Research Advances and Application Prospects of Cross-kingdom RNA Interference in Plant-microbe Interactions
YAN Geng-Xuan1,2, TIAN Yuan1,3, LIU Yu-Tong4, ZHANG Shu-Mei1, TIAN Jie-Ping1, YU De-Shui1,*
1 Institute of Microbiology, Heilongjiang Academy of Sciences, Harbin 150010, China; 2 College of Life Sciences, Northeast Forestry University, Harbin 150006, China; 3 College of Food Science, Northeast Agricultural University, Harbin 150030, China; 4 Heilongjiang Agricultural Engineering Vocational College, Harbin 150088, China
Abstract：RNA interference (RNAi) is a conserved mechanism that regulates gene expression in eukaryotes. Within the domains of plants and microbes, this mechanism not only governs intracellular gene expression but also transcends species boundaries, mediating gene silencing across distinct biological kingdoms. This phenomenon, termed Cross-kingdom RNAi (ckRNAi), enables RNAi signals to operate bidirectionally between organisms from different taxonomic groups. Notably, ckRNAi is widely observed in plant-fungal systems, where it reciprocally regulates growth and behaviors of both interacting partners. This review summarizes recent advances in ckRNAi research within plant-microbe interactions and explores its application scenarios, aiming to provide reference for developing ckRNAi-based technologies or products to combat plant diseases.
[1] Akbar S, Wei Y, Zhang M Q.2022. RNA interference: Promising approach to combat plant viruses[J]. International Journal of Molecular Sciences, 23(10): 5312. [2] Attia S, Khan R S, Iqbal A, et al.2022. Host-induced gene silencing: An effective control strategy against Fusarium species[J]. Journal of Plant Diseases and Protection, 129(5): 1025-1030. [3] Axtell M J, Bowman J L.2008. Evolution of plant microRNAs and their targets[J]. Trends in Plant Science, 13(7): 343-349. [4] Baldrich P, Meyers B.2019. Bacteria send messages to colonize plant roots[J]. Science, 365(6456): 868-869. [5] Baldrich P, Rutter B D, Karimi H Z, et al.2019. Plant extracellular vesicles contain diverse small RNA species and are enriched in 10-to 17-nucleotide “tiny” RNAs[J]. The Plant Cell, 31(2): 315-324. [6] Baulcombe D C.2015. VIGS, HIGS and FIGS: Small RNA silencing in the interactions of viruses or filamentous organisms with their plant hosts[J]. Current Opinion in Plant Biology, 26: 141-146. [7] Cai Q, He B, Kogel K H, et al.2018. Cross-kingdom RNA trafficking and environmental RNAi-nature's blueprint for modern crop protection strategies[J]. Current Opinion in Microbiology, 46: 58-64. [8] Carreras N, Esquivel E U, Villalobos J M, et al.2013. The RNAi machinery regulates growth and development in the filamentous fungus Trichoderma atroviride[J]. Molecular Microbiology, 89(1): 96-112. [9] Chang P K, Scharfenstein LL, Wei Q, et al.2010. Development and refinement of a high-efficiency gene-targeting system for Aspergillus flavus[J]. Journal of Microbiological Methods, 81(3): 240-246. [10] Dallaire A, Manley B, Wilkens M, et al.2021. Transcriptional activity and epigenetic regulation of transposable elements in the symbiotic fungus Rhizophagus irregularis[J]. Genome Research, 31(12): 2290-2302. [11] Derbyshire M, Mbengue M, Barascud M, et al.2019. Small RNAs from the plant pathogenic fungus Sclerotinia sclerotiorum highlight host candidate genes associated with quantitative disease resistance[J]. Molecular Plant Pathology, 20(9): 1279-1297. [12] Duanis D, Galsurker O, Davydov O, et al.2022. Double-stranded RNA targeting fungal ergosterol biosynthesis pathway controls Botrytis cinerea and postharvest grey mould[J]. Plant Biotechnology Journal, 20(1): 226-237. [13] Fairbairn D J, Cavallaro A S, Bernard M, et al.2007. Host-delivered RNAi: An effective strategy to silence