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Review
. 2023 Oct 9;12(19):3508.
doi: 10.3390/plants12193508.

Regulation of Flowering Time and Other Developmental Plasticities by 3' Splicing Factor-Mediated Alternative Splicing in Arabidopsis thaliana

Keh Chien Lee  1 , Young-Cheon Kim  2 , Jeong-Kook Kim  3 , Horim Lee  4 , Jeong Hwan Lee  2
Affiliations
Review

Regulation of Flowering Time and Other Developmental Plasticities by 3' Splicing Factor-Mediated Alternative Splicing in Arabidopsis thaliana

Keh Chien Lee et al. Plants (Basel). .

Abstract

Plants, as sessile organisms, show a high degree of plasticity in their growth and development and have various strategies to cope with these alterations under continuously changing environments and unfavorable stress conditions. In particular, the floral transition from the vegetative and reproductive phases in the shoot apical meristem (SAM) is one of the most important developmental changes in plants. In addition, meristem regions, such as the SAM and root apical meristem (RAM), which continually generate new lateral organs throughout the plant life cycle, are important sites for developmental plasticity. Recent findings have shown that the prevailing type of alternative splicing (AS) in plants is intron retention (IR) unlike in animals; thus, AS is an important regulatory mechanism conferring plasticity for plant growth and development under various environmental conditions. Although eukaryotes exhibit some similarities in the composition and dynamics of their splicing machinery, plants have differences in the 3' splicing characteristics governing AS. Here, we summarize recent findings on the roles of 3' splicing factors and their interacting partners in regulating the flowering time and other developmental plasticities in Arabidopsis thaliana.

Keywords: 3’ splicing factors; alternative splicing; developmental plasticity; flowering time; root apical meristem; shoot apical meristem.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 2
Figure 2
A regulatory mechanism of temperature-dependent flowering by AtSF1-mediated alternative splicing of FLM pre-mRNAs. At low ambient temperatures (blue thermometer), Arabidopsis splicing factor1 (AtSF1) strongly binds to the branch point site (BPS) of FLOWERING LOCUS M (FLM) pre-mRNA intron 1 to produce major functional FLM-β transcripts, thereby leading to the formation of the SHORT VEGETATIVE PHASE (SVP)–FLM-β repressor complex, which in turn represses flowering by binding its complex to the genomic regions of the floral activators such as FLOWERING LOCUS T (FT) and LEAFY (LFY) in the leaves and shoot apices, respectively [41,42,47]. At warm ambient temperatures (red thermometer), the binding of AtSF1 to the BPS in intron 1 of FLM pre-mRNA is significantly reduced. The lower level of FLM-β transcripts and the degradation of SVP results in decreased levels of the SVP–FLM-β complex and thus release the repression of FT and LFY expression in the leaves and shoot apices, respectively, thereby inducing flowering. Thick and thin lines of AtSF1 denote strong and weak binding to the BPS in intron 1 of FLM pre-mRNA, respectively. Solid and T-shaped arrows indicate activation and repression of _target genes’ expression, respectively.
Figure 1
Figure 1
Regulatory mechanisms of flowering time by AtU2AF35 and AtU2AF65. (a) A possible mechanism of flowering by Arabidopsis U2 auxiliary factor 35 (AtU2AF35)-mediated alternative splicing of FLOWERING CONTROL LOCUS A (FCA) pre-mRNA. Normal levels of AtU2AF35 produce major functional FCA-γ transcripts from FCA pre-mRNA, thereby leading to the binding of FCA-γ to FLOWERING LOCUS C (FLC) locus, which in turn represses flowering under unfavorable conditions. (b) A possible mechanism of flowering by Arabidopsis U2 auxiliary factor 65a (AtU2AF65a)-mediated production of COOLAIR transcripts. COOLAIR long non-coding antisense RNAs expressed from the FLC locus are important in regulating FLC chromatin silencing and transcriptional repression in nonvernalized plants [25,34,35,36]. COOLAIR RNAs are classified into Class I (proximal isoforms) and Class II (distal isoforms) according to the positions where polyadenylation occurs by 3’ end-processing factors [37,38,39]. AtU2AF65a binds to the FLC locus to affect the expression of COOLAIR Class I and Class II RNAs, leading to the binding of COOLAIR Class I RNAs to the FLC locus, which affects the histone methylation of H3K4me2, H3K36me3, and H3K27me3. In addition, two classes of COOLAIR transcripts bind to FCA and recruit PRC2 complex to the FLC locus, thereby repressing FLC expression. (c) A possible mechanism of flowering by AtU2AF65b-mediated alternative splicing of _targets’ pre-mRNAs. Increased expression levels of AtU2AF65b induced by abscisic acid (ABA) binds to the pre-mRNA of ABSCISIC ACID-INSENSITIVE 5 (ABI5), thereby leading to binding of ABI5 to FLC genomic regions, which in turn represses flowering by increased FLC expression [25]. In addition, AtU2AF65b binds to FLC pre-mRNA to affect FLC splicing. However, AtU2AF65b may regulate flowering time in an ABA-independent manner [24]. Solid and T-shaped arrows indicate activation and repression of _target genes’ expression, respectively.
Figure 3
Figure 3
Model of SR proteins in the regulating flowering time and other developmental plasticity. SR proteins as components of spliceosome mediate the pre-mRNA splicing of flowering time, plant morphology, circadian clock, and abiotic stress responses-related genes at the post-transcriptional level.
Figure 4
Figure 4
A scheme of developmental plasticity in apical meristems by alternative splicing. The 3’ splicing factors in primary apical meristems [shoot apical meristem (SAM) and root apical meristem (RAM)] are associated with various environmental and abiotic stress signals. ROOT HAIR SIX-LIKE2 (RSL2) and ROOT HAIR DEFECTIVE2 (RHD2) are directly alternatively spliced by RNA-directed DNA METHYLATION (RDM16)/Pre-mRNA-splicing factor 3 (Prp3) and LIGHT-SENSITIVE ROOT-HAIR DEVELOPMENT 1 (LRH1)/p14 (solid arrows), respectively, for root growth and development. In contrast, SAM maintenance via CLAVATA3 (CLV3)-WUSCHEL (WUS) negative feedback and SHOOT MERISTEMLESS (STM) is indirectly (dashed arrows) regulated by 3’ splicing factors such as PORCUPINE (PCP)/SmE1 and SNW/SKI INTERACTING PROTEIN (SKIP).
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