The Kalanchoë genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism

Xiaohan Yang; Rongbin Hu; Hengfu Yin; Jerry Jenkins; Shengqiang Shu; Haibao Tang; Degao Liu; Deborah A. Weighill; Won Cheol Yim; Jungmin Ha; Karolina Heyduk; David M. Goodstein; Hao Bo Guo; Robert C. Moseley; Elisabeth Fitzek; Sara Jawdy; Zhihao Zhang; Meng Xie; James Hartwell; Jane Grimwood; Paul E. Abraham; Ritesh Mewalal; Juan D. Beltrán; Susanna F. Boxall; Louisa V. Dever; Kaitlin J. Palla; Rebecca Albion; Travis Garcia; Jesse A. Mayer; Sung Don Lim; Ching Man Wai; Paul Peluso; Robert Van Buren; Henrique Cestari De Paoli; Anne M. Borland; Hong Guo; Jin Gui Chen; Wellington Muchero; Yanbin Yin; Daniel A. Jacobson; Timothy J. Tschaplinski; Robert L. Hettich; Ray Ming; Klaus Winter; James H. Leebens-Mack; J. Andrew C. Smith; John C. Cushman; Jeremy Schmutz; Gerald A. Tuskan

doi:10.1038/s41467-017-01491-7

The Kalanchoë genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism

Xiaohan Yang, Rongbin Hu, Hengfu Yin, Jerry Jenkins, Shengqiang Shu, Haibao Tang, Degao Liu, Deborah A. Weighill, Won Cheol Yim, Jungmin Ha, Karolina Heyduk, David M. Goodstein, Hao Bo Guo, Robert C. Moseley, Elisabeth Fitzek, Sara Jawdy, Zhihao Zhang, Meng Xie, James Hartwell, Jane GrimwoodPaul E. Abraham, Ritesh Mewalal, Juan D. Beltrán, Susanna F. Boxall, Louisa V. Dever, Kaitlin J. Palla, Rebecca Albion, Travis Garcia, Jesse A. Mayer, Sung Don Lim, Ching Man Wai, Paul Peluso, Robert Van Buren, Henrique Cestari De Paoli, Anne M. Borland, Hong Guo, Jin Gui Chen, Wellington Muchero, Yanbin Yin, Daniel A. Jacobson, Timothy J. Tschaplinski, Robert L. Hettich, Ray Ming, Klaus Winter, James H. Leebens-Mack, J. Andrew C. Smith, John C. Cushman, Jeremy Schmutz, Gerald A. Tuskan

Research output: Contribution to journal › Article › peer-review

126 Scopus citations

Abstract

Crassulacean acid metabolism (CAM) is a water-use efficient adaptation of photosynthesis that has evolved independently many times in diverse lineages of flowering plants. We hypothesize that convergent evolution of protein sequence and temporal gene expression underpins the independent emergences of CAM from C₃ photosynthesis. To test this hypothesis, we generate a de novo genome assembly and genome-wide transcript expression data for Kalanchoë fedtschenkoi, an obligate CAM species within the core eudicots with a relatively small genome (~260 Mb). Our comparative analyses identify signatures of convergence in protein sequence and re-scheduling of diel transcript expression of genes involved in nocturnal CO₂ fixation, stomatal movement, heat tolerance, circadian clock, and carbohydrate metabolism in K. fedtschenkoi and other CAM species in comparison with non-CAM species. These findings provide new insights into molecular convergence and building blocks of CAM and will facilitate CAM-into-C₃ photosynthesis engineering to enhance water-use efficiency in crops.

Original language	English (US)
Article number	1899
Journal	Nature communications
Volume	8
Issue number	1
DOIs	https://doi.org/10.1038/s41467-017-01491-7
State	Published - Dec 1 2017
Externally published	Yes

Bibliographical note

Funding Information:
This manuscript has been authored by UT-Battelle, LLC under Contract No. DE-AC05-00OR22725 with the U.S. Department of Energy. This research was supported by the U.S. Department of Energy, Office of Science, Genomic Science Program under Award Number DE-SC0008834. Additional support was provided by the UK Biotechnology and Biological Sciences Research Council (grant no. BB/F009313/1) and the Laboratory Directed Research and Development (LDRD) Program (Project ID: 7758) of Oak Ridge National Laboratory. The work conducted by the U.S. Department of Energy Joint Genome Institute is supported by the Office of Science of the U.S. Department of Energy under Contract No. DE-AC02–05CH11231. This research used resources of the Oak Ridge Leadership Computing Facility at the Oak Ridge National Laboratory. This research also used the Compute and Data Environment for Science (CADES) at the Oak Ridge National Laboratory. We thank Daniel Rokhsar, Mary Ann Cushman, and Lee Gunter for critical review and comments on the manuscript and Lori Kunder (Kunder Design Studio) for assistance with figure preparation. Oak Ridge National Laboratory is managed by UT-Battelle, LLC for the U.S. Department of Energy under Contract Number DE-AC05-00OR22725.

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© 2017 The Author(s).

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Yang, X., Hu, R., Yin, H., Jenkins, J., Shu, S., Tang, H., Liu, D., Weighill, D. A., Cheol Yim, W., Ha, J., Heyduk, K., Goodstein, D. M., Guo, H. B., Moseley, R. C., Fitzek, E., Jawdy, S., Zhang, Z., Xie, M., Hartwell, J., ... Tuskan, G. A. (2017). The Kalanchoë genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism. Nature communications, 8(1), Article 1899. https://doi.org/10.1038/s41467-017-01491-7

Yang, X, Hu, R, Yin, H, Jenkins, J, Shu, S, Tang, H, Liu, D, Weighill, DA, Cheol Yim, W, Ha, J, Heyduk, K, Goodstein, DM, Guo, HB, Moseley, RC, Fitzek, E, Jawdy, S, Zhang, Z, Xie, M, Hartwell, J, Grimwood, J, Abraham, PE, Mewalal, R, Beltrán, JD, Boxall, SF, Dever, LV, Palla, KJ, Albion, R, Garcia, T, Mayer, JA, Don Lim, S, Man Wai, C, Peluso, P, Van Buren, R, De Paoli, HC, Borland, AM, Guo, H, Chen, JG, Muchero, W, Yin, Y, Jacobson, DA, Tschaplinski, TJ, Hettich, RL, Ming, R, Winter, K, Leebens-Mack, JH, Smith, JAC, Cushman, JC, Schmutz, J & Tuskan, GA 2017, 'The Kalanchoë genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism', Nature communications, vol. 8, no. 1, 1899. https://doi.org/10.1038/s41467-017-01491-7

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abstract = "Crassulacean acid metabolism (CAM) is a water-use efficient adaptation of photosynthesis that has evolved independently many times in diverse lineages of flowering plants. We hypothesize that convergent evolution of protein sequence and temporal gene expression underpins the independent emergences of CAM from C3 photosynthesis. To test this hypothesis, we generate a de novo genome assembly and genome-wide transcript expression data for Kalancho{\"e} fedtschenkoi, an obligate CAM species within the core eudicots with a relatively small genome (~260 Mb). Our comparative analyses identify signatures of convergence in protein sequence and re-scheduling of diel transcript expression of genes involved in nocturnal CO2 fixation, stomatal movement, heat tolerance, circadian clock, and carbohydrate metabolism in K. fedtschenkoi and other CAM species in comparison with non-CAM species. These findings provide new insights into molecular convergence and building blocks of CAM and will facilitate CAM-into-C3 photosynthesis engineering to enhance water-use efficiency in crops.",

author = "Xiaohan Yang and Rongbin Hu and Hengfu Yin and Jerry Jenkins and Shengqiang Shu and Haibao Tang and Degao Liu and Weighill, {Deborah A.} and {Cheol Yim}, Won and Jungmin Ha and Karolina Heyduk and Goodstein, {David M.} and Guo, {Hao Bo} and Moseley, {Robert C.} and Elisabeth Fitzek and Sara Jawdy and Zhihao Zhang and Meng Xie and James Hartwell and Jane Grimwood and Abraham, {Paul E.} and Ritesh Mewalal and Beltr{\'a}n, {Juan D.} and Boxall, {Susanna F.} and Dever, {Louisa V.} and Palla, {Kaitlin J.} and Rebecca Albion and Travis Garcia and Mayer, {Jesse A.} and {Don Lim}, Sung and {Man Wai}, Ching and Paul Peluso and {Van Buren}, Robert and {De Paoli}, {Henrique Cestari} and Borland, {Anne M.} and Hong Guo and Chen, {Jin Gui} and Wellington Muchero and Yanbin Yin and Jacobson, {Daniel A.} and Tschaplinski, {Timothy J.} and Hettich, {Robert L.} and Ray Ming and Klaus Winter and Leebens-Mack, {James H.} and Smith, {J. Andrew C.} and Cushman, {John C.} and Jeremy Schmutz and Tuskan, {Gerald A.}",

