Comparison of important features of common types of scnRNAs found in plants.
1. Introduction
1.1. The “zigzag model” of plant-pathogen interactions
During millions of years of co-evolution, plants have established sophisticated genetic mechanisms to protect their integrity against invading pathogens. Pathogens in turn have coped with such barriers to gain access to nutrients and proliferate inside the plant. The “zigzag model” illustrates in a simple way the different layers of innate immunity during interactions of plants with their pathogen [1]. This model describes two main immunity responses, the first one relies on plants' ability to recognize so-called microbial-associated molecular patterns (MAMPs), which are highly conserved structures and molecules in all kinds of pathogenic and nonpathogenic microorganisms. This response is known as MAMP-triggered immunity (MTI) and is efficient against non-adapted or non-host pathogens [2]. The best-studied MAMPs are the flagelline peptide, the elongation factor Tu protein (EF-Tu), chitin whis is a major component of fungal cell walls and lipopolysacharides (LPS). MAMPs perception depends on plant pathogen recognition receptors (PRRs), with FLS2 and EFR recognizing flagelline and EF-Tu, respectively. These two PRRs share a similar structural architecture formed by extracellular Leucine Rich Repeats (LRR) and a cytoplasmic kinase domain. CERK1, on the other hand, which is the Arabidopsis PRR involved in the recognition of chitine, contains three extracellular LysM domains and a cytoplasmic kinase domain. In response to MTI, pathogens developed strategies to overcome it by sending effector proteins inside plant cells. These effector proteins abolish MTI by either suppressing early recognition or interfering with down-stream signaling events [3]. A second layer of plant immunity known as effector-triggered immunity (ETI) relies on a more sophisticated mechanism to detect pathogens, based on the specific recognition of particular effector proteins by Resistance (R) proteins. In this case the effector proteins are named Avr factors. The Avr-R proteins interaction can be direct or mediated by another protein, referred to as pathogenicity target. In the later case the R protein guards the pathogenicity target and detects its modification caused by the effector protein [4]. The largest group of R proteins includes a Nucleotide Binding Site (NBS) and a LRR domain. This group can be subdivided in two subclasses based on the presence or not of a Toll-Interleukin Related (TIR) domain in the N terminus. Upon the perception of pathogen’s molecules by PRRs or R proteins, a signaling cascade including MAP kinases is activated, leading to a reprogramming in host's gene expression along with the activation of genes with antimicrobial function (PR, pathogenesis related) [2, 5]. In the last years a great effort in research has focused on understanding how gene expression is modified in response to pathogens, revealing some crucial factors for the interaction such as transcription factors, DNA regulatory elements and non-coding small RNAs.
2. An overview of beneficial interactions
Plant-microbe interactions are not always disadvantageous to plants. During millions of years of co-evolution, plants established symbiotic interactions with bacteria and fungi. The best-studied models illustrating this kind of interaction are the rhizobial and mycorrhizal symbiosis, which involve a particular group of bacteria and fungi, respectively. The establishment of symbiosis requires a concerted molecular dialogue involving the correct recognition and the activation/repression of specific signaling pathways [6]. In the rhizobial symbiosis,
However, these types of beneficial interactions are not always successful. Plants indeed tolerate the invasion of these microorganisms only under nitrogen or nutrient-deficient conditions. In consequence, a sophisticated perception mechanism should exist in plants in order to simultaneously estimate nutrient deficiency and distinguish between beneficial microbes and pathogens. To achieve symbiosis, a fine regulation of the plant immune responses is therefore required for accepting or not candidate microorganisms [6]. In the last years we have learned a lot about how non coding RNAs are a crucial players in regulating such responses as well others.
3. Non-coding small RNAs
In eukaryotes, the endogenous regulation of gene expression is mostly dependent on the control of the RNA polymerase II by accessory proteins including activators, repressors and the mediator complex. Then, small non-coding RNAs (sncRNA) were discovered and found to be new key elements of gene expression regulation [9, 10]. sncRNAs are short molecules of typically 18 to 30 nt, involved in gene expression control, defense against other parasitic nucleic acids, epigenetic modification and heterochromatin regulation.
