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Journal of Integrative Agriculture  2025, Vol. 24 Issue (11): 4282-4293    DOI: 10.1016/j.jia.2025.06.001
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Unlocking Dendrobium officinale’s drought resistance: Insights from transcriptomic analysis and enhanced drought tolerance in tomato

Lulu Yu1, 2, Muhammad Ahsan Asghar3, Antonios Petridis3, Fei Xu1, 2#

Center of Applied Biotechnology, Wuhan University of Bioengineering, Wuhan 430415, China

School of Life Sciences, Yangtze University, Jingzhou 434025, China

Department of Food Science, Aarhus University, Aarhus 8210, Denmark

 Highlights 
Dendrobium officinale demonstrated survival through 6 months of water deficit and exhibited rapid growth recovery within 2 d after rehydration.
Drought tolerance mechanisms in D. officinale encompass stress responses, photosynthesis, phytohormone signaling, and metabolism, providing valuable insights for crop breeding.
Tomato plants overexpressing D. officinale genes PEROXIDASE 4 (POD4) and NAC37 exhibited enhanced drought tolerance.
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摘要  

铁皮石斛是一种兰科植物,耐干旱的能力强。铁皮石斛表现出的高耐旱性可以归因于其结构和成分特征,包括富含多糖和其他胶体物质的厚叶和茎。尽管如此,其有助于提高铁皮石斛耐旱性的分子机制还不清楚。在本研究中,我们让铁皮石斛缺水一到六个月,并进行生理和RNA测序分析,以确定它如何应对长期缺水以及哪些基因可以保护抵御干旱。研究发现,缺水六个月后,铁皮石斛仍然具有活力,这可从它仅补水两天后就快速复苏中看出。对经过一个月水处理的铁皮石斛植株进行转录组分析发现,参与诸多程的基因表达发生了变化,其中最突出的是应激反应、光合作用、植物激素信号传导、碳代谢和果糖/甘露糖途径等。在这些差异表达基因中,过氧化物酶4POD4NAC37被显著上调,因此我们选择这两个基因来进一步研究增强植物耐旱性中的作用。值得注意的是,过表达铁皮石斛POD4NAC37基因的转基因番茄植株比对照植株更耐旱,表现为活力更强、结实率更高,并维持更高的呼吸速率和叶绿素水平,以及较低氧化损伤等。这些研究证明探索未充分利用的物种以挖掘抗旱相关基因具有重要价值,并确定了POD4NAC37作为提升植物抗旱性的潜在候选基因



Abstract  

Dendrobium officinale is an orchid herb distinguished by its exceptional drought resistance capabilities.  The remarkable drought tolerance of Dofficinale stems from its structural and compositional features, including thick leaves and stems containing abundant polysaccharides and colloidal substances.  Despite these adaptations, the underlying molecular mechanisms responsible for enhanced drought tolerance remain inadequately understood.  This study subjected Dofficinale to water restriction for periods ranging from 1 to 6 months, conducting physiological and RNA sequencing analyses to elucidate its long-term dehydration response mechanisms and identify drought-protective genes.  Following 6 months of dehydration, Dofficinale maintained viability, demonstrated by rapid growth resumption after merely 2 d of rehydration.  Transcriptome analysis of Dofficinale plants under 1-month dehydration revealed differential gene expression across various processes, predominantly in stress responses, photosynthesis, phytohormone signaling, carbon metabolism, and fructose/mannose pathways.  Among these, PEROXIDASE4 (POD4) and NAC37 showed significant upregulation and were selected for further investigation of their roles in drought protection.  Transgenic tomato plants overexpressing Dofficinale’s POD4 and NAC37 genes exhibited superior drought tolerance compared to controls, displaying enhanced vigor, increased fruit production, higher respiration rates, elevated chlorophyll levels, and reduced oxidative damage.  This research demonstrates the value of exploring underutilized species for drought-tolerance genes and identifies POD4 and NAC37 as promising candidates for improving drought tolerance through breeding programs.

Keywords:  Dendrobium officinale       drought stress       drought tolerance       tomato       transcriptomics  
Received: 22 July 2024   Accepted: 05 December 2024 Online: 02 June 2025  
Fund: 

This work was supported by the Hubei Provincial Natural Science Foundation, China (2022CFB009) and the National Natural Science Foundation of China (31900242).

About author:  Lulu Yu, E-mail: lulu2019@whsw.edu.cn; #Correspondence Fei Xu, E-mail: feixu666@hotmail.com

Cite this article: 

Lulu Yu, Muhammad Ahsan Asghar, Antonios Petridis, Fei Xu. 2025. Unlocking Dendrobium officinale’s drought resistance: Insights from transcriptomic analysis and enhanced drought tolerance in tomato. Journal of Integrative Agriculture, 24(11): 4282-4293.

