Arabidopsis Cys2/His2 Zinc Finger Transcription Factor ZAT18 Modulates the Plant Growth-Defense Tradeoff
Abstract
:1. Introduction
2. Results
2.1. ZAT18 Mediated Plant Responses to SA
2.2. ZAT18 Enhanced Plant Resistance to Psm ES4326
2.3. ZAT18 Suppressed Plant Growth by Repressing Auxin Signaling
2.4. ZAT18 Oppositely Regulated Defense- and Growth-Related Pathways
3. Discussion
4. Materials and Methods
4.1. Plant Materials, Growth Conditions and Phytohormone Treatments
4.2. Pathogen Inoculation
4.3. Construction for Creating Transgenic Plants
4.4. Total RNA Extraction and qRT-PCR
4.5. Transcriptome Sequencing
4.6. Statistical Analyses
4.7. The Measurements of Root Length, Fresh Weight, Cell Size and Cell Number
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Ngou, B.P.M.; Ding, P.T.; Jones, J.D.G. Thirty years of resistance: Zig-zag through the plant immune system. Plant Cell 2022, 34, 1447–1478. [Google Scholar] [PubMed]
- Jones, J.D.; Dangl, J.L. The plant immune system. Nature 2006, 444, 323–329. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Huot, B.; Yao, J.; Montgomery, B.L.; He, S.Y. Growth-defense tradeoffs in plants: A balancing act to optimize fitness. Mol. Plant 2014, 7, 1267–1287. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hammoudi, V.; Fokkens, L.; Beerens, B.; Vlachakis, G.; Chatterjee, S.; Arroyo-Mateos, M.; Wackers, P.F.K.; Jonker, M.J.; van den Burg, H.A. The Arabidopsis SUMO E3 ligase SIZ1 mediates the temperature dependent trade-off between plant immunity and growth. PLoS Genet. 2018, 14, e1007157. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, X.; Yin, Z.; Wang, Y.; Cao, S.; Yao, W.; Liu, J.; Lu, X.; Wang, F.; Zhang, G.; Xiao, Y.; et al. Rice cellulose synthase-like protein OsCSLD4 coordinates the trade-off between plant growth and defense. Front. Plant Sci. 2022, 13, 980424. [Google Scholar] [CrossRef]
- Liu, N.; Xu, Y.; Li, Q.; Cao, Y.; Yang, D.; Liu, S.; Wang, X.; Mi, Y.; Liu, Y.; Ding, C.; et al. A lncRNA fine-tunes salicylic acid biosynthesis to balance plant immunity and growth. Cell Host Microbe 2022, 30, 1124–1138.e8. [Google Scholar] [CrossRef]
- Lee, H.; Khatri, A.; Plotnikov, J.M.; Zhang, X.C.; Sheen, J. Complexity in differential peptide-receptor signaling: Response to Segonzac et al. and Mueller et al. commentaries. Plant Cell 2012, 24, 3177–3185. [Google Scholar] [CrossRef] [Green Version]
- Pajerowska-Mukhtar, K.M.; Wang, W.; Tada, Y.; Oka, N.; Tucker, C.L.; Fonseca, J.P.; Dong, X. The HSF-like transcription factor TBF1 is a major molecular switch for plant growth-to-defense transition. Curr. Biol. 2012, 22, 103–112. [Google Scholar] [CrossRef] [Green Version]
- Xu, G.; Yuan, M.; Ai, C.; Liu, L.; Zhuang, E.; Karapetyan, S.; Wang, S.; Dong, X. uORF-mediated translation allows engineered plant disease resistance without fitness costs. Nature 2017, 545, 491–494. [Google Scholar] [CrossRef] [Green Version]
- Van Butselaar, T.; Van den Ackerveken, G. Salicylic Acid Steers the Growth-Immunity Tradeoff. Trends Plant Sci. 2020, 25, 566–576. [Google Scholar] [CrossRef]
