The Peptide-Encoding CLE25 Gene Modulates Drought Response in Cotton
Abstract
:1. Introduction
2. Materials and Methods
2.1. Plant Materials and Growth Conditions
2.2. qRT-PCR Analysis
2.3. Virus-Induced Gene Silencing
2.4. Drought Stress Treatment
2.5. Synthesis of Peptide CLE25p and Spraying Assay
2.6. Determination of Physiological Indexes and Phenotypic Parameters
2.7. RNA-Seq Analysis
2.8. Statistical Analyses
3. Results
3.1. GhCLE25 Is Involved in the Response to Drought and Salt Stresses
3.2. The Downregulation of GhCLE25 Reduces Drought Tolerance in Cotton
3.3. Exogenous CLE25p Application Enhances Drought Tolerance
3.4. Comparative Transcriptome Analysis Revealed the CLE25-Mediated Signaling Pathway
4. Discussion
4.1. GhCLE25 Probably Played a Positive Role in the Response to Drought Stress in Cotton
4.2. CLE25-Mediated Signaling Pathway Mainly Involved in Defense Response in Cotton
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
CLE | CLAVATA3 (CLV3)/ENDOSPERM SURROUNDING REGION CLE (ESR) |
NCED3 | 9-CISEPOXYCAROTENOID DIOXYGENASE 3 |
ABA | Abscisic acid |
ROS | Reactive oxygen species |
References
- Casal, J.J.; Balasubramanian, S. Thermomorphogenesis. Annu. Rev. Plant Biol. 2019, 70, 321–346. [Google Scholar] [CrossRef]
- van Zelm, E.; Zhang, Y.; Testerink, C. Salt Tolerance Mechanisms of Plants. Annu. Rev. Plant Biol. 2020, 71, 403–433. [Google Scholar] [CrossRef]
- Saranga, Y.; Paterson, A.H.; Levi, A. Bridging Classical and Molecular Genetics of Abiotic Stress Resistance in Cotton. Genet. Genom. Cotton 2009, 3, 337–352. [Google Scholar]
- Fiers, M.; Ku, K.; Liu, C. CLE Peptide Ligands and Their Roles in Establishing Meristems. Curr. Opin. Plant Biol. 2007, 10, 39–43. [Google Scholar] [CrossRef]
- Betsuyaku, S.; Sawa, S.; Yamada, M. The Function of the CLE Peptides in Plant Development and Plant-Microbe Interactions. Arab. Book 2011, 9, e0149. [Google Scholar] [CrossRef]
- Hirakawa, Y.; Sawa, S. Diverse Function of Plant Peptide Hormones in Local Signaling and Development. Curr. Opin. Plant Biol. 2019, 51, 81–87. [Google Scholar] [CrossRef]
- Fletcher, J.C. Recent Advances in Arabidopsis CLE Peptide Signaling. Trends Plant Sci. 2020, 25, 1005–1016. [Google Scholar] [CrossRef]
- Jeon, B.W.; Kim, M.-J.; Pandey, S.K.; Oh, E.; Seo, P.J.; Kim, J. Recent Advances in Peptide Signaling during Arabidopsis Root Development. J. Exp. Bot. 2021, 72, 2889–2902. [Google Scholar] [CrossRef]
- Matsubayashi, Y. Posttranslationally Modified Small-Peptide Signals in Plants. Annu. Rev. Plant Biol. 2014, 65, 385–413. [Google Scholar] [CrossRef] [PubMed]
- Takahashi, F.; Suzuki, T.; Osakabe, Y.; Betsuyaku, S.; Kondo, Y.; Dohmae, N.; Fukuda, H.; Yamaguchi-Shinozaki, K.; Shinozaki, K. A Small Peptide Modulates Stomatal Control via Abscisic Acid in Long-Distance Signalling. Nature 2018, 556, 235–238. [Google Scholar] [CrossRef] [PubMed]
- Hellens, R.P.; Brown, C.M.; Chisnall, M.A.W.; Waterhouse, P.M.; Macknight, R.C. The Emerging World of Small ORFs. Trends Plant Sci. 2016, 21, 317–328. [Google Scholar] [CrossRef]
