RNA-Based Control of Fungal Pathogens in Plants
Abstract
:1. Introduction
2. RNA-Based Biopesticides
2.1. Plant Gene Silencing Pathways
2.1.1. The miRNA Pathway
2.1.2. The phasiRNA Pathway
2.1.3. The tasiRNA Pathway
2.1.4. The natsiRNA Pathway
2.1.5. The rasiRNA Pathway (RdDM Pathway)
3. Fungal Gene Silencing Pathways
3.1. Core Proteins of Fungal Gene Silencing Pathways
3.2. The Fungal miRNA Pathway
3.3. Non-Canonical Fungal Gene Silencing Pathways
4. Plant Defense and Cross-Kingdom RNAi
5. RNA Crop Protection Strategies: HIGS versus SIGS
6. Target Gene Selection for RNA-Based Control of Fungal Pathogens
7. Factors Mediating the Efficacy of Spray-Induced Gene Silencing (SIGS)
7.1. RNA Uptake and Movement in Plants
7.2. RNA Delivery and Uptake in Fungal Pathogens
8. Potential Limitations of SIGS-Based Biopesticides
9. Potential Limitations of the HIGS Approach
10. Recent Advances and Prospects for the SIGS Approach
10.1. RNA Carriers
10.2. Structural Modifications of RNA
10.3. Artificial miRNA (amiRNA)
11. Conclusions and Future Considerations
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
References
- Molotoks, A.; Smith, P.; Dawson, T.P. Impacts of land use, population, and climate change on global food security. Food Energy Secur. 2021, 10, e261. [Google Scholar] [CrossRef]
- Steinberg, G.; Gurr, S.J. Fungi, fungicide discovery and global food security. Fungal Genet. Biol. 2020, 144, 103476. [Google Scholar] [CrossRef] [PubMed]
- van Dijk, M.; Morley, T.; Rau, M.L.; Saghai, Y. A meta-analysis of projected global food demand and population at risk of hunger for the period 2010–2050. Nat. Food 2021, 2, 494–501. [Google Scholar] [CrossRef] [PubMed]
- Behnassi, M.; Pollmann, O.; Gupta, H. Climate Change, Food Security and Natural Resource Management: Regional Case Studies from Three Continents; Springer: Cham, Switzerland, 2019. [Google Scholar]
- Wheeler, T.; Von Braun, J. Climate Change Impacts on Global Food Security. Science 2013, 341, 508–511. [Google Scholar] [CrossRef] [PubMed]
- Beddington, J. Food security: Contributions from science to a new and greener revolution. Philos. Trans. R. Soc. B Biol. Sci. 2010, 365, 61–71. [Google Scholar] [CrossRef] [Green Version]
- Moore, D.; Robson, G.D.; Trinci, A.P.J. 21st Century Guidebook to Fungi; Cambridge University Press: Cambridge, NY, USA, 2011. [Google Scholar]
- Eskola, M.; Kos, G.; Elliott, C.T.; Hajslova, J.; Mayar, S.; Krska, R. Worldwide contamination of food-crops with mycotoxins: Validity of the widely cited ‘FAO estimate’ of 25%. Crit. Rev. Food Sci. Nutr. 2020, 60, 2773–2789. [Google Scholar] [CrossRef]
- de Chaves, M.A.; Reginatto, P.; da Costa, B.S.; de Paschoal, R.I.; Teixeira, M.L.; Fuentefria, A.M. Fungicide Resistance in Fusarium graminearum Species Complex. Curr. Microbiol. 2022, 79, 62. [Google Scholar] [CrossRef]
- Vielba-Fernández, A.; Polonio, Á.; Ruiz-Jiménez, L.; De Vicente, A.; Pérez-García, A.; Fernández-Ortuño, D. Fungicide Resistance in Powdery Mildew Fungi. Microorganisms 2020, 8, 1431. [Google Scholar] [CrossRef]
- Borges, F.; Martienssen, R.A. The expanding world of small RNAs in plants. Nat. Rev. Mol. Cell Biol. 2015, 16, 727–741. [Google Scholar] [CrossRef] [Green Version]
- Billmyre, R.B.; Calo, S.; Feretzaki, M.; Wang, X.; Heitman, J. RNAi function, diversity, and loss in the fungal kingdom. Chromosom. Res. 2013, 21, 561–572. [Google Scholar] [CrossRef] [Green Version]
- Huang, C.-Y.; Wang, H.; Hu, P.; Hamby, R.; Jin, H. Small RNAs—Big Players in Plant-Microbe Interactions. Cell Host Microbe 2019, 26, 173–182. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Baulcombe, D. RNA silencing in plants. Nature 2004, 431, 356–363. [Google Scholar] [CrossRef] [PubMed]
- Dalakouras, A.; Wassenegger, M.; Dadami, E.; Ganopoulos, I.; Pappas, M.L.; Papadopoulou, K. Genetically Modified Organism-Free RNA Interference: Exogenous Application of RNA Molecules in Plants. Plant Physiol. 2020, 182, 38–50. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Qiao, L.; Lan, C.; Capriotti, L.; Ah-Fong, A.; Sanchez, J.N.; Hamby, R.; Heller, J.; Zhao, H.; Glass, N.L.; Judelson, H.S.; et al. Spray-induced gene silencing for disease control is dependent on the efficiency of pathogen RNA uptake. Plant Biotechnol. J. 2021, 19, 1756–1768. [Google Scholar] [CrossRef]
- Šečić, E.; Kogel, K.-H. Requirements for fungal uptake of dsRNA and gene silencing in RNAi-based crop protection strategies. Curr. Opin. Biotechnol. 2021, 70, 136–142. [Google Scholar] [CrossRef]
- Carbonell, A.; Carrington, J.C. Antiviral roles of plant ARGONAUTES. Curr. Opin. Plant Biol. 2015, 27, 111–117. [Google Scholar] [CrossRef] [Green Version]
- Gaffar, F.Y.; Koch, A. Catch Me If You Can! RNA Silencing-Based Improvement of Antiviral Plant Immunity. Viruses 2019, 11, 673. [Google Scholar] [CrossRef] [Green Version]
- Xie, Z.; Johansen, L.K.; Gustafson, A.M.; Kasschau, K.D.; Lellis, A.D.; Zilberman, D.; E Jacobsen, S.; Carrington, J.C. Genetic and Functional Diversification of Small RNA Pathways in Plants. PLoS Biol. 2004, 2, e104. [Google Scholar] [CrossRef] [Green Version]
- Borsani, O.; Zhu, J.; Verslues, P.E.; Sunkar, R.; Zhu, J.-K. Endogenous siRNAs Derived from a Pair of Natural cis-Antisense Transcripts Regulate Salt Tolerance in Arabidopsis. Cell 2005, 123, 1279–1291. [Google Scholar] [CrossRef] [Green Version]
- Baeg, K.; Iwakawa, H.-O.; Tomari, Y. The poly(A) tail blocks RDR6 from converting self mRNAs into substrates for gene silencing. Nat. Plants 2017, 3, 17036. [Google Scholar] [CrossRef]
- Llave, C.; Kasschau, K.D.; Rector, M.A.; Carrington, J.C. Endogenous and Silencing-Associated Small RNAs in Plants. Plant Cell 2002, 14, 1605–1619. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Matzke, M.A.; Kanno, T.; Matzke, A.J. RNA-Directed DNA Methylation: The Evolution of a Complex Epigenetic Pathway in Flowering Plants. Annu. Rev. Plant Biol. 2015, 66, 243–267. [Google Scholar] [CrossRef] [PubMed]
- Matzke, M.A.; Mosher, R.A. RNA-directed DNA methylation: An epigenetic pathway of increasing complexity. Nat. Rev. Genet. 2014, 15, 394–408. [Google Scholar] [CrossRef] [PubMed]
- Margis, R.; Fusaro, A.F.; Smith, N.A.; Curtin, S.J.; Watson, J.M.; Finnegan, E.J.; Waterhouse, P.M. The evolution and diversification of Dicers in plants. FEBS Lett. 2006, 580, 2442–2450. [Google Scholar] [CrossRef]
- Mi, S.; Cai, T.; Hu, Y.; Chen, Y.; Hodges, E.; Ni, F.; Wu, L.; Li, S.; Zhou, H.; Long, C.; et al. Sorting of Small RNAs into Arabidopsis Argonaute Complexes Is Directed by the 5′ Terminal Nucleotide. Cell 2008, 133, 116–127. [Google Scholar] [CrossRef] [Green Version]
- Hannon, G.J. RNA interference. Nature 2002, 418, 244–251. [Google Scholar] [CrossRef]
