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Liu, Y.; Zhu, Q.; Li, W.; Chen, P.; Xue, J.; Yu, Y.; Feng, Y. Noncoding RNAs Involved in Diverse Flowering Pathways. Encyclopedia. Available online: https://encyclopedia.pub/entry/52317 (accessed on 01 September 2024).
Liu Y, Zhu Q, Li W, Chen P, Xue J, Yu Y, et al. Noncoding RNAs Involved in Diverse Flowering Pathways. Encyclopedia. Available at: https://encyclopedia.pub/entry/52317. Accessed September 01, 2024.
Liu, Yun, Qing-Feng Zhu, Wen-Yan Li, Pei Chen, Jiao Xue, Yang Yu, Yan-Zhao Feng. "Noncoding RNAs Involved in Diverse Flowering Pathways" Encyclopedia, https://encyclopedia.pub/entry/52317 (accessed September 01, 2024).
Liu, Y., Zhu, Q., Li, W., Chen, P., Xue, J., Yu, Y., & Feng, Y. (2023, December 04). Noncoding RNAs Involved in Diverse Flowering Pathways. In Encyclopedia. https://encyclopedia.pub/entry/52317
Liu, Yun, et al. "Noncoding RNAs Involved in Diverse Flowering Pathways." Encyclopedia. Web. 04 December, 2023.
Noncoding RNAs Involved in Diverse Flowering Pathways
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This entry is adapted from the peer-reviewed paper 10.3390/genes14122114

Noncoding RNAs constitute a substantial portion of the transcriptome and play pivotal roles in plant growth and development. Among these processes, flowering stands out as a crucial trait, ensuring reproductive success and seed set, and is meticulously controlled by genetic and environmental factors. With remarkable advancements in the identification and characterization of noncoding RNAs in plants, it has become evident that noncoding RNAs are intricately linked to the regulation of flowering time. The regulation of flowering encompasses a complex network of interconnected pathways influenced by both internal and external factors. Early investigations in model plants unveiled several key pathways governing flowering time, including the photoperiodic, autonomous and vernalization, age, and GA pathways. Among the pivotal regulators of flowering, noncoding RNAs have emerged as participants in various flowering pathways.

noncoding RNAs flowering time biological role molecular mechanism

1. Photoperiodic Pathway

The photoperiodic pathway, characterized by the differential stability and activity of CONSTANS (CO), plays a pivotal role in modulating flowering time. CO, a rhythmically expressed gene, exhibits responsiveness to both circadian rhythms and light stimuli under varying daylengths [1]. This dynamic regulation influences the accumulation of FT, thereby contributing to the precise temporal control of flowering events. Noncoding RNAs play a crucial regulatory role in photoperiodic flowering by influencing circadian rhythms or upstream factors of CO. For instance, miR397b targets CKB3, impacting the activity of CCA1, a central component of the circadian clock. Overexpressing miR397b extends the circadian clock period, consequently delaying flowering. Conversely, miR397b is negatively regulated by CCA1, establishing a negative feedback loop of miR397b-CKB3-CCA1 [2]. The lncRNA FLORE, a natural antisense transcript of CDF5, inhibited the expression of CDF5. CDFs, under circadian transcriptional and post-translational control, are repressors of CO and FT; thus, overexpression of FLORE promotes flowering by upregulation of CO and FT [1][3]. The reciprocal inhibition of FLORE and CDF5 is crucial for maintaining their oscillations [4].
Besides functioning upstream of CO, evidence also shows that noncoding RNAs function downstream of CO to regulate flowering. Overexpression of RIFLA, an lncRNA transcribed from the intron of OsMADS56, results in earlier flowering than the wild type under long-day conditions [5]. OsMADS56 is the ortholog of the Arabidopsis SOC1 in rice, positioned downstream of CO, facilitating the integration of signals conveyed by CO to promote flowering in plants. However, in contrast to facultative long-day plants, overexpression of OsMADS56 in short-day crop plants like rice delays flowering under long-day conditions. Additionally, miR5200 in Brachypodium distachyon is epigenetically regulated by daylength and short-day induction, leading to delayed flowering by targeting FTL1 and FTL2 [6]. However, the diurnal or circadian expression patterns of these genes have not been elucidated. Understanding their expression patterns would significantly contribute to researchers' comprehension of their roles within the photoperiodic pathway, allowing for better utilization and manipulation of their functions.

