Long-term cold, freezing and drought: overlapping and specific regulatory mechanisms and signal transduction in tea plant (Camellia sinensis (L.) Kuntze)

IntroductionLow temperatures and drought are two main environmental constraints reducing the yield and geographical distribution of horticultural crops worldwide. Understanding the genetic crosstalk between stress responses has potential importance for crop improvement.MethodsIn this study, Illumina...

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Main Authors: Lidiia Samarina, Songbo Wang, Lyudmila Malyukova, Alexandr Bobrovskikh, Alexey Doroshkov, Natalia Koninskaya, Ruset Shkhalakhova, Alexandra Matskiv, Jaroslava Fedorina, Anastasia Fizikova, Karina Manakhova, Svetlana Loshkaryova, Tsiala Tutberidze, Alexey Ryndin, Elena Khlestkina
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-05-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2023.1145793/full
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author Lidiia Samarina
Lidiia Samarina
Songbo Wang
Lyudmila Malyukova
Alexandr Bobrovskikh
Alexey Doroshkov
Natalia Koninskaya
Ruset Shkhalakhova
Alexandra Matskiv
Jaroslava Fedorina
Jaroslava Fedorina
Anastasia Fizikova
Anastasia Fizikova
Karina Manakhova
Karina Manakhova
Svetlana Loshkaryova
Tsiala Tutberidze
Alexey Ryndin
Elena Khlestkina
Elena Khlestkina
author_facet Lidiia Samarina
Lidiia Samarina
Songbo Wang
Lyudmila Malyukova
Alexandr Bobrovskikh
Alexey Doroshkov
Natalia Koninskaya
Ruset Shkhalakhova
Alexandra Matskiv
Jaroslava Fedorina
Jaroslava Fedorina
Anastasia Fizikova
Anastasia Fizikova
Karina Manakhova
Karina Manakhova
Svetlana Loshkaryova
Tsiala Tutberidze
Alexey Ryndin
Elena Khlestkina
Elena Khlestkina
author_sort Lidiia Samarina
collection DOAJ
description IntroductionLow temperatures and drought are two main environmental constraints reducing the yield and geographical distribution of horticultural crops worldwide. Understanding the genetic crosstalk between stress responses has potential importance for crop improvement.MethodsIn this study, Illumina RNA-seq and Pac-Bio genome resequencing were used to annotate genes and analyze transcriptome dynamics in tea plants under long-term cold, freezing, and drought.ResultsThe highest number of differentially expressed genes (DEGs) was identified under long-term cold (7,896) and freezing (7,915), with 3,532 and 3,780 upregulated genes, respectively. The lowest number of DEGs was observed under 3-day drought (47) and 9-day drought (220), with five and 112 genes upregulated, respectively. The recovery after the cold had 6.5 times greater DEG numbers as compared to the drought recovery. Only 17.9% of cold-induced genes were upregulated by drought. In total, 1,492 transcription factor genes related to 57 families were identified. However, only 20 transcription factor genes were commonly upregulated by cold, freezing, and drought. Among the 232 common upregulated DEGs, most were related to signal transduction, cell wall remodeling, and lipid metabolism. Co-expression analysis and network reconstruction showed 19 genes with the highest co-expression connectivity: seven genes are related to cell wall remodeling (GATL7, UXS4, PRP-F1, 4CL, UEL-1, UDP-Arap, and TBL32), four genes are related to calcium-signaling (PXL1, Strap, CRT, and CIPK6), three genes are related to photo-perception (GIL1, CHUP1, and DnaJ11), two genes are related to hormone signaling (TTL3 and GID1C-like), two genes are involved in ROS signaling (ERO1 and CXE11), and one gene is related to the phenylpropanoid pathway (GALT6).DiscussionBased on our results, several important overlapping mechanisms of long-term stress responses include cell wall remodeling through lignin biosynthesis, o-acetylation of polysaccharides, pectin biosynthesis and branching, and xyloglucan and arabinogalactan biosynthesis. This study provides new insight into long-term stress responses in woody crops, and a set of new target candidate genes were identified for molecular breeding aimed at tolerance to abiotic stresses.
