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The Role of MicroRNA in Plant Response to Abiotic Stress

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24 May 2023

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26 May 2023

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Abstract
MicroRNAs (MiRNAs) are a class of non-coding single-stranded RNA molecules of approximately 20-24 nucleotides in plants that play an important regulatory role in a variety of biological processes such as plant growth and development and response to various abiotic stresses. For example Drought, Salt, Cold, High temperature, Heavy metals and Nutrition. MiRNAs affect gene expression by manipulating the cleavage, translational expression or DNA methylation of target mRNAs. This review describes the current progress made on the way miRNAs are produced and regulated and the way miRNA/target gene is used in plant responses to abiotic stresses. Studying the molecular mechanism of action of miRNAs downstream target genes can optimize the genetic manipulation of crop growth and development conditions that provide a more theoretical basis for improving crop production.
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Subject: Biology and Life Sciences  -   Biochemistry and Molecular Biology

1. Introduction

MicroRNAs, a class of plant non-coding single-stranded RNA molecules of approximately 20-24 nucleotides in length encoded by endogenous genes, have a variety of important regulatory roles in cells, participating in the regulation of plant growth and development, stress responses and hormone signalling through the negative regulation of plant gene expression, and post-transcriptional regulation of gene expression in plants [1]. microRNAs can complementarily bind to the 3’UTR region of the target mRNA, thus achieving negative regulation of gene expression. Several miRNAs can also regulate the same gene and be regulated by a combination of several miRNAs. It has been shown that miRNAs are not only conserved in gene location, but also exhibit a high degree of sequence homology, that most mammalian miRNAs are located in transcriptionunits (TUs), and most of them are located in intronic regions [2,3,4]. The high degree of conservation is strongly related to its functional importance, potentially demonstrating that homologous miRNAs serve similar functions across different species. The purpose of this review is to provide a deeper understanding of molecular mechanisms of miRNA involvement in response to abiotic stresses, For example Drought, Salt, Cold, High temperature, Heavy metals and Nutrition. Since the first discovery of microRNAs in animals in 1993, more and more researchers have become interested in this non-coding RNA [3]. Furthermore, the aim of this paper is to provide a functional perspective on the role of miRNAs in plant adaptation to agronomic abiotic stress conditions, as well as to provide a theoretical basis for miRNA improving plant resistance in abiotic stress with a view to increasing crop yields.

2. Production and Mechanism of miRNAs

2.1. Production of miRNAs

Gene transcription processing: RNA polymerase II in most cases and RNA polymerase III in a few cases transcribe from genomic sequences to form the precursor pri-miRNA. pri-miRNA is very long, ranging from a few hundred to several thousand nucleotides. pri-miRNA maintains its non-activated state by cap structure and polyadenylation and coiling of the spatial structure. Intranuclear processing: pri-miRNA is edited by the adenylate deaminase of RNA and forms pre-miRNA hairpin sequences after being sheared by the microprocessor formed by the enzyme.
Nuclear export processing: The nucleoplasmic transporter protein recognizes the two nucleotides protruding from the 3′ ends of the pre-miRNA hairpin sequence and transports the pre-miRNA from the nucleus to the cytoplasm. Nucleus processing: The nuclease Dicer begins to shear the stem-loop structure in the hairpin sequence, after which it is able to produce miRNA double strands. Pre-miRNA precursors are processed into miRNA/miRNA double-stranded bodies via the DICER-LIKE 1 (DCL1) protein, nucleocapsid binding complex (CBC), mushroom (DDL) and sawtooth (SE), then the double-stranded body is translocated into the cytoplasm.The pre-miRNA is then processed into a mature double-stranded miRNA/miRNA complex with the help of the HUA ENHANCER 1 (HEN1) protein helper complex. When the mature miRNA is embedded in an RNA-induced silencing complex, the antisense miRNA is degraded in the cytoplasm. The RNA-induced silencing complex (RISC), known as the miRNA-ribonucleoprotein complex (miRNP), contains mature miRNAs and proteins. The ribonucleoprotein complex miRNP interacts with target mRNAs through its cognate mature miRNAs, negatively regulates the expression of target genes at the post-transcriptional level, leading to mRNA degradation or translational repression under specific mechanisms of action [5,6,7](Figure 1).

