Next Article in Journal
Transcriptomic and Metabolic Profiling Reveals a Lignin Metabolism Network Involved in Mesocotyl Elongation during Maize Seed Germination
Next Article in Special Issue
Characteristics of Sunburn Browning Fruit and Rootstock-Dependent Damage-Free Yield of Ambrosia™ Apple after Sustained Summer Heat Events
Previous Article in Journal
Smilax weniae, a New Species of Smilacaceae from Limestone Areas Bordering Guizhou and Guangxi, China
Previous Article in Special Issue
The Photosynthetic Efficiency and Carbohydrates Responses of Six Edamame (Glycine max. L. Merrill) Cultivars under Drought Stress
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:

Epitranscriptomics: An Additional Regulatory Layer in Plants’ Development and Stress Response

Graduate School of Biotechnology and Crop Biotech Institute, Kyung Hee University, Yongin-si 17104, Korea
Department of Applied Biology, College of Agriculture and Life Sciences, Chonnam National University, Gwangju 61186, Korea
Author to whom correspondence should be addressed.
Plants 2022, 11(8), 1033;
Submission received: 13 March 2022 / Revised: 4 April 2022 / Accepted: 4 April 2022 / Published: 11 April 2022
(This article belongs to the Special Issue Responses of Plants to Environmental Stresses Volume II)


Epitranscriptomics has added a new layer of regulatory machinery to eukaryotes, and the advancement of sequencing technology has revealed more than 170 post-transcriptional modifications in various types of RNAs, including messenger RNA (mRNA), transfer RNA (tRNA), ribosomal RNA (rRNA), and long non-coding RNA (lncRNA). Among these, N6-methyladenosine (m6A) and N5-methylcytidine (m5C) are the most prevalent internal mRNA modifications. These regulate various aspects of RNA metabolism, mainly mRNA degradation and translation. Recent advances have shown that regulation of RNA fate mediated by these epitranscriptomic marks has pervasive effects on a plant’s development and responses to various biotic and abiotic stresses. Recently, it was demonstrated that the removal of human-FTO-mediated m6A from transcripts in transgenic rice and potatoes caused a dramatic increase in their yield, and that the m6A reader protein mediates stress responses in wheat and apple, indicating that regulation of m6A levels could be an efficient strategy for crop improvement. However, changing the overall m6A levels might have unpredictable effects; therefore, the identification of precise m6A levels at a single-base resolution is essential. In this review, we emphasize the roles of epitranscriptomic modifications in modulating molecular, physiological, and stress responses in plants, and provide an outlook on epitranscriptome engineering as a promising tool to ensure food security by editing specific m6A and m5C sites through robust genome-editing technology.

1. Introduction

Recently, biochemical modifications of RNAs designated as epitranscriptomes have added a new layer of regulatory networks to DNA methylation and histone modifications by fine-tuning key developmental processes and stress responses in all living organisms [1,2,3]. In eukaryotes, covalent RNA modifications add ubiquitous layers of information, and more than 170 post-transcriptional RNA modifications are found in different cellular RNAs, including messenger RNA (mRNA), ribosomal RNA (rRNA), transfer RNA (tRNA), long non-coding (lncRNA), micro RNA (miRNA), and small interfering RNA (siRNA) [4,5]. RNA modifications were studied exclusively in non-coding RNAs, including rRNA, tRNA, and small nuclear (snRNA), and they play critical roles in stabilizing structural conformations and modulating base pairing [6,7]. However, the advancement of genomic approaches has led to the discovery and mapping of various mRNA modifications and the elucidation of their roles in regulating the mRNA fate [8,9]. Many of the RNA modifications and enzymes responsible for installation and removal are highly conserved across all three domains of life [10], suggesting the importance of complex and flexible RNA regulation. The loss of these modifications affects key regulatory processes and can cause multiple human diseases [11,12] as well as defective development and stress responses in plants [13,14]. The RNA epitranscriptomic modification profiles vary according to the organs, cell types, and developmental stages under study. In Arabidopsis thaliana, transcriptome-wide N6-methyladenosine (m6A) sequencing revealed that 33.5% of transcripts exhibited differential m6A levels in leaves, roots, and flowers [15]. Consistently, the transcript levels of m6A writers, erasers, and reader proteins vary in different tissues and at different developmental stages [16]. Therefore, the effects of m6A and other epitranscriptome regulatory marks on plant development and abiotic and biotic stress responses will be an important avenue of future inquiry. The diverse eukaryotic modifications found on mRNA, tRNA, and rRNA are at first briefly described here.

1.1. mRNA Modification

The various modifications found in mRNA include m6A [17], 7-methylguanosine (m7G) [18], 2′-O, N6-dimethyladenosine (m6Am) [19], N1-methyladenosine (m1A) [20], 4-acetylcytidine (ac4C) [21], 5-hydroxymethylcytidine (5hmC) [22], 2′-O methylation at any nucleotide (Nm) [23], Inosine (I) [24], and pseudouridine (Ψ) [5]. They do not alter the coding capacity of mRNA [25], but they do alter the chemical properties of the transcripts, thereby affecting base pairing and the formation of ribonucleoprotein complexes [1]. Among these, m6A is the most abundant and dynamic mRNA internal modification in more than 5000 transcripts and is installed, erased, and read by methyltransferases, demethylases, and RNA binding proteins, respectively [5,24,25]. It affects transcripts’ fate and translation [26,27,28] in the nucleus and cytoplasm by regulating a wide variety of cellular processes including RNA turnover [29,30,31,32], stability [33,34], mRNA abundance [35], 3′UTR processing [36], alternative polyadenylation [37,38], mRNA splicing [39], and primary micro RNA processing [40]. In chloroplast and mitochondria, about 98–100% and 86–90% of transcripts are m6A-modified, respectively, with approximately 4–6 m6A sites per transcript [41]. RNA metabolism, including the processing, splicing, editing, and decaying processes, is important for the genetic regulation of chloroplasts and mitochondria, which is essential for plants’ survival and responses to changing environmental conditions [42,43]. RNA analysis of terrestrial plants has shown that RNA editing involving cytosine-to-uracil (C–U) transitions occurs prevalently in mitochondria and chloroplasts and affects their coding sequences, RNA structure, splicing and stability [44]. Transcriptome-wide profiling by m6A RNA sequencing has revealed the abundance of m6A near the stop codon and 3′UTR in the RRACH consensus sequence, which is highly conserved in various organisms [8,45,46] and in the UGUAY motif found exclusively in plants [16,33]. Another important epitranscriptomic mark located mainly at the 3′UTR and mRNA coding regions is 5-methylcytosine (m5C), which plays an essential role in development and stress responses, but very limited information is available on its roles in plants [47,48].

1.2. tRNA Modification

The tRNA is the richest source of modifications, and on average, 25% of its nucleotides are modified, presenting the greatest chemical variety and complexity [49,50]. These modifications range from simple methylation to complex multi-step transformations and include the incorporation of a range of low-molecular-weight metabolites [50]. The various tRNA modifications include ribose 2-O methylation, pseudouridine (ψ), dihydrouridine, methylguanosine (m1G, m2G, and m7G) [51], dimethylguanosine (m2,2G) [52], N1-methyladenosine (m1A) [53], 3-amino-3-propylcarboxyuridine (acp3U) [54], cytosine 2′-O-methylation (Cm) [55], and RNA editing from adenosine to inosine (A–I). m5C and 1-methylguanidine (m1G) are the most abundant tRNA modifications [2,56]. The post-transcriptional modifications of tRNA are critical for protein translation and proper cell growth [52,57]. The thirty-fourth and thirty-seventh wobble positions of the tRNA anticodon loop are most frequently modified, and they play essential roles in tRNA’s structure and function, codon recognition, and decoding, along with its translation initiation and elongation processes [58]. Deficiencies in nucleoside modification produce a wide variety of effects ranging from decreased virulence in bacteria, disease of the neural system in humans, and regulation of gene expression and stress responses in plants. A recent study revealed that more than 90 tRNA-modifying enzymes are present in the Arabidopsis genome. Modification genes of tRNA including AtTRM10, AtTRM11, AtTRM82, AtKTI12, and AtELP1, are responsible for modifications including m1G, m2G, m7G, and ncm5U, respectively [49]. In Arabidopsis and rice, tRNA marks increase in response to abiotic stresses including drought, salt, or cold temperatures [57,59].

1.3. rRNA Modification

The rRNA methylation processes evolved to refine the rRNA structure and optimize its functions [60,61]. In Arabidopsis, the various rRNA modifications include ribose 2′-O-methylation, pseudouridine (ψ), and base modifications including m1N, m6N, m7N, m3U, and acp3N [51,62]. Most of the modified bases in rRNA are located at the interface between the large and small subunits of the ribosome, corresponding to the P-site and the A-site [63]. Pseudouridine (ψ) and 2′-O-ribose methylation are regulated by small nucleolar ribonucleoprotein (snoRNPs) complexes that direct sequence-specific targeting. In contrast, rRNA base modifications are catalyzed by site-specific base methyltransferases [51]. The ribose 2′-O methylation can stabilize rRNA–mRNA, rRNA–tRNA, and rRNA–protein interactions [62]. Methylation in the rRNA of the chloroplast plays a vital role in regulating translation, and it has recently been established that chloroplast MraW-like (CMAL) protein catalyzes the m4C methylation of C1352 in the chloroplast’s 16S ribosomal subunit and plays an important role in ribosome biogenesis, plant development, and hormonal responses in Arabidopsis. RsmD is a chloroplast-localized m2G methyltransferase that affects plant developmental processes under cold stress [64].
This review focused mainly on the roles of m6A and m5C in the context of regulating molecular, cellular, and physiological processes during plants’ development and responses to stress. The robust genome editing technology for improving crops quality, survival, and productivity has highlighted future implications of m6A and m5C editing.

