Small Cationic Cysteine-Rich Defensin-Derived Antifungal Peptide Controls White Mold in Soybean
Abstract
:1. Introduction
2. Materials and Methods
2.1. Plant and Fungal Materials
2.2. In Vitro Antifungal Activity of GMA4CG_V6 against S. sclerotiorum
2.3. Semi-In Planta Antifungal Activity of GMA4CG_V6 against S. sclerotiorum 555
2.4. In Planta Antifungal Activity of GMA4CG_V6 against S. sclerotiorum 555
2.5. Effect of GMA4CG_V6 on Sclerotia Production in S. sclerotiorum 555
2.6. Effect of GMA4CG_V6 on the Expression of S. sclerotiorum Genes Related to Sclerotia Production
2.7. Plasma Membrane Permeabilization Assay
2.8. Uptake of GMA4CG_V6 by S. sclerotiorum 555 Cells
2.9. Assessment of the Effects of GMA4CG_V6 Treatment on Growth of Soybean Plants
2.10. Statistical Analysis
3. Results
3.1. In Vitro Antifungal Activity of GMA4CG_V6 against S. sclerotiorum 555
3.2. Semi-In Planta Antifungal Activity of GMA4CG_V6 against S. sclerotiorum 555
3.3. Spray Application of GMA4CG_V6 Protects against White Mold Disease in Soybean and N. benthamiana
3.4. GMA4CG_V6 Inhibits Sclerotia Production in S. sclerotiorum 555
3.5. Effect of GMA4CG_V6 on the Expression of S. sclerotiorum Genes Related to Sclerotia Production
3.6. GMA4CG_V6 Is Rapidly Internalized into the Cells of S. sclerotiorum Prior to Permeabilizing Their Plasma Membrane
3.7. GMA4CG_V6 Has No Negative Effect on the Growth of Soybean Plants
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Shahbandeh, M. Production Value of Soybeans in the U.S. 2000–2021. 2022. Available online: www.statista.com/statistics/192071/production-value-of-soybeans-for-beans-in-the-us-since-2000 (accessed on 25 April 2023).
- Allen, T.W.; Bradley, C.A.; Sisson, A.J.; Byamukama, E.; Chilvers, M.I.; Coker, C.M. Soybean yield loss estimates due to diseases in the United States and Ontario, Canada from 2010 to 2014. Plant Health Prog. 2017, 18, 19–27. [Google Scholar] [CrossRef]
- O’Sullivan, C.A.; Belt, K.; Thatcher, L.F. Tackling control of a cosmopolitan phytopathogen: Sclerotinia. Front. Plant Sci. 2021, 12, 707509. [Google Scholar] [CrossRef]
- Bolton, M.D.; Thomma, B.P.; Nelson, B.D. Sclerotinia sclerotiorum (Lib.) de Bary: Biology and molecular traits of a cosmopolitan pathogen. Mol. Plant Pathol. 2006, 7, 1–16. [Google Scholar] [CrossRef]
- Derbyshire, M.C.; Newman, T.E.; Khentry, Y.; Owolabi Taiwo, A. The evolutionary and molecular features of the broad-host-range plant pathogen Sclerotinia sclerotiorum. Mol. Plant Pathol. 2022, 23, 1075–1090. [Google Scholar] [CrossRef] [PubMed]
- Gambhir, N.; Kamvar, Z.N.; Higgins, R.; Amaradasa, B.S.; Everhart, S.E. Spontaneous and fungicide-induced genomic variation in Sclerotinia sclerotiorum. Phytopathology 2021, 111, 160–169. [Google Scholar] [CrossRef] [PubMed]
- Liu, S.; Fu, L.; Chen, J.; Wang, S.; Liu, J.; Jiang, J.; Che, Z.; Tian, Y.; Chen, G. Baseline sensitivity of Sclerotinia sclerotiorum to metconazole and the analysis of cross-resistance with carbendazim, dimethachlone, boscalid, fluazinam, and fludioxonil. Phytoparasitica 2021, 49, 123–130. [Google Scholar] [CrossRef]
- Goyal, R.K.; Mattoo, A.K. Multitasking antimicrobial peptides in plant development and host defense against biotic/abiotic stress. Plant Sci. 2014, 228, 135–149. [Google Scholar] [CrossRef] [PubMed]
- Tavormina, P.; De Coninck, B.; Nikonorova, N.; De Smet, I.; Cammue, B.P. The plant peptidome: An expanding repertoire of structural features and biological functions. Plant Cell 2015, 27, 2095–2118. [Google Scholar] [CrossRef]