Ahmad I Z. 2019. Chapter 13 - Role of sugars in abiotic stress signaling in plants. In: Khan M I R, Reddy P S, Ferrante A, Khan N A, eds. Plant Signaling Molecules. Woodhead Publishing, United Kingdom. pp. 207–217.

Alshareef N O, Wang J Y, Ali S, Al-Babili S, Tester M, Schmöckel S M. 2019. Overexpression of the NAC transcription factor JUNGBRUNNEN1 (JUB1) increases salinity tolerance in tomato. Plant Physiology and Biochemistry140, 113–121.

Aluko O O, Ninkuu V, Ziemah J, Jianpei Y, Taiwo E, Ninkuu S B, Sabuli N, Adetunde L A, Imoro A W M, Ozavize S F, Onyiro Q A, Dogee G, Adedire O M, Hunpatin O S, Opoku N. 2024. Genome-wide identification and expression analysis of EIN3/EIL gene family in rice (Oryza sativa). Plant Stress12, 100437.

Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B (Methodological), 57, 289–300.

Chen H, Bullock D A, Alonso J M, Stepanova A N. 2021. To fight or to grow: The balancing role of ethylene in plant abiotic stress responses. Plants11, 33.

Cutler S R, Rodriguez P L, Finkelstein R R, Abrams S R. 2010. Abscisic acid: Emergence of a core signaling network. Annual Review of Plant Biology61, 651–679.

Guo F, Han A, Gao H, Liang J, Zhao K, Cao S, Wang H, Wei Y, Shao X, Xu F. 2022. Mannose alleviates yellowing process of broccoli florets by regulating chlorophyll catabolism and delaying programmed cell death. Scientia Horticulturae295, 110888.

Huang H, Jiao Y, Tong Y, Wang Y. 2023. Comparative analysis of drought-responsive biochemical and transcriptomic mechanisms in two Dendrobium officinale genotypes. Industrial Crops and Products199, 116766.

Huang W, Duan W, Chen Y. 2022. Unravelling lake water storage change in Central Asia: Rapid decrease in tail-end lakes and increasing risks to water supply. Journal of Hydrology614, 128546.

Jian W, Zheng Y, Yu T, Cao H, Chen Y, Cui Q, Xu C, Li Z. 2021. SlNAC6, a NAC transcription factor, is involved in drought stress response and reproductive process in tomato. Journal of Plant Physiology264, 153483.

Jyoti S D, Azim J B, Robin A H K. 2021. Genome-wide characterization and expression profiling of EIN3/EIL family genes in Zea maysPlant Gene25, 100270.

Lai C H, Huo C Y, Xu J, Han Q B, Li L F. 2024. Critical review on the research of chemical structure, bioactivities, and mechanism of actions of Dendrobium officinale polysaccharide. International Journal of Biological Macromolecules263, 130315.

Li Q, Xu F, Chen Z, Teng Z, Sun K, Li X, Yu J, Zhang G, Liang Y, Huang X, Du L, Qian Y, Wang Y, Chu C, Tang J. 2021. Synergistic interplay of ABA and BR signal in regulating plant growth and adaptation. Nature Plants7, 1108–1118.

Li X D, Zhuang K Y, Liu Z M, Yang D Y, Ma N N, Meng Q W. 2016. Overexpression of a novel NAC-type tomato transcription factor, SlNAM1, enhances the chilling stress tolerance of transgenic tobacco. Journal of Plant Physiology204, 54–65.

Liu C, Li J, Zhu P, Yu J, Hou J, Wang C, Long D, Yu M, Zhao A. 2019. Mulberry EIL3 confers salt and drought tolerances and modulates ethylene biosynthetic gene expression. PeerJ7.

Masri R, Kiss E. 2023. The role of NAC genes in response to biotic stresses in plants. Physiological and Molecular Plant Pathology126, 102034.

Puranik S, Sahu P P, Srivastava P S, Prasad M. 2012. NAC proteins: Regulation and role in stress tolerance. Trends in Plant Science17, 369–381.

Ramadoss B R, Gangola M P, Gurunathan S. 2020. Chapter 4-NAC transcription factor family in rice: Recent advancements in the development of stress-tolerant rice. In: Wani S H, ed., Transcription Factors for Abiotic Stress Tolerance in Plants. Academic Press, United States. pp. 47–61.

