Comparative genomics analysis of drought response between obligate CAM and C3 photosynthesis plants

Rongbin Hu; Jin Zhang; Sara Jawdy; Avinash Sreedasyam; Anna Lipzen; Mei Wang; Vivian Ng; Christopher Daum; Keykhosrow Keymanesh; Degao Liu; Haiwei Lu; Priya Ranjan; Jin Gui Chen; Wellington Muchero; Timothy J. Tschaplinski; Gerald A. Tuskan; Jeremy Schmutz; Xiaohan Yang

doi:10.1016/j.jplph.2022.153791

Comparative genomics analysis of drought response between obligate CAM and C₃ photosynthesis plants

Rongbin Hu, Jin Zhang, Sara Jawdy, Avinash Sreedasyam, Anna Lipzen, Mei Wang, Vivian Ng, Christopher Daum, Keykhosrow Keymanesh, Degao Liu, Haiwei Lu, Priya Ranjan, Jin Gui Chen, Wellington Muchero, Timothy J. Tschaplinski, Gerald A. Tuskan, Jeremy Schmutz, Xiaohan Yang

Genetics, Cell Biology and Development (CBS)

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

3 Scopus citations

Abstract

Crassulacean acid metabolism (CAM) plants exhibit elevated drought and heat tolerance compared to C₃ and C₄ plants through an inverted pattern of day/night stomatal closure and opening for CO₂ assimilation. However, the molecular responses to water-deficit conditions remain unclear in obligate CAM species. In this study, we presented genome-wide transcription sequencing analysis using leaf samples of an obligate CAM species Kalanchoë fedtschenkoi under moderate and severe drought treatments at two-time points of dawn (2-h before the start of light period) and dusk (2-h before the dark period). Differentially expressed genes were identified in response to environmental drought stress and a whole genome wide co-expression network was created as well. We found that the expression of CAM-related genes was not regulated by drought stimuli in K. fedtschenkoi. Our comparative analysis revealed that CAM species (K. fedtschenkoi) and C₃ species (Arabidopsis thaliana, Populus deltoides ‘WV94’) share some common transcriptional changes in genes involved in multiple biological processes in response to drought stress, including ABA signaling and biosynthesis of secondary metabolites.

Original language	English (US)
Article number	153791
Journal	Journal of Plant Physiology
Volume	277
DOIs	https://doi.org/10.1016/j.jplph.2022.153791
State	Published - Oct 2022

Bibliographical note

Funding Information:
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 Community Science Program (project 503025) at the Department of Energy Joint Genome Institute and the DOE Center for Bioenergy Innovation at the Oak Ridge National Laboratory. The writing of this manuscript was supported by the Center for Bioenergy Innovation, a U.S. Department of Energy (DOE) Bioenergy Research Center supported by the Biological and Environmental Research (BER) program. J.Z. is funded by the Zhejiang A&F University Research and Development Fund Talent Startup Project (2021LFR013).The work (proposal: 10.46936/10.25585/60001095) conducted by the U.S. Department of Energy Joint Genome Institute (https://ror.org/04xm1d337), a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy operated under Contract No. DE-AC02-05CH11231. This research is also supported by the U.S. Department of Energy (DOE), Office of Science, Genomic Science Program under Award Number DE-SC0008834, and the Center for Bioenergy Innovation (CBI), which is a DOE Bioenergy Research Center supported by the Biological and Environmental Research program in the DOE Office of Science. Oak Ridge National Laboratory is managed by UT-Battelle, LLC for the DOE under Contract Number DE-AC05–00OR22725. This research used resources of the Compute and Data Environment for Science (CADES) and the Oak Ridge Leadership Computing Facility at the Oak Ridge National Laboratory.

Funding Information:
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 Community Science Program (project 503025 ) at the Department of Energy Joint Genome Institute and the DOE Center for Bioenergy Innovation at the Oak Ridge National Laboratory . The writing of this manuscript was supported by the Center for Bioenergy Innovation , a U.S. Department of Energy (DOE) Bioenergy Research Center supported by the Biological and Environmental Research (BER) program. J.Z. is funded by the Zhejiang A&F University Research and Development Fund Talent Startup Project ( 2021LFR013 ).

