Diverse photoperiodic gene expression patterns are likely mediated by distinct transcriptional systems in Arabidopsis

Abstract

Photoperiod is an annual cue measured by biological systems to align growth and reproduction with the seasons. In plants, photoperiodic flowering has been intensively studied for over 100 years, but we lack a complete picture of the transcriptional networks and cellular processes that are photoperiodic. We performed a transcriptomics experiment on Arabidopsis plants grown in 3 different photoperiods, and find that nearly one-third of the known genes show photoperiodic alteration in gene expression. Gene clustering, daily expression integral calculations and cis-element analysis then separate photoperiodic genes into co-expression subgroups that display 19 diverse seasonal expression patterns, opening the possibility that many photoperiod measurement systems work in parallel in Arabidopsis. Then, functional enrichment analysis predicts co-expression of important cellular pathways. To test these predictions, we generated a comprehensive catalog of genes in the phenylpropanoid biosynthesis pathway, overlaid gene expression data and demonstrated that photoperiod intersects with the two major phenylpropanoid pathways differentially, controlling flavonoids but not lignin. Finally, we describe the development of a new app that visualizes photoperiod transcriptomic data for the wider community.

Parallel mechanisms detect different photoperiods to independently control seasonal flowering and growth in plants

“…In 16L:8D, MIPS1 expression is biphasic, containing the ZT4 peak seen in 8L:16D and a second photoperiod-specific peak phased to dusk at ZT16. This results in a rDEI 16L:8D/8L:16D (relative Daily Expression Integral 8,9 ) of 1.44 in the microarray experiment, 2.77 in the RNA-seq experiment, and 1.70 in the qRT-PCR. These results indicate that plants grown in 16L:8D have higher MIPS1 expression due to a photoperiod-specific peak in expression at ZT16.…”

“…Recently, the metabolic daylength measurement (MDLM) system was shown to induce expression of genes in short-day photoperiods, but it remains to be seen if MDLM can also cause induction of gene expression in long-day photoperiods 8,9 . This system relies on light sensing by photosynthesis and the circadian clock-controlled balance between starch and sucrose to control gene expression in a photoperiodic manner.…”

New Horizons in Plant Photoperiodism

“…At least one-third of the Arabidopsis transcriptome is under the control of the circadian clock or displays diurnal rhythms, and recently researchers estimated that one-third of the transcriptome also changes in response to photoperiod ( 26 , 47 , 74 , 90 , 92 ). The first glimpses of the full scope of photoperiod-regulated genes and cellular processes came from a microarray time-course analysis of SD- and LD-grown Arabidopsis ( 90 , 92 ).…”

“…The aforementioned Arabidopsis photoperiod time-course RNA-seq data set was also used to suggest that a variety of photoperiod transcriptional networks are likely operating in Arabidopsis ( 74 ). The data set was generated with Arabidopsis grown in three photoperiods (16L:8D, 12L:12D, and 8L:16D) with 4-h resolution across 24 h of each photoperiod.…”

“…These included known clusters such as clock-regulated genes that phase shift but also unknown clusters such as a group of genes encoding ribosomal proteins that respond to photoperiod with a specific expression trough. This work suggests that many photoperiod measurement systems are likely working in parallel to control the expression of genes involved in specific biological and cellular processes ( 74 ).…”