Transcriptomic Analysis of the CAM Species <i>Kalanchoë fedtschenkoi</i> Under Low- and High-Temperature Regimes

Temperature stress is one of the major limiting environmental factors that negatively impact global crop yields. <i>Kalanchoë fedtschenkoi</i> is an obligate crassulacean acid metabolism (CAM) plant species, exhibiting much higher water-use efficiency and tolerance to drought and heat st...

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Main Authors: Rongbin Hu, Jin Zhang, Sara Jawdy, Avinash Sreedasyam, Anna Lipzen, Mei Wang, Vivian Ng, Christopher Daum, Keykhosrow Keymanesh, Degao Liu, Alex Hu, Jin-Gui Chen, Gerald A. Tuskan, Jeremy Schmutz, Xiaohan Yang
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Language:English
Published: MDPI AG 2024-12-01
Series:Plants
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Online Access:https://www.mdpi.com/2223-7747/13/23/3444
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author Rongbin Hu
Jin Zhang
Sara Jawdy
Avinash Sreedasyam
Anna Lipzen
Mei Wang
Vivian Ng
Christopher Daum
Keykhosrow Keymanesh
Degao Liu
Alex Hu
Jin-Gui Chen
Gerald A. Tuskan
Jeremy Schmutz
Xiaohan Yang
author_facet Rongbin Hu
Jin Zhang
Sara Jawdy
Avinash Sreedasyam
Anna Lipzen
Mei Wang
Vivian Ng
Christopher Daum
Keykhosrow Keymanesh
Degao Liu
Alex Hu
Jin-Gui Chen
Gerald A. Tuskan
Jeremy Schmutz
Xiaohan Yang
author_sort Rongbin Hu
collection DOAJ
description Temperature stress is one of the major limiting environmental factors that negatively impact global crop yields. <i>Kalanchoë fedtschenkoi</i> is an obligate crassulacean acid metabolism (CAM) plant species, exhibiting much higher water-use efficiency and tolerance to drought and heat stresses than C<sub>3</sub> or C<sub>4</sub> plant species. Previous studies on gene expression responses to low- or high-temperature stress have been focused on C<sub>3</sub> and C<sub>4</sub> plants. There is a lack of information about the regulation of gene expression by low and high temperatures in CAM plants. To address this knowledge gap, we performed transcriptome sequencing (RNA-Seq) of leaf and root tissues of <i>K. fedtschenkoi</i> under cold (8 °C), normal (25 °C), and heat (37 °C) conditions at dawn (i.e., 2 h before the light period) and dusk (i.e., 2 h before the dark period). Our analysis revealed differentially expressed genes (DEGs) under cold or heat treatment in comparison to normal conditions in leaf or root tissue at each of the two time points. In particular, DEGs exhibiting either the same or opposite direction of expression change (either up-regulated or down-regulated) under cold and heat treatments were identified. In addition, we analyzed gene co-expression modules regulated by cold or heat treatment, and we performed in-depth analyses of expression regulation by temperature stresses for selected gene categories, including CAM-related genes, genes encoding heat shock factors and heat shock proteins, circadian rhythm genes, and stomatal movement genes. Our study highlights both the common and distinct molecular strategies employed by CAM and C<sub>3</sub>/C<sub>4</sub> plants in adapting to extreme temperatures, providing new insights into the molecular mechanisms underlying temperature stress responses in CAM species.
