Trans-kingdom RNA interactions drive the evolutionary arms race between hosts and pathogens.

Trans-kingdom RNA plays a key role in host-parasite interactions. Hosts export specific endogenous microRNAs (miRNAs) into pathogens to target pathogen virulence genes and inhibit their invasion. In addition, trans-kingdom sRNAs produced by parasites may function as RNA effectors to suppress host immunity. Here, we summarize recent, important findings regarding trans-kingdom RNA and focus on the roles of trans-kingdom RNA in driving an evolutionary arms race between host and pathogen. We suggest that trans-kingdom RNA is a new platform for such arms races. Furthermore, we conjecture that trans-kingdom RNA contributes to horizontal gene transfer (HGT) involved in host-pathogen interactions. In addition, we propose that trans-kingdom RNA exchange and RNA driven HGT can have a great impact on the evolutionary ecology of interacting species.

• Publication year

  2019

• Venue

  Current Opinion in Genetics and Development

• Publication date

  2019-10-01

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1016/j.gde.2019.07.019PMID 31472442
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• A fungal milRNA mediates epigenetic repression of a virulence gene in Verticillium dahliae

  2019cited by this paper
• A novel fungal effector from Puccinia graminis suppressing RNA silencing and plant defense responses.

  2019cited by this paper
• Horizontal gene transfer allowed the emergence of broad host range entomopathogens

  2019cited by this paper
• The Enterococcus: a Model of Adaptability to Its Environment

  2019cited by this paper
• A Phytophthora Effector Suppresses Trans-Kingdom RNAi to Promote Disease Susceptibility.

  2019cited by this paper
• From pathogen to endophyte: an endophytic population of Verticillium dahliae evolved from a sympatric pathogenic population.

  2019cited by this paper
• Agrobacterium-mediated horizontal gene transfer: Mechanism, biotechnological application, potential risk and forestalling strategy.

  2019cited by this paper
• Evolution of Plasmid-Mediated Antibiotic Resistance in the Clinical Context.

  2018cited by this paper
• Horizontal transfer of BovB and L1 retrotransposons in eukaryotes

  2018cited by this paper
• Unity in diversity: structural and functional insights into the ancient partnerships between plants and fungi.

  2018cited by this paper
• The nonstop decay and the RNA silencing systems operate cooperatively in plants

  2018cited by this paper
• Microbiomes as Metacommunities: Understanding Host-Associated Microbes through Metacommunity Ecology.

  2018cited by this paper
• Dietary plant miRNAs as an augmented therapy: cross-kingdom gene regulation

  2018cited by this paper
• The Genome of the Fungal Pathogen Verticillium dahliae Reveals Extensive Bacterial to Fungal Gene Transfer

  2018cited by this paper
• Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes

  2018cited by this paper
• Plant-Derived Exosomal MicroRNAs Shape the Gut Microbiota.

  2018cited by this paper
• Prokaryotic horizontal gene transfer within the human holobiont: ecological-evolutionary inferences, implications and possibilities

  2018cited by this paper
• Strategies to combat antimicrobial resistance: anti-plasmid and plasmid curing

  2018cited by this paper
• Small RNA-based antimicrobial immunity

  2018cited by this paper
• Microbial Interkingdom Interactions in Roots Promote Arabidopsis Survival

  2018cited by this paper
• RNA decay is an antiviral defense in plants that is counteracted by viral RNA silencing suppressors

  2018cited by this paper
• Cross-kingdom RNA trafficking and environmental RNAi-nature's blueprint for modern crop protection strategies.

  2018cited by this paper
• Trans-Kingdom RNA Silencing in Plant-Fungal Pathogen Interactions.

  2017cited by this paper
• MicroRNAs from the parasitic plant Cuscuta campestris target host messenger RNAs

  2017cited by this paper
• Cross-kingdom RNA trafficking and environmental RNAi for powerful innovative pre- and post-harvest plant protection.

  2017cited by this paper
• Function, Discovery, and Exploitation of Plant Pattern Recognition Receptors for Broad-Spectrum Disease Resistance.

  2017cited by this paper
• From Chaos to Harmony: Responses and Signaling upon Microbial Pattern Recognition.

