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Title: Light-responsive expression atlas reveals the effects of light quality and intensity in Kalanchoë fedtschenkoi, a plant with crassulacean acid metabolism

Abstract

Abstract Background Crassulacean acid metabolism (CAM), a specialized mode of photosynthesis, enables plant adaptation to water-limited environments and improves photosynthetic efficiency via an inorganic carbon-concentrating mechanism. Kalanchoë fedtschenkoi is an obligate CAM model featuring a relatively small genome and easy stable transformation. However, the molecular responses to light quality and intensity in CAM plants remain understudied. Results Here we present a genome-wide expression atlas of K. fedtschenkoi plants grown under 12 h/12 h photoperiod with different light quality (blue, red, far-red, white light) and intensity (0, 150, 440, and 1,000 μmol m–2 s–1) based on RNA sequencing performed for mature leaf samples collected at dawn (2 h before the light period) and dusk (2 h before the dark period). An eFP web browser was created for easy access of the gene expression data. Based on the expression atlas, we constructed a light-responsive co-expression network to reveal the potential regulatory relationships in K. fedtschenkoi. Measurements of leaf titratable acidity, soluble sugar, and starch turnover provided metabolic indicators of the magnitude of CAM under the different light treatments and were used to provide biological context for the expression dataset. Furthermore, CAM-related subnetworks were highlighted to showcase genes relevant to CAM pathway, circadian clock, andmore » stomatal movement. In comparison with white light, monochrome blue/red/far-red light treatments repressed the expression of several CAM-related genes at dusk, along with a major reduction in acid accumulation. Increasing light intensity from an intermediate level (440 μmol m−2 s−1) of white light to a high light treatment (1,000 μmol m–2 s–1) increased expression of several genes involved in dark CO2 fixation and malate transport at dawn, along with an increase in organic acid accumulation. Conclusions This study provides a useful genomics resource for investigating the molecular mechanism underlying the light regulation of physiology and metabolism in CAM plants. Our results support the hypothesis that both light intensity and light quality can modulate the CAM pathway through regulation of CAM-related genes in K. fedtschenkoi.« less

Authors:
ORCiD logo [1];  [2];  [3];  [4];  [5];  [5];  [4];  [2];  [5];  [6];  [4];  [7];  [8];  [8];  [1];  [1];  [1]; ORCiD logo [1]
  1. Biosciences Division, Oak Ridge National Laboratory, 1 Bethel Valley Rd, Oak Ridge, TN 37831, USA, The Center for Bioenergy Innovation, Oak Ridge National Laboratory, 1 Bethel Valley Rd, Oak Ridge, TN 37831, USA
  2. Biosciences Division, Oak Ridge National Laboratory, 1 Bethel Valley Rd, Oak Ridge, TN 37831, USA
  3. HudsonAlpha Institute for Biotechnology, 601 Genome Way, Huntsville, AL 35801, USA
  4. Department of Biochemistry and Molecular Biology, University of Nevada, 1664 N. Virginia St, Reno, NV 89557, USA
  5. US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, 1 Cyclotron Road, Berkeley, CA 94720, USA
  6. HudsonAlpha Institute for Biotechnology, 601 Genome Way, Huntsville, AL 35801, USA, US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, 1 Cyclotron Road, Berkeley, CA 94720, USA
  7. Biosciences Division, Oak Ridge National Laboratory, 1 Bethel Valley Rd, Oak Ridge, TN 37831, USA, School of Natural and Environmental Science, Newcastle University, Newcastle upon Tyne NE1 7RU, UK
  8. Department of Cell and Systems Biology, Centre for the Analysis of Genome Evolution and Function, University of Toronto, 25 Willcocks St #4038, Toronto, ON M5S 3B2, Canada
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1603213
Grant/Contract Number:  
[SC0008834; 503025]
Resource Type:
Published Article
Journal Name:
GigaScience
Additional Journal Information:
[Journal Name: GigaScience Journal Volume: 9 Journal Issue: 3]; Journal ID: ISSN 2047-217X
Publisher:
Oxford University Press
Country of Publication:
United Kingdom
Language:
English

