Independent and parallel evolution of new genes by gene duplication in two origins of C4 photosynthesis provides new insight into the mechanism of phloem loading in C4 species
Abstract
C4 photosynthesis is considered one of the most remarkable examples of evolutionary convergence in eukaryotes. However, it is unknown whether the evolution of C4 photosynthesis required the evolution of new genes. Genome-wide gene-tree species-tree reconciliation of seven monocot species that span two origins of C4 photosynthesis revealed that there was significant parallelism in the duplication and retention of genes coincident with the evolution of C4 photosynthesis in these lineages. Specifically, 21 orthologous genes were duplicated and retained independently in parallel at both C4 origins. Analysis of this gene cohort revealed that the set of parallel duplicated and retained genes is enriched for genes that are preferentially expressed in bundle sheath cells, the cell type in which photosynthesis was activated during C4 evolution. Moreover, functional analysis of the cohort of parallel duplicated genes identified SWEET-13 as a potential key transporter in the evolution of C4 photosynthesis in grasses, and provides new insight into the mechanism of phloem loading in these C4 species.
- Authors:
-
- Univ. of Oxford, Oxford (United Kingdom)
- Univ. of Cambridge, Cambridge (United Kingdom)
- Publication Date:
- Research Org.:
- Univ. of Oxford, Oxford (United Kingdom)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1344533
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Molecular Biology and Evolution
- Additional Journal Information:
- Journal Volume: 33; Journal Issue: 7; Journal ID: ISSN 0737-4038
- Publisher:
- Oxford University Press
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; C4 photosynthesis; gene duplication; gene families; parallel evolution
Citation Formats
Emms, David M., Covshoff, Sarah, Hibberd, Julian M., and Kelly, Steven. Independent and parallel evolution of new genes by gene duplication in two origins of C4 photosynthesis provides new insight into the mechanism of phloem loading in C4 species. United States: N. p., 2016.
Web. doi:10.1093/molbev/msw057.
Emms, David M., Covshoff, Sarah, Hibberd, Julian M., & Kelly, Steven. Independent and parallel evolution of new genes by gene duplication in two origins of C4 photosynthesis provides new insight into the mechanism of phloem loading in C4 species. United States. https://doi.org/10.1093/molbev/msw057
Emms, David M., Covshoff, Sarah, Hibberd, Julian M., and Kelly, Steven. Thu .
"Independent and parallel evolution of new genes by gene duplication in two origins of C4 photosynthesis provides new insight into the mechanism of phloem loading in C4 species". United States. https://doi.org/10.1093/molbev/msw057. https://www.osti.gov/servlets/purl/1344533.
@article{osti_1344533,
title = {Independent and parallel evolution of new genes by gene duplication in two origins of C4 photosynthesis provides new insight into the mechanism of phloem loading in C4 species},
author = {Emms, David M. and Covshoff, Sarah and Hibberd, Julian M. and Kelly, Steven},
abstractNote = {C4 photosynthesis is considered one of the most remarkable examples of evolutionary convergence in eukaryotes. However, it is unknown whether the evolution of C4 photosynthesis required the evolution of new genes. Genome-wide gene-tree species-tree reconciliation of seven monocot species that span two origins of C4 photosynthesis revealed that there was significant parallelism in the duplication and retention of genes coincident with the evolution of C4 photosynthesis in these lineages. Specifically, 21 orthologous genes were duplicated and retained independently in parallel at both C4 origins. Analysis of this gene cohort revealed that the set of parallel duplicated and retained genes is enriched for genes that are preferentially expressed in bundle sheath cells, the cell type in which photosynthesis was activated during C4 evolution. Moreover, functional analysis of the cohort of parallel duplicated genes identified SWEET-13 as a potential key transporter in the evolution of C4 photosynthesis in grasses, and provides new insight into the mechanism of phloem loading in these C4 species.},
doi = {10.1093/molbev/msw057},
journal = {Molecular Biology and Evolution},
number = 7,
volume = 33,
place = {United States},
year = {Thu Mar 24 00:00:00 EDT 2016},
month = {Thu Mar 24 00:00:00 EDT 2016}
}
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Figures / Tables:
Fig. 1: Schematic overview of the gene duplication identification method used in this analysis. 1) Clustering genes into orthogroups using OrthoFinder. 2) Construction of multiple sequence alignments using MAFFT and inference of gene trees using Phyldog. 3) Reconciliation of gene trees with species tree using Phyldog. 4) Filtering of reconciledmore »
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Function Relaxation Followed by Diversifying Selection after Whole-Genome Duplication in Flowering Plants
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Evolution of the Phospho enol pyruvate Carboxylase Protein Kinase Family in C 3 and C 4 Flaveria spp.
journal, May 2014
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C 4 Photosynthesis in the Rice Paddy: Insights from the Noxious Weed Echinochloa glabrescens
journal, November 2015
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Identification and Characterization of Shared Duplications between Rice and Wheat Provide New Insight into Grass Genome Evolution
journal, January 2008
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Structural and Metabolic Transitions of C 4 Leaf Development and Differentiation Defined by Microscopy and Quantitative Proteomics in Maize
journal, November 2010
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Evolution of C 4 Photosynthesis in the Genus Flaveria : How Many and Which Genes Does It Take to Make C 4 ?