- Hsu, P.Y.; Benfey, P.N. Small but Mighty: Functional Peptides Encoded by Small ORFs in Plants. Proteomics 2017, 18, 1700038. [Google Scholar] [CrossRef]
- Ong, S.N.; Tan, B.C.; Al-Idrus, A.; Teo, C.H. Small Open Reading Frames in Plant Research: From Prediction to Functional Characterization. 3 Biotech 2022, 12, 76. [Google Scholar] [CrossRef]
- Tavormina, P.; De Coninck, B.; Nikonorova, N.; De Smet, I.; Cammue, B.P.A. The Plant Peptidome: An Expanding Repertoire of Structural Features and Biological Functions. Plant Cell 2015, 27, 2095–2118. [Google Scholar] [CrossRef]
- Wang, G.; Fiers, M. CLE Peptide Signaling during Plant Development. Protoplasma 2009, 240, 33–43. [Google Scholar] [CrossRef]
- Yamaguchi, Y.L.; Ishida, T.; Sawa, S. CLE Peptides and Their Signaling Pathways in Plant Development. J. Exp. Bot. 2016, 67, 4813–4826. [Google Scholar] [CrossRef]
- Datta, T.; Kumar, R.S.; Sinha, H.; Trivedi, P.K. Small but Mighty: Peptides Regulating Abiotic Stress Responses in Plants. Plant Cell Environ. 2024, 47, 1207–1223. [Google Scholar] [CrossRef]
- Wang, G.; Zhang, G.; Wu, M. CLE Peptide Signaling and Crosstalk with Phytohormones and Environmental Stimuli. Front. Plant Sci. 2016, 6, 1211. [Google Scholar] [CrossRef]
- Zhang, L.; Shi, X.; Zhang, Y.; Wang, J.; Yang, J.; Ishida, T.; Jiang, W.; Han, X.; Kang, J.; Wang, X.; et al. CLE9 Peptide-induced Stomatal Closure Is Mediated by Abscisic Acid, Hydrogen Peroxide, and Nitric Oxide in Arabidopsis Thaliana. Plant Cell Environ. 2019, 42, 1033–1044. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Z.; Liu, C.; Li, K.; Li, X.; Xu, M.; Guo, Y. CLE14 Functions as a “Brake Signal” to Suppress Age-Dependent and Stress-Induced Leaf Senescence by Promoting JUB1-Mediated ROS Scavenging in Arabidopsis. Mol. Plant 2022, 15, 179–188. [Google Scholar] [CrossRef] [PubMed]
- Goad, D.M.; Zhu, C.; Kellogg, E.A. Comprehensive Identification and Clustering of CLV3/ESR-related (CLE) Genes in Plants Finds Groups with Potentially Shared Function. New Phytol. 2016, 216, 605–616. [Google Scholar] [CrossRef] [PubMed]
- Wan, K.; Lu, K.; Gao, M.; Zhao, T.; He, Y.; Yang, D.-L.; Tao, X.; Xiong, G.; Guan, X. Functional Analysis of the Cotton CLE Polypeptide Signaling Gene Family in Plant Growth and Development. Sci. Rep. 2021, 11, 5060. [Google Scholar] [CrossRef] [PubMed]
- McGarry, R.C.; Kaur, H.; Lin, Y.-T.; Puc, G.L.; Eshed Williams, L.; van der Knaap, E.; Ayre, B.G. Altered Expression of SELF-PRUNING Disrupts Homeostasis and Facilitates Signal Delivery to Meristems. Plant Physiol. 2023, 192, 1517–1531. [Google Scholar] [CrossRef]
- Chen, C.; Zhang, D.; Niu, X.; Jin, X.; Xu, H.; Li, W.; Guo, W. MYB30-INTERACTING E3 LIGASE 1 Regulates LONELY GUY 5-Mediated Cytokinin Metabolism to Promote Drought Tolerance in Cotton. Plant Physiol. 2024, 197, kiae580. [Google Scholar] [CrossRef]
- Livak, K.J.; Schmittgen, T.D. Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method. Methods 2001, 25, 402–408. [Google Scholar] [CrossRef]
- Gao, X.; Guo, Y. CLE Peptides in Plants: Proteolytic Processing, Structure-Activity Relationship, and Ligand-Receptor InteractionF. J. Integr. Plant Biol. 2012, 54, 738–745. [Google Scholar] [CrossRef]
