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Diel rewiring and positive selection of ancient plant proteins enabled evolution of CAM photosynthesis in Agave

Lookup NU author(s): Professor Anne Borland



This work is licensed under a Creative Commons Attribution 4.0 International License (CC BY 4.0).


© 2018 The Author(s). 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 appeared 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.

Publication metadata

Author(s): Yin H, Guo H-B, Weston DJ, Borland AM, Ranjan P, Abraham PE, Jawdy SS, Wachira J, Tuskan GA, Tschaplinski TJ, Wullschleger SD, Guo H, Hettich RL, Gross SM, Wang Z, Visel A, Yang X

Publication type: Article

Publication status: Published

Journal: BMC Genomics

Year: 2018

Volume: 19

Online publication date: 06/08/2018

Acceptance date: 26/07/2018

Date deposited: 31/10/2018

ISSN (electronic): 1471-2164

Publisher: BioMed Central Ltd


DOI: 10.1186/s12864-018-4964-7


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