- Taochy, C.; Gursanscky, N.R.; Cao, J.; Fletcher, S.J.; Dressel, U.; Mitter, N.; Tucker, M.R.; Koltunow, A.M.; Bowman, J.L.; Vaucheret, H.; et al. A Genetic Screen for Impaired Systemic RNAi Highlights the Crucial Role of DICER-LIKE 2. Plant Physiol. 2017, 175, 1424–1437. [Google Scholar] [CrossRef]
- Chen, H.-M.; Chen, L.-T.; Patel, K.; Li, Y.-H.; Baulcombe, D.C.; Wu, S.-H. 22-nucleotide RNAs trigger secondary siRNA biogenesis in plants. Proc. Natl. Acad. Sci. USA 2010, 107, 15269–15274. [Google Scholar] [CrossRef]
- Cuperus, J.T.; Carbonell, A.; Fahlgren, N.; Garcia-Ruiz, H.; Burke, R.T.; Takeda, A.; Sullivan, C.M.; Gilbert, S.D.; Montgomery, T.A.; Carrington, J.C. Unique functionality of 22-nt miRNAs in triggering RDR6-dependent siRNA biogenesis from target transcripts in Arabidopsis. Nat. Struct. Mol. Biol. 2010, 17, 997–1003. [Google Scholar] [CrossRef]
- Parent, J.-S.; Bouteiller, N.; Elmayan, T.; Vaucheret, H. Respective contributions of Arabidopsis DCL2 and DCL4 to RNA silencing. Plant J. 2015, 156, 223–232. [Google Scholar] [CrossRef]
- Cao, J.; Gursanscky, N.R.; Fletcher, S.J.; Sawyer, A.; Wadia, M.; McKeough, L.; Coleman, M.; Dressel, U.; Taochy, C.; Mitter, N.; et al. Can-Seq: A PCR and DNA sequencing strategy for identifying new alleles of known and candidate genes. Plant Methods 2020, 16, 1. [Google Scholar] [CrossRef]
- Park, M.Y.; Wu, G.; Gonzalez-Sulser, A.; Vaucheret, H.; Poethig, R.S. Nuclear processing and export of microRNAs in Arabidopsis. Proc. Natl. Acad. Sci. USA 2005, 102, 3691–3696. [Google Scholar] [CrossRef]
- Song, X.; Li, Y.; Cao, X.; Qi, Y. MicroRNAs and Their Regulatory Roles in Plant–Environment Interactions. Annu. Rev. Plant Biol. 2019, 70, 489–525. [Google Scholar] [CrossRef] [PubMed]
- Li, J.; Yang, Z.; Yu, B.; Liu, J.; Chen, X. Methylation Protects miRNAs and siRNAs from a 3′-End Uridylation Activity in Arabidopsis. Curr. Biol. 2005, 15, 1501–1507. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Baranauskė, S.; Mickutė, M.; Plotnikova, A.; Finke, A.; Venclovas, Č.; Klimašauskas, S.; Vilkaitis, G. Functional mapping of the plant small RNA methyltransferase: HEN1 physically interacts with HYL1 and DICER-LIKE 1 proteins. Nucleic Acids Res. 2015, 43, 2802–2812. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, T.; Cui, P.; Xiong, L. The RNA-binding protein HOS5 and serine/arginine-rich proteins RS40 and RS41 participate in miRNA biogenesis in Arabidopsis. Nucleic Acids Res. 2015, 43, 8283–8298. [Google Scholar] [CrossRef] [Green Version]
- Bologna, N.G.; Iselin, R.; Abriata, L.A.; Sarazin, A.; Pumplin, N.; Jay, F.; Grentzinger, T.; Dal Peraro, M.; Voinnet, O. Nucleo-cytosolic Shuttling of ARGONAUTE1 Prompts a Revised Model of the Plant MicroRNA Pathway. Mol. Cell 2018, 69, 709–719.e5. [Google Scholar] [CrossRef] [Green Version]
- Cambiagno, D.A.; Giudicatti, A.J.; Arce, A.L.; Gagliardi, D.; Li, L.; Yuan, W.; Lundberg, D.S.; Weigel, D.; Manavella, P.A. HASTY modulates miRNA biogenesis by linking pri-miRNA transcription and processing. Mol. Plant 2020, 14, 426–439. [Google Scholar] [CrossRef]
- Brodersen, P.; Sakvarelidze-Achard, L.; Bruun-Rasmussen, M.; Dunoyer, P.; Yamamoto, Y.Y.; Sieburth, L.; Voinnet, O. Widespread Translational Inhibition by Plant miRNAs and siRNAs. Science 2008, 320, 1185–1190. [Google Scholar] [CrossRef]
- Reis, R.S.; Hart-Smith, G.; Eamens, A.L.; Wilkins, M.R.; Waterhouse, P.M. Gene regulation by translational inhibition is determined by Dicer partnering proteins. Nat. Plants 2015, 1, 14027. [Google Scholar] [CrossRef]
- Adenot, X.; Elmayan, T.; Lauressergues, D.; Boutet, S.; Bouché, N.; Gasciolli, V.; Vaucheret, H. DRB4-Dependent TAS3 trans-Acting siRNAs Control Leaf Morphology through AGO7. Curr. Biol. 2006, 16, 927–932. [Google Scholar] [CrossRef] [Green Version]
- Fukudome, A.; Kanaya, A.; Egami, M.; Nakazawa, Y.; Hiraguri, A.; Moriyama, H.; Fukuhara, T. Specific requirement of DRB4, a dsRNA-binding protein, for the in vitro dsRNA-cleaving activity of Arabidopsis Dicer-like 4. RNA 2011, 17, 750–760. [Google Scholar] [CrossRef] [Green Version]
- Deng, P.; Muhammad, S.; Cao, M.; Wu, L. Biogenesis and regulatory hierarchy of phased small interfering RNAs in plants. Plant Biotechnol. J. 2018, 16, 965–975. [Google Scholar] [CrossRef] [Green Version]
- Fei, Q.; Xia, R.; Meyers, B.C. Phased, Secondary, Small Interfering RNAs in Posttranscriptional Regulatory Networks. Plant Cell 2013, 25, 2400–2415. [Google Scholar] [CrossRef] [Green Version]
- Teng, C.; Zhang, H.; Hammond, R.; Huang, K.; Meyers, B.C.; Walbot, V. Dicer-like 5 deficiency confers temperature-sensitive male sterility in maize. Nat. Commun. 2020, 11, 2912. [Google Scholar] [CrossRef]
- Xia, R.; Chen, C.; Pokhrel, S.; Ma, W.; Huang, K.; Patel, P.; Wang, F.; Xu, J.; Liu, Z.; Li, J.; et al. 24-nt reproductive phasiRNAs are broadly present in angiosperms. Nat. Commun. 2019, 10, 627. [Google Scholar] [CrossRef] [Green Version]
- Vazquez, F.; Vaucheret, H.; Rajagopalan, R.; Lepers, C.; Gasciolli, V.; Mallory, A.C.; Hilbert, J.-L.; Bartel, D.P.; Crété, P. Endogenous trans-Acting siRNAs Regulate the Accumulation of Arabidopsis mRNAs. Mol. Cell 2004, 16, 69–79. [Google Scholar] [CrossRef]
- Gasciolli, V.; Mallory, A.C.; Bartel, D.P.; Vaucheret, H. Partially Redundant Functions of Arabidopsis DICER-like Enzymes and a Role for DCL4 in Producing trans-Acting siRNAs. Curr. Biol. 2005, 15, 1494–1500. [Google Scholar] [CrossRef] [Green Version]
- Liu, Y.; Teng, C.; Xia, R.; Meyers, B.C. PhasiRNAs in Plants: Their Biogenesis, Genic Sources, and Roles in Stress Responses, Development, and Reproduction. Plant Cell 2020, 32, 3059–3080. [Google Scholar] [CrossRef]
- Katiyar-Agarwal, S.; Morgan, R.; Dahlbeck, D.; Borsani, O.; Villegas, A.; Zhu, J.-K.; Staskawicz, B.J.; Jin, H. A pathogen-inducible endogenous siRNA in plant immunity. Proc. Natl. Acad. Sci. USA 2006, 103, 18002–18007. [Google Scholar] [CrossRef]
- Ron, M.; Saez, M.A.; Williams, L.E.; Fletcher, J.C.; McCormick, S. Proper regulation of a sperm-specific cis-nat-siRNA is essential for double fertilization in Arabidopsis. Genes Dev. 2010, 24, 1010–1021. [Google Scholar] [CrossRef] [Green Version]
- Zhang, H.; Lang, Z.; Zhu, J.-K. Dynamics and function of DNA methylation in plants. Nat. Rev. Mol. Cell Biol. 2018, 19, 489–506. [Google Scholar] [CrossRef]
- Matzke, M.A.; Birchler, J.A. RNAi-mediated pathways in the nucleus. Nat. Rev. Genet. 2005, 6, 24–35. [Google Scholar] [CrossRef]
- Panda, K.; McCue, A.D.; Slotkin, R.K. Arabidopsis RNA Polymerase IV generates 21–22 nucleotide small RNAs that can participate in RNA-directed DNA methylation and may regulate genes. Philos. Trans. R. Soc. B Biol. Sci. 2020, 375, 20190417. [Google Scholar] [CrossRef]