- van der Weerden, N.L.; Bleackley, M.R.; Anderson, M.A. Properties and mechanisms of action of naturally occurring antifungal peptides. Cell Mol. Life Sci. 2013, 70, 3545–3570. [Google Scholar] [CrossRef]
- Cools, T.L.; Struyfs, C.; Cammue, B.P.; Thevissen, K. Antifungal plant defensins: Increased insight in their mode of action as a basis for their use to combat fungal infections. Future Microbiol. 2017, 12, 441–454. [Google Scholar] [CrossRef]
- Parisi, K.; Shafee, T.M.A.; Quimbar, P.; van der Weerden, N.L.; Bleackley, M.R.; Anderson, M.A. The evolution, function and mechanisms of action for plant defensins. Semin Cell Dev. Biol. 2019, 88, 107–118. [Google Scholar] [CrossRef]
- Slezina, M.P.; Istomina, E.A.; Korostyleva, T.V.; Odintsova, T.I. The gamma-core motif peptides of plant AMPs as novel antimicrobials for medicine and agriculture. Int. J. Mol. Sci. 2022, 24, 483. [Google Scholar] [CrossRef]
- Rosa, S.; Pesaresi, P.; Mizzotti, C.; Bulone, V.; Mezzetti, B.; Baraldi, E.; Masiero, S. Game-changing alternatives to conventional fungicides: Small RNAs and short peptides. Trends Biotechnol. 2022, 40, 320–337. [Google Scholar] [CrossRef]
- Terras, F.R.; Schoofs, H.M.; De Bolle, M.F.; Van Leuven, F.; Rees, S.B.; Vanderleyden, J.; Cammue, B.P.; Broekaert, W.F. Analysis of two novel classes of plant antifungal proteins from radish (Raphanus sativus L.) seeds. J. Biol. Chem. 1992, 267, 15301–15309. [Google Scholar] [CrossRef]
- Kovaleva, V.; Bukhteeva, I.; Kit, O.Y.; Nesmelova, I.V. Plant defensins from a structural perspective. Int. J. Mol. Sci. 2020, 21, 5307. [Google Scholar] [CrossRef]
- Tetorya, M.; Li, H.; Djami-Tchatchou, A.T.; Buchko, G.W.; Czymmek, C.J.; Shah, D.M. Plant defensin MtDef4-derived antifungal peptide with multiple modes of action and potential as a bioinspired fungicide. Mol. Plant Pathol. 2023, 24, 896–913. [Google Scholar] [CrossRef]
- Velivelli, S.L.S.; Czymmek, K.J.; Li, H.; Shaw, J.B.; Buchko, G.W.; Shah, D.M. Antifungal symbiotic peptide NCR044 exhibits unique structure and multifaceted mechanisms of action that confer plant protection. Proc. Natl. Acad. Sci. USA 2020, 117, 16043–16054. [Google Scholar] [CrossRef]
- Amselem, J.; Cuomo, C.A.; van Kan, J.A.; Viaud, M.; Benito, E.P.; Couloux, A.; Coutinho, P.M.; de Vries, R.P.; Dyer, P.S.; Fillinger, S.; et al. Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet. 2011, 7, e1002230. [Google Scholar] [CrossRef]
- Liang, J.; Shah, D.M.; Wu, Y.; Rosenberger, C.A.; Hakimi, S.M. Antifungal Polypeptide from Alfalfa and Methods for Controlling Plant Pathogenic Fungi. U.S. Patent 6,316,407 B1, 13 November 2001. [Google Scholar]
- Ordóñez-Valencia, C.; Ferrera-Cerrato, R.; Quintanar-Zúñiga, R.E. Morphological development of sclerotia by Sclerotinia sclerotiorum: A view from light and scanning electron microscopy. Ann. Microbiol. 2015, 65, 765–770. [Google Scholar] [CrossRef]
- Chen, C.; Harel, A.; Gorovoits, R.; Yarden, O.; Dickman, M.B. MAPK regulation of sclerotial development in Sclerotinia sclerotiorum is linked with pH and cAMP sensing. Mol. Plant Microbe Interact. 2004, 17, 404–413. [Google Scholar] [CrossRef]
- Wang, Y.; Sun, Y.; Wang, J.; Zhou, M.; Wang, M.; Feng, J. Antifungal activity and action mechanism of the natural product cinnamic acid against Sclerotinia sclerotiorum. Plant Dis. 2019, 103, 944–950. [Google Scholar] [CrossRef] [PubMed]
- Pfaffl, M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29, e45. [Google Scholar] [CrossRef]
- Harel, A.; Bercovich, S.; Yarden, O. Calcineurin is required for sclerotial development and pathogenicity of Sclerotinia sclerotiorum in an oxalic acid-independent manner. Mol. Plant Microbe Interact. 2006, 19, 682–693. [Google Scholar] [CrossRef]