- Ito, Y.; Nakanomyo, I.; Motose, H.; Iwamoto, K.; Sawa, S.; Dohmae, N.; Fukuda, H. Dodeca-CLE Peptides as Suppressors of Plant Stem Cell Differentiation. Science 2006, 313, 842–845. [Google Scholar] [CrossRef] [PubMed]
- Cock, J.M.; McCormick, S. A Large Family of Genes That Share Homology withCLAVATA3. Plant Physiol. 2001, 126, 939–942. [Google Scholar] [CrossRef]
- Fiers, M.; Golemiec, E.; Xu, J.; van der Geest, L.; Heidstra, R.; Stiekema, W.; Liu, C.-M. The 14–Amino Acid CLV3, CLE19, and CLE40 Peptides Trigger Consumption of the Root Meristem in Arabidopsis through aCLAVATA2-Dependent Pathway. Plant Cell 2005, 17, 2542–2553. [Google Scholar] [CrossRef]
- Kondo, T.; Sawa, S.; Kinoshita, A.; Mizuno, S.; Kakimoto, T.; Fukuda, H.; Sakagami, Y. A Plant Peptide Encoded by CLV3 Identified by in Situ MALDI-TOF MS Analysis. Science 2006, 313, 845–848. [Google Scholar] [CrossRef]
- Meng, L.; Feldman, L.J. CLE14/CLE20 Peptides May Interact with CLAVATA2/CORYNE Receptor-like Kinases to Irreversibly Inhibit Cell Division in the Root Meristem of Arabidopsis. Planta 2010, 232, 1061–1074. [Google Scholar] [CrossRef] [PubMed]
- Kondo, Y.; Hirakawa, Y.; Kieber, J.J.; Fukuda, H. CLE Peptides Can Negatively Regulate Protoxylem Vessel Formation via Cytokinin Signaling. Plant Cell Physiol. 2010, 52, 37–48. [Google Scholar] [CrossRef]
- Pallakies, H.; Simon, R. The CLE40 and CRN/CLV2 Signaling Pathways Antagonistically Control Root Meristem Growth in Arabidopsis. Mol. Plant 2014, 7, 1619–1636. [Google Scholar] [CrossRef]
- Czyzewicz, N.; Shi, C.-L.; Vu, L.D.; Van De Cotte, B.; Hodgman, C.; Butenko, M.A.; Smet, I.D. Modulation ofArabidopsisand Monocot Root Architecture by CLAVATA3/EMBRYO SURROUNDING REGION 26 Peptide. J. Exp. Bot. 2015, 66, 5229–5243. [Google Scholar] [CrossRef]
- Zhang, Y.; Tan, S.; Gao, Y.; Kan, C.; Wang, H.; Yang, Q.; Xia, X.; Ishida, T.; Sawa, S.; Guo, H.; et al. CLE42 Delays Leaf Senescence by Antagonizing Ethylene Pathway in Arabidopsis. New Phytol. 2022, 235, 550–562. [Google Scholar] [CrossRef]
- Yang, W.; Feng, M.; Yu, K.; Cao, J.; Cui, G.; Zhang, Y.; Peng, H.; Yao, Y.; Hu, Z.; Ni, Z.; et al. The TaCLE24b peptide signaling cascade modulates lateral root development and drought tolerance in wheat. Nat. Commun. 2025, 16, 1952. [Google Scholar] [CrossRef]
- Kant, S.; Bi, Y.-M.; Zhu, T.; Rothstein, S.J. SAUR39, a Small Auxin-Up RNA Gene, Acts as a Negative Regulator of Auxin Synthesis and Transport in Rice. Plant Physiol. 2009, 151, 691–701. [Google Scholar] [CrossRef]
- Kant, S.; Rothstein, S. Auxin-responsiveSAUR39gene Modulates Auxin Level in Rice. Plant Signal. Behav. 2009, 4, 1174–1175. [Google Scholar] [CrossRef]
- Zhang, S.; Yang, R.; Huo, Y.; Liu, S.; Yang, G.; Huang, J.; Zheng, C.; Wu, C. Expression of Cotton PLATZ1 in Transgenic Arabidopsis Reduces Sensitivity to Osmotic and Salt Stress for Germination and Seedling Establishment Associated with Modification of the Abscisic Acid, Gibberellin, and Ethylene Signalling Pathways. BMC Plant Biol. 2018, 18, 218. [Google Scholar] [CrossRef] [PubMed]
