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Volná, A.;  Bartas, M.;  Pečinka, P.;  Špunda, V.;  Červeň, J. miRNAs in Barley Physiology and Stress Responses. Encyclopedia. Available online: https://encyclopedia.pub/entry/37693 (accessed on 15 June 2024).
Volná A,  Bartas M,  Pečinka P,  Špunda V,  Červeň J. miRNAs in Barley Physiology and Stress Responses. Encyclopedia. Available at: https://encyclopedia.pub/entry/37693. Accessed June 15, 2024.
Volná, Adriana, Martin Bartas, Petr Pečinka, Vladimír Špunda, Jiří Červeň. "miRNAs in Barley Physiology and Stress Responses" Encyclopedia, https://encyclopedia.pub/entry/37693 (accessed June 15, 2024).
Volná, A.,  Bartas, M.,  Pečinka, P.,  Špunda, V., & Červeň, J. (2022, December 01). miRNAs in Barley Physiology and Stress Responses. In Encyclopedia. https://encyclopedia.pub/entry/37693
Volná, Adriana, et al. "miRNAs in Barley Physiology and Stress Responses." Encyclopedia. Web. 01 December, 2022.
miRNAs in Barley Physiology and Stress Responses
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MicroRNAs (miRNAs) are important players in post-transcriptional gene expression regulation in multicellular species. miRNAs can modify/decrease the expression of fully or partially complementary mRNA molecules. Plant miRNAs are powerful regulators of gene expression at the post-transcriptional level, which was repeatedly proved in several model plant species. miRNAs are considered to be key regulators of many developmental, homeostatic, and immune processes in plants. 

miRNAs plants gene barley

1. Plant miRNAs

Mature plant miRNAs are 19–25-nucleotide-long ribonucleic acids that can have either intergenic (miRNA gene is localized between two protein-coding sequences of the DNA) or intragenic origin [1], where miRNAs are cleaved from the mRNA sequences during the splicing (also called intron-derived miRNAs [2]). Specifically, in barley, more than 75% of miRNAs are transcribed from intergenic loci [3]. The biogenesis of miRNAs is ensured by the DNA-dependent RNA polymerase II which is responsible for the biosynthesis itself [4]. In some cases, multiple plant miRNAs are synthesized all at once (multiple miRNAs localized in one long transcript) [5] and often form a miRNA family, which is a group of miRNAs derived from a common ancestor [6]. Emerging miRNAs can be modified co-transcriptionally, or post-transcriptionally. Similar to other transcripts, a 7-methylguanosine (m7G) cap is attached to the 5′ end of the miRNA, and the 3′ end is polyadenylated (or can be spliced) [7]. Later, the transcript encoding miRNA (or multiple miRNAs) is folded to the stem-loop structure which is called pri-miRNA [4] (meaning primary miRNA transcript). Such pri-miRNAs are further cleaved by the dicing bodies. Dicing bodies consists of several proteins including DICER-LIKE 1 (DCL1), DAWDLE (DDL), HYL1, TGH, and SE [8][9], resulting in miRNA duplex formation which can be later 2′-O-methylated by the HEN1 methylase [10] and incorporated into the RNA-induced silencing complex (RISC) [4][11]. The complex issue of further proteins involved in plant miRNA biogenesis is reviewed in Li et al., 2021 [12]. miRNAs of both origins (intragenic as well as intergenic) lead to the formation of a mature RISC with incorporated mature miRNA. In most cases, only the sense/guide miRNA strand is incorporated into the RISC, while the antisense/passenger miRNA (miRNA*) strand is disrupted, but recently also the regulation potential of the passenger miRNA became the center of interest [13][14][15]. For a clear summary of miRNA biogenesis see Figure 1 below.
Figure 1. Schematic representation of the miRNAs biogenesis. Genes encoding miRNAs are transcribed by RNA polymerase II and modified on their ends (m7G cap and polyA tail) and thus the primary microRNA (pri-miRNA) arise. Then, the typical stem-loop structure is formed by complementary base pairing and cleaved at the dicing bodies (consisting of several proteins including DCL1, HYL1, SE, TIGH, and DDL) resulting in miRNA duplex formation which can be later 2′-O-methylated (ensured by the HEN1 protein). Guide miRNA is incorporated into the RISC consisting of several proteins, and transported into the cytoplasm, where mRNA target recognition and cleavage can take place while the passenger miRNA is released away. Proteins from the Argonaute family (AGOs) can modify the stability of the miRNAs and also affect the interaction with target mRNAs. This figure was created using BioRender (https://biorender.com/; accessed on 20 June 2022).
miRNAs interact with their target mRNAs mostly at their 3′ UTRs, but interactions occurring in the 5′ UTRs or coding regions were documented as well [16][17]. RISC is directed to the complementary mRNA transcript, whereby the Watson–Crick base-pairing aligns guide miRNA and target mRNA transcript, and depending on the central miRNA region complementarity, mRNA is cleaved (usually when there is perfect base-pair complementarity), or translation repression occurs (central miRNA region is not completely complementary to mRNA) [18]. Moreover, in the case the target mRNA is cleaved, so-called phased secondary small interfering RNAs (phasiRNAs) can arise [19]. phasiRNAs are 21 or 24-nucleotide-long siRNAs having important roles in plant stress responses [19], development [20], and reproduction [21].
Similar to the other genes, miRNA transcription is precisely fine-tuned. This is assured mainly by transcription factors binding [22] and methylation status of DNA [23], both heavily influenced by endogenous and exogenous stimuli. In 2018, protein WHIRLY1 was found to be involved in increased levels of nuclear miRNAs in high-light conditions in barley. It was therefore proposed that WHIRLY1 can bind to RNA and it might be a general factor influencing the biogenesis and/or stability of various miRNAs [24].
An additional level of miRNA complexity is their dynamic stability [9][25]. It was documented that the processes such as 3′-end modifications and interaction with Argonaute proteins (AGOs) can both reduce and increase the stability of miRNAs depending on the actual needs of the plant. For example, AGO1 from Arabidopsis thaliana was proposed to stabilize miRNAs, and miRNA–mRNA target interaction [4].
Besides post-transcriptional gene silencing (PTGS), miRNAs can regulate plant genes via RNA-induced methylation of DNA [26][27]. Such a process was in detail described in the Arabidopsis thaliana, where miRNAs (miR165, miR166) regulate the methylation status of PHB and PHV genes [28], and are responsible for the determination of the abaxial and adaxial leaf side. Similarly, the miRNA-induced gene methylation was described even in the Oryza sativa where the miR1873 ensures the methylation of its own gene [27]. To make understanding of miRNAs-based regulation of gene expression more challenging, the stimulative effect of miRNAs on gene expression was observed and documented as well [29].
Last but not least, in 2015 it was proposed that plant pri-miRNAs are capable of encoding small functional peptides [30][31] described as miPEPs. The best-characterized miPEPs (miPEP171d, miPEP172c, and miPEP858a) were found in plant species including Arabidopsis thaliana (miPEP165a [30], miPEP858 [32]), Medicago truncatula (miPEP171b [18]), Glycine max (miPEP172c [33]), and Vitis vinifera (miPEP171d1 [34]). The mechanism of miPEPs molecular function is still largely unclear, but generally, miPEPs positively affect the accumulation of their associated miRNAs [31]. It is also likely that many of miPEPs will be species-specific [34].

