Transcriptional and physiological insights into calcium-mediated waterlogging tolerance in peach

Muhammad Atiq Ashraf , Muhammad Ateeq , Haowei Du , Jinzhi Yang , Xusheng Gao , Muhammad Mohsin Kaleem , Muhammad Daud , Burhan Khalid , Muhammad Asim , Shumaila Nawaz , Sergey Shabala , Kaijie Zhu , Junwei Liu

Horticulture Advances ›› 2026, Vol. 4 ›› Issue (1) : 22

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Horticulture Advances ›› 2026, Vol. 4 ›› Issue (1) :22 DOI: 10.1007/s44281-026-00124-8
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Transcriptional and physiological insights into calcium-mediated waterlogging tolerance in peach
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Abstract

Waterlogging (WL) stress severely affects the growth and productivity of fruit crops. Cytosolic calcium (Ca2+) is recognized as a secondary messenger that initiates adaptive responses to environmental stresses. However, the mechanisms by which exogenously applied Ca2+ enhances WL tolerance remain poorly understood. In this study, we investigated whether exogenous Ca2+, applied as calcium chloride (CaCl2) and calcium oxide nanoparticles (CaO-NPs), might mitigate WL-induced damage in peach (Prunus persica) seedlings. We found that both Ca2+ formulations significantly alleviated WL-induced growth inhibition, restored photosynthetic efficiency, and maintained root system architecture and metabolic activity. Two Ca2+ treatments markedly reduced intracellular superoxide (SOD) and hydrogen peroxide accumulation, thus attenuating membrane lipid peroxidation and electrolyte leakage. Hormonal profiling demonstrated that Ca2+ suppressed excessive abscisic acid and salicylic acid accumulation while restoring jasmonate homeostasis under WL conditions. Furthermore, at the transcriptional level, Ca2+ enhanced stress tolerance by upregulating the expression of genes encoding antioxidant (PpSOD; and peroxidase, PpPOD), photosynthetic (photosystem II subunit Q, PpPsbQ; and photosystem I subunit K, PpPsaK), and Ca2+ (CBL-interacting protein kinases, PpCIPK5 and PpCIPK11). In line with reduced oxidative stress, Ca2+ also adaptively downregulated genes related to the fermentative pathway (alcohol dehydrogenase, PpADH; and lactate dehydrogenase, PpLDH), indicating a shift away from anaerobic metabolism. Notably, comparative analysis revealed that ionic Ca2+ and CaO-NP treatments resulted in largely similar outcomes under WL conditions, with only marginal differences in some parameters. Taken together, these results indicate that Ca2+-associated signaling is a putative regulatory network underlying adaptive responses to WL stress in woody fruit crops.

Keywords

Ca2+ signaling / Hormonal regulation / Hypoxia / Peach / Photosynthetic efficiency / ROS homeostasis

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Muhammad Atiq Ashraf, Muhammad Ateeq, Haowei Du, Jinzhi Yang, Xusheng Gao, Muhammad Mohsin Kaleem, Muhammad Daud, Burhan Khalid, Muhammad Asim, Shumaila Nawaz, Sergey Shabala, Kaijie Zhu, Junwei Liu. Transcriptional and physiological insights into calcium-mediated waterlogging tolerance in peach. Horticulture Advances, 2026, 4 (1) : 22 DOI:10.1007/s44281-026-00124-8

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References

[1]

Allahverdiyeva Y, Suorsa M, Rossi F, Pavesi A, Kater MM, Antonacci A, et al. . Arabidopsis plants lacking PsbQ and PsbR subunits of the oxygen-evolving complex show altered PSII super-complex organization and short-term adaptive mechanisms. Plant J, 2013, 75: 671-684

[2]

Arbona V, López-Climent MF, Pérez-Clemente RM, Gómez-Cadenas A. Maintenance of a high photosynthetic performance is linked to flooding tolerance in Citrus. Environ Exp Bot, 2009, 66: 135-142

[3]

Asada K. Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol, 2006, 141: 391-396

[4]