The best-studied sncRNAs are microRNAs (miRNAs) and small interference RNAs (siRNAs). miRNAs derive from nuclear genes. A gene coding for a miRNA (
In contrast, siRNAs originate from transgenes, viruses, transposons or other RNAs that form perfectly complementary double-stranded RNA precursors (dsRNAs). In particular, virus-derived siRNAs also known as virus induced RNAs (vsiRNAs), have been extensively studied in plants. From a siRNA precursor, multiple siRNAs are generated and the silencing signal can be further amplified upon the generation of secondary siRNAs subsequently processed by RNA dependent RNA polymerases (RDRs), SILENCING DEFECTIVE3 (SDE3), NRPD1a and NRPD1b (largest subunits of Pol IVa and Pol IVb isoforms of RNA polymerase IV, respectively) [14-16].
Recently, various new types of ncRNAs have been described. Among them are the trans-acting siRNAs (ta-siRNAs) (21-22nt) which combine both the siRNA and miRNA pathways since they originate from a nuclear
siRNA | miRNA | ta-siRNA | nat-siRNAs | |
Derived from | Invasive nucleic acids (virus, transgenes) | non-coding regions | non-coding regions | antisense genes |
Transcribed by | Depends of origin | RNA pol II | RNA pol II | RNA pol II |
Processed by | DCL, RDR, SDE, NRPD | DCL1, HYL1, HEN1 | RDR6/SGS3, DCL, miRNAs | DCL1, HYL1 |
Targets transcripts in | cis | trans | trans | cis |
Binds to | AGO1, AGO2 | AGO1 | AGO1,AGO7 | AGO1? |
4. The “zigzag model” in plant-virus interactions
The seminal work achieved on plant-virus interactions studies led to the discovery of post-transcriptional gene silencing (PTGS) as a genuine plant defense mechanism against virus. Most of the plant viruses are positive single stranded RNAs (ssRNAs). To colonize and multiply into new plant cells, virus have to replicate several thousands of times. During this process of replication and infection, RNA viruses produce double-stranded RNAs (dsRNAs). A DCL protein, usually DCL4 in Arabidopsis
In line with the “zigzag model”, virus evolved strategies to overcome this first layer of immunity. As a matter of fact, viruses carry silencing suppressors (SS) are able to act at different levels of the silencing pathway [26]. Considering these suppressors as bona fide pathogen effector proteins, this scenario is reminiscent of effector-triggered susceptibility or ETS. SS proteins were previously considered as pathogenicity factors with an important function in the development of symptoms on plant hosts during infection [26]. A single SS can exert suppressor activity at different steps of the silencing pathways. One of the best-studied and more versatile SS is HC-Pro which is able to block silencing by either interfering with DCL proteins [27] and/or sequestering 21-nt siRNA duplexes [28]. The TCV P38 coat protein [29] and CMV 2b protein [30] affect the processing of dsRNA through the inactivation of DCL proteins. The P21 and P19 proteins respectively produced by the Beet yellows virus (BYV; Closterovirus, Closteroviridae) and the Tomato bushy stunt virus (TBSV, Tombusvirus, Tombusviridae), exert their function by interacting with miRNA duplexes and hairpin derived siRNAs [28, 31, 32]. Additionally, these SS interfere with the small RNAs stability by blocking the activity of the methyltransferase protein HEN1 [33, 34]. The Beet western yellows virus (BWYV; Polerovirus, Luteoviridae) P0 protein interacts via an F-box domain with AGO1 which results in its degradation, illustrating again how important components of the RNA silencing machinery are targeted in order to affect silencing [35].
