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Physiological and transcriptional regulation in Taxodium hybrid ‘Zhongshanshan’ leaves in acclimation to prolonged partial submergence

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Abstract

Main conclusion

Taxodium 703 leaves activate fermentation, amino acids metabolism and ROS detoxification, and reduce TCA cycle and ABA biosynthesis in acclimation to prolonged partial submergence stress.

Abstract

Taxodium hybrid ‘Zhongshanshan 703’ (T. mucronatum × T. distichum; Taxodium 703) is a highly flooding-tolerant woody plant. To investigate the physiological and transcriptional regulatory mechanisms underlying its leaves in acclimation to long-term flooding, we exposed cuttings of Taxodium 703 to either non-flooding (control) or partial submergence for 2 months. The leaf tissues above (AL) and below (BL) flooding-water were separately harvested. Partial submergence decreased concentrations of chlorophyll (a + b) and dehydroascorbate (DHA) and lactate dehydrogenase (LDH) activity in AL, and reduced biomass, concentrations of succinic acid, fumaric acid and malic acid, and transcript levels of genes involved in tricarboxylic acid (TCA) cycle in BL. Under partial submergence, concentrations of starch, malondialdehyde and abscisic acid (ABA) decreased, and also mRNA levels of nine-cis-epoxycarotenoid dioxygenases that are involved in ABA biosynthesis in AL and BL of Taxodium 703. Partial submergence increased O2− content in AL, and improved concentrations of pyruvate and soluble sugars and activities of LDH and peroxidase in BL. In addition, partial submergence increased concentrations of ethanol, lactate, alanine, γ-aminobutyric acid, total amino acids and ascorbic acid (ASA), and ASA/DHA, activities of alcohol dehydrogenases (ADH) and ascorbate peroxidase, as well as transcript levels of ADH1A, ADH1B and genes involved in alanine biosynthesis and starch degradation in AL and BL of Taxodium 703. Overall, these results suggest that Taxodium 703 leaves activate fermentation, amino acids metabolism and reactive oxygen species detoxification, and maintain a steady supply of sugars, and reduce TCA cycle and ABA biosynthesis in acclimation to prolonged partial submergence stress.

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All the data are presented in figures, tables, and Supporting Information.

Abbreviations

ADH:

Alcohol dehydrogenase

APX:

Ascorbate peroxidase

ASA:

Ascorbic acid

CAT:

Catalase

DHA:

Dehydroascorbate

GR:

Glutathione reductase

GSSG:

Oxidized glutathione

GSH:

Glutathione

GABA:

γ-Aminobutyric acid

LDH:

Lactate dehydrogenase

MDA:

Malondialdehyde

NCED :

Nine-cis-epoxycarotenoid dioxygenase

POD:

Peroxidase

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

TCA:

Tricarboxylic acid

References

  • Abdelsalam NR, Salem MZM, Ali HM, Mackled MI, El-Hefny M, Elshikh MS, Hatamleh AA (2019) Morphological, biochemical, molecular, and oil toxicity properties of Taxodium trees from different locations. Ind Crops Prod 139:11. https://doi.org/10.1016/j.indcrop.2019.111515

    Article  CAS  Google Scholar 

  • Antonio C, Papke C, Rocha M, Diab H, Limami AM, Obata T, Fernie AR, van Dongen JT (2016) Regulation of primary metabolism in response to low oxygen availability as revealed by carbon and nitrogen isotope redistribution. Plant Physiol 170(1):43–56. https://doi.org/10.1104/pp.15.00266

    Article  CAS  PubMed  Google Scholar 

  • Azahar I, Ghosh S, Adhikari A, Adhikari S, Roy D, Shaw AK, Singh K, Hossain Z (2020) Comparative analysis of maize root sRNA transcriptome unveils the regulatory roles of miRNAs in submergence stress response mechanism. Environ Exp Bot 171:103924. https://doi.org/10.1016/j.envexpbot.2019.103924

    Article  CAS  Google Scholar 

  • Bailey-Serres J, Voesenek LA (2008) Flooding stress: acclimations and genetic diversity. Annu Rev Plant Biol 59:313–339. https://doi.org/10.1146/annurev.arplant.59.032607.092752

