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Title: The Kalanchoe genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism

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.

Authors:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [2];  [3];  [4]; ORCiD logo [5];  [2]; ORCiD logo [1]; ORCiD logo [6];  [6];  [7];  [4];  [8];  [1];  [9];  [2];  [2]; ORCiD logo [2]; ORCiD logo [10];  [3] more »;  [2]; ORCiD logo [2];  [11];  [10];  [10];  [1];  [6];  [6];  [6];  [6];  [12];  [13];  [14]; ORCiD logo [1];  [15];  [8]; ORCiD logo [2];  [2];  [9]; ORCiD logo [1]; ORCiD logo [2];  [2];  [16];  [17];  [7];  [11];  [6];  [18];  [2] « less
+ Show Author Affiliations
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  3. HudsonAlpha Institute for Biotechnology, Huntsville, AL (United States)
  4. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  5. Fujian Agriculture and Forestry Univ., Fujian (China)
  6. Univ. of Nevada, Reno, NV (United States)
  7. Univ. of Georgia, Athens, GA (United States)
  8. Univ. of Tennessee, Knoxville, TN (United States)
  9. Northern Illinois Univ., DeKalb, IL (United States)
  10. Univ. of Liverpool, Liverpool (United Kingdom)
  11. Univ. of Oxford, Oxford (United Kingdom)
  12. Univ. of Illinois at Urbana-Champaign, Urbana, IL (United States)
  13. Pacific Biosciences, Inc., Menlo Park, CA (United States)
  14. Michigan State Univ., East Lansing, MI (United States)
  15. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Newcastle Univ., Newcastle upon Tyne (United Kingdom)
  16. Fujian Agriculture and Forestry Univ., Fujian (China); Univ. of Illinois at Urbana-Champaign, Urbana, IL (United States)
  17. Smithsonian Tropical Research Institute, Ancon (Republic of Panama)
  18. HudsonAlpha Institute for Biotechnology, Huntsville, AL (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). Oak Ridge Leadership Computing Facility (OLCF); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1413629
Alternate Identifier(s):
OSTI ID: 1435095
Grant/Contract Number:  
AC05-00OR22725; AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 8; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES

Citation Formats

Yang, Xiaohan, Hu, Rongbin, Yin, Hengfu, Jenkins, Jerry, Shu, Shengqiang, Tang, Haibao, Liu, Degao, Weighill, Deborah A., Yim, Won Cheol, Ha, Jungmin, Heyduk, Karolina, Goodstein, David M., Guo, Hao -Bo, Moseley, Robert C., Fitzek, Elisabeth, Jawdy, Sara, Zhang, Zhihao, Xie, Meng, Hartwell, James, Grimwood, Jane, Abraham, Paul E., Mewalal, Ritesh, Beltran, Juan D., Boxall, Susanna F., Dever, Louisa V., Palla, Kaitlin J., Albion, Rebecca, Garcia, Travis, Mayer, Jesse A., Lim, Sung Don, Wai, Ching Man, Peluso, Paul, Van Buren, Robert, De Paoli, Henrique Cestari, Borland, Anne M., Guo, Hong, Chen, Jin -Gui, Muchero, Wellington, Yin, Yanbin, Jacobson, Daniel A., Tschaplinski, Timothy J., Hettich, Robert L., Ming, Ray, Winter, Klaus, Leebens-Mack, James H., Smith, J. Andrew C., Cushman, John C., Schmutz, Jeremy, and Tuskan, Gerald A. The Kalanchoe genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism. United States: N. p., 2017. Web. doi:10.1038/s41467-017-01491-7.
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Yang, Xiaohan, Hu, Rongbin, Yin, Hengfu, Jenkins, Jerry, Shu, Shengqiang, Tang, Haibao, Liu, Degao, Weighill, Deborah A., Yim, Won Cheol, Ha, Jungmin, Heyduk, Karolina, Goodstein, David M., Guo, Hao -Bo, Moseley, Robert C., Fitzek, Elisabeth, Jawdy, Sara, Zhang, Zhihao, Xie, Meng, Hartwell, James, Grimwood, Jane, Abraham, Paul E., Mewalal, Ritesh, Beltran, Juan D., Boxall, Susanna F., Dever, Louisa V., Palla, Kaitlin J., Albion, Rebecca, Garcia, Travis, Mayer, Jesse A., Lim, Sung Don, Wai, Ching Man, Peluso, Paul, Van Buren, Robert, De Paoli, Henrique Cestari, Borland, Anne M., Guo, Hong, Chen, Jin -Gui, Muchero, Wellington, Yin, Yanbin, Jacobson, Daniel A., Tschaplinski, Timothy J., Hettich, Robert L., Ming, Ray, Winter, Klaus, Leebens-Mack, James H., Smith, J. Andrew C., Cushman, John C., Schmutz, Jeremy, & Tuskan, Gerald A. The Kalanchoe genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism. United States. https://doi.org/10.1038/s41467-017-01491-7
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Yang, Xiaohan, Hu, Rongbin, Yin, Hengfu, Jenkins, Jerry, Shu, Shengqiang, Tang, Haibao, Liu, Degao, Weighill, Deborah A., Yim, Won Cheol, Ha, Jungmin, Heyduk, Karolina, Goodstein, David M., Guo, Hao -Bo, Moseley, Robert C., Fitzek, Elisabeth, Jawdy, Sara, Zhang, Zhihao, Xie, Meng, Hartwell, James, Grimwood, Jane, Abraham, Paul E., Mewalal, Ritesh, Beltran, Juan D., Boxall, Susanna F., Dever, Louisa V., Palla, Kaitlin J., Albion, Rebecca, Garcia, Travis, Mayer, Jesse A., Lim, Sung Don, Wai, Ching Man, Peluso, Paul, Van Buren, Robert, De Paoli, Henrique Cestari, Borland, Anne M., Guo, Hong, Chen, Jin -Gui, Muchero, Wellington, Yin, Yanbin, Jacobson, Daniel A., Tschaplinski, Timothy J., Hettich, Robert L., Ming, Ray, Winter, Klaus, Leebens-Mack, James H., Smith, J. Andrew C., Cushman, John C., Schmutz, Jeremy, and Tuskan, Gerald A. Fri . "The Kalanchoe genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism". United States. https://doi.org/10.1038/s41467-017-01491-7. https://www.osti.gov/servlets/purl/1413629.
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@article{osti_1413629,
title = {The Kalanchoe genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism},
author = {Yang, Xiaohan and Hu, Rongbin and Yin, Hengfu and Jenkins, Jerry and Shu, Shengqiang and Tang, Haibao and Liu, Degao and Weighill, Deborah A. and Yim, Won Cheol and Ha, Jungmin and Heyduk, Karolina and Goodstein, David M. and Guo, Hao -Bo and Moseley, Robert C. and Fitzek, Elisabeth and Jawdy, Sara and Zhang, Zhihao and Xie, Meng and Hartwell, James and Grimwood, Jane and Abraham, Paul E. and Mewalal, Ritesh and Beltran, Juan D. and Boxall, Susanna F. and Dever, Louisa V. and Palla, Kaitlin J. and Albion, Rebecca and Garcia, Travis and Mayer, Jesse A. and Lim, Sung Don and Wai, Ching Man and Peluso, Paul and Van Buren, Robert and De Paoli, Henrique Cestari and Borland, Anne M. and Guo, Hong and Chen, Jin -Gui and Muchero, Wellington and Yin, Yanbin and Jacobson, Daniel A. and Tschaplinski, Timothy J. and Hettich, Robert L. and Ming, Ray and Winter, Klaus and Leebens-Mack, James H. and Smith, J. Andrew C. and Cushman, John C. and Schmutz, Jeremy and Tuskan, Gerald A.},
abstractNote = {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.},
doi = {10.1038/s41467-017-01491-7},
journal = {Nature Communications},
number = 1,
volume = 8,
place = {United States},
year = {Fri Dec 01 00:00:00 EST 2017},
month = {Fri Dec 01 00:00:00 EST 2017}
}
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