Integrated Physiological, Transcriptomic, and Metabolomic Analysis Reveals Mechanism Underlying the <i>Serendipita indica</i>-Enhanced Drought Tolerance in Tea Plants

Drought stress significantly impairs the output of tea plants and the quality of tea products. Although <i>Serendipita indica</i> has demonstrated the ability to enhance drought tolerance in host plants, its impact on tea plants (<i>Camellia sinensis</i>) experiencing drought...

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Main Authors: Gaojian Shen, Hongli Cao, Qin Zeng, Xiaoyu Guo, Huixin Shao, Huiyi Wang, Liyong Luo, Chuan Yue, Liang Zeng
Format: Article
Language:English
Published: MDPI AG 2025-03-01
Series:Plants
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Online Access:https://www.mdpi.com/2223-7747/14/7/989
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author Gaojian Shen
Hongli Cao
Qin Zeng
Xiaoyu Guo
Huixin Shao
Huiyi Wang
Liyong Luo
Chuan Yue
Liang Zeng
author_facet Gaojian Shen
Hongli Cao
Qin Zeng
Xiaoyu Guo
Huixin Shao
Huiyi Wang
Liyong Luo
Chuan Yue
Liang Zeng
author_sort Gaojian Shen
collection DOAJ
description Drought stress significantly impairs the output of tea plants and the quality of tea products. Although <i>Serendipita indica</i> has demonstrated the ability to enhance drought tolerance in host plants, its impact on tea plants (<i>Camellia sinensis</i>) experiencing drought stress is unknown. This study assessed the response of tea plants by inoculating <i>S. indica</i> under drought conditions. Phenotypic and physiological analyses demonstrated that <i>S. indica</i> mitigated drought damage in tea plants by regulating osmotic equilibrium and antioxidant enzyme activity. Metabolome analysis showed that <i>S. indica</i> promoted the accumulation of flavonoid metabolites, including naringin, (-)-epiafzelechin, naringenin chalcone, and dihydromyricetin, while inhibiting the content of amino acids and derivatives, such as homoarginine, L-arginine, N6-acetyl-L-lysine, and N-palmitoylglycine, during water deficit. The expression patterns of <i>S. indica</i>-stimulated genes were investigated using transcriptome analysis. <i>S. indica</i>-induced drought-responsive genes involved in osmotic regulation, antioxidant protection, transcription factors, and signaling were identified and recognized as possibly significant in <i>S. indica</i>-mediated drought tolerance in tea plants. Particularly, the flavonoid biosynthesis pathway was identified from the metabolomic and transcriptomic analysis using Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analysis. Moreover, flavonoid biosynthesis-related genes were identified. <i>S. indica</i>-inoculation significantly upregulated the expression of <i>cinnamate 4-hydroxylase</i> (<i>C4H</i>), <i>chalcone synthase</i> (<i>CHS</i>), <i>flavanone 3-hydroxylase</i> (<i>F3H</i>), <i>dihydroflavonol 4-reductase</i> (<i>DFR</i>), <i>anthocyanidin reductase</i> (<i>ANR</i>), and <i>leucoanthocyanidin reductase</i> (<i>LAR</i>) genes compared to uninoculated plants subjected to water stress. Consequently, we concluded that <i>S. indica</i> inoculation primarily alleviates drought stress in tea plants by modulating the flavonoid biosynthesis pathway. These results will provide insights into the mechanisms of <i>S. indica</i>-enhanced drought tolerance in tea plants and establish a solid foundation for its application as a microbial agent in the management of drought in tea plants cultivation.