note = "Funding Information: This manuscript has been authored by UT-Battelle, LLC under Contract No. DE-AC05-00OR22725 with the U.S. Department of Energy. This research was supported by the U.S. Department of Energy, Office of Science, Genomic Science Program under Award Number DE-SC0008834. Additional support was provided by the UK Biotechnology and Biological Sciences Research Council (grant no. BB/F009313/1) and the Laboratory Directed Research and Development (LDRD) Program (Project ID: 7758) of Oak Ridge National Laboratory. The work conducted by the U.S. Department of Energy Joint Genome Institute is supported by the Office of Science of the U.S. Department of Energy under Contract No. DE-AC02–05CH11231. This research used resources of the Oak Ridge Leadership Computing Facility at the Oak Ridge National Laboratory. This research also used the Compute and Data Environment for Science (CADES) at the Oak Ridge National Laboratory. We thank Daniel Rokhsar, Mary Ann Cushman, and Lee Gunter for critical review and comments on the manuscript and Lori Kunder (Kunder Design Studio) for assistance with figure preparation. Oak Ridge National Laboratory is managed by UT-Battelle, LLC for the U.S. Department of Energy under Contract Number DE-AC05-00OR22725. Publisher Copyright: {\textcopyright} 2017 The Author(s).",

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AU - Yang, Xiaohan

AU - Hu, Rongbin

AU - Yin, Hengfu

AU - Jenkins, Jerry

AU - Shu, Shengqiang

AU - Tang, Haibao

AU - Liu, Degao

AU - Weighill, Deborah A.

AU - Cheol Yim, Won

AU - Ha, Jungmin

AU - Heyduk, Karolina

AU - Goodstein, David M.

AU - Guo, Hao Bo

AU - Moseley, Robert C.

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AU - Xie, Meng

AU - Hartwell, James

AU - Grimwood, Jane

AU - Abraham, Paul E.

AU - Mewalal, Ritesh

AU - Beltrán, Juan D.

AU - Boxall, Susanna F.

AU - Dever, Louisa V.

AU - Palla, Kaitlin J.

AU - Albion, Rebecca

AU - Garcia, Travis

AU - Mayer, Jesse A.

AU - Don Lim, Sung

AU - Man Wai, Ching

AU - Peluso, Paul

AU - Van Buren, Robert

AU - De Paoli, Henrique Cestari

AU - Borland, Anne M.

AU - Guo, Hong

AU - Chen, Jin Gui

AU - Muchero, Wellington

AU - Yin, Yanbin

AU - Jacobson, Daniel A.

AU - Tschaplinski, Timothy J.

AU - Hettich, Robert L.

AU - Ming, Ray

AU - Winter, Klaus

AU - Leebens-Mack, James H.

AU - Smith, J. Andrew C.

AU - Cushman, John C.

AU - Schmutz, Jeremy

AU - Tuskan, Gerald A.

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N2 - Crassulacean acid metabolism (CAM) is a water-use efficient adaptation of photosynthesis that has evolved independently many times in diverse lineages of flowering plants. We hypothesize that convergent evolution of protein sequence and temporal gene expression underpins the independent emergences of CAM from C3 photosynthesis. To test this hypothesis, we generate a de novo genome assembly and genome-wide transcript expression data for Kalanchoë fedtschenkoi, an obligate CAM species within the core eudicots with a relatively small genome (~260 Mb). Our comparative analyses identify signatures of convergence in protein sequence and re-scheduling of diel transcript expression of genes involved in nocturnal CO2 fixation, stomatal movement, heat tolerance, circadian clock, and carbohydrate metabolism in K. fedtschenkoi and other CAM species in comparison with non-CAM species. These findings provide new insights into molecular convergence and building blocks of CAM and will facilitate CAM-into-C3 photosynthesis engineering to enhance water-use efficiency in crops.

AB - Crassulacean acid metabolism (CAM) is a water-use efficient adaptation of photosynthesis that has evolved independently many times in diverse lineages of flowering plants. We hypothesize that convergent evolution of protein sequence and temporal gene expression underpins the independent emergences of CAM from C3 photosynthesis. To test this hypothesis, we generate a de novo genome assembly and genome-wide transcript expression data for Kalanchoë fedtschenkoi, an obligate CAM species within the core eudicots with a relatively small genome (~260 Mb). Our comparative analyses identify signatures of convergence in protein sequence and re-scheduling of diel transcript expression of genes involved in nocturnal CO2 fixation, stomatal movement, heat tolerance, circadian clock, and carbohydrate metabolism in K. fedtschenkoi and other CAM species in comparison with non-CAM species. These findings provide new insights into molecular convergence and building blocks of CAM and will facilitate CAM-into-C3 photosynthesis engineering to enhance water-use efficiency in crops.

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The Kalanchoë genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism

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