2. Autonomous Pathway and Vernalization Pathway

Plants require exposure to low temperatures to induce flowering, a phenomenon known as vernalization. Vernalization induces the inactivation of FLC, thereby promoting flowering. The autonomous pathway comprises the complex of FLOWERING LOCUS CA (FCA), FLOWERING LOCUS PA (FPA), FLOWERING LOCUS KH DOMAIN (FLK), and FLOWERING LOCUS Y (FY), responsible for repressing the expression of FLC by modifying 3′ end processing and antisense RNA polyadenylation at FLC [7]. If the complex of the autonomous pathway is absent, even vernalized plants cannot flower early. Hence, FLC occupies a central position between the vernalization and autonomous pathways [8]. LncRNAs such as COOLAIR, COLDAIR, and COLDWRAP are induced by cold treatment, mimicking winter conditions, and repress FLC expression. COOLAIR, an antisense lncRNA originating from the 3′ end of FLC, promotes flowering by repressing FLC expression [9][10]. COLDAIR is a sense lncRNA from the intron of FLC, and perturbating the association between COLDAIR and FLC delays flowering time in Arabidopsis [11]. Another lncRNA, COLDWRAP, derived from the promoter of FLC, also contributes to the de-repression of flowering in coordination with COLDAIR [12]. In addition, FPA, FCA, and FY can also regulate the alternative splicing of COOLAIR, recruiting FLD for H3K4me2 demethylation on FLC. These findings suggest that FLC is intricately regulated by noncoding RNAs, involving both the vernalization and autonomous pathways [7][13]. However, the interplay between noncoding RNAs such as COOLAIR, COLDAIR, and COLDWRAP in coordinating FLC modifications and regulating FLC expression requires further in-depth investigation. Additionally, datasets have shown that the flowering repressor genes FLC and FLM in Arabidopsis produce circRNAs [14]. These findings indicate that FLC, positioned at the intersection of the vernalization and autonomous pathways, is subject to regulation by various noncoding RNAs.
Besides the FLC locus, long noncoding RNAs generated from other loci have also been reported to regulate the vernalization pathway. A natural antisense transcript (NAT) from MADS AFFECTING FLOWERING 4 (MAF4) called MAS is also cold-induced and activates MAF4 expression to inhibit premature flowering [15]. Although the function of MAF4 appears to oppose the long noncoding RNAs generated from the FLC locus, this ensures that the plant flowers only after experiencing a sufficiently long period of low temperatures. Additionally, there are other long noncoding RNAs that have been identified through transcriptome data screening. LncRNA TCONS_00035129 in Brassica rapa is induced by vernalization, positively correlating with BraZF-HD21 [16]. LncRNA AGL15X2 in Beta vulgaris L. reaches peak expression after 16 weeks of vernalization, promoting flowering by repressing BvFT1 [17]. An intergenic lncRNA, FLINC from Arabidopsis, has been identified to play a role in temperature-mediated flowering. Overexpression of FLINC increases sensitivity to changes in ambient temperature [18]. However, how these long noncoding RNAs respond to vernalization and are induced for expression and the mechanistic understanding of these long noncoding RNAs remain incomplete, necessitating further molecular biology and genetic research for elucidation.