Funding Information:
The work (proposal: 10.46936/10.25585/60001095 ) conducted by the U.S. Department of Energy Joint Genome Institute ( https://ror.org/04xm1d337 ), a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy operated under Contract No. DE-AC02-05CH11231 . This research is also supported by the U.S. Department of Energy (DOE), Office of Science , Genomic Science Program under Award Number DE-SC0008834 , and the Center for Bioenergy Innovation (CBI) , which is a DOE Bioenergy Research Center supported by the Biological and Environmental Research program in the DOE Office of Science . Oak Ridge National Laboratory is managed by UT-Battelle, LLC for the DOE under Contract Number DE-AC05–00OR22725 . This research used resources of the Compute and Data Environment for Science (CADES) and the Oak Ridge Leadership Computing Facility at the Oak Ridge National Laboratory .

Publisher Copyright:
© 2022 The Authors

Keywords

Abscisic acid
Crassulacean acid metabolism
Drought stress
Kalanchoë fedtschenkoi
RNA-Seq
Secondary metabolism

Publisher link

10.1016/j.jplph.2022.153791

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Cite this

Hu, R., Zhang, J., Jawdy, S., Sreedasyam, A., Lipzen, A., Wang, M., Ng, V., Daum, C., Keymanesh, K., Liu, D., Lu, H., Ranjan, P., Chen, J. G., Muchero, W., Tschaplinski, T. J., Tuskan, G. A., Schmutz, J., & Yang, X. (2022). Comparative genomics analysis of drought response between obligate CAM and C₃ photosynthesis plants. Journal of Plant Physiology, 277, Article 153791. https://doi.org/10.1016/j.jplph.2022.153791

Hu, R, Zhang, J, Jawdy, S, Sreedasyam, A, Lipzen, A, Wang, M, Ng, V, Daum, C, Keymanesh, K, Liu, D, Lu, H, Ranjan, P, Chen, JG, Muchero, W, Tschaplinski, TJ, Tuskan, GA, Schmutz, J & Yang, X 2022, 'Comparative genomics analysis of drought response between obligate CAM and C₃ photosynthesis plants', Journal of Plant Physiology, vol. 277, 153791. https://doi.org/10.1016/j.jplph.2022.153791

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title = "Comparative genomics analysis of drought response between obligate CAM and C3 photosynthesis plants",

abstract = "Crassulacean acid metabolism (CAM) plants exhibit elevated drought and heat tolerance compared to C3 and C4 plants through an inverted pattern of day/night stomatal closure and opening for CO2 assimilation. However, the molecular responses to water-deficit conditions remain unclear in obligate CAM species. In this study, we presented genome-wide transcription sequencing analysis using leaf samples of an obligate CAM species Kalancho{\"e} fedtschenkoi under moderate and severe drought treatments at two-time points of dawn (2-h before the start of light period) and dusk (2-h before the dark period). Differentially expressed genes were identified in response to environmental drought stress and a whole genome wide co-expression network was created as well. We found that the expression of CAM-related genes was not regulated by drought stimuli in K. fedtschenkoi. Our comparative analysis revealed that CAM species (K. fedtschenkoi) and C3 species (Arabidopsis thaliana, Populus deltoides {\textquoteleft}WV94{\textquoteright}) share some common transcriptional changes in genes involved in multiple biological processes in response to drought stress, including ABA signaling and biosynthesis of secondary metabolites.",

keywords = "Abscisic acid, Crassulacean acid metabolism, Drought stress, Kalancho{\"e} fedtschenkoi, RNA-Seq, Secondary metabolism",

author = "Rongbin Hu and Jin Zhang and Sara Jawdy and Avinash Sreedasyam and Anna Lipzen and Mei Wang and Vivian Ng and Christopher Daum and Keykhosrow Keymanesh and Degao Liu and Haiwei Lu and Priya Ranjan and Chen, {Jin Gui} and Wellington Muchero and Tschaplinski, {Timothy J.} and Tuskan, {Gerald A.} and Jeremy Schmutz and Xiaohan Yang",