Citation Formats

Zhang, Jin, Hu, Rongbin, Sreedasyam, Avinash, Garcia, Travis M., Lipzen, Anna, Wang, Mei, Yerramsetty, Pradeep, Liu, Degao, Ng, Vivian, Schmutz, Jeremy, Cushman, John C., Borland, Anne M., Pasha, Asher, Provart, Nicholas J., Chen, Jin-Gui, Muchero, Wellington, Tuskan, Gerald A., and Yang, Xiaohan. Light-responsive expression atlas reveals the effects of light quality and intensity in Kalanchoë fedtschenkoi, a plant with crassulacean acid metabolism. United Kingdom: N. p., 2020. Web. doi:10.1093/gigascience/giaa018.
Zhang, Jin, Hu, Rongbin, Sreedasyam, Avinash, Garcia, Travis M., Lipzen, Anna, Wang, Mei, Yerramsetty, Pradeep, Liu, Degao, Ng, Vivian, Schmutz, Jeremy, Cushman, John C., Borland, Anne M., Pasha, Asher, Provart, Nicholas J., Chen, Jin-Gui, Muchero, Wellington, Tuskan, Gerald A., & Yang, Xiaohan. Light-responsive expression atlas reveals the effects of light quality and intensity in Kalanchoë fedtschenkoi, a plant with crassulacean acid metabolism. United Kingdom. doi:10.1093/gigascience/giaa018.
Zhang, Jin, Hu, Rongbin, Sreedasyam, Avinash, Garcia, Travis M., Lipzen, Anna, Wang, Mei, Yerramsetty, Pradeep, Liu, Degao, Ng, Vivian, Schmutz, Jeremy, Cushman, John C., Borland, Anne M., Pasha, Asher, Provart, Nicholas J., Chen, Jin-Gui, Muchero, Wellington, Tuskan, Gerald A., and Yang, Xiaohan. Thu . "Light-responsive expression atlas reveals the effects of light quality and intensity in Kalanchoë fedtschenkoi, a plant with crassulacean acid metabolism". United Kingdom. doi:10.1093/gigascience/giaa018.
@article{osti_1603213,
title = {Light-responsive expression atlas reveals the effects of light quality and intensity in Kalanchoë fedtschenkoi, a plant with crassulacean acid metabolism},
author = {Zhang, Jin and Hu, Rongbin and Sreedasyam, Avinash and Garcia, Travis M. and Lipzen, Anna and Wang, Mei and Yerramsetty, Pradeep and Liu, Degao and Ng, Vivian and Schmutz, Jeremy and Cushman, John C. and Borland, Anne M. and Pasha, Asher and Provart, Nicholas J. and Chen, Jin-Gui and Muchero, Wellington and Tuskan, Gerald A. and Yang, Xiaohan},
abstractNote = {Abstract Background Crassulacean acid metabolism (CAM), a specialized mode of photosynthesis, enables plant adaptation to water-limited environments and improves photosynthetic efficiency via an inorganic carbon-concentrating mechanism. Kalanchoë fedtschenkoi is an obligate CAM model featuring a relatively small genome and easy stable transformation. However, the molecular responses to light quality and intensity in CAM plants remain understudied. Results Here we present a genome-wide expression atlas of K. fedtschenkoi plants grown under 12 h/12 h photoperiod with different light quality (blue, red, far-red, white light) and intensity (0, 150, 440, and 1,000 μmol m–2 s–1) based on RNA sequencing performed for mature leaf samples collected at dawn (2 h before the light period) and dusk (2 h before the dark period). An eFP web browser was created for easy access of the gene expression data. Based on the expression atlas, we constructed a light-responsive co-expression network to reveal the potential regulatory relationships in K. fedtschenkoi. Measurements of leaf titratable acidity, soluble sugar, and starch turnover provided metabolic indicators of the magnitude of CAM under the different light treatments and were used to provide biological context for the expression dataset. Furthermore, CAM-related subnetworks were highlighted to showcase genes relevant to CAM pathway, circadian clock, and stomatal movement. In comparison with white light, monochrome blue/red/far-red light treatments repressed the expression of several CAM-related genes at dusk, along with a major reduction in acid accumulation. Increasing light intensity from an intermediate level (440 μmol m−2 s−1) of white light to a high light treatment (1,000 μmol m–2 s–1) increased expression of several genes involved in dark CO2 fixation and malate transport at dawn, along with an increase in organic acid accumulation. Conclusions This study provides a useful genomics resource for investigating the molecular mechanism underlying the light regulation of physiology and metabolism in CAM plants. Our results support the hypothesis that both light intensity and light quality can modulate the CAM pathway through regulation of CAM-related genes in K. fedtschenkoi.},
doi = {10.1093/gigascience/giaa018},
journal = {GigaScience},
number = [3],
volume = [9],
place = {United Kingdom},
year = {2020},
month = {3}
}

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DOI: 10.1093/gigascience/giaa018

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