- Ito, H.; Gaubert, H.; Bucher, E.; Mirouze, M.; Vaillant, I.; Paszkowski, J. An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature 2011, 472, 115–119. [Google Scholar] [CrossRef]
- Slotkin, R.K.; Vaughn, M.; Borges, F.; Tanurdžić, M.; Becker, J.D.; Feijó, J.A.; Martienssen, R.A. Epigenetic Reprogramming and Small RNA Silencing of Transposable Elements in Pollen. Cell 2009, 136, 461–472. [Google Scholar] [CrossRef] [Green Version]
- Lister, R.; O’Malley, R.C.; Tonti-Filippini, J.; Gregory, B.D.; Berry, C.C.; Millar, A.H.; Ecker, J.R. Highly Integrated Single-Base Resolution Maps of the Epigenome in Arabidopsis. Cell 2008, 133, 523–536. [Google Scholar] [CrossRef] [Green Version]
- Lax, C.; Tahiri, G.; Patiño-Medina, J.A.; Cánovas-Márquez, J.T.; Pérez-Ruiz, J.A.; Osorio-Concepción, M.; Navarro, E.; Calo, S. The Evolutionary Significance of RNAi in the Fungal Kingdom. Int. J. Mol. Sci. 2020, 21, 9348. [Google Scholar] [CrossRef]
- Djulic, A.; Schmid, A.; Lenz, H.; Sharma, P.; Koch, C.; Wirsel, S.G.; Voegele, R.T. Transient transformation of the obligate biotrophic rust fungus Uromyces fabae using biolistics. Fungal Biol. 2011, 115, 633–642. [Google Scholar] [CrossRef]
- Dang, Y.; Yang, Q.; Xue, Z.; Liu, Y. RNA Interference in Fungi: Pathways, Functions, and Applications. Eukaryot. Cell 2011, 10, 1148–1155. [Google Scholar] [CrossRef] [Green Version]
- Gaffar, F.Y.; Imani, J.; Karlovsky, P.; Koch, A.; Kogel, K.-H. Different Components of the RNA Interference Machinery Are Required for Conidiation, Ascosporogenesis, Virulence, Deoxynivalenol Production, and Fungal Inhibition by Exogenous Double-Stranded RNA in the Head Blight Pathogen Fusarium graminearum. Front. Microbiol. 2019, 10, 1662. [Google Scholar] [CrossRef] [Green Version]
- Sperschneider, J.; Jones, A.W.; Nasim, J.; Xu, B.; Jacques, S.; Zhong, C.; Upadhyaya, N.M.; Mago, R.; Hu, Y.; Figueroa, M.; et al. The stem rust fungus Puccinia graminis f. sp. tritici induces centromeric small RNAs during late infection that are associated with genome-wide DNA methylation. BMC Biol. 2021, 19, 203. [Google Scholar] [CrossRef]
- Weiberg, A.; Wang, M.; Lin, F.-M.; Zhao, H.; Zhang, Z.; Kaloshian, I.; Huang, H.-D.; Jin, H. Fungal Small RNAs Suppress Plant Immunity by Hijacking Host RNA Interference Pathways. Science 2013, 342, 118–123. [Google Scholar] [CrossRef] [Green Version]
- Catalanotto, C.; Pallotta, M.; ReFalo, P.; Sachs, M.S.; Vayssie, L.; Macino, G.; Cogoni, C. Redundancy of the Two Dicer Genes in Transgene-Induced Posttranscriptional Gene Silencing in Neurospora crassa. Mol. Cell. Biol. 2004, 24, 2536–2545. [Google Scholar] [CrossRef] [Green Version]
- Kadotani, N.; Nakayashiki, H.; Tosa, Y.; Mayama, S.; Raman, V.; Simon, S.A.; Demirci, F.; Nakano, M.; Meyers, B.C.; Donofrio, N.M.; et al. RNA Silencing in the Phytopathogenic Fungus Magnaporthe oryzae. Mol. Plant-Microbe Interact. 2003, 16, 769–776. [Google Scholar] [CrossRef] [Green Version]
- Chen, Y.; Gao, Q.; Huang, M.; Liu, Y.; Liu, Z.; Liu, X.; Ma, Z. Characterization of RNA silencing components in the plant pathogenic fungus Fusarium graminearum. Sci. Rep. 2015, 5, srep12500. [Google Scholar] [CrossRef] [Green Version]
- Feng, H.; Xu, M.; Liu, Y.; Dong, R.; Gao, X.; Huang, L. Dicer-Like Genes Are Required for H2O2 and KCl Stress Responses, Pathogenicity and Small RNA Generation in Valsa mali. Front. Microbiol. 2017, 8, 1166. [Google Scholar] [CrossRef] [Green Version]
- Jeseničnik, T.; Štajner, N.; Radišek, S.; Jakše, J. RNA interference core components identified and characterised in Verticillium nonalfalfae, a vascular wilt pathogenic plant fungi of hops. Sci. Rep. 2019, 9, 8651. [Google Scholar] [CrossRef] [Green Version]
- Reichel, M.; Liao, Y.; Rettel, M.; Ragan, C.; Evers, M.; Alleaume, A.-M.; Horos, R.; Hentze, M.W.; Preiss, T.; Millar, A.A. In Planta Determination of the mRNA-Binding Proteome of Arabidopsis Etiolated Seedlings. Plant Cell 2016, 28, 2435–2452. [Google Scholar] [CrossRef] [Green Version]
- Li, Z.; Li, W.; Guo, M.; Liu, S.; Liu, L.; Yu, Y.; Mo, B.; Chen, X.; Gao, L. Origin, evolution and diversification of plant ARGONAUTE proteins. Plant J. 2021, 109, 1086–1097. [Google Scholar] [CrossRef]
- Nakayashiki, H.; Kadotani, N.; Mayama, S. Evolution and Diversification of RNA Silencing Proteins in Fungi. J. Mol. Evol. 2006, 63, 127–135. [Google Scholar] [CrossRef] [Green Version]
- Nguyen, Q.; Iritani, A.; Ohkita, S.; Vu, B.V.; Yokoya, K.; Matsubara, A.; Ikeda, K.-I.; Suzuki, N.; Nakayashiki, H. A fungal Argonaute interferes with RNA interference. Nucleic Acids Res. 2018, 46, 2495–2508. [Google Scholar] [CrossRef] [Green Version]
- Yoshimoto, R.; Ishida, F.; Yamaguchi, M.; Tanaka, S. The production and secretion of tRNA-derived RNA fragments in the corn smut fungus Ustilago maydis. Front. Fungal Biol. 2022, 3, 958798. [Google Scholar] [CrossRef]
- Laurie, J.D.; Linning, R.; Bakkeren, G. Hallmarks of RNA silencing are found in the smut fungus Ustilago hordei but not in its close relative Ustilago maydis. Curr. Genet. 2007, 53, 49–58. [Google Scholar] [CrossRef]
- Donaldson, M.E.; Saville, B.J. Ustilago maydis natural antisense transcript expression altersm RNA stability and pathogenesis. Mol. Microbiol. 2013, 89, 29–51. [Google Scholar] [CrossRef] [Green Version]
- Li, L.; Chang, S.-S.; Liu, Y. RNA interference pathways in filamentous fungi. Cell. Mol. Life Sci. 2010, 67, 3849–3863. [Google Scholar] [CrossRef] [Green Version]
- Degnan, R.M.; McTaggart, A.R.; Shuey, L.S.; Pame, L.J.S.; Smith, G.R.; Gardiner, D.M.; Nock, V.; Soffe, R.; Sale, S.; Garrill, A.; et al. Exogenous double-stranded RNA inhibits the infection physiology of rust fungi to reduce symptoms in planta. Mol. Plant Pathol. 2022, 24, 191–207. [Google Scholar] [CrossRef]
- Song, X.-S.; Gu, K.-X.; Duan, X.-X.; Xiao, X.-M.; Hou, Y.-P.; Duan, Y.-B.; Wang, J.-X.; Yu, N.; Zhou, M.-G. Secondary amplification of siRNA machinery limits the application of spray-induced gene silencing. Mol. Plant Pathol. 2018, 19, 2543–2560. [Google Scholar] [CrossRef] [Green Version]
- Zhang, T.; Zhao, J.-H.; Fang, Y.-Y.; Guo, H.-S.; Jin, Y. Exploring the Effectiveness and Durability of Trans-Kingdom Silencing of Fungal Genes in the Vascular Pathogen Verticillium dahliae. Int. J. Mol. Sci. 2022, 23, 2742. [Google Scholar] [CrossRef]
- Calo, S.; Nicolás, F.E.; Vila, A.; Torres-Martínez, S.; Ruiz-Vázquez, R.M. Two distinct RNA-dependent RNA polymerases are required for initiation and amplification of RNA silencing in the basal fungus Mucor circinelloides. Mol. Microbiol. 2012, 83, 379–394. [Google Scholar] [CrossRef]