2. Developmental and Physiological Regulation by Epitranscriptomic Modifications in Plants

Epitranscriptomic modifications play important roles during plant development and in various responses to biotic and abiotic stresses. The major developmental processes affected by these modifications include organogenesis, embryonic and cotyledon development, seed development and seed yield, root and shoot growth, leaf morphology, trichome branching, floral transition, the proliferation of shoot apical meristem, and fruit ripening, as illustrated in Table 1.

2.1. Seed Development

Seed development is a complex process integrating different genetic, metabolic, and physiological pathways regulated by transcriptional, epigenetic, peptide hormone, and sugar regulators [75,76]. The chemical modifications associated with seed development, such as oxidation and methylation in mRNA and genomic DNA, affect gene expression during the later stages of seed development. DNA methylation in Arabidopsis is a dynamic process, and during seed development, there is a drastic increase in the global level of non-CG methylation throughout the seed, whereas CG and CHG-methylations do not change significantly. DNA methylation regulates the maternal expression of DOG4 and ALN, which are the negative regulators of seed dormancy. However, the special methylation marks associated with seed dormancy and the germination transcriptomes remain to be elucidated [77]. MTA, an m6A mRNA methyltransferase, is essential for embryogenesis, and its homozygous insertional knockout mutant “mta” showed an embryo arrest at the globular stage due to a lack of m6A at the poly(A) RNA, whereas the hemizygotes produced green and white seeds in immature siliques. However, the complementation lines rescued the embryo-lethal phenotype, indicating that the insertion mutation in MTA was embryo-lethal [69,78]. AtTRM61 and AtTRM6 cause N1 methylation of adensoine58 (A58) in tRNA, and the loss of function of either of these tRNA methyltransferases causes seed abortion. Mutations in the complex AtTRM61/AtTRM6 subunits result in developmental defects in the embryo and endosperm. However, conditional complementation of AtTRM61 showed that tRNA m1A58 modification is crucial for endosperm and embryo development [79]. CMAL is responsible for the methylation of N4-methylcytidine rRNA in the chloroplast and plays a key role in the chloroplast’s function, development, and abscisic acid (ABA) response in Arabidopsis. The loss-of-function cmal mutant exhibited a reduction in silique size, the number of seeds per silique, and total seed yield compared with wild-type (WT) plants, indicating its important role in seed development [80].

2.2. Root Development and Growth

Root development is a critical aspect of plant growth and allows the effective use of water resources. Plants, being sessile by nature, must adapt to various environmental cues. Epitranscriptomic modifications play a crucial role in root development processes. In Arabidopsis, AtTRM4B is involved in the methylation of m5C sites in the root transcriptome and positively regulates its growth through cell proliferation of root apical meristem. A T-DNA insertion mutant, trm4b, had a shorter primary root than the WT. The trm4b/trdmt1 double mutant also exhibited a shorter root phenotype. Furthermore, the TRM4B mutant was more sensitive to oxidation stress, implying that TRM4B contributes to root growth by regulating the response to oxidative stress [47]. Another study has shown that TRM4B contributes to primary and lateral root development in Arabidopsis by regulating the transcript levels of SHY2 and IAA16. The m5C levels in TRM4B were reduced by 20–30% in roots and exhibited a shorter root phenotype; however, its level remains unchanged in aerial tissues [81]. AtTRM5 is a bifunctional guanine and inosine-N1-methyltransferase tRNA and trm5-1 mutant with reduced levels of m1G and m1I and a reduced number of lateral roots and total root length compared with WT plants. However, TRM5 complementation lines reversed the knockout mutant phenotypes, indicating that TRM5 is involved in regulating the root development of Arabidopsis [67]. The m6A writer and reader proteins are highly expressed in the root meristems, apexes, and lateral root primordia [69,73,82]. In poplar, root development is affected by PtrMTA and OE-PtrMTA-14, OE-PtrMTA-10, and OE-PtrMTA-6 lines with almost double the m6A level, exhibiting better root and root tip growth compared with those of WT [83]. Recent research showed that the m6A level changes in response to ammonium (NH4+) nutrition and regulates the proteome response through altered translation in maritime pine roots [84]. Rice cultivar (cv.9311) exposed to cadmium stress exhibited abnormal root development caused by altered methylation profiles in transcripts involved in various biosynthetic, metabolic, and signaling processes, indicating that m6A plays an important role in regulating the gene expression level of various cellular pathways [85]. In Arabidopsis, correct m6A methylation plays an important role in developmental decisions, and Virilizer-1 (m6A methyltransferase) plays an important role in maintaining m6A levels. The deletion of vir-1 showed aberrant root cap formation and defective protoxylem development, indicating that m6A is essential for root development [73]. Another study has shown that multi-walled carbon nanotubes inhibit root growth by reducing m6A levels [86]. In rice, FTO expression increases root apical meristem cell proliferation and modulation of m6A RNA levels, which is a promising strategy to improve growth. FTO-transgenic plants showed a 35% and 45% increase in the total number and length of their lateral roots, respectively, and the number and length of their primary roots increased more than 3.3 fold at the tillering stage compared with the WT plants [87]. The m6A reader proteins named ECT2, ECT3, and ECT4 are highly expressed at the root apex and throughout the lateral root formation. Loss of ECT2 function caused a right-ward tilt in root growth, and the ect2/ect3 double mutants show slower root growth, whereas the ect2/ect3/ect4 triple mutants show agravitropic behavior along with a slower root growth compared with the WT [82]. Genes affecting various plant developmental processes such as floral transition [26,88], seed development [37,74,77], root growth [51,77], leaf growth [82], and fruit ripening [15,78] are illustrated in Figure 1.

2.3. Anther/Pollen Development

Anthers produce male gametes and certain sporophytic and gametophytic tissues in flowering plants. The tapetum of anthers acts as a bridge for nutrient exchange and communication between sporophytic and gametophytic cells. A recent study has shown the involvement of m6A in anther development in rice. OsEMD2L contains an N6-adenine methyltransferase-like (MLT) domain, and the osemd2l mutant showed an altered m6A landscape with Eternal Tapetum 1 (EAT1) transcription. The dysregulated alternative splicing and polyadenylation of EAT1 resulted in the suppression of OsAP25 and OsAP37 and led to delayed tapetal-programmed cell death and male sterility [71]. Another study showed that the transgenic expression of FTO in rice increased the total number of productive tillers per plant by 42% and improved productivity [87]. OsFIP and OsMTA2 are the components of the m6A RNA methyltransferase complex in rice. OsFIP is essential for male rice gametogenesis and modifies m6A during sporogenesis by recognizing a panicle-specific “UGWAMH” motif. The osfip knockout mutant showed an early degeneration of microspores and abnormal meiosis in prophase I, and had 1.4 tillers per plant compared with 4.7 in WT plants. Furthermore, at the late reproductive stage, fip plants were almost sterile and had shorter panicles and reduced seed numbers, and 84.8% of the pollen grains lacked starch, indicating that OsFIP plays an important role in microspore development [18]. In tomatoes, the widely spread m6A modification in anthers is disrupted under cold stress conditions and affects the expression level of genes involved in tapetum and microspore development. The moderately low-temperature-induced pollen abortion is due to impaired micro gametogenesis, tapetum degeneration, and pollen wall formation. Additionally, m6A is associated with ABA transport in anthers or sterol accumulation for pollen wall formation, and targets the ATP-binding cassette G gene, SLABCG31 [89].

2.4. Floral Regulation

Precise initiation of flowering is essential for plant reproductive success, and several epigenetic modifications play important roles during floral transition. A recent report showed that m6A-mediated RNA modification was involved in the complex genetic regulation that controls floral regulation. The loss of function of the RNA demethylase, ALKBH10B, increased m6A modification and delayed floral transition due to the increased mRNA decay of the flowering regulator FT and its up-regulators, SPL3, and SPL9 [26]. AtTRM5 encodes nuclear-localized bifunctional tRNA guanine and inosine-N1-methyltransferase and is important for growth and development. The loss-of-function Attrm5 mutant showed an overall slow growth and delayed flowering. At the inflorescence emergence stage, trm5-1 plants exhibited a reduced number of rosette leaves, smaller leaves, reduced fresh weight, and took longer to flower; however, TRM5-overexpressing plants flowered slightly earlier than WT. The delayed flowering phenotype in trm5-1 mutants was due to a deficiency in floral time regulators, including GI, CO, and FT, the downstream floral meristem identity gene LEAFY (LFY), and circadian clock-related genes [67]. CMAL is a chloroplast-localized rRNA methyltransferase and is responsible for the modification of N4-methylcytidine (m4C) in 16S chloroplast rRNA. The loss-of-function cmal mutant showed stunted growth and delayed flowering due to altered expression levels of various flowering-related genes, including APETALA1 (AP1), SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1 (SOC1), FRUITFULL (FUL), CAULIFLOWER (CAL), and Flowering Locus C (FLC); however, the CMAL complementation lines recovered stunted growth phenotypes, indicating that stunted growth is due to the lack of m4C modification [90].