2.2. Mechanism of miRNAs

Since most plant miRNAs are derived from the reverse copy of the target gene, the bases of the miRNA are complementary to those of the target mRNA. after the plant miRNA recognizes and binds to the target mRNA, the AGO will shear the target mRNA at the 10th and 11th nucleotides of the miRNA binding site. the AGO is the protein for the miRNA to carry out its function, miRNAs must bind to AGO to function. Since most plant miRNAs are derived from the reverse replication of target genes, the bases of miRNAs are complementary to those of target mRNAs, and when plant miRNAs bind to target mRNAs, the AGO will shear the target mRNA of the miRNA binding site [8,9]. Ten AGOs have been identified in Arabidopsis, which AGO1 has four structural domains, PAZ, Mid, PIWI and the N-terminal domain, respectively. The PIWI domain has nucleic acid endonuclease activity and functions as a shear for its target mRNA. Complete base complementarity between bases near the miRNA shear site and the target mRNA is important for AGO shear [8] (Figure 2A).
Another mechanism of plant miRNAs is through translational repression. The miRNA does not bind to the 3′ UTR region of the target mRNA in its entirety and the RNA-induced silencing complex inhibits the initiation of translation or the specific degradation of the synthetic ribosome to achieve translation inhibition. Aukerman found that overexpression of miR172 did not reduce the expression abundance of target mRNAs, but the corresponding levels of proteins encoded by target mRNAs were significantly reduced [10]. they therefore proposed for the first time that plant miRNAs could also repress translation of target genes. Subsequently, several studies have shown that translational repression of target genes by plant miRNAs is also a common phenomenon, and even the same miRNA may regulate target genes in both a shearing and translational repression manner. This is one of the reasons why plant miRNAs are not fully complementary to the expression of their target genes [11,12] (Figure 2B). In plants, miRNAs are an important modality for mRNA regulation through translational repression.

3. For miRNA and Drought Stress

Water is a vital resource for the survival of all life and has played an important role in the evolution of life. The most abundant substance in plant cells is water, which is an essential component of the plant body. With sufficient water, the stalks and branches of plants can stand up and stretch in the air, and the flowers can bloom better and facilitate the completion of pollination. Water is also one of the raw materials for photosynthesis in green plants and if there is a lack of water, the plant’s photosynthesis will be weakened. Leaves will wilt and in severe cases can lead to the death of the plant [13,14,15]. MiRNA156 was one of the first miRNAs identified in plants, and numerous studies have linked miRNA156 to drought stress. anthocyanins act as a secondary metabolite by scavenging ROS to protect plants from stress. In Arabidopsis, rice, alfalfa and poplar, miR156/SPL is present in Arabidopsis, rice, alfalfa and poplar by regulating anthocyanin accumulation levels in response to plant drought stress. mechanism in response to plant drought stress by regulating the level of anthocyanin accumulation [16,17]. López-Galiano et al. showed that drought conditions lead to down-regulation of miRNA159 and up-regulation of its target gene transcription factor MYB33 in tomato [18]. Reyeset al showed that during Arabidopsis seed germination, ABA induces the accumulation of microRNA 159 (miR159) in an ABI3-dependent manner, and miRNA159 mediates the cleavage of MYB101 and MYB33 transcripts in vitro and in vivo [19]. Zhang et al. showed that fine localization and functional analysis identified the candidate gene ZmLRT of qLRT5-1 as expressing the major transcript of microRNA miR166a, and that knockdown of ZmLRT enhanced drought tolerance in maize seedlings [20].
Stomata play a central role in the exchange of gases between plants and their environment, and their opening and closing is influenced by environmental signals, as well as being regulated by endogenous hormones, which in turn affect the plant’s response and tolerance to drought stress. ABA is the most critical hormone in drought stress, it regulating water loss, stomatal opening and closing [21,22,23,24]. MiR393 positively regulated stomatal density and negatively regulated guard cell length, while overexpressing plants had the opposite phenotype to the deletion mutant, possibly due to miR393 regulating the expression of growth hormone response factor 5 (ARF5) and three stomatal development-related genes, epidermal pattern factor 1 (EPF1), SPEECHLESS (SPCH) and MUTE. The miR393 overexpression strain was more sensitive to drought treatment, accumulating more malondialdehyde (MDA) and hydrogen peroxide (H2O2) compared to the wild type, and also inhibiting the accumulation of ABA in leaves. These results also demonstrate that miR393 responds to plant drought stress by interacting with ABA and regulating stomatal density [25]. Zhao et al. showed that plants overexpressing miR393a exhibited enhanced drought stress tolerance associated with stomatal density and epidermal densification. MiR393 regulates the expression of Auxin signalling F-BOX 2 (AsAFB2) and TRANSPORTINHIBITOR RESPONSE 1 (AsTIR1) [26]. To adapt to drought stress plants require a hormone monocrotaline lactone, and exogenous monocrotaline lactone applied to tomato induces the accumulation of miR156. miR156-OE and monocrotaline lactone treatments both result in reduced stomatal conductance and increased ABA sensitivity in plants [27]. MiR398c was able to negatively regulate drought resistance in soybean. Overexpression of miR398c in Arabidopsis reduced the expression of GmCSD1a/b, GmCSD2a/b/c and GmCCS, impaired the ability to scavenge active oxygen, and increased relative electrolyte leakage and stomatal opening. This resulted in reduced germination, increased water loss from leaves, reduced survival under water deficit and demonstrated sensitivity to drought during seed germination and seedling growth [28].
Plants can also improve their drought stress tolerance by altering root conformation and adjusting leaf size and curl to reduce water evaporation. Hang et al. showed that the increased drought tolerance in OsmiR408 transgenic plants may be due to changes in leaf morphology that facilitate the maintenance of water status, as well as increased antioxidant capacity to protect against damage from reactive oxygen specie (ROS) under stress [29]. Wang et al. showed that miR9674a showed progressive up-regulation in response to drought stress treatment. Overexpressing miR9674a lines exhibited different growth characteristics under drought and salt treatment in tobacco, with significant improvements in plant biomass, leaf area and root length, while its knockout expression line showed significant alleviation in the above growth traits compared to the wild type [30].