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spelling doaj.art-746751598c67486db2e6440c22ee8f642023-05-10T05:10:46ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-05-011410.3389/fpls.2023.11457931145793Long-term cold, freezing and drought: overlapping and specific regulatory mechanisms and signal transduction in tea plant (Camellia sinensis (L.) Kuntze)Lidiia Samarina0Lidiia Samarina1Songbo Wang2Lyudmila Malyukova3Alexandr Bobrovskikh4Alexey Doroshkov5Natalia Koninskaya6Ruset Shkhalakhova7Alexandra Matskiv8Jaroslava Fedorina9Jaroslava Fedorina10Anastasia Fizikova11Anastasia Fizikova12Karina Manakhova13Karina Manakhova14Svetlana Loshkaryova15Tsiala Tutberidze16Alexey Ryndin17Elena Khlestkina18Elena Khlestkina19Federal Research Centre the Subtropical Scientific Centre, Russian Academy of Sciences, Sochi, RussiaCenter of Genetics and Life Sciences, Sirius University of Science and Technology, Sirius, RussiaFederal Research Centre the Subtropical Scientific Centre, Russian Academy of Sciences, Sochi, RussiaFederal Research Centre the Subtropical Scientific Centre, Russian Academy of Sciences, Sochi, RussiaInstitute of Cytology and Genetics Siberian Branch, Russian Academy of Sciences, Novosibirsk, RussiaInstitute of Cytology and Genetics Siberian Branch, Russian Academy of Sciences, Novosibirsk, RussiaFederal Research Centre the Subtropical Scientific Centre, Russian Academy of Sciences, Sochi, RussiaFederal Research Centre the Subtropical Scientific Centre, Russian Academy of Sciences, Sochi, RussiaFederal Research Centre the Subtropical Scientific Centre, Russian Academy of Sciences, Sochi, RussiaFederal Research Centre the Subtropical Scientific Centre, Russian Academy of Sciences, Sochi, RussiaCenter of Genetics and Life Sciences, Sirius University of Science and Technology, Sirius, RussiaFederal Research Centre the Subtropical Scientific Centre, Russian Academy of Sciences, Sochi, RussiaCenter of Genetics and Life Sciences, Sirius University of Science and Technology, Sirius, RussiaFederal Research Centre the Subtropical Scientific Centre, Russian Academy of Sciences, Sochi, RussiaCenter of Genetics and Life Sciences, Sirius University of Science and Technology, Sirius, RussiaFederal Research Centre the Subtropical Scientific Centre, Russian Academy of Sciences, Sochi, RussiaFederal Research Centre the Subtropical Scientific Centre, Russian Academy of Sciences, Sochi, RussiaFederal Research Centre the Subtropical Scientific Centre, Russian Academy of Sciences, Sochi, RussiaCenter of Genetics and Life Sciences, Sirius University of Science and Technology, Sirius, RussiaFederal Research Center, N. I. Vavilov All-Russian Institute of Plant Genetic Resources (VIR), Saint Petersburg, RussiaIntroductionLow temperatures and drought are two main environmental constraints reducing the yield and geographical distribution of horticultural crops worldwide. Understanding the genetic crosstalk between stress responses has potential importance for crop improvement.MethodsIn this study, Illumina RNA-seq and Pac-Bio genome resequencing were used to annotate genes and analyze transcriptome dynamics in tea plants under long-term cold, freezing, and drought.ResultsThe highest number of differentially expressed genes (DEGs) was identified under long-term cold (7,896) and freezing (7,915), with 3,532 and 3,780 upregulated genes, respectively. The lowest number of DEGs was observed under 3-day drought (47) and 9-day drought (220), with five and 112 genes upregulated, respectively. The recovery after the cold had 6.5 times greater DEG numbers as compared to the drought recovery. Only 17.9% of cold-induced genes were upregulated by drought. In total, 1,492 transcription factor genes related to 57 families were identified. However, only 20 transcription factor genes were commonly upregulated by cold, freezing, and drought. Among the 232 common upregulated DEGs, most were related to signal transduction, cell wall remodeling, and lipid metabolism. Co-expression analysis and network reconstruction showed 19 genes with the highest co-expression connectivity: seven genes are related to cell wall remodeling (GATL7, UXS4, PRP-F1, 4CL, UEL-1, UDP-Arap, and TBL32), four genes are related to calcium-signaling (PXL1, Strap, CRT, and CIPK6), three genes are related to photo-perception (GIL1, CHUP1, and DnaJ11), two genes are related to hormone signaling (TTL3 and GID1C-like), two genes are involved in ROS signaling (ERO1 and CXE11), and one gene is related to the phenylpropanoid pathway (GALT6).DiscussionBased on our results, several important overlapping mechanisms of long-term stress responses include cell wall remodeling through lignin biosynthesis, o-acetylation of polysaccharides, pectin biosynthesis and branching, and xyloglucan and arabinogalactan biosynthesis. This study provides new insight into long-term stress responses in woody crops, and a set of new target candidate genes were identified for molecular breeding aimed at tolerance to abiotic stresses.https://www.frontiersin.org/articles/10.3389/fpls.2023.1145793/fulltea plant (Camellia sinensis)stress tolerancecell wall biosynthesislipid metabolismlight perceptionphenilpropanoid pathway
spellingShingle Lidiia Samarina
Lidiia Samarina
Songbo Wang
Lyudmila Malyukova
Alexandr Bobrovskikh
Alexey Doroshkov
Natalia Koninskaya
Ruset Shkhalakhova
Alexandra Matskiv
Jaroslava Fedorina
Jaroslava Fedorina
Anastasia Fizikova
Anastasia Fizikova
Karina Manakhova
Karina Manakhova
Svetlana Loshkaryova
Tsiala Tutberidze
Alexey Ryndin
Elena Khlestkina
Elena Khlestkina
Long-term cold, freezing and drought: overlapping and specific regulatory mechanisms and signal transduction in tea plant (Camellia sinensis (L.) Kuntze)
Frontiers in Plant Science
tea plant (Camellia sinensis)
stress tolerance
cell wall biosynthesis
lipid metabolism
light perception
phenilpropanoid pathway
title Long-term cold, freezing and drought: overlapping and specific regulatory mechanisms and signal transduction in tea plant (Camellia sinensis (L.) Kuntze)
title_full Long-term cold, freezing and drought: overlapping and specific regulatory mechanisms and signal transduction in tea plant (Camellia sinensis (L.) Kuntze)
title_fullStr Long-term cold, freezing and drought: overlapping and specific regulatory mechanisms and signal transduction in tea plant (Camellia sinensis (L.) Kuntze)
title_full_unstemmed Long-term cold, freezing and drought: overlapping and specific regulatory mechanisms and signal transduction in tea plant (Camellia sinensis (L.) Kuntze)
title_short Long-term cold, freezing and drought: overlapping and specific regulatory mechanisms and signal transduction in tea plant (Camellia sinensis (L.) Kuntze)
title_sort long term cold freezing and drought overlapping and specific regulatory mechanisms and signal transduction in tea plant camellia sinensis l kuntze
topic tea plant (Camellia sinensis)
stress tolerance
cell wall biosynthesis
lipid metabolism
light perception
phenilpropanoid pathway
url https://www.frontiersin.org/articles/10.3389/fpls.2023.1145793/full
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