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

Jin Zhang, Rongbin Hu, Avinash Sreedasyam, Travis M. Garcia, Anna Lipzen, Mei Wang, Pradeep Yerramsetty, Degao Liu, Vivian Ng, Jeremy Schmutz, John C. Cushman, Anne M. Borland, Asher Pasha, Nicholas J. Provart, Jin Gui Chen, Wellington Muchero, Gerald A. Tuskan, Xiaohan Yang

Research output: Contribution to journalArticlepeer-review

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.

Original languageEnglish (US)
Article numbergiaa018
JournalGigaScience
Volume9
Issue number3
DOIs
StatePublished - Mar 12 2020
Externally publishedYes

Bibliographical note

Funding Information:
This research was supported by the U.S. Department of Energy, Office of Science, Genomic Science Program under Award No. 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. This manuscript has been authored by UT-Battelle, LLC, under Contract No. DEAC05- 00OR22725 with the U.S. Department of Energy. 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.

Funding Information:
This research was supported by the U.S. Department of Energy, Office of Science, Genomic Science Program under Award No. 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. This manuscript has been authored by UT-Battelle, LLC, under Contract No. DE-AC05-00OR22725 with the U.S. Department of Energy. 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 Compute and Data Environment for Science (CADES) and the Oak Ridge Leadership Computing Facility at the Oak Ridge National Laboratory.

Publisher Copyright:
© 2020 The Author(s) 2020.

Keywords

  • crassulacean acid metabolism
  • eFP browser
  • gene atlas
  • Kalanchoë fedtschenkoi
  • transcriptome

PubMed: MeSH publication types

  • Journal Article
  • Research Support, U.S. Gov't, Non-P.H.S.

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