  2017cited by this paper
• Red blood cells release microparticles containing human argonaute 2 and miRNAs to target genes of Plasmodium falciparum

  2017cited by this paper
• Comparative genomics reveals cotton‐specific virulence factors in flexible genomic regions in Verticillium dahliae and evidence of horizontal gene transfer from Fusarium

  2017cited by this paper
• Receptor Kinases in Plant-Pathogen Interactions: More Than Pattern Recognition[OPEN]

  2017cited by this paper
• Viral reverse transcriptases.

  2017cited by this paper
• Transfer of DNA from Bacteria to Eukaryotes

  2016cited by this paper
• Cotton plants export microRNAs to inhibit virulence gene expression in a fungal pathogen

  2016cited by this paper
• Transcriptional Regulation of Pattern-Triggered Immunity in Plants.

  2016cited by this paper
• RNA Quality Control as a Key to Suppressing RNA Silencing of Endogenous Genes in Plants.

  2016cited by this paper
• The Discovery of Reverse Transcriptase.

  2016cited by this paper
• In plants, decapping prevents RDR6-dependent production of small interfering RNAs from endogenous mRNAs

  2015cited by this paper
• Microbiota and Host Nutrition across Plant and Animal Kingdoms.

  2015cited by this paper
• SKI2 mediates degradation of RISC 5′-cleavage fragments and prevents secondary siRNA production from miRNA targets in Arabidopsis

  2015cited by this paper
• Nicotiana Small RNA Sequences Support a Host Genome Origin of Cucumber Mosaic Virus Satellite RNA

  2015cited by this paper
• Conversations between kingdoms: small RNAs.

  2015cited by this paper
• Supplementary Materials for Suppression of endogenous gene silencing by bidirectional cytoplasmic RNA decay in Arabidopsis

  2015cited by this paper
• Roots shaping their microbiome: global hotspots for microbial activity.

  2015cited by this paper
• Macromolecule exchange in Cuscuta-host plant interactions.

  2015cited by this paper
• Small RNAs--the secret agents in the plant-pathogen interactions.

  2015cited by this paper
• The RNA Helicases AtMTR4 and HEN2 Target Specific Subsets of Nuclear Transcripts for Degradation by the Nuclear Exosome in Arabidopsis thaliana

  2014cited by this paper
• New wind in the sails: improving the agronomic value of crop plants through RNAi-mediated gene silencing.

  2014cited by this paper
• Genomic-scale exchange of mRNA between a parasitic plant and its hosts

  2014cited by this paper
• Small RNAs: a new paradigm in plant-microbe interactions.

  2014cited by this paper
• Horizontal gene transfer in eukaryotic plant pathogens.

  2014cited by this paper
• Extracellular Vesicle-Mediated Transfer of Genetic Information between the Hematopoietic System and the Brain in Response to Inflammation

  2014cited by this paper
• Mechanisms of nutrient acquisition and utilization during fungal infections of leaves.

  2014cited by this paper
• Extensive Intra-Kingdom Horizontal Gene Transfer Converging on a Fungal Fructose Transporter Gene

  2013cited by this paper
• Oomycete pathogens encode RNA silencing suppressors

  2013cited by this paper
• Fungal Small RNAs Suppress Plant Immunity by Hijacking Host RNA Interference Pathways

  2013cited by this paper
• Translocation of sickle cell erythrocyte microRNAs into Plasmodium falciparum inhibits parasite translation and contributes to malaria resistance.

  2012cited by this paper
• Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing

  2012cited by this paper
• Silencing and Innate Immunity in Plant Defense Against Viral and Non-Viral Pathogens

  2012cited by this paper
• Multiple horizontal gene transfers of ammonium transporters/ammonia permeases from prokaryotes to eukaryotes: toward a new functional and evolutionary classification.

  2012cited by this paper
• RNA-guided genetic silencing systems in bacteria and archaea

  2012cited by this paper
• Genomic Analysis of the Necrotrophic Fungal Pathogens Sclerotinia sclerotiorum and Botrytis cinerea

  2011cited by this paper
• The Arabidopsis thaliana natriuretic peptide AtPNP-A is a systemic regulator of leaf dark respiration and signals via the phloem.