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Systems Analysis of a Maize Leaf Developmental Gradient Redefines the Current C 4 Model and Provides Candidates for Regulation
journal, December 2011
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C 4 Cycles: Past, Present, and Future Research on C 4 Photosynthesis
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New grass phylogeny resolves deep evolutionary relationships and discovers C4 origins
journal, November 2011
- Working Group, Grass Phylogeny
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The fate of duplicated genes in a polyploid plant genome
journal, October 2012
- Roulin, Anne; Auer, Paul L.; Libault, Marc
- The Plant Journal, Vol. 73, Issue 1
Genome-wide transcript analysis of early maize leaf development reveals gene cohorts associated with the differentiation of C 4 Kranz anatomy
journal, June 2013
- Wang, Peng; Kelly, Steven; Fouracre, Jim P.
- The Plant Journal, Vol. 75, Issue 4
Gene targeting by the TAL effector PthXo2 reveals cryptic resistance gene for bacterial blight of rice
journal, May 2015
- Zhou, Junhui; Peng, Zhao; Long, Juying
- The Plant Journal, Vol. 82, Issue 4
BRAD, the genetics and genomics database for Brassica plants
journal, January 2011
- Cheng, Feng; Liu, Shengyi; Wu, Jian
- BMC Plant Biology, Vol. 11, Issue 1
OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy
journal, August 2015
- Emms, David M.; Kelly, Steven
- Genome Biology, Vol. 16, Issue 1
Deep Evolutionary Comparison of Gene Expression Identifies Parallel Recruitment of Trans-Factors in Two Independent Origins of C4 Photosynthesis
journal, June 2014
- Aubry, Sylvain; Kelly, Steven; Kümpers, Britta M. C.
- PLoS Genetics, Vol. 10, Issue 6
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
journal, March 2010
- Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P.
- PLoS ONE, Vol. 5, Issue 3
Polyploidy and angiosperm diversification
journal, January 2009
- Soltis, Douglas E.; Albert, Victor A.; Leebens-Mack, Jim
- American Journal of Botany, Vol. 96, Issue 1
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- Watson-Lazowski, Alexander; Papanicolaou, Alexie; Sharwood, Robert
- Photosynthesis Research, Vol. 138, Issue 2
Molecular adaptations of NADP-malic enzyme for its function in C4 photosynthesis in grasses
journal, June 2019
- Alvarez, Clarisa E.; Bovdilova, Anastasiia; Höppner, Astrid
- Nature Plants, Vol. 5, Issue 7
The genetics of convergent evolution: insights from plant photosynthesis
journal, March 2019
- Heyduk, Karolina; Moreno-Villena, Jose J.; Gilman, Ian S.
- Nature Reviews Genetics, Vol. 20, Issue 8
Herbarium genomics retraces the origins of C 4 -specific carbonic anhydrase in Andropogoneae (Poaceae)
journal, March 2018
- Besnard, Guillaume; Bianconi, Matheus E.; Hackel, Jan
- Botany Letters, Vol. 165, Issue 3-4
Landscape of gene transposition–duplication within the Brassicaceae family
journal, October 2018
- Oh, Dong-Ha; Dassanayake, Maheshi
- DNA Research, Vol. 26, Issue 1
Gene duplication and dosage effects during the early emergence of C4 photosynthesis in the grass genus Alloteropsis
journal, February 2018
- Bianconi, Matheus E.; Dunning, Luke T.; Moreno-Villena, Jose J.
- Journal of Experimental Botany, Vol. 69, Issue 8
The molecular evolution of C4 photosynthesis: opportunities for understanding and improving the world’s most productive plants
journal, November 2018
- Niklaus, Michael; Kelly, Steven
- Journal of Experimental Botany, Vol. 70, Issue 3
Key changes in gene expression identified for different stages of C4 evolution in Alloteropsis semialata
journal, April 2019
- Dunning, Luke T.; Moreno-Villena, Jose J.; Lundgren, Marjorie R.
