Research Progress in Molecular Response Mechanisms of Strawberry to High-Temperature Stress

doi:10.13560/j.cnki.biotech.bull.1985.2025-0913

Abstract

Abstract:

High-temperature stress is one of the main abiotic stresses leading to stunted growth, sharp yield reduction, and deterioration of fruit quality of strawberries in South China. Understanding the research status of the molecular response mechanisms of strawberry to high-temperature tolerance not only provides precise gene targets and theoretical support for the breeding of high-temperature-tolerant strawberry varieties, but also can guide the formulation of targeted cultivation and management measures such as sunshade cooling and spraying of stress-resistant regulators. These measures can effectively enhance the high-temperature resistance of strawberry plants, ensuring the stable annual output of the strawberry industry in South China and the improvement of the rate of high-quality fruits. This article reviews the latest research progress on the molecular response mechanisms of strawberry to high-temperature tolerance. Starting from the physiological effects of high-temperature stress on strawberries, the article systematically expounds on key molecular response pathways such as heat shock proteins, antioxidant systems, osmotic adjustment substances, and hormone signal transduction. Among them, the heat shock protein family can protect cell structures by maintaining protein homeostasis under high-temperature induction; in the antioxidant system, the activities of enzymes such as superoxide dismutase (SOD) and catalase (CAT) increase significantly, which work together to scavenge excessive reactive oxygen species (ROS) and reduce the damage of cell membrane lipid peroxidation. Osmotic adjustment substances enhance water retention capacity by increasing cell osmotic pressure. In hormone signal transduction, abscisic acid (ABA) and salicylic acid (SA) construct a multi-level heat tolerance regulatory network by regulating the expression of downstream stress-resistant genes. In addition, it also introduces the application of transcriptomics, proteomics, and metabolomics in the research on plant high-temperature tolerance, providing technical support for the analysis of the strawberry heat tolerance mechanism. These research results provide a theoretical basis for in-depth understanding of the molecular mechanisms underlying strawberry heat tolerance and stress-resistant cultivation, and also offer resources for accelerating molecular design breeding of high-temperature-tolerant strawberries.

Key words: strawberry, high-temperature stress, heat shock protein, antioxidant system, osmotic adjustment substances, plant hormones, signal transduction, omics

WU Xia-ming, LIU Chuan-he, HE Han, ZHOU Chen-ping, YANG Min, KUANG Rui-bin, XU Ze, WEI Yue-rong. Research Progress in Molecular Response Mechanisms of Strawberry to High-Temperature Stress[J]. Biotechnology Bulletin, 2026, 42(6): 175-185.

Figures/Tables 2

Fig. 1 Effects of high-temperature stress on strawberry growth and developmentROS: Reactive oxygen species. ↓: Decrease. ↑: Increase. →: Promote

Fig. 2 Molecular response mechanisms in strawberries under high temperature stressHigh temperature first triggers signal activation through changes in membrane fluidity. On one hand, it induces the activation of HSFs family transcription factors, initiating the synergistic expression of heat shock proteins (HSPs) such as HSP70, HSP90, and sHsps to maintain protein stability and photosynthetic system function. On the other hand, it activates the MAPK signaling pathway, which interacts with hormones including IAA, CTK, GA, ABA, SA, JA, and BR to participate in signal transduction and regulate downstream stress responses. Meanwhile, antioxidant enzymes such as SOD, CAT, POD, and APX cooperate with the ROS module to scavenge reactive oxygen species, reducing oxidative damage caused by MDA accumulation. Additionally, it accumulates osmoprotectants such as proline to maintain cellular osmotic balance. These multiple pathways work synergistically to resist high-temperature damage and ensure the normal growth and development of the plant