2. miRNAs in Barley Physiology and Stress Responses

miRNAs in plants are important regulators of various physiological processes including shoot apical meristem development [35], leaf growth [36], flower formation [37], seed production [38], and root expansion [36]. It was found that miRNA171 in barley is responsible for the regulation of shoot meristem development through three independent pathways, i.e., firstly through the down-regulation of SCARECROW-LIKE (SCL) transcription factors, secondly via up-regulation of miRNA156 and repressing vegetative phase transitions (a possibly monocotyledon-specific mechanism), and thirdly by repressing expression of TRD and HvPLA1 genes [39]. Additionally, flower development in grasses including barley is tightly regulated by miRNAs. It was found that miRNA159, miRNA171, miRNA172, and miRNA396 regulate the expression of floral organ identity genes in barley, rice, and maize [40]. In barley, cleistogamous flowering (i.e., shedding its pollen before opening) arises from the suppression of the AP2 transcription factor via miR172, originally thought to be a result of target mRNA cleavage [41], but later it was proved that miR172-mediated AP2 regulation occurs at the translational level [42]. It is also known that the expression of barley miR393 is active in the developmental period, and its misexpression affects seedling growth and stomatal density [43]. In 2018, it was found that miR160 in barley simultaneously targets class II ARF members which are functionally involved in developmental stages by regulating the auxin-mediated genes [44]. Figure 2 illustratively depicts some of the most known barley miRNAs (and their targets) that play important roles in developmental processes.
Figure 2. miRNAs play important roles also in the developmental processes. In spring barley (Hordeum vulgare), specific miRNAs were linked with the targets involved in the regulation of flowering, root development, seed germination, and also with stomata development. Inhibition is indicated by the red ┴ mark, while positive effect by the green arrow. This figure was created using BioRender (https://biorender.com/; accessed on 20 June 2022).
Besides the non-stress conditions, miRNAs play key roles in gene expression regulation in response to a variety of abiotic stimuli, including several stress responses. In plants, their involvement in many abiotic stress responses including heat stress responses, low-temperature responses, drought exposure responses, carbon dioxide responses, light stress responses, or gamma radiation responses was reported [45][46][47][48][49]. Specifically in barley, miRNAs responsive to salinity stress [50][51][52][53], drought [54][55][56][57][58], nitrogen [59], boron [60], phosphorus [61][62], aluminum [51][63][64], cadmium [65], cold deacclimation [66], heat stress [67], and possibly to light [68] were identified till date. A chronological summary of the most impactful miRNA studies in barley (starting from 2010) can be found below in Table 1.
From the above-mentioned studies, it is evident that barley miRNAs play a complex role in responses to various abiotic and biotic stresses or stimuli, which is schematically depicted in Figure 3.
Figure 3. miRNAs form a complex regulatory network in barley (Hordeum vulgare). Environmental cues, both abiotic (i.e., spectral quality and intensity of the incident light, growth temperature, drought, high salinity, heavy metals exposure, etc.) and biotic (for example pathogens) can affect the expression of miRNAs and thus also their target genes. This figure was created using BioRender (https://biorender.com/; accessed on 20 June 2022).

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