3. Biotic and Abiotic Regulation by Epitranscriptomic Modifications in Plants

RNA methylation plays an important role in the response to various environmental stresses by regulating the expression level of key stress-responsive genes. Drought stress increased the m6A marks in the 5′UTR region and promoted the translation of several drought-resistant transcripts. Cellular stress also altered the characteristic distribution of m6A and metagenic analysis followed by heat shock, and showed that m6A was highly enriched in the 5′UTR region in heat-shocked cells compared with the control [28]. Recently, anther development in tomatoes was modulated by the m6A-mediated expression level of several pollen development-related genes under a low temperature [91]. In tea (Camellia sinensis), m6A regulatory genes play an important role in resistance to environmental stresses and the withering process of tea. Drought stress decreased the expression level of several m6A writers, including CsMTB1, CsMTC, CsMTA1, CsMTA2, CsMTB2, and CsVIR2, whereas the level of m6A erasers and readers was enhanced. Furthermore, the interaction of the methylation regulatory genes of RNA and DNA methylation formed a negative feedback loop, indirectly inhibited flavonoid biosynthesis, and improved the palatability of the oolong tea during the withering process [92]. CIMTB is an m6A methyltransferase in watermelon, and it helps in adapting to drought stress by regulating reactive oxygen species (ROS) scavenging, photosystem components, phytohormones, and multiple stress-responsive transcription factors [93]. The global m6A levels in Arabidopsis increase in response to salt stress, and its dysregulation disrupts the salt stress tolerance mechanism. The m6A writer mutants, including mta, mtb, vir, and hakai, exhibited salt-sensitive phenotypes in an m6A-dependent manner. VIR-mediated m6A methylation modulated ROS homeostasis by down-regulating the mRNA stability of key salt stress negative regulators, including GI, ATAF1, and GSTU17, by affecting 3′UTR lengthening [36]. In Arabidopsis alkbh10b mutants, global m6A levels increased under salt stress conditions and exhibited salt-tolerant phenotypes caused by the decreased expression level for several negative regulators of salt stress, including ATAF1, MYB73, and BGLU22 [91]. m6A regulates the expression level of some transcription factors, including WRKY81 and heat shock proteins (HSP70) in tomatoes during chilling injury, and helps the plant combat cold stress [94]. In wheat, YTH domain-containing RNA-binding m6A reader proteins are regulated by various abiotic stresses [95].
It has recently been established that m6A plays an important role in regulating the life cycle of various viruses by modifying viral and host RNAs. However, there is conflicting evidence on the role of m6A in regulating the viral life cycle. Recent research showed that m6A suppresses the replication of rice black-streaked dwarf viruses and is associated with viral persistence in its insect vector [96]. ALKBH9B is an m6A RNA demethylase in Arabidopsis and its demethylation activity affects the infectivity of alfalfa mosaic viruses (AMV). The suppression of atalkbh9b increased the relative abundance of m6A in the AMV genome and impaired virus accumulation and systemic invasion of the plant. Therefore, m6A modification may act as a regulatory strategy in plants by controlling cytoplasmic-replicating RNA viruses [97]. Infection with a cucumber green mottle mosaic virus (GGMMV) significantly decreased m6A levels of 422 differentially methylated transcripts in watermelon because of the increased expression level of the m6A demethylase gene ClALKBH4B. The decreased m6A levels enhanced the transcription of several defense response factors involved in virus-induced gene silencing, such as transcription factors, carbohydrate allocation, and signaling genes, and ultimately activated the immune responses of the plant in the early stages of GGMMV infection [93]. In apples, the m6A reader protein, MhYTP2, conferred resistance to powdery mildew by regulating the stability of MdMLO19 mRNA and the translation efficiency of several antioxidant genes [98]. In rice, m6A is involved in the conidiation and virulence of the rice blast fungus Pyriculariaoryzae, and the N6-adenosine-methyltransferase (PoIme4), m6A mRNA demethylase (PoALKB1), and m6A binding proteins (PoYth1 andPoYth2) are involved in the virulence of rice in P. Oryzae [99]. The m6A modification levels of rice mRNA increased in genes that were expressed at low levels during the viral infection of plants. This modification regulates the expression level of key antiviral genes involved in RNA silencing, resistance, and fundamental antiviral phytohormone metabolic pathways [100]. However, another study showed that in tobacco, the m6A level is associated with the tobacco mosaic virus, and its infection increased the expression level of potential demethylase XM-009801708 on the twelfth and twenty-first days of infection, thereby decreasing m6A levels [101]. These conflicting pieces of evidence need to be addressed further to illustrate the m6A-regulated mechanism in defensive responses to viral infections. Several plant viruses containing a single-stranded RNA genome contain an ALKB domain in their genome and have evolved mechanisms to respond to the regulation of the host m6A system [102]. The regulatory roles of post-transcriptional modifications in various stress responses are illustrated in Table 2.

4. Molecular Regulation by Epitranscriptomic Modifications in Plants

m6A is important in the regulation of various aspects of mRNA metabolism, and m6A readers play a precise and complex regulatory role by recognizing changes in m6A modification in mRNA. The fate of modified transcripts depends on the reader protein recognizing the modification that may cause the export of modified transcripts from the nucleus to the cytoplasm, where they may be translated, stored in granules, or decayed by the P-bodies [2], as shown in Figure 2.
A recent study showed that the modification of m6A regulates alternative polyadenylation (APA) of nitrate signaling-related genes through recognition by the CPSF30-L reader protein [37]. A recent study provided the evidence for m6A-regulated protein translation, illustrating that m6A is deposited in the 3′-UTR region in response to ammonium nutrition and is correlated with poly(A) lengthening and transcript abundance, thereby an optimal response to the N-supply in maritime pine roots is acquired [84]. An m6A reader protein, ECT2, functions in polyadenylation and 3′UTR processing in the nucleus by selectively binding to the m6A-containing poly(A) signal FUEs and recruiting polyadenylation machinery to promote mRNA stability and regulate the morphology of trichomes in Arabidopsis [33]. In Zea mays, transcriptome-wide m6A–mRNA profiling has shown that m6A is widely distributed in thousands of protein-coding genes primarily enriched in the 3′UTR region, and strongly correlated with protein translation, and regulates gene expression [106]. Additionally, it also positively regulates the translation of mitochondrial transcripts in Arabidopsis and Brassica [107]. The YTHDF1 and YTHDF3 reader proteins recognize m6A residues in the 3′UTR region and enhance translation through interaction with initiation factors or ribosomal subunit proteins [108,109,110]. However, YTHCF2 proteins decrease the amount of m6A-modified mRNA in translatable fractions by causing degradation through the sequestering of modified transcripts in processing bodies [109]. Furthermore, in Arabidopsis, m6A enhances the stability of transcripts during the salt stress response through the widespread prevention of ribonucleolytic cleavage and an enhanced abundance of salt and osmotic stress-related transcripts [111]. Recently, m6A has been found to regulate miRNA processing through the interaction between m6A-methyltransferase and TGH, a miRNA biogenesis factor [27]. Being another important internal modification of mRNA, m5C also tends to stabilize and translate modified transcripts. Recent research showed that m5C methylation promoted the translation of heat-induced mRNAs and induced heat resistance in WT rice plants at high temperatures [103]. Another study showed that m5C-containing mRNAs were more stable and enriched in the fractions of graft-mobile transcripts that move from root to shoot, indicating that m5C plays an important role in the mobility of transcripts throughout the plant body [68]. There is still a need to further explore m5C-mediated mRNA metabolism, especially for specific transcripts involved in plant development and stress responses. The molecular and physiological processes regulated by post-transcriptional modifications are illustrated in Figure 3; however, multiple RNA regulatory mechanisms mediated by epitranscriptomic modifications still need to be discovered.

5. Future Perspectives

Climate change and the increase in world population have caused a great threat to sustainable food production; however, recent discoveries on the involvement of post-transcriptional modifications in the regulation of RNA metabolism, plant development, and stress responses have shown that it has a great potential to improve crop survival and productivity, but it is limited by some factors. Firstly, the modulation of epitranscriptomic machinery may cause changes in global m6A levels, causing unpredictable effects. Thus, transcriptome-wide mapping at a single-base resolution is critical for precise m6A editing without affecting the overall m6A levels or the sequences of genes involved in crop development and stress responses [35]. Various advanced sequencing techniques including miCLIP (m6A individual-nucleotide-resolution cross-linking and immunoprecipitation) [112], Mazter-seq (RNA digestion via m6A-sensitive RNase and sequencing) [113], Nanopore DRS (Direct RNA Sequencing) [114], and m6A REF-Seq (m6A-sensitive RNA-endoribonuclease-facilitated sequencing) may facilitate the accurate mapping of m6A modifications at the cellular level [115].
The second challenge is the precise addition or removal of m6A at a specific site in transcripts, which can be resolved by recent advances in CRISPR technology that have revolutionized the editing capabilities of the entire genome [115]. Recently, a new CRISPR-based m6A editing system was proposed, in which m6A enzymes (writers/erasers) are fused to a dCas13 protein that binds to the targeted RNA transcripts without mediating their cleavage, and the fused m6A writers or erasers can add or remove the m6A modification at the target site. Furthermore, editing of the transcript target site requires dynamic m6A modification maps at a single-base resolution, which are useful for designing sgRNA [102]. Therefore, editing m6A modifications in key transcripts involved in growth, development, photosynthesis, and biotic (viral and bacterial infections) and abiotic stress (salt, heat, drought) responses through CRISPR technology may be a feasible method to improve crops’ productivity and stress resistance [102].
Additionally, a CRISPR-based strategy has been developed that can induce targeted epigenetic modifications in DNA by fusing the epigenetic modifier with dCas9. Targeted epigenetic modifications and related phenotypes are stably transmitted to subsequent generations even without transgenes [116,117]. Gallego-Bartolome et al. developed a CRISPR/dCas9 based targeted demethylation system using TET1cd and a modified SunTag system, in which TET1cd (a DNA demethylase) up-regulates the expression level of the FLOWERING WAGENINGEN (FWA) gene. This approach was successful in achieving the targeted removal of 5mC at specific loci with high specificity and minimal off-target effects.
The various processes that can be modified by epitranscriptome engineering are shown in Figure 4.
Another approach toward epitranscriptome engineering is through manipulation of the activities of RNA modification-related enzymes in crops. Recently, it has been reported that over-expression of human RNA demethylase (FTO) in rice has up-regulated several pathways related to photosynthesis and nitrogen regulation and greater crop yields by increasing the plants’ root cell proliferation, tiller numbers, photosynthesis rate, and drought resistance [87]. Furthermore, over-expression of an m6A-methyltransferase has increased drought resistance in poplars by increasing trichome branching in roots [83], suggesting potential applications of epitranscriptome manipulation to improve survival and productivity.
mRNA modifications such as m6A and m5C are highly conserved in many plant species, thus epitranscriptome engineering is a promising tool in crop breeding. However, it is essential to understand the specific and generic functions of mRNA modifications and discover additional epitranscriptome components and their associated regulatory mechanisms. The integration of advanced sequencing techniques involving a single-base resolution into genome editing and genetic transformation holds great promise for epitranscriptome engineering to improve food security despite climate change and the global population increase.