- Berens, M.L.; Wolinska, K.W.; Spaepen, S.; Ziegler, J.; Nobori, T.; Nair, A.; Kruler, V.; Winkelmuller, T.M.; Wang, Y.; Mine, A.; et al. Balancing trade-offs between biotic and abiotic stress responses through leaf age-dependent variation in stress hormone cross-talk. Proc. Natl. Acad. Sci. USA 2019, 116, 2364–2373. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Campos, M.L.; Yoshida, Y.; Major, I.T.; de Oliveira Ferreira, D.; Weraduwage, S.M.; Froehlich, J.E.; Johnson, B.F.; Kramer, D.M.; Jander, G.; Sharkey, T.D.; et al. Rewiring of jasmonate and phytochrome B signalling uncouples plant growth-defense tradeoffs. Nat. Commun. 2016, 7, 12570. [Google Scholar] [CrossRef] [Green Version]
- Peng, Y.; Yang, J.; Li, X.; Zhang, Y. Salicylic Acid: Biosynthesis and Signaling. Annu. Rev. Plant Biol. 2021, 72, 761–791. [Google Scholar] [CrossRef]
- Rekhter, D.; Ludke, D.; Ding, Y.; Feussner, K.; Zienkiewicz, K.; Lipka, V.; Wiermer, M.; Zhang, Y.; Feussner, I. Isochorismate-derived biosynthesis of the plant stress hormone salicylic acid. Science 2019, 365, 498–502. [Google Scholar] [CrossRef] [PubMed]
- Torrens-Spence, M.P.; Bobokalonova, A.; Carballo, V.; Glinkerman, C.M.; Pluskal, T.; Shen, A.; Weng, J.K. PBS3 and EPS1 Complete Salicylic Acid Biosynthesis from Isochorismate in Arabidopsis. Mol. Plant 2019, 12, 1577–1586. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, Y.; Sun, T.; Sun, Y.; Zhang, Y.; Radojicic, A.; Ding, Y.; Tian, H.; Huang, X.; Lan, J.; Chen, S.; et al. Diverse Roles of the Salicylic Acid Receptors NPR1 and NPR3/NPR4 in Plant Immunity. Plant Cell 2020, 32, 4002–4016. [Google Scholar] [CrossRef]
- Kumar, S.; Zavaliev, R.; Wu, Q.; Zhou, Y.; Cheng, J.; Dillard, L.; Powers, J.; Withers, J.; Zhao, J.; Guan, Z.; et al. Structural basis of NPR1 in activating plant immunity. Nature 2022, 605, 561–566. [Google Scholar] [CrossRef] [PubMed]
- Pokotylo, I.; Hodges, M.; Kravets, V.; Ruelland, E. A ménage à trois: Salicylic acid, growth inhibition, and immunity. Trends Plant Sci. 2021, 27, 460–471. [Google Scholar] [CrossRef]
- Li, A.; Sun, X.; Liu, L. Action of Salicylic Acid on Plant Growth. Front. Plant Sci. 2022, 13, 878076. [Google Scholar] [CrossRef]
- Tan, S.; Abas, M.; Verstraeten, I.; Glanc, M.; Molnar, G.; Hajny, J.; Lasak, P.; Petrik, I.; Russinova, E.; Petrasek, J.; et al. Salicylic Acid Targets Protein Phosphatase 2A to Attenuate Growth in Plants. Curr. Biol. 2020, 30, 381–395.e8. [Google Scholar] [CrossRef]
- Yu, X.; Cui, X.; Wu, C.; Shi, S.; Yan, S. Salicylic acid inhibits gibberellin signaling through receptor interactions. Mol. Plant 2022, 15, 1759–1771. [Google Scholar] [CrossRef]