3. Aging Pathway

Plant age is a critical factor in regulating the transition to flowering, and research has indicated a close correlation between age and miR156/miR172. MiR156 exhibits higher expression levels in juvenility, gradually decreasing with age, crucial for maintaining the juvenile phase. Subsequent studies have demonstrated that the temporal expression of miR156 is regulated by sugars synthesized during photosynthesis. MiR156 targets the SQUAMOSA promoter binding protein-like (SPL) family, known as flowering-promoting factors, where the gradual downregulation of miR156 leads to a progressive increase in SPL expression. Overexpression of miR156 extends the juvenile stage and delays flowering in several plant species, including Arabidopsis, rice, Zea mays ssp. mays (maize), Lycopersicon esculentum (tomato), Populus × canadensis , Lilium × formolongi, and Gossypium hirsutum L. (cotton), underscoring the conserved function of this miRNA family [19][20][21][22][23]. Notably, in Physcomitrella patens, miR156 exhibits an opposing role by promoting the formation of leafy gametophores [24]. The SPL family encodes a group of transcription factors targeted by miR156. In Arabidopsis, miR156 targets 11 of 17 SPL members, with SPL3/4/5/9/15 being key contributors to flowering time regulation [25]. Gradually increased SPL9, 10, and 15 can bind to the promoter region of MIR172B, enhancing its expression and consequently downregulating the expression of the flowering repressor genes APETALA2 (AP2) and AP2-like. Thus, miR172 acts downstream of miR156 and SPL9 and its abundance increases with plant age, exhibiting an expression pattern opposite to miR156. Overexpressing miR172 accelerates flowering in plants, contrasting the effects of miR156 [26]. Target analysis reveals that miR172 represses AP2, SMZ, SNZ, and TOE1/2/3 [27][28][29]. Therefore, miR156-SPLs-miR172 defines an age pathway in a wide range of plants.
It is interesting that some other noncoding RNAs are predicted to target miR156 and miR172, acting as decoys to inhibit their binding to their respective target genes. For example, circ-CCR2, circ-SEC5A, and circ-EF1B may be involved in aging pathways, as they sponge miR156 or miR172 in soybean [30]. However, whether these circRNAs have an impact on aging and their actual role in regulating flowering time remains to be studied. Recently, heterologous expression of lncRNA bra-miR156HG from Brassica campestris (Chinese cabbage), which is assumed to be the precursor of miR156, leads to delayed flowering in Arabidopsis. However, overexpression of this lncRNA alters leaf morphology instead of changing flowering time in Chinese cabbage [31]. This indicates that various types of noncoding RNAs collaborate to regulate flowering in a single pathway, a phenomenon that is relatively scarce in plants currently.
Furthermore, age can also regulate miRNA splicing in a post-transcriptional manner. The splicing isoforms of miR528 are regulated by age. Pri-miR528 has two splicing variants, MIR528-T1 and MIR528-T2. In MIR528-T1, the 3′ end is shortened by 103 nucleotides due to proximal polyadenylation, while in MIR528-T2, it is shortened by 98 nucleotides due to intron splicing, although the mature sequence of miR528 is the same. Older plants tend to produce the MIR528-T2 isoform, which weakens the ability to yield mature miR528, which promotes flowering by targeting OsRFI2 [32]. This age-regulated splicing of miR528 represents a fine-tuning mechanism, enhancing its ability to promote flowering just before the reproductive transition. Further investigation is required to elucidate which factor regulates the splicing of miR528 and whether it is correlated with miR156 or miR172.

