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

Here, Crassulacean acid metabolism (CAM) enhances plant water-use efficiency through an inverse day/night pattern of stomatal closure/opening that facilitates nocturnal CO 2 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. 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 C 3, C 4 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 C 3, C 4 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 ofmore » CAM in Agave. Furthermore, we highlighted the potential candidates contributing to the adaptation of CAM functional modules. In conclusion, 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 C 3 ancestors in Agave.« less
Authors:
 [1] ;  [2] ; ORCiD logo [3] ;  [4] ;  [3] ; ORCiD logo [3] ;  [3] ;  [5] ; ORCiD logo [3] ; ORCiD logo [3] ; ORCiD logo [3] ;  [2] ; ORCiD logo [3] ;  [6] ;  [7] ;  [7] ; ORCiD logo [3]
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Chinese Academy of Forestry, Hangzhou (China)
  2. Univ. of Tennessee, Knoxville, TN (United States)
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  4. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Newcastle Univ., Newcastle upon Tyne (United Kingdom)
  5. Morgan State Univ., Baltimore, MD (United States)
  6. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Illumina, Inc., San Diego, CA (United States)
  7. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Merced, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Publication Date:
Grant/Contract Number:
AC05-00OR22725
Type:
Accepted Manuscript
Journal Name:
BMC Genomics
Additional Journal Information:
Journal Volume: 19; Journal Issue: 1; Journal ID: ISSN 1471-2164
Publisher:
Springer
Research Org:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org:
USDOE
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Crassulacean acid metabolism; Photosynthesis; Comparative genomics; Transcriptome; Positive selection; Circadian rhythm
OSTI Identifier:
1464029