Author Contributions

Writing—original draft preparation, Y.S. and K.-H.J.; writing—reviewing and editing Y.S., K.-H.J., B.U. and H.K. All authors have read and agreed to the published version of the manuscript.


This work was supported by grants from the New Breeding Technologies Development Program (PJ01661002 to K.-H.J.), the Rural Development Administration, Republic of Korea, and the National Research Foundation (NRF), Ministry of Education, Science and Technology (2021R1A2C2010448 to K.-H.J.).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.


We thank Gynheung An, who established the Crop Biotech Institute at Kyung Hee University.

Conflicts of Interest

The authors declare no conflict of interest.


  1. Vandivier, L.E.; Gregory, B.D. New insights into the plant epitranscriptome. J. Exp. Bot. 2018, 69, 4659–4665. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  2. Hu, J.; Manduzio, S.; Kang, H. Epitranscriptomic RNA Methylation in Plant Development and Abiotic Stress Responses. Front. Plant Sci. 2019, 10, 500. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  3. Yu, X.; Sharma, B.; Gregory, B.D. The impact of epitranscriptomic marks on post-transcriptional regulation in plants. Brief. Funct. Genom. 2021, 20, 113–124. [Google Scholar] [CrossRef] [PubMed]
  4. Wiener, D.; Schwartz, S. The epitranscriptome beyond m6A. Nat. Rev. Genet. 2021, 22, 119–131. [Google Scholar] [CrossRef] [PubMed]
  5. Shen, L.; Liang, Z.; Wong, C.E.; Yu, H. Messenger RNA Modifications in Plants. Trends Plant Sci. 2019, 24, 328–341. [Google Scholar] [CrossRef] [PubMed]
  6. Pan, T. Modifications and functional genomics of human transfer RNA. Cell Res. 2018, 28, 395–404. [Google Scholar] [CrossRef]
  7. Sharma, S.; Lafontaine, D.L.J. View from a bridge’: A new perspective on eukaryotic rRNA base modification. Trends Biochem. Sci. 2015, 40, 560–575. [Google Scholar] [CrossRef]
  8. Dominissini, D.; Moshitch-Moshkovitz, S.; Schwartz, S.; Salmon-Divon, M.; Ungar, L.; Osenberg, S.; Cesarkas, K.; Jacob-Hirsch, J.; Amariglio, N.; Kupiec, M.; et al. Topology of the human and mouse m6A RNA methylomes revealed by m6A-seq. Nature 2012, 485, 201–206. [Google Scholar] [CrossRef]
  9. Meyer, K.D.; Saletore, Y.; Zumbo, P.; Elemento, O.; Mason, C.E.; Jaffrey, S.R. Comprehensive Analysis of mRNA Methylation Reveals Enrichment in 3′ UTRs and near Stop Codons. Cell 2012, 149, 1635–1646. [Google Scholar] [CrossRef] [Green Version]
  10. Jackman, J.E.; Alfonzo, J.D. RNA modifications: Nature’s combinatorial chemistry playground. Wiley Interdiscip Rev. RNA 2013, 4, 35–48. [Google Scholar] [CrossRef] [Green Version]
  11. Blanco, S.; Dietmann, S.; Flores, J.V.; Hussain, S.; Kutter, C.; Humphreys, P.; Lukk, M.; Lombard, P.; Treps, L.; Popis, M.; et al. Aberrant methylation of t RNA s links cellular stress to neuro-developmental disorders. EMBO J. 2014, 33, 2020–2039. [Google Scholar] [CrossRef] [PubMed]
  12. Torres, A.G.; Batlle, E.; de Pouplana, L.R. Role of tRNA modifications in human diseases. Trends Mol. Med. 2014, 20, 306–314. [Google Scholar] [CrossRef] [PubMed]
  13. Motorin, Y.; Helm, M. RNA nucleotide methylation. Wiley Interdiscip. Rev. RNA 2011, 2, 611–631. [Google Scholar] [CrossRef] [PubMed]
  14. El Yacoubi, B.; Bailly, M.; de Crécy-Lagard, V. Biosynthesis and Function of Posttranscriptional Modifications of Transfer RNAs. Annu. Rev. Genet. 2012, 46, 69–95. [Google Scholar] [CrossRef]
  15. Zhou, L.; Tian, S.; Qin, G. RNA methylomes reveal the m6A-mediated regulation of DNA demethylase gene SlDML2 in tomato fruit ripening. Genome Biol. 2019, 20, 156. [Google Scholar] [CrossRef] [Green Version]
  16. Shen, L.; Liang, Z.; Gu, X.; Chen, Y.; Teo, Z.W.N.; Hou, X.; Cai, W.M.; Dedon, P.C.; Liu, L.; Yu, H. N 6 -Methyladenosine RNA Modification Regulates Shoot Stem Cell Fate in Arabidopsis. Dev. Cell 2016, 38, 186–200. [Google Scholar] [CrossRef] [Green Version]
  17. Dominissini, D.; Nachtergaele, S.; Moshitch-Moshkovitz, S.; Peer, E.; Kol, N.; Ben-Haim, M.S.; Dai, Q.; Di Segni, A.; Salmon-Divon, M.; Clark, W.C.; et al. The dynamic N1-methyladenosine methylome in eukaryotic messenger RNA. Nature 2016, 530, 441–446. [Google Scholar] [CrossRef] [Green Version]
  18. Zhang, X.; Wei, L.-H.; Wang, Y.; Xiao, Y.; Liu, J.; Zhang, W.; Yan, N.; Amu, G.; Tang, X.; Zhang, L.; et al. Structural insights into FTO’s catalytic mechanism for the demethylation of multiple RNA substrates. Proc. Natl. Acad. Sci. USA 2019, 116, 2919–2924. [Google Scholar] [CrossRef] [Green Version]
  19. Boulias, K.; Toczydłowska-Socha, D.; Hawley, B.R.; Liberman, N.; Takashima, K.; Zaccara, S.; Guez, T.; Vasseur, J.-J.; Debart, F.; Aravind, L.; et al. Identification of the m6Am Methyltransferase PCIF1 Reveals the Location and Functions of m6Am in the Transcriptome. Mol. Cell 2019, 75, 631–643.e8. [Google Scholar] [CrossRef]
  20. Safra, M.; Sas-Chen, A.; Nir, R.; Winkler, R.; Nachshon, A.; Bar-Yaacov, D.; Erlacher, M.; Rossmanith, W.; Stern-Ginossar, N.; Schwartz, S. The m1A landscape on cytosolic and mitochondrial mRNA at single-base resolution. Nature 2017, 551, 251–255. [Google Scholar] [CrossRef]
  21. Arango, D.; Sturgill, D.; Alhusaini, N.; Dillman, A.A.; Sweet, T.J.; Hanson, G.; Hosogane, M.; Sinclair, W.R.; Nanan, K.K.; Mandler, M.D.; et al. Acetylation of Cytidine in mRNA Promotes Translation Efficiency. Cell 2018, 175, 1872–1886.e24. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  22. Delatte, B.; Wang, F.; Ngoc, L.V.; Collignon, E.; Bonvin, E.; Deplus, R.; Calonne, E.; Hassabi, B.; Putmans, P.; Awe, S.; et al. RNA biochemistry. Transcriptome-wide distribution and function of RNA hydroxymethylcytosine. Science 2016, 351, 282–285. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  23. Bartoli, K.M.; Schaening, C.; Carlile, T.M.; Gilbert, W.V. Conserved methyltransferase Spb1 targets mRNAs for regulated modification with 2′-O-methyl ribose. bioRxiv 2018. [Google Scholar] [CrossRef]
  24. Shevchenko, G.; Morris, K.V. All I’s on the RADAR: Role of ADAR in gene regulation. FEBS Lett. 2018, 592, 2860–2873. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Balacco, D.L.; Soller, M. The m6A Writer: Rise of a Machine for Growing Tasks. Biochemistry 2019, 58, 363–378. [Google Scholar] [CrossRef]
  26. Duan, H.-C.; Wei, L.-H.; Zhang, C.; Wang, Y.; Chen, L.; Lu, Z.; Chen, P.R.; He, C.; Jia, G. ALKBH10B Is an RNA N6-Methyladenosine Demethylase Affecting Arabidopsis Floral Transition. Plant Cell 2017, 29, 2995–3011. [Google Scholar] [CrossRef] [Green Version]
  27. Bhat, S.S.; Bielewicz, D.; Gulanicz, T.; Bodi, Z.; Yu, X.; Anderson, S.J.; Szewc, L.; Bajczyk, M.; Dolata, J.; Grzelak, N.; et al. mRNA adenosine methylase (MTA) deposits m6A on pri-miRNAs to modulate miRNA biogenesis in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 2020, 117, 21785–21795. [Google Scholar] [CrossRef]
  28. Meyer, K.; Patil, D.; Zhou, J.; Zinoviev, A.; Skabkin, M.A.; Elemento, O.; Pestova, T.V.; Qian, S.-B.; Jaffrey, S.R. 5′ UTR m6A Promotes Cap-Independent Translation. Cell 2015, 163, 999–1010. [Google Scholar] [CrossRef] [Green Version]