4. For miRNA and Salt Stress

Soil salinity affects around 6% of the world’s land and 23% of arable land, causing considerable economic losses through crop stress and reduced yields. Because salinity plays a vital role in plant growth, above a certain limit, excess soluble salts will have a toxic effect on plants, affecting the levels of a wide range of endogenous plant signalling molecules such as ABA, ethylene, gibberellin (GA), ROS, and Nitric oxide (NO), These hormones can greatly affect the growth and development of plants, ultimately resulting in reduced yields [31,32]. In recent years, a number of miRNAs have been identified through miRNA studies in response to salt stress. The increased abundance of miR399 under salt stress, and therefore the altered expression of PHO2 target genes, resulted in significant changes in the expression levels of two PO4 transporter genes, PHOSPHATE TRANSPORTER1;4 (PHT1;4) and PHT1;9. In salt-stressed Arabidopsis would enhance PO4 transport from roots to shoot tissues, and these aerial tissues could use these resources to maintain essential biological processes or to generate adaptive responses to salt stress [33]. The mRNA for PpDCL1a encodes an essential Dicer protein for microRNA (miRNA) biogenesis and contains an intron miRNA (miR1047). Precise deletion of the intron containing MIR1047 to abrogate PpDCL1a autoregulatory feedback control revealed a hypersensitive response to salt stress and an insensitive response to the phytohormone ABA, and the physiological importance of feedback control of miR1047 on the abundance of PpDCL1a transcripts, which controls miRNA expression and its homologous target RNAs during salt stress adaptation[34]. Overexpression of sly-miR398b inhibited plant growth under salinity conditions in tomato, including less above-ground and root biomass and shorter plant height. Further analysis showed that overexpression of sly-miR398b down-regulated the expression of Cu/Zn superoxide dismutase (CSD) [35]. Liu et al. identified that two contrasting F. velutina cuttings clones, salt-tolerant (R7) and salt-sensitive (S4), and found to exhibit higher salt tolerance in R7 than in S4. In R7 leaves, miR164d, miR171b/c, miR396a and miR160g targeting NAC1, SCL22, GRF1 and ARF18, respectively, were involved in salt tolerance. In R7 roots, miR396a, miR156a/b, miR8175, miR319a/d and miR393a targeting TGA2.3, SBP14, GR-RBP, TCP2/4 and TIR1, respectively. That were involved in salt stress response [36]. Yuan et al. found that Osa-miR396c transgenic plants exhibited reduced biomass, shorter internodes, reduced leaf area and reduced leaf size compared with wild-type, while The transgenic plants showed increased water retention under high salt stress [37].