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spelling doaj-art-2cee7cdd29f3495d98439aef2d0d13f72024-12-13T16:30:26ZengMDPI AGPlants2223-77472024-12-011323344410.3390/plants13233444Transcriptomic Analysis of the CAM Species <i>Kalanchoë fedtschenkoi</i> Under Low- and High-Temperature RegimesRongbin Hu0Jin Zhang1Sara Jawdy2Avinash Sreedasyam3Anna Lipzen4Mei Wang5Vivian Ng6Christopher Daum7Keykhosrow Keymanesh8Degao Liu9Alex Hu10Jin-Gui Chen11Gerald A. Tuskan12Jeremy Schmutz13Xiaohan Yang14Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831, USABiosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831, USABiosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831, USAHudsonAlpha Institute for Biotechnology, 601 Genome Way, Huntsville, AL 35801, USADepartment of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94589, USADepartment of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94589, USADepartment of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94589, USADepartment of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94589, USADepartment of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94589, USABiosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831, USADepartment of Chemical and Environmental Engineering, University of California-Riverside, Riverside, CA 92521, USABiosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831, USABiosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831, USAHudsonAlpha Institute for Biotechnology, 601 Genome Way, Huntsville, AL 35801, USABiosciences Division, Oak Ridge National Laboratory, Oak Ridge, TN 37831, USATemperature stress is one of the major limiting environmental factors that negatively impact global crop yields. <i>Kalanchoë fedtschenkoi</i> is an obligate crassulacean acid metabolism (CAM) plant species, exhibiting much higher water-use efficiency and tolerance to drought and heat stresses than C<sub>3</sub> or C<sub>4</sub> plant species. Previous studies on gene expression responses to low- or high-temperature stress have been focused on C<sub>3</sub> and C<sub>4</sub> plants. There is a lack of information about the regulation of gene expression by low and high temperatures in CAM plants. To address this knowledge gap, we performed transcriptome sequencing (RNA-Seq) of leaf and root tissues of <i>K. fedtschenkoi</i> under cold (8 °C), normal (25 °C), and heat (37 °C) conditions at dawn (i.e., 2 h before the light period) and dusk (i.e., 2 h before the dark period). Our analysis revealed differentially expressed genes (DEGs) under cold or heat treatment in comparison to normal conditions in leaf or root tissue at each of the two time points. In particular, DEGs exhibiting either the same or opposite direction of expression change (either up-regulated or down-regulated) under cold and heat treatments were identified. In addition, we analyzed gene co-expression modules regulated by cold or heat treatment, and we performed in-depth analyses of expression regulation by temperature stresses for selected gene categories, including CAM-related genes, genes encoding heat shock factors and heat shock proteins, circadian rhythm genes, and stomatal movement genes. Our study highlights both the common and distinct molecular strategies employed by CAM and C<sub>3</sub>/C<sub>4</sub> plants in adapting to extreme temperatures, providing new insights into the molecular mechanisms underlying temperature stress responses in CAM species.https://www.mdpi.com/2223-7747/13/23/3444crassulacean acid metabolismRNA-Seqgene regulationheat shock proteins
spellingShingle Rongbin Hu
Jin Zhang
Sara Jawdy
Avinash Sreedasyam
Anna Lipzen
Mei Wang
Vivian Ng
Christopher Daum
Keykhosrow Keymanesh
Degao Liu
Alex Hu
Jin-Gui Chen
Gerald A. Tuskan
Jeremy Schmutz
Xiaohan Yang
Transcriptomic Analysis of the CAM Species <i>Kalanchoë fedtschenkoi</i> Under Low- and High-Temperature Regimes
Plants
crassulacean acid metabolism
RNA-Seq
gene regulation
heat shock proteins
title Transcriptomic Analysis of the CAM Species <i>Kalanchoë fedtschenkoi</i> Under Low- and High-Temperature Regimes
title_full Transcriptomic Analysis of the CAM Species <i>Kalanchoë fedtschenkoi</i> Under Low- and High-Temperature Regimes
title_fullStr Transcriptomic Analysis of the CAM Species <i>Kalanchoë fedtschenkoi</i> Under Low- and High-Temperature Regimes
title_full_unstemmed Transcriptomic Analysis of the CAM Species <i>Kalanchoë fedtschenkoi</i> Under Low- and High-Temperature Regimes
title_short Transcriptomic Analysis of the CAM Species <i>Kalanchoë fedtschenkoi</i> Under Low- and High-Temperature Regimes
title_sort transcriptomic analysis of the cam species i kalanchoe fedtschenkoi i under low and high temperature regimes
topic crassulacean acid metabolism
RNA-Seq
gene regulation
heat shock proteins
url https://www.mdpi.com/2223-7747/13/23/3444
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