  29. Kuppers, D.A.; Arora, S.; Lim, Y.; Lim, A.R.; Carter, L.M.; Corrin, P.D.; Plaisier, C.L.; Basom, R.; Delrow, J.J.; Wang, S.; et al. N6-methyladenosine mRNA marking promotes selective translation of regulons required for human erythropoiesis. Nat. Commun. 2019, 10, 4596. [Google Scholar] [CrossRef] [Green Version]
  30. Luo, J.-H.; Wang, Y.; Wang, M.; Zhang, L.-Y.; Peng, H.-R.; Zhou, Y.-Y.; Jia, G.-F.; He, Y. Natural Variation in RNA m6A Methylation and Its Relationship with Translational Status. Plant Physiol. 2020, 182, 332–344. [Google Scholar] [CrossRef] [Green Version]
  31. Yue, J.; Wei, Y.; Zhao, M. The Reversible Methylation of m6A Is Involved in Plant Virus Infection. Biology 2022, 11, 271. [Google Scholar] [CrossRef] [PubMed]
  32. Ke, S.; Pandya-Jones, A.; Saito, Y.; Fak, J.J.; Vågbø, C.B.; Geula, S.; Hanna, J.H.; Black, D.L.; Darnell, J.E.; Darnell, R.B. m6A mRNA modifications are deposited in nascent pre-mRNA and are not required for splicing but do specify cytoplasmic turnover. Genes Dev. 2017, 31, 990–1006. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  33. Wei, L.-H.; Song, P.; Wang, Y.; Lu, Z.; Tang, Q.; Yu, Q.; Xiao, Y.; Zhang, X.; Duan, H.-C.; Jia, G. The m6A Reader ECT2 Controls Trichome Morphology by Affecting mRNA Stability in Arabidopsis. Plant Cell 2018, 30, 968–985. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  34. Boo, S.H.; Kim, Y.K. The emerging role of RNA modifications in the regulation of mRNA stability. Exp. Mol. Med. 2020, 52, 400–408. [Google Scholar] [CrossRef] [Green Version]
  35. Zheng, H.; Sun, X.; Li, J.; Song, Y.; Song, J.; Wang, F.; Liu, L.; Zhang, X.; Sui, N. Analysis of N6-methyladenosine reveals a new important mechanism regulating the salt tolerance of sweet sorghum. Plant Sci. 2021, 304, 110801. [Google Scholar] [CrossRef]
  36. Hu, J.; Cai, J.; Park, S.J.; Lee, K.; Li, Y.; Chen, Y.; Yun, J.; Xu, T.; Kang, H. N 6 -Methyladenosine mRNA methylation is important for salt stress tolerance in Arabidopsis. Plant J. 2021, 106, 1759–1775. [Google Scholar] [CrossRef]
  37. Hou, Y.; Sun, J.; Wu, B.; Gao, Y.; Nie, H.; Nie, Z.; Quan, S.; Wang, Y.; Cao, X.; Li, S. CPSF30-L-mediated recognition of mRNA m6A modification controls alternative polyadenylation of nitrate signaling-related gene transcripts in Arabidopsis. Mol. Plant 2021, 14, 688–699. [Google Scholar] [CrossRef]
  38. Brodersen, P.; Arribas-Hernández, L.; Rennie, S.; Schon, M.; Porcelli, C.; Enugutti, B.; Andersson, R.; Nodine, M.D. The Arabidopsis m6A-binding proteins ECT2 and ECT3 bind largely overlapping mRNA target sets and influence target mRNA abundance, not alternative polyadenylation. bioRxiv 2021. [Google Scholar] [CrossRef]
  39. Xiao, W.; Adhikari, S.; Dahal, U.; Chen, Y.S.; Hao, Y.J.; Sun, B.F.; Sun, H.Y.; Li, A.; Ping, X.L.; Lai, W.Y.; et al. Nuclear m(6)A Reader YTHDC1 Regulates mRNA Splicing. Mol Cell. 2016, 61, 507–519. [Google Scholar] [CrossRef] [Green Version]
  40. Bhat, S.S.; Bielewicz, D.; Jarmolowski, A.; Szweykowska-Kulińska, Z. N6-methyladenosine (m6A): Revisiting the Old with Focus on New, an Arabidopsis thaliana Centered Review. Genes 2018, 9, 596. [Google Scholar] [CrossRef] [Green Version]
  41. Wang, Z.; Tang, K.; Zhang, D.; Wan, Y.; Wen, Y.; Lu, Q.; Wang, L. High-throughput m6A-seq reveals RNA m6A methylation patterns in the chloroplast and mitochondria transcriptomes of Arabidopsis thaliana. PLoS ONE 2017, 12, e0185612. [Google Scholar] [CrossRef] [PubMed]
  42. Hammani, K.; Giegé, P. RNA metabolism in plant mitochondria. Trends Plant Sci. 2014, 19, 380–389. [Google Scholar] [CrossRef] [PubMed]
  43. Stern, D.B.; Goldschmidt-Clermont, M.; Hanson, M.R. Chloroplast RNA Metabolism. Annu. Rev. Plant Biol. 2010, 61, 125–155. [Google Scholar] [CrossRef] [PubMed]
  44. Small, I.D.; Schallenberg-Rüdinger, M.; Takenaka, M.; Mireau, H.; Ostersetzer-Biran, O. Plant organellar RNA editing: What 30 years of research has revealed. Plant J. 2020, 101, 1040–1056. [Google Scholar] [CrossRef] [PubMed]
  45. Luo, G.-Z.; MacQueen, A.; Zheng, G.; Duan, H.; Dore, L.; Lu, Z.; Liu, J.; Chen, K.; Jia, G.; Bergelson, J.; et al. Unique features of the m6A methylome in Arabidopsis thaliana. Nat. Commun. 2014, 5, 5630. [Google Scholar] [CrossRef] [Green Version]
  46. Zhao, X.; Yang, Y.; Sun, B.-F.; Shi, Y.; Yang, X.; Xiao, W.; Hao, Y.-J.; Ping, X.-L.; Chen, Y.-S.; Wang, W.-J.; et al. FTO-dependent demethylation of N6-methyladenosine regulates mRNA splicing and is required for adipogenesis. Cell Res. 2014, 24, 1403–1419. [Google Scholar] [CrossRef] [PubMed]
  47. David, R.; Burgess, A.; Parker, B.; Li, J.; Pulsford, K.; Sibbritt, T.; Preiss, T.; Searle, I.R. Transcriptome-Wide Mapping of RNA 5-Methylcytosine in Arabidopsis mRNAs and Noncoding RNAs. Plant Cell 2017, 29, 445–460. [Google Scholar] [CrossRef] [Green Version]
  48. Litholdo, C.G.; Bousquet-Antonelli, C. Chemical RNA Modifications: The Plant Epitranscriptome. In Epigenetics in Plants of Agronomic Importance: Fundamentals and Applications; Springer: Berlin/Heidelberg, Germany, 2019; pp. 291–310. [Google Scholar]
  49. Chen, P.; Jäger, G.; Zheng, B. Transfer RNA modifications and genes for modifying enzymes in Arabidopsis thaliana. BMC Plant Biol. 2010, 10, 201. [Google Scholar] [CrossRef] [Green Version]
  50. Helm, M.; Motorin, Y. Detecting RNA modifications in the epitranscriptome: Predict and validate. Nat. Rev. Genet. 2017, 18, 275–291. [Google Scholar] [CrossRef]
  51. Burgess, A.; David, R.; Searle, I.R. Deciphering the epitranscriptome: A green perspective. J. Integr. Plant Biol. 2016, 58, 822–835. [Google Scholar] [CrossRef] [Green Version]
  52. Funk, H.M.; Zhao, R.; Thomas, M.; Spigelmyer, S.M.; Sebree, N.J.; Bales, R.O.; Burchett, J.B.; Mamaril, J.B.; Limbach, P.A.; Guy, M.P. Identification of the enzymes responsible for m2,2G and acp3U formation on cytosolic tRNA from insects and plants. PLoS ONE 2020, 15, e0242737. [Google Scholar] [CrossRef] [PubMed]
  53. Tang, J.; Jia, P.; Xin, P.; Chu, J.; Shi, D.-Q.; Yang, W.-C. The Arabidopsis TRM61/TRM6 complex is a bona fide tRNA N1-methyladenosine methyltransferase. J. Exp. Bot. 2020, 71, 3024–3036. [Google Scholar] [CrossRef] [PubMed]
  54. Spigelmyer, S.M. Identification of the Enzyme Required for the acp3U Modification in Plastidic tRNA; Northern Kentucky University: Highland Heights, KY, USA, 2021. [Google Scholar]
  55. Ramírez, V.; González, B.; López, A.; Castelló, M.J.; Gil, M.J.; Zheng, B.; Chen, P.; Vera, P. A 2′-O-Methyltransferase Responsible for Transfer RNA Anticodon Modification Is Pivotal for Resistance to Pseudomonas syringae DC3000 in Arabidopsis. Mol. Plant Microbe Interact. 2018, 31, 1323–1336. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  56. Chou, H.-J.; Donnard, E.; Gustafsson, H.T.; Garber, M.; Rando, O.J. Transcriptome-wide Analysis of Roles for tRNA Modifications in Translational Regulation. Mol. Cell 2017, 68, 978–992.e4. [Google Scholar] [CrossRef] [Green Version]
  57. Dannfald, A.; Favory, J.-J.; Deragon, J.-M. Variations in transfer and ribosomal RNA epitranscriptomic status can adapt eukaryote translation to changing physiological and environmental conditions. RNA Biol. 2021, 18, 4–18. [Google Scholar] [CrossRef]