5. For miRNA and Temperature Stress

5.1. For miRNA and Cold Stress

Temperature is the main environmental factor affecting plant growth and development and the quality of life of the fruit after harvest. Low temperature can inhibit plant growth and is a very important abiotic stressor. A variety of miRNAs can be involved in the low temperature stress response of plants by affecting the IAA or ABA signalling pathway [38]. Wang et al. found that miR319 has been shown to target the TEOSINTE BRANCHED/CYCLOIDEA/PCF (TCP) transcription factors, which are involved in regulating multiple processes in plant growth and development by controlling cell proliferation. miR319 expression is down-regulated by low temperature induction, while its target genes, OsPCF6 and OsTCP21 are reversed. Osa-miRNA319 overexpression enhanced tolerance to low temperature stress [39]. Overexpression of miRNA156 resulted in increased cell viability and growth rate under cold stress in Arabidopsis, pine and rice. OsmiR156 increased plant cold tolerance by targeting OsSPL3, which positively regulates the expression of OsWRKY71, a negative regulator of the transcription factors OsMYB2 and OsMYB3R-2 [40]. Dong et al. found that SlNAM3 enhances cold tolerance and Sl-miR164a/b-5p plays a negative role in cold tolerance by repressing the expression upstream of SlNAM3. miR164a-NAM3 module induces ethylene synthesis by directly regulating the expression of SlACS1A, SlACS1B, SlACO1 and SlACO4, thereby conferring cold tolerance in tomato [41]. The APETALA2/ethylene response factor (ERF) transcription factor OsERF096 was identified as a target of miR1320, which negatively regulates cold stress tolerance. Overexpression miR1320 leads to increased cold tolerance, while miR1320 knockdown lines decreases cold tolerance. The MiR1320-OsERF096 module regulates cold tolerance by inhibiting the JA-mediated cold signalling pathway [42].

5.2. For miRNA and High Temperature Stress

The response of plants to temperature stress is a complex process involving a variety of metabolic and biochemical processes. Not only low temperatures affect plant growth and development, but also high temperatures negatively affect processes such as growth, development and reproduction [43,44,45,46,47,48]. Wang et al. found that SRL10, a double-stranded RNA-binding protein, regulates leaf morphology and heat tolerance in rice by altering microRNA biogenesis. The srl10 mutant has a semi-curled leaf phenotype and increased heat sensitivity. SRL10 interacts directly with catalase isozyme B (CATB) to enhance hydrogen peroxide (H2O2) scavenging, thereby promoting heat tolerance [49]. Li et al. found that Overexpression of cucumber miR9748 in Arabidopsis thaliana increased high temperature tolerance. Transcriptome analysis suggests that miR9748 may mediate high temperature tolerance through the phytohormone signalling pathway. The target gene of miR9748 is CsNPF4.4, which negatively regulates high temperature stress tolerance by repressing the JA signalling pathway [50]. Ahmed et al. found that Novel and conserved heat responsive miRNAs were identified in Chinese cabbage using a high-throughput sequencing approach using heat stress treatment at 38°C . This analysis identified 41 conserved miRNAs from 19 families, with miRNA156, miRNA159, miRNA168, miRNA171 and miRNA1885 having the most abundant molecules [51].

6. For miRNA and Heavy Metals Stress

The excessive accumulation of heavy metals in plants can poison plants, affect their growth and productivity, affect humans and animals through enrichment in the food chain, cause disease and induce cell damage. Metal elements include essential and non-essential elements. Essential metals are required for many physiological processes in living organisms, such as zinc, manganese and copper, non-essential metals are cadmium, lead or mercury [52,53,54,55,56,57,58,59,60,61,62]. Zhang et al. found that overexpressing miR156 accumulated significantly less Cd in their branches and showed enhanced tolerance to Cd stress in plants. The reason for this is that miR156 positively regulates Cd stress tolerance by regulating ROS levels and Cd uptake/transport gene expression [63]. Plants overexpressing miR408 showed severe susceptibility to low sulphur (LS), arsenite As(III) and LS+As(III) stresses due to altered and miR408 knockout mutants showed tolerance that regulated expression of genes involved in the sulphur reduction pathway and affecting the accumulation of sulphate and glutathione [64]. Nie et al. found miRNA167a, novel_miRNA15, novel_miRNA22 and their targets may be involved in Cr transport and chelation. In addition, miRNA156a, miRNA164, miRNA396d and novel_miRNA155 were identified as being involved in the detoxification of plant Cr [65]. Zhou et al. by comparing miRNAs and transcriptome analysis, a total of three known and 19 new differentially expressed microRNAs (DEMs) and 1561 differentially expressed genes (DEGs) were identified following Cd treatment, mainly because miRNAs play an important role in Cd-stressed wheat by regulating targets such as TaHMA2;1 [66]. Overexpression of miR393 abolished the inhibition of root elongation by aluminium ions. In addition, overexpression miR393 attenuated the effect of exogenous growth hormone on aluminium-induced root growth inhibition and down-regulated the expression of growth hormone-responsive genes under aluminium stress [67].

