Comparative Genomic Analysis of C4 Photosynthesis Pathway Evolution in Grasses
C4 plants are among the most productive crops, in part due to the efficiency at which their distinctive photosynthetic pathway fixes carbon at high temperatures. Sorghum and maize are C4 plants with full genome sequences available, facilitating a whole-ge
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Comparative Genomic Analysis of C4 Photosynthesis Pathway Evolution in Grasses Xiyin Wang and Andrew H. Paterson
Abstract C4 plants are among the most productive crops, in part due to the efficiency at which their distinctive photosynthetic pathway fixes carbon at high temperatures. Sorghum and maize are C4 plants with full genome sequences available, facilitating a whole-genome level exploration of C4 pathway formation by comparing their respective versions of these key photosynthetic enzyme genes to those in the C3 plants rice and Brachypodium. A reservoir of duplicated genes was previously hypothesized to be a prerequisite for the evolution of C4 photosynthesis from a C3 progenitor. Grasses have been affected both by a whole-genome duplication (WGD) and individual gene duplications, and we show each of these mechanisms to have contributed to evolution of C4 photosynthesis. Some C4 genes appear to have been recruited directly from WGD duplicates followed by neofunctionalization. Others, such as the sorghum and maize carbonic anhydrase (CA) genes, have been recursively affected by tandem duplication, and mutations in stop codons have produced distinct C4 CA genes having 1–3 functional units, implying an interesting type of new gene formation accompanied by adaptive evolution. Key C4 enzymes in sorghum and maize show evidence of adaptive evolution, though differing in the level and mode. Intriguingly, a phosphoenolpyruvate carboxylase (PEPC) gene has
X. Wang (*) Plant Genome Mapping Laboratory, Departments of Crop and Soil Science, Plant Biology, and Genetics, University of Georgia, 2091 South Milledge Ave, C67, Athens, GA 30602, USA Center for Genomics and Computational Biology, School of Life Sciences, Hebei United University, Tangshan, Hebei 063009, China e-mail: [email protected] A.H. Paterson Plant Genome Mapping Laboratory, Departments of Crop and Soil Science, Plant Biology, and Genetics, University of Georgia, 2091 South Milledge Ave, C67, Athens, GA 30602, USA A.H. Paterson (ed.), Genomics of the Saccharinae, Plant Genetics and Genomics: Crops and Models 11, DOI 10.1007/978-1-4419-5947-8_19, © Springer Science+Business Media New York 2013
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X. Wang and A.H. Paterson
also been evolving rapidly in both rice and Brachypodium and shows evidence of adaptive evolution, though lacking key mutations that are characteristic of C4 genes. The heterogeneity of origins of C4 genes suggests that there may have been a long transition process before the eventual establishment of C4 photosynthesis. Keywords C4 photosynthesis pathway • Grass • Comparative genomics • Gene duplication • Adaptive evolution • Sorghum • Maize • Rice • Brachypodium
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Introduction to the C4 Photosynthetic Pathway
Many of the most productive crops in agriculture are C4 plants. Despite their multiple origins, they are all characterized by high rates of photosynthesis and efficient use of water and nitrogen. As a morphological and biochemical innovation (Hatch and Slack 1966), the C4 photosynthetic pathway is proposed to have been an
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