Packaged or unpackaged: appearance and transport of extracellular noncoding RNAs in the plant apoplast

Nasfi, Sabrine; Kogel, Karl‐Heinz

doi:10.21037/exrna-22-11

Cited by 5 publications

(6 citation statements)

References 30 publications

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“…While the exact mechanism of sRNA transport between organisms during ckRNAi is still unresolved and debated (Nasfi & Kogel 2022), sRNAs traveling from pathogen to host and functions in silencing can be identified via AGO co-immunoprecipitation (Dunker et al 2020). While this technique is applied to the question of pathogen-derived ckRNAi a sorting mechanism of sRNAs remains undescribed (Weiberg et al 2013; Wang et al 2016; Dunker et al 2020).…”

Section: Discussionmentioning

confidence: 99%

“…In 2016, Hui-Shan Guo’s group also demonstrated the transfer of plant sRNAs into an interacting fungus: cotton plants export micro (mi)RNAs into the pathogenic ascomycete fungus Verticillium dahliae , and some of these miRNAs target fungal virulence genes (Zhang et al 2016). Further work has shown that this exchange takes place via extracellular vesicles, which, in addition to other cellular components, also carry sRNAs as cargo (Cai et al 2018a; Rutter and Innes 2018; Zand Karima et al 2022; for review: Cai et al 2021; Nasfi and Kogel 2022). Proof in principle of the transfer of sRNA from the host plant to a fungus had already been provided in 2010 by the discovery of the process of host-induced gene silencing (HIGS; Nowara et al 2010).…”

Section: Introductionmentioning

confidence: 99%

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Analysis of codon usage and allele frequencies reveal the double-edged nature of cross-kingdom RNAi

Werner

Kopp‐Schneider

Kogel

2022

Preprint

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BackgroundIn recent years, a new class of small 21- to 24-nt-(s)RNAs has been discovered from microbial pathogens that interfere with their host’s gene expression during infection, reducing the host’s defence in a process called cross-kingdom RNA interference (ckRNAi). According to this model, microbial sRNAs should exert selection pressure on plants so that gene sequences that reduce complementarity to sRNAs are preferred. In this paper, we test this consequence of the ckRNA model by analyzing changes to target sequences considering codon usage and allele frequencies in the model system Arabidopsis thaliana (At) – Hyaloperonospora arabidopsidis (Ha) and Hordeum vulgare (Hv) – Fusarium graminearum (Fg). In both pathosystems, some selected sRNA and their corresponding target have been described and experimentally validated, while the lengthy methodology prevents the analysis of all discovered sRNAs. To expand the understanding of ckRNAi, we apply a new in silico approach that integrates the majority of sRNAs.ResultsWe calculated the probability (PCHS) that synonymous host plant codons in a predicted sRNA target region would show the same or stronger complementarity as actually observed and compared this probability to sets of virtual analogous sRNAs. For the sets of Ha and Fg sRNAs, there was a significant difference in codon usage in their plant gene target regions (for Ha: PCHS 24.9% lower than in the virtual sets; for Fg: PCHS 19.3% lower than in the virtual sets), but unexpectedly for both sets of microbial sRNA we found a tendency towards codons with an unexpectedly high complementarity. To distinguish between complementarity caused by balancing sRNA-gene coevolution and directional selection we estimated Wright’s F-statistic (FST), a measurement of population structure, in which positive deviations from the background indicate directional and negative deviations balancing selection at the respective loci. We found a negative correlation between PCHS and FST (p=0.03) in the At-Ha system indicating deviations from codon usage favoring complementarity are generally directionally selected.ConclusionThe directional selection of complementary codons in host plants suggests an evolutionary pressure to facilitate silencing by exogenous microbial sRNAs, which is not consistent with the anticipated biological role of pathogen sRNAs as exclusively effectors in cross-kingdom RNAi. To resolve this conflict, we propose an extended model in which microbial sRNAs are perceived by plants via RNA interference and, via coevolution, primarily help to fine-tune plant gene expression.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Analysis of codon usage and allele frequencies reveal the double-edged nature of cross-kingdom RNAi

