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MicroRNA and Transcription Factor: Key Players in Plant Regulatory Network

Abdul F. A. Samad, Muhammad Sajad, Nazaruddin Nazaruddin and 4 more

Frontiers in Plant Science · 2017 · Review

doi:10.3389/fpls.2017.00565

Abstract

Recent achievements in plant microRNA (miRNA), a large class of small and non-coding RNAs, are very exciting. A wide array of techniques involving forward genetic, molecular cloning, bioinformatic analysis, and the latest technology, deep sequencing have greatly advanced miRNA discovery. A tiny miRNA sequence has the ability to target single/multiple mRNA targets. Most of the miRNA targets are transcription factors (TFs) which have paramount importance in regulating the plant growth and development. Various families of TFs, which have regulated a range of regulatory networks, may assist plants to grow under normal and stress environmental conditions. This present review focuses on the regulatory relationships between miRNAs and different families of TFs like; NF-Y, MYB, AP2, TCP, WRKY, NAC, GRF, and SPL. For instance NF-Y play important role during drought tolerance and flower development, MYB are involved in signal transduction and biosynthesis of secondary metabolites, AP2 regulate the floral development and nodule formation, TCP direct leaf development and growth hormones signaling. WRKY have known roles in multiple stress tolerances, NAC regulate lateral root formation, GRF are involved in root growth, flower, and seed development, and SPL regulate plant transition from juvenile to adult. We also studied the relation between miRNAs and TFs by consolidating the research findings from different plant species which will help plant scientists in understanding the mechanism of action and interaction between these regulators in the plant growth and development under normal and stress environmental conditions.

Full text

From PubMed Central, U.S. National Library of Medicine, as current on Oct 19, 2026. Paragraph numbers are ours, so an answer can point at one.

Introduction

The recent discovery of complex regulatory network in higher organisms like; plants and animals have been recognized in plants. These complex networks which consist of chromatin modification (at epigenetic level), mRNA splicing, cell signaling, polyadenylation, and mechanisms of protein activation and degradation demanded substantial attention in order to achieve complete understanding on how plant system are being regulated. This review has been intended to focus on gene regulation at transcriptional and post-transcriptional levels which involving microRNAs (miRNAs) and transcription factors (TFs) as key regulatory players.

At the transcriptional level, the interaction of TFs interact with enhancers to coordinate gene expression has been well established in the past decade. This can be obviously seen in the discovery of many types of TFs families which play a diverse role in plant system. At the post-transcriptional level, another attractive mechanism of gene regulation has been discovered a couple of decades ago, involving a large class of small non-coding RNAs, known as miRNAs. These miRNAs act as gene regulators in plants and animals by negatively regulate mRNAs. With the increasing number of regulators involved in gene networks, it is interesting to observe and understand a dynamic relationship between miRNAs, TFs, and mRNAs.

To date, about 28,645 miRNAs from plants, animals, and viruses have been registered in public miRNA database. These miRNAs are able to modulate and fine-tune majority of biological processes by regulating a large number of target genes. Thus, screening of the potential target genes can provide an efficient and critical approach to explore the miRNA-mediated regulatory functions in depth at post-transcriptional level. Early exploration of some empirical parameters and algorithms deduced for known miRNA-target interactions using computational prediction in Arabidopsis had been applied to determine miRNA targets in other plants. The prediction approaches have further been validated through wet lab techniques and methods like PAGE, Northern Blot, Rapid Amplification of cDNA Ends at 5′ (5′-RACE), and Degradome Sequencing analysis.

Currently there are 58 families of TFs which consist of 320,370 members from 165 plant species. miRNAs only downregulate their targets while TFs activate or repress the transcription of their targets, eventually determining the fate of particular gene, either to be switched “on” or switched “off”. Interestingly, majority of miRNA targets are TFs. Since both regulators demonstrate great impact toward plant genetic system, the circuiting of miRNAs-TFs will allow orchestration of numerous biological processes with high reliability.

Recent trends in miRNA research were focused on plant responses to abiotic rather than biotic stresses. The prevailing environmental stresses like; drought, salinity, and cold, which significantly affect plant growth and development, are the prominent factors of plant research shift toward abiotic stress. The present review will provide a better understanding of miRNAs regulation and their interaction with the TFs, which can assist the researchers to explore more about plant survival mechanism under unfavorable environmental conditions. The newly developed relationship among the above mentioned gene regulators will assist the plant scientists to gain insight into the relationship among these regulators in different plant species.

miRNA Biogenesis and Mode of Action in Plant

In plants, miRNA genes are transcribed by RNA polymerase II to produce primary miRNA (Pri-miRNA) and their length is highly variable between themselves. Unlike animal, plant miRNA processing is accomplished inside the nucleus because they lack protein processor like Drosha and DGCR8. In plant, DICER-LIKE 1 (DCL1) process most of pri-miRNAs by cleavage. Pri-miRNAs are stabilized with a type of RNA binding protein, DAWDLE (DDL), which interacts with DCL1 in nuclear foci, named dicing bodies (D-bodies). The combined action of couple of proteins like; SERRATE (SE) and HYPONASTIC LEAVES 1 (HYL1), followed by DCL1 and the nuclear cap-binding complex, led to form a short duplex miRNA which consist of mature miRNA guide cleavage and passenger miRNA strand (miRNA∗). Further processing of this duplex leds to the 2′-O-methylation at 3′ by the methyltransferase HEN1. A family of enzymes, called SMALL RNA DEGRADING NUCLEASE (SDN) genes, is responsible for the accumulation of miRNAs. SDN1 have shown 3′-5′ exoribonuclease activity against short and single-stranded RNA substrates. In plants, HASTY (HST), which is homolog to EXPORTIN5 (EXP5), plays a crucial role in exporting pre-miRNAs or mature miRNAs to cytoplasm. Another export pathway of miRNAs seems to be involved but the exact mechanism is still not clear.

In the cytoplasm, ARGONAUTE (AGO) proteins form an assembly with miRNA, known as RNA-induced silencing complex (RISC). AGO1 in the RISC is the major player for the miRNA pathway. AGO protein consist of PAZ and PIWI domain. Particularly, PIWI domain form RNaseH-like fold which catalyze endonuclease activity. This endonuclease activity is capable of chopping RNA targets that are complementary to the miRNA strand loaded inside the AGO. AGO proteins in Arabidopsis thaliana such as AGO1, AGO2, and AGO10 has been reported to have the endonuclease activity, which leds to splicing the mRNA targets. Identification of the sliced mRNA targets by miRNA can be discovered through sequencing of mRNA degradome. Previous study reveals that plant miRNAs bind to their targets with high complementary which results in the cleavage of target mRNA. Beside of cleavage, there are several cases where the miRNA target is regulated at protein level without significant changes in mRNA level. These findings suggest that plant miRNAs are capable in interfering the translation process of mRNA.

TFs for Gene Regulation in Plant

Transcription factors are essential for the regulation of gene expression, and usually belong to members of multigene families. Generally TFs exist as modular proteins containing of DNA-binding domain that interacts with cis-elements of their target genes. Besides, it also consists of protein–protein interaction domain that assists oligomerization between TFs or with other regulators. Many TFs have been recognized by X-ray crystallography and Nuclear Magnetic Resonance spectroscopy. TFs families can be evolved in many ways such as exon capture, duplication, translocation and mutation. In plants, the regulation of TFs genes occurs at transcriptional and post-transcriptional levels. They participate in genetic system via many ways such as developmental control, elicitation of defense, and stress responses by expressing the gene at right time and right place.

Hence, understanding the activity of TFs expression is crucial for building regulatory networks. Mode of action of TFs is considered to occur mainly through the binding of TFs to cis-regulatory element within the promoter regions of their targets genes. However, with various post-transcriptional regulatory mechanisms that recently have been discovered, including; miRNA regulation, nonsense-mediated mRNA decay, and nuclear export control, it evidences that mRNAs are regulated at many layers of gene regulation. Undoubtedly, there is a potential for altering expression patterns mediated by cis-elements through post-transcriptional regulation. Beside, a single TF has the ability to regulate multiple genes in certain metabolic pathways. Further, it is also quite clear through recent investigations that changes in gene transcription are closely related to changes in the expression of TFs. Therefore, alteration in the expression of TF genes normally results in remarkable changes during plant growth and development. As a future consequence, engineering of transcription factor genes may provide a valuable means for manipulation of desired traits in plants. Here we have reviewed briefly TF families that involve in plant growth and development under normal and stress environmental condition.

NF-Y or also known as Nuclear factor Y, are TFs that consist of three subunits, NF-YA (CBF-B or HAP2), NF-YB (CBF-A or HAP3), and NF-YC (CBF-C or HAP5). All of these subunits are essential for DNA binding. NF-Y, in the promoter region, recognize CCAAT box with high specificity and affinity due to the presence of its highly conserved trimeric activator. These transcription factors have different functions according to their subunits. For instances, NF-YA and NF-YB involve in drought tolerance and NF-YC, appears to be important regulator in flowering and photomorphogenesis. Nf-y mutant plant exhibited dark grown phenotype, although in the present of light, thus indicate NF-Y TF were positive regulators of photomorphogenesis. NY-FA participated in flowering process when in complex with NF-YB/NF-YC by activating FLOWERING LOCUS T gene. Transgenic Arabidopsis plants overexpressing NFYA5 resulted to high drought tolerance.

MYB (myeloblastosis) is a large family of proteins, playing diverse role in gene network in eukaryotes. Most MYB proteins act as TFs with different numbers of MYB domain repeats; MYB-related, R2R3-MYB, R1R2R3-MYB, and atypical MYB family which exhibited their ability to bind DNA. They are widely distributed in plants and also interact with other TFs. MYB have been involved in growth and development of different plant species, e.g., in Glycine max, they are involved in flower color development, and in signal transduction pathways in A. thaliana, Oryza sativa, and cassava. In A. thaliana and Medicago truncatula they regulate the biosynthesis of secondary metabolites.

APETALA2 (AP2) family of TFs plays a pivotal role in regulating the complex developmental process of floral development. AP2 family, also called class “A” of TFs, interacts with other two classes (B and C) of TFs and determines the final development of the floral organs, and this interaction was summarized as ABC model. Complexity of floral formation shown by co-regulation of three classes of TFs, class A, B, and C genes, which determine the four floral organ types. Family of class A TFs (AP2) itself alone regulate the identity of sepal in whorl 1. It’s co-action with B class genes, PISTILLATA (PI), determines petal identity in whorl 2. Further the interaction of class B TFs with class C, AGAMOUS (AG), determines stamen identity in whorl 3. Carpel identity in whorl 4 specified by AG itself. AP2 which belong to Class A gene, interacts with class C gene and AG by suppressing each other’s roles in order to determine the identities and properties of the reproductive organs and perianth. Loss-of-function of AP2 turns sepals and petals into carpels since there are in excess of AG activity into the outer two whorls of the flower.

Most of the miRNA targets are TFs which regulate plant growth and developments. One of the important plant developmental processes is flowering stage, which is regulated by complex gene networks that integrate multiple environmental and endogenous cues to ensure flowering at the appropriate time. This mechanism is eventually regulated by the induction and activity of three main TFs; LEAFY (LFY), FRUITFULL (FUL), and APETALA1 (AP1). Among these three genes, LFY has been considered to play a role as major regulator, since, the loss of LFY function causes the most remarkable delay in flowering process. However, these three genes are controlled by TF SQUAMOSA PROMOTER BINDING PROTEINLIKE 3 (SPL3). In general, SQUAMOSA PROMOTER BINDING PROTEINLIKE (SPL) genes are featured by their SQUAMOSA PROMOTER-BINDING (SBP) domain, which consists of a novel zinc finger with two zinc ion binding sites.

TCP TF contains a TCP domain, which codes a motif that is predicted to form basic helix-loop-helix structure known for distinct DNA-binding domains. TCP TF is named after the first four characterized members, namely TEOSINTE BRANCHED1 (TB1) from maize, CYCLOIDEA (CYC) from snapdragon, and PROLIFERATING CELL NUCLEAR ANTIGEN FACTOR1 (PCF1) from rice. Previous finding unravel that TCP have been involved in different ways to promote leaf development by cell division, growth, and differentiation. TCP TFs also involve in flower development, leaf senescence, auxin and jasmonic acid signaling, development of male and female gametophyte, mitochondrial biogenesis, and interaction with the circadian clock. In Arabidopsis, there are 24 predicted TCP proteins. These predicted TCP were classified into two groups; class I and class II proteins. Class I made up of 13 proteins, whereas, remaining 11 proteins were placed in class II proteins. Both of these classes act as activator and repressor.

WRKY TFs belong to huge and diverse family of TFs. Till now, 74 members had been identified in A. thaliana and 109 in O. sativa. Members of this family have at least one conserved DNA-binding region, WRKY domain, comprising of a conserved WRKYGQK peptide sequence and a zinc finger motif. In general, this domain binds to the W box, a DNA element, even though alternative binding sites also have been identified. WRKY TFs involve in various networks in genetic system to govern multiple responses at once; whether it is biotic and abiotic stresses, or physiological. Besides, WRKY TFs are also responsible to regulate production of some secondary metabolites such as phenolic compounds along with lignin, flavanols, and tannins.

NAC [no apical meristem (NAM), Arabidopsis transcription activation factor [ATAF1/2], and cup-shaped cotyledon (CUC2)] are among of major families of transcriptional regulators in plants, and present in a wide range of land plants. In Arabidopsis, 9 of the 10, NAC domains are known to bind with conserved DNA target sequence having a CGT[GA] core with different affinity levels. Interestingly, NAC TFs play diverse roles in plant system which includes; regulation of plant development and responses to biotic and abiotic stresses.

Plant-specific TFs, growth-regulating factor (GRF) were initially identified for their role in developing stem and leaf. But later studies revealed that in addition to stem and leaves, other important for other developmental processes including root growth, flower and seed development, and plant responses under extreme environmental conditions. GRF forms complexes by combining with GRF-interacting factors (GIFs), a type of transcriptional co-activators.

Homeo domain-leucine zipper (HD-Zip) proteins are among the TFs that belong to plants kingdom. In A. thaliana, these TFs are encoded by more than 25 genes. Two important domains HD-Zip proteins are characterized by the presence of a homeo domain (HD) and a leucine zipper domain (Zip) which are responsible for DNA binding and involved in protein–protein interaction, respectively. Based on previous sequence similarities findings, these proteins have been divided into four groups. Among these groups, HD-Zip I proteins are involved in plant responses related to abiotic stress, blue light, de-etiolation, abscisic acid (ABA), and embryogenesis. Second group, HD-Zip II proteins take part in auxin signaling, light response, and shade avoidance. Similarly, HD-Zip III governs embryogenesis, lateral organ initiation, leaf polarity, and meristem function. Whereas, HD-Zip IV proteins play important role during trichome formation, root development, differentiation of epidermal cells, and anthocyanin accumulation.

miRNAs and TFs: Partnership in Plant Gene Regulation

It is essential to illustrate an integrated picture for the regulatory relationships between miRNAs, TFs, and target genes. However, it is quite difficult to develop a clear cut regulatory relationship between miRNAs and TFs, because, in addition to the interaction of these regulators with their target genes, they sometimes interact with each other; leading to some different results. Here, we have summarized the similarities (Table 1) and differences (Table 2) between miRNAs and TFs mediated regulatory system. We also propose a model to relate these two regulators with their target genes and the consequences of this model to the plant regulatory network under normal (Figure 1) and stress condition (Figure 2). The existence of both miRNAs and TFs in gene regulatory networks will reveal the regulatory role involving both direct and indirect regulatory relationships. In this review, we have tried to bring together previous findings, related to the interaction between miRNAs and TFs, mostly in model plants and some non-model plant (Table 3). Rigorous and time consuming web lab/experimental work was a big hurdle in developing interactions between miRNAs and TFs in plants. But now, with the advancement in the public data bases and bioinformatics tools, to develop an interaction between above mentioned regulators it is relatively easy.

miRNAs and TFs During Plant Growth and Development

Plant growth and development are reflection of genes expression. Appropriate timing and pattern of gene expression and production of proteins are required to ensure proper growth and development in plant. miRNAs and TFs are among the key regulators which determine how gene expression being regulated, thus affect the physiology and phenotype of the plant.

miRNA and NY-FA: Regulate Root Architecture and Facilitate Nodule Formation

In Arabidopsis, four isoforms of miR169 were identified to target NF-YA transcription factor. Those miR169 isoforms (miR169defg) and the NF-YA2 TF were recognized to control the root architecture since loss-of-function miR169defg led to improper root initiation. On the other hand, interaction of miR169 and NF-YA transcription factor also seems to be affect nodule formation in Arabidopsis. The overexpression of miR169 against NFYA transcription factor family member, HAP2-1, resulted in late nodulation and detained meristem development, thus led to improper development of nodules.

miRNA and MYB: Regulate Flowering Time, Phosphate Homeostasis, Leaf Senescence and Root and Fiber Development

Loss-of-function of miR858 plants led to the robust growth and early flowering. Further expression of artificial miRNA (amiRNA) target mimic (MIM858) cause the reduction of plant growth and delayed flowering. MYB transcription factor was able to activate miR399, which responsed to phosphate (Pi) starvation in Arabidopsis. Overexpressing AtMYB2 showed high miR399f expression and tissue Pi contents which may resulted via elevated expression of a subset of Pi starvation-induced genes.

In maize inbred line, ELS-1, zma-miR159d which targeted MYB transcription factor was significantly downregulated in the leaves during senescence, while in another inbred line, Yu87-1, zma-miR159d was upregulated. In cotton, ghr-miR447a and ghr-miR5255a/b/c/e/f/g/h targeted CPC, a type of MYB transcription factor showing that ghr-miR447a and ghr-miR5255a/b/c/e/f/g/h might play a significant role in root and fiber development under drought and salinity stresses by regulating CPC in cotton. Similar study was carried out in cotton where two miRNAs; miR828 and miR858, targeted MYB2, which is responsible for fiber development.

miRNAs Determine the Age of the Plant

Couple of decades ago, there had been numerous studies which illustrated that different miRNA families play role in regulating floral timing and development, by targeting transcription factors involved in these processes. At least 11 different miRNA families have been involved in regulating the induction of floral development at each stage. In plant miR156, miR172, and miR390 were involved during transition from juvenile to adult stage. Similarly, in transition from vegetative to reproductive stage, miR159, miR169, miR172, and miR399 were involved. A large group of miRNAs, including; miR159, miR160, miR164, miR166/5, miR167, miR169, miR172, and miR319 regulate flower development stage.

miRNA and AP2: Regulate Floral and Nodule Formation

In Arabidopsis, miRNA172 targeted mRNA of a floral homeotic gene AP2 that involve in floral development. Unlike most plant miRNAs which mostly turn off their own targets by cleavage, miR172 regulate its target via translational inhibition. Prominent miRNA172 accumulation causes defect in floral organ identity, which looks similar to those loss-of-function ap2 mutants. High levels of mutant ap2 mRNA with disrupted base for miR172 base pairing resulted floral pattern defects.

In common beans and soybean miR172 and its target; AP2, involved in nodule formation. Nodulation occurs when plant roots establish a symbiotic relationship with nitrogen-fixing bacteria (rhizobia) to obtain nitrogen. Rhizobial infection on bean caused the expression level of miR172c to increase until during nodule development stage, while uninfected nodules show low level of miR172c and high level of AP2. In addition, overexpression of miR172c resulted in enhanced root growth, improved rhizobial infection, improved expression of early nodulation and autoregulation of nodulation genes, and improved nodulation and nitrogen uptake.

miRNA and SPL: Regulate Plant Transition From Juvenile to Adult

In Arabidopsis, SPL gene family is a well evident target of miR156. Out of 17 SPL genes, 11 have been reported as downregulated by miR156 through mRNA cleavage and translational inhibition. A reduced level of miR156 over time with increasing plant age, resulted in increased expression level of SPL transcription factors which induced flowering through the activation of FT, LFY, and MADS-box gene. In contrast, overexpressing miR156 in transgenic plant resulted delayed flowering and extended juvenile phase. Interestingly, miR156 was downregulated when temperature was increased by elevated carbon dioxide concentration. miR156 have conserved role in regulating flowering in rice, tomato, and maize.

miRNA and TCP: Regulate Leaf Morphogenesis

In Arabidopsis, role of TCPs and their regulation by miR319 was first identified using microarray in jaw-D mutants. Overexpressing miR319 in Arabidopsis mutants delayed the flowering phenotype in long day conditions. Late-flowering phenotype was observed due to loss-of-function; where miR319 had targeted TCP4. Another functional analysis revealed that loss-of-function of miR319, which was regulating TCP genes, led to slightly increase in the leaves size. Additionally, misexpression of tissue-specific promoters at later stages of leaf development had significantly reduced the leaf size in Arabidopsis. Beside, miRNA319 targeted TCPs which involved in regulation of KNOTTED1-Like HOMEOBOX (KNOX) genes, BREVIPEDICELLUS (BP) and KNAT2 through ASYMMETRIC LEAVES 2 (AS2) which can affect the leaf morphogenesis. Recent study reported that TCP transcription factor was regulated by RABBIT EARS (RBE) during leaf development. In tomato, overexpression of miR319 resulted into formation of a giant tomato leaf.

Interaction Between miR159-MYB and miR319-TCP

In model plant, Arabidopsis, miR159 and miR319 targeted the MYB and TCP transcription factors, respectively. Interestingly, both miRNA-target nodes had abilities to regulate miR167 and the target, ARF6/ARF8 node. The direct interaction of MYB and TCP transcription factor may contribute to the functional redundancy. Regardless of high sequence similarity of these miRNAs, the regulation of target TCP and MYB transcripts remain conserved for each miRNA families. Although, miR319 was able to bind MYB transcripts, but it exhibited an incomplete temporal and spatial expression pattern corresponding to miR159. On the other hand, miR159 was unable to bind TCP transcripts. This unique interaction suggested that miR159 and miR319 were able to perform different regulatory roles in plant development.

miRNA and NAC: Regulate Lateral Root Formation

Previous evidences suggested that NAC TFs could enhance lateral root development. In Arabidopsis, endogenous and transgenic NAC1 transcript were cleavaged by miR164, producing a 39 nucleotide long specific fragments. However, the action of miR164 was blocked by NAC1 mutations that interrupted the base pairing with miR164. Arabidopsis mir164a and mir164b mutant plants had reduced miR164 expression, thus upregulated NAC1 transcript level, resulting to more lateral roots as compared to wild type plants. Overexpression of ZmNAC1 in transgenic Arabidopsis had enhanced lateral roots formation in comparison to the wild type plant.

miRNA and GRF: Regulate Leaf Morphogenesis, Stem Cell Development, and Grain Filling

In Arabidopsis, miR396a and miR396b were involved in regulating the leaf morphology by targeting GRF TFs family. Liu and his colleagues, using northern blot hybridizations approach, found that miR396 was predominantly expressed in leaf and seedling. Overexpression of miR396a or miR396b in Arabidopsis resulted into a phenotype with narrow leaves, which probably was due to decreased in cell numbers. The overexpression of miR396 had also led to suppression of six GRF genes and GIF1 which acted as key players in cell division in leaves. Additionally, the overexpression of miR396 resulted in reduced stomata density, a feature that favors drought tolerance in plants. Moreover, additional target for miR396 had been identified which were basic Helix-Loop-Helix (bHLH74) TF, required for Arabidopsis normal growth and development. Further, in Populus trichocarpa, precursor of the miR396c, which possess mature sequence identical to miR396b in Arabidopsis, was expressed in tobacco plant using CaMV35S promoter. The transgenic plant exhibited altered organ development, where the third and fourth whorls were turned into stigmatoid anthers and fasciated carpels and delayed the flower development process.

Recent findings has discovered that miR396 and GRF regulatory network may regulates the transition of stem cells which are located at specific cellular context or stem cell niche (SCN) to transit-amplifying cells (TACs) in the Arabidopsis root meristem. In SCN, miR396 is expressed, but in TACs GRFs are expressed. The GRFs are essential for the function of the TACs. Low expression level of GRFs in TACs resulted in a low rate of the cell cycle. Additionally, it would affect TACs by generating periclinal cell divisions typical of stem cells. In opposite, the regulation of miR396 is required to repress the GRFs from the SCN.

In maize, in an attempt was carried out to explore the profile changes profiles of miR396 and GRF TF and also to analyze their potential regulatory roles during maize effective grain filling period. RNA sequencing was carried out in developing maize. It was observed that miR396 was highly expressed at initial stages, and gradually declined during later grain filling stages. By contrast, its target GRF TF was initially negatively regulated, decreased at the beginning, but increased continuously at later stages. Further analysis of expression pattern provide the information that other miRNAs like miR319, miR166, and RNA dependent RNA polymerase may involve in the interaction between miR396 and GRF TF during grain development in maize. Similar study was carried out in rice, where LOC_Os02g47280, which is responsible for grain shape, was downregulated by miR396. The evidences obtained from A. thaliana, Zea mays, and O. sativa clearly support that networking between miR396 and GRF TF plays an important role in plant leaf growth and grain development.

miRNA and HD-Zip: Regulate Shoot Apical Meristem and Vascular Patterning Development

Among four classes of HD-Zip TFs, the interaction of HD-Zip III with miRNA families, 165 and 166, has been well studied. In Arabidopsis, an overexpression of miR166 had downregulated three HD-ZIP III genes; ATHB-9/PHV, ATHB-14/PHB, and ATHB-15, resulting in recapitulate phenotypes. The same phenotype was also observed in loss-of-function mutations of these genes. Similarly, overexpression of miR165 had turned off all five HD-ZIP III genes, which led to recapitulated phenotypes caused by loss-of-function of mutations of hd-zip III genes, such as loss of shoot apical meristem (SAM), changed in organ polarity and defects in vascular tissues development and inter fascicular fibers. Beside, miR165 and miR166 were also reported to regulate SAM and floral development through WUSCHEL (WUS)-CLAVATA (CLV) pathway. Although miR165 and miR166 target the same genes, individual miR165 and miR166 display different expression domains in different part of plant tissues. For instances, overexpression of miR165 and miR166 plant resulted in the alterations in SAM activities and floral formation.

