.327
Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227. https://doi.org/10.1093/jxb/erl164
Tao Y, Chen M, Shu Y, Zhu Y, Wang S, Huang L, Yu X, Wang Z, Qian P, Gu W, Ma H (2018) Identification and functional characterization of a novel BEL1-LIKE homeobox transcription factor GmBLH4 in soybean. Plant Cell Tissue Organ Cult (PCTOC) 134:331–344. https://doi.org/10.1007/s11240-018-1419-4
Verslues PE, Agarwal M, Katiyar-Agarwal S, Zhu J, Zhu JK (2006) Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant J 45:523–539. https://doi.org/10.1111/j.1365-313X.2005.02593.x
Wei Q, Song HL, Xiang CB (2010) Preliminary study on improving drought tolerance of ryegrass (Lolium perenne) by overexpressing a HD-START transcription factor AtHDG11 from Arabidopsis. Plant Physiol Commun 46:1140–1146
Wei Q, Kuai B, Hu P, Ding Y (2012) Ectopic-overexpression of an HD-zip IV transcription factor from Ammopiptanthus mongolicus (Leguminosae) promoted upward leaf curvature and non-dehiscent anthers in Arabidopsis thaliana. Plant Cell Tissue Organ Cult (PCTOC) 110:299–306. https://doi.org/10.1007/s11240-012-0151-8
Wu Z, Liang J, Wang C, Zhao X, Zhong X, Cao X, Li G, He J, Yi M (2018) Overexpression of lily HsfA3s in Arabidopsis confers increased thermotolerance and salt sensitivity via alterations in proline catabolism. J Exp Bot 69:2005–2021. https://doi.org/10.1093/jxb/ery035
Xiong L, Wang RG, Mao G, Koczan JM (2006) Identification of drought tolerance determinants by genetic analysis of root response to drought stress and abscisic. Acid Plant Physiol 142:1065–1074. https://doi.org/10.1104/pp.106.084632
Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803. https://doi.org/10.1146/annurev.arplant.57.032905.105444
Yoshiba Y, Nanjo T, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Stress-responsive and developmental regulation of Delta(1)-pyrroline-5-carboxylate synthetase 1 (P5CS1) gene expression in Arabidopsis thaliana. Biochem Biophys Res Commun 261:766–772. https://doi.org/10.1006/bbrc.1999.1112
Yu L et al (2013) Arabidopsis enhanced drought tolerance1/HOMEODOMAIN GLABROUS11 confers drought tolerance in transgenic rice without yield penalty. Plant Physiol 162:1378–1391. https://doi.org/10.1104/pp.113.217596
Yu LH et al (2016) Arabidopsis EDT1/HDG11 improves drought and salt tolerance in cotton and poplar and increases cotton yield in the field. Plant Biotechnol J 14:72–84. https://doi.org/10.1111/pbi.12358
Zhao Y, Zhou Y, Jiang H, Li X, Gan D, Peng X, Zhu S, Cheng B (2011) Systematic analysis of sequences and expression patterns of drought-responsive members of the HD-Zip gene family in maize. PLoS One 6:e28488. https://doi.org/10.1371/journal.pone.0028488
Zhao Y et al (2014) A novel maize homeodomain-leucine zipper (HD-Zip) I gene, Zmhdz10, positively regulates drought and salt tolerance in both rice and Arabidopsis. Plant Cell Physiol 55:1142–1156. https://doi.org/10.1093/pcp/pcu054
Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273. https://doi.org/10.1146/annurev.arplant.53.091401.143329
Zhu Z et al (2016) Overexpression of AtEDT1/HDG11 in Chinese kale (Brassica oleracea var. alboglabra) enhances drought and osmotic stress tolerance. Front Plant Sci 7:1285. https://doi.org/10.3389/fpls.2016.01285
Funding
This research was supported by the Research Program Sponsored by Gansu Provincial Key Laboratory of Aridland Crop Science, Gansu Agricultural University (No. GHSJ-2020-Z5), National Key R&D Program of China (No. 2018YFD0100203-4), the CAS “Light of West China” Program (No. 20180504), the Natural Science Foundation of Gansu, China (No. 18JR3RA189), the Fuxi Talent Project of Gansu Agricultural University, China (No. GAUFX-02Y09), and the Major R&D Program of Gansu, China (No. 18YF1NA071).
Author information
Authors and Affiliations
Contributions
YP designed the experiments. PF and HY performed the experiments. PF and HY analyzed the data. YP, PF, and FC wrote the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Competing Interests
The authors declared that they have no competing interests.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Key Message
• ZmHDZIV14 was isolated from maize HD-Zip IV transcription factor family for the first time.
• Heterologous overexpression of ZmHDZIV14 in Arabidopsis increased tolerance of salt and mannitol at germination stage, and increased drought tolerance of seedlings.
• ZmHDZIV14 modified ABA-dependent signaling pathway to regulate the drought response in plants.
Rights and permissions
About this article
Cite this article
Fang, P., Yan, H., Chen, F. et al. Overexpression of Maize ZmHDZIV14 Increases Abscisic Acid Sensitivity and Mediates Drought and Salt Stress in Arabidopsis and Tobacco. Plant Mol Biol Rep 39, 275–287 (2021). https://doi.org/10.1007/s11105-020-01252-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11105-020-01252-9