  58. Väre, V.Y.P.; Eruysal, E.R.; Narendran, A.; Sarachan, K.L.; Agris, P.F. Chemical and Conformational Diversity of Modified Nucleosides Affects tRNA Structure and Function. Biomolecules 2017, 7, 29. [Google Scholar] [CrossRef] [Green Version]
  59. Wang, Y.; Pang, C.; Li, X.; Hu, Z.; Lv, Z.; Zheng, B.; Chen, P. Identification of tRNA nucleoside modification genes critical for stress response and development in rice and Arabidopsis. BMC Plant Biol. 2017, 17, 261. [Google Scholar] [CrossRef]
  60. Decatur, W.A.; Fournier, M.J. rRNA modifications and ribosome function. Trends Biochem. Sci. 2002, 27, 344–351. [Google Scholar] [CrossRef]
  61. Zou, M.; Mu, Y.; Chai, X.; Ouyang, M.; Yu, L.-J.; Zhang, L.; Meurer, J.; Chi, W. The critical function of the plastid rRNA methyltransferase, CMAL, in ribosome biogenesis and plant development. Nucleic Acids Res. 2020, 48, 3195–3210. [Google Scholar] [CrossRef] [Green Version]
  62. Azevedo-Favory, J.; Gaspin, C.; Ayadi, L.; Montacié, C.; Marchand, V.; Jobet, E.; Rompais, M.; Carapito, C.; Motorin, Y.; Sáez-Vásquez, J. Mapping rRNA 2’-O-methylations and identification of C/D snoRNAs in Arabidopsis thaliana plants. RNA Biol. 2021, 18, 1760–1777. [Google Scholar] [CrossRef]
  63. Sloan, K.E.; Warda, A.S.; Sharma, S.; Entian, K.-D.; Lafontaine, D.; Bohnsack, M.T. Tuning the ribosome: The influence of rRNA modification on eukaryotic ribosome biogenesis and function. RNA Biol. 2017, 14, 1138–1152. [Google Scholar] [CrossRef] [PubMed]
  64. Ngoc, L.N.T.; Park, S.J.; Cai, J.; Huong, T.T.; Lee, K.; Kang, H. RsmD, a Chloroplast rRNA m2G Methyltransferase, Plays a Role in Cold Stress Tolerance by Possibly Affecting Chloroplast Translation in Arabidopsis. Plant Cell Physiol. 2021, 62, 948–958. [Google Scholar] [CrossRef] [PubMed]
  65. Anderson, J.; Phan, L.; Cuesta, R.; Carlson, B.A.; Pak, M.; Asano, K.; Björk, G.R.; Tamame, M.; Hinnebusch, A.G. The essential Gcd10p–Gcd14p nuclear complex is required for 1-methyladenosine modification and maturation of initiator methionyl-tRNA. Genes Develop. 1998, 12, 3650–6362. [Google Scholar] [CrossRef] [Green Version]
  66. Yang, W.; Meng, J.; Liu, J.; Ding, B.; Tan, T.; Wei, Q.; Yu, Y. The N1-Methyladenosine Methylome of Petunia mRNA. Plant Physiol. 2020, 183, 1710–1724. [Google Scholar] [CrossRef] [PubMed]
  67. Guo, Q.; Ng, P.Q.; Shi, S.; Fan, D.; Li, J.; Zhao, J.; Wang, H.; David, R.; Mittal, P.; Do, T.; et al. Arabidopsis TRM5 encodes a nuclear-localised bifunctional tRNA guanine and inosine-N1-methyltransferase that is important for growth. PLoS ONE 2019, 14, e0225064. [Google Scholar] [CrossRef] [Green Version]
  68. Yang, L.; Perrera, V.; Saplaoura, E.; Apelt, F.; Bahin, M.; Kramdi, A.; Olas, J.; Mueller-Roeber, B.; Sokolowska, E.; Zhang, W.; et al. m5C Methylation Guides Systemic Transport of Messenger RNA over Graft Junctions in Plants. Curr. Biol. 2019, 29, 2465–2476.e5. [Google Scholar] [CrossRef] [Green Version]
  69. Zhong, S.; Li, H.; Bodi, Z.; Button, J.; Vespa, L.; Herzog, M.; Fray, R.G. MTA Is an Arabidopsis Messenger RNA Adenosine Methylase and Interacts with a Homolog of a Sex-Specific Splicing Factor. Plant Cell 2008, 20, 1278–1288. [Google Scholar] [CrossRef] [Green Version]
  70. Vespa, L.; Vachon, G.; Berger, F.; Perazza, D.; Faure, J.-D.; Herzog, M. The Immunophilin-Interacting Protein AtFIP37 from Arabidopsis Is Essential for Plant Development and Is Involved in Trichome Endoreduplication. Plant Physiol. 2004, 134, 1283–1292. [Google Scholar] [CrossRef] [Green Version]
  71. Ma, K.; Han, J.; Zhang, Z.; Li, H.; Zhao, Y.; Zhu, Q.; Xie, Y.; Liu, Y.; Chen, L. OsEDM2L mediates m6A of EAT1 transcript for proper alternative splicing and polyadenylation regulating rice tapetal degradation. J. Integr. Plant Biol. 2021, 63, 1982–1994. [Google Scholar] [CrossRef]
  72. Scutenaire, J.; Deragon, J.-M.; Jean, V.; Benhamed, M.; Raynaud, C.; Favory, J.-J.; Merret, R.; Bousquet-Antonelli, C. The YTH Domain Protein ECT2 Is an m6A Reader Required for Normal Trichome Branching in Arabidopsis. Plant Cell 2018, 30, 986–1005. [Google Scholar] [CrossRef] [Green Version]
  73. Ruužička, K.; Zhang, M.; Campilho, A.; Bodi, Z.; Kashif, M.; Saleh, M.; Eeckhout, D.; El-Showk, S.; Li, H.; Zhong, S.; et al. Identification of factors required for m6A mRNA methylation in Arabidopsis reveals a role for the conserved E3 ubiquitin ligase HAKAI. New Phytol. 2017, 215, 157–172. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  74. Zhou, L.; Tang, R.; Li, X.; Tian, S.; Li, B.; Qin, G. N6-methyladenosine RNA modification regulates strawberry fruit ripening in an ABA-dependent manner. Genome Biol. 2021, 22, 168. [Google Scholar] [CrossRef] [PubMed]
  75. Dante, R.A.; Larkins, B.A.; Sabelli, P.A. Cell cycle control and seed development. Front. Plant Sci. 2014, 5, 493. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  76. Savadi, S. Molecular regulation of seed development and strategies for engineering seed size in crop plants. Plant Growth Regul. 2017, 84, 401–422. [Google Scholar] [CrossRef]
  77. Katsuya-Gaviria, K.; Caro, E.; Carrillo-Barral, N.; Iglesias-Fernández, R. Reactive Oxygen Species (ROS) and Nucleic Acid Modifications during Seed Dormancy. Plants 2020, 9, 679. [Google Scholar] [CrossRef]
  78. Bodi, Z.; Zhong, S.; Mehra, S.; Song, J.; Graham, N.; Li, H.; May, S.; Fray, R.G. Adenosine Methylation in Arabidopsis mRNA is Associated with the 3′ End and Reduced Levels Cause Developmental Defects. Front. Plant Sci. 2012, 3, 48. [Google Scholar] [CrossRef] [Green Version]
  79. Aslam, M.; Huang, X.; Yan, M.; She, Z.; Lu, X.; Fakher, B.; Chen, Y.; Li, G.; Qin, Y. TRM61 is essential for Arabidopsis embryo and endosperm development. Plant Reprod. 2021, 35, 31–46. [Google Scholar] [CrossRef]
  80. Huong, T.T.; Ngoc, L.N.T.; Kang, H. Functional Characterization of a Putative RNA Demethylase ALKBH6 in Arabidopsis Growth and Abiotic Stress Responses. Int. J. Mol. Sci. 2020, 21, 6707. [Google Scholar] [CrossRef]
  81. Cui, X.; Liang, Z.; Shen, L.; Zhang, Q.; Bao, S.; Geng, Y.; Zhang, B.; Leo, V.; Vardy, L.; Lu, T.; et al. 5-Methylcytosine RNA Methylation in Arabidopsis thaliana. Mol. Plant 2017, 10, 1387–1399. [Google Scholar] [CrossRef] [Green Version]
  82. Arribas-Hernández, L.; Brodersen, P. Occurrence and Functions of m6A and Other Covalent Modifications in Plant mRNA. Plant Physiol. 2020, 182, 79–96. [Google Scholar] [CrossRef] [Green Version]
  83. Lu, L.; Zhang, Y.; He, Q.; Qi, Z.; Zhang, G.; Xu, W.; Yi, T.; Wu, G.; Li, R. MTA, an RNA m6A Methyltransferase, Enhances Drought Tolerance by Regulating the Development of Trichomes and Roots in Poplar. Int. J. Mol. Sci. 2020, 21, 2462. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  84. Ortigosa, F.; Lobato-Fernández, C.; Pérez-Claros, J.A.; Cantón, F.R.; Ávila, C.; Cánovas, F.M.; Cañas, R.A. Epitranscriptome changes triggered by ammonium nutrition regulate the proteome response of maritime pine roots. bioRxiv 2021. [Google Scholar] [CrossRef]