Ashraf MA, Khan AS, Shireen F, Nawaz S, Ayyub S, Mohibullah S, et al. . Peach diseases in a changing climate: Pathogens, resistance, and sustainable solutions. Microb Pathog, 2025, 209 108110

[5]

Ashraf MA, Ateeq M, Zhu K, Asim M, Mohibullah S, Riaz T, et al. . Phytohormone networks orchestrating lateral organ adaptations to hypoxia and reoxygenation in fruit crops. Plant Cell Environ, 2026, 49: 607-622

[6]

Asim M, Ateeq M, Shen X, An S, Ahmed MM, Ashraf MA, et al. . Molecular mechanisms and adaptive strategies for hypoxia tolerance in horticultural crops: Beyond model systems. Hortic Adv, 2025, 3: 34

[7]

Ateeq M, Khan AH, Zhang D, Alam SM, Shen W, Wei M, et al. . Comprehensive physio-biochemical and transcriptomic characterization to decipher the network of key genes under waterlogging stress and its recuperation in Prunus persica. Tree Physiol, 2023, 43: 1265-1283

[8]

Ateeq M, Zhang D, Xiao J, Zhang H, Shen X, Meng J, et al. . Decoding submergence tolerance in Prunus persica: Integrated transcriptomic and metabolomic acclimations of antioxidant system, cell wall dynamics, and hormonal signaling. Hortic Adv, 2025, 3: 5

[9]

Ateeq M, Alam SM, Kaleem MM, Fahad S, Ashraf MA, Asim M, et al. . Unlocking plant abiotic stress resilience through biostimulants and omics-driven innovations. J Integr Plant Biol, 2026, 00: 1-19

[10]

Ayyaz A, Fang R, Ma J, Hannan F, Huang Q, Athar HR, et al. . Calcium nanoparticles (Ca-NPs) improve drought stress tolerance in Brassica napus by modulating the photosystem II, nutrient acquisition and antioxidant performance. NanoImpact, 2022, 28 100423

[11]

Bailey-Serres J, Voesenek LACJ. Flooding stress: Acclimations and genetic diversity. Annu Rev Plant Biol, 2008, 59: 313-339

[12]

Bakshi A, Gilroy S. Calcium signaling in hypoxic response. Plant Physiol. 2025;197:kiae654. https://doi.org/10.1093/plphys/kiae654.

[13]

Benech-Arnold RL, Gualano N, Leymarie J, Côme D, Corbineau F. Hypoxia interferes with ABA metabolism and increases ABA sensitivity in embryos of dormant barley grains. J Exp Bot, 2006, 57: 1423-1430

[14]

Chen Y, Su WY, Ren CJ, Lin YL, Wang WQ, Zhang HQ, et al. . Restricted responses of AcMYB68 and AcERF74/75 enhanced waterlogging tolerance in kiwifruit. Plant J, 2024, 119: 1059-1072

[15]

Daniel K, Hartman S. How plant roots respond to waterlogging. J Exp Bot, 2024, 75: 511-525

[16]

Demidchik V, Shabala S. Mechanisms of cytosolic calcium elevation in plants: The role of ion channels, calcium extrusion systems and NADPH oxidase-mediated ‘ROS-Ca2+ Hub’. Funct Plant Biol, 2018, 45: 9-27

[17]

Fan B, Liao K, Wang LN, Shi LL, Zhang Y, Xu LJ, et al. . Calcium-dependent activation of CPK12 facilitates its cytoplasm-to-nucleus translocation to potentiate plant hypoxia sensing by phosphorylating ERF-VII transcription factors. Mol Plant, 2023, 16: 979-998

[18]

Fang X, Fan L, Zhou H, Yan H, Ding F, Li R, et al. . Multi-omic analyses reveal the waterlogging induced responses in Magnolia sinostellata. Front Plant Sci, 2025, 16: 1653464

[19]

Feng D, Wang X, Gao J, Zhang C, Liu H, Liu P, et al. . Exogenous calcium: Its mechanisms and research advances involved in plant stress tolerance. Front Plant Sci, 2023, 14: 1143963

[20]

Foyer CH, Noctor G. Ascorbate and glutathione: The heart of the redox hub. Plant Physiol, 2011, 155: 2-18

