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Usman, B.; Jung, K.H.; Shoaib, Y.; Kang, H. Developmental and Physiological Regulation by Epitranscriptomic Modifications. Encyclopedia. Available online: https://encyclopedia.pub/entry/22736 (accessed on 20 November 2024).
Usman B, Jung KH, Shoaib Y, Kang H. Developmental and Physiological Regulation by Epitranscriptomic Modifications. Encyclopedia. Available at: https://encyclopedia.pub/entry/22736. Accessed November 20, 2024.
Usman, Babar, Ki Hong Jung, Yasira Shoaib, Hunseung Kang. "Developmental and Physiological Regulation by Epitranscriptomic Modifications" Encyclopedia, https://encyclopedia.pub/entry/22736 (accessed November 20, 2024).
Usman, B., Jung, K.H., Shoaib, Y., & Kang, H. (2022, May 10). Developmental and Physiological Regulation by Epitranscriptomic Modifications. In Encyclopedia. https://encyclopedia.pub/entry/22736
Usman, Babar, et al. "Developmental and Physiological Regulation by Epitranscriptomic Modifications." Encyclopedia. Web. 10 May, 2022.
Developmental and Physiological Regulation by Epitranscriptomic Modifications
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This entry is adapted from the peer-reviewed paper 10.3390/plants11081033

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.

epitranscriptomics plant development plants methylation genome editing

1. 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.
Table 1. Role of post-transcriptional modifications in plants’ growth and development.
Gene Modification Developmental Role Plant Species Reference
TRM61/TRM6 tRNA (m1A) Embryogenesis Arabidopsis thaliana [1][2]
Complex        
PhTRMT61A mRNA (m1A) leaf development Petunia [3]
AtTRM5 tRNA leaf and root development Arabidopsis thaliana [4]
  (m1G, m1I) flowering time regulastion    
TCTP1 mRNA (m5C) root growth Arabidopsis thaliana [5]
FIP37 mRNA (m6A) embryo development Arabidopsis thaliana [6]
    trichome endoreduplication
and shoot stem cell fate		   [7][8]
OsEMD2L mRNA (m6A) anther development Oryza sativa [9]
ECT2 mRNA (m6A) trichome branching, Arabidosis thaliana [10][11]
    trichome morphology    
MTA, MTB, mRNA (m6A) vascular formation in Arabidopsis thaliana [12]
FIP37, VIR,   roots, pattern formation    
HAKAI        
MTA, MTB mRNA (m6A) fruit ripening Fragaria ananassa [13]

2. Seed Development

Seed development is a complex process integrating different genetic, metabolic, and physiological pathways regulated by transcriptional, epigenetic, peptide hormone, and sugar regulators [14][15]. 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 [16]. 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 [6][17]. 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 [18]. 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 [19].

3. 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 [20]. 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 [21]. 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 [4]. The m6A writer and reader proteins are highly expressed in the root meristems, apexes, and lateral root primordia [6][12][22]. 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 [23]. 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 [24]. 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 [25]. 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 [12]. Another study has shown that multi-walled carbon nanotubes inhibit root growth by reducing m6A levels [26]. 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 [27]. 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 [22]. Genes affecting various plant developmental processes such as floral transition [28][29], seed development [13][16][30], root growth [16][31], leaf growth [22], and fruit ripening [17][32] are illustrated in Figure 1.
Plants 11 01033 g001 550
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.

4. 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 [9]. 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 [27]. 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 [33]. 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 [34].

5. 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 [28]. 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 [4]. 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 [35].

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Subjects: Agriculture, Dairy & Animal Science
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Babar Usman
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Ki Hong Jung
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Yasira Shoaib
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Hunseung Kang
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Update Date: 10 May 2022
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