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The pineapple genome and the evolution of CAM photosynthesis.

ABSTRACT: Pineapple (Ananas comosus (L.) Merr.) is the most economically valuable crop possessing crassulacean acid metabolism (CAM), a photosynthetic carbon assimilation pathway with high water-use efficiency, and the second most important tropical fruit. We sequenced the genomes of pineapple varieties F153 and MD2 and a wild pineapple relative, Ananas bracteatus accession CB5. The pineapple genome has one fewer ancient whole-genome duplication event than sequenced grass genomes and a conserved karyotype with seven chromosomes from before the ? duplication event. The pineapple lineage has transitioned from C3 photosynthesis to CAM, with CAM-related genes exhibiting a diel expression pattern in photosynthetic tissues. CAM pathway genes were enriched with cis-regulatory elements associated with the regulation of circadian clock genes, providing the first cis-regulatory link between CAM and circadian clock regulation. Pineapple CAM photosynthesis evolved by the reconfiguration of pathways in C3 plants, through the regulatory neofunctionalization of preexisting genes and not through the acquisition of neofunctionalized genes via whole-genome or tandem gene duplication.

SUBMITTER: Ming R

PROVIDER: S-EPMC4867222 | biostudies-literature | 2015 Dec

REPOSITORIES: biostudies-literature

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The pineapple genome and the evolution of CAM photosynthesis.

Ming Ray R VanBuren Robert R Wai Ching Man CM Tang Haibao H Schatz Michael C MC Bowers John E JE Lyons Eric E Wang Ming-Li ML Chen Jung J Biggers Eric E Zhang Jisen J Huang Lixian L Zhang Lingmao L Miao Wenjing W Zhang Jian J Ye Zhangyao Z Miao Chenyong C Lin Zhicong Z Wang Hao H Zhou Hongye H Yim Won C WC Priest Henry D HD Zheng Chunfang C Woodhouse Margaret M Edger Patrick P PP Guyot Romain R Guo Hao-Bo HB Guo Hong H Zheng Guangyong G Singh Ratnesh R Sharma Anupma A Min Xiangjia X Zheng Yun Y Lee Hayan H Gurtowski James J Sedlazeck Fritz J FJ Harkess Alex A McKain Michael R MR Liao Zhenyang Z Fang Jingping J Liu Juan J Zhang Xiaodan X Zhang Qing Q Hu Weichang W Qin Yuan Y Wang Kai K Chen Li-Yu LY Shirley Neil N Lin Yann-Rong YR Liu Li-Yu LY Hernandez Alvaro G AG Wright Chris L CL Bulone Vincent V Tuskan Gerald A GA Heath Katy K Zee Francis F Moore Paul H PH Sunkar Ramanjulu R Leebens-Mack James H JH Mockler Todd T Bennetzen Jeffrey L JL Freeling Michael M Sankoff David D Paterson Andrew H AH Zhu Xinguang X Yang Xiaohan X Smith J Andrew C JA Cushman John C JC Paull Robert E RE Yu Qingyi Q

Nature genetics 20151102 12

Pineapple (Ananas comosus (L.) Merr.) is the most economically valuable crop possessing crassulacean acid metabolism (CAM), a photosynthetic carbon assimilation pathway with high water-use efficiency, and the second most important tropical fruit. We sequenced the genomes of pineapple varieties F153 and MD2 and a wild pineapple relative, Ananas bracteatus accession CB5. The pineapple genome has one fewer ancient whole-genome duplication event than sequenced grass genomes and a conserved karyotype ...[more]

PMID: 26523774

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Project description:BackgroundCrassulacean 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.ResultsUsing 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.ConclusionsThis 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.

Dataset Information

The pineapple genome and the evolution of CAM photosynthesis.

Publications

The pineapple genome and the evolution of CAM photosynthesis.

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