Genome-wide analysis of light-regulated alternative splicing mediated by photoreceptors in Physcomitrella patens

Abstract

BackgroundLight is one of the most important factors regulating plant growth and development. Light-sensing photoreceptors tightly regulate gene expression to control photomorphogenic responses. Although many levels of gene expression are modulated by photoreceptors, regulation at the mRNA splicing step remains unclear.ResultsWe performed high-throughput mRNA sequencing to analyze light-responsive changes in alternative splicing in the moss Physcomitrella patens, and found that a large number of alternative splicing events were induced by light in the moss protonema. Light-responsive intron retention preferentially occurred in transcripts involved in photosynthesis and translation. Many of the alternatively spliced transcripts were expressed from genes with a function relating to splicing or light signaling, suggesting a potential impact on pre-mRNA splicing and photomorphogenic gene regulation in response to light. Moreover, most light-regulated intron retention was induced immediately upon light exposure, while motif analysis identified a repetitive GAA motif that may function as an exonic regulatory cis element in light-mediated alternative splicing. Further analysis in gene-disrupted mutants was consistent with a function for multiple red-light photoreceptors in the upstream regulation of light-responsive alternative splicing.ConclusionsOur results indicate that intensive alternative splicing occurs in non-vascular plants and that, during photomorphogenesis, light regulates alternative splicing with transcript selectivity. We further suggest that alternative splicing is rapidly fine-tuned by light to modulate gene expression and reorganize metabolic processes, and that pre-mRNA cis elements are involved in photoreceptor-mediated splicing regulation.

Evolutionarily Conserved Alternative Splicing Across Monocots

“…AS isoforms that are translated can influence proteome diversity, while others that are purposefully nonfunctional can act to post-transcriptionally modulate protein levels (Fu et al 2009;Hammond et al 2009). AS participates in many important processes during the lifecycle of plants (Staiger and Brown 2013), and AS occurs in response to many abiotic stresses (Mastrangelo et al 2012), for example red/ blue light (Shikata et al 2014;Wu et al 2014), salt stress , drought (Thatcher et al 2016), flooding (Syed et al 2015), and temperature (James et al 2012;Streitner et al 2013).…”

Changes in cell wall polysaccharide composition, gene transcription and alternative splicing in germinating barley embryos

“…Arabidopsis, oil formation in soybean; and temperature and light responses in Physcomitrella patens (Chang et al , 2014, Eckardt, 2013, Li et al , 2013, Wu, Su, 2014. However, little is known whether AS is involved in cell wall modifications.…”

“…It regulates many biological processes including hormone-mediated signal transduction and stress-or light-induced responses (Eckardt, 2013, Reddy et al , 2013, Staiger and Brown, 2013, Wu et al , 2014. It determines tissue-specific differentiation patterns and controls plant development and adaptation to environmental conditions.…”

Shedding light on the chloroplast as a remote control of nuclear gene expression

“…17 Moreover, photoreceptor proteins are also able to modulate alternative splicing. Recent report on P. patens 8 showed that alternative splicing is rapidly fine-tuned by light to modulate gene expression and reorganize metabolic processes in a way that might be dependent on red-light photoreceptors.…”

“…In Arabidopsis, around 61% of multi-exonic genes encode pre-mRNAs that are alternatively spliced under normal growth conditions, 7 and light seems to drive alternative splicing regulation of several genes in plants as revealed by recent publications. 8,9 For example, Wu and colleagues 8 have shown that photoreceptor pathways regulate alternative splicing genome-wide in the moss Physcomitrella patens. More recently, we have demonstrated that chloroplasts are able to regulate nuclear alternative splicing in response to changes in the redox state of the photosynthetic electron transport components.…”