Werner

Kopp‐Schneider

Kogel

2022

Preprint

Self Cite

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“…The experimental research discussed in the previous section suggests that the apoplastic sRNAs either get encapsulated in the EVs or tightly bound to the RNA binding proteins to avoid degradation [ 63 ]. However, the removal of EVs from the AWF does not always deplete the concentration of sRNAs, suggesting that EVs are not the primary location of these siRNAs and miRNAs [ 56 ].…”

Section: Srnas Transportation Outside the Extracellular Vesiclesmentioning

confidence: 99%

Cross-kingdom small RNA communication between plants and fungal phytopathogens-recent updates and prospects for future agriculture

2023

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Small RNAs (sRNAs) are short non-coding regulatory RNA sequences that silence the complementary expressive transcripts through an endogenous RNA mediated interference mechanism (RNAi). These sRNAs typically move through plasmodesmata and phloem in plants to support disease resistance, and also through septal pores and vesicles in fungi to act as effector of pathogenicity. Notably, recent reports have shown the occurrence of a bidirectional trafficking of these sRNAs between the host plants and the attacking fungal phytopathogen which have significant implication in the nature of the infection. While the trans-species sRNAs from the pathogen can silence the host mRNAs and inhibit the host immunity genes, the sRNA modules from the host plants can silence the mRNA in the pathogen by impeding the expression of the pathogenicity-related genes. In the present review, we discuss the current state of sRNA trafficking between the plant and the pathogen with special emphasis on the mechanism of cross-kingdom communication which could contribute to the development of pathogen and pest control in future agriculture.

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“…2022). Despite the well-established association of different types of biomolecules with plant- and microbe-derived EVs, the precise localisation of these, inside or outside of EVs, remains in many cases unresolved and a matter of an ongoing debate (Nasfi & Kogel 2022; Zand Karimi et al . 2022; Cai et al .…”

Section: Introductionmentioning

confidence: 99%

Barley powdery mildew invasion coincides with the dynamic accumulation of leaf apoplastic extracellular vesicles that are associated with host stress response proteins

Thieron,

Spanu,

Buhl

et al. 2024

Preprint

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The mutual exchange of extracellular vesicles across kingdom borders is a feature of many plant-microbe interactions. The occurrence and cargos of extracellular vesicles has been studied in several instances, but their dynamics in the course of infection have remained elusive. Here we used two different procedures, differential high-speed centrifugation and polymer-based enrichment, to collect extracellular vesicles from the apoplastic wash fluid of barley (Hordeum vulgare) leaves challenged by its fungal powdery mildew pathogen,Blumeria hordei. Both methods yielded extracellular vesicles of similar quality and morphological characteristics, though the polymer approach was associated with higher reproducibility. We noted that extracellular vesicles derived from the apoplastic wash fluid constitute polydisperse populations that are selectively responsive to leaf infection byB. hordei. Extracellular vesicles of ~100 nm - 300 nm diameter became progressively more abundant, in particular from 72 hours post inoculation onwards, resulting in a major peak late during fungal infection. Vesicles of ~300 nm - 500 nm showed similar accumulation dynamics but reached much lower levels, suggesting they might constitute a separate population. Proteome analysis uncovered an enrichment of biotic stress response proteins associated with the extracellular vesicles. The barley t-SNARE protein Ror2, the ortholog of the PEN1 marker protein of extracellular vesicles inArabidopsis thaliana, accumulates in extracellular vesicles during powdery mildew infection, hence also qualifying as a potential marker protein. Our study serves as a starting point for investigating the role of extracellular vesicles at different stages of plant-microbe interactions.

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Packaged or unpackaged: appearance and transport of extracellular noncoding RNAs in the plant apoplast

Cited by 5 publications

References 30 publications

Analysis of codon usage and allele frequencies reveal the double-edged nature of cross-kingdom RNAi

Analysis of codon usage and allele frequencies reveal the double-edged nature of cross-kingdom RNAi

Cross-kingdom small RNA communication between plants and fungal phytopathogens-recent updates and prospects for future agriculture

Barley powdery mildew invasion coincides with the dynamic accumulation of leaf apoplastic extracellular vesicles that are associated with host stress response proteins

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