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Background: Crassulacean acid metabolism (CAM) enhances plant water-use
efficiency through an inverse day/night pattern of stomatal
closure/opening that facilitates nocturnal CO2 uptake. CAM has evolved
independently in over 35 plant lineages, accounting for ~ 6% of all higher
plants. Agave species are highly heat- and drought-tolerant, and have been
domesticated as model CAM crops for beverage, fiber, and biofuel
production in semi-arid and arid regions. However, the genomic basis of
evolutionary innovation of CAM in genus Agave is largely unknown. Results:
Using an approach that integrated genomics, gene co-expression networks,
comparative genomics and protein structure analyses, we investigated the
molecular evolution of CAM as exemplified in Agave. Comparative genomics
analyses among C3, C4 and CAM species revealed that core metabolic
components required for CAM have ancient genomic origins traceable to
non-vascular plants while regulatory proteins required for diel
re-programming of metabolism have a more recent origin shared among C3, C4
and CAM species. We showed that accelerated evolution of key functional
domains in proteins responsible for primary metabolism and signaling,
together with a diel re-programming of the transcription of genes involved
in carbon fixation, carbohydrate processing, redox homeostasis, and
circadian control is required for the evolution of CAM in Agave.
Furthermore, we highlighted the potential candidates contributing to the
adaptation of CAM functional modules. Conclusions: This work provides
evidence of adaptive evolution of CAM related pathways. We showed that the
core metabolic components required for CAM are shared by non-vascular
plants, but regulatory proteins involved in re-reprogramming of carbon
fixation and metabolite transportation appear more recently. We propose
that the accelerated evolution of key proteins together with a diel
re-programming of gene expression were required for CAM evolution from C3
ancestors in Agave.
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