  2011cited by this paper
• Widespread Endogenization of Genome Sequences of Non-Retroviral RNA Viruses into Plant Genomes

  2011cited by this paper
• Horizontal gene transfer facilitated the evolution of plant parasitic mechanisms in the oomycetes

  2011cited by this paper
• Comparative Genomics Yields Insights into Niche Adaptation of Plant Vascular Wilt Pathogens

  2011cited by this paper
• Unique Functionality of 22 nt miRNAs in Triggering RDR6-Dependent siRNA Biogenesis from Target Transcripts in Arabidopsis

  2010cited by this paper
• Plant immunity triggered by microbial molecular signatures.

  2010cited by this paper
• 22-nucleotide RNAs trigger secondary siRNA biogenesis in plants

  2010cited by this paper
• Horizontal Gene Transfer by the Parasitic Plant Striga hermonthica

  2010cited by this paper
• FSY1, a horizontally transferred gene in the Saccharomyces cerevisiae EC1118 wine yeast strain, encodes a high-affinity fructose/H+ symporter.

  2010cited by this paper
• Endogenous non-retroviral RNA virus elements in mammalian genomes

  2010cited by this paper
• Suppression of the MicroRNA Pathway by Bacterial Effector Proteins

  2008cited by this paper
• The powdery mildews: a review of the world's most familiar (yet poorly known) plant pathogens.

  2008cited by this paper
• Horizontal gene transfer in eukaryotic evolution

  2008cited by this paper
• Effects of retroviruses on host genome function.

  2008cited by this paper
• The hemibiotrophic lifestyle of Colletotrichum species.

  2008cited by this paper
• The Reacquisition of Biotin Prototrophy in Saccharomyces cerevisiae Involved Horizontal Gene Transfer, Gene Duplication and Gene Clustering

  2007cited by this paper
• The plant immune system

  2006cited by this paper
• Licensed to kill: the lifestyle of a necrotrophic plant pathogen.

  2006cited by this paper
• Horizontal gene transfer promoted evolution of the ability to propagate under anaerobic conditions in yeasts

  2004cited by this paper
• How big is the iceberg of which organellar genes in nuclear genomes are but the tip?

  2003cited by this paper
• Millions of years of evolution preserved: a comprehensive catalog of the processed pseudogenes in the human genome.

  2003cited by this paper
• A Phosphate Transporter from Medicago truncatula Involved in the Acquisition of Phosphate Released by Arbuscular Mycorrhizal Fungi Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.004861.

  2002cited by this paper
• Horizontal gene transfer in prokaryotes: quantification and classification.

  2001cited by this paper
• The role of haustoria in sugar supply during infection of broad bean by the rust fungus Uromyces fabae

  2001cited by this paper
• Cells of the yeast Saccharomyces cerevisiae are transformable by DNA under non‐artificial conditions

  2000cited by this paper
• Osmoregulated periplasmic glucans in Proteobacteria.

  2000cited by this paper
• Agrobacterium VirE2 protein mediates nuclear uptake of single-stranded DNA in plant cells.

  1996cited by this paper
• The yeast Saccharomyces kluyveri as a recipient eukaryote in transkingdom conjugation: behavior of transmitted plasmids in transconjugants

  1994cited by this paper
• Movement of shuttle plasmids from Escherichia coli into yeasts other than Saccharomyces cerevisiae using trans-kingdom conjugation.

  1993cited by this paper
• Movement of shuttle plasmids from Escherichia coli into yeasts other than Saccharomyces cerevisiae using trans-kingdom conjugation.

  1993cited by this paper
• Characterization of the restriction site of a prokaryotic intron-encoded endonuclease.

  1990cited by this paper
• Reverse transcriptase in bacteria

  1989cited by this paper
• Bacterial conjugative plasmids mobilize DNA transfer between bacteria and yeast

  1989cited by this paper
• Activation of Agrobacterium tumefaciens vir gene expression generates multiple single‐stranded T‐strand molecules from the pTiA6 T‐region: requirement for 5′ virD gene products.

  1987cited by this paper
• Processed pseudogenes: characteristics and evolution.

