Integrated small RNA, transcriptome and physiological approaches provide insight into Taxodium hybrid ‘Zhongshanshan’ roots in acclimation to prolonged flooding (2024)

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Yan Lu

Jiangsu Key Laboratory for the Research and Utilization of Plant Resources

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Institute of Botany, Jiangsu Province and Chinese Academy of Sciences

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No. 1 Qianhu Houcun, Zhongshanmen Wai, Nanjing 210014

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China

Nanjing Botanical Garden Mem. Sun Yat-Sen

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No. 1 Qianhu Houcun, Zhongshanmen Wai, Nanjing 210014

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China

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Shuqing Zhang

Jiangsu Key Laboratory for the Research and Utilization of Plant Resources

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Institute of Botany, Jiangsu Province and Chinese Academy of Sciences

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No. 1 Qianhu Houcun, Zhongshanmen Wai, Nanjing 210014

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China

Nanjing Botanical Garden Mem. Sun Yat-Sen

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No. 1 Qianhu Houcun, Zhongshanmen Wai, Nanjing 210014

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China

Co-Innovation Center for the Sustainable Forestry in Southern China

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Nanjing Forestry University

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159 Longpan Road, Nanjing 210037

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China

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Peng Xiang

Jiangsu Key Laboratory for the Research and Utilization of Plant Resources

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Institute of Botany, Jiangsu Province and Chinese Academy of Sciences

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No. 1 Qianhu Houcun, Zhongshanmen Wai, Nanjing 210014

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China

Nanjing Botanical Garden Mem. Sun Yat-Sen

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No. 1 Qianhu Houcun, Zhongshanmen Wai, Nanjing 210014

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China

Co-Innovation Center for the Sustainable Forestry in Southern China

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Nanjing Forestry University

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159 Longpan Road, Nanjing 210037

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China

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Yunlong Yin

Jiangsu Key Laboratory for the Research and Utilization of Plant Resources

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Institute of Botany, Jiangsu Province and Chinese Academy of Sciences

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No. 1 Qianhu Houcun, Zhongshanmen Wai, Nanjing 210014

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China

Nanjing Botanical Garden Mem. Sun Yat-Sen

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China

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Chaoguang Yu

Jiangsu Key Laboratory for the Research and Utilization of Plant Resources

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Institute of Botany, Jiangsu Province and Chinese Academy of Sciences

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No. 1 Qianhu Houcun, Zhongshanmen Wai, Nanjing 210014

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China

Nanjing Botanical Garden Mem. Sun Yat-Sen

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China

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Jianfeng Hua

Jiangsu Key Laboratory for the Research and Utilization of Plant Resources

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Institute of Botany, Jiangsu Province and Chinese Academy of Sciences

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No. 1 Qianhu Houcun, Zhongshanmen Wai, Nanjing 210014

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China

Nanjing Botanical Garden Mem. Sun Yat-Sen

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No. 1 Qianhu Houcun, Zhongshanmen Wai, Nanjing 210014

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China

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Qin Shi

Jiangsu Key Laboratory for the Research and Utilization of Plant Resources

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Institute of Botany, Jiangsu Province and Chinese Academy of Sciences

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No. 1 Qianhu Houcun, Zhongshanmen Wai, Nanjing 210014

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China

Nanjing Botanical Garden Mem. Sun Yat-Sen

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No. 1 Qianhu Houcun, Zhongshanmen Wai, Nanjing 210014

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China

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Tingting Chen

Jiangsu Key Laboratory for the Research and Utilization of Plant Resources

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Institute of Botany, Jiangsu Province and Chinese Academy of Sciences

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No. 1 Qianhu Houcun, Zhongshanmen Wai, Nanjing 210014

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China

Nanjing Botanical Garden Mem. Sun Yat-Sen

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No. 1 Qianhu Houcun, Zhongshanmen Wai, Nanjing 210014

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China

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Zhidong Zhou

Jiangsu Key Laboratory for the Research and Utilization of Plant Resources

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Institute of Botany, Jiangsu Province and Chinese Academy of Sciences

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No. 1 Qianhu Houcun, Zhongshanmen Wai, Nanjing 210014

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China

Nanjing Botanical Garden Mem. Sun Yat-Sen

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No. 1 Qianhu Houcun, Zhongshanmen Wai, Nanjing 210014

