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Title: Temporal and spatial transcriptomic and microRNA dynamics of CAM photosynthesis in pineapple

Authors:
 [1]; ORCiD logo [2];  [3];  [3];  [3];  [4];  [5];  [6]; ORCiD logo [6];  [6];  [7]; ORCiD logo [5];  [1]
  1. FAFU and UIUC Joint Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Key Laboratory of Genetics, Breeding and Multiple Utilization of Corps, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou 350002 Fujian China, Department of Plant Biology, University of Illinois at Urbana-Champaign, Urbana IL 61801 USA
  2. FAFU and UIUC Joint Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Key Laboratory of Genetics, Breeding and Multiple Utilization of Corps, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou 350002 Fujian China, Department of Plant Biology, University of Illinois at Urbana-Champaign, Urbana IL 61801 USA, Donald Danforth Plant Science Center, St. Louis MO USA, Department of Horticulture, Michigan State University, East Lansing MI 48823 USA
  3. FAFU and UIUC Joint Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Key Laboratory of Genetics, Breeding and Multiple Utilization of Corps, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou 350002 Fujian China
  4. Department of Horticulture, Michigan State University, East Lansing MI 48823 USA
  5. Department of Biochemistry and Molecular Biology, MS330, University of Nevada, Reno NV 89557-0330 USA
  6. Donald Danforth Plant Science Center, St. Louis MO USA
  7. Department of Plant Sciences, University of Oxford, South Parks Road Oxford OX1 3RB UK
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1375654
Grant/Contract Number:
SC0008834
Resource Type:
Journal Article: Publisher's Accepted Manuscript
Journal Name:
The Plant Journal
Additional Journal Information:
Related Information: CHORUS Timestamp: 2017-10-20 16:25:20; Journal ID: ISSN 0960-7412
Publisher:
Society for Experimental Biology
Country of Publication:
United Kingdom
Language:
English

Citation Formats

Wai, Ching M., VanBuren, Robert, Zhang, Jisen, Huang, Lixian, Miao, Wenjing, Edger, Patrick P., Yim, Won C., Priest, Henry D., Meyers, Blake C., Mockler, Todd, Smith, J. Andrew C., Cushman, John C., and Ming, Ray. Temporal and spatial transcriptomic and microRNA dynamics of CAM photosynthesis in pineapple. United Kingdom: N. p., 2017. Web. doi:10.1111/tpj.13630.
Wai, Ching M., VanBuren, Robert, Zhang, Jisen, Huang, Lixian, Miao, Wenjing, Edger, Patrick P., Yim, Won C., Priest, Henry D., Meyers, Blake C., Mockler, Todd, Smith, J. Andrew C., Cushman, John C., & Ming, Ray. Temporal and spatial transcriptomic and microRNA dynamics of CAM photosynthesis in pineapple. United Kingdom. doi:10.1111/tpj.13630.
Wai, Ching M., VanBuren, Robert, Zhang, Jisen, Huang, Lixian, Miao, Wenjing, Edger, Patrick P., Yim, Won C., Priest, Henry D., Meyers, Blake C., Mockler, Todd, Smith, J. Andrew C., Cushman, John C., and Ming, Ray. Mon . "Temporal and spatial transcriptomic and microRNA dynamics of CAM photosynthesis in pineapple". United Kingdom. doi:10.1111/tpj.13630.
@article{osti_1375654,
title = {Temporal and spatial transcriptomic and microRNA dynamics of CAM photosynthesis in pineapple},
author = {Wai, Ching M. and VanBuren, Robert and Zhang, Jisen and Huang, Lixian and Miao, Wenjing and Edger, Patrick P. and Yim, Won C. and Priest, Henry D. and Meyers, Blake C. and Mockler, Todd and Smith, J. Andrew C. and Cushman, John C. and Ming, Ray},
abstractNote = {},
doi = {10.1111/tpj.13630},
journal = {The Plant Journal},
number = ,
volume = ,
place = {United Kingdom},
year = {Mon Jul 03 00:00:00 EDT 2017},
month = {Mon Jul 03 00:00:00 EDT 2017}
}

Journal Article:
Free Publicly Available Full Text
This content will become publicly available on August 21, 2018
Publisher's Accepted Manuscript