- Fernandez, E.Q.; Moyer, D.L.; Maiyuran, S.; Labaro, A.; Brody, H. Vector-initiated transitive RNA interference in the filamentous fungus Aspergillus oryzae. Fungal Genet. Biol. 2012, 49, 294–301. [Google Scholar] [CrossRef]
- Hammond, T.M.; Keller, N.P. RNA Silencing in Aspergillus nidulans Is Independent of RNA-Dependent RNA Polymerases. Genetics 2005, 169, 607–617. [Google Scholar] [CrossRef] [Green Version]
- Makeyev, E.V.; Bamford, D.H. Cellular RNA-Dependent RNA Polymerase Involved in Posttranscriptional Gene Silencing Has Two Distinct Activity Modes. Mol. Cell 2002, 10, 1417–1427. [Google Scholar] [CrossRef]
- Lee, H.-C.; Aalto, A.P.; Yang, Q.; Chang, S.-S.; Huang, G.; Fisher, D.; Cha, J.; Poranen, M.M.; Bamford, D.H.; Liu, Y. The DNA/RNA-Dependent RNA Polymerase QDE-1 Generates Aberrant RNA and dsRNA for RNAi in a Process Requiring Replication Protein A and a DNA Helicase. PLoS Biol. 2010, 8, e1000496. [Google Scholar] [CrossRef] [Green Version]
- Cui, R.; Li, H.; Zhao, J.; Li, X.; Gan, J.; Ma, J. Structural insights into the dual activities of the two-barrel RNA polymerase QDE-1. Nucleic Acids Res. 2022, 50, 10169–10186. [Google Scholar] [CrossRef]
- Shiu, P.K.; Raju, N.B.; Zickler, D.; Metzenberg, R.L. Meiotic Silencing by Unpaired DNA. Cell 2001, 107, 905–916. [Google Scholar] [CrossRef] [Green Version]
- Espino, J.; González, M.; González, C.; Brito, N. Efficiency of different strategies for gene silencing in Botrytis cinerea. Appl. Microbiol. Biotechnol. 2014, 98, 9413–9424. [Google Scholar] [CrossRef]
- Jin, Y.; Zhao, J.-H.; Zhao, P.; Zhang, T.; Wang, S.; Guo, H.-S. A fungal milRNA mediates epigenetic repression of a virulence gene in Verticillium dahliae. Philos. Trans. R. Soc. B Biol. Sci. 2019, 374, 20180309. [Google Scholar] [CrossRef] [Green Version]
- Nai, Y.-S.; Huang, Y.-C.; Yen, M.-R.; Chen, P.-Y. Diversity of Fungal DNA Methyltransferases and Their Association with DNA Methylation Patterns. Front. Microbiol. 2021, 11, 616922. [Google Scholar] [CrossRef]
- Vazquez, F.; Hohn, T. Biogenesis and Biological Activity of Secondary siRNAs in Plants. Scientifica 2013, 2013, 783253. [Google Scholar] [CrossRef] [Green Version]
- Wang, X.-B.; Wu, Q.; Ito, T.; Cillo, F.; Li, W.-X.; Chen, X.; Yu, J.-L.; Ding, S.-W. RNAi-mediated viral immunity requires amplification of virus-derived siRNAs in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 2009, 107, 484–489. [Google Scholar] [CrossRef]
- Lee, H.-C.; Li, L.; Gu, W.; Xue, Z.; Crosthwaite, S.K.; Pertsemlidis, A.; Lewis, Z.A.; Freitag, M.; Selker, E.U.; Mello, C.C.; et al. Diverse Pathways Generate MicroRNA-like RNAs and Dicer-Independent Small Interfering RNAs in Fungi. Mol. Cell 2010, 38, 803–814. [Google Scholar] [CrossRef] [Green Version]
- Dutta, S.; Jha, S.K.; Prabhu, K.V.; Kumar, M.; Mukhopadhyay, K. Leaf rust (Puccinia triticina) mediated RNAi in wheat (Triticum aestivum L.) prompting host susceptibility. Funct. Integr. Genom. 2019, 19, 437–452. [Google Scholar] [CrossRef]
- Wang, B.; Sun, Y.; Song, N.; Zhao, M.; Liu, R.; Feng, H.; Wang, X.; Kang, Z. Puccinia striiformis f. sp. tritici mi croRNA -like RNA 1 (Pst -milR1), an important pathogenicity factor of Pst, impairs wheat resistance to Pst by suppressing the wheat pathogenesis-related 2 gene. New Phytol. 2017, 215, 338–350. [Google Scholar] [CrossRef] [Green Version]
- Xia, Z.; Wang, Z.; Kav, N.N.; Ding, C.; Liang, Y. Characterization of microRNA-like RNAs associated with sclerotial development in Sclerotinia sclerotiorum. Fungal Genet. Biol. 2020, 144, 103471. [Google Scholar] [CrossRef]
- Guo, M.; Yang, P.; Zhang, J.; Liu, G.; Yuan, Q.; He, W.; Nian, J.; Yi, S.; Huang, T.; Liao, Y. Expression of microRNA-like RNA-2 (Fgmil-2) and bioH1 from a single transcript in Fusarium graminearum are inversely correlated to regulate biotin synthesis during vegetative growth and host infection. Mol. Plant Pathol. 2019, 20, 1574–1581. [Google Scholar] [CrossRef] [Green Version]
- Yao, Y.; Zhang, H.; Deng, H. milRNApredictor: Genome-free prediction of fungi milRNAs by incorporating k-mer scheme and distance-dependent pair potential. Genomics 2019, 112, 2233–2240. [Google Scholar] [CrossRef]
- Axtell, M.J. ShortStack: Comprehensive annotation and quantification of small RNA genes. RNA 2013, 19, 740–751. [Google Scholar] [CrossRef] [Green Version]
- Kerpedjiev, P.; Hammer, S.; Hofacker, I.L. Forna (force-directed RNA): Simple and effective online RNA secondary structure diagrams. Bioinformatics 2015, 31, 3377–3379. [Google Scholar] [CrossRef] [Green Version]
- Höfle, L.; Biedenkopf, D.; Werner, B.T.; Shrestha, A.; Jelonek, L.; Koch, A. Study on the efficiency of dsRNAs with increasing length in RNA-based silencing of the Fusarium CYP51 genes. RNA Biol. 2020, 17, 463–473. [Google Scholar] [CrossRef]
- Jones, J.D.G.; Vance, R.E.; Dangl, J.L. Intracellular innate immune surveillance devices in plants and animals. Science 2016, 354, aaf6395. [Google Scholar] [CrossRef] [Green Version]
- Katiyar-Agarwal, S.; Jin, H. Role of Small RNAs in Host-Microbe Interactions. Annu. Rev. Phytopathol. 2010, 48, 225–246. [Google Scholar] [CrossRef] [Green Version]
- Petit-Houdenot, Y.; Fudal, I. Complex Interactions between Fungal Avirulence Genes and Their Corresponding Plant Resistance Genes and Consequences for Disease Resistance Management. Front. Plant Sci. 2017, 8, 1072. [Google Scholar] [CrossRef] [Green Version]
- Gualtieri, C.; Leonetti, P.; Macovei, A. Plant miRNA Cross-Kingdom Transfer Targeting Parasitic and Mutualistic Organisms as a Tool to Advance Modern Agriculture. Front. Plant Sci. 2020, 11, 930. [Google Scholar] [CrossRef]
- Schaefer, L.K.; Parlange, F.; Buchmann, G.; Jung, E.; Wehrli, A.; Herren, G.; Müller, M.C.; Stehlin, J.; Schmid, R.; Wicker, T.; et al. Cross-Kingdom RNAi of Pathogen Effectors Leads to Quantitative Adult Plant Resistance in Wheat. Front. Plant Sci. 2020, 11, 253. [Google Scholar] [CrossRef]
- Dunker, F.; Trutzenberg, A.; Rothenpieler, J.S.; Kuhn, S.; Pröls, R.; Schreiber, T.; Tissier, A.; Kemen, A.; Kemen, E.; Hückelhoven, R.; et al. Oomycete small RNAs bind to the plant RNA-induced silencing complex for virulence. eLife 2020, 9, e56096. [Google Scholar] [CrossRef]
- Cai, Q.; Qiao, L.; Wang, M.; He, B.; Lin, F.-M.; Palmquist, J.; Huang, S.-D.; Jin, H. Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes. Science 2018, 360, 1126–1129. [Google Scholar] [CrossRef] [Green Version]
- Wang, M.; Weiberg, A.; Dellota, E.; Yamane, D.; Jin, H. Botrytis small RNA Bc-siR37 suppresses plant defense genes by cross-kingdom RNAi. RNA Biol. 2017, 14, 421–428. [Google Scholar] [CrossRef] [Green Version]