    Article  CAS  PubMed  Google Scholar 

  • Behnam B, Iuchi S, Fujita M, Fujita Y, Takasaki H, Osakabe Y, Yamaguchi-Shinozaki K, Kobayashi M, Shinozaki K (2013) Characterization of the promoter region of an Arabidopsis gene for 9-cis-epoxycarotenoid dioxygenase involved in dehydration-inducible transcription. DNA Res 20(4):315–324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bui LT, Shukla V, Giorgi FM, Trivellini A, Perata P, Licausi F, Giuntoli B (2020) Differential submergence tolerance between juvenile and adult Arabidopsis plants involves the ANAC017 transcription factor. Plant J 104(4):979–994. https://doi.org/10.1111/tpj.14975

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Han Y, Jiang H, Korpelainen H, Li C (2011) Nitrogen nutrient status induces sexual differences in responses to cadmium in Populus yunnanensis. J Exp Bot 62(14):5037–5050

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Z, Wang C, Chen X, Yuan Z, Song H, Li C (2020) Heterogeneous leaves of predominant trees species enhance decomposition and nutrient release in the riparian zone of the Three Gorges Reservoir. Sci Rep 10(1):1–9

    Google Scholar 

  • Crawford LA, Bown AW, Breitkreuz KE, Guinel FC (1994) The synthesis of [gamma]-aminobutyric acid in response to treatments reducing cytosolic pH. Plant Physiol 104(3):865–871

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Creech D, Zhou L, Yunlong Y, Eguiluz-Piedra T (2011) Can Taxodium be improved. Arnoldia 69(2):11–20

    Google Scholar 

  • Denny GC, Arnold MA (2007) Taxonomy and nomenclature of baldcypress, pondcypress, and montezuma cypress: one, two, or three species? HortTechnol 17(1):125–127

    Article  Google Scholar 

  • Ella ES, Kawano N, Ito O (2003) Importance of active oxygen-scavenging system in the recovery of rice seedlings after submergence. Plant Sci 165(1):85–93

    Article  CAS  Google Scholar 

  • Ferner E, Rennenberg H, Kreuzwieser J (2012) Effect of flooding on C metabolism of flood-tolerant (Quercus robur) and non-tolerant (Fagus sylvatica) tree species. Tree Physiol 32(2):135–145. https://doi.org/10.1093/treephys/tps009

    Article  CAS  PubMed  Google Scholar 

  • Gupta KJ, Zabalza A, Van Dongen JT (2009) Regulation of respiration when the oxygen availability changes. Physiol Plant 137(4):383–391

    Article  CAS  PubMed  Google Scholar 

  • Hartman S, Sasidharan R, Voesenek L (2021) The role of ethylene in metabolic acclimations to low oxygen. New Phytol 229(1):64–70. https://doi.org/10.1111/nph.16378

    Article  CAS  PubMed  Google Scholar 

  • Hattori Y, Nagai K, Furukawa S, Song X-J, Kawano R, Sakakibara H, Wu J, Matsumoto T, Yoshimura A, Kitano H (2009) The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature 460(7258):1026–1030

    Article  CAS  PubMed  Google Scholar 

  • He J, Ma C, Ma Y, Li H, Kang J, Liu T, Polle A, Peng C, Luo Z-B (2013) Cadmium tolerance in six poplar species. Environ Sci Poll Res 20(1):163–174

    Article  CAS  Google Scholar 

  • Hebbelmann I, Selinski J, Wehmeyer C, Goss T, Voss I, Mulo P, Kangasjärvi S, Aro E-M, Oelze M-L, Dietz K-J (2012) Multiple strategies to prevent oxidative stress in Arabidopsis plants lacking the malate valve enzyme NADP-malate dehydrogenase. J Exp Bot 63(3):1445–1459

    Article  CAS  PubMed  Google Scholar 

  • Herzog M, Fukao T, Winkel A, Konnerup D, Lamichhane S, Alpuerto JB, Hasler-Sheetal H, Pedersen O (2018) Physiology, gene expression, and metabolome of two wheat cultivars with contrasting submergence tolerance. Plant Cell Environ 41(7):1632–1644. https://doi.org/10.1111/pce.13211