[21]

Fukao T, Bailey-Serres J. Plant responses to hypoxia–is survival a balancing act?. Trends Plant Sci, 2004, 9: 449-456

[22]

Geng R, Xu M, Xu L, Yan G, Cai G. Biological mechanisms of waterlogging tolerance in plants. Plant Cell Environ, 2026, 49: 685-699

[23]

Ghani MI, Saleem S, Rather SA, Rehmani MS, Alamri S, Rajput VD, et al. . Foliar application of zinc oxide nanoparticles: An effective strategy to mitigate drought stress in cucumber seedling by modulating antioxidant defense system and osmolytes accumulation. Chemosphere, 2022, 289 133202

[24]

Gong X, Xu Y, Li H, Chen X, Song Z. Antioxidant activation, cell wall reinforcement, and reactive oxygen species regulation promote resistance to waterlogging stress in hot pepper (Capsicum annuum L.). BMC Plant Biol. 2022;22:425. https://doi.org/10.1186/s12870-022-03807-2.

[25]

Habibi F, Liu T, Shahid MA, Schaffer B, Sarkhosh A. Physiological, biochemical, and molecular responses of fruit trees to root zone hypoxia. Environ Exp Bot, 2023, 206 105179

[26]

He W, Luo L, Xie R, Chai J, Wang H, Wang Y, et al. . Transcriptome sequencing analyses uncover mechanisms of citrus rootstock seedlings under waterlogging stress. Front Plant Sci, 2023, 14: 1198930

[27]

He L, Yu L, Li B, Du N, Guo S. The effect of exogenous calcium on cucumber fruit quality, photosynthesis, chlorophyll fluorescence, and fast chlorophyll fluorescence during the fruiting period under hypoxic stress. BMC Plant Biol. 201818:180. https://doi.org/10.1186/s12870-018-1393-3.

[28]

Herrera-Vásquez A, Salinas P, Holuigue L. Salicylic acid and reactive oxygen species interplay in the transcriptional control of defense genes expression. Front Plant Sci, 2015, 6: 171

[29]

Huang S, Roelfsema MRG, Gilliham M, Hetherington AM, Hedrich R. Guard cells count the number of unitary cytosolic Ca2+ signals to regulate stomatal dynamics. Curr Biol, 2024, 34: 5409-5416

[30]

Islam MM, Jahan K, Sen A, Urmi TA, Haque MM, Ali HM, et al. Exogenous application of calcium ameliorates salinity stress tolerance of tomato (Solanum lycopersicum L.) and enhances fruit quality. Antioxidants. 2023;12:558. https://doi.org/10.3390/antiox12030558.

[31]

Kaleem M, Shah AA, Usman S, Xu W, Alfarhan AH. Foliar application of calcium phosphate nanoparticles improves photosynthetic efficiency, nutrient uptake, and antioxidant capacity in Coriandrum sativum L. under salinity stress. ACS Omega. 2025;10:46393–409. https://doi.org/10.1021/acsomega.5c00987.

[32]

Kudla J, Batistič O, Hashimoto K. Calcium signals: The lead currency of plant information processing. Plant Cell, 2010, 22: 541-563

[33]

Kudla J, Becker D, Grill E, Hedrich R, Hippler M, Kummer U, et al. . Advances and current challenges in calcium signaling. New Phytol, 2018, 218: 414-431

[34]

Li Y, Hu J, Qi J, Zhao F, Liu J, Chen L, et al. . Improvement of leaf K+ retention is a shared mechanism behind CeO2 and Mn3O4 nanoparticles improved rapeseed salt tolerance. Stress Biol, 2022, 2: 46

[35]

Li L, Dong M, Tang K, Zhang H, Zeng N, Yang H, et al. . The effects of calcium fertilization on morphological and physio-biochemical characteristics in peanut seedlings under waterlogging stress. J Plant Nutr, 2023, 46: 2865-2881

[36]

Li K, Yu Y, Liu H, Yan S, Zhu W, Xie L, et al. . Unraveling the genetic mechanisms of waterlogging stress through the leaf metabolome of a sweet corn panel. BMC Plant Biol, 2025, 25: 1-14