To overcome virus-deployed strategies suppressing silencing, plants evolved R proteins recognizing specific viral proteins to trigger an immune response, which can be considered as a sort of effector-triggered immunity. This R-protein dependent ETI depends on the recognition of so called Avr proteins, which can virtually be encoded by any viral coding-gene. Examples of viral Avr proteins include the coat, helicase, replicase and movement proteins [36]. More than 15 anti-viral R proteins and belonging to the large class of NBS-LRRs have been characterized, including R proteins N [37], Y-1 [38] and RT4-4 [39] respectively isolated from
5. sncRNAs and viruses: new frontiers of defense
Recent studies suggest that sncRNAs are involved in global gene expression changes during plant-virus interaction. It has been proposed that the expression of plant miRNAs targeting plant transcripts is altered in response to virus recognition with the aim of affecting viral replication and spreading. Indeed various plant miRNAs are known to be up- or down-regulated following viral infection [48-52]. For example miR1885 is induced in response to infection of
It has also been suggested that miRNAs directly target viral RNAs, as it occurs in animals [57, 58]. Indeed several studies demonstrated that artificial miRNAs (amiRNAs) targeting key components of the viral replication machinery can efficiently impair viral growth upon infection [59-65]. These efforts have revealed that such resistance is cell-autonomous, inheritable, more efficient than siRNA-mediated strategies and successful in blocking viral replication and movement [59, 66]. Furthermore transgenic plants expressing dimeric or polycistronic amiRNAs directed against different viruses result in a wider spectrum of viral resistance [60, 61, 63].
The hypothesis of plant microRNAs naturally evolving to target viral genomes has long being discussed, taking in account the potential disadvantages of the miRNA pathway over the siRNA one. The miRNA pathway is not an adaptive response since the evolution of viral genomes would be fast enough to surpass the evolution of miRNAs rendering them ineffective in a very short term. However some miRNA families may be adapted to target viral genomes, as suggested by bioinformatic analysis [67, 68].
Viruses also encode miRNAs (or similar ncRNAs) directed against the plant genomes (or even their own genomes), that will use the host miRNA machinery to be processed and execute their silencing effect. This mechanism has been described only in animal infecting viruses [69]. So far, the only mechanisms found resembling viral miRNAs in plant viruses refer to sRNAs encoded by the Cauliflower mosaic virus (CaMV) that are partially complementary to regions of the Arabidopsis genome [70] and viral sRNAs that bind the RNAi machinery to divert the silencing machinery from viral promoter and coding regions [71].
A general model of the way sncRNAs mediate the interaction between plants and viruses (as well as with bacteria discussed below) can be seen in Figure 1.
6. The need for auxin: responses to bacteria, fungi and symbiotic microbes
Auxin is a relatively well-known plant hormone mainly implicated in growth which acts, under particular conditions, as a repressor of salicylic acid (SA). SA is a hormone involved in the activation of plant defenses in response to biotrophic pathogens [72, 73]. It is therefore not surprising that plants, in response to microbes, have evolved sophisticated mechanism for fine-tuning of SA-mediated responses.
The best-studied miRNA induced upon bacterial infection is miR393. By comparing the gene expression profile of wild type and transgenic plants expressing several viral SS, it was elegantly demonstrated that upon treatment with flagellin (flg22), some transcripts were more abundant in transgenic plants. Among them was found a transcript coding for the F-box auxin receptor TIR1. By RACE (rapid amplification of cDNA ends) the authors demonstrated that this particular mRNA is targeted and cleaved by miR393. The perception of flagellin by plants induced the expression of miR393 which correlates with a clear reduction of the TIR1 protein content. This led in turn to the stabilization of Aux/IAA proteins which repress auxin signaling by heterodimerization with Auxin Response Factors (ARF). Flagellin perception leads to a repression of auxin signaling and consequently restricted the growth
miR393 was shown to be induced in Arabidopsis plants inoculated with
The complex interplay between auxin and miRNAs goes beyond miR393. Several reports have shown that different ARFs and auxin receptors coding genes are regulated by other miRNAs such as miR160, miR166 and miR167, not only in response to phytopathogenic bacteria and fungi but also during beneficial interactions involving
miR393 is highly conserved and was also detected in cassava plants challenged with
During the symbiosis occurring between soybean and
7. MTI and silencing: beyond miR393 and auxin