  85. Cheng, Q.; Wang, P.; Wu, G.; Wang, Y.; Tan, J.; Li, C.; Zhang, X.; Liu, S.; Huang, S.; Huang, T.; et al. Coordination of m6A mRNA methylation and gene transcriptome in rice response to cadmium stress. Rice 2021, 14, 62. [Google Scholar] [CrossRef] [PubMed]
  86. Yang, Z.; Deng, C.; Wu, Y.; Dai, Z.; Tang, Q.; Cheng, C.; Xu, Y.; Hu, R.; Liu, C.; Chen, X.; et al. Insights into the mechanism of multi-walled carbon nanotubes phytotoxicity in Arabidopsis through transcriptome and m6A methylome analysis. Sci. Total Environ. 2021, 787, 147510. [Google Scholar] [CrossRef]
  87. Yu, Q.; Liu, S.; Yu, L.; Xiao, Y.; Zhang, S.; Wang, X.; Xu, Y.; Yu, H.; Li, Y.; Yang, J.; et al. RNA demethylation increases the yield and biomass of rice and potato plants in field trials. Nat. Biotechnol. 2021, 39, 1581–1588. [Google Scholar] [CrossRef] [PubMed]
  88. Song, P.; Yang, J.; Wang, C.; Lu, Q.; Shi, L.; Tayier, S.; Jia, G. Arabidopsis N6-methyladenosine reader CPSF30-L recognizes FUE signals to control polyadenylation site choice in liquid-like nuclear bodies. Mol. Plant 2021, 14, 571–587. [Google Scholar] [CrossRef]
  89. Yang, D.; Xu, H.; Liu, Y.; Li, M.; Ali, M.; Xu, X.; Lu, G. RNA N6-Methyladenosine Responds to Low-Temperature Stress in Tomato Anthers. Front. Plant Sci. 2021, 12, 1077. [Google Scholar] [CrossRef]
  90. Ngoc, L.N.T.; Park, S.J.; Huong, T.T.; Lee, K.H.; Kang, H. N4-methylcytidine ribosomal RNA methylation in chloroplasts is crucial for chloroplast function, development, and abscisic acid response in Arabidopsis. J. Integr. Plant Biol. 2021, 63, 570–582. [Google Scholar] [CrossRef]
  91. Shoaib, Y.; Hu, J.; Manduzio, S.; Kang, H. Alpha-ketoglutarate-dependent dioxygenase homolog 10B, an N 6 -methyladenosine mRNA demethylase, plays a role in salt stress and abscisic acid responses in Arabidopsis thaliana. Physiol. Plant. 2021, 173, 1078–1089. [Google Scholar] [CrossRef]
  92. Zhu, C.; Zhang, S.; Zhou, C.; Xie, S.; Chen, G.; Tian, C.; Xu, K.; Lin, Y.; Lai, Z.; Guo, Y. Genome-Wide Investigation of N6-Methyladenosine Regulatory Genes and Their Roles in Tea (Camellia sinensis) Leaves During Withering Process. Front. Plant Sci. 2021, 12, 1183. [Google Scholar] [CrossRef]
  93. He, Y.; Li, L.; Yao, Y.; Li, Y.; Zhang, H.; Fan, M. Transcriptome-wide N6-methyladenosine (m6A) methylation in watermelon under CGMMV infection. BMC Plant Biol. 2021, 21, 516. [Google Scholar] [CrossRef] [PubMed]
  94. Bai, C.; Fang, M.; Zhai, B.; Ma, L.; Fu, A.; Gao, L.; Kou, X.; Meng, D.; Wang, Q.; Zheng, S.; et al. Regulations of m6A methylation on tomato fruit chilling injury. Hortic. Plant J. 2021, 7, 434–442. [Google Scholar] [CrossRef]
  95. Sun, J.; Bie, X.M.; Wang, N.; Zhang, X.S.; Gao, X.-Q. Genome-wide identification and expression analysis of YTH domain-containing RNA-binding protein family in common wheat. BMC Plant Biol. 2020, 20, 351. [Google Scholar] [CrossRef] [PubMed]
  96. Tian, S.; Wu, N.; Zhang, L.; Wang, X. RNA N 6 -methyladenosine modification suppresses replication of rice black streaked dwarf virus and is associated with virus persistence in its insect vector. Mol. Plant Pathol. 2021, 22, 1070–1081. [Google Scholar] [CrossRef] [PubMed]
  97. Martínez-Pérez, M.; Aparicio, F.; López-Gresa, M.P.; Bellés, J.M.; Sanchez-Navarro, J.A.; Pallás, V. Arabidopsis m6A demethylase activity modulates viral infection of a plant virus and the m6A abundance in its genomic RNAs. Proc. Natl. Acad. Sci. USA 2017, 114, 10755–10760. [Google Scholar] [CrossRef] [Green Version]
  98. Guo, T.; Liu, C.; Meng, F.; Hu, L.; Fu, X.; Yang, Z.; Wang, N.; Jiang, Q.; Zhang, X.; Ma, F. The m6A reader MhYTP2 regulates MdMLO19 mRNA stability and antioxidant genes translation efficiency conferring powdery mildew resistance in apple. Plant Biotechnol. J. 2021, 20, 511–525. [Google Scholar] [CrossRef]
  99. Shi, Y.; Wang, H.; Wang, J.; Liu, X.; Lin, F.; Lu, J. N6-methyladenosine RNA methylation is involved in virulence of the rice blast fungus Pyricularia oryzae (syn. Magnaporthe oryzae). FEMS Microbiol. Lett. 2019, 366, 286. [Google Scholar] [CrossRef]
  100. Zhang, K.; Zhuang, X.; Dong, Z.; Xu, K.; Chen, X.; Liu, F.; He, Z. The dynamics of N6-methyladenine RNA modification in interactions between rice and plant viruses. Genome Biol. 2021, 22, 579–589. [Google Scholar] [CrossRef]
  101. Li, Z.; Shi, J.; Yu, L.; Zhao, X.; Ran, L.; Hu, D.; Song, B. N 6 -methyl-adenosine level in Nicotiana tabacum is associated with tobacco mosaic virus. Virol. J. 2018, 15, 87. [Google Scholar] [CrossRef] [Green Version]
  102. Zheng, H.; Li, S.; Zhang, X.; Sui, N. Functional Implications of Active N6-Methyladenosine in Plants. Front. Cell Dev. Biol. 2020, 8, 291. [Google Scholar] [CrossRef]
  103. Tang, Y.; Gao, C.-C.; Gao, Y.; Yang, Y.; Shi, B.; Yu, J.-L.; Lyu, C.; Sun, B.-F.; Wang, H.-L.; Xu, Y.; et al. OsNSUN2-Mediated 5-Methylcytosine mRNA Modification Enhances Rice Adaptation to High Temperature. Dev. Cell 2020, 53, 272–286.e7. [Google Scholar] [CrossRef] [PubMed]
  104. Wang, W.; Li, W.; Cheng, Z.; Sun, J.; Gao, J.; Li, J.; Niu, X.; Amjid, M.W.; Yang, H.; Zhu, G.; et al. Transcriptome-wide N6-methyladenosine profiling of cotton root provides insights for salt stress tolerance. Environ. Exp. Bot. 2021, 194, 104729. [Google Scholar] [CrossRef]
  105. Motley, J. Exploring the Roles of GCN2 and the m6A RNA Modification in Plant Immunity. Ph.D. Thesis, University Program in Genetics and Genomics Duke University, Durham, NC, USA, 2019. [Google Scholar]
  106. Luo, J.-H.; Wang, M.; Jia, G.-F.; He, Y. Transcriptome-wide analysis of epitranscriptome and translational efficiency associated with heterosis in maize. J. Exp. Bot. 2021, 72, 2933–2946. [Google Scholar] [CrossRef] [PubMed]
  107. Murik, O.; Chandran, S.A.; Nevo-Dinur, K.; Sultan, L.D.; Best, C.; Stein, Y.; Hazan, C.; Ostersetzer-Biran, O. Topologies of N6-adenosine methylation (m6A) in land plant mitochondria and their putative effects on organellar gene expression. Plant J. 2019, 101, 1269–1286. [Google Scholar] [CrossRef]
  108. Li, A.; Chen, Y.-S.; Ping, X.-L.; Yang, X.; Xiao, W.; Yang, Y.; Sun, H.-Y.; Zhu, Q.; Baidya, P.; Wang, X.; et al. Cytoplasmic m6A reader YTHDF3 promotes mRNA translation. Cell Res. 2017, 27, 444–447. [Google Scholar] [CrossRef] [Green Version]
  109. Wang, X.; Lu, Z.; Gomez, A.; Hon, G.C.; Yue, Y.; Han, D.; Fu, Y.; Parisien, M.; Dai, Q.; Jia, G.; et al. N6-methyladenosine-dependent regulation of messenger RNA stability. Nature 2014, 505, 117–120. [Google Scholar] [CrossRef]
  110. Shi, H.; Wang, X.; Lu, Z.; Zhao, B.S.; Ma, H.; Hsu, P.J.; Liu, C.; He, C. YTHDF3 facilitates translation and decay of N6-methyladenosine-modified RNA. Cell Res. 2017, 27, 315–328. [Google Scholar] [CrossRef] [Green Version]
  111. Anderson, S.J.; Kramer, M.C.; Gosai, S.J.; Yu, X.; Vandivier, L.E.; Nelson, A.D.; Anderson, Z.D.; Beilstein, M.A.; Fray, R.G.; Lyons, E.; et al. N6-Methyladenosine Inhibits Local Ribonucleolytic Cleavage to Stabilize mRNAs in Arabidopsis. Cell Rep. 2018, 25, 1146–1157.e3. [Google Scholar] [CrossRef] [Green Version]