- Wang, M.; Weiberg, A.; Lin, F.-M.; Thomma, B.P.H.J.; Huang, H.-D.; Jin, H. Bidirectional cross-kingdom RNAi and fungal uptake of external RNAs confer plant protection. Nat. Plants 2016, 2, 16151. [Google Scholar] [CrossRef] [Green Version]
- Ji, H.; Mao, H.; Li, S.; Feng, T.; Zhang, Z.; Cheng, L.; Luo, S.; Borkovich, K.A.; Ouyang, S. Fol-milR1, a pathogenicity factor of Fusarium oxysporum, confers tomato wilt disease resistance by impairing host immune responses. New Phytol. 2021, 232, 705–718. [Google Scholar] [CrossRef]
- Zhang, T.; Zhao, Y.-L.; Zhao, J.-H.; Wang, S.; Jin, Y.; Chen, Z.-Q.; Fang, Y.-Y.; Zhao, J.-H.; Ding, S.-W.; Guo, H.-S. Cotton plants export microRNAs to inhibit virulence gene expression in a fungal pathogen. Nat. Plants 2016, 2, 16153. [Google Scholar] [CrossRef] [PubMed]
- Xu, M.; Li, G.; Guo, Y.; Gao, Y.; Zhu, L.; Liu, Z.; Tian, R.; Gao, C.; Han, P.; Wang, N.; et al. A fungal microRNA-like RNA subverts host immunity and facilitates pathogen infection by silencing two host receptor-like kinase genes. New Phytol. 2022, 233, 2503–2519. [Google Scholar] [CrossRef] [PubMed]
- Wu, Z.; Wang, L.; Li, J.; Wang, L.; Wu, Z.; Sun, X. Extracellular Vesicle-Mediated Communication Within Host-Parasite Interactions. Front. Immunol. 2019, 9, 3066. [Google Scholar] [CrossRef] [Green Version]
- Rutter, B.D.; Innes, R.W. Extracellular vesicles as key mediators of plant–microbe interactions. Curr. Opin. Plant Biol. 2018, 44, 16–22. [Google Scholar] [CrossRef] [PubMed]
- Rutter, B.D.; Innes, R.W. Extracellular Vesicles Isolated from the Leaf Apoplast Carry Stress-Response Proteins. Plant Physiol. 2017, 173, 728–741. [Google Scholar] [CrossRef] [Green Version]
- Regente, M.; Pinedo, M.; Clemente, H.S.; Balliau, T.; Jamet, E.; de la Canal, L. Plant extracellular vesicles are incorporated by a fungal pathogen and inhibit its growth. J. Exp. Bot. 2017, 68, 5485–5495. [Google Scholar] [CrossRef] [Green Version]
- Schlemmer, T.; Barth, P.; Weipert, L.; Preußer, C.; Hardt, M.; Möbus, A.; Busche, T.; Koch, A. Isolation and Characterization of Barley (Hordeum vulgare) Extracellular Vesicles to Assess Their Role in RNA Spray-Based Crop Protection. Int. J. Mol. Sci. 2021, 22, 7212. [Google Scholar] [CrossRef]
- Schlemmer, T.; Lischka, R.; Wegner, L.; Ehlers, K.; Biedenkopf, D.; Koch, A. Extracellular vesicles isolated from dsRNA-sprayed barley plants exhibit no growth inhibition or gene silencing in Fusarium graminearum. Fungal Biol. Biotechnol. 2022, 9, 14. [Google Scholar] [CrossRef]
- He, B.; Cai, Q.; Qiao, L.; Huang, C.-Y.; Wang, S.; Miao, W.; Ha, T.; Wang, Y.; Jin, H. RNA-binding proteins contribute to small RNA loading in plant extracellular vesicles. Nat. Plants 2021, 7, 342–352. [Google Scholar] [CrossRef]
- Rutter, B.D.; Innes, R.W. Growing pains: Addressing the pitfalls of plant extracellular vesicle research. New Phytol. 2020, 228, 1505–1510. [Google Scholar] [CrossRef]
- Koch, A.; Wassenegger, M. Host-induced gene silencing—Mechanisms and applications. New Phytol. 2021, 231, 54–59. [Google Scholar] [CrossRef] [PubMed]
- Nowara, D.; Gay, A.; Lacomme, C.; Shaw, J.; Ridout, C.; Douchkov, D.; Hensel, G.; Kumlehn, J.; Schweizer, P. HIGS: Host-Induced Gene Silencing in the Obligate Biotrophic Fungal Pathogen Blumeria graminis. Plant Cell 2010, 22, 3130–3141. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Koch, A.; Kumar, N.; Weber, L.; Keller, H.; Imani, J.; Kogel, K.-H. Host-induced gene silencing of cytochrome P450 lanosterol C14α-demethylase–encoding genes confers strong resistance to Fusarium species. Proc. Natl. Acad. Sci. USA 2013, 110, 19324–19329. [Google Scholar] [CrossRef]
- Panwar, V.; Jordan, M.; McCallum, B.; Bakkeren, G. Host-induced silencing of essential genes in Puccinia triticina through transgenic expression of RNAi sequences reduces severity of leaf rust infection in wheat. Plant Biotechnol. J. 2018, 16, 1013–1023. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sanju, S.; Siddappa, S.; Thakur, A.; Shukla, P.K.; Srivastava, N.; Pattanayak, D.; Sharma, S.; Singh, B.P. Host-mediated gene silencing of a single effector gene from the potato pathogen Phytophthora infestans imparts partial resistance to late blight disease. Funct. Integr. Genom. 2015, 15, 697–706. [Google Scholar] [CrossRef] [PubMed]
- Andrade, C.M.; Tinoco, M.L.P.; Rieth, A.F.; Maia, F.C.O.; Aragão, F.J.L. Host-induced gene silencing in the necrotrophic fungal pathogen Sclerotinia sclerotiorum. Plant Pathol. 2015, 65, 626–632. [Google Scholar] [CrossRef] [Green Version]
- Sikora, D.; Rzymski, P. Chapter 13—Public Acceptance of GM Foods: A Global Perspective (1999–2019). In Policy Issues in Genetically Modified Crops; Singh, P., Borthakur, A., Singh, A.A., Kumar, A., Singh, K.K., Eds.; Academic Press: Cambridge, MA, USA, 2021; pp. 293–315. [Google Scholar]
- McLoughlin, A.G.; Wytinck, N.; Walker, P.L.; Girard, I.J.; Rashid, K.Y.; de Kievit, T.; Fernando, W.G.D.; Whyard, S.; Belmonte, M.F. Identification and application of exogenous dsRNA confers plant protection against Sclerotinia sclerotiorum and Botrytis cinerea. Sci. Rep. 2018, 8, 7314–7320. [Google Scholar] [CrossRef] [Green Version]
- Niño-Sánchez, J.; Sambasivam, P.T.; Sawyer, A.; Hamby, R.; Chen, A.; Czislowski, E.; Li, P.; Manzie, N.; Gardiner, D.M.; Ford, R.; et al. BioClay™ prolongs RNA interference-mediated crop protection against Botrytis cinerea. J. Integr. Plant Biol. 2022, 64, 2187–2198. [Google Scholar] [CrossRef]
- Islam, T.; Davis, Z.; Chen, L.; Englaender, J.; Zomorodi, S.; Frank, J.; Bartlett, K.; Somers, E.; Carballo, S.M.; Kester, M.; et al. Minicell-based fungal RNAi delivery for sustainable crop protection. Microb. Biotechnol. 2021, 14, 1847–1856. [Google Scholar] [CrossRef]
- Koch, A.; Biedenkopf, D.; Furch, A.; Weber, L.; Rossbach, O.; Abdellatef, E.; Linicus, L.; Johannsmeier, J.; Jelonek, L.; Goesmann, A.; et al. An RNAi-Based Control of Fusarium graminearum Infections Through Spraying of Long dsRNAs Involves a Plant Passage and Is Controlled by the Fungal Silencing Machinery. PLoS Pathog. 2016, 12, e1005901. [Google Scholar] [CrossRef]
- A Mosa, M.; Youssef, K. Topical delivery of host induced RNAi silencing by layered double hydroxide nanosheets: An efficient tool to decipher pathogenicity gene function of Fusarium crown and root rot in tomato. Physiol. Mol. Plant Pathol. 2021, 115, 101684. [Google Scholar] [CrossRef]
- Hu, D.; Chen, Z.; Zhang, C.; Ganiger, M. Reduction of Phakopsora pachyrhizi infection on soybean through host- and spray-induced gene silencing. Mol. Plant Pathol. 2020, 21, 794–807. [Google Scholar] [CrossRef] [Green Version]