    Article  CAS  PubMed  Google Scholar 

  • Hua J, Han L, Wang Z, Gu C, Yin Y (2017) Morpho-anatomical and photosynthetic responses of Taxodium hybrid “Zhongshanshan” 406 to prolonged flooding. Flora 231:29–37. https://doi.org/10.1016/j.flora.2017.04.007

    Article  Google Scholar 

  • Ismond KP, Dolferus R, De Pauw M, Dennis ES, Good AG (2003) Enhanced low oxygen survival in Arabidopsis through increased metabolic flux in the fermentative pathway. Plant Physiol 132(3):1292–1302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jia J, Li S, Cao X, Li H, Shi W, Polle A, Liu TX, Peng C, Luo ZB (2016) Physiological and transcriptional regulation in poplar roots and leaves during acclimation to high temperature and drought. Physiol Plant 157(1):38–53. https://doi.org/10.1111/ppl.12400

    Article  CAS  PubMed  Google Scholar 

  • Kawano N, Ella E, Ito O, Yamauchi Y, Tanaka K (2002) Metabolic changes in rice seedlings with different submergence tolerance after desubmergence. Environ Exp Bot 47(3):195–203. https://doi.org/10.1016/S0098-8472(01)00126-5

    Article  CAS  Google Scholar 

  • Kim Y, Seo CW, Khan AL, Mun BG, Shahzad R, Ko JW, Yun BW, Park SK, Lee IJ (2018) Exo-ethylene application mitigates waterlogging stress in soybean (Glycine max L.). BMC Plant Biol 18(1):254. https://doi.org/10.1186/s12870-018-1457-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kolb RM, Joly CA (2009) Flooding tolerance of Tabebuia cassinoides: metabolic, morphological and growth responses. Flora 204(7):528–535

    Article  Google Scholar 

  • Kreuzwieser J, Hauberg J, Howell KA, Carroll A, Rennenberg H, Millar AH, Whelan J (2009) Differential response of gray poplar leaves and roots underpins stress adaptation during hypoxia. Plant Physiol 149(1):461–473. https://doi.org/10.1104/pp.108.125989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • León G, Holuigue L, Jordana X (2007) Mitochondrial complex II is essential for gametophyte development in Arabidopsis. Plant Physiol 143(4):1534–1546

    Article  PubMed  PubMed Central  Google Scholar 

  • Li C, Zhong Z, Geng Y, Schneider R (2009) Comparative studies on physiological and biochemical adaptation of Taxodium distichum and Taxodium ascendens seedlings to different soil water regimes. Plant Soil 329(1–2):481–494. https://doi.org/10.1007/s11104-009-0174-z

    Article  CAS  Google Scholar 

  • Liu J, Hasanuzzaman M, Sun H, Zhang J, Peng T, Sun H, Xin Z, Zhao Q (2020) Comparative morphological and transcriptomic responses of lowland and upland rice to root-zone hypoxia. Environ Exp Bot 169:103916. https://doi.org/10.1016/j.envexpbot.2019.103916

    Article  CAS  Google Scholar 

  • Lu Y, Deng S, Li Z, Wu J, Liu Q, Liu W, Yu WJ, Zhang Y, Shi W, Zhou J, Li H, Polle A, Luo ZB (2019) Competing endogenous RNA networks underlying anatomical and physiological characteristics of poplar wood in acclimation to low nitrogen availability. Plant Cell Physiol 60(11):2478–2495. https://doi.org/10.1093/pcp/pcz146

    Article  CAS  PubMed  Google Scholar 

  • Lu Y, Deng S, Li Z, Wu J, Zhu D, Shi W, Zhou J, Fayyaz P, Luo ZB (2022) Physiological characteristics and transcriptomic dissection in two root segments with contrasting net fluxes of ammonium and nitrate of poplar under low nitrogen availability. Plant Cell Physiol 63(1):30–44. https://doi.org/10.1093/pcp/pcab137

    Article  CAS  PubMed  Google Scholar 

  • Mallik AU, Richardson JS (2009) Riparian vegetation change in upstream and downstream reaches of three temperate rivers dammed for hydroelectric generation in British Columbia, Canada. Ecol Eng 35(5):810–819. https://doi.org/10.1016/j.ecoleng.2008.12.005

