Abstract

BackgroundThe circadian clock enables living organisms to anticipate recurring daily and seasonal fluctuations in their growth habitats and synchronize their biology to the environmental cycle. The plant circadian clock consists of multiple transcription-translation feedback loops that are entrained by environmental signals, such as light and temperature. In recent years, alternative splicing emerges as an important molecular mechanism that modulates the clock function in plants. Several clock genes are known to undergo alternative splicing in response to changes in environmental conditions, suggesting that the clock function is intimately associated with environmental responses via the alternative splicing of the clock genes. However, the alternative splicing events of the clock genes have not been studied at the molecular level.ResultsWe systematically examined whether major clock genes undergo alternative splicing under various environmental conditions in Arabidopsis. We also investigated the fates of the RNA splice variants of the clock genes. It was found that the clock genes, including EARLY FLOWERING 3 (ELF3) and ZEITLUPE (ZTL) that have not been studied in terms of alternative splicing, undergo extensive alternative splicing through diverse modes of splicing events, such as intron retention, exon skipping, and selection of alternative 5′ splice site. Their alternative splicing patterns were differentially influenced by changes in photoperiod, temperature extremes, and salt stress. Notably, the RNA splice variants of TIMING OF CAB EXPRESSION 1 (TOC1) and ELF3 were degraded through the nonsense-mediated decay (NMD) pathway, whereas those of other clock genes were insensitive to NMD.ConclusionTaken together, our observations demonstrate that the major clock genes examined undergo extensive alternative splicing under various environmental conditions, suggesting that alternative splicing is a molecular scheme that underlies the linkage between the clock and environmental stress adaptation in plants. It is also envisioned that alternative splicing of the clock genes plays more complex roles than previously expected.

Highlights

  • The circadian clock enables living organisms to anticipate recurring daily and seasonal fluctuations in their growth habitats and synchronize their biology to the environmental cycle

  • Major clock genes undergo extensive alternative splicing On the basis of the prevalence of alternative splicing events in the plant circadian clock genes in the literature [20,26,27,34,35], we anticipated that alternative splicing of the core clock genes constitutes a critical component of the clock function

  • The alternative protein isoform (CCA1β), which lacks the protein domain required for DNA binding, acts as a dominant negative regulator of the authentic CLOCK ASSOCIATED 1 (CCA1) transcription factor (CCA1α), providing a selfregulatory circuit that links the clock with temperature stress response

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Summary

Introduction

The circadian clock enables living organisms to anticipate recurring daily and seasonal fluctuations in their growth habitats and synchronize their biology to the environmental cycle. Alternative splicing emerges as an important molecular mechanism that modulates the clock function in plants. The central loop is mediated by the reciprocal repression between the morningphased MYB transcription factors, CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY), and the evening-phased pseudo-response regulator TIMING OF CAB EXPRESSION 1 (TOC1) [6,7]. The PRR members inhibit the transcription of CCA1 and LHY genes by sequentially binding to the gene promoters from early morning (PRR9) through mid-day (PRR7) to evening (PRR5) [10,11]. Recent studies have shown that three eveningphased factors, EARLY FLOWERING 3 (ELF3), ELF4, and LUX ARRHYTHMO (LUX), form the EVENING COMPLEX (EC), which represses PRR9 gene and LUX gene itself [13,14], indicating that the auto-inhibition of EC replaces the component Y in the evening loop [15]

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