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spelling doaj-art-d84a1fe04d044ab0affb58eb4891caf02025-08-20T03:08:55ZengMDPI AGPlants2223-77472025-03-0114798910.3390/plants14070989Integrated Physiological, Transcriptomic, and Metabolomic Analysis Reveals Mechanism Underlying the <i>Serendipita indica</i>-Enhanced Drought Tolerance in Tea PlantsGaojian Shen0Hongli Cao1Qin Zeng2Xiaoyu Guo3Huixin Shao4Huiyi Wang5Liyong Luo6Chuan Yue7Liang Zeng8Integrative Science Center of Germplasm Creation in Western China (CHONGQING) Science City, College of Food Science, Southwest University, Chongqing 400715, ChinaIntegrative Science Center of Germplasm Creation in Western China (CHONGQING) Science City, College of Food Science, Southwest University, Chongqing 400715, ChinaIntegrative Science Center of Germplasm Creation in Western China (CHONGQING) Science City, College of Food Science, Southwest University, Chongqing 400715, ChinaIntegrative Science Center of Germplasm Creation in Western China (CHONGQING) Science City, College of Food Science, Southwest University, Chongqing 400715, ChinaIntegrative Science Center of Germplasm Creation in Western China (CHONGQING) Science City, College of Food Science, Southwest University, Chongqing 400715, ChinaIntegrative Science Center of Germplasm Creation in Western China (CHONGQING) Science City, College of Food Science, Southwest University, Chongqing 400715, ChinaIntegrative Science Center of Germplasm Creation in Western China (CHONGQING) Science City, College of Food Science, Southwest University, Chongqing 400715, ChinaIntegrative Science Center of Germplasm Creation in Western China (CHONGQING) Science City, College of Food Science, Southwest University, Chongqing 400715, ChinaIntegrative Science Center of Germplasm Creation in Western China (CHONGQING) Science City, College of Food Science, Southwest University, Chongqing 400715, ChinaDrought stress significantly impairs the output of tea plants and the quality of tea products. Although <i>Serendipita indica</i> has demonstrated the ability to enhance drought tolerance in host plants, its impact on tea plants (<i>Camellia sinensis</i>) experiencing drought stress is unknown. This study assessed the response of tea plants by inoculating <i>S. indica</i> under drought conditions. Phenotypic and physiological analyses demonstrated that <i>S. indica</i> mitigated drought damage in tea plants by regulating osmotic equilibrium and antioxidant enzyme activity. Metabolome analysis showed that <i>S. indica</i> promoted the accumulation of flavonoid metabolites, including naringin, (-)-epiafzelechin, naringenin chalcone, and dihydromyricetin, while inhibiting the content of amino acids and derivatives, such as homoarginine, L-arginine, N6-acetyl-L-lysine, and N-palmitoylglycine, during water deficit. The expression patterns of <i>S. indica</i>-stimulated genes were investigated using transcriptome analysis. <i>S. indica</i>-induced drought-responsive genes involved in osmotic regulation, antioxidant protection, transcription factors, and signaling were identified and recognized as possibly significant in <i>S. indica</i>-mediated drought tolerance in tea plants. Particularly, the flavonoid biosynthesis pathway was identified from the metabolomic and transcriptomic analysis using Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analysis. Moreover, flavonoid biosynthesis-related genes were identified. <i>S. indica</i>-inoculation significantly upregulated the expression of <i>cinnamate 4-hydroxylase</i> (<i>C4H</i>), <i>chalcone synthase</i> (<i>CHS</i>), <i>flavanone 3-hydroxylase</i> (<i>F3H</i>), <i>dihydroflavonol 4-reductase</i> (<i>DFR</i>), <i>anthocyanidin reductase</i> (<i>ANR</i>), and <i>leucoanthocyanidin reductase</i> (<i>LAR</i>) genes compared to uninoculated plants subjected to water stress. Consequently, we concluded that <i>S. indica</i> inoculation primarily alleviates drought stress in tea plants by modulating the flavonoid biosynthesis pathway. These results will provide insights into the mechanisms of <i>S. indica</i>-enhanced drought tolerance in tea plants and establish a solid foundation for its application as a microbial agent in the management of drought in tea plants cultivation.https://www.mdpi.com/2223-7747/14/7/989<i>Camellia sinensis</i><i>Serendipita indica</i>drought stresstranscriptomemetabolome
spellingShingle Gaojian Shen
Hongli Cao
Qin Zeng
Xiaoyu Guo
Huixin Shao
Huiyi Wang
Liyong Luo
Chuan Yue
Liang Zeng
Integrated Physiological, Transcriptomic, and Metabolomic Analysis Reveals Mechanism Underlying the <i>Serendipita indica</i>-Enhanced Drought Tolerance in Tea Plants
Plants
<i>Camellia sinensis</i>
<i>Serendipita indica</i>
drought stress
transcriptome
metabolome
title Integrated Physiological, Transcriptomic, and Metabolomic Analysis Reveals Mechanism Underlying the <i>Serendipita indica</i>-Enhanced Drought Tolerance in Tea Plants
title_full Integrated Physiological, Transcriptomic, and Metabolomic Analysis Reveals Mechanism Underlying the <i>Serendipita indica</i>-Enhanced Drought Tolerance in Tea Plants
title_fullStr Integrated Physiological, Transcriptomic, and Metabolomic Analysis Reveals Mechanism Underlying the <i>Serendipita indica</i>-Enhanced Drought Tolerance in Tea Plants
title_full_unstemmed Integrated Physiological, Transcriptomic, and Metabolomic Analysis Reveals Mechanism Underlying the <i>Serendipita indica</i>-Enhanced Drought Tolerance in Tea Plants
title_short Integrated Physiological, Transcriptomic, and Metabolomic Analysis Reveals Mechanism Underlying the <i>Serendipita indica</i>-Enhanced Drought Tolerance in Tea Plants
title_sort integrated physiological transcriptomic and metabolomic analysis reveals mechanism underlying the i serendipita indica i enhanced drought tolerance in tea plants
topic <i>Camellia sinensis</i>
<i>Serendipita indica</i>
drought stress
transcriptome
metabolome
url https://www.mdpi.com/2223-7747/14/7/989
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