Evolution of Daily Gene Co-expression Patterns from Algae to Plants

Abstract

Daily rhythms play a key role in transcriptome regulation in plants and microalgae orchestrating responses that, among other processes, anticipate light transitions that are essential for their metabolism and development. The recent accumulation of genome-wide transcriptomic data generated under alternating light:dark periods from plants and microalgae has made possible integrative and comparative analysis that could contribute to shed light on the evolution of daily rhythms in the green lineage. In this work, RNA-seq and microarray data generated over 24 h periods in different light regimes from the eudicot Arabidopsis thaliana and the microalgae Chlamydomonas reinhardtii and Ostreococcus tauri have been integrated and analyzed using gene co-expression networks. This analysis revealed a reduction in the size of the daily rhythmic transcriptome from around 90% in Ostreococcus, being heavily influenced by light transitions, to around 40% in Arabidopsis, where a certain independence from light transitions can be observed. A novel Multiple Bidirectional Best Hit (MBBH) algorithm was applied to associate single genes with a family of potential orthologues from evolutionary distant species. Gene duplication, amplification and divergence of rhythmic expression profiles seems to have played a central role in the evolution of gene families in the green lineage such as Pseudo Response Regulators (PRRs), CONSTANS-Likes (COLs), and DNA-binding with One Finger (DOFs). Gene clustering and functional enrichment have been used to identify groups of genes with similar rhythmic gene expression patterns. The comparison of gene clusters between species based on potential orthologous relationships has unveiled a low to moderate level of conservation of daily rhythmic expression patterns. However, a strikingly high conservation was found for the gene clusters exhibiting their highest and/or lowest expression value during the light transitions.

Genome and time-of-day transcriptome ofWolffia australianalink morphological extreme minimization with un-gated plant growth

“…Therefore, we compared the Wolffia cycling genes against two high quality datasets generated from Arabidopsis (Ath) and rice (Osa) under the same conditions of light-dark cycles and constant temperature (LDHH) used here (Michael et al 2008b;Filichkin et al 2011). In general, cycling genes had similar phases of expression between species as seen in other across-species comparisons (Filichkin et al 2011;Reyes et al 2017), although there were some differences in the phase of Wolffia cycling genes ( Figure S12). As expected, certain GO terms are overrepresented at specific TOD patterns consistent with Wolffia partitioning its biology over the day much like Ath and Osa ( Figure 7A; Figure S13).…”

Kingdom-wide comparison reveals conserved diurnal gene expression in Archaeplastida

“…Different photoperiods where used because for species such as P. abies (herein referred to as spruce), a shorter photoperiod would cause dormancy and growth cessation (HEIDE, 1974; Singh et al , 2017). The difference in photoperiod was shown to have a relatively small impact on the organization of daily rhythms (de los Reyes et al , 2017). Starting from ZT1 (Zeitgeber time), defined as one hour after the onset of illumination, we extracted RNA from the six organisms every two hours, resulting in twelve time points per species.…”

“…Many studies have addressed how organisms perform under different diurnal conditions and how they coordinate the activity of their biological pathways. Diurnal regulation actively controls physiological processes, such as cell division, metabolic activity, and growth in all domains of life (Covington et al , 2008; Stockel et al , 2008; Bell-Pedersen et al , 2005; Zones et al , 2015; de los Reyes et al , 2017). Gene expression plays a fundamental role in controlling the activity of biological pathways and is under strict diurnal regulation.…”

“…Gene expression plays a fundamental role in controlling the activity of biological pathways and is under strict diurnal regulation. For example, in Ostreococcus tauri most of the genes are under control of light/dark cycles and specifically, genes involved in cell division, the Krebs cycle and protein synthesis, have the highest amplitude within the diurnal cycle (Monnier et al , 2010; de los Reyes et al , 2017). Studies in Drosophila melanogaster show that in addition to gene expression, splicing, RNA editing and non-coding RNA expression are highly affected by diurnal regulation (Hughes et al , 2012), whereas studies in mammals highlight the importance of diurnal regulation when applied to pharmaceutical applications (Zhang et al , 2014; Archer et al , 2014; Mure et al , 2018).…”

“…Studies in Drosophila melanogaster show that in addition to gene expression, splicing, RNA editing and non-coding RNA expression are highly affected by diurnal regulation (Hughes et al , 2012), whereas studies in mammals highlight the importance of diurnal regulation when applied to pharmaceutical applications (Zhang et al , 2014; Archer et al , 2014; Mure et al , 2018). Furthermore, recent studies on plants have shown a moderate level of conservation of diurnal responses among distantly related species, along with occasional divergent evolution of specific mechanisms (de los Reyes et al , 2017; Serrano-Bueno et al , 2017).…”