- Werner, B.T.; Gaffar, F.Y.; Schuemann, J.; Biedenkopf, D.; Koch, A.M. RNA-Spray-Mediated Silencing of Fusarium graminearum AGO and DCL Genes Improve Barley Disease Resistance. Front. Plant Sci. 2020, 11, 476. [Google Scholar] [CrossRef]
- Koch, A.; Höfle, L.; Werner, B.T.; Imani, J.; Schmidt, A.; Jelonek, L.; Kogel, K. SIGS vs HIGS: A study on the efficacy of two dsRNA delivery strategies to silence Fusarium FgCYP51 genes in infected host and non-host plants. Mol. Plant Pathol. 2019, 20, 1636–1644. [Google Scholar] [CrossRef] [Green Version]
- Gu, K.-X.; Song, X.-S.; Xiao, X.-M.; Duan, X.-X.; Wang, J.-X.; Duan, Y.-B.; Hou, Y.-P.; Zhou, M.-G. A β-tubulin dsRNA derived from Fusarium asiaticum confers plant resistance to multiple phytopathogens and reduces fungicide resistance. Pestic. Biochem. Physiol. 2018, 153, 36–46. [Google Scholar] [CrossRef]
- Hu, W.; Sillaots, S.; Lemieux, S.; Davison, J.; Kauffman, S.; Breton, A.; Linteau, A.; Xin, C.; Bowman, J.; Becker, J.; et al. Essential Gene Identification and Drug Target Prioritization in Aspergillus fumigatus. PLoS Pathog. 2007, 3, e24. [Google Scholar] [CrossRef]
- Zhao, Z.; Liu, H.; Luo, Y.; Zhou, S.; An, L.; Wang, C.; Jin, Q.; Zhou, M.; Xu, J.-R. Molecular evolution and functional divergence of tubulin superfamily in the fungal tree of life. Sci. Rep. 2014, 4, 6746. [Google Scholar] [CrossRef] [Green Version]
- Yin, C.; Jurgenson, J.E.; Hulbert, S.H.; Bakkeren, G.; Szabo, L.J.; Cooper, B.; Campbell, K.B.; Ramachandran, S.R.; Kud, J.; Tanaka, K.; et al. Development of a Host-Induced RNAi System in the Wheat Stripe Rust Fungus Puccinia striiformis f. sp. tritici. Mol. Plant-Microbe Interact. 2011, 24, 554–561. [Google Scholar] [CrossRef] [Green Version]
- Yin, C.; Downey, S.I.; Klages-Mundt, N.L.; Ramachandran, S.; Chen, X.; Szabo, L.J.; Pumphrey, M.; Hulbert, S.H. Identification of promising host-induced silencing targets among genes preferentially transcribed in haustoria of Puccinia. BMC Genom. 2015, 16, 1–13. [Google Scholar] [CrossRef] [Green Version]
- Qi, T.; Zhu, X.; Tan, C.; Liu, P.; Guo, J.; Kang, Z.; Guo, J. Host-induced gene silencing of an important pathogenicity factor PsCPK1 in Puccinia striiformis f. sp. tritici enhances resistance of wheat to stripe rust. Plant Biotechnol. J. 2017, 16, 797–807. [Google Scholar] [CrossRef] [Green Version]
- Li, W.L.; Faris, J.D.; Muthukrishnan, S.; Liu, D.J.; Chen, P.D.; Gill, B.S. Isolation and characterization of novel cDNA clones of acidic chitinases and β-1,3-glucanases from wheat spikes infected by Fusarium graminearum. Theor. Appl. Genet. 2001, 102, 353–362. [Google Scholar] [CrossRef]
- Qin, S.; Veloso, J.; Baak, M.; Boogmans, B.; Bosman, T.; Puccetti, G.; Shi-Kunne, X.; Smit, S.; Grant-Downton, R.; Leisen, T.; et al. Molecular characterization reveals no functional evidence for naturally occurring cross-kingdom RNA interference in the early stages of Botrytis cinereal—Tomato interaction. Mol. Plant Pathol. 2022, 24, 3–15. [Google Scholar] [CrossRef]
- Coy, L.R.; Plummer, K.M.; Khalifa, M.E.; MacDiarmid, R.M. Mycovirus-encoded suppressors of RNA silencing: Possible allies or enemies in the use of RNAi to control fungal disease in crops. Front. Fungal Biol. 2022, 3, 965781. [Google Scholar] [CrossRef]
- Hoang, B.T.L.; Fletcher, S.J.; Brosnan, C.A.; Ghodke, A.B.; Manzie, N.; Mitter, N. RNAi as a Foliar Spray: Efficiency and Challenges to Field Applications. Int. J. Mol. Sci. 2022, 23, 6639. [Google Scholar] [CrossRef]
- Myung, K.; Satchivi, N.M.; Kingston, C.K. Retention, Uptake, and Translocation of Agrochemicals in Plants; American Chemical Society: Washington, DC, USA, 2014; Volume 1171. [Google Scholar]
- Forster, W.A.; O Kimberley, M. The contribution of spray formulation component variables to foliar uptake of agrichemicals. Pest Manag. Sci. 2015, 71, 1324–1334. [Google Scholar] [CrossRef]
- Jibrin, M.O.; Liu, Q.; Jones, J.B.; Zhang, S. Surfactants in plant disease management: A brief review and case studies. Plant Pathol. 2021, 70, 495–510. [Google Scholar] [CrossRef]
- Jain, R.G.; Fletcher, S.J.; Manzie, N.; Robinson, K.E.; Li, P.; Lu, E.; Brosnan, C.A.; Xu, Z.P.; Mitter, N. Foliar application of clay-delivered RNA interference for whitefly control. Nat. Plants 2022, 8, 535–548. [Google Scholar] [CrossRef]
- Voinnet, O.; Vain, P.; Angell, S.; Baulcombe, D.C. Systemic Spread of Sequence-Specific Transgene RNA Degradation in Plants Is Initiated by Localized Introduction of Ectopic Promoterless DNA. Cell 1998, 95, 177–187. [Google Scholar] [CrossRef] [Green Version]
- Yan, Y.; Ham, B.-K.; Chong, Y.H.; Yeh, S.-D.; Lucas, W.J. A Plant small rna-binding protein 1 Family Mediates Cell-to-Cell Trafficking of RNAi Signals. Mol. Plant 2020, 13, 321–335. [Google Scholar] [CrossRef] [Green Version]
- Dunoyer, P.; Schott, G.; Himber, C.; Meyer, D.; Takeda, A.; Carrington, J.C.; Voinnet, O. Small RNA Duplexes Function as Mobile Silencing Signals between Plant Cells. Science 2010, 328, 912–916. [Google Scholar] [CrossRef]
- Biedenkopf, D.; Will, T.; Knauer, T.; Jelonek, L.; Furch, A.C.U.; Busche, T.; Koch, A. Systemic spreading of exogenous applied RNA biopesticides in the crop plant Hordeum vulgare. Exrna 2020, 2, 12. [Google Scholar] [CrossRef]
- Dalakouras, A.; Jarausch, W.; Buchholz, G.; Bassler, A.; Braun, M.; Manthey, T.; Krczal, G.; Wassenegger, M. Delivery of Hairpin RNAs and Small RNAs Into Woody and Herbaceous Plants by Trunk Injection and Petiole Absorption. Front. Plant Sci. 2018, 9, 1253. [Google Scholar] [CrossRef] [Green Version]
- Konakalla, N.C.; Kaldis, A.; Masarapu, H.; Voloudakis, A.E. Topical application of double stranded RNA molecules deriving from Sesbania mosaic virus (SeMV) CP and MP genes protects Sesbania plants against SeMV. Eur. J. Plant Pathol. 2019, 155, 1345–1352. [Google Scholar] [CrossRef]
- Mitter, N.; Worrall, E.A.; Robinson, K.E.; Li, P.; Jain, R.G.; Taochy, C.; Fletcher, S.J.; Carroll, B.J.; Lu, G.Q.; Xu, Z.P. Clay nanosheets for topical delivery of RNAi for sustained protection against plant viruses. Nat. Plants 2017, 3, 16207. [Google Scholar] [CrossRef]
- Mitter, N.; Worrall, E.A.; Robinson, K.E.; Xu, Z.P.; Carroll, B.J. Induction of virus resistance by exogenous application of double-stranded RNA. Curr. Opin. Virol. 2017, 26, 49–55. [Google Scholar] [CrossRef]
- Robinson, K.E.; Worrall, E.A.; Mitter, N. Double stranded RNA expression and its topical application for non-transgenic resistance to plant viruses. J. Plant Biochem. Biotechnol. 2014, 23, 231–237. [Google Scholar] [CrossRef]
- Mao, Y.-B.; Cai, W.-J.; Wang, J.-W.; Hong, G.-J.; Tao, X.-Y.; Wang, L.-J.; Huang, Y.-P.; Chen, X.-Y. Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nat. Biotechnol. 2007, 25, 1307–1313. [Google Scholar] [CrossRef]