7. For miRNA and Nutrient Stress

The nutrients of plants include nitrogen, phosphorus and potassium, which play a very important role in the growth and development of plants [68,69,70,71]. Nitrogen is a major component of many important compounds in plants, participating in a range of biochemical reactions and playing an important role in crop biomass accumulation and yield enhancement [72]. Phosphorus is involved in photosynthesis, respiration, energy storage and transfer, cell division, cell enlargement and a number of other processes in the plant [73]. Potassium is involved in osmoregulation, material transport and other processes, and can improve plant stress tolerance [74]. It has been found in studies that nutrient deficiencies in plants cause plants to exhibit reduced dry weight of tissues in the above and below ground parts, reduced root length, root surface area, root volume, root vigour and reduced root respiration. Therefore, a deficiency of elements will greatly affect plant growth and in severe cases cause plant death [75].
Nitrogen stress: In past studies miRNA functions were identified in response to nitrate and N deficiency. MiR167 is able to limit root growth, mainly because it controls the response of adventitious plants to N and even controls N metabolizing enzymes produced downstream of nitrification and uptake, thereby affecting plant growth through N [76]. miR393 is activated by N signalling transmitted during nitrification and uptake. Nitrate had no effect on primary root development in overexpressing miR393 plants or afb3-1 mutants, but it controlled horizontal root development in response to nitrate treatment [77,78].
Phosphorus stress: In past studies miRNA functions were identified in response to phosphorus. MiR399 is an important component of the phosphorus starvation signalling pathway. The function of miR399 in phosphorus starvation signalling was first elucidated in Arabidopsis. miR399 expression was increased under phosphorus starvation conditions, increasing the uptake and translocation of inorganic phosphorus by plants in response to phosphorus deficiency [79]. Hu et al. showed that up-regulation of genes in response to phosphorus starvation, many genes involved in iron, potassium, sodium and calcium uptake were also significantly up-regulated in overexpression miR399 strains, with increased concentrations of iron, potassium, sodium and calcium. In addition, function of Ospho2 mutant also resulted in increased concentrations of these nutrients as well as upregulation of related genes. This demonstrates that miRNA399 influences plant responses to nutrient stress by regulating PHO2 expression [80].
Potassium stress: In past studies miRNA functions were identified in response to potassium. Researchers have demonstrated that miRNA expression in cotton and wheat is altered by low dietary potassium utilisation. K deficiency treatment resulted in altered expression of 16 of the 20 miRNAs. As a response to K deficiency, wheat increases root growth and nutrient uptake through molecular mechanisms. In peanut plants, root development is influenced by miRNAs, which play a key role in K deficiency conditions. miR156 and miR390, together with miR160, miR164 and miR393, are proposed to be up-regulated in response to potassium deficiency [81,82]. Under low K stress in barley, many miRNAs appear to be differentially expressed including Hvu-miR160a, Hvu-miR169h and Hvu-miR396c. Due to the induction of Hvu-miR319 under low K, it is able to repress the expression of growth response factor (HvGRF) and thus promote Hvu-miR396 transcription in barley [83]. The dormancy-associated MADS-box (OsMADS23) target gene is significantly up-regulated in response to potassium deficiency, while Osa-miR444a clearly regulates N and P accumulation [84].
Except nitrogen, phosphorus and potassium, there are other elements in plants that play a very important role in plant growth, such as magnesium (Mg), Iron (Fe), sulfate (S), manganese (Mn), copperand (Cu), and boron (B). Mg is one of the main components of chlorophyll and promotes the activation of phosphatase and glucose convertase, facilitating the conversion of monosaccharides. Fe is an essential element for chlorophyll formation and is directly or indirectly involved in the formation of chloroplast proteins. S is protein, amino acid, vitamin and enzyme component. Promotes redox, growth regulation and is involved in chlorophyll formation and sugar metabolism. Cu is a core element in the activation groups of various oxidative enzymes in the crop and plays an important role in catalysing redox reactions in the crop. Mn is an activator of enzymes and a component of chloroplasts. B is involved in water, sugar and nitrogen metabolism and cell membrane pectin formation, it is involved in promoting the differentiation of meristematic tissues, the development of flowering organs and seed formation [85,86,87,88,89]. During sulfate limitation, miR395 expression is significantly upregulated. miR395 targets two genes capable of participating in the sulfate metabolism pathway, ATP sulfatase (encoded by the APS gene) and sulfate transporter protein 2;1 (SULTR2;1, also known as AST68) [90]. Valdés et al. found Discovery of novel common bean stress response miRNAs for manganese toxicity [91]. Kayihan et al. found expression levels of miRNAs for transcription factors related to JA and ethylene metabolism were significantly induced in moderate B toxicity but not in severe B toxicity, with the most significant regulation obtained in Arabidopsis by miR172 and miR319 [92]. Ozhuner et al. found a total of 31 known miRNAs and 3 new miRNAs were identified in barley, 25 of these were found to be responsive to boron treatment [93]. Thus, miRNAs may therefore plant regulate the expression of downstream genes to help plants to resist the stress.