4. Phytohormone-Related Pathways

GA was initially considered the primary plant hormone regulating flowering, and its pathway has been extensively studied. DELLA proteins function as negative regulators in the GA signaling pathway, inhibiting the floral integrator factor SOC1 and thereby impeding flowering. GA promotes the degradation of DELLA proteins, relieving SOC1 inhibition and promoting flowering [33]. MiR159 targets MYB transcription factors responsive to GA [34]. However, the inconsistencies in flowering phenotypes between miR159 and target MYB mutants suggest the involvement of other factors in this regulatory module [35].
Other plant hormone signaling components may indirectly regulate flowering by interacting with DELLA proteins. MiR390-TAS3-tasiRNAs participate in auxin-mediated flowering by targeting auxin response factor (ARF) 3/4 [36]. ARFs are negatively regulated by the auxin receptor Aux/IAA, which can indirectly modulate flowering by promoting GA20ox or inhibiting GA2ox to increase GA levels [37]. Additionally, Aux/IAA negatively regulates DELLA proteins, demonstrating the collaborative role of auxin and GA in flowering [38]. Similarly, OsmiR393 targets the auxin receptors OsTIR1 and OsAFB2, and overexpression of miR393 affects auxin signaling, thereby impacting flowering time [39].
Brassinosteroids (BRs) are a group of polyhydroxylated steroidal hormones crucial in plant growth and development. Mutants lacking BRs exhibit delayed flowering, a phenotype restored by exogenous GA supplementation, demonstrating the synergistic action between BRs and GA [40]. Additionally, BR signaling can function independently of GA. In Arabidopsis, the BR signaling component BZR1 recruits the H3K27 demethylase ELF6 to the FLC gene locus, inducing H3K27 demethylation and consequently activating FLC expression and promoting flowering [41]. In rice, although there is no homologous gene to FLC [42], a study has indicated that overexpression of OsmiR397 enhances the plant’s BR signal, with an earlier heading time [43]. While the exact cause remains unclear, this suggests the potential existence of an alternative mechanism for BR-mediated flowering regulation in rice.
Additionally, some noncoding RNA-mediated pathways regulating flowering remain unclear or challenging to categorize into specific pathways. For instance, in rice, overexpression of miR168 can elevate miR164 levels, delaying flowering [44]. MiR164 targets the transcription factors CUC1 and CUC2, which are crucial for the formation of floral organ boundaries [45]. Ef-cd is an antisense lncRNA overlapping with OsSOC1, and it shortens the maturity duration, thereby accelerating heading in rice [46]. This example is challenging to categorize within the mentioned pathways since SOC1 is a gene downstream in the process, where all pathways converge to trigger flowering. Recently, an intergenic lncRNA, FLAIL, was identified, and its mutants displayed an early flowering phenotype, indicating that FLAIL acts as a flowering repressor [47]. Mechanistic studies indicate that FLAIL reduces the expression of LAC8 by influencing alternative splicing, consequently altering the flowering time. Interestingly, LAC8 belongs to the laccase family along with the OsmiR397 target gene OsLAC13, hinting at potential flowering control pathways associated with laccase-related mechanisms in plants [43]. In citrus, overexpression of miR3954 promotes the production of phasiRNAs that target NAC genes, facilitating the regulation of flowering time [3].
In Arabidopsis, a circRNA derived from the intron of At5g37720 significantly delays flowering time, with reduced expression of FT [19]. However, its mechanism of action remains unclear, potentially involving the circRNA binding to certain proteins and exerting trans-regulation over FT expression. Recently, the loss of function of miR394a and miR394b in Arabidopsis resulted in early flowering with reduced branching and lower seed production [1]. However, the phenotypic alteration in flowering time does not correlate with the known target gene LCR. Therefore, the mechanism by which miR394 regulates flowering remains unknown. Further in-depth research in the future will help researchers comprehend these unknown regulatory mechanisms. It may establish connections with known pathways or create novel pathways to explain these phenomena.