Additionally, in both Arabidopsis and maize, miR165 and 166 were observed with abundance on the abaxial side of leaf, and in developing phloem of the leaf primordium, since both miRNAs play critical role in leaf asymmetry patterning. Adaxialization and overexpression of the rolled leaf1 gene occur when miRNA target site of a REV homolog was mutated in maize rolled leaf1 (rld1) mutant. Hence, in both eudicots and monocots, HD-ZIP III which is responsible for vascular patterning of leaves and stems has been suppressed by miRNA from abaxial domains.

miRNAs Under Stress Response

MicroRNAs and TFs are the gene regulators which play an important role under biotic and abiotic stresses in plant. In this section, we have summarized latest information on the interaction between miRNAs and TFs under biotic and abiotic stresses and their effect on phenotypic and physiological changes in plants.

miRNA and NY-FA: Contribute Drought Resistance

In Arabidopsis, interaction between miR169 and NF-YA transcription factor regulates the drought tolerance. Coexpression of miR169 members and NFYA5 revealed that miR169a was more effective than miR169c in suppressing the NFYA5 at mRNA level. Arabidopsis nfya5 mutants and transgenic plants overexpressing miR169a showed more susceptibility toward drought as compared to wild type plants. In contrast, overexpression of NFYA5, resulted plants with enhanced drought tolerance. However, during salinity stress, miR169 was significantly induced which halted the expression of nfya5 in Arabidopsis. In addition, ABA treatment to the Arabidopsis had significantly induced NFYA5 TF and caused the downregulated of miR169 level.

miRNA and MYB: Involved in Flavonoid Biosynthesis Pathway and Response to High Temperature

A study had been carried out to functionally characterized miR858a in Arabidopsis. The miR858a, which putatively targets R2R3-MYB transcription factors involved in flavonoid biosynthesis. Overexpression of miR858a in Arabidopsis resulted in the downregulation of several MYB TFs involved in flavonoid biosynthesis pathway, hence decrease the flavonoid production. In contrast, knockdown of miR858a by target mimic led to plant growth reduction and delayed flowering.

In cotton, MYB TF was found to be upregulated in response to high temperature. Like the previous study, MYB TF was targeted by miR828a and miR858. From this finding, we suggest MYB TF and miR828 and miR858 may have dual role in cotton, during fiber development and adaptation against high temperature.

miRNA and WRKY: Response to High Temperature

In sunflower, when plant exposed to high temperatures, a WRKY TF (HaWRKY6) exhibited inverse correlation with miR396. High level of miR396 was observed in older leaves in contrast to the distal portion where the expression was low. In rice treated with arsenic, miR396 was downregulated which resulted in the upregulation of its target, WRKY TF. Currently, as per our knowledge, no functional study involving the overexpression or loss-of-function of miRNA and WRKY TF has been carried out.

miRNA and TCP: Regulate Jasmonic Acid Biosynthesis

Last decade, a combination of genome-wide, biochemical and genetic studies discovered TCP were responsible for the jasmonic acid biosynthesis. Leaf extracts analysis from plants with high activity of miR319 regulate the expression of the biosynthetic genes, which subsequently led to change in jasmonic acid levels. Moreover, recent finding demonstrated that root-knot nematode (RKN) resistance in tomato was established by using reverse genetic approaches in the interaction of miR319 and TCP4. These interactions affected both jasmonic acid synthetic genes and the endogenous jasmonic acid level in leaves. These finding suggest that the negative interaction between miR319 and TCP4 acted as a systemic signal responder and regulator that modulated the systemic defensive response, mediated via jasmonic acid responsive to RKN.

miRNA and NAC: Regulate Drought Resistance and Contribute Resistance Against Fungus

The interaction between miR164 and NAC TF is well known in developmental process in Arabidopsis. In addition to that, miR164 and NAC TFs play an important role in regulating drought resistance in rice; where overexpression of miR164 against NAC TFs led to susceptibility toward drought.

In wheat, interaction between miR164 and novel TF NAC21/22 was confirmed experimentally via co-transformation of both genes in tobacco leaves. Transcript accumulation of NAC21/22 and miR164 exhibited contrasting expression patterns in wheat response to Puccinia striiformis f. sp. tritici (Pst). Silencing of the NAC21/22 showed reduced stripe rust resistance in wheat. These results indicate that the target of miR164 is a novel NAC TF from wheat and plays an essential role in developing stripe rust resistance in host plants.

miRNA as Secondary Metabolite Regulator

Gathering all information above, interaction between miRNAs and TFs will help in understanding the regulatory networks influenced directly by these regulators and cross talking between various biological processes in plants. As miRNAs has been found to be related in secondary metabolite regulation which need to be further explored. In Arabidopsis, the interaction between miR156 and SPL resulted in the negative regulation of anthocyanin biosynthesis. Moreover, in Arabidopsis, loss-of-function of miR163 also led to the accumulation of methyl farnesoate. miR163 also found to regulate another mRNA encoding S-adenosylmethionine dependent methyltransferases that is responsible for methylation of secondary metabolites and different signaling molecules.

In opium, miR13, miR2161, and miR408 were involved in indole alkaloid biosynthesis. In medicinal herb, Picrorhiza kurroa, miR4995 was involved in the regulation of terpenoid biosynthesis. These interactions can be utilized as a tool to enhance secondary metabolite production either by overexpressing miRNA or transcription factor. Other approach can be the knockdown of miRNA/TF which interfere in the secondary metabolite production. In Persicaria minor plant, an interaction among different miRNAs and TFs investigated. For instance, the targets of miR156 and miR172 (SPL and AP2) were downregulated, whereas targets of miR858 and miR894 (MYB and WRKY) were upregulated under elicitation by Fusarium oxysporum. These finding supported the previous studies; especially, in model plant where the TFs that played role in defense mechanism were upregulated while those TFs which mostly involved in plant development were downregulated by miRNA under stress condition.

Artificial miRNA (amiRNA) for Secondary Metabolites and Disease Resistance in Plants

One of the most important global issues is food security to ensure everyone living in this globe can access sufficient food. Since world population is increasing on an alarming rate every effort must be taken in account to obtain higher food production. Genetic modification technology based on miRNA and TFs approaches, can be one of the solutions that contribute to crop yields directly by developing superior plants which can survive under environmental stresses, with high yield and nutrients. This technology will also promote a healthy environment due to less pesticide usage, and this reduced pesticide cost will be used to elevate the living standard of the poor agricultural community across the globe.

After the breakthrough of miRNA discovery, extensive studies had been done which led to development of new version of miRNA called amiRNA. This approach utilize the unique stem-loop structure of endogenous pri-miRNAs, in which the miRNA/miRNA∗ duplex sequences are being replaced with amiRNA/amiRNA∗ sequences that direct the silencing of target gene with high efficiency. AmiRNA technique exhibited some advantages when compared with conventional RNA interference (RNAi), where amiRNA can be useful for targeting groups of closely related genes, including tandem arrayed and the prediction of gene targeted by amiRNA could be more precise. This approach was effectively used for the downregulation of Chalcone synthase genes in Arabidopsis.

Beside, amiRNA can be a new approach for developing pathogen tolerant plants, especially virus. T2 transgenic tomato plants expressing amiR-AV1-1 were highly tolerant to Tomato leaf curl New Delhi virus (ToLCNDV), while those plants expressing amiR-AV1-3 showed moderate tolerance. Moreover, recent study in cassava showed transgenic plants which carry four amiRNA challenged with Cassava brown streak virus (CBSV) and Ugandan cassava brown streak virus (UCBSV) isolates, showed resistance levels that ranged between ∼20 and 60%.

Conclusion and Remarks

In the present article, we have reviewed the regulatory relationships between miRNAs and various families of TFs like; NF-YA, MYB, AP2, TCP, WRKY, NAC, GRF, and SPL, from different plant species. The studied interactions between various miRNAs and above mentioned TFs have important roles during drought tolerance, signal transduction and biosynthesis of secondary metabolites, floral development and nodule formation, leaf development, multiple stresses tolerances, lateral root growth, and plant transition from juvenile to adult, respectively. Being the major gene regulators, miRNAs and TFs determine the phenotype, physiology and response to various environmental stresses. Our current review, with lots of newly developed relations between different miRNAs and TFs, will help plant scientists to develop plants with desired phenotypes and stress tolerance ability against particular stress. The plants with stresses tolerance will help to secure the food production for the ever increasing world population. Moreover, some studied interactions have important role in regulation of secondary metabolites biosynthesis and can be used as tool for the production of plant based medicinal biomolecules.