References 78

[1]	Langer SE, Oviedo NC, Marina M, et al. Effects of heat treatment on enzyme activity and expression of key genes controlling cell wall remodeling in strawberry fruit [J]. Plant Physiol Biochem, 2018, 130: 334-344.
[2]	Fan Z, Whitaker VM. Genomic signatures of strawberry domestication and diversification [J]. Plant Cell, 2024, 36(5): 1622-1636.
[3]	高清山. 我国草莓产业的现状分析及发展趋势研究 [J]. 果树资源学报, 2024, 5(5): 79-82, 87.
	Gao QS. Status analysis and development trend research of strawberry industry in China [J]. J Fruit Resour, 2024, 5(5): 79-82, 87.
[4]	武冲, 姜莉莉, 宗晓娟, 等. 中国草莓育种研究进展 [J]. 落叶果树, 2022, 54(2): 28-30.
	Wu C, Jiang LL, Zong XJ, et al. Advances in strawberry breeding in China [J]. Deciduous Fruits, 2022, 54(2): 28-30.
[5]	李薇, 王哲, 刘妍, 等. 我国草莓产业发展新形势、存在的问题及建议 [J]. 中国南方果树, 2025, 54(2): 240-248.
	Li W, Wang Z, Liu Y, et al. New situation, problems and recommendations of the development of strawberry industry in China [J]. South China Fruits, 2025, 54(2): 240-248.
[6]	Matthews HD, Wynes S. Current global efforts are insufficient to limit warming to 1.5 ℃[J]. Science, 2022, 376(6600): 1404-1409.
[7]	Wang SY, Camp MJ. Temperatures after bloom affect plant growth and fruit quality of strawberry [J]. Sci Hortic, 2000, 85(3): 183-199.
[8]	Himali NB, Kithsiri BD, BruceTomkins, et al. Impacts of elevated carbon dioxide and temperature on physicochemical and nutrient properties in strawberries [J]. J Hortic Sci Res, 2017, 1(1): 19-29.
[9]	Bacelar E, Pinto T, Anjos R, et al. Impacts of climate change and mitigation strategies for some abiotic and biotic constraints influencing fruit growth and quality [J]. Plants, 2024, 13(14): 1942.
[10]	万群. 芸薹素内酯对高温胁迫下草莓幼苗生化物质的影响 [J]. 中国南方果树, 2016, 45(3): 117-121, 125.
	Wan Q. Effects of brassinolide on biochemical substances of strawberry seedlings under high temperature stress[J]. South China Fruits, 2016, 45(3): 117-121, 125.
[11]	王朋. 高温处理对结果期草莓叶片衰老特征的影响 [J]. 农业与技术, 2018, 38(6): 44.
	Wang P. Effect of high temperature treatment on senescence characteristics of strawberry leaves at fruiting stage[J]. Agric Technol, 2018, 38(6): 44.
[12]	López ME, Denoyes B, Bucher E. Epigenomic and transcriptomic persistence of heat stress memory in strawberry (Fragaria vesca) [J]. BMC Plant Biol, 2024, 24(1): 405.
[13]	Wang H, Zhang SH, Wang ZD, et al. Resistance index and browning mechanism of apple peel under high temperature stress [J]. Hortic Plant J, 2024, 10(2): 305-317.
[14]	孙永江, 王琪, 邵琪雯, 等. 高温胁迫对植物光合作用的影响研究进展 [J]. 植物学报, 2023, 58(3): 486-498.
	Sun YJ, Wang Q, Shao QW, et al. Research advances on the effect of high temperature stress on plant photosynthesis[J]. Bull Bot, 2023, 58(3): 486-498.
[15]	Arief MAA, Kim H, Kurniawan H, et al. Chlorophyll fluorescence imaging for early detection of drought and heat stress in strawberry plants [J]. Plants, 2023, 12(6): 1387.
[16]	鲁雪利, 于海业, 赵红星, 等. 高、低温胁迫对雾培嫁接苗根系生长发育的影响 [J]. 北方园艺, 2016(8): 6-10.
	Lu XL, Yu HY, Zhao HX, et al. Effect of high and low temperature stress on root growth and development of fog grafted seedling [J]. North Hortic, 2016(8): 6-10.
[17]	Arndal AT M F. Fine root growth and vertical distribution in response to elevated CO₂, warming and drought in a mixed heathland-grassland [J]. Ecosystems, 2018, 21(1): 15-30.
[18]	Amin I, Rasool S, Mir MA, et al. Ion homeostasis for salinity tolerance in plants: a molecular approach [J]. Physiol Plant, 2021, 171(4): 578-594.
[19]	Osman M, Qaryouti M, Alharbi S, et al. Impact of CO₂ enrichment on growth, yield and fruit quality of F1 hybrid strawberry grown under controlled greenhouse condition [J]. Horticulturae, 2024, 10(9): 941.
[20]	Ledesma NA, Nakata M, Sugiyama N. Effect of high temperature stress on the reproductive growth of strawberry cvs. 'Nyoho' and 'Toyonoka' [J]. Sci Hortic, 2008, 116(2): 186-193.
[21]	Karapatzak EK, Wagstaffe A, Hadley P, et al. High‐temperature‐induced reductions in cropping in everbearing strawberries (Fragaria × ananassa) are associated with reduced pollen performance[J]. Ann Appl Biol, 2012, 161(3): 255-265.
[22]	Kadir S, Sidhu G, Al-Khatib K. Strawberry (Fragaria × Ananassa duch.) growth and productivity as affected by temperature [J]. HortScience, 2006, 41(6): 1423-1430.
[23]	Menzel CM. Temperature has a greater effect on fruit growth than defoliation or fruit thinning in strawberries in the subtropics [J]. Agriculture, 2019, 9(6): 127.
[24]	Manafi H, Baninasab B, Gholami M, et al. Nitric oxide induced thermotolerance in strawberry plants by activation of antioxidant systems and transcriptional regulation of heat shock proteins [J]. J Hortic Sci Biotechnol, 2021, 96(6): 783-796.
[25]	Ergİn S, Gülen H, Kesİcİ M, et al. Effects of high temperature stress on enzymatic and nonenzymaticantioxidants and proteins in strawberry plants [J]. Turk J Agric For, 2016, 40: 908-917.
[26]	Lu HF, Hu YY, Wang CY, et al. Effects of high temperature and drought stress on the expression of gene encoding enzymes and the activity of key enzymes involved in starch biosynthesis in wheat grains [J]. Front Plant Sci, 2019, 10: 1414.
[27]	Wang WX, Vinocur B, Shoseyov O, et al. Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response [J]. Trends Plant Sci, 2004, 9(5): 244-252.
[28]	Hasanuzzaman M, Nahar K, Alam MM, et al. Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants [J]. Int J Mol Sci, 2013, 14(5): 9643-9684.
[29]	Liao WY, Lin LF, Jheng JL, et al. Identification of heat shock transcription factor genes involved in thermotolerance of octoploid cultivated strawberry [J]. Int J Mol Sci, 2016, 17(12): 2130.
[30]	Zhao P, Wang DD, Wang RQ, et al. Genome-wide analysis of the potato Hsp20 gene family: identification, genomic organization and expression profiles in response to heat stress [J]. BMC Genomics, 2018, 19(1): 61.
[31]	Hahn A, Bublak D, Schleiff E, et al. Crosstalk between Hsp90 and Hsp70 chaperones and heat stress transcription factors in tomato[J]. Plant Cell, 2011, 23(2): 741-755.
[32]	Kesici M, Ipek A, Ersoy F, et al. Genotype-dependent gene expression in strawberry (Fragaria × Ananassa) plants under high temperature stress [J]. Biochem Genet, 2020, 58(6): 848-866.
[33]	Medina-Escobar N, Cárdenas J, Muñoz-Blanco J, et al. Cloning and molecular characterization of a strawberry fruit ripening-related cDNA corresponding a mRNA for a low-molecular-weight heat-shock protein [J]. Plant Mol Biol, 1998, 36(1): 33-42.
[34]	Ullah I, Toor MD, Ali Yerlikaya B, et al. High-temperature stress in strawberry: understanding physiological, biochemical and molecular responses [J]. Planta, 2024, 260(5): 118.
[35]	Manafi H, Baninasab B, Gholami M, et al. Exogenous melatonin alleviates heat‐induced oxidative damage in strawberry (Fragaria × ananassa duch. cv. ventana) plant [J]. J Plant Growth Regul, 2022, 41(1): 52-64.
[36]	吴夏明, 杨敏, 周陈平, 等. 不同浓度褪黑素处理对高温胁迫下草莓苗生理特性的影响 [J]. 生物技术通报, 2025, 41(3): 181-189.
	Wu XM, Yang M, Zhou CP, et al. Effects of different concentrations of melatonin on the physiological characteristics of strawberry seedlings under high-temperature stress [J]. Biotechnol Bull, 2025, 41(3): 181-189.
[37]	Menzel CM. Temperatures above 30 ℃ decrease leaf growth in strawberry under global warming [J]. J Hortic Sci Biotechnol, 2024, 99(5): 507-530.
[38]	Lv JH, Zheng T, Song ZL, et al. Strawberry proteome responses to controlled hot and cold stress partly mimic post-harvest storage temperature effects on fruit quality [J]. Front Nutr, 2021, 8: 812666.
[39]	Fu ET, Zhang YZ, Li HL, et al. Chitosan reduces damages of strawberry seedlings under high-temperature and high-light stress [J]. Agronomy, 2023, 13(2): 517.
[40]	Hayat S, Hayat Q, Alyemeni MN, et al. Role of proline under changing environments: a review [J]. Plant Signal Behav, 2012, 7(11): 1456-1466.