[37]

Li Y, Qi J, Gao Q, He C, Gu J, Xie Z, et al. . Plants primed with CeO2 nanoparticles increased DNA methylation level to convey transgenerational salinity tolerance. Plant Nano Biol, 2025, 14 100214

[38]

Liang SM, Hashem A, Abd-Allah EF, Wu QS. Root-associated symbiotic fungi enhance waterlogging tolerance of peach seedlings by increasing flavonoids and activities and gene expression of antioxidant enzymes. Chem Biol Technol Agric, 2023, 10: 124

[39]

Liu C, Lan C, Li C, Li C, Huang J. Exogenous spermidine and calcium alleviate waterlogging stress in cherry tomato at the seedling stage. Sci Hortic, 2023, 307 111504

[40]

Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods, 2001, 25: 402-408

[41]

Lopez Del Egido L, Navarro-Miró D, Martinez-Heredia V, Toorop PE, Iannetta PP. A spectrophotometric assay for robust viability testing of seed batches using 2, 3, 5-triphenyl tetrazolium chloride: Using Hordeum vulgare L. as a model. Front Plant Sci. 2017;8:747. https://doi.org/10.3389/fpls.2017.00747.

[42]

Ma C, Pei ZQ, Bai X, Lu SH, Su M, Kang X, et al. . Exogenous melatonin and CaCl2 alleviate cold-induced oxidative stress and photosynthetic inhibition in cucumber seedlings. J Plant Growth Regul, 2023, 42: 3441-3458

[43]

Meng J, Zhang D, An S, Du Y, Huang X, Zhu K, et al. An apoplastic Lasiodiplodia theobromae effector triggers plant immunity through a lectin receptor-like kinase in peach. Plant Cell. 2026;38:koag011. https://doi.org/10.1093/plcell/koag011.

[44]

Mudasir M, Shahzad A. Decoding plant responses to waterlogging: from stress signals to molecular mechanisms and their future implications. Plant Mol Biol, 2025, 115: 78

[45]

Porra RJ, Thompson WA, Kriedemann PE. Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: Verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta (BBA)-Bioenergetics. 1989;975:384–94. https://doi.org/10.1016/S0005-2728(89)80347-0.

[46]

Pucciariello C, Perata P. New insights into reactive oxygen species and nitric oxide signalling under low oxygen in plants. Plant Cell Environ, 2017, 40: 473-482

[47]

Raza A, Li Y, Prakash CS, Hu Z. Panomics to manage combined abiotic stresses in plants. Trends Plant Sci, 2025, 30: 1079-1084

[48]

Renziehausen T, Chaudhury R, Hartman S, Mustroph A, Schmidt-Schippers RR. A mechanistic integration of hypoxia signaling with energy, redox, and hormonal cues. Plant Physiol. 2025;197:kiae596. https://doi.org/10.1093/plphys/kiae596.

[49]

Saleem S, Pan Y, Liu H, Kareem HA, Yang Y, Cheng Z. Calcium oxide nanoparticle and jasmonic acid interplay drives cucumber salt tolerance: Insights from mechanistic, histological, and molecular analyses. Plant Physiol Biochem, 2025, 230 110816

[50]

Sang Q, Kong F. Applications for single-cell and spatial transcriptomics in plant research. New Crops, 2024, 1 100025

[51]

Shen W, Zeng C, Sun J, Meng J, Yuan P, Bu F, et al. . PpHSP20-26, a small heat shock protein, confers enhanced autotoxicity stress tolerance in peach. Hortic Plant J, 2025, 11: 1012-1025

[52]

Sui J, Tian H, Ding Z, Kong X. Crop designs: The ideal root architecture for future crop breeding. New Crops, 2024, 1 100030

[53]

Ventura I, Brunello L, Iacopino S, Valeri MC, Novi G, Dornbusch T, et al. . Arabidopsis phenotyping reveals the importance of alcohol dehydrogenase and pyruvate decarboxylase for aerobic plant growth. Sci Rep, 2020, 10: 16669

[54]

