Conservation and Diversification of Circadian Rhythmicity Between a Model Crassulacean Acid Metabolism Plant Kalanchoë fedtschenkoi and a Model C3 Photosynthesis Plant Arabidopsis thaliana.

Robert C Moseley,Steve Haase,Xiaohan Yang,Francis Motta,Gerald A Tuskan,Ritesh Mewalal

doi:10.3389/fpls.2018.01757

Abstract

Crassulacean acid metabolism (CAM) improves photosynthetic efficiency under limited water availability relative to C3 photosynthesis. It is widely accepted that CAM plants have evolved from C3 plants and it is hypothesized that CAM is under the control of the internal circadian clock. However, the role that the circadian clock plays in the evolution of CAM is not well understood. To identify the molecular basis of circadian control over CAM evolution, rhythmic gene sets were identified in a CAM model plant species (Kalanchoë fedtschenkoi) and a C3 model plant species (Arabidopsis thaliana) through analysis of diel time-course gene expression data using multiple periodicity detection algorithms. Based on protein sequences, ortholog groups were constructed containing genes from each of these two species. The ortholog groups were categorized into five gene sets based on conservation and diversification of rhythmic gene expression. Interestingly, minimal functional overlap was observed when comparing the rhythmic gene sets of each species. Specifcally, metabolic processes were enriched in the gene set under circadian control in K. fedtschenkoi and numerous genes were found to have retained or gained rhythmic expression in K. fedtsechenkoi. Additonally, several rhythmic orthologs, including CAM-related orthologs, displayed phase shifts between species. Results of this analysis point to several mechanisms by which the circadian clock plays a role in the evolution of CAM. These genes provide a set of testable hypotheses for future experiments.

Highlights

All organisms confront environmental fluctuations on a daily basis, including changes in light, temperature, predation risk and water availability
Through comparative analysis of time-course data using rhythmic detection algorithms (Deckard et al, 2013) we identified commonalities and differences in rhythmic genes between A. thaliana and K. fedtschenkoi
Our results provide further lines of evidence supporting the hypothesis that the circadian clock played a role in the evolution of Crassulacean acid metabolism (CAM)

Summary

Introduction

All organisms confront environmental fluctuations on a daily basis, including changes in light, temperature, predation risk and water availability. Many of these changes exhibit predictable diurnal oscillations, which incentivized organisms to evolve internal timekeeping systems in anticipation of environmental changes. An emergent circadian clock enabled organisms to synchronize their biological activity with external cues (Bell-Pederson et al, 2005). The circadian clock is important for plant survival, due to their sessile habit, and controls time-of-day specific biology. Greenham and McClung (2015) demonstrated that defense pathways become subordinate to the circadian clock, allowing the plant to activate defense pathways to the time of day when the threat posed by herbivores is maximal. Numerous processes have been documented to be under the control of the circadian clock; the extent to which the clock controls basic physiology is still not well understood (Piechulla, 1988; Merida et al, 1999; Thain et al, 2000; Hotta et al, 2007; Mallona et al, 2011; McClung, 2013; Ming et al, 2015)

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