Fahlgreen
A first connection between miRNAs-mediated silencing and MTI emerged from the study of Arabidopsis AGO1 mutant lines, found to be compromised in MTI [78]. These plants are characterized by a reduction in seedling growth inhibition, callose deposition, expression of MTI-markers genes and the activation of MAP kinases and ROS production upon treatment with flagellin. Also, the growth of TTSS-mutant strains was increased in these plants. These results demonstrate that AGO1, and indirectly the silencing pathway, are key elements of MTI. These phenotypes are not observed in AGO7 mutant plants, indicating that only AGO1 activity is associated with MTI. Interestingly, the involvement of miRNAs in regulating plant immunity is not restricted to MTI. It may also be associated to ETI, as exemplified by cases of plant resistance responses against fungal pathogens, where several components of the silencing machinery were showed to play a role [88]. More precisely, Arabidopsis
8. Towards ETS
Accordingly to the “zigzag model”, adapted pathogens overcome MTI to infect particular host plants. Based on the study of Arabidopsis mutants affected in genes involved in the silencing pathway like
9. The arms race goes on: miRNA's role in ETI
As mentioned previously, the specific recognition of effectors by R proteins triggers ETI, which involves gene expression reprogramming. In a survey aimed at determining the role of siRNAs in gene expression during R-protein-mediated responses it was found that a 22 nt nat-siRNA was induced specifically by
10. R genes, my favorite targets: miRNAs
Since the expression of
Some reports have indeed demonstrated a direct regulation of
Another example of regulation of
During the infection of pine with the fusiform rust fungus
R proteins play a pivotal role in triggering immune responses and should be able to recognize a broad spectrum of effector proteins (Jones and Dangl, 2006). The high repertory of plant immunity genes raises the question as to the control of their activity. Not surprisingly, several mechanisms were reported explaining the regulation of the expression and activity of this important type of genes. Because of the constitutive nature of many resistance genes expression, fitness costs translating into reduction of growth and productivity are significant. The regulation of
On the other hand, to achieve successful colonization, symbiotic microbes must be able to block plant immune responses triggered by non-self recognition. An expected strategy would be trough the control of plant immunity master regulators, such as
Besides disease resistance-related genes, other genes involved in defense pathways signaling are regulated by miRNAs. In the above-mentioned study of
In conclusion it appears obvious that a successful symbiosis requires suppression of host defenses. Altogether these reports stress that
11. Novel and specific miRNAs in beneficial interactions
sRNA studies for beneficial interactions have focused mainly on the study of legumes, and had benefited from the identification of sRNA loci in model legumes as
miRNA expression was studied in soybean mutants nod49 (mutant for a Nod factor receptor
As stated before, rhizobacteria and AM share several elements of their symbiosis pathway [6] and miRNAs-mediated regulation is not an exception. miR169 which targets the CCAAT-binding transcription factor MtHAP2-1, was identified in the symbiotic interaction occuring between
12. Conclusions and perspectives
Research in sncRNAs is ultimately one of the most active and promising fields in plant biology, and it is expected to grow even more in importance in the near future, however many aspects of sncRNAs functions during plant-microbe interactions still remain unclear. How are these sncRNAs regulated? Are there common regulatory and feedback regulatory circuits between the different classes of sncRNAs? Are there core sncRNAs and targets for different class of pathogens and for different plant species? What is the evolutionary history of these different families of sncRNAs and how did they shape plant evolution? How did differences in sncRNA regulation across the plant kingdom arise? How are new sncRNA-specificities generated and how variable can these molecules be within species or populations? Studies reviewed here highlight the importance of sncRNAs in gene regulation in response of plants to pathogens as diverse as viruses, bacteria and fungi. Some sncRNAs have been shown to be induced or repressed in response to these diverse pathogens during incompatible and compatible interactions indicating a dual role of these RNAs as positive and negative regulators of plant immunity. This fact demonstrates the complex network of gene expression during plant-microbe interactions and should be considered in biotechnological programs focused to enhance the crop resistance to plant diseases. The notable repression of
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