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China

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Wanwen Yu

Co-Innovation Center for the Sustainable Forestry in Southern China

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Nanjing Forestry University

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159 Longpan Road, Nanjing 210037

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China

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David L Creech

Department of Agriculture

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Arthur Temple College of Forestry and Agriculture, Stephen F. Austin State University

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1936 North St, Nacogdoches, TX 75962-3000

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USA

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Zhiguo Lu

Jiangsu Key Laboratory for the Research and Utilization of Plant Resources

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Institute of Botany, Jiangsu Province and Chinese Academy of Sciences

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No. 1 Qianhu Houcun, Zhongshanmen Wai, Nanjing 210014

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China

Nanjing Botanical Garden Mem. Sun Yat-Sen

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No. 1 Qianhu Houcun, Zhongshanmen Wai, Nanjing 210014

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China

Corresponding author (lzgjs@cnbg.net)

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Tree Physiology, Volume 44, Issue 4, April 2024, tpae031, https://doi.org/10.1093/treephys/tpae031

Published:

18 March 2024

Article history

Received:

14 February 2023

Accepted:

13 March 2024

Published:

18 March 2024

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    Yan Lu, Shuqing Zhang, Peng Xiang, Yunlong Yin, Chaoguang Yu, Jianfeng Hua, Qin Shi, Tingting Chen, Zhidong Zhou, Wanwen Yu, David L Creech, Zhiguo Lu, Integrated small RNA, transcriptome and physiological approaches provide insight into Taxodium hybrid ‘Zhongshanshan’ roots in acclimation to prolonged flooding, Tree Physiology, Volume 44, Issue 4, April 2024, tpae031, https://doi.org/10.1093/treephys/tpae031

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Abstract

Although Taxodium hybrid ‘Zhongshanshan’ 406 (Taxodium mucronatum Tenore×Taxodium distichum; Taxodium 406) is an extremely flooding-tolerant woody plant, the physiological and molecular mechanisms underlying acclimation of its roots to long-term flooding remain largely unknown. Thus, we exposed saplings of Taxodium 406 to either non-flooding (control) or flooding for 2months. Flooding resulted in reduced root biomass, which is in line with lower concentrations of citrate, α-ketoglutaric acid, fumaric acid, malic acid and adenosine triphosphate (ATP) in Taxodium 406 roots. Flooding led to elevated activities of pyruvate decarboxylase, alcohol dehydrogenase and lactate dehydrogenase, which is consistent with higher lactate concentration in the roots of Taxodium 406. Flooding brought about stimulated activities of superoxide dismutase and catalase and elevated reduced glutathione (GSH) concentration and GSH/oxidized glutathione, which is in agreement with reduced concentrations of O2 and H2O2 in Taxodium 406 roots. The levels of starch, soluble protein, indole-3-acetic acid, gibberellin A4 and jasmonate were decreased, whereas the concentrations of glucose, total non-structural carbohydrates, most amino acids and 1-aminocyclopropane-1-carboxylate (ACC) were improved in the roots of flooding-treated Taxodium 406. Underlying these changes in growth and physiological characteristics, 12,420 mRNAs and 42 miRNAs were significantly differentially expressed, and 886 miRNA–mRNA pairs were identified in the roots of flooding-exposed Taxodium 406. For instance, 1-aminocyclopropane-1-carboxylate synthase 8 (ACS8) was a target of Th-miR162-3p and 1-aminocyclopropane-1-carboxylate oxidase 4 (ACO4) was a target of Th-miR166i, and the downregulation of Th-miR162-3p and Th-miR166i results in the upregulation of ACS8 and ACO4, probably bringing about higher ACC content in flooding-treated roots. Overall, these results indicate that differentially expressed mRNA and miRNAs are involved in regulating tricarboxylic acid cycle, ATP production, fermentation, and metabolism of carbohydrates, amino acids and phytohormones, as well as reactive oxygen species detoxification of Taxodium 406 roots. These processes play pivotal roles in acclimation to flooding stress. These results will improve our understanding of the molecular and physiological bases underlying woody plant flooding acclimation and provide valuable insights into breeding-flooding tolerant trees.

© The Author(s) 2024. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permission@oup.com.

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Janice Cooke

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