8. Conclusion and Prospects

Environmental stresses, such as drought, salt, temperature, heavy metals and nutrient stress, affect the metabolic processes of plants, which in turn regulate the expression of secondary metabolites, the synthesis of which reduces the toxic effects of reactive oxygen groups through signal transduction, redox and other mechanisms to ensure the continued survival of the plant (Table 1). Much research have shown that differential expression of miRNAs is induced in plants in response to different environmental stresses. MiRNAs are important regulators in the gene regulatory network and have various functions in regulating the growth, development, programmed cell death and metabolism of organisms [120,121]. MiRNAs can cause changes in the expression of various genes in plants, and therefore their study can help improve the resistance of plants to abiotic stresses. Although miRNAs have been studied for a long time, there is little data available on the link between secondary metabolites and abiotic stresses, and there are still many plant miRNA functions that have not yet been verified. Most articles focus on the role of miRNAs and their target genes in biological processes, while the molecular mechanisms of how miRNAs receive upstream signals and influence various downstream regulatory pathways through cascade responses are still unclear.
With in-depth research on the formation, function and mechanism of action of plant miRNAs and continuous improvement and innovation in miRNA research method, more and more miRNAs will be validated to play a critical role in plant resistance to abiotic stresses, laying the foundation for a more systematic miRNA regulatory network. In summary, miRNAs are essential for plants to regulate mRNA translation in plants, and research to explore the mechanisms of miRNA downstream target gene action can provide a more theoretical basis for improving food production. In the future researchers focus on miRNAs, where genomic information is scarce, will be of great significance in broadening the scope of species and research areas.

Author Contributions

All the authors contributed to the present form of the manuscript. Z.M collected the data, drafted the manuscript; Z.M. and L.J. edited; Z.M. and L.J. created figures and tables; Z.M. and L.J. supervised; Z.M. and L.J. finalized and approved the final version of manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by National Natural Science Foundation of China (32201695) and Scientific Research Project of Education Department of Jilin Province of China (JJKH20211130KJ).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no competing interests.

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Figure 1. The origin, biogenesis of miRNAs in the plant: (a) RNA polymerase II in most cases and RNA polymerase III in a few cases transcribe from genomic sequences to form the precursor pri-miRNA. In the nuclear pri-miRNA is edited by the adenylate deaminase of RNA and forms pre-miRNA hairpin sequences after being sheared by the microprocessor formed by the enzyme. (b) The nucleoplasmic transporter protein recognises the two nucleotides protruding from the 3’ end of the pre-miRNA hairpin sequence and transports the pre-miRNA from the nucleus to the cytoplasm. The nuclease begins to shear the stem-loop structure in the hairpin sequence, after which it is able to produce the miRNA duplex. The pre-miRNA precursor is processed into a mature double-stranded miRNA/miRNA complex by processing the miRNA/miRNA double-stranded body and then the double-stranded body translocates with the help of a protein helper complex. When the mature miRNA is embedded in the RNA-induced silencing complex, the antisense miRNA is degraded in the cytoplasm. The ribonucleoprotein complex miRNP negatively regulates the expression of target genes at the post-transcriptional level through the interaction of its cognate mature miRNA with the target mRNA.
Figure 1. The origin, biogenesis of miRNAs in the plant: (a) RNA polymerase II in most cases and RNA polymerase III in a few cases transcribe from genomic sequences to form the precursor pri-miRNA. In the nuclear pri-miRNA is edited by the adenylate deaminase of RNA and forms pre-miRNA hairpin sequences after being sheared by the microprocessor formed by the enzyme. (b) The nucleoplasmic transporter protein recognises the two nucleotides protruding from the 3’ end of the pre-miRNA hairpin sequence and transports the pre-miRNA from the nucleus to the cytoplasm. The nuclease begins to shear the stem-loop structure in the hairpin sequence, after which it is able to produce the miRNA duplex. The pre-miRNA precursor is processed into a mature double-stranded miRNA/miRNA complex by processing the miRNA/miRNA double-stranded body and then the double-stranded body translocates with the help of a protein helper complex. When the mature miRNA is embedded in the RNA-induced silencing complex, the antisense miRNA is degraded in the cytoplasm. The ribonucleoprotein complex miRNP negatively regulates the expression of target genes at the post-transcriptional level through the interaction of its cognate mature miRNA with the target mRNA.
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Figure 2. The mechanism of miRNAs in the plant: (a) After the plant miRNA recognizes and binds to the target mRNA, the AGO will shear the target mRNA at the 10th and 11th nucleotides of the miRNA binding site. When plant miRNAs bind to target mRNAs, the AGO will shear the target mRNA of the miRNA binding site. (b) Another mechanism of plant miRNAs is through translational repression. The miRNA does not bind to the 3′ UTR region of the target mRNA in its entirety and the RNA-induced silencing complex inhibits the initiation of translation or the specific degradation of the synthetic ribosome to achieve translation inhibition.
Figure 2. The mechanism of miRNAs in the plant: (a) After the plant miRNA recognizes and binds to the target mRNA, the AGO will shear the target mRNA at the 10th and 11th nucleotides of the miRNA binding site. When plant miRNAs bind to target mRNAs, the AGO will shear the target mRNA of the miRNA binding site. (b) Another mechanism of plant miRNAs is through translational repression. The miRNA does not bind to the 3′ UTR region of the target mRNA in its entirety and the RNA-induced silencing complex inhibits the initiation of translation or the specific degradation of the synthetic ribosome to achieve translation inhibition.
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Table 1. Abiotic stress responsive miRNAs: their regulations and target genes in plants.
Table 1. Abiotic stress responsive miRNAs: their regulations and target genes in plants.
Abiotic Stress Type miRNA Expression Species Target Genes Reference