    Article  Google Scholar 

  • Millward LS, Wilson TM, Weldy MJ, Rowland MM, Duarte A, Lesmeister DB, Ripple WJ (2022) Small mammal relative abundance within riparian ecosystems of the Blue Mountains. For Ecol Manage 505:119899

    Article  Google Scholar 

  • Minami A, Yano K, Gamuyao R, Nagai K, Kuroha T, Ayano M, Nakamori M, Koike M, Kondo Y, Niimi Y, Kuwata K, Suzuki T, Higashiyama T, Takebayashi Y, Kojima M, Sakakibara H, Toyoda A, Fujiyama A, Kurata N, Ashikari M, Reuscher S (2018) Time-course transcriptomics analysis reveals key responses of submerged deepwater rice to flooding. Plant Physiol 176(4):3081–3102. https://doi.org/10.1104/pp.17.00858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miyashita Y, Dolferus R, Ismond KP, Good AG (2007) Alanine aminotransferase catalyses the breakdown of alanine after hypoxia in Arabidopsis thaliana. Plant J 49(6):1108–1121

    Article  CAS  PubMed  Google Scholar 

  • Mustroph A, Barding GA Jr, Kaiser KA, Larive CK, Bailey-Serres J (2014) Characterization of distinct root and shoot responses to low-oxygen stress in Arabidopsis with a focus on primary C- and N-metabolism. Plant Cell Environ 37(10):2366–2380. https://doi.org/10.1111/pce.12282

    Article  CAS  PubMed  Google Scholar 

  • Mutava RN, Prince SJK, Syed NH, Song L, Valliyodan B, Chen W, Nguyen HT (2015) Understanding abiotic stress tolerance mechanisms in soybean: a comparative evaluation of soybean response to drought and flooding stress. Plant Physiol Biochem 86:109–120. https://doi.org/10.1016/j.plaphy.2014.11.010

    Article  CAS  PubMed  Google Scholar 

  • Narsai R, Rocha M, Geigenberger P, Whelan J, van Dongen JT (2011) Comparative analysis between plant species of transcriptional and metabolic responses to hypoxia. New Phytol 190(2):472–487. https://doi.org/10.1111/j.1469-8137.2010.03589.x

    Article  CAS  PubMed  Google Scholar 

  • Nguyen TN, Tuan PA, Mukherjee S, Son S, Ayele BT (2018) Hormonal regulation in adventitious roots and during their emergence under waterlogged conditions in wheat. J Exp Bot 69(16):4065–4082. https://doi.org/10.1093/jxb/ery190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng Y, Zhou Z, Zhang Z, Yu X, Zhang X, Du K (2018) Molecular and physiological responses in roots of two full-sib poplars uncover mechanisms that contribute to differences in partial submergence tolerance. Sci Rep 8(1):12829. https://doi.org/10.1038/s41598-018-30821-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Planchet E, Lothier J, Limami AM (2017) Hypoxic respiratory metabolism in plants: reorchestration of nitrogen and carbon metabolisms. In: Tcherkez G, Ghashghaie J (eds) Plant respiration: metabolic fluxes and carbon balance. Adv Photosynthesis ‘Respiration, vol 43. Springer, Berlin, pp 209–226

    Chapter  Google Scholar 

  • Ponnamperuma F (1984) Effects of flooding on soils, vol 10. Academic Press, New York

    Google Scholar 

  • Qi B, Yang Y, Yin Y, Xu M, Li H (2014) De novo sequencing, assembly, and analysis of the Taxodium ‘Zhongshansa’roots and shoots transcriptome in response to short-term waterlogging. BMC Plant Biol 14(1):1–12

    Article  Google Scholar 

  • Qi X, Li Q, Ma X, Qian C, Wang H, Ren N, Shen C, Huang S, Xu X, Xu Q, Chen X (2019) Waterlogging-induced adventitious root formation in cucumber is regulated by ethylene and auxin through reactive oxygen species signalling. Plant Cell Environ 42(5):1458–1470. https://doi.org/10.1111/pce.13504