genes in plant Parasitic nematodes[J]. Planta, 226: 1525-1533. [14] Guan R, Miao X, Li H.2024. Bacteria-based Double-stranded RNA Production to Develop Cost-effective RNA Interference Application for Insect Pest Management[M]. Double-Stranded RNA: Methods and Protocols, Humana Press, New York, America, pp. 73-81. [15] He B, Cai Q, Qiao L, et al.2021. RNA-binding proteins contribute to small RNA loading in plant extracellular vesicles[J]. Nature Plants, 7(3): 342-352. [16] He F, Zhang R, Zhao J, et al.2019. Host-induced silencing of Fusarium graminearum genes enhances the resistance of Brachypodium distachyon to Fusarium head blight[J]. Frontiers in Plant Science, 10: 1362. [17] Hu S, Li Y, Shen J.2020. A diverse membrane interaction network for plant multivesicular bodies: Roles in proteins vacuolar delivery and unconventional secretion[J]. Frontiers in Plant Science, 11: 425. [18] Islam M, Davis Z, Chen L, et al.2021. Minicell-based fungal RNAi delivery for sustainable crop protection[J]. Microbial Biotechnology, 14(4): 1847-1856. [19] Katiyar S, Morgan R, Dahlbeck D, et al.2006. A pathogen-inducible endogenous siRNA in plant immunity[J]. Proceedings of the National Academy of Sciences of the USA, 103(47): 18002-18007. [20] Kikuchi Y, Hijikata N, Ohtomo R, et al.2016. Aquaporin-mediated long-distance polyphosphate translocation directed towards the host in arbuscular mycorrhizal symbiosis: Application of virus-induced gene silencing[J]. New Phytologist, 211(4): 1202-1208. [21] Kim D H, Rossi J J.2008. RNAi mechanisms and applications[J]. Biotechniques, 44(5): 613-616. [22] Koch A, Biedenkopf D, Furch A, et al.2016. 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[J]. PLOS Pathogens, 12(10): e1005901. [23] Koch A, Höfle L, Werner B, et al.2019. 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[J]. Molecular Plant Pathology, 20(12): 1636-1644. [24] Koch A, Schlemmer T, Höfle L, et al.2020. Host-induced gene silencing involves transfer of dsRNA-derived siRNA via extracellular vesicles[J]. BioRxiv, 02: 945154. [25] Kong X, Yang M, Le B H, et al.2022. The master role of siRNAs in plant immunity[J]. Molecular Plant Pathology, 23(10): 1565-1574. [26] Ledford W, Silvestri A, Fiorilli V, et al.2024. A journey into the world of small RNAs in the Arbuscular mycorrhizal symbiosis[J]. New Phytologist, 242(4): 1534-1544. [27] Lopez S, Baulcombe D.2022. Roles of RNA silencing in viral and non-viral plant immunity and in the crosstalk between disease resistance systems[J]. Nature Reviews Molecular Cell Biology, 23(10): 645-662. [28] Mueth N, Ramachandran S, Hulbert S.2015. Small RNAs from the wheat stripe rust fungus (Puccinia striiformis f. sp. tritici)[J]. BMC Genomics, 16: 1-6. [29] Nowara D, Gay A, Lacomme C, et al.2010. HIGS: Host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis[J]. The Plant Cell, 22(9): 3130-3141. [30] Pallis S, Alyokhin A, Manley B, et al.2023. Effects of low doses of a novel dsRNA-based biopesticide (Calantha) on the Colorado potato beetle[J]. Journal of Economic Entomology, 116(2): 456-461. [31] Panwar V, McCallum B, Bakkeren G.2013. Host-induced gene silencing of wheat leaf rust fungus Puccinia triticina pathogenicity genes mediated by the Barley stripe mosaic virus[J]. Plant Molecular Biology, 81: 595-608. [32] Popp C, Ott T.2011. Regulation of signal transduction and bacterial infection during root nodule symbiosis[J]. Current Opinion in Plant Biology, 14(4): 458-467. [33] Preall J B, Sontheimer E J.2005. RNAi: RISC gets loaded[J]. Cell, 123(4): 543-545. [34] Qiao S A, Gao Z, Roth R.2023. A perspective on cross-kingdom RNA interference in mutualistic symbioses[J]. New Phytologist, 240(1): 68-79. [35] Read D J, Duckett J G, Francis R, et al.2000. Symbiotic fungal associations in 'lower' land plants[J]. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 355(1398): 815-831. [36] Ren B, Wang X, Duan J, et al.2019. Rhizobial tRNA-derived small RNAs are signal molecules regulating plant nodulation[J]. Science, 365(6456): 919-922. [37] Shivakumara T N, Chaudhary S, Kamaraju D, et al.2017. Host-induced silencing of two pharyngeal gland genes conferred transcriptional alteration of cell wall-modifying enzymes of Meloidogyne incognita vis-à-vis perturbed nematode infectivity in eggplant[J]. Frontiers in Plant Science, 8: 473. [38] Silvestri A, Fiorilli V, Miozzi L, et al.2019. In silico analysis of fungal small RNA accumulation reveals putative plant mRNA targets in the symbiosis between an arbuscular mycorrhizal fungus and its host plant[J]. BMC Genomics, 20: 1-8. [39] Spada M, Pugliesi C, Fambrini M, et al.2024. Challenges and opportunities arising from host-botrytis cinerea interactions to outline novel and sustainable control strategies: The key role of RNA interference[J]. International Journal of Molecular Sciences, (12): 6798. [40] Stanton B A.2021. Extracellular vesicles and host-pathogen interactions: A review of inter-kingdom signaling by small noncoding RNA[J]. Genes, 12(7): 1010. [41] Tetorya M, Rajam M.2021. RNAi-mediated silencing of PEX6 and GAS1 genes of Fusarium oxysporum f. sp. lycopersici confers resistance against Fusarium wilt in tomato[J]. 3 Biotech, 11(10): 443. [42] Torres S, Ruiz R M.2017. The RNAi universe in fungi: A varied landscape of small RNAs and biological functions[J]. Annual Review of Microbiology, 71(1): 371-391. [43] Villalobos J, Herrera A, Carrerasr N.2016. The interaction of fungi with the environment orchestrated by RNAi[J]. Mycologia, 108(3): 556-571. [44] Wang S, Xie X, Che X, et al.2023. Host- and virus- induced gene silencing of HOG1-MAPK cascade genes in Rhizophagus irregularis inhibit arbuscule development and reduce resistance of plants to drought stress[J]. Plant Biotechnology Journal, 21(4): 866-883. [45] Weiberg A, Wang M, Lin F M, et al.2013. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways[J]. Science, 342(6154): 118-123. [46] Wen H, Zhao J, Zhang B, et al.2023. Microbe-induced gene silencing boosts crop protection against soil-borne fungal pathogens[J]. Nature Plants, 9(9): 1409-1418. [47] Wong J, Singan V, Monti R, et al.2022. The ectomycorrhizal fungus Pisolithus microcarpus encodes a microRNA involved in cross-kingdom gene silencing during symbiosis[J]. Proceedings of the National Academy of Sciences of the USA, 119(3): e2103527119. [48] Xie X, Lin H, Peng X, et al.2016. Arbuscular mycorrhizal symbiosis requires a phosphate transceptor in the Gigaspora margarita fungal symbiont[J]. Molecular Plant, 9(12): 1583-1608. [49] Zand H, Innes R W.2022. Molecular mechanisms underlying host-induced gene silencing[J]. The Plant Cell, 34(9): 3183-3199. [50] Zeng J, Gupta V K, Jiang Y, et al.2019. Cross-kingdom small RNAs among animals, plants and microbes[J]. Cells, 8(4): 371. [51] Zeng T, Rodriguez L, Mansurkhodzaev A, et al.2020. A lysin motif effector subverts chitin-triggered immunity to facilitate arbuscular mycorrhizal symbiosis[J]. New Phytologist, 225(1): 448-460. [52] Zhang B, Pan X, Cobb G P, et al.2006. Plant microRNA: A small regulatory molecule with big impact[J]. Developmental Biology, 289(1): 3-16. [53] Zhang T, Zhao Y L, Zhao J H, et al.2016. Cotton plants export microRNAs to inhibit virulence gene expression in a fungal pathogen[J]. Nature Plants, 2(10): 1-6. [54] Zhu C, Liu J H, Zhao J H, et al.2022. A fungal effector suppresses the nuclear export of AGO1-miRNA complex to promote infection in plants[J]. Proceedings of the National Academy of Sciences of the USA, 119(12): e2114583119.