[41]	Paliwal A, Verma A, Tiwari H, et al. Effect and importance of compatible solutes in plant growth promotion under different stress conditions [M]//Compatible Solutes Engineering for Crop Plants Facing Climate Change. Cham: Springer International Publishing, 2021: 223-239.
[42]	Bolen DW, Baskakov IV. The osmophobic effect: natural selection of a thermodynamic force in protein folding [J]. J Mol Biol, 2001, 310(5): 955-963.
[43]	Hoque MA, Okuma E, Nasrin Akhter Banu M, et al. Exogenous proline mitigates the detrimental effects of salt stress more than exogenous betaine by increasing antioxidant enzyme activities [J]. J Plant Physiol, 2007, 164(5): 553-561.
[44]	Liu YH, Offler CE, Ruan YL. Regulation of fruit and seed response to heat and drought by sugars as nutrients and signals [J]. Front Plant Sci, 2013, 4: 282.
[45]	Wang YH, Yan ZM, Tang WH, et al. Impact of chitosan, sucrose, glucose, and fructose on the postharvest decay, quality, enzyme activity, and defense-related gene expression of strawberries [J]. Horticulturae, 2021, 7(12): 518.
[46]	Sehar Z, Gautam H, Masood A, et al. Ethylene- and proline-dependent regulation of antioxidant enzymes to mitigate heat stress and boost photosynthetic efficacy in wheat plants [J]. J Plant Growth Regul, 2023, 42(5): 2683-2697.
[47]	Ahmad P, Abdel Latef AA, Hashem A, et al. Nitric oxide mitigates salt stress by regulating levels of osmolytes and antioxidant enzymes in chickpea [J]. Front Plant Sci, 2016, 7: 347.
[48]	Angon PB, Das A, Roy AR, et al. Plant development and heat stress: role of exogenous nutrients and phytohormones in thermotolerance [J]. Discov Plants, 2024, 1(1): 17.
[49]	Chen Q, Long Y, Yang M, et al. FaPKc2.2 negatively modulates strawberry fruit ripening by reprograming the carbon metabolic pathway [J]. Sci Hortic, 2022, 301: 111114.
[50]	Guo LL, Lu SX, Liu T, et al. Genome-wide identification and abiotic stress response analysis of PP2C gene family in woodland and pineapple strawberries [J]. Int J Mol Sci, 2023, 24(4): 4049.
[51]	Li DD, Mou WS, Luo ZS, et al. Developmental and stress regulation on expression of a novel miRNA, Fan-miR73, and its target ABI5 in strawberry [J]. Sci Rep, 2016, 6: 28385.
[52]	Han Y, Dang RH, Li JX, et al. Sucrose nonfermenting1-related protein kinase2.6, an ortholog of open stomata1, is a negative regulator of strawberry fruit development and ripening [J]. Plant Physiol, 2015, 167(3): 915-930.
[53]	苏建波. 水杨酸对草莓幼苗抗热性的影响 [J]. 安徽农业科学, 2015, 43(12): 64-65.
	Su JB. Effects of salicylic acid(SA) on heat resistance of strawberry seedlings [J]. J Anhui Agric Sci, 2015, 43(12): 64-65.
[54]	Coltro S, Broetto L, Rotilli MCC, et al. Heat shock and salicylic acid on postharvest preservation of organic strawberries [J]. Rev Ceres, 2014, 61(3): 306-312.
[55]	Niazi AR, Ghanbari F, Erfani-Moghadam J. Simultaneous effects of hot water treatment with calcium and salicylic acid on shelf life and qualitative characteristics of strawberry during refrigerated storage [J]. J Food Process Preserv, 2021, 45(1): e15005.
[56]	Snyman M, Cronjé MJ. Modulation of heat shock factors accompanies salicylic acid-mediated potentiation of Hsp70 in tomato seedlings [J]. J Exp Bot, 2008, 59(8): 2125-2132.
[57]	Samakovli D, Roka L, Dimopoulou A, et al. HSP90 affects root growth in Arabidopsis by regulating the polar distribution of PIN1 [J]. New Phytol, 2021, 231(5): 1814-1831.
[58]	Zheng T, Lv JH, Sadeghnezhad E, et al. Transcriptomic and metabolomic profiling of strawberry during postharvest cooling and heat storage [J]. Front Plant Sci, 2022, 13: 1009747.
[59]	Hogan JD, Murray EE, Harrison MA. Ethylene production as an indicator of stress conditions in hydroponically-grown strawberries [J]. Sci Hortic, 2006, 110(4): 311-318.
[60]	Yosefi A, Mozafari AA, Javadi T. Jasmonic acid improved in vitro strawberry (Fragaria × ananassa Duch.) resistance to PEG-induced water stress [J]. Plant Cell Tissue Organ Cult 2020, 142(3): 549-558.