    Article  CAS  PubMed  Google Scholar 

  • Qin Y-M, Hu C-Y, Pang Y, Kastaniotis AJ, Hiltunen JK, Zhu Y-X (2007) Saturated very-long-chain fatty acids promote cotton fiber and Arabidopsis cell elongation by activating ethylene biosynthesis. Plant Cell 19(11):3692–3704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rahman M, Grover A, Peacock WJ, Dennis ES, Ellis MH (2001) Effects of manipulation of pyruvate decarboxylase and alcohol dehydrogenase levels on the submergence tolerance of rice. Funct Plant Biol 28(12):1231–1241

    Article  CAS  Google Scholar 

  • Ribeiro IM, Vinson CC, Coca GC, Ferreira CDS, Franco AC, Williams TCR (2022) Differences in the metabolic and functional mechanisms used to tolerate flooding in Guazuma ulmifolia (Lam.) from flood-prone Amazonian and dry Cerrado savanna populations. Tree Physiol 42(10):2116–2132. https://doi.org/10.1093/treephys/tpac059

    Article  CAS  PubMed  Google Scholar 

  • Rocha M, Licausi F, Araujo WL, Nunes-Nesi A, Sodek L, Fernie AR, van Dongen JT (2010) Glycolysis and the tricarboxylic acid cycle are linked by alanine aminotransferase during hypoxia induced by waterlogging of Lotus japonicus. Plant Physiol 152(3):1501–1513. https://doi.org/10.1104/pp.109.150045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salah A, Zhan M, Cao C, Han Y, Ling L, Liu Z, Li P, Ye M, Jiang Y (2019) Gamma-aminobutyric acid promotes chloroplast ultrastructure, antioxidant capacity, and growth of waterlogged maize seedlings. Sci Rep 9(1):484. https://doi.org/10.1038/s41598-018-36334-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salvatierra A, Pimentel P, Almada R, Hinrichsen P (2016) Exogenous GABA application transiently improves the tolerance to root hypoxia on a sensitive genotype of Prunus rootstock. Environ Exp Bot 125:52–66

    Article  CAS  Google Scholar 

  • Shabala S, Shabala L, Barcelo J, Poschenrieder C (2014) Membrane transporters mediating root signalling and adaptive responses to oxygen deprivation and soil flooding. Plant Cell Environ 37(10):2216–2233. https://doi.org/10.1111/pce.12339

    Article  CAS  PubMed  Google Scholar 

  • Shingaki-Wells R, Millar AH, Whelan J, Narsai R (2014) What happens to plant mitochondria under low oxygen? An omics review of the responses to low oxygen and reoxygenation. Plant Cell Environ 37(10):2260–2277. https://doi.org/10.1111/pce.12312

    Article  CAS  PubMed  Google Scholar 

  • Suzan-Azpiri H, Enriquez-Pena G, Malda-Barrera G (2007) Population structure of the Mexican baldcypress (Taxodium mucronatum Ten.) in Queretaro, Mexico. For Ecol Manage 242(2–3):243–249. https://doi.org/10.1016/j.foreco.2007.01.041

    Article  Google Scholar 

  • Takahashi H, Greenway H, Matsumura H, Tsutsumi N, Nakazono M (2014) Rice alcohol dehydrogenase 1 promotes survival and has a major impact on carbohydrate metabolism in the embryo and endosperm when seeds are germinated in partially oxygenated water. Ann Bot 113(5):851–859. https://doi.org/10.1093/aob/mct305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamang BG, Li S, Rajasundaram D, Lamichhane S, Fukao T (2021) Overlapping and stress-specific transcriptomic and hormonal responses to flooding and drought in soybean. Plant J 107(1):100–117. https://doi.org/10.1111/tpj.15276

    Article  CAS  PubMed  Google Scholar 

  • Thalmann M, Pazmino D, Seung D, Horrer D, Nigro A, Meier T, Kölling K, Pfeifhofer HW, Zeeman SC, Santelia D (2016) Regulation of leaf starch degradation by abscisic acid is important for osmotic stress tolerance in plants. Plant Cell 28(8):1860–1878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Z, Gu C, Xuan L, Hua J, Shi Q, Fan W, Yin Y, Yu F (2017) Identification of suitable reference genes in Taxodium ‘Zhongshanshan’ under abiotic stresses. Trees 31(5):1519–1530. https://doi.org/10.1007/s00468-017-1566-y

