Diel rewiring and positive selection of ancient plant proteins enabled evolution of CAM photosynthesis in Agave
Abstract 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...
| Main Authors: | , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2018-08-01
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| Series: | BMC Genomics |
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| Online Access: | http://link.springer.com/article/10.1186/s12864-018-4964-7 |
| _version_ | 1818853193804677120 |
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| author | Hengfu Yin Hao-Bo Guo David J. Weston Anne M. Borland Priya Ranjan Paul E. Abraham Sara S. Jawdy James Wachira Gerald A. Tuskan Timothy J. Tschaplinski Stan D. Wullschleger Hong Guo Robert L. Hettich Stephen M. Gross Zhong Wang Axel Visel Xiaohan Yang |
| author_facet | Hengfu Yin Hao-Bo Guo David J. Weston Anne M. Borland Priya Ranjan Paul E. Abraham Sara S. Jawdy James Wachira Gerald A. Tuskan Timothy J. Tschaplinski Stan D. Wullschleger Hong Guo Robert L. Hettich Stephen M. Gross Zhong Wang Axel Visel Xiaohan Yang |
| author_sort | Hengfu Yin |
| collection | DOAJ |
| description | Abstract 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. |
| first_indexed | 2024-12-19T07:32:56Z |
| format | Article |
| id | doaj.art-57b43c1305bb455cb7d6e82b3a122c99 |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-12-19T07:32:56Z |
| publishDate | 2018-08-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Genomics |
| spelling | doaj.art-57b43c1305bb455cb7d6e82b3a122c992022-12-21T20:30:39ZengBMCBMC Genomics1471-21642018-08-0119111610.1186/s12864-018-4964-7Diel rewiring and positive selection of ancient plant proteins enabled evolution of CAM photosynthesis in AgaveHengfu Yin0Hao-Bo Guo1David J. Weston2Anne M. Borland3Priya Ranjan4Paul E. Abraham5Sara S. Jawdy6James Wachira7Gerald A. Tuskan8Timothy J. Tschaplinski9Stan D. Wullschleger10Hong Guo11Robert L. Hettich12Stephen M. Gross13Zhong Wang14Axel Visel15Xiaohan Yang16Biosciences Division, Oak Ridge National LaboratoryDepartment of Biology, University of TennesseeBiosciences Division, Oak Ridge National LaboratoryBiosciences Division, Oak Ridge National LaboratoryBiosciences Division, Oak Ridge National LaboratoryDOE-Center for Bioenergy Innovation (CBI), Oak Ridge National LaboratoryBiosciences Division, Oak Ridge National LaboratoryDepartment of Biology, Morgan State UniversityBiosciences Division, Oak Ridge National LaboratoryBiosciences Division, Oak Ridge National LaboratoryEnvironmental Sciences Division, Oak Ridge National LaboratoryDepartment of Biology, University of TennesseeDOE-Center for Bioenergy Innovation (CBI), Oak Ridge National LaboratoryDOE Joint Genome InstituteDOE Joint Genome InstituteDOE Joint Genome InstituteBiosciences Division, Oak Ridge National LaboratoryAbstract 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.http://link.springer.com/article/10.1186/s12864-018-4964-7Crassulacean acid metabolismPhotosynthesisComparative genomicsTranscriptomePositive selectionCircadian rhythm |
| spellingShingle | Hengfu Yin Hao-Bo Guo David J. Weston Anne M. Borland Priya Ranjan Paul E. Abraham Sara S. Jawdy James Wachira Gerald A. Tuskan Timothy J. Tschaplinski Stan D. Wullschleger Hong Guo Robert L. Hettich Stephen M. Gross Zhong Wang Axel Visel Xiaohan Yang Diel rewiring and positive selection of ancient plant proteins enabled evolution of CAM photosynthesis in Agave BMC Genomics Crassulacean acid metabolism Photosynthesis Comparative genomics Transcriptome Positive selection Circadian rhythm |
| title | Diel rewiring and positive selection of ancient plant proteins enabled evolution of CAM photosynthesis in Agave |
| title_full | Diel rewiring and positive selection of ancient plant proteins enabled evolution of CAM photosynthesis in Agave |
| title_fullStr | Diel rewiring and positive selection of ancient plant proteins enabled evolution of CAM photosynthesis in Agave |
| title_full_unstemmed | Diel rewiring and positive selection of ancient plant proteins enabled evolution of CAM photosynthesis in Agave |
| title_short | Diel rewiring and positive selection of ancient plant proteins enabled evolution of CAM photosynthesis in Agave |
| title_sort | diel rewiring and positive selection of ancient plant proteins enabled evolution of cam photosynthesis in agave |
| topic | Crassulacean acid metabolism Photosynthesis Comparative genomics Transcriptome Positive selection Circadian rhythm |
| url | http://link.springer.com/article/10.1186/s12864-018-4964-7 |
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