Saidi M N, Mergby D, Souibgui A, Yacoubi I. 2022. Overexpression of durum wheat NAC transcription factor TtNTL3A promotes early flowering and increases multiple stress tolerance in transgenic arabidopsis. Plant Physiology and Biochemistry192, 1–9.

Samanta S, Seth C S, Roychoudhury A. 2024. The molecular paradigm of reactive oxygen species (ROS) and reactive nitrogen species (RNS) with different phytohormone signaling pathways during drought stress in plants. Plant Physiology and Biochemistry206, 108259.

Sharma A, Gupta A, Ramakrishnan M, Ha C V, Zheng B, Bhardwaj M, Tran L S P. 2023. Roles of abscisic acid and auxin in plants during drought: A molecular point of view. Plant Physiology and Biochemistry204, 108129.

Sreenivasulu N, Harshavardhan V T, Govind G, Seiler C, Kohli A. 2012. Contrapuntal role of ABA: Does it mediate stress tolerance or plant growth retardation under long-term drought stress? Gene506, 265–273.

Srivastava R, Kobayashi Y, Koyama H, Sahoo L. 2022. Overexpression of cowpea NAC transcription factors promoted growth and stress tolerance by boosting photosynthetic activity in Arabidopsis. Plant Science319, 111251.

Thanmalagan R R, Jayaprakash A, Roy A, Arunachalam A, Lakshmi P T V. 2022. A review on applications of plant network biology to understand the drought stress response in economically important cereal crops. Plant Gene29, 100345.

Thirumalaikumar V P, Devkar V, Mehterov N, Ali S, Ozgur R, Turkan I, Mueller-Roeber B, Balazadeh S. 2018. NAC transcription factor JUNGBRUNNEN1 enhances drought tolerance in tomato. Plant Biotechnology Journal16, 354–366.

Velikova V, Yordanov I, Edreva A. 2000. Oxidative stress and some antioxidant systems in acid rain-treated bean plants: Protective role of exogenous polyamines. Plant Science151, 59–66.

Vurukonda S S K P, Vardharajula S, Shrivastava M, Skz A. 2016. Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiological Research184, 13–24.

Wu X, Yuan J, Luo A, Chen Y, Fan Y. 2016. Drought stress and re-watering increase secondary metabolites and enzyme activity in Dendrobium moniliformeIndustrial Crops and Products94, 385–393.

Xu F, Yuan S, Zhang D W, Lv X, Lin H H. 2012a. The role of alternative oxidase in tomato fruit ripening and its regulatory interaction with ethylene. Journal of Experimental Botany63, 5705–5716.

Xu F, Zhang D W, Zhu F, Tang H, Lv X, Cheng J, Xie H F, Lin H H. 2012b. A novel role for cyanide in the control of cucumber (Cucumis sativus L.) seedlings response to environmental stress. Plant Cell and Environment35, 1983–1997.

Yadav B, Jogawat A, Rahman M S, Narayan O P. 2021. Secondary metabolites in the drought stress tolerance of crop plants: A review. Gene Reports23, 101040.

Yu L L, Liu C J, Peng Y, He Z Q, Xu F. 2022. New insights into the role of cyanide in the promotion of seed germination in tomato. BMC Plant Biology22, 28.

Yu L L, Liu Y, Peng Y, Zhu F, Xu F. 2021. Overexpression of cyanoalanine synthase 1 improves germinability of tobacco seeds under salt stress conditions. Environmental and Experimental Botany182, 104332.

Yu L L, Liu Y, Xu F. 2019. Comparative transcriptome analysis reveals significant differences in the regulation of gene expression between hydrogen cyanide- and ethylene-treated Arabidopsis thalianaBMC Plant Biology19, 92.

Yu L L, Liu Y, Zhu F, Geng X X, Yang Y, He Z Q, Xu F. 2020. The enhancement of salt stress tolerance by salicylic acid pretreatment in Arabidopsis thalianaBiologia Plantarum64, 150–158.

Zhang H, Sun X, Dai M. 2022. Improving crop drought resistance with plant growth regulators and rhizobacteria: Mechanisms, applications, and perspectives. Plant Communications3, 100228.

Zhang H, Zhao Y, Zhu J K. 2020. Thriving under stress: How plants balance growth and the stress response. Developmental Cell55, 529–543.

Zhao S Y, Zeng W H, Li Z, Peng Y. 2020. Mannose regulates water balance, leaf senescence, and genes related to stress tolerance in white clover under osmotic stress. Biologia Plantarum64, 406–416.

Zia R, Nawaz M S, Siddique M J, Hakim S, Imran A. 2021. Plant survival under drought stress: Implications, adaptive responses, and integrated rhizosphere management strategy for stress mitigation. Microbiological Research242, 126626.

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