[61]	忻雅, 张青, 裘劼人, 等. 油菜素内酯对夏季草莓育苗素质及耐逆性的影响 [J]. 浙江农业学报, 2015, 27(10): 1735-1738.
	Xin Y, Zhang Q, Qiu JR, et al. Effects of brassinolide on quality and stress tolerance of summer strawberry seedlings [J]. Acta Agric Zhejiangensis, 2015, 27(10): 1735-1738.
[62]	Aghdam O A, Hajilou J, Bolandnazar S, et al. Effect of 24-Epi brassinolide on some biochemical characteristics of parus and gaviota strawberry cultivars under heat stress conditions[J]. YYU J Agr Sci, 2020, 30(2): 429-437.
[63]	Shi HT, Tan DX, Reiter RJ, et al. Melatonin induces class A1 heat-shock factors (HSFA1s) and their possible involvement of thermotolerance in Arabidopsis [J]. J Pineal Res, 2015, 58(3): 335-342.
[64]	Xia H, Zhou YJ, Deng HH, et al. Melatonin improves heat tolerance in Actinidia deliciosa via carotenoid biosynthesis and heat shock proteins expression [J]. Physiol Plant, 2021, 172(3): 1582-1593.
[65]	Li Z, Li ZR, Ji YL, et al. The heat shock factor 20-HSF4-cellulose synthase A2 module regulates heat stress tolerance in maize [J]. Plant Cell, 2024, 36(7): 2652-2667.
[66]	张圣美, 裘波音, 徐谦, 等. 外源钙离子对高温胁迫下草莓幼苗影响的转录组分析[J]. 分子植物育种, 2024, 22(11): 3525-3532.
	Zhang SM, Qiu BY, Xu Q, et al. Transcriptome analysis of the effect of exogenous calcium ions on strawberry seedlings under high temperature stress[J]. Mol Plant Breeding, 2024, 22(11): 3525-3532.
[67]	Zhang L, Wang L, Zeng X, et al. Comparative transcriptome analysis reveals fruit discoloration mechanisms in postharvest strawberries in response to high ambient temperature[J]. Food Chem X, 2019, 2: 100025.
[68]	Zhang H, Kang H, Su C, et al. Genome-wide identification and expression profile analysis of the NAC transcription factor family during abiotic and biotic stress in woodland strawberry[J]. PLoS One, 2018, 13(6): e0197892.
[69]	Garrido-Gala J, Higuera J J, Rodríguez-Franco A, et al. A comprehensive study of the WRKY transcription factor family in strawberry[J]. Plants, 2022, 11(12): 1585.
[70]	Jiang CH, Bi YK, Mo JB, et al. Proteome and transcriptome reveal the involvement of heat shock proteins and antioxidant system in thermotolerance of Clematis florida [J]. Sci Rep, 2020, 10(1): 8883.
[71]	Luo D, Ding Q, Ma XX, et al. Proteomic and physiological responses of contrasting two different heat-resistant orchardgrass genotypes to heat stress [J]. Int J Biol Macromol, 2023, 245: 125463.
[72]	Wang BF, Xue P, Zhang YX, et al. OsCPK12 phosphorylates OsCATA and OsCATC to regulate H₂O₂ homeostasis and improve oxidative stress tolerance in rice [J]. Plant Commun, 2024, 5(3): 100780.
[73]	Hu Z, Li J, Ding S, et al. The protein kinase CPK28 phosphorylates ascorbate peroxidase and enhances thermotolerance in tomato[J]. Plant Physiol, 2021, 186(2): 1302-1317.
[74]	Song J, CampbellPalmer L, Vinqvist-Tymchuk M, et al. Proteomic changes in antioxidant system in strawberry during ripening [J]. Front Plant Sci, 2020, 11: 594156.
[75]	Muneer S, Park YG, Kim S, et al. Foliar or subirrigation silicon supply mitigates high temperature stress in strawberry by maintaining photosynthetic and stress-responsive proteins [J]. J Plant Growth Regul, 2017, 36(4): 836-845.
[76]	Zhang HN, Meng XZ, Liu R, et al. Heat shock factor ZmHsf17 positively regulates phosphatidic acid phosphohydrolase ZmPAH1 and enhances maize thermotolerance [J]. J Exp Bot, 2025, 76(2): 493-512.
[77]	Balasooriya B, Dassanayake K, Ajlouni S. High temperature effects on strawberry fruit quality and antioxidant contents[C]//International Conference on Postharvest and Quality Management of Horticultural Products of Interest for Tropical Regions 1278, 2017: 225-234.
[78]	Cordenunsi BR, Genovese MI, Oliveira do Nascimento JR, et al. Effects of temperature on the chemical composition and antioxidant activity of three strawberry cultivars [J]. Food Chem, 2005, 91(1): 113-121.