Abstract

Plants with facultative crassulacean acid metabolism (CAM) maximize performance through utilizing C3 or C4 photosynthesis under ideal conditions while temporally switching to CAM under water stress (drought). While genome-scale analyses of constitutive CAM plants suggest that time of day networks are shifted, or phased to the evening compared to C3, little is known for how the shift from C3 to CAM networks is modulated in drought induced CAM. Here we generate a draft genome for the drought-induced CAM-cycling species Sedum album. Through parallel sampling in well-watered (C3) and drought (CAM) conditions, we uncover a massive rewiring of time of day expression and a CAM and stress-specific network. The core circadian genes are expanded in S. album and under CAM induction, core clock genes either change phase or amplitude. While the core clock cis-elements are conserved in S. album, we uncover a set of novel CAM and stress specific cis-elements consistent with our finding of rewired co-expression networks. We identified shared elements between constitutive CAM and CAM-cycling species and expression patterns unique to CAM-cycling S. album. Together these results demonstrate that drought induced CAM-cycling photosynthesis evolved through the mobilization of a stress-specific, time of day network, and not solely the phasing of existing C3 networks. These results will inform efforts to engineer water use efficiency into crop plants for growth on marginal land.

Highlights

  • Drought is the most pervasive abiotic stress and plants have evolved diverse strategies to mitigate the effects of water deficit [1]

  • Crassulacean acid metabolism (CAM) photosynthesis represents an important adaptation to arid environments as CAM plants take up CO2 at night when evapotranspiration rates are lower

  • Genomes and large-scale datasets are available for several plants with constitutive CAM activity, but they provided little insight on how this trait evolved from C3

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Summary

Introduction

Drought is the most pervasive abiotic stress and plants have evolved diverse strategies to mitigate the effects of water deficit [1]. Crassulacean acid metabolism (CAM) plants have evolved an alternative carbon assimilation pathway to store CO2 nocturnally when evapotranspiration rates are lower [2]. Malic acid is decarboxylated to release the CO2 for fixation by Rubisco. Because of this temporal separation, CAM plants have remarkably high water use efficiency, and use roughly 35% less water than C4 plants and up to 80% less water than comparable C3 species [4, 5]. These traits make CAM an attractive model for engineering improved water use efficiency and drought tolerance into crop plants that may be grown on more marginal land prone to seasonal droughts[6]

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