  112. Linder, B.; Grozhik, A.V.; Olarerin-George, A.O.; Meydan, C.; Mason, C.E.; Jaffrey, S.R. Single-nucleotide-resolution mapping of m6A and m6Am throughout the transcriptome. Nat. Methods 2016, 12, 767–772. [Google Scholar] [CrossRef]
  113. Garcia-Campos, M.A.; Edelheit, S.; Toth, U.; Safra, M.; Shachar, R.; Viukov, S.; Winkler, R.; Nir, R.; Lasman, L.; Brandis, A.; et al. Deciphering the “m6A Code” via Antibody-Independent Quantitative Profiling. Cell 2019, 178, 731–747.e16. [Google Scholar] [CrossRef]
  114. Parker, M.T.; Knop, K.; Sherwood, A.V.; Schurch, N.J.; Mackinnon, K.; Gould, P.D.; Hall, A.J.; Barton, G.J.; Simpson, G.G. Nanopore direct RNA sequencing maps the complexity of Arabidopsis mRNA processing and m6A modification. eLife 2020, 9, 1–35. [Google Scholar] [CrossRef] [PubMed]
  115. Zhou, L.; Gao, G.; Tang, R.; Wang, W.; Wang, Y.; Tian, S.; Qin, G. m6A-mediated regulation of crop development and stress responses. Plant Biotechnol. J. 2022, 1–9. [Google Scholar] [CrossRef]
  116. Gallego-Bartolome, J.; Gardiner, J.; Liu, W.; Papikian, A.; Ghoshal, B.; Kuo, H.Y.; Zhao, J.M.-C.; Segal, D.J.; Jacobsen, S.E. Targeted DNA demethylation of the Arabidopsis genome using the human TET1 catalytic domain. Proc. Natl. Acad. Sci. USA 2018, 115, E2125–E2134. [Google Scholar] [CrossRef] [Green Version]
  117. Papikian, A.; Liu, W.; Gallego-Bartolomé, J.; Jacobsen, S.E. Site-specific manipulation of Arabidopsis loci using CRISPR-Cas9 SunTag systems. Nat. Commun. 2019, 10, 729. [Google Scholar] [CrossRef] [PubMed]
Figure 1. Regulation of plant’s development by post-transcriptional modifications (m6A and m5C); post-transcriptional modifications regulated by different writer, eraser, and reader proteins affect various plant developmental processes including seed development, leaf and root growth, floral transitions, and fruit ripening.
Figure 1. Regulation of plant’s development by post-transcriptional modifications (m6A and m5C); post-transcriptional modifications regulated by different writer, eraser, and reader proteins affect various plant developmental processes including seed development, leaf and root growth, floral transitions, and fruit ripening.
Plants 11 01033 g001
Figure 2. Various cellular processes affected by m6A RNA methylation; m6A RNA reader proteins determine the fate of modified transcripts and direct their export from the nucleus to the cytoplasm, where transcripts may be translated by the ribosomes, and stored in the granules, or decayed by the P-bodies.
Figure 2. Various cellular processes affected by m6A RNA methylation; m6A RNA reader proteins determine the fate of modified transcripts and direct their export from the nucleus to the cytoplasm, where transcripts may be translated by the ribosomes, and stored in the granules, or decayed by the P-bodies.
Plants 11 01033 g002
Figure 3. Molecular and physiological regulation by m6A and m5C; m6A and m5C modifications regulate various molecular processes including mRNA stability, translation and alternative polyadenylation that affect plant growth and development processes such as anther development, trichome morphology, flowering, SAM proliferation, leaf growth, root growth, and stress responses.
Figure 3. Molecular and physiological regulation by m6A and m5C; m6A and m5C modifications regulate various molecular processes including mRNA stability, translation and alternative polyadenylation that affect plant growth and development processes such as anther development, trichome morphology, flowering, SAM proliferation, leaf growth, root growth, and stress responses.
Plants 11 01033 g003
Figure 4. Improving useful traits through m6A editing; Various plant developmental processes such as seed development, anther development, root growth, floral transition, photosynthesis, fruit ripening, seed yield, and stress resistance can be improved through m6A editing.
Figure 4. Improving useful traits through m6A editing; Various plant developmental processes such as seed development, anther development, root growth, floral transition, photosynthesis, fruit ripening, seed yield, and stress resistance can be improved through m6A editing.
Plants 11 01033 g004
Table 1. Role of post-transcriptional modifications in plants’ growth and development.
Table 1. Role of post-transcriptional modifications in plants’ growth and development.
GeneModificationDevelopmental RolePlant SpeciesReference
TRM61/TRM6tRNA (m1A)EmbryogenesisArabidopsis thaliana[53,65]
PhTRMT61AmRNA (m1A)leaf developmentPetunia[66]
AtTRM5tRNAleaf and root developmentArabidopsis thaliana[67]
(m1G, m1I)flowering time regulastion
TCTP1mRNA (m5C)root growthArabidopsis thaliana[68]
FIP37mRNA (m6A)embryo developmentArabidopsis thaliana[69]
trichome endoreduplication
and shoot stem cell fate
OsEMD2LmRNA (m6A)anther developmentOryza sativa[71]
ECT2mRNA (m6A)trichome branching,Arabidosis thaliana[33,72]
trichome morphology
MTA, MTB,mRNA (m6A)vascular formation inArabidopsis thaliana[73]
FIP37, VIR, roots, pattern formation
MTA, MTBmRNA (m6A)fruit ripeningFragaria ananassa[74]
Table 2. Role of post-transcriptional modifications in stress responses.
Table 2. Role of post-transcriptional modifications in stress responses.
ModificationSpeciesStressRegulatory RoleReference
rRNAArabidopsis thalianaLowConfers cold stress tolerance[64]
(m2G) temperatureby resulting translation of chloroplast proteins including RbcL, AtpB, PsbA, Ycf3, and PetC
mRNAOryzahighConfers heat acclimation through regulating translation of transcripts involved in photosynthesis and detoxification such as β- OsLCY, OsHO2, OsPAL1, and OsGLYI4[103]
tRNAOryzasalinityConfers salts stress tolerance by[59]
(Am)sativa regulating the expression level of ABA-related (SnRK2.1, ABA1, ABI5, AAO3, and RCAR1) and salt-related (HKT1, NHX1, and SOS1) genes
mRNASorghumsalinityConfers salts stress tolerance by regulating the mRNA stability of several stress-responsive transcripts including AVP1 and IAR4[35]
mRNAGossypiumsalinityConfers salt stress tolerance by stabilizing the salt-responsive gene transcripts and regulating the levels of genes involved in zeatin biosynthesis, taurine and hypotaurine metabolism, and ribosome and proteasome processes[104]
(m6A)hirsutum acc.
mRNAPopulusdroughtConfers drought resistance by affecting trichome and root development[83]
mRNAArabidopsis thalianabacterialInduced pattern-triggered immunity (PTI) and salicylic acid (SA)-mediated immune responses through an enhanced abundance of defense-related transcripts[105]
(m6A) attack
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Shoaib, Y.; Usman, B.; Kang, H.; Jung, K.-H. Epitranscriptomics: An Additional Regulatory Layer in Plants’ Development and Stress Response. Plants 2022, 11, 1033.

AMA Style

Shoaib Y, Usman B, Kang H, Jung K-H. Epitranscriptomics: An Additional Regulatory Layer in Plants’ Development and Stress Response. Plants. 2022; 11(8):1033.

Chicago/Turabian Style

Shoaib, Yasira, Babar Usman, Hunseung Kang, and Ki-Hong Jung. 2022. "Epitranscriptomics: An Additional Regulatory Layer in Plants’ Development and Stress Response" Plants 11, no. 8: 1033.

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop