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The Role of MicroRNAs in Plants

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A special issue of Plants (ISSN 2223-7747). This special issue belongs to the section "Plant Molecular Biology".

Deadline for manuscript submissions: closed (10 May 2019) | Viewed by 68324

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Dr. Anthony A. Millar

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Guest Editor

Research School of Biology, Australian National University, Canberra ACT 260, Australia
Interests: microRNAs; RNA-binding proteins; post-transcriptional gene regulation

Special Issue Information

Dear Colleagues,

Discovered at the turn of the century, microRNAs (miRNAs) have been found to be fundamental to many aspects of plant biology. They are predominantly derived from non-coding primary-miRNAs (pri-miRNAs) that are able to form double stranded hairpin structures, which are then processed into mature miRNAs (20-24 nt) via a complex process. These miRNAs are then incorporated into the RNA Induced Silencing Complex (RISC), where the miRNA guides RISC to (m)RNAs of high sequence complementarity. The RISC then represses the expression of these target mRNAs via a complex mechanism that includes RNA degradation and translational inhibition. Consistent with their importance, there is a core set of conserved miRNA that are ancient, being present throughout land plants, controlling processes such as phase change, organ polarity, leaf and root development, flowering and responses to environmental stimuli. The mRNA targets of these ancient miRNAs are mainly regulatory genes such as transcription factors, explaining why these miRNAs act as master regulators of gene expression and phenotypic outcomes.

Despite this wealth of knowledge, there are still many unanswered questions regarding miRNA biology. Our understanding of miRNA biogenesis is still incomplete; how a mature miRNA is precisely processed from a pri-miRNA is far from resolved. Regarding the actual silencing process, the mechanism of translational repression remains largely elusive, as does the extent it plays in silencing. Our understanding of target recognition is far from perfect, of the many bioinformatically predicted targets, only a few of these ever appear to be functionally significant targets. Beyond the conserved set of miRNAs, deep sequencing of small RNAs from many different plant species has identify a myriad of less conserved miRNAs, that correspond to immense regulatory potential. However, for the majority of these miRNAs, there is little functional evidence regarding the (m)RNAs they target, and the role, if any, they play in the plant. Finally, the extent to which miRNAs move between cells, tissues, plants and kingdoms to regulate genes in trans, is an area of great interest, but with still many unknowns. This Special Issues of Plants aims to touch on some of these issues.

Dr. Anthony A Millar
Guest Editor

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Keywords

miRNAs
miRNA biogenesis
silencing mechanism
miRNA target recognition
bioinformatics for miRNA identification and target prediction
functional analysis
developmental and stress responsive miRNAs

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Published Papers (11 papers)

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Editorial

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4 pages, 199 KiB

Open AccessEditorial

The Function of miRNAs in Plants

by Anthony A Millar

Plants 2020, 9(2), 198; https://doi.org/10.3390/plants9020198 - 5 Feb 2020

Cited by 55 | Viewed by 6071

Abstract

MicroRNAs (miRNAs) are a class of small RNAs (sRNAs) that repress gene expression via high complementary binding sites in target mRNAs (messenger RNAs). Many miRNAs are ancient, and their intricate integration into gene expression programs have been fundamental for plant life, controlling developmental programs and executing responses to biotic/abiotic cues. Additionally, there are many less conserved miRNAs in each plant species, raising the possibility that the functional impact of miRNAs extends into virtually every aspect of plant biology. This Special Issue of Plants presents papers that investigate the function and mechanism of miRNAs in controlling development and abiotic stress response. This includes how miRNAs adapt plants to nutrient availability, and the silencing machinery that is responsible for this. Several papers profile changes in miRNA abundances during stress, and another study raises the possibility of circular RNAs acting as endogenous decoys to sequester and inhibit plant miRNA function. These papers act as foundational studies for the more difficult task ahead of determining the functional significance of these changes to miRNA abundances, or the presence of these circular RNAs. Finally, how miRNAs trigger the production of secondary sRNAs is reviewed, along with the potential agricultural impact of miRNAs and these secondary sRNA in the exemplar crop maize. Full article

(This article belongs to the Special Issue The Role of MicroRNAs in Plants)

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13 pages, 2078 KiB

Open AccessArticle

Circular and Micro RNAs from Arabidopsis thaliana Flowers Are Simultaneously Isolated from AGO-IP Libraries

by Érika Frydrych Capelari, Guilherme Cordenonsi da Fonseca, Frank Guzman and Rogerio Margis

Plants 2019, 8(9), 302; https://doi.org/10.3390/plants8090302 - 26 Aug 2019

Cited by 23 | Viewed by 4510

Abstract

Competing endogenous RNAs (ceRNAs) are natural transcripts that can act as endogenous sponges of microRNAs (miRNAs), modulating miRNA action upon target mRNAs. Circular RNAs (circRNAs) are one among the various classes of ceRNAs. They are produced from a process called back-splicing and have been identified in many eukaryotes. In plants, their effective action as a miRNA sponge was not yet demonstrated. To address this question, public mRNAseq data from Argonaute-immunoprecipitation libraries (AGO-IP) of Arabidopsis thaliana flowers were used in association with a bioinformatics comparative multi-method to identify putative circular RNAs. A total of 27,812 circRNAs, with at least two reads at the back-splicing junction, were identified. Further analyses were used to select those circRNAs with potential miRNAs binding sites. As AGO forms a ternary complex with miRNA and target mRNA, targets count in AGO-IP and input libraries were compared, demonstrating that mRNA targets of these miRNAs are enriched in AGO-IP libraries. Through this work, five circRNAs that may function as miRNA sponges were identified and one of them were validated by PCR and sequencing. Our findings indicate that this post-transcriptional regulation can also occur in plants. Full article

(This article belongs to the Special Issue The Role of MicroRNAs in Plants)

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11 pages, 1390 KiB

Open AccessArticle

Expression of miR159 Is Altered in Tomato Plants Undergoing Drought Stress

by María José López-Galiano, Inmaculada García-Robles, Ana I. González-Hernández, Gemma Camañes, Begonya Vicedo, M. Dolores Real and Carolina Rausell

Plants 2019, 8(7), 201; https://doi.org/10.3390/plants8070201 - 2 Jul 2019

Cited by 65 | Viewed by 6216

Abstract

In a scenario of global climate change, water scarcity is a major threat for agriculture, severely limiting crop yields. Therefore, alternatives are urgently needed for improving plant adaptation to drought stress. Among them, gene expression reprogramming by microRNAs (miRNAs) might offer a biotechnologically sound strategy. Drought-responsive miRNAs have been reported in many plant species, and some of them are known to participate in complex regulatory networks via their regulation of transcription factors involved in water stress signaling. We explored the role of miR159 in the response of Solanum lycopersicum Mill. plants to drought stress by analyzing the expression of sly-miR159 and its target SlMYB transcription factor genes in tomato plants of cv. Ailsa Craig grown in deprived water conditions or in response to mechanical damage caused by the Colorado potato beetle, a devastating insect pest of Solanaceae plants. Results showed that sly-miR159 regulatory function in the tomato plants response to distinct stresses might be mediated by differential stress-specific MYB transcription factor targeting. sly-miR159 targeting of SlMYB33 transcription factor transcript correlated with accumulation of the osmoprotective compounds proline and putrescine, which promote drought tolerance. This highlights the potential role of sly-miR159 in tomato plants’ adaptation to water deficit conditions. Full article

(This article belongs to the Special Issue The Role of MicroRNAs in Plants)

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14 pages, 2175 KiB

Open AccessArticle

Conserved Cu-MicroRNAs in Arabidopsis thaliana Function in Copper Economy under Deficiency

by Muhammad Shahbaz and Marinus Pilon

Plants 2019, 8(6), 141; https://doi.org/10.3390/plants8060141 - 29 May 2019

Cited by 25 | Viewed by 3811

Abstract

Copper (Cu) is a micronutrient for plants. Three small RNAs, which are up-regulated by Cu deficiency and target transcripts for Cu proteins, are among the most conserved microRNAs in plants. It was hypothesized that these Cu-microRNAs help save Cu for the most essential Cu-proteins under deficiency. Testing this hypothesis has been a challenge due to the redundancy of the Cu microRNAs and the properties of the regulatory circuits that control Cu homeostasis. In order to investigate the role of Cu-microRNAs in Cu homeostasis during vegetative growth, we used a tandem target mimicry strategy to simultaneously inhibit the function of three conserved Cu-microRNAs in Arabidopsis thaliana. When compared to wild-type, transgenic lines that express the tandem target mimicry construct showed reduced Cu-microRNA accumulation and increased accumulation of transcripts that encode Cu proteins. As a result, these mimicry lines showed impaired photosynthesis and growth compared to wild type on low Cu, which could be ascribed to a defect in accumulation of plastocyanin, a Cu-containing photosynthetic electron carrier, which is itself not a Cu-microRNA target. These data provide experimental support for a Cu economy model where the Cu-microRNAs together function to allow maturation of essential Cu proteins under impending deficiency. Full article

(This article belongs to the Special Issue The Role of MicroRNAs in Plants)

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26 pages, 2276 KiB

Open AccessArticle

DRB1, DRB2 and DRB4 Are Required for Appropriate Regulation of the microRNA399/PHOSPHATE2 Expression Module in Arabidopsis thaliana

by Joseph L. Pegler, Jackson M. J. Oultram, Christopher P. L. Grof and Andrew L. Eamens

Plants 2019, 8(5), 124; https://doi.org/10.3390/plants8050124 - 13 May 2019

Cited by 11 | Viewed by 4900

Abstract

Adequate phosphorous (P) is essential to plant cells to ensure normal plant growth and development. Therefore, plants employ elegant mechanisms to regulate P abundance across their developmentally distinct tissues. One such mechanism is PHOSPHATE2 (PHO2)-directed ubiquitin-mediated degradation of a cohort of phosphate (PO₄) transporters. PHO2 is itself under tight regulation by the PO₄ responsive microRNA (miRNA), miR399. The DOUBLE-STRANDED RNA BINDING (DRB) proteins, DRB1, DRB2 and DRB4, have each been assigned a specific functional role in the Arabidopsis thaliana (Arabidopsis) miRNA pathway. Here, we assessed the requirement of DRB1, DRB2 and DRB4 to regulate the miR399/PHO2 expression module under PO₄ starvations conditions. Via the phenotypic and molecular assessment of the knockout mutant plant lines, drb1, drb2 and drb4, we show here that; (1) DRB1 and DRB2 are required to maintain P homeostasis in Arabidopsis shoot and root tissues; (2) DRB1 is the primary DRB required for miR399 production; (3) DRB2 and DRB4 play secondary roles in regulating miR399 production, and; (4) miR399 appears to direct expression regulation of the PHO2 transcript via both an mRNA cleavage and translational repression mode of RNA silencing. Together, the hierarchical contribution of DRB1, DRB2 and DRB4 demonstrated here to be required for the appropriate regulation of the miR399/PHO2 expression module identifies the extreme importance of P homeostasis maintenance in Arabidopsis to ensure that numerous vital cellular processes are maintained across Arabidopsis tissues under a changing cellular environment. Full article

(This article belongs to the Special Issue The Role of MicroRNAs in Plants)

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18 pages, 2489 KiB

Open AccessEditor’s ChoiceArticle

Profiling the Abiotic Stress Responsive microRNA Landscape of Arabidopsis thaliana

by Joseph L. Pegler, Jackson M. J. Oultram, Christopher P. L. Grof and Andrew L. Eamens

Plants 2019, 8(3), 58; https://doi.org/10.3390/plants8030058 - 10 Mar 2019

Cited by 55 | Viewed by 6940

Abstract

It is well established among interdisciplinary researchers that there is an urgent need to address the negative impacts that accompany climate change. One such negative impact is the increased prevalence of unfavorable environmental conditions that significantly contribute to reduced agricultural yield. Plant microRNAs (miRNAs) are key gene expression regulators that control development, defense against invading pathogens and adaptation to abiotic stress. Arabidopsis thaliana (Arabidopsis) can be readily molecularly manipulated, therefore offering an excellent experimental system to alter the profile of abiotic stress responsive miRNA/target gene expression modules to determine whether such modification enables Arabidopsis to express an altered abiotic stress response phenotype. Towards this goal, high throughput sequencing was used to profile the miRNA landscape of Arabidopsis whole seedlings exposed to heat, drought and salt stress, and identified 121, 123 and 118 miRNAs with a greater than 2-fold altered abundance, respectively. Quantitative reverse transcriptase polymerase chain reaction (RT-qPCR) was next employed to experimentally validate miRNA abundance fold changes, and to document reciprocal expression trends for the target genes of miRNAs determined abiotic stress responsive. RT-qPCR also demonstrated that each miRNA/target gene expression module determined to be abiotic stress responsive in Arabidopsis whole seedlings was reflective of altered miRNA/target gene abundance in Arabidopsis root and shoot tissues post salt stress exposure. Taken together, the data presented here offers an excellent starting platform to identify the miRNA/target gene expression modules for future molecular manipulation to generate plant lines that display an altered response phenotype to abiotic stress. Full article

(This article belongs to the Special Issue The Role of MicroRNAs in Plants)

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16 pages, 9029 KiB

Open AccessArticle

Functional Characterization of microRNA171 Family in Tomato

by Michael Kravchik, Ran Stav, Eduard Belausov and Tzahi Arazi

Plants 2019, 8(1), 10; https://doi.org/10.3390/plants8010010 - 4 Jan 2019

Cited by 32 | Viewed by 6401

Abstract

Deeply conserved plant microRNAs (miRNAs) function as pivotal regulators of development. Nevertheless, in the model crop Solanum lycopersicum (tomato) several conserved miRNAs are still poorly annotated and knowledge about their functions is lacking. Here, the tomato miR171 family was functionally analyzed. We found that the tomato genome contains at least 11 SlMIR171 genes that are differentially expressed along tomato development. Downregulation of sly-miR171 in tomato was successfully achieved by transgenic expression of a short tandem target mimic construct (STTM171). Consequently, sly-miR171-targeted mRNAs were upregulated in the silenced plants. Target upregulation was associated with irregular compound leaf development and an increase in the number of axillary branches. A prominent phenotype of STTM171 expressing plants was their male sterility due to a production of a low number of malformed and nonviable pollen. We showed that sly-miR171 was expressed in anthers along microsporogenesis and significantly silenced upon STTM171 expression. Sly-miR171-silenced anthers showed delayed tapetum ontogenesis and reduced callose deposition around the tetrads, both of which together or separately can impair pollen development. Collectively, our results show that sly-miR171 is involved in the regulation of anther development as well as shoot branching and compound leaf morphogenesis. Full article

(This article belongs to the Special Issue The Role of MicroRNAs in Plants)

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13 pages, 2875 KiB

Open AccessArticle

Genome-Wide Investigation of the Role of MicroRNAs in Desiccation Tolerance in the Resurrection Grass Tripogon loliiformis

by Isaac Njaci, Brett Williams, Claudia Castillo-González, Martin B. Dickman, Xiuren Zhang and Sagadevan Mundree

Plants 2018, 7(3), 68; https://doi.org/10.3390/plants7030068 - 31 Aug 2018

Cited by 9 | Viewed by 5740

Abstract

Drought causes approximately two-thirds of crop and yield loss worldwide. To sustain future generations, there is a need to develop robust crops with enhanced water use efficiency. Resurrection plants are naturally resilient and tolerate up to 95% water loss with the ability to revive upon watering. Stress is genetically encoded and resilient species may garner tolerance by tightly regulating the expression of stress-related genes. MicroRNAs (miRNAs) post-transcriptionally regulate development and other stress response processes in eukaryotes. However, their role in resurrection plant desiccation tolerance is poorly understood. In this study, small RNA sequencing and miRNA expression profiling was conducted using Tripogon loliiformis plants subjected to extreme water deficit conditions. Differentially expressed miRNA profiles, target mRNAs, and their regulatory processes were elucidated. Gene ontology enrichment analysis revealed that development, stress response, and regulation of programmed cell death biological processes; Oxidoreductase and hydrolyase molecular activities; and SPL, MYB, and WRKY transcription factors were targeted by miRNAs during dehydration stress, indicating the indispensable regulatory role of miRNAs in desiccation tolerance. This study provides insights into the molecular mechanisms of desiccation tolerance in the resurrection plant T. loliiformis. This information will be useful in devising strategies for crop improvement on enhanced drought tolerance and water use efficiency. Full article

(This article belongs to the Special Issue The Role of MicroRNAs in Plants)

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Review

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17 pages, 1666 KiB

Open AccessEditor’s ChoiceReview

Biology and Function of miR159 in Plants

by Anthony A. Millar, Allan Lohe and Gigi Wong

Plants 2019, 8(8), 255; https://doi.org/10.3390/plants8080255 - 30 Jul 2019

Cited by 105 | Viewed by 7976

Abstract

MicroR159 (miR159) is ancient, being present in the majority of land plants where it targets a class of regulatory genes called GAMYB or GAMYB-like via highly conserved miR159-binding sites. These GAMYB genes encode R2R3 MYB domain transcription factors that transduce the gibberellin (GA) signal in the seed aleurone and the anther tapetum. Here, GAMYB plays a conserved role in promoting the programmed cell death of these tissues, where miR159 function appears weak. By contrast, GAMYB is not involved in GA-signaling in vegetative tissues, but rather its expression is deleterious, leading to the inhibition of growth and development. Here, the major function of miR159 is to mediate strong silencing of GAMYB to enable normal growth. Highlighting this requirement of strong silencing are conserved RNA secondary structures associated with the miR159-binding site in GAMYB mRNA that promotes miR159-mediated repression. Although the miR159-GAMYB pathway in vegetative tissues has been implicated in a number of different functions, presently no conserved role for this pathway has emerged. We will review the current knowledge of the different proposed functions of miR159, and how this ancient pathway has been used as a model to help form our understanding of miRNA biology in plants. Full article

(This article belongs to the Special Issue The Role of MicroRNAs in Plants)

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17 pages, 3184 KiB

Open AccessReview

Perspectives on microRNAs and Phased Small Interfering RNAs in Maize (Zea mays L.): Functions and Big Impact on Agronomic Traits Enhancement

by Zhanhui Zhang, Sachin Teotia, Jihua Tang and Guiliang Tang

Plants 2019, 8(6), 170; https://doi.org/10.3390/plants8060170 - 12 Jun 2019

Cited by 20 | Viewed by 6930

Abstract

Small RNA (sRNA) population in plants comprises of primarily micro RNAs (miRNAs) and small interfering RNAs (siRNAs). MiRNAs play important roles in plant growth and development. The miRNA-derived secondary siRNAs are usually known as phased siRNAs, including phasiRNAs and tasiRNAs. The miRNA and phased siRNA biogenesis mechanisms are highly conserved in plants. However, their functional conservation and diversification may differ in maize. In the past two decades, lots of miRNAs and phased siRNAs have been functionally identified for curbing important maize agronomic traits, such as those related to developmental timing, plant architecture, sex determination, reproductive development, leaf morphogenesis, root development and nutrition, kernel development and tolerance to abiotic stresses. In contrast to Arabidopsis and rice, studies on maize miRNA and phased siRNA biogenesis and functions are limited, which restricts the small RNA-based fundamental and applied studies in maize. This review updates the current status of maize miRNA and phased siRNA mechanisms and provides a survey of our knowledge on miRNA and phased siRNA functions in controlling agronomic traits. Furthermore, improvement of those traits through manipulating the expression of sRNAs or their targets is discussed. Full article

(This article belongs to the Special Issue The Role of MicroRNAs in Plants)

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15 pages, 1189 KiB

Open AccessReview

Gene Regulation Mediated by microRNA-Triggered Secondary Small RNAs in Plants

by Felipe Fenselau de Felippes

Plants 2019, 8(5), 112; https://doi.org/10.3390/plants8050112 - 26 Apr 2019

Cited by 21 | Viewed by 6570

Abstract

In plants, proper development and response to abiotic and biotic stimuli requires an orchestrated regulation of gene expression. Small RNAs (sRNAs) are key molecules involved in this process, leading to downregulation of their target genes. Two main classes of sRNAs exist, the small interfering RNAs (siRNAs) and microRNAs (miRNAs). The role of the latter class in plant development and physiology is well known, with many examples of how miRNAs directly impact the expression of genes in cells where they are produced, with dramatic consequences to the life of the plant. However, there is an aspect of miRNA biology that is still poorly understood. In some cases, miRNA targeting can lead to the production of secondary siRNAs from its target. These siRNAs, which display a characteristic phased production pattern, can act in cis, reinforcing the initial silencing signal set by the triggering miRNA, or in trans, affecting genes that are unrelated to the initial target. In this review, the mechanisms and implications of this process in the gene regulation mediated by miRNAs will be discussed. This work will also explore techniques for gene silencing in plants that are based on this unique pathway. Full article

(This article belongs to the Special Issue The Role of MicroRNAs in Plants)

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