- Stokes, M.E.; Chattopadhyay, A.; Wilkins, O.; Nambara, E.; Campbell, M.M. Interplay between Sucrose and Folate Modulates Auxin Signaling in Arabidopsis. Plant Physiol. 2013, 162, 1552–1565. [Google Scholar] [CrossRef] [PubMed]
- Vikas, V.K.; Pradhan, A.K.; Budhlakoti, N.; Mishra, D.C.; Chandra, T.; Bhardwaj, S.C.; Kumar, S.; Sivasamy, M.; Jayaprakash, P.; Nisha, R.; et al. Multi-Locus Genome-Wide Association Studies (ML-GWAS) Reveal Novel Genomic Regions Associated with Seedling and Adult Plant Stage Leaf Rust Resistance in Bread Wheat (Triticum aestivum L.). Heredity 2022, 128, 434–449. [Google Scholar] [CrossRef]
- Juliana, P.; Singh, R.P.; Singh, P.K.; Poland, J.A.; Bergstrom, G.C.; Huerta-Espino, J.; Bhavani, S.; Crossa, J.; Sorrells, M.E. Genome-Wide Association Mapping for Resistance to Leaf Rust, Stripe Rust and Tan Spot in Wheat Reveals Potential Candidate Genes. Theor. Appl. Genet. 2018, 131, 1405–1422. [Google Scholar] [CrossRef] [PubMed]
- Wu, J.; Gao, J.; Bi, W.; Zhao, J.; Yu, X.; Li, Z.; Liu, D.; Liu, B.; Wang, X. Genome-Wide Expression Profiling of Genes Associated with the Lr47-Mediated Wheat Resistance to Leaf Rust (Puccinia triticina). Int. J. Mol. Sci. 2019, 20, 4498. [Google Scholar] [CrossRef]
- Ning, J.; Li, X.; Hicks, L.M.; Xiong, L. A Raf-like MAPKKK gene DSM1 mediates drought resistance through reactive oxygen species scavenging in rice. Plant Physiol. 2010, 152, 876–890. [Google Scholar] [CrossRef] [PubMed]
- Shen, H.; Liu, C.; Zhang, Y.; Meng, X.; Zhou, X.; Chu, C.; Wang, X. OsWRKY30 is activated by MAP kinases to confer drought tolerance in rice. Plant Mol. Biol. 2012, 80, 241–253. [Google Scholar] [CrossRef] [PubMed]
- Depuydt, S.; Rodriguez-Villalon, A.; Santuari, L.; Wyser-Rmili, C.; Ragni, L.; Hardtke, C.S. Suppression of Arabidopsis Protophloem Differentiation and Root Meristem Growth by CLE45 Requires the Receptor-like Kinase BAM3. Proc. Natl. Acad. Sci. USA 2013, 110, 7074–7079. [Google Scholar] [CrossRef]
- Kang, Y.H.; Hardtke, C.S. Arabidopsis MAKR5 Is a Positive Effector of BAM3-Dependent CLE45 Signaling. EMBO Rep. 2016, 17, 1145–1154. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2025 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Zhang, D.; Zhu, Q.; Qin, P.; Yu, L.; Li, W.; Sun, H. The Peptide-Encoding CLE25 Gene Modulates Drought Response in Cotton. Agriculture 2025, 15, 1226. https://doi.org/10.3390/agriculture15111226
Zhang D, Zhu Q, Qin P, Yu L, Li W, Sun H. The Peptide-Encoding CLE25 Gene Modulates Drought Response in Cotton. Agriculture. 2025; 15(11):1226. https://doi.org/10.3390/agriculture15111226
Chicago/Turabian StyleZhang, Dayong, Qingfeng Zhu, Pu Qin, Lu Yu, Weixi Li, and Hao Sun. 2025. "The Peptide-Encoding CLE25 Gene Modulates Drought Response in Cotton" Agriculture 15, no. 11: 1226. https://doi.org/10.3390/agriculture15111226
APA StyleZhang, D., Zhu, Q., Qin, P., Yu, L., Li, W., & Sun, H. (2025). The Peptide-Encoding CLE25 Gene Modulates Drought Response in Cotton. Agriculture, 15(11), 1226. https://doi.org/10.3390/agriculture15111226