- Journal of Experimental Botany, Vol. 70, Issue 12
Highly Expressed Genes Are Preferentially Co-Opted for C4 Photosynthesis
journal, October 2017
- Moreno-Villena, Jose J.; Dunning, Luke T.; Osborne, Colin P.
- Molecular Biology and Evolution, Vol. 35, Issue 1
Synergistic Binding of bHLH Transcription Factors to the Promoter of the Maize NADP-ME Gene Used in C4 Photosynthesis Is Based on an Ancient Code Found in the Ancestral C3 State
journal, April 2018
- Borba, Ana Rita; Serra, Tânia S.; Górska, Alicja
- Molecular Biology and Evolution, Vol. 35, Issue 7
Synergistic binding of bHLH transcription factors to the promoter of the maize NADP-ME gene used in C 4 photosynthesis is based on an ancient code found in the ancestral C 3 state
journal, January 2018
- Borba, Ana Rita; Serra, Tânia S.; Górska, Alicja
- Molecular Biology and Evolution
Impaired phloem loading in zmsweet13a,b,c sucrose transporter triple knock-out mutants in Zea mays
journal, February 2018
- Bezrutczyk, Margaret; Hartwig, Thomas; Horschman, Marc
- New Phytologist, Vol. 218, Issue 2
On the road to C 4 rice: advances and perspectives
journal, November 2019
- Ermakova, Maria; Danila, Florence R.; Furbank, Robert T.
- The Plant Journal, Vol. 101, Issue 4
Genome-wide analysis of UDP-glycosyltransferase super family in Brassica rapa and Brassica oleracea reveals its evolutionary history and functional characterization
journal, June 2017
- Yu, Jingyin; Hu, Fan; Dossa, Komivi
- BMC Genomics, Vol. 18, Issue 1
New insights into the evolution and functional divergence of the SWEET family in Saccharum based on comparative genomics
journal, November 2018
- Hu, Weichang; Hua, Xiuting; Zhang, Qing
- BMC Plant Biology, Vol. 18, Issue 1
Data from: Independent and parallel evolution of new genes by gene duplication in two origins of C4 photosynthesis provides new insight into the mechanism of phloem loading in C4 species
dataset, April 2016
- Emms, David M.; Covshoff, Sarah; Hibberd, Julian M.
- Dryad Digital Repository-Supplementary information for journal article at DOI: 10.1093/molbev/msw057, 1 ZIP file (1.587 Mb)
Data from: Independent and parallel evolution of new genes by gene duplication in two origins of C4 photosynthesis provides new insight into the mechanism of phloem loading in C4 species
dataset, April 2016
- Emms, David M.; Covshoff, Sarah; Hibberd, Julian M.
- Dryad Digital Repository-Supplementary information for journal article at DOI: 10.1093/molbev/msw057, 1 ZIP file (1.587 Mb)
Cross species selection scans identify components of C 4 photosynthesis in the grasses
journal, July 2016
- Huang, Pu; Studer, Anthony J.; Schnable, James C.
- Journal of Experimental Botany, Vol. 68, Issue 2
Multiple mechanisms for enhanced plasmodesmata density in disparate subtypes of C4 grasses
journal, January 2018
- Danila, Florence R.; Quick, William Paul; White, Rosemary G.
- Journal of Experimental Botany, Vol. 69, Issue 5
Gene duplication and dosage effects during the early emergence of C4 photosynthesis in the grass genus Alloteropsis
journal, February 2018
- Bianconi, Matheus E.; Dunning, Luke T.; Moreno-Villena, Jose J.
- Journal of Experimental Botany, Vol. 69, Issue 8
Key changes in gene expression identified for different stages of C4 evolution in Alloteropsis semialata
journal, April 2019
- Dunning, Luke T.; Moreno-Villena, Jose J.; Lundgren, Marjorie R.
- Journal of Experimental Botany, Vol. 70, Issue 12
Synergistic binding of bHLH transcription factors to the promoter of the maize NADP-ME gene used in C 4 photosynthesis is based on an ancient code found in the ancestral C 3 state
journal, January 2018
- Borba, Ana Rita; Serra, Tânia S.; Górska, Alicja
- Molecular Biology and Evolution
Genome-wide analysis of UDP-glycosyltransferase super family in Brassica rapa and Brassica oleracea reveals its evolutionary history and functional characterization
journal, June 2017
- Yu, Jingyin; Hu, Fan; Dossa, Komivi
- BMC Genomics, Vol. 18, Issue 1
New insights into the evolution and functional divergence of the SWEET family in Saccharum based on comparative genomics
journal, November 2018
- Hu, Weichang; Hua, Xiuting; Zhang, Qing
- BMC Plant Biology, Vol. 18, Issue 1
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