- Wang, D.; Pajerowska-Mukhtar, K.; Culler, A.H.; Dong, X. Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Curr. Biol. 2007, 17, 1784–1790. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xie, M.; Sun, J.; Gong, D.; Kong, Y. The Roles of Arabidopsis C1-2i Subclass of C2H2-type Zinc-Finger Transcription Factors. Genes 2019, 10, 653. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mittler, R.; Kim, Y.; Song, L.; Coutu, J.; Coutu, A.; Ciftci-Yilmaz, S.; Lee, H.; Stevenson, B.; Zhu, J.K. Gain- and loss-of-function mutations in Zat10 enhance the tolerance of plants to abiotic stress. FEBS Lett. 2006, 580, 6537–6542. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sakamoto, H.; Maruyama, K.; Sakuma, Y.; Meshi, T.; Iwabuchi, M.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Arabidopsis Cys2/His2-type zinc-finger proteins function as transcription repressors under drought, cold, and high-salinity stress conditions. Plant Physiol. 2004, 136, 2734–2746. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rossel, J.B.; Wilson, P.B.; Hussain, D.; Woo, N.S.; Gordon, M.J.; Mewett, O.P.; Howell, K.A.; Whelan, J.; Kazan, K.; Pogson, B.J. Systemic and intracellular responses to photooxidative stress in Arabidopsis. Plant Cell 2007, 19, 4091–4110. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sakamoto, H.; Araki, T.; Meshi, T.; Iwabuchi, M. Expression of a subset of the Arabidopsis Cys(2)/His(2)-type zinc-finger protein gene family under water stress. Gene 2000, 248, 23–32. [Google Scholar] [CrossRef]
- Dang, F.; Li, Y.; Wang, Y.; Lin, J.; Du, S.; Liao, X. ZAT10 plays dual roles in cadmium uptake and detoxification in Arabidopsis. Front. Plant Sci. 2022, 13, 994100. [Google Scholar] [CrossRef]
- Nguyen, X.C.; Kim, S.H.; Lee, K.; Kim, K.E.; Liu, X.M.; Han, H.J.; Hoang, M.H.; Lee, S.W.; Hong, J.C.; Moon, Y.H.; et al. Identification of a C2H2-type zinc finger transcription factor (ZAT10) from Arabidopsis as a substrate of MAP kinase. Plant Cell Rep. 2012, 31, 737–745. [Google Scholar] [CrossRef]
- Ciftci-Yilmaz, S.; Morsy, M.R.; Song, L.; Coutu, A.; Krizek, B.A.; Lewis, M.W.; Warren, D.; Cushman, J.; Connolly, E.L.; Mittler, R. The EAR-motif of the Cys2/His2-type zinc finger protein Zat7 plays a key role in the defense response of Arabidopsis to salinity stress. J. Biol. Chem. 2007, 282, 9260–9268. [Google Scholar] [CrossRef]
- Yin, M.; Wang, Y.; Zhang, L.; Li, J.; Quan, W.; Yang, L.; Wang, Q.; Chan, Z. The Arabidopsis Cys2/His2 zinc finger transcription factor ZAT18 is a positive regulator of plant tolerance to drought stress. J. Exp. Bot. 2017, 68, 2991–3005. [Google Scholar] [CrossRef] [PubMed]
- Ding, Y.; Sun, T.; Ao, K.; Peng, Y.; Zhang, Y.; Li, X.; Zhang, Y. Opposite Roles of Salicylic Acid Receptors NPR1 and NPR3/NPR4 in Transcriptional Regulation of Plant Immunity. Cell 2018, 173, 1454–1467.e15. [Google Scholar] [CrossRef] [PubMed]
- Wang, D.; Amornsiripanitch, N.; Dong, X. A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. PLoS Pathog. 2006, 2, e123. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kong, X.; Pan, W.; Sun, N.; Zhang, T.; Liu, L.; Zhang, H. GLABRA2-based selection efficiently enriches Cas9-generated nonchimeric mutants in the T1 generation. Plant Physiol. 2021, 187, 758–768. [Google Scholar] [CrossRef]
- Zhang, Y.; Li, X. Salicylic acid: Biosynthesis, perception, and contributions to plant immunity. Curr. Opin. Plant Biol. 2019, 50, 29–36. [Google Scholar] [CrossRef]
- Okumura, K.; Goh, T.; Toyokura, K.; Kasahara, H.; Takebayashi, Y.; Mimura, T.; Kamiya, Y.; Fukaki, H. GNOM/FEWER ROOTS is Required for the Establishment of an Auxin Response Maximum for Arabidopsis Lateral Root Initiation. Plant Cell Physiol. 2013, 54, 406–417. [Google Scholar] [CrossRef] [Green Version]
- Goh, T.; Kasahara, H.; Mimura, T.; Kamiya, Y.; Fukaki, H. Multiple AUX/IAA-ARF modules regulate lateral root formation: The role of Arabidopsis SHY2/IAA3-mediated auxin signalling. Philos. Trans. R Soc. Lond. B Biol. Sci. 2012, 367, 1461–1468. [Google Scholar] [CrossRef] [Green Version]
- Chen, Q.; Dai, X.; De-Paoli, H.; Cheng, Y.; Takebayashi, Y.; Kasahara, H.; Kamiya, Y.; Zhao, Y. Auxin overproduction in shoots cannot rescue auxin deficiencies in Arabidopsis roots. Plant Cell Physiol. 2014, 55, 1072–1079. [Google Scholar] [CrossRef] [Green Version]
- Hou, S.; Tsuda, K. Salicylic acid and jasmonic acid crosstalk in plant immunity. Essays Biochem. 2022, 66, 647–656. [Google Scholar]
- Muller, M. Foes or Friends: ABA and Ethylene Interaction under Abiotic Stress. Plants 2021, 10, 448. [Google Scholar] [CrossRef]
- Lee, S.C.; Luan, S. ABA signal transduction at the crossroad of biotic and abiotic stress responses. Plant Cell Environ. 2012, 35, 53–60. [Google Scholar] [CrossRef] [PubMed]
- Ali, M.S.; Baek, K.H. Jasmonic Acid Signaling Pathway in Response to Abiotic Stresses in Plants. Int. J. Mol. Sci. 2020, 21, 621. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Huang, H.; Liu, B.; Liu, L.; Song, S. Jasmonate action in plant growth and development. J. Exp. Bot. 2017, 68, 1349–1359. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xie, Q.; Essemine, J.; Pang, X.; Chen, H.; Jin, J.; Cai, W. Abscisic Acid Regulates the Root Growth Trajectory by Reducing Auxin Transporter PIN2 Protein Levels in Arabidopsis thaliana. Front. Plant Sci. 2021, 12, 632676. [Google Scholar] [CrossRef]
- Rehman, A.; Wang, N.; Peng, Z.; He, S.; Zhao, Z.; Gao, Q.; Wang, Z.; Li, H.; Du, X. Identification of C2H2 subfamily ZAT genes in Gossypium species reveals GhZAT34 and GhZAT79 enhanced salt tolerance in Arabidopsis and cotton. Int. J. Biol. Macromol. 2021, 184, 967–980. [Google Scholar] [CrossRef]
- Shi, H.; Wang, X.; Ye, T.; Chen, F.; Deng, J.; Yang, P.; Zhang, Y.; Chan, Z. The Cysteine2/Histidine2-Type Transcription Factor Zinc Finger of Arabidopsis thaliana6 Modulates Biotic and Abiotic Stress Responses by Activating Salicylic Acid-Related Genes and C-repeat-binding factor genes in Arabidopsis. Plant Physiol. 2014, 165, 1367–1379. [Google Scholar] [CrossRef] [Green Version]
- Chen, J.; Yang, L.; Yan, X.; Liu, Y.; Wang, R.; Fan, T.; Ren, Y.; Tang, X.; Xiao, F.; Liu, Y.; et al. Zinc-Finger Transcription Factor ZAT6 Positively Regulates Cadmium Tolerance through the Glutathione-Dependent Pathway in Arabidopsis. Plant Physiol. 2016, 171, 707–719. [Google Scholar] [CrossRef]
- Chang, M.; Chen, H.; Liu, F.; Fu, Z.Q. PTI and ETI: Convergent pathways with diverse elicitors. Trends Plant Sci. 2022, 27, 113–115. [Google Scholar] [CrossRef]