In summary, noncoding RNAs intricately modulate plant flowering time through the complex web of pathways described above (Figure 1), although the mechanisms of some newly identified flowering-related noncoding RNAs are yet to be fully explored. The multifaceted involvement of noncoding RNAs underscores their pivotal role in the regulation of flowering time across various plant species (Table 1).
Genes 14 02114 g002
Figure 1. Noncoding RNAs involved in flowering time and their targets/downstream genes. Different colors of background represent different pathways, indicated by the word in red. CKB3: Casein Kinase Beta subunit 3; CDF5: CYCLING DOF FACTOR 5; CO: CONSTANS; FT: FLOWERING LOCUS T; COOLAIR: COLD INDUCED LONG ANTISENSE INTRAGENIC RNA; COLDAIR: COLD-ASSISTED INTRONIC NONCODING RNA; FLORE: CDF5 LONG NONCODING RNA; FLC: FLOWERING LOCUS C; MAF4: MADS AFFECTING FLOWERING 4; BraZF-HD21:Bra026812; MYB: v-myb avian myeloblastosis viral oncogene homolog transcription factor; TCP: TEOSINTE BRANCHED 1, CYCLOIDEA, POLIFERATING CELL FACTORS; TIR1:TRANSPORT INHIBITOR RESISTANT1; AFB:AUXIN SIGNALING F-BOX; TAS3: Trans-Acting Short Interference RNA3; ARF: auxin response factor; SPL: SQUAMOSA promoter binding protein-like; AP2: APETALA2 transcription factors; SNZ: SCHNARCHZAPFEN; SMZ: SCHLAFMUTZE;TOE: TARGET OF EAT.
Table 1. Summary of noncoding RNAs in regulating flowering time.
Species Categories Names Targets Functions Reference
Arabidopsis/rice/maize/tomato, etc. miRNA miR156 SPLs delays flowering [20][21]
Arabidopsis miRNA miR172 AP2/SMZ/SNZ /TOE accelerates flowering [48]
rice miRNA miR528 OsRFI2 promotes flowering under long-day conditions [32]
Arabidopsis miRNA miR159 MYB delays flowering in short day [49]
Arabidopsis miRNA miR319 TCP delays flowering in short day [50]
B. distachyon miRNA miR5200 FT promotes flowering under short-day conditions and inhibits flowering under long-day conditions [51]
rice miRNA miR393 OsTIR1/OsAFB2 increases tiller number and promotes heading [39]
rice miRNA miR168 AGO1 suppression of miR168 shortens flowering time [44]
Arabidopsis miRNA miR397 CKB3 delays flowering time by modulating the circadian clock [2]
Arabidopsis miRNA miR394a/
miR394b		 LCR loss-of-function showed early flowering with decreased branching and lower seed production [52]
Arabidopsis miRNA miR390 ARF3/ARF4 delays flowering time [24]
citrus miRNA miR3954 NAC facilitates flowering time [53]
Arabidopsis miRNA miR169 NF-YA promotes early flowering through the abiotic stress response [54]
Arabidopsis miRNA miR399 PHO2 promotes flowering at normal temperature [55]
Arabidopsis lncRNA COOLAIR FLC promotes flowering [56]
Arabidopsis lncRNA COLDAIR FLC promotes flowering [11]
Arabidopsis lncRNA COLDWRAP FLC promotes flowering [12]
B. rapa lncRNA TCONS_00035129 BraZF-HD21 promotes flowering [16]
sugar beet lncRNA AGL15X2 BvFT1 promotes reproductive growth upon vernalization [17]
Arabidopsis lncRNA FLINC not clear regulates temperature-mediated flowering [18]
Arabidopsis lncRNA FLORE FT promotes flowering in a circadian-dependent manner [4]
rice lncRNA Ef-cd OsSOC1 shortens maturity duration with no yield penalty [46]
Arabidopsis lncRNA FLAIL LAC8 represses flowering [47]
rice lncRNA RIFLA OsMADS56 promotes flowering [5]
Soybean circRNA circ-CCR2, circ-SEC5A, circ-EF1B miR172, miR156 induces the floral meristem [30]
Arabidopsis circRNA laciRNA from At5g37720 FT delays flowering [57]

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Subjects: Plant Sciences
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Yun Liu
,
Qing-Feng Zhu
,
Wen-Yan Li
,
Pei Chen
,
Jiao Xue
,
Yang Yu
,
Yan-Zhao Feng
View Times: 213
Revisions: 2 times (View History)
Update Date: 05 Dec 2023
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