Author Contributions

The first version of this manuscript was written by AS, MS, NN, and IF. AM, ZZ, and II revised the manuscript and advised the writing style. All authors made substantial contribution and approved the final version of the manuscript.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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    Li J. Han S. Ding X. He T. Dai J. Yang S. (2015 ). Comparative transcriptome analysis between the cytoplasmic male sterile line NJCMS1A and its maintainer NJCMS1B in soybean (Glycine max (L.) Merr.). PLoS ONE 10:e0126771

    Not in our library10.1371/journal.pone.0126771

  102. 102.

    Li J. Wang Y. Zhang Y. Wang W. Irish V. F. Huang T. (2016 ). RABBIT EARS regulates the transcription of TCP4 during petal development in Arabidopsis. J. Exp. Bot. 67 6473–6480.

    Not in our library10.1093/jxb/erw419

  103. 103.

    Li S. (2015 ). The Arabidopsis thaliana TCP transcription factors: a broadening horizon beyond development. Plant Signal. Behav. 10:e1044192

    Not in our library10.1080/15592324.2015.1044192

  104. 104.

    Li S. Liu L. Zhuang X. Yu Y. Liu X. Cui X. (2013 ). microRNAs inhibit the translation of target mRNAs on the endoplasmic reticulum in Arabidopsis. Cell 153 562–574.

    Not in our library10.1016/j.cell.2013.04.005

  105. 105.

    Li W. X. Oono Y. Zhu J. He X. J. Wu J. M. Iida K. (2008 ). The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell 20 2238–2251.

    Not in our library10.1105/tpc.108.059444

  106. 106.

    Li Z. Li B. Shen W.-H. Huang H. Dong A. (2012 ). TCP transcription factors interact with AS2 in the repression of class-I KNOX genes in Arabidopsis thaliana. Plant J. 71 99–107.

    Not in our library10.1111/j.1365-313x.2012.04973.x

  107. 107.

    Liao W. Yang Y. Li Y. Wang G. Peng M. (2016 ). Genome-wide identification of cassava R2R3 MYB family genes related to abscission zone separation after environmental-stress-induced abscission. Sci. Rep. 6:32006

    Not in our library10.1038/srep32006

  108. 108.

    Lindemose S. Jensen M. K. de Velde J. V. O’Shea C. Heyndrickx K. S. Workman C. T. (2014 ). A DNA-binding-site landscape and regulatory network analysis for NAC transcription factors in Arabidopsis thaliana. Nucleic Acids Res. 42 7681–7693.

    Not in our library10.1093/nar/gku502

  109. 109.

    Liu D. Song Y. Chen Z. Yu D. (2009 ). Ectopic expression of miR396 suppresses GRF target gene expression and alters leaf growth in Arabidopsis. Physiol. Plant. 136 223–236.

    Not in our library10.1111/j.1399-3054.2009.01229.x

  110. 110.

    Liu J. Osbourn A. Ma P. (2015 ). MYB transcription factors as regulators of phenylpropanoid metabolism in plants. Mol. Plant 8 689–708.

    Not in our library10.1016/j.molp.2015.03.012

  111. 111.

    Liu L. Du H. Tang X. F. Wu Y. M. Huang Y. B. Tang Y. X. (2008 ). [The roles of MYB transcription factors on plant defense responses and its molecular mechanism.]. Yi Chuan 30 1265–1271.

    Not in our library10.3724/sp.j.1005.2008.01265

  112. 112.

    Liu L. White M. J. MacRae T. H. (1999 ). Transcription factors and their genes in higher plants functional domains, evolution and regulation. Eur. J. Biochem. 262 247–257.

    Not in our library10.1046/j.1432-1327.1999.00349.x

  113. 113.

    Liu Q. Zhang H. (2012 ). Molecular identification and analysis of arsenite stress-responsive miRNAs in rice. J. Agric. Food Chem. 60 6524–6536.

    Not in our library10.1021/jf300724t

  114. 114.

    Liu Z. Gu C. Chen F. Jiang J. Yang Y. Li P. (2012 ). Identification and expression of an APETALA2-Like gene from Nelumbo nucifera. Appl. Biochem. Biotechnol. 168 383–391.

    Not in our library10.1007/s12010-012-9782-9

  115. 115.

    Luo Y. Guo Z. Li L. (2013 ). Evolutionary conservation of microRNA regulatory programs in plant flower development. Dev. Biol. 380 133–144.

    Not in our library10.1016/j.ydbio.2013.05.009

  116. 116.

    Lv D. K. Bai X. Li Y. Ding X. D. Ge Y. Cai H. (2010 ). Profiling of cold-stress-responsive miRNAs in rice by microarrays. Gene 459 39–47.

    Not in our library10.1016/j.gene.2010.03.011

  117. 117.

    Ly L. L. Yoshida H. Yamaguchi M. (2013 ). Nuclear transcription factor Y and its roles in cellular processes related to human disease. Am. J. Cancer Res. 3 339–346.

    Not in our library

  118. 118.

    Ma J. Wang Q. Sun R. Xie F. Jones D. C. Zhang B. (2014 ). Genome-wide identification and expression analysis of TCP transcription factors in Gossypium raimondii. Sci. Rep. 4:6645

    Not in our library10.1038/srep06645

  119. 119.

    Ma X. Tang Z. Qin J. Meng Y. (2015 ). The use of high-throughput sequencing methods for plant microRNA research. RNA Biol. 12 709–719.

    Not in our library10.1080/15476286.2015.1053686

  120. 120.

    Maizel A. Weigel D. (2004 ). Temporally and spatially controlled induction of gene expression in Arabidopsis thaliana. Plant J. 38 164–171.

    Not in our library10.1111/j.1365-313x.2004.02027.x

  121. 121.
    TCP transcription factors: architectures of plant form · 2013
    Not checked
  122. 122.

    Mao H. Yu L. Li Z. Liu H. Han R. (2016 ). Molecular evolution and gene expression differences within the HD-Zip transcription factor family of Zea mays L. Genetica 144 243–257.

    Not in our library10.1007/s10709-016-9896-z

  123. 123.

    Maunoury N. Vaucheret H. (2011 ). AGO1 and AGO2 act redundantly in miR408-mediated Plantacyanin regulation. PLoS ONE 6:e28729

    Not in our library10.1371/journal.pone.0028729

  124. 124.

    May P. Liao W. Wu Y. Shuai B. Richard McCombie W. Zhang M. Q. (2013 ). The effects of carbon dioxide and temperature on microRNA expression in Arabidopsis development. Nat. Commun. 4 2145

    Not in our library10.1038/ncomms3145

  125. 125.

    Meng Y. Shao C. Chen M. (2011 ). Toward microRNA-mediated gene regulatory networks in plants. Brief. Bioinform. 12 645–659.

    Not in our library10.1093/bib/bbq091

  126. 126.
    Overexpression of Arabidopsis thaliana ERI, the homolog of C. elegans Enhancer of RNAinterference, leads to enhanced growth · 2015
    Not checked
  127. 127.

    Mitsuda N. Ohme-Takagi M. (2009 ). Functional analysis of transcription factors in Arabidopsis. Plant Cell Physiol. 50 1232–1248.

    Not in our library10.1093/pcp/pcp075

  128. 128.

    Mittler R. (2006 ). Abiotic stress, the field environment and stress combination. Trends Plant Sci. 11 15–19.

    Not in our library10.1016/j.tplants.2005.11.002

  129. 129.
    Structural basis for the recognition of guide RNA and target DNA heteroduplex by Argonaute · 2016
    No notice
  130. 130.

    Mlotshwa S. Yang Z. Kim Y. Chen X. (2006 ). Floral patterning defects induced by Arabidopsis APETALA2 and microRNA172 expression in Nicotiana benthamiana. Plant Mol. Biol. 61 781–793.

    Not in our library10.1007/s11103-006-0049-0

  131. 131.

    Morris K. V. Mattick J. S. (2014 ). The rise of regulatory RNA. Nat. Rev. Genet. 15 423–437.

    Not in our library10.1038/nrg3722

  132. 132.

    Mutum R. D. Kumar S. Balyan S. Kansal S. Mathur S. Raghuvanshi S. (2016 ). Identification of novel miRNAs from drought tolerant rice variety Nagina 22. Sci. Rep. 6:30786

    Not in our library10.1038/srep30786

  133. 133.
    NUCLEAR FACTOR Y, Subunit C (NF-YC) Transcription Factors Are Positive Regulators of Photomorphogenesis in Arabidopsis thaliana. · 2016
    Not checked
  134. 134.

    Naeem H. Kuffner R. Zimmer R. (2011 ). MIRTFnet: analysis of miRNA regulated transcription factors. PLoS ONE 6:e22519

    Not in our library10.1371/journal.pone.0022519

  135. 135.

    Nag A. King S. Jack T. (2009 ). miR319a targeting of TCP4 is critical for petal growth and development in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 106 22534–22539.

    Not in our library10.1073/pnas.0908718106

  136. 136.

    Nazarov P. V. Reinsbach S. E. Muller A. Nicot N. Philippidou D. Vallar L. (2013 ). Interplay of microRNAs, transcription factors and target genes: linking dynamic expression changes to function. Nucleic Acids Res. 41 2817–2831.

    Not in our library10.1093/nar/gks1471

  137. 137.

    Ng D. W. Zhang C. Miller M. Palmer G. Whiteley M. Tholl D. (2011 ). cis- and trans-Regulation of miR163 and target genes confers natural variation of secondary metabolites in two Arabidopsis species and their allopolyploids. Plant Cell 23 1729–1740.

    Not in our library10.1105/tpc.111.083915

  138. 138.

    Nguyen N. H. Lee H. (2016 ). MYB-related transcription factors function as regulators of the circadian clock and anthocyanin biosynthesis in Arabidopsis. Plant Signal. Behav. 11:e1139278

    Not in our library10.1080/15592324.2016.1139278

  139. 139.

    Niemeier S. Alves Junior L. Merkle T. (2010 ). Improvement of the design and generation of highly specific plant knockdown lines using primary synthetic microRNAs (pri-smiRNAs). BMC Res Notes 3:59

    Not in our library10.1186/1756-0500-3-59

  140. 140.

    Nova-Franco B. Íñiguez L. P. Valdés-López O. Alvarado-Affantranger X. Leija A. Fuentes S. I. (2015 ). The Micro-RNA172c-APETALA2-1 node as a key regulator of the common bean-Rhizobium etli Nitrogen Fixation Symbiosis. Plant Physiol. 168 273–291.

    Not in our library10.1104/pp.114.255547

  141. 141.

    Olsen A. N. Ernst H. A. Leggio L. L. Skriver K. (2005 ). NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci. 10 79–87.

    Not in our library10.1016/j.tplants.2004.12.010

  142. 142.

    Omidbakhshfard M. A. Proost S. Fujikura U. Mueller-Roeber B. (2015 ). Growth-Regulating Factors (GRFs): a small transcription factor family with important functions in plant biology. Mol. Plant 8 998–1010.

    Not in our library10.1016/j.molp.2015.01.013

  143. 143.

    Orenstein Y. Shamir R. (2016 ). Modeling protein–DNA binding via high-throughput in vitro technologies. Brief. Funct. Genomics [Epub ahead of print].

    Not in our library10.1093/bfgp/elw030

  144. 144.

    Ori N. Cohen A. R. Etzioni A. Brand A. Yanai O. Shleizer S. (2007 ). Regulation of LANCEOLATE by miR319 is required for compound-leaf development in tomato. Nat. Genet. 39 787–791.

    Not in our library10.1038/ng2036

  145. 145.

    Osorio J. (2016 ). Gene regulation: landscape and mechanisms of transcription factor cooperativity. Nat. Rev. Genet. 17 5

    Not in our library10.1038/nrg.2015.11

  146. 146.

    Ossowski S. Schwab R. Weigel D. (2008 ). Gene silencing in plants using artificial microRNAs and other small RNAs. Plant J. 53 674–690.

    Not in our library10.1111/j.1365-313x.2007.03328.x

  147. 147.

    Padi M. Quackenbush J. (2015 ). Integrating transcriptional and protein interaction networks to prioritize condition-specific master regulators. BMC Syst. Biol. 9 80

    Not in our library10.1186/s12918-015-0228-1

  148. 148.

    Palatnik J. F. Wollmann H. Schommer C. Schwab R. Boisbouvier J. Rodriguez R. (2007 ). Sequence and expression differences underlie functional specialization of Arabidopsis microRNAs miR159 and miR319. Dev. Cell 13 115–125.

    Not in our library10.1016/j.devcel.2007.04.012

  149. 149.

    Pandey A. Misra P. Bhambhani S. Bhatia C. Trivedi P. K. (2014 ). Expression of Arabidopsis MYB transcription factor, AtMYB111, in tobacco requires light to modulate flavonol content. Sci. Rep. 4:5018

    Not in our library10.1038/srep05018

  150. 150.
    Identification, cloning and characterization of the tomato TCP transcription factor family · 2014
    No notice
  151. 151.

    Park J. H. Shin C. (2014 ). MicroRNA-directed cleavage of targets: mechanism and experimental approaches. BMB Rep. 47 417–423.

    Not in our library10.5483/bmbrep.2014.47.8.109

  152. 152.
    Mechanisms of Mutational Robustness in Transcriptional Regulation · 2015
    Not checked
  153. 153.

    Pecenova L. Farkas R. (2016 ). Multiple functions and essential roles of nuclear receptor coactivators of bHLH-PAS family. Endocr. Regul. 50 165–181.

    Not in our library10.1515/enr-2016-0019

  154. 154.

    Pelaz S. Ditta G. S. Baumann E. Wisman E. Yanofsky M. F. (2000 ). B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405 200–203.

    Not in our library10.1038/35012103

  155. 155.

    Petroni K. Kumimoto R. W. Gnesutta N. Calvenzani V. Fornari M. Tonelli C. (2012 ). The Promiscuous life of plant NUCLEAR FACTOR Y transcription factors. Plant Cell 24 4777–4792.

    Not in our library10.1105/tpc.112.105734

  156. 156.
    WRKY Transcription Factors: Molecular Regulation and Stress Responses in Plants · 2016
    No notice
  157. 157.

    Pireyre M. Burow M. (2015 ). Regulation of MYB and bHLH transcription factors: a glance at the protein level. Mol. Plant 8 378–388.

    Not in our library10.1016/j.molp.2014.11.022

  158. 158.

    Raffaele S. Rivas S. Roby D. (2006 ). An essential role for salicylic acid in AtMYB30-mediated control of the hypersensitive cell death program in Arabidopsis. FEBS Lett. 580 3498–3504.

    Not in our library10.1016/j.febslet.2006.05.027

  159. 159.

    Ramachandran P. Carlsbecker A. Etchells J. P. (2016 ). Class III HD-ZIPs govern vascular cell fate: an HD view on patterning and differentiation. J. Exp. Bot. 68 55–69.

    Not in our library10.1093/jxb/erw370

  160. 160.

    Ramachandran V. Chen X. (2008 ). Degradation of microRNAs by a family of exoribonucleases in Arabidopsis. Science 321 1490–1492.

    Not in our library10.1126/science.1163728

  161. 161.

    Ren C. Zhang Z. Wang Y. Li S. Liang Z. (2016 ). Genome-wide identification and characterization of the NF-Y gene family in grape (vitis vinifera L.). BMC Genomics 17:605

    Not in our library10.1186/s12864-016-2989-3

  162. 162.

    Reyes J. L. Chua N.-H. (2007 ). ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. Plant J. 49 592–606.

    Not in our library10.1111/j.1365-313x.2006.02980.x

  163. 163.

    Rhoades M. Reinhart B. Lim L. Burge C. Bartel B. Bartel D. (2002 ). Prediction of plant microRNA targets. Cell 110 513–520.

    Not in our library10.1016/s0092-8674(02)00863-2

  164. 164.
    The evolution of WRKY transcription factors · 2015
    No notice
  165. 165.

    Rodriguez R. E. Ercoli M. F. Debernardi J. M. Breakfield N. W. Mecchia M. A. Sabatini M. (2015 ). MicroRNA miR396 regulates the switch between stem cells and transit-amplifying cells in Arabidopsis Roots. Plant Cell 27 3354–3366.

    Not in our library10.1105/tpc.15.00452

  166. 166.

    Rogers K. Chen X. (2013 ). Biogenesis, turnover, and mode of action of plant MicroRNAs. Plant Cell 25 2383–2399.

    Not in our library10.1105/tpc.113.113159

  167. 167.

    Roy S. (2016 ). Function of MYB domain transcription factors in abiotic stress and epigenetic control of stress response in plant genome. Plant Signal. Behav. 11:e1117723

    Not in our library10.1080/15592324.2015.1117723

  168. 168.

    Rubio-Somoza I. Weigel D. (2013 ). Coordination of flower maturation by a regulatory circuit of three microRNAs. PLoS Genet. 9:e1003374

    Not in our library10.1371/journal.pgen.1003374

  169. 169.

    Salih H. Gong W. He S. Sun G. Sun J. Du X. (2016 ). Genome-wide characterization and expression analysis of MYB transcription factors in Gossypium hirsutum. BMC Genet. 17:129

    Not in our library10.1186/s12863-016-0436-8

  170. 170.

    Samad A. F. A. Ali N. M. Ismail I. Murad A. M. A. (2016 ). Analysis of miRNAs targeting transcription factors in Persicaria minor induced by Fusarium oxysporum. AIP Conf. Proc. 1784 020009

    Not in our library10.1063/1.4966719

  171. 171.

    Sarvepalli K. Nath U. (2011 ). Hyper-activation of the TCP4 transcription factor in Arabidopsis thaliana accelerates multiple aspects of plant maturation. Plant J. 67 595–607.

    Not in our library10.1111/j.1365-313x.2011.04616.x

  172. 172.

    Sasaki T. Suzaki T. Soyano T. Kojima M. Sakakibara H. Kawaguchi M. (2014 ). Shoot-derived cytokinins systemically regulate root nodulation. Nat. Commun. 5 4983

    Not in our library10.1038/ncomms5983

  173. 173.

    Schommer C. Bresso E. G. Spinelli S. V. Palatnik J. F. (2012 ). “Role of MicroRNA miR319 in plant development,” in MicroRNAs in Plant Development and Stress Responses ed. Sunkar R. (Berlin: Springer) 29-47.

    Not in our library

  174. 174.
    Control of Jasmonate Biosynthesis and Senescence by miR319 Targets · 2008
    No notice
  175. 175.

    Schwab R. Ossowski S. Riester M. Warthmann N. Weigel D. (2006 ). Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18 1121–1133.

    Not in our library10.1105/tpc.105.039834

  176. 176.

    Shao C. Dong A.-W. Ma X. Meng Y. (2014 ). Is Argonaute 1 the only effective slicer of small RNA-mediated regulation of gene expression in plants? J. Exp. Bot. 65 6293–6299.

    Not in our library10.1093/jxb/eru382

  177. 177.

    Sharma D. Tiwari M. Pandey A. Bhatia C. Sharma A. Trivedi P. K. (2016 ). MicroRNA858 is a potential regulator of phenylpropanoid pathway and plant development in Arabidopsis. Plant Physiol. 171 944–959.

    Not in our library10.1104/pp.15.01831

  178. 178.

    Sharma N. Bhalla P. L. Singh M. B. (2013 ). Transcriptome-wide profiling and expression analysis of transcription factor families in a liverwort, Marchantia polymorpha. BMC Genomics 14:915

    Not in our library10.1186/1471-2164-14-915

  179. 179.

    Shiu S. H. Shih M. C. Li W. H. (2005 ). Transcription factor families have much higher expansion rates in plants than in animals. Plant Physiol. 139 18–26.

    Not in our library10.1104/pp.105.065110

  180. 180.
    MicroRNAs As Potential Targets for Abiotic Stress Tolerance in Plants · 2016
    No notice
  181. 181.

    Shu Y. Liu Y. Li W. Song L. Zhang J. Guo C. (2016 ). Genome-Wide Investigation of MicroRNAs and their targets in response to freezing stress in Medicago sativa L., based on high-throughput sequencing. G3 (Bethesda). 6 755–765.

    Not in our library10.1534/g3.115.025981

  182. 182.
    NUCLEAR FACTOR Y, Subunit A (NF-YA) Proteins Positively Regulate Flowering and Act Through FLOWERING LOCUS T. · 2016
    Not checked
  183. 183.

    Sorin C. Declerck M. Christ A. Blein T. Ma L. Lelandais-Briere C. (2014 ). A miR169 isoform regulates specific NF-YA targets and root architecture in Arabidopsis. New Phytol. 202 1197–1211.

    Not in our library10.1111/nph.12735

  184. 184.

    Spanudakis E. Jackson S. (2014 ). The role of microRNAs in the control of flowering time. J. Exp. Bot. 65 365–380.

    Not in our library10.1093/jxb/ert453

  185. 185.

    Suzaki T. Yoro E. Kawaguchi M. (2015 ). Leguminous plants: inventors of root nodules to accommodate symbiotic bacteria. Int. Rev. Cell Mol. Biol. 316 111–158.

    Not in our library10.1016/bs.ircmb.2015.01.004

  186. 186.

    Takahashi R. Yamagishi N. Yoshikawa N. (2013 ). A MYB transcription factor controls flower color in soybean. J. Hered. 104 149–153.

    Not in our library10.1093/jhered/ess081

  187. 187.

    Takeda T. Amano K. Ohto M. A. Nakamura K. Sato S. Kato T. (2006 ). RNA interference of the Arabidopsis putative transcription factor TCP16 gene results in abortion of early pollen development. Plant Mol. Biol. 61 165–177.

    Not in our library10.1007/s11103-006-6265-9

  188. 188.

    Tang M. Tao Y.-B. Fu Q. Song Y. Niu L. Xu Z.-F. (2016 ). An ortholog of LEAFY in Jatropha curcas regulates flowering time and floral organ development. Sci. Rep. 6:37306

    Not in our library10.1038/srep37306

  189. 189.

    Teotia S. Tang G. (2015 ). To bloom or not to bloom: role of MicroRNAs in plant flowering. Mol. Plant 8 359–377.

    Not in our library10.1016/j.molp.2014.12.018

  190. 190.

    Terzi L. C. Simpson G. G. (2008 ). Regulation of flowering time by RNA processing. Curr. Top. Microbiol. Immunol. 326 201–218.

    Not in our library10.1007/978-3-540-76776-3_11

  191. 191.

    Thomson D. W. Dinger M. E. (2016 ). Endogenous microRNA sponges: evidence and controversy. Nat. Rev. Genet. 17 272–283.

    Not in our library10.1038/nrg.2016.20

  192. 192.

    Turchi L. Baima S. Morelli G. Ruberti I. (2015 ). Interplay of HD-Zip II and III transcription factors in auxin-regulated plant development. J. Exp. Bot. 66 5043–5053.

    Not in our library10.1093/jxb/erv174

  193. 193.

    Vashisht I. Mishra P. Pal T. Chanumolu S. Singh T. R. Chauhan R. S. (2015 ). Mining NGS transcriptomes for miRNAs and dissecting their role in regulating growth, development, and secondary metabolites production in different organs of a medicinal herb, Picrorhiza kurroa. Planta 241 1255–1268.

    Not in our library10.1007/s00425-015-2255-y

  194. 194.

    Verdier J. Zhao J. Torres-Jerez I. Ge S. Liu C. He X. (2012 ). MtPAR MYB transcription factor acts as an on switch for proanthocyanidin biosynthesis in Medicago truncatula. Proc. Natl. Acad. Sci. U.S.A. 109 1766–1771.

    Not in our library10.1073/pnas.1120916109

  195. 195.

    Voinnet O. (2009 ). Origin, biogenesis, and activity of plant microRNAs. Cell 136 669–687.

    Not in our library10.1016/j.cell.2009.01.046

  196. 196.

    Vu T. V. Choudhury N. R. Mukherjee S. K. (2013 ). Transgenic tomato plants expressing artificial microRNAs for silencing the pre-coat and coat proteins of a begomovirus, Tomato leaf curl New Delhi virus, show tolerance to virus infection. Virus Res. 172 35–45.

    Not in our library10.1016/j.virusres.2012.12.008

  197. 197.

    Wagaba H. Patil B. L. Mukasa S. Alicai T. Fauquet C. M. Taylor N. J. (2016 ). Artificial microRNA-derived resistance to Cassava brown streak disease. J. Virol. Methods 231 38–43.

    Not in our library10.1016/j.jviromet.2016.02.004

  198. 198.

    Wang B. Geng S. Wang D. Feng N. Zhang D. Wu L. (2015 ). Characterization of squamosa promoter binding protein-LIKE genes in wheat. J. Plant Biol. 58 220–229.

    Not in our library10.1007/s12374-015-0105-x

  199. 199.

    Wang H. Avci U. Nakashima J. Hahn M. G. Chen F. Dixon R. A. (2010 ). Mutation of WRKY transcription factors initiates pith secondary wall formation and increases stem biomass in dicotyledonous plants. Proc. Natl. Acad. Sci. U.S.A. 107 22338–22343.

    Not in our library10.1073/pnas.1016436107

  200. 200.

    Wang H. Li G. B. Zhang D. Y. Lin J. Sheng B. L. Han J. L. (2013 ). [Biological functions of HD-Zip transcription factors]. Yi Chuan 35 1179–1188.

    Not in our library10.3724/sp.j.1005.2013.01179

  201. 201.
    Recent Advances in Utilizing Transcription Factors to Improve Plant Abiotic Stress Tolerance by Transgenic Technology · 2016
    No notice
  202. 202.

    Wang Q. Liu N. Yang X. Tu L. Zhang X. (2016 ). Small RNA-mediated responses to low- and high-temperature stresses in cotton. Sci. Rep. 6:35558

    Not in our library10.1038/srep35558

  203. 203.

    Wang Y. Lan Q. Zhao X. Xu W. Li F. Wang Q. (2016 ). Comparative profiling of microRNA expression in soybean seeds plants from genetically modified near their-isogenic parental lines. PLoS ONE 11:e0155896

    Not in our library10.1371/journal.pone.0155896

  204. 204.
    Coordination of plant mitochondrial biogenesis: keeping pace with cellular requirements. · 2014
    Not checked
  205. 205.

    Weng L. Bai X. Zhao F. Li R. Xiao H. (2016 ). Manipulation of flowering time and branching by overexpression of the tomato transcription factor SlZFP2. Plant Biotechnol. J. 14 2310–2321.

    Not in our library10.1111/pbi.12584

  206. 206.

    Wickramasinghe V. O. Andrews R. Ellis P. Langford C. Gurdon J. B. Stewart M. (2014 ). Selective nuclear export of specific classes of mRNA from mammalian nuclei is promoted by GANP. Nucleic Acids Res. 42 5059–5071.

    Not in our library10.1093/nar/gku095

  207. 207.

    Wickramasinghe V. O. Laskey R. A. (2015 ). Control of mammalian gene expression by selective mRNA export. Nat. Rev. Mol. Cell Biol. 16 431–442.

    Not in our library10.1038/nrm4010

  208. 208.

    Wollmann H. Mica E. Todesco M. Long J. A. Weigel D. (2010 ). On reconciling the interactions between APETALA2, miR172 and AGAMOUS with the ABC model of flower development. Development 137 3633–3642.

    Not in our library10.1242/dev.036673

  209. 209.

    Wong D. C. J. Schlechter R. Vannozzi A. Höll J. Hmmam I. Bogs J. (2016 ). A systems-oriented analysis of the grapevine R2R3-MYB transcription factor family uncovers new insights into the regulation of stilbene accumulation. DNA Res. [Epub ahead of print].

    Not in our library10.1093/dnares/dsw028

  210. 210.

    Wu G. Park M. Y. Conway S. R. Wang J.-W. Weigel D. Poethig R. S. (2009 ). The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138 750–759.

    Not in our library10.1016/j.cell.2009.06.031

  211. 211.

    Wu X. Ding D. Shi C. Xue Y. Zhang Z. Tang G. (2016 ). microRNA-dependent gene regulatory networks in maize leaf senescence. BMC Plant Biol. 16:73

    Not in our library10.1186/s12870-016-0755-y

  212. 212.
    Deep sequencing reveals important roles of microRNAs in response to drought and salinity stress in cotton · 2014
    No notice
  213. 213.

    Xie K. Wu C. Xiong L. (2006 ). Genomic organization, differential expression, and interaction of SQUAMOSA promoter-binding-like transcription factors and microRNA156 in rice. Plant Physiol. 142 280–293.

    Not in our library10.1104/pp.106.084475

  214. 214.

    Xie Q. Frugis G. Colgan D. Chua N. H. (2000 ). Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev. 14 3024–3036.

    Not in our library10.1101/gad.852200

  215. 215.
    Exploring potential new floral organ morphogenesis genes of Arabidopsis thaliana using systems biology approach · 2015
    Not checked
  216. 216.

    Yamaguchi A. Abe M. (2012 ). Regulation of reproductive development by non-coding RNA in Arabidopsis: to flower or not to flower. J. Plant Res. 125 693–704.

    Not in our library10.1007/s10265-012-0513-7

  217. 217.

    Yamaguchi A. Wu M. F. Yang L. Wu G. Poethig R. S. Wagner D. (2009 ). The microRNA-regulated SBP-Box transcription factor SPL3 is a direct upstream activator of LEAFY, FRUITFULL, and APETALA1. Dev. Cell 17 268–278.

    Not in our library10.1016/j.devcel.2009.06.007

  218. 218.

    Yamaguchi N. Jeong C. W. Nole-Wilson S. Krizek B. A. Wagner D. (2016 ). AINTEGUMENTA and AINTEGUMENTA-LIKE6/PLETHORA3 Induce LEAFY expression in response to auxin to promote the onset of flower formation in Arabidopsis. Plant Physiol. 170 283–293.

    Not in our library10.1104/pp.15.00969

  219. 219.

    Yamasaki K. Kigawa T. Inoue M. Tateno M. Yamasaki T. Yabuki T. (2004 ). A novel zinc-binding motif revealed by solution structures of DNA-binding domains of Arabidopsis SBP-family transcription factors. J. Mol. Biol. 337 49–63.

    Not in our library10.1016/j.jmb.2004.01.015

  220. 220.
    Transcriptome profile analysis of young floral buds of fertile and sterile plants from the self-pollinated offspring of the hybrid between novel restorer line NR1 and <it>Nsa</it> CMS line in <it>Brassica napus</it> · 2013
    Not checked
  221. 221.

    Yan Z. Hossain M. S. Wang J. Valdes-Lopez O. Liang Y. Libault M. (2013 ). miR172 regulates soybean nodulation. Mol. Plant Microbe Interact. 2 1371–1377.

    Not in our library10.1094/mpmi-04-13-0111-r

  222. 222.

    Yang J. Liu X. Xu B. Zhao N. Yang X. Zhang M. (2013 ). Identification of miRNAs and their targets using high-throughput sequencing and degradome analysis in cytoplasmic male-sterile and its maintainer fertile lines of Brassica juncea. BMC Genomics 14:9

    Not in our library10.1186/1471-2164-14-9

  223. 223.

    Yu H. Gerstein M. (2006 ). Genomic analysis of the hierarchical structure of regulatory networks. Proc. Natl. Acad. Sci. U.S.A. 103 14724–14731.

    Not in our library10.1073/pnas.0508637103

  224. 224.

    Zhang B. (2015 ). MicroRNA: a new target for improving plant tolerance to abiotic stress. J. Exp. Bot. 66 1749–1761.

    Not in our library10.1093/jxb/erv013

  225. 225.

    Zhang K. Shi X. Zhao X. Ding D. Tang J. Niu J. (2015 ). Investigation of miR396 and growth-regulating factor regulatory network in maize grain filling. Acta Physiol. Plant. 37 28

    Not in our library10.1007/s11738-014-1767-6

  226. 226.

    Zhang W. Sun P. He Q. Shu F. Wang J. Deng H. (2013 ). Fine mapping of GS2, a dominant gene for big grain rice. Crop J. 1 160–165.

    Not in our library10.1016/j.cj.2013.10.003

  227. 227.

    Zhang X. Dong J. Liu H. Wang J. Qi Y. Liang Z. (2016 ). Transcriptome sequencing in response to salicylic acid in Salvia miltiorrhiza. PLoS ONE 11:e0147849

    Not in our library10.1371/journal.pone.0147849

  228. 228.

    Zhang X. Zou Z. Zhang J. Zhang Y. Han Q. Hu T. (2011 ). Over-expression of sly-miR156a in tomato results in multiple vegetative and reproductive trait alterations and partial phenocopy of the sft mutant. FEBS Lett. 585 435–439.

    Not in our library10.1016/j.febslet.2010.12.036

  229. 229.

    Zhang Z. Zhang X. (2012 ). Argonautes compete for miR165/166 to regulate shoot apical meristem development. Curr. Opin. Plant Biol. 15 652–658.

    Not in our library10.1016/j.pbi.2012.05.007

  230. 230.

    Zhao L. Kim Y. Dinh T. T. Chen X. (2007 ). miR172 regulates stem cell fate and defines the inner boundary of APETALA3 and PISTILLATA expression domain in Arabidopsis floral meristems. Plant J. 51 840–849.

    Not in our library10.1111/j.1365-313x.2007.03181.x

  231. 231.

    Zhao W. Li Z. Fan J. Hu C. Yang R. Qi X. (2015 ). Identification of jasmonic acid-associated microRNAs and characterization of the regulatory roles of the miR319/TCP4 module under root-knot nematode stress in tomato. J. Exp. Bot. 66 4653–4667.

    Not in our library10.1093/jxb/erv238

  232. 232.

    Zhong R. Ye Z.-H. (2007 ). Regulation of HD-ZIP III Genes by MicroRNA 165. Plant Signal. Behav. 2 351–353.

    Not in our library10.4161/psb.2.5.4119

  233. 233.

    Zhou C. M. Wang J. W. (2013 ). Regulation of flowering time by MicroRNAs. J. Genet. Genomics 40 211–215.

    Not in our library10.1016/j.jgg.2012.12.003

  234. 234.

    Zhou G. K. Kubo M. Zhong R. Demura T. Ye Z. H. (2007 ). Overexpression of miR165 affects apical meristem formation, organ polarity establishment and vascular development in Arabidopsis. Plant Cell Physiol. 48 391–404.

    Not in our library10.1093/pcp/pcm008

  235. 235.

    Zhu H. Hu F. Wang R. Zhou X. Sze S. H. Liou L. W. (2011 ). Arabidopsis Argonaute10 specifically sequesters miR166/165 to regulate shoot apical meristem development. Cell 145 242–256.

    Not in our library10.1016/j.cell.2011.03.024

  236. 236.

    Zhu Q. H. Helliwell C. A. (2011 ). Regulation of flowering time and floral patterning by miR172. J. Exp. Bot. 62 487–495.

    Not in our library10.1093/jxb/erq295

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