Wang Z, Han Y, Luo S, Rong X, Song H, Jiang N, et al. . Calcium peroxide alleviates the waterlogging stress of rapeseed by improving root growth status in a rice-rape rotation field. Front Plant Sci, 2022, 13: 1048227

[55]

Wang L, Wang W, Liao K, Xu L, Xie D, Xie R, et al. . Survival mechanisms of plants under hypoxic stress: Physiological acclimation and molecular regulation. J Integr Plant Biol, 2025, 67: 440-454

[56]

Wu J, Chen S, Wang C, Lin W, Huang C, Fan C, et al. . Regulatory dynamics of the higher-plant PSI–LHCI supercomplex during state transitions. Mol Plant, 2023, 16: 1937-1950

[57]

Xu F, Cai H, Zhang X, Su M, Zhou H, Li X, et al. . Comparison of waterlogging tolerance of three peach rootstock seedlings based on physiological, anatomical and ultra-structural changes. Horticulturae, 2022, 8: 720

[58]

Xu X, Wang H, Qi X, Xu Q, Chen X. Waterlogging-induced increase in fermentation and related gene expression in the root of cucumber (Cucumis sativus L.). Sci Hortic. 2014;179:388–95. https://doi.org/10.1016/j.scienta.2014.10.001.

[59]

Yang P, Zhang C, Li H, Wang X, Zhou Y, Kyaw HWW, et al. . Nano-silica improves the emergence of pepper seeds and the growth of seedlings under waterlogging stress by reducing oxidative damage. BMC Plant Biol, 2025, 25: 1511

[60]

Yu WW, Chen QF, Liao K, Zhou DM, Yang YC, He M, et al. . The calcium-dependent protein kinase CPK16 regulates hypoxia-induced ROS production by phosphorylating the NADPH oxidase RBOHD in Arabidopsis. Plant Cell, 2024, 36: 3451-3466

[61]

Yuan LB, Dai YS, Xie LJ, Yu LJ, Zhou Y, Lai YX, et al. . Jasmonate regulates plant responses to postsubmergence reoxygenation through transcriptional activation of antioxidant synthesis. Plant Physiol, 2017, 173: 1864-1880

[62]

Yun P, Shabala S. Optimizing plant nutrient acquisition under hypoxia: Likely trade-offs, implications for breeders, and lessons from wetland species. J Exp Bot. 2026;erag093. https://doi.org/10.1093/jxb/erag093.

[63]

Zhang C, Song Y, Kudla J. Calcium signaling in crops. New Phytol, 2026, 249: 1644-1658

[64]

Zhang D, Shen X, Zhang H, Huang X, He H, Ye J, et al. Integrated transcriptomic and metabolic analyses reveal that ethylene enhances peach susceptibility to Lasiodiplodia theobromae-induced gummosis. Hortic Res. 2022;9:uhab019. https://doi.org/10.1093/hr/uhab019.

[65]

Zhao X, Lin S, Yu S, Zhang Y, Su L, Geng L, et al. . Exogenous calcium enhances the physiological status and photosynthetic capacity of rose under drought stress. Hortic Plant J, 2024, 10: 853-865

[66]

Zhao S, Chen QF, Chen L, Zhou Y, Liao K, Wang F, et al. . The plant-specific protein IQD22 interacts with calcium sensors to activate anaerobic respiration during hypoxia in Arabidopsis. Mol Plant, 2025, 18: 1330-1350

[67]

Zhu K, Feng Y, Huang Y, Zhang D, Ateeq M, Zheng X, et al. . β-Cyclocitric acid enhances drought tolerance in peach (Prunus persica) seedlings. Tree Physiol, 2023, 43: 1933-1949

[68]

Zhu K, Ateeq M, Wang X, Huang X, Yang J, Noor I, et al. . PpMATE49, a multidrug and toxic compound extrusion transporter, confers manganese toxicity tolerance in peach (Prunus persica). J Hazard Mater, 2025, 496 139270

[69]

Zhu W, Chen X, Gan Z, Zhu K, He H, Ashraf MA, et al. . Integrated molecular sensory profiling reveals the distinct aroma signatures of peach fruit types. Food Res Int, 2026, 237 119353

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