    Article  CAS  Google Scholar 

  • Wang C, Xie Y, Ren Q, Li C (2018) Leaf decomposition and nutrient release of three tree species in the hydro-fluctuation zone of the Three Gorges Dam Reservoir, China. Environ Sci Poll Res 25:23261–23275

    Article  CAS  Google Scholar 

  • Wu YS, Yang CY (2016) Physiological responses and expression profile of NADPH oxidase in rice (Oryza sativa) seedlings under different levels of submergence. Rice (n Y) 9(1):2. https://doi.org/10.1186/s12284-016-0074-9

    Article  PubMed  Google Scholar 

  • Xuan L, Hua J, Zhang F, Wang Z, Pei X, Yang Y, Yin Y, Creech DL (2021) Identification and functional analysis of ThADH1 and ThADH4 genes involved in tolerance to waterlogging stress in Taxodium hybrid “Zhongshanshan 406.” Genes (basel) 12(2):225. https://doi.org/10.3390/genes12020225

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Li C, Li J, Schneider R, Lamberts W (2013) Growth dynamics of Chinese wingnut (Pterocarya stenoptera) seedlings and its effects on soil chemical properties under simulated water change in the Three Gorges Reservoir Region of Yangtze River. Environ Sci Poll Res 20:7112–7123

    Article  Google Scholar 

  • Yin D, Chen S, Chen F, Guan Z, Fang W (2009) Morphological and physiological responses of two chrysanthemum cultivars differing in their tolerance to waterlogging. Environ Exp Bot 67(1):87–93. https://doi.org/10.1016/j.envexpbot.2009.06.006

    Article  CAS  Google Scholar 

  • Yu W, Liu H, Luo J, Zhang S, Xiang P, Wang W, Cai J, Lu Z, Zhou Z, Hu J, Lu Y (2022) Partial root-zone simulated drought induces greater flavonoid accumulation than full root-zone simulated water deficiency in the leaves of Ginkgo biloba. Environ Exp Bot 201:104998. https://doi.org/10.1016/j.envexpbot.2022.104998

    Article  CAS  Google Scholar 

  • Zhang B, Liu H, Ding X, Qiu J, Zhang M, Chu Z (2018) Arabidopsis thaliana AtACS8 plays a crucial role in the early biosynthesis of ethylene elicited by Cu2+ ions’. Cell Sci 131(2):jcs202424

    Google Scholar 

  • Zhao N, Li C, Yan Y, Cao W, Song A, Wang H, Chen S, Jiang J, Chen F (2018) Comparative transcriptome analysis of waterlogging-sensitive and waterlogging-tolerant Chrysanthemum morifolium cultivars under waterlogging stress and reoxygenation conditions. Int J Mol Sci 19(5):1455. https://doi.org/10.3390/ijms19051455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou W, Chen F, Meng Y, Chandrasekaran U, Luo X, Yang W, Shu K (2020) Plant waterlogging/flooding stress responses: from seed germination to maturation. Plant Physiol Biochem 148:228–236. https://doi.org/10.1016/j.plaphy.2020.01.020

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This study was jointly supported by the National Natural Science Foundation of China (32101490), the Jiangsu Province Innovation and extension project of forestry science and technology (LYKJ[2020]08), the Jiangsu Long-Term Scientific Research Base for Taxodium Rich. Breeding and Cultivation (LYKJ[2021]05), and the Jiangsu Institute of Botany Talent Fund (JIBTF202208).

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  1. Jiangsu Key Laboratory for the Research and Utilization of Plant Resources, Institute of Botany, Jiangsu Province and Chinese Academy of Sciences (Nanjing Botanical Garden Mem. Sun Yat-Sen), Nanjing, 210014, China

    Yan Lu, Zhiguo Lu, Zhidong Zhou, Yunlong Yin, Jianfeng Hua, Qin Shi & Chaoguang Yu

  2. Co-Innovation Center for the Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing, 210037, China

    Peng Xiang, Shuqing Zhang & Wanwen Yu

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  1. Yan Lu
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Lu, Y., Xiang, P., Zhang, S. et al. Physiological and transcriptional regulation in Taxodium hybrid ‘Zhongshanshan’ leaves in acclimation to prolonged partial submergence. Planta 258, 66 (2023). https://doi.org/10.1007/s00425-023-04225-w

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