- Gao, Y.; Li, Z.; Yang, C.; Li, G.; Zeng, H.; Li, Z.; Zhang, Y.; Yang, X. Pseudomonas syringae activates ZAT18 to inhibit salicylic acid accumulation by repressing EDS1 transcription for bacterial infection. New Phytol. 2022, 233, 1274–1288. [Google Scholar] [CrossRef]
- Rong, D.; Luo, N.; Mollet, J.C.; Liu, X.; Yang, Z. Salicylic Acid Regulates Pollen Tip Growth through an NPR3/NPR4-Independent Pathway. Mol. Plant 2016, 9, 1478–1491. [Google Scholar] [CrossRef] [Green Version]
- Yuan, H.M.; Liu, W.C.; Lu, Y.T. CATALASE2 Coordinates SA-Mediated Repression of Both Auxin Accumulation and JA Biosynthesis in Plant Defenses. Cell Host Microbe 2017, 21, 143–155. [Google Scholar] [CrossRef] [PubMed]
- Manohar, M.; Tian, M.; Moreau, M.; Park, S.W.; Choi, H.W.; Fei, Z.; Friso, G.; Asif, M.; Manosalva, P.; von Dahl, C.C.; et al. Identification of multiple salicylic acid-binding proteins using two high throughput screens. Front. Plant Sci. 2014, 5, 777. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Spoel, S.H.; Mou, Z.; Tada, Y.; Spivey, N.W.; Genschik, P.; Dong, X. Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity. Cell 2009, 137, 860–872. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, Y.L.; Tessaro, M.J.; Lassner, M.; Li, X. Knockout analysis of Arabidopsis transcription factors TGA2, TGA5, and TGA6 reveals their redundant and essential roles in systemic acquired resistance. Plant Cell 2003, 15, 2647–2653. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xing, H.L.; Dong, L.; Wang, Z.P.; Zhang, H.Y.; Han, C.Y.; Liu, B.; Wang, X.C.; Chen, Q.J. A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol. 2014, 14, 327. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, W.W.; Zhao, D.; Dong, J.W.; Kong, X.L.; Zhang, Q.; Li, T.T.; Meng, Y.L.; Shan, W.X. AtRTP5 negatively regulates plant resistance to Phytophthora pathogens by modulating the biosynthesis of endogenous jasmonic acid and salicylic acid. Mol. Plant Pathol. 2020, 21, 95–108. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Clough, S.J.; Bent, A.F. Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1998, 16, 735–743. [Google Scholar] [CrossRef]
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Li, W.; Zhang, M.; Zhang, T.; Liu, Y.; Liu, L. Arabidopsis Cys2/His2 Zinc Finger Transcription Factor ZAT18 Modulates the Plant Growth-Defense Tradeoff. Int. J. Mol. Sci. 2022, 23, 15436. https://doi.org/10.3390/ijms232315436
Li W, Zhang M, Zhang T, Liu Y, Liu L. Arabidopsis Cys2/His2 Zinc Finger Transcription Factor ZAT18 Modulates the Plant Growth-Defense Tradeoff. International Journal of Molecular Sciences. 2022; 23(23):15436. https://doi.org/10.3390/ijms232315436
Chicago/Turabian StyleLi, Weiwei, Min Zhang, Tingyu Zhang, Yueyan Liu, and Lijing Liu. 2022. "Arabidopsis Cys2/His2 Zinc Finger Transcription Factor ZAT18 Modulates the Plant Growth-Defense Tradeoff" International Journal of Molecular Sciences 23, no. 23: 15436. https://doi.org/10.3390/ijms232315436