note = "Funding Information: 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 Community Science Program (project 503025) at the Department of Energy Joint Genome Institute and the DOE Center for Bioenergy Innovation at the Oak Ridge National Laboratory. The writing of this manuscript was supported by the Center for Bioenergy Innovation, a U.S. Department of Energy (DOE) Bioenergy Research Center supported by the Biological and Environmental Research (BER) program. J.Z. is funded by the Zhejiang A&F University Research and Development Fund Talent Startup Project (2021LFR013).The work (proposal: 10.46936/10.25585/60001095) conducted by the U.S. Department of Energy Joint Genome Institute (https://ror.org/04xm1d337), a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy operated under Contract No. DE-AC02-05CH11231. This research is also supported by the U.S. Department of Energy (DOE), Office of Science, Genomic Science Program under Award Number DE-SC0008834, and the Center for Bioenergy Innovation (CBI), which is a DOE Bioenergy Research Center supported by the Biological and Environmental Research program in the DOE Office of Science. Oak Ridge National Laboratory is managed by UT-Battelle, LLC for the DOE under Contract Number DE-AC05–00OR22725. This research used resources of the Compute and Data Environment for Science (CADES) and the Oak Ridge Leadership Computing Facility at the Oak Ridge National Laboratory. Funding Information: 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 Community Science Program (project 503025 ) at the Department of Energy Joint Genome Institute and the DOE Center for Bioenergy Innovation at the Oak Ridge National Laboratory . The writing of this manuscript was supported by the Center for Bioenergy Innovation , a U.S. Department of Energy (DOE) Bioenergy Research Center supported by the Biological and Environmental Research (BER) program. J.Z. is funded by the Zhejiang A&F University Research and Development Fund Talent Startup Project ( 2021LFR013 ). Funding Information: The work (proposal: 10.46936/10.25585/60001095 ) conducted by the U.S. Department of Energy Joint Genome Institute ( https://ror.org/04xm1d337 ), a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy operated under Contract No. DE-AC02-05CH11231 . This research is also supported by the U.S. Department of Energy (DOE), Office of Science , Genomic Science Program under Award Number DE-SC0008834 , and the Center for Bioenergy Innovation (CBI) , which is a DOE Bioenergy Research Center supported by the Biological and Environmental Research program in the DOE Office of Science . Oak Ridge National Laboratory is managed by UT-Battelle, LLC for the DOE under Contract Number DE-AC05–00OR22725 . This research used resources of the Compute and Data Environment for Science (CADES) and the Oak Ridge Leadership Computing Facility at the Oak Ridge National Laboratory . Publisher Copyright: {\textcopyright} 2022 The Authors",

year = "2022",

month = oct,

doi = "10.1016/j.jplph.2022.153791",

language = "English (US)",

volume = "277",

journal = "Journal of Plant Physiology",

issn = "0176-1617",

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T1 - Comparative genomics analysis of drought response between obligate CAM and C3 photosynthesis plants

AU - Hu, Rongbin

AU - Zhang, Jin

AU - Jawdy, Sara

AU - Sreedasyam, Avinash

AU - Lipzen, Anna

AU - Wang, Mei

AU - Ng, Vivian

AU - Daum, Christopher

AU - Keymanesh, Keykhosrow

AU - Liu, Degao

AU - Lu, Haiwei

AU - Ranjan, Priya

AU - Chen, Jin Gui

AU - Muchero, Wellington

AU - Tschaplinski, Timothy J.

AU - Tuskan, Gerald A.