- Islam, K.T.; Velivelli, S.L.S.; Berg, R.H.; Oakley, B.; Shah, D.M. A novel bi-domain plant defensin MtDef5 with potent broad-spectrum antifungal activity binds to multiple phospholipids and forms oligomers. Sci. Rep. 2017, 7, 16157. [Google Scholar] [CrossRef]
- Li, H.; Velivelli, S.L.; Shah, D.M. Antifungal potency and modes of action of a novel olive tree defensin against closely related ascomycete fungal pathogens. Mol. Plant Microbe Interact. 2019, 32, 164901664. [Google Scholar] [CrossRef]
- McCaghey, M.; Willbur, J.; Ranjan, A.; Grau, C.R.; Chapman, S.; Diers, B.; Groves, C.; Kabbage, M.; Smith, D.L. Development and Evaluation of Glycine max Germplasm Lines with Quantitative Resistance to Sclerotinia sclerotiorum. Front. Plant Sci. 2017, 8, 1495. [Google Scholar] [CrossRef]
- McCaghey, M.; Willbur, J.; Smith, D.L.; Kabbage, M. The complexity of the Sclerotinia sclerotiorum pathosystem in soybean: Virulence factors, resistance mechanisms, and their exploitation to control Sclerotinia stem rot. Trop. Plant Pathol. 2019, 44, 12–22. [Google Scholar] [CrossRef]
- Smith, M.E.; Henkel, T.W.; Rollins, J.A. How many fungi make sclerotia? Fungal Ecol. 2015, 13, 211–220. [Google Scholar] [CrossRef]
- Rollins, J.A.; Dickman, M.B. Increase in endogenous and exogenous Cyclic AMP levels inhibits sclerotial development in Sclerotinia sclerotiorum. Appl. Environ. Microbiol. 1998, 64, 2539–2544. [Google Scholar] [CrossRef]
- Smolinska, U.; Kowalska, B. Biological control of the soil-borne fungal pathogen Sclerotinia sclerotiorum—A review. J. Plant Pathol. 2018, 100, 1–12. [Google Scholar] [CrossRef]
- De Coninck, B.M.; Cammue, B.P.A.; Thevissen, K. Modes of antifungal action and in planta functions of plant defensins and defensin-like peptides. Fungal Biol. Rev. 2013, 26, 109–120. [Google Scholar] [CrossRef]
- Kaur, J.; Sagaram, U.S.; Shah, D.M. Can plant defensins be used to engineer durable commercially useful fungal resistance in crop plants? Fungal Biol. Rev. 2011, 25, 128–135. [Google Scholar] [CrossRef]
- Zarinpanjeh, N.; Motallebi, M.; Zamani, M.R.; Ziaei, M. Enhanced resistance to Sclerotinia sclerotiorum in Brassica napus by co-expression of defensin and chimeric chitinase genes. J. Appl. Genet. 2016, 57, 417–425. [Google Scholar] [CrossRef] [PubMed]
- Luo, X.; Wu, W.; Feng, L.; Treves, H.; Ren, M. Short peptides make a big difference: The role of botany-derived AMPs in disease control and protection of human health. Int. J. Mol. Sci. 2021, 22, 11363. [Google Scholar] [CrossRef]
- Lobo, F.; Boto, A. Host-defense peptides as new generation phytosanitaries: Low toxicity and low induction of antimicrobial resistance. Agronomy 2022, 12, 1614. [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. |
© 2023 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
Djami-Tchatchou, A.T.; Tetorya, M.; Godwin, J.; Codjoe, J.M.; Li, H.; Shah, D.M. Small Cationic Cysteine-Rich Defensin-Derived Antifungal Peptide Controls White Mold in Soybean. J. Fungi 2023, 9, 873. https://0-doi-org.brum.beds.ac.uk/10.3390/jof9090873
Djami-Tchatchou AT, Tetorya M, Godwin J, Codjoe JM, Li H, Shah DM. Small Cationic Cysteine-Rich Defensin-Derived Antifungal Peptide Controls White Mold in Soybean. Journal of Fungi. 2023; 9(9):873. https://0-doi-org.brum.beds.ac.uk/10.3390/jof9090873
Chicago/Turabian StyleDjami-Tchatchou, Arnaud Thierry, Meenakshi Tetorya, James Godwin, Jennette M. Codjoe, Hui Li, and Dilip M. Shah. 2023. "Small Cationic Cysteine-Rich Defensin-Derived Antifungal Peptide Controls White Mold in Soybean" Journal of Fungi 9, no. 9: 873. https://0-doi-org.brum.beds.ac.uk/10.3390/jof9090873