Drought MicroRNA-157 Upregulated Arabidopsis thaliana SPB Transcription factor [94]
Drought MicroRNA-159 Upregulated Arabidopsis thaliana MYB and TCP Transcription factors [95]
Drought MicroRNA-160 Downregulated Arabidopsis thaliana ARF10, ARF16, ARF17 [96]
Drought MicroRNA-166 Upregulated Medicago truncatula HD-ZIPIII Transcription factors [97,98]
Drought MicroRNA-167 Upregulated Arabidopsis thaliana ARF6,ARF8 [94]
Drought MicroRNA-168 Upregulated Arabidopsis thaliana ARGONAUTE, MAPK [94]
Drought MicroRNA-169 Downregulated Arabidopsis thaliana NF-YA transcription factor, SIMRP1 [99]
Drought MicroRNA-171 Upregulated Arabidopsis thaliana GRAS transcription factor [94]
Drought MicroRNA-319 Upregulated Arabidopsis thaliana TCP Family [100]
Drought MicroRNA-390 Upregulated Vigna unguiculata ARF Family [101]
Drought MicroRNA-393 Upregulated Arabidopsis thaliana (TIR1, AFB2, AFB3) (ARF5, EPF1, SPCH) [102,103]
Drought MicroRNA-396 Upregulated Arabidopsis thaliana GRL transcription factor [94]
Drought MicroRNA-397 Downregulated Oryza sativa Laccase genes [104]
Drought MicroRNA-398 Upregulated Medicago truncatula Superoxide dismutase [98]
Drought MicroRNA-398c Downregulated Soybean GmCSD1a/b,GmCSD2a/b/c,GmCCS [28]
Drought MicroRNA-408 Upregulated Arabidopsis thaliana Chemocyanin precursor, kinases [94]
Drought MicroRNA-474 Upregulated Zea mays PDH, PPR [105]
Drought MicroRNA-528 Downregulated Zea mays POD [105]
Drought MicroRNA-811 Downregulated Catharanthus roseus MYB transcription factor [106]
Drought MicroRNA-814 Downregulated Phaseolus vulgaris Hydroxyproline-rich glycoprotein [106]
Drought MicroRNA-835 Downregulated Ricinus communis Aquaporin [106]
Drought MicroRNA-4398 Downregulated Solanum tuberosum WRKY transcription factor [106]
Salt MicroRNA-319b Upregulated Switchgrass PvPCF5 [107]
Salt MicroRNA-390 Downregulated Poplar ARF3.1, ARF3.2,ARF4 [108]
Salt MicroRNA-390a Downregulated Creeping bentgrass AsTIR1, AsAFB2 [26]
Salt MicroRNA-396c Upregulated Creeping bentgrass GRF [37]
Salt MicroRNA-408 Upregulated Wheat TaCP,TaMP,TaBCP,TaFP,TaKRP,TaABP [109]
Salt MicroRNA-408 Upregulated Salvia miltiorrhiza NbSOD, NbPOD, NbCAT [110]
Salt MicroRNA-414c Downregulated Cotton GhFSD1 [111]
Cold MicroRNA-160 Downregulated Maize [112]
Cold MicroRNA-319 Downregulated Rice PCF6/TCP21 [113]
Cold MicroRNA-319 Downregulated Maize [112]
Cold MicroRNA-408a Upregulated Maize [112]
Cold MicroRNA-528 Upregulated Maize [112]
Cold MicroRNA-5125 Upregulated Potato ABF8011 [114]
Cold MicroRNA-10881 Upregulated Potato GA3ox123158 [114]
High temperature MicroRNA-156 Downregulated Arabidopsis thaliana SPL transcription factor [115]
High temperature MicroRNA-159 Downregulated Maize MYB transcription factor [116]
High temperature MicroRNA-164 Downregulated Maize NAC transcription factor [116]
High temperature MicroRNA-166 Downregulated Maize HD zip [116]
High temperature MicroRNA-169 Downregulated Maize SBP [116]
High temperature MicroRNA-172 Downregulated Maize AP2/ERF [116]
High temperature MicroRNA-396 Downregulated Maize GRF, [116]
High temperature MicroRNA-5381 Downregulated Maize SAC2 [116]
Heavy metals-Cd MicroRNA-167 Zea mays [117]
Heavy metals-Cd MicroRNA-393 Zea mays [117]
Heavy metals-Cu MicroRNA-398 Grape VvCSD1 and VvCSD2 [63]
Heavy metals-Al MicroRNA-160 Sugarcance [117]
Heavy metals-Al MicroRNA-162 Sugarcance [117]
Heavy metals-Al MicroRNA-164 Sugarcance [117]
Heavy metals-Al MicroRNA-166 Sugarcance [117]
Heavy metals-Al MicroRNA-167 Sugarcance [117]
Nutrients-Zn MicroRNA-158 Upregulated Brassica juncea FUT1 [118]
Nutrients-K MicroRNA-169 Triticum aestivum Pentose pathway [119]
Nutrients-N MicroRNA-169 Downregulated Arabidopsis thaliana HAP2 [81]
Nutrients-B MicroRNA-319 Upregulated Riticum aestivum MYB transcription factor [92]
Nutrients-K MicroRNA-319 Downregulated Hordeum vulgare TCP [92]
Nutrients-K MicroRNA-396 Downregulated Hordeum vulgare GRF [83]
Nutrients-P MicroRNA-399 Downregulated Arabidopsis thaliana Ubiquitin conjugase E2 [117]
Nutrients-Mn MicroRNA-781 Upregulated Arabidopsis thaliana MCM2 [117]
Nutrients-Mn MicroRNA-826 Upregulated Arabidopsis thaliana Alkenylhydroxalkylproducing 2 [117]
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