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  • 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 ρ duplication event. The pineapple lineage has transitioned from C 3 photosynthesis to CAM, with CAM-related genes exhibiting a diel expression pattern in photosynthetic tissues.more » 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. Lastly, we found pineapple CAM photosynthesis evolved by the reconfiguration of pathways in C 3 plants, through the regulatory neofunctionalization of preexisting genes and not through the acquisition of neofunctionalized genes via whole-genome or tandem gene duplication.« less
  • 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 ρ duplication event. The pineapple lineage has transitioned from C 3 photosynthesis to CAM, with CAM-related genes exhibiting a diel expression pattern in photosyntheticmore » 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 C 3 plants, through the regulatory neofunctionalization of preexisting genes and not through the acquisition of neofunctionalized genes via whole-genome or tandem gene duplication.« less
  • Already a proven mechanism for drought resilience, crassulacean acid metabolism (CAM) is a specialized type of photosynthesis that maximizes water-use efficiency (WUE) via an inverse (compared to C 3 and C 4 photosynthesis-performing species) day/night pattern of stomatal closure/opening to shift CO 2 uptake to the night, when evapotranspiration rates are low. A systems-level understanding of temporal molecular and metabolic controls is needed to define the cellular behavior that underpins CAM. Here, we report high-resolution temporal behaviors of transcript, protein and metabolite abundances across a CAM diel cycle and, where applicable, compare those observations to the well-established C 3 modelmore » plant, Arabidopsis thaliana. A mechanistic finding that emerged is that CAM operates with a diel redox poise that is shifted relative to that in Arabidopsis thaliana. Moreover, we identified widespread rescheduled expression of genes associated with signal transduction mechanisms that regulate stomatal opening/closing. Controlled production and degradation of transcripts and proteins represents a timing mechanism by which to regulate cellular function, yet how this molecular timekeeping regulates CAM physiology remains unclear. In this paper, we provide new insights into complex post-transcriptional and -translational hierarchies that govern CAM in Agave. These data sets together provide a resource to inform efforts to engineer more water-use efficient CAM pathway traits into economically valuable C 3 crops.« less
  • Improved worker protection from accidental releases of radioactive aerosols requires optimal placement of Continuous Air Monitoring (CAM) instrumentation. CAMs should be positioned around the workspace such that, no matter where a release occurs, the cloud of aerosol will be quickly and efficiently sampled by a CAM. Then the most rapid alarm can be generated to alert all occupants to vacate. Although smoke studies and S176 gas releases have been used for placement studies, the process is costly and may not provide adequate representation of transport and sampling process when very dilute puff releases of particulate are involved. Techniques of three-dimensionalmore » computational fluid dynamics (CFD) modeling in conjunction with spatial mapping and decision-making tools are being used to characterize room flow fields and both spatial and temporal patterns of redistribution of contaminants. With input of CFD-predicted CAM responses throughout the room and other data such as space utilization and history of accidental releases, spatial map analysis reveals locations where CAM placement will be most effective. These concepts are being developed using near real-time aerosol concentration data from tracer particle puff releases in a plutonium facility workroom and through more detailed studies in a controlled aerosol test room environment. The initial findings from these studies indicate that a selected pattern of CAM placement in the interior of a workroom (based on the particular flow field for that room and other data) will provide optimum CAM response to a release from anywhere in the room.« less
  • C 4 photosynthesis is used by only three percent of all flowering plants, but explains a quarter of global primary production, including some of the worlds’ most important cereals and bioenergy grasses. Recent advances in our understanding of C 4 development can be attributed to the application of comparative transcriptomics approaches that has been fueled by high throughput sequencing. Global surveys of gene expression conducted between different developmental stages or on phylogenetically closely related C 3 and C 4 species are providing new insights into C 4 function, development and evolution. Importantly, through co-expression analysis and comparative genomics, these studiesmore » help define novel candidate genes that transcend traditional genetic screens. In this review, we briefly summarize the major findings from recent transcriptomic studies, compare and contrast these studies to summarize emerging consensus, and suggest new approaches to exploit the data. Lastly, we suggest using Setaria viridis as a model system to relieve a major bottleneck in genetic studies of C 4 photosynthesis, and discuss the challenges and new opportunities for future comparative transcriptomic studies.« less
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