- Sarkar, A.; Roy-Barman, S. Spray-Induced Silencing of Pathogenicity Gene MoDES1 via Exogenous Double-Stranded RNA Can Confer Partial Resistance Against Fungal Blast in Rice. Front. Plant Sci. 2021, 12, 733129. [Google Scholar] [CrossRef]
- Yong, J.; Wu, M.; Zhang, R.; Bi, S.; Mann, C.W.G.; Mitter, N.; Carroll, B.J.; Xu, Z.P. Clay nanoparticles efficiently deliver small interfering RNA to intact plant leaf cells. Plant Physiol. 2022, 190, 2187–2202. [Google Scholar] [CrossRef]
- Uslu, V.V.; Bassler, A.; Krczal, G.; Wassenegger, M. High-Pressure-Sprayed Double Stranded RNA Does Not Induce RNA Interference of a Reporter Gene. Front. Plant Sci. 2020, 11, 534391. [Google Scholar] [CrossRef]
- Dalakouras, A.; McMillan, J.N.; Cardoza, V.; Maegele, I.; Dadami, E.; Runne, M.; Krczal, G.; Wassenegger, M. Induction of Silencing in Plants by High-Pressure Spraying of In vitro-Synthesized Small RNAs. Front. Plant Sci. 2016, 7, 1327. [Google Scholar] [CrossRef] [Green Version]
- Wytinck, N.; Manchur, C.L.; Li, V.H.; Whyard, S.; Belmonte, M.F. dsRNA Uptake in Plant Pests and Pathogens: Insights into RNAi-Based Insect and Fungal Control Technology. Plants 2020, 9, 1780. [Google Scholar] [CrossRef]
- Wytinck, N.; Sullivan, D.S.; Biggar, K.T.; Crisostomo, L.; Pelka, P.; Belmonte, M.F.; Whyard, S. Clathrin mediated endocytosis is involved in the uptake of exogenous double-stranded RNA in the white mold phytopathogen Sclerotinia sclerotiorum. Sci. Rep. 2020, 10, 12773. [Google Scholar] [CrossRef]
- Kettles, G.J.; Hofinger, B.J.; Hu, P.; Bayon, C.; Rudd, J.J.; Balmer, D.; Courbot, M.; Hammond-Kosack, K.E.; Scalliet, G.; Kanyuka, K. sRNA Profiling Combined with Gene Function Analysis Reveals a Lack of Evidence for Cross-Kingdom RNAi in the Wheat—Zymoseptoria tritici Pathosystem. Front. Plant Sci. 2019, 10, 892. [Google Scholar] [CrossRef]
- Panwar, V.; McCallum, B.; Bakkeren, G. Host-induced gene silencing of wheat leaf rust fungus Puccinia triticina pathogenicity genes mediated by the Barley stripe mosaic virus. Plant Mol. Biol. 2013, 81, 595–608. [Google Scholar] [CrossRef]
- Duanis-Assaf, D.; Galsurker, O.; Davydov, O.; Maurer, D.; Feygenberg, O.; Sagi, M.; Poverenov, E.; Fluhr, R.; Alkan, N. Double-stranded RNA targeting fungal ergosterol biosynthesis pathway controls Botrytis cinerea and postharvest grey mould. Plant Biotechnol. J. 2022, 20, 226–237. [Google Scholar] [CrossRef]
- Eduardo, C.d.A.; Wayne, B.H. RNA Interference—Natural Gene-Based Technology for Highly Specific Pest Control (HiSPeC). In RNA Interference; Ibrokhim, Y.A., Ed.; IntechOpen: Rijeka, Croatia, 2016; p. Ch. 19. [Google Scholar]
- Biosciences, G. Our Technology Allows Us to Make Cost-Effective RNA. Available online: https://www.greenlightbiosciences.com/how-do-we-make-rna/ (accessed on 22 March 2023).
- Khangura, R.; van Burgel, A.J. Foliar fungicides and their optimum timing reduce sclerotinia stem rot incidence, improve yield and profitability in canola (Brassica napus L.). Indian Phytopathol. 2021, 74, 549–558. [Google Scholar] [CrossRef]
- Mehlhorn, S.; Ulrich, J.; Baden, C.U.; Buer, B.; Maiwald, F.; Lueke, B.; Geibel, S.; Bucher, G.; Nauen, R. The mustard leaf beetle, Phaedon cochleariae, as a screening model for exogenous RNAi-based control of coleopteran pests. Pestic. Biochem. Physiol. 2021, 176, 104870. [Google Scholar] [CrossRef]
- De Schutter, K.; Taning, C.N.T.; Van Daele, L.; Van Damme, E.J.M.; Dubruel, P.; Smagghe, G. RNAi-Based Biocontrol Products: Market Status, Regulatory Aspects, and Risk Assessment. Front. Insect Sci. 2022, 1, 818037. [Google Scholar] [CrossRef]
- Romeis, J.; Widmer, F. Assessing the Risks of Topically Applied dsRNA-Based Products to Non-target Arthropods. Front. Plant Sci. 2020, 11, 679. [Google Scholar] [CrossRef]
- Castellanos-Arévalo, A.P.; Cabrera-Ponce, J.L.; Nava-Sandoval, C.; Délano-Frier, J.P. How to Overcome Recalcitrance? Novel Strategies and Recent Advances in the Genetic Transformation of Grain Amaranth. In The Amaranth Genome; Springer: Berlin/Heidelberg, Germany, 2021; pp. 125–149. [Google Scholar] [CrossRef]
- Imai, R.; Hamada, H.; Liu, Y.; Linghu, Q.; Kumagai, Y.; Nagira, Y.; Miki, R.; Taoka, N. In planta particle bombardment (iPB): A new method for plant transformation and genome editing. Plant Biotechnol. 2020, 37, 171–176. [Google Scholar] [CrossRef]
- Cody, J.P.; Maher, M.F.; Nasti, R.A.; Starker, C.G.; Chamness, J.C.; Voytas, D.F. Direct delivery and fast-treated Agrobacterium co-culture (Fast-TrACC) plant transformation methods for Nicotiana benthamiana. Nat. Protoc. 2022, 18, 81–107. [Google Scholar] [CrossRef]
- Zhi, H.; Zhou, S.; Pan, W.; Shang, Y.; Zeng, Z.; Zhang, H. The Promising Nanovectors for Gene Delivery in Plant Genome Engineering. Int. J. Mol. Sci. 2022, 23, 8501. [Google Scholar] [CrossRef]
- Zhang, D.; Zhong, C.; Smith, N.A.; de Feyter, R.; Greaves, I.K.; Swain, S.M.; Zhang, R.; Wang, M.-B. Nucleotide mismatches prevent intrinsic self-silencing of hpRNA transgenes to enhance RNAi stability in plants. Nat. Commun. 2022, 13, 3926. [Google Scholar] [CrossRef]
- Zhang, H.; Cao, Y.; Xu, D.; Goh, N.S.; Demirer, G.S.; Cestellos-Blanco, S.; Chen, Y.; Landry, M.P.; Yang, P. Gold-Nanocluster-Mediated Delivery of siRNA to Intact Plant Cells for Efficient Gene Knockdown. Nano Lett. 2021, 21, 5859–5866. [Google Scholar] [CrossRef]
- Demirer, G.S.; Zhang, H.; Goh, N.S.; Pinals, R.L.; Chang, R.; Landry, M.P. Carbon nanocarriers deliver siRNA to intact plant cells for efficient gene knockdown. Sci. Adv. 2020, 6, eaaz0495. [Google Scholar] [CrossRef]
- Schwartz, S.H.; Hendrix, B.; Hoffer, P.; Sanders, R.A.; Zheng, W. Carbon Dots for Efficient Small Interfering RNA Delivery and Gene Silencing in Plants. Plant Physiol. 2020, 184, 647–657. [Google Scholar] [CrossRef]
- Santana, I.; Wu, H.; Hu, P.; Giraldo, J.P. Targeted delivery of nanomaterials with chemical cargoes in plants enabled by a biorecognition motif. Nat. Commun. 2020, 11, 2045. [Google Scholar] [CrossRef]
- Yong, J.; Zhang, R.; Bi, S.; Li, P.; Sun, L.; Mitter, N.; Carroll, B.J.; Xu, Z.P. Sheet-like clay nanoparticles deliver RNA into developing pollen to efficiently silence a target gene. Plant Physiol. 2021, 187, 886–899. [Google Scholar] [CrossRef]
- Zhang, H.; Goh, N.S.; Wang, J.W.; Pinals, R.L.; González-Grandío, E.; Demirer, G.S.; Butrus, S.; Fakra, S.C.; Flores, A.D.R.; Zhai, R.; et al. Nanoparticle cellular internalization is not required for RNA delivery to mature plant leaves. Nat. Nanotechnol. 2022, 17, 197–205. [Google Scholar] [CrossRef]
- Burjoski, V.; Reddy, A.S.N. The Landscape of RNA-Protein Interactions in Plants: Approaches and Current Status. Int. J. Mol. Sci. 2021, 22, 2845. [Google Scholar] [CrossRef]