AU - Schmutz, Jeremy

AU - Yang, Xiaohan

N1 - Funding Information: 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 Community Science Program (project 503025) at the Department of Energy Joint Genome Institute and the DOE Center for Bioenergy Innovation at the Oak Ridge National Laboratory. The writing of this manuscript was supported by the Center for Bioenergy Innovation, a U.S. Department of Energy (DOE) Bioenergy Research Center supported by the Biological and Environmental Research (BER) program. J.Z. is funded by the Zhejiang A&F University Research and Development Fund Talent Startup Project (2021LFR013).The work (proposal: 10.46936/10.25585/60001095) conducted by the U.S. Department of Energy Joint Genome Institute (https://ror.org/04xm1d337), a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy operated under Contract No. DE-AC02-05CH11231. This research is also supported by the U.S. Department of Energy (DOE), Office of Science, Genomic Science Program under Award Number DE-SC0008834, and the Center for Bioenergy Innovation (CBI), which is a DOE Bioenergy Research Center supported by the Biological and Environmental Research program in the DOE Office of Science. Oak Ridge National Laboratory is managed by UT-Battelle, LLC for the DOE under Contract Number DE-AC05–00OR22725. This research used resources of the Compute and Data Environment for Science (CADES) and the Oak Ridge Leadership Computing Facility at the Oak Ridge National Laboratory. Funding Information: 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 Community Science Program (project 503025 ) at the Department of Energy Joint Genome Institute and the DOE Center for Bioenergy Innovation at the Oak Ridge National Laboratory . The writing of this manuscript was supported by the Center for Bioenergy Innovation , a U.S. Department of Energy (DOE) Bioenergy Research Center supported by the Biological and Environmental Research (BER) program. J.Z. is funded by the Zhejiang A&F University Research and Development Fund Talent Startup Project ( 2021LFR013 ). Funding Information: The work (proposal: 10.46936/10.25585/60001095 ) conducted by the U.S. Department of Energy Joint Genome Institute ( https://ror.org/04xm1d337 ), a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy operated under Contract No. DE-AC02-05CH11231 . This research is also supported by the U.S. Department of Energy (DOE), Office of Science , Genomic Science Program under Award Number DE-SC0008834 , and the Center for Bioenergy Innovation (CBI) , which is a DOE Bioenergy Research Center supported by the Biological and Environmental Research program in the DOE Office of Science . Oak Ridge National Laboratory is managed by UT-Battelle, LLC for the DOE under Contract Number DE-AC05–00OR22725 . This research used resources of the Compute and Data Environment for Science (CADES) and the Oak Ridge Leadership Computing Facility at the Oak Ridge National Laboratory . Publisher Copyright: © 2022 The Authors

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N2 - Crassulacean acid metabolism (CAM) plants exhibit elevated drought and heat tolerance compared to C3 and C4 plants through an inverted pattern of day/night stomatal closure and opening for CO2 assimilation. However, the molecular responses to water-deficit conditions remain unclear in obligate CAM species. In this study, we presented genome-wide transcription sequencing analysis using leaf samples of an obligate CAM species Kalanchoë fedtschenkoi under moderate and severe drought treatments at two-time points of dawn (2-h before the start of light period) and dusk (2-h before the dark period). Differentially expressed genes were identified in response to environmental drought stress and a whole genome wide co-expression network was created as well. We found that the expression of CAM-related genes was not regulated by drought stimuli in K. fedtschenkoi. Our comparative analysis revealed that CAM species (K. fedtschenkoi) and C3 species (Arabidopsis thaliana, Populus deltoides ‘WV94’) share some common transcriptional changes in genes involved in multiple biological processes in response to drought stress, including ABA signaling and biosynthesis of secondary metabolites.

AB - Crassulacean acid metabolism (CAM) plants exhibit elevated drought and heat tolerance compared to C3 and C4 plants through an inverted pattern of day/night stomatal closure and opening for CO2 assimilation. However, the molecular responses to water-deficit conditions remain unclear in obligate CAM species. In this study, we presented genome-wide transcription sequencing analysis using leaf samples of an obligate CAM species Kalanchoë fedtschenkoi under moderate and severe drought treatments at two-time points of dawn (2-h before the start of light period) and dusk (2-h before the dark period). Differentially expressed genes were identified in response to environmental drought stress and a whole genome wide co-expression network was created as well. We found that the expression of CAM-related genes was not regulated by drought stimuli in K. fedtschenkoi. Our comparative analysis revealed that CAM species (K. fedtschenkoi) and C3 species (Arabidopsis thaliana, Populus deltoides ‘WV94’) share some common transcriptional changes in genes involved in multiple biological processes in response to drought stress, including ABA signaling and biosynthesis of secondary metabolites.

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KW - Drought stress

KW - Kalanchoë fedtschenkoi

KW - RNA-Seq

KW - Secondary metabolism

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