  1985cited by this paper
• Microbiota and Host Nutrition across Plant and Animal Kingdoms Figure 1. Physiological Functions of the Plant Roots and Human Gut in Nutrient Uptake, Spatial Aspects of Microbiota Composition, and Factors Driving Community Establishment

  year unknowncited by this paper

• Trans-Kingdom RNA Dialogues: miRNA and milRNA Networks as Biotechnological Tools for Sustainable Crop Defense and Pathogen Control

  2025cites this paper
• A novel role of Dermatophagoides farinae-derived miR-276-3p in aggravating mite-induced allergic airway inflammation

  2025cites this paper
• Cross-kingdom RNAi: A universal mechanism of inter-organismal communication with many unknowns.

  2025cites this paper
• Mechanisms of Interaction Between Yeast, Bacterial Biota, and Local Immune Response in Recurrent Vulvovaginal Candidiasis (A Review)

  2025cites this paper
• Trans-kingdom RNAi in plant–pathogen interactions: mechanisms and biocontrol strategies

  2025cites this paper
• A non-classical PUF family protein in oomycetes functions as a pre-rRNA processing regulator and a target for RNAi-based disease control

  2025cites this paper
• Prion–like Proteins in Plants: Key Regulators of Development and Environmental Adaptation via Phase Separation

  2024cites this paper
• OsPIPK-FAB, A Negative Regulator in Rice Immunity Unveiled by OsMBL1 Inhibition

  2024cites this paper
• A virulent milRNA inhibits host immunity by silencing a host receptor‐like kinase MaLYK3 and facilitates infection by Fusarium oxysporum f. sp. cubense

  2024cites this paper
• Plant microRNAs regulate the defense response against pathogens

  2024cites this paper
• High-efficiency green management of potato late blight by a self-assembled multicomponent nano-bioprotectant

  2023cites this paper
• Recent Advances in the Genetic and Biochemical Mechanisms of Rice Resistance to Brown Planthoppers (Nilaparvata lugens Stål)

  2023cites this paper
• Cellular and Natural Viral Engineering in Cognition-Based Evolution

  2023cites this paper
• FoQDE2-dependent milRNA promotes Fusarium oxysporum f. sp. cubense virulence by silencing a glycosyl hydrolase coding gene expression

  2022cites this paper
• Verticillium dahliae Secretes Small RNA to Target Host MIR157d and Retard Plant Floral Transition During Infection

  2022cites this paper
• Molecular Defense Response of Pine Trees (Pinus spp.) to the Parasitic Nematode Bursaphelenchus xylophilus

  2022cites this paper
• Potential Mechanisms Linking Food-Derived MicroRNAs, Gut Microbiota and Intestinal Barrier Functions in the Context of Nutrition and Human Health

  2021cites this paper
• RNA silencing: From discovery and elucidation to application and perspectives.

  2021cites this paper
• FoQDE2-dependent milRNA promotes Fusarium oxysporum f. sp. cubense virulence by targeting a glycosyl hydrolase coding gene at transcriptional level

  2021cites this paper
• MicroRNA-Like Small RNAs in the edible mushroom Agaricus

  2021cites this paper
• RNA-Seq, Bioinformatic Identification of Potential MicroRNA-like Small RNAs in the Edible Mushroom Agaricus bisporus and Experimental Approach for Their Validation

  2021cites this paper
• Satellite-Like W-Elements: Repetitive, Transcribed, and Putative Mobile Genetic Factors with Potential Roles for Biology and Evolution of Schistosoma mansoni

  2021cites this paper
• Versatile Effectors of Phytopathogenic Fungi Target Host Immunity.

  2021cites this paper
• Role of Functional Defence Signalling Molecules in Plant–Microbe Interactions

  2021cites this paper
• Trans-kingdom RNAs and their fates in recipient cells: advances, utilization, and perspectives

  2021influential citation
• Determinants of Host Range Specificity in Legume-Rhizobia Symbiosis

  2020cites this paper
• An aphid RNA transcript migrates systemically within plants and is a virulence factor

  2020cites this paper
• Editorial overview: Investigating phenotype evolution in the post-genomic era.

  2019cites this paper
• An aphid host-responsive RNA transcript that migrates systemically in plants promotes aphid reproduction

  2019cites this paper
• The origin and evolution of cell-intrinsic antibacterial defenses in eukaryotes.

  2019cites this paper