- Wu, S.; Li, X.; Wang, G. tRNA-like structures and their functions. FEBS J. 2022, 289, 5089–5099. [Google Scholar] [CrossRef]
- Sherlock, M.E.; Hartwick, E.W.; MacFadden, A.; Kieft, J.S. Structural diversity and phylogenetic distribution of valyl tRNA-like structures in viruses. RNA 2020, 27, 27–39. [Google Scholar] [CrossRef]
- Mochizuki, T.; Ohki, S.T. Cucumber mosaic virus: Viral genes as virulence determinants. Mol. Plant Pathol. 2012, 13, 217–225. [Google Scholar] [CrossRef]
- Wilusz, J.E.; Freier, S.M.; Spector, D.L. 3′ End Processing of a Long Nuclear-Retained Noncoding RNA Yields a tRNA-like Cytoplasmic RNA. Cell 2008, 135, 919–932. [Google Scholar] [CrossRef] [Green Version]
- Mans, R.M.W.; Pleij, C.W.A.; Bosch, L. tRNA-like structures. Structure, function and evolutionary significance. JBIC J. Biol. Inorg. Chem. 1991, 201, 303–324. [Google Scholar] [CrossRef]
- Yot, P.; Pinck, M.; Haenni, A.-L.; Duranton, H.M.; Chapeville, F. Valine-Specific tRNA-like Structure in Turnip Yellow Mosaic Virus RNA. Proc. Natl. Acad. Sci. USA 1970, 67, 1345–1352. [Google Scholar] [CrossRef]
- Colussi, T.M.; Costantino, D.A.; Hammond, J.A.; Ruehle, G.M.; Nix, J.C.; Kieft, J.S. The structural basis of transfer RNA mimicry and conformational plasticity by a viral RNA. Nature 2014, 511, 366–369. [Google Scholar] [CrossRef] [Green Version]
- Lezzhov, A.A.; Atabekova, A.K.; Tolstyko, E.A.; Lazareva, E.A.; Solovyev, A.G. RNA phloem transport mediated by pre-miRNA and viral tRNA-like structures. Plant Sci. 2019, 284, 99–107. [Google Scholar] [CrossRef]
- Tolstyko, E.A.; Lezzhov, A.A.; Morozov, S.Y.; Solovyev, A.G. Phloem transport of structured RNAs: A widening repertoire of trafficking signals and protein factors. Plant Sci. 2020, 299, 110602. [Google Scholar] [CrossRef]
- Zhang, W.; Thieme, C.J.; Kollwig, G.; Apelt, F.; Yang, L.; Winter, N.; Andresen, N.; Walther, D.; Kragler, F. tRNA-Related Sequences Trigger Systemic mRNA Transport in Plants. Plant Cell 2016, 28, 1237–1249. [Google Scholar] [CrossRef] [Green Version]
- Thieme, C.J.; Rojas-Triana, M.; Stecyk, E.; Schudoma, C.; Zhang, W.; Yang, L.; Miñambres, M.; Walther, D.; Schulze, W.X.; Paz-Ares, J.; et al. Endogenous Arabidopsis messenger RNAs transported to distant tissues. Nat. Plants 2015, 1, 15025. [Google Scholar] [CrossRef]
- Park, S.-Y.; Shimizu, K.; Brown, J.; Aoki, K.; Westwood, J.H. Mobile Host mRNAs Are Translated to Protein in the Associated Parasitic Plant Cuscuta campestris. Plants 2021, 11, 93. [Google Scholar] [CrossRef]
- Yang, L.; Machin, F.; Wang, S.; Saplaoura, E.; Kragler, F. Heritable transgene-free genome editing in plants by grafting of wild-type shoots to transgenic donor rootstocks. Nat. Biotechnol. 2023, 41, 958–967. [Google Scholar] [CrossRef]
- Tolstyko, E.A.; Lezzhov, A.A.; Pankratenko, A.V.; Serebryakova, M.V.; Solovyev, A.G.; Morozov, S.Y. Detection and in vitro studies of Cucurbita maxima phloem serpin-1 RNA-binding properties. Biochimie 2020, 170, 118–127. [Google Scholar] [CrossRef]
- Yang, L.; Perrera, V.; Saplaoura, E.; Apelt, F.; Bahin, M.; Kramdi, A.; Olas, J.; Mueller-Roeber, B.; Sokolowska, E.; Zhang, W.; et al. m5C Methylation Guides Systemic Transport of Messenger RNA over Graft Junctions in Plants. Curr. Biol. 2019, 29, 2465–2476.e5. [Google Scholar] [CrossRef] [Green Version]
- Zeng, Y.; Wagner, E.J.; Cullen, B.R. Both Natural and Designed Micro RNAs Can Inhibit the Expression of Cognate mRNAs When Expressed in Human Cells. Mol. Cell 2002, 9, 1327–1333. [Google Scholar] [CrossRef]
- Parizotto, E.A.; Dunoyer, P.; Rahm, N.; Himber, C.; Voinnet, O. In vivo investigation of the transcription, processing, endonucleolytic activity, and functional relevance of the spatial distribution of a plant miRNA. Genes Dev. 2004, 18, 2237–2242. [Google Scholar] [CrossRef] [Green Version]
- Thakur, A.; Sanju, S.; Siddappa, S.; Srivastava, N.; Shukla, P.K.; Pattanayak, D.; Sharma, S.; Singh, B. Artifical MicroRNA Mediated Gene Silencing of Phytophthora infestans Single Effector Avr3a Gene Imparts Moderate Type of Late Blight Resistance in Potato. Plant Pathol. J. 2015, 14, 1–12. [Google Scholar] [CrossRef] [Green Version]
- Liu, P.; Zhang, X.; Zhang, F.; Xu, M.; Ye, Z.; Wang, K.; Liu, S.; Han, X.; Cheng, Y.; Zhong, K.; et al. A virus-derived siRNA activates plant immunity by interfering with ROS scavenging. Mol. Plant 2021, 14, 1088–1103. [Google Scholar] [CrossRef]
- Faisal, M.; Abdel-Salam, E.M.; Alatar, A.A. Artificial microRNA-Based RNA Interference and Specific Gene Silencing for Developing Insect Resistance in Solanum lycopersicum. Agronomy 2021, 11, 136. [Google Scholar] [CrossRef]
- Saini, R.P.; Raman, V.; Dhandapani, G.; Malhotra, E.V.; Sreevathsa, R.; Kumar, P.A.; Sharma, T.R.; Pattanayak, D. Silencing of HaAce1 gene by host-delivered artificial microRNA disrupts growth and development of Helicoverpa armigera. PLoS ONE 2018, 13, e0194150. [Google Scholar] [CrossRef]
- Yogindran, S.; Rajam, M.V. Artificial miRNA-mediated silencing of ecdysone receptor (EcR) affects larval development and oogenesis in Helicoverpa armigera. Insect Biochem. Mol. Biol. 2016, 77, 21–30. [Google Scholar] [CrossRef]
- Bally, J.; Fishilevich, E.; Doran, R.L.; Lee, K.; De Campos, S.B.; German, M.A.; Narva, K.E.; Waterhouse, P.M. Plin-amiR, a pre-microRNA-based technology for controlling herbivorous insect pests. Plant Biotechnol. J. 2020, 18, 1925–1932. [Google Scholar] [CrossRef]
- Bolognesi, R.; Ramaseshadri, P.; Anderson, J.; Bachman, P.; Clinton, W.; Flannagan, R.; Ilagan, O.; Lawrence, C.; Levine, S.; Moar, W.; et al. Characterizing the Mechanism of Action of Double-Stranded RNA Activity against Western Corn Rootworm (Diabrotica virgifera virgifera LeConte). PLoS ONE 2012, 7, e47534. [Google Scholar] [CrossRef]
- Oliver, R.; Hewitt, H.G. Fungicides in Crop Protection, 2nd ed.; CABI: Wallingford, UK, 2014. [Google Scholar]
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Mann, C.W.G.; Sawyer, A.; Gardiner, D.M.; Mitter, N.; Carroll, B.J.; Eamens, A.L. RNA-Based Control of Fungal Pathogens in Plants. Int. J. Mol. Sci. 2023, 24, 12391. https://doi.org/10.3390/ijms241512391
Mann CWG, Sawyer A, Gardiner DM, Mitter N, Carroll BJ, Eamens AL. RNA-Based Control of Fungal Pathogens in Plants. International Journal of Molecular Sciences. 2023; 24(15):12391. https://doi.org/10.3390/ijms241512391
Chicago/Turabian StyleMann, Christopher W. G., Anne Sawyer, Donald M. Gardiner, Neena Mitter, Bernard J. Carroll, and Andrew L. Eamens. 2023. "RNA-Based Control of Fungal Pathogens in Plants" International Journal of Molecular Sciences 24, no. 15: 12391. https://doi.org/10.3390/ijms241512391