Cold stress tolerance in pepper: role of transcription factors in molecular signaling and adaptive responses

Abstract

Pepper (Capsicum annum L.) is an important horticultural commodity known for its nutritional and medicinal properties. However, cold stress severely hinders its growth, development, and productivity, posing a major challenge to stable production in many cultivation regions. Cold stress disrupts membrane integrity and impairs photosynthesis, cellular homeostasis, and osmotic balance, while also promoting excessive accumulation of reactive oxygen species (ROS), leading to oxidative damage and metabolic imbalance. To mitigate these adverse effects, pepper plants initiate complex molecular signal transduction pathways, which are controlled by transcription factors (TFs) that regulate the expression of stress-responsive genes. Major TF families involved in cold stress responses include MYB, WRKY, Cys2/His2-type zinc finger protein (C2H2), NAC, Phytochrome-Interacting Factor (PIF), C-repeat Binding Factor/Dehydration-Responsive Element Binding protein (CBF/DREB), and bHLH. These genes are responsible mainly for perceiving and transmitting cold signals in pepper via abscisic acid (ABA)-mediated and ABA-independent pathways, calcium–mitogen-activated protein kinase (MAPK) cascades, ROS signaling, and hormone regulation. Functional investigations have revealed that multiple TFs, such as CaNAC064, SNF1-Related Protein Kinase 2.4 (CaSnRK2.4), CaNAC035, CaCBF1B, CaWRKY40, and CaMYB80, are essential positive regulators of cold tolerance, resulting in improved scavenging of ROS, osmotic balance, and membrane integrity. Recent advances in genomics and transgenic strategies, such as CRISPR/Cas-based genome editing, has further elucidated these TF-mediated regulatory pathways, providing potential approaches for developing cold-tolerant pepper cultivars. By elucidating the molecular mechanisms underlying cold stress responses, it offers key perspectives for the breeding of climate-tolerant pepper varieties to ensure sustainable agricultural production.

Keywords

Pepper / Cold Stress / Transcription Factors / Signaling / Response

References

[1] Abe H, Yamaguchi-Shinozaki K, Urao T, Iwasaki T, Hosokawa D, Shinozaki K. Role of Arabidopsis MYC and MYB homologs in drought- and abscisic acid-regulated gene expression. Plant Cell, 1997, 9: 1859-1868

[2] Adhikari L, Baral R, Paudel D, Min D, Makaju SO, Poudel HP, et al.. Cold stress in plants: Strategies to improve cold tolerance in forage species. Plant Stress, 2022, 4 ArticleID: 100081

[3] Agarwal PK, Jha B. Transcription factors in plants and ABA-dependent and independent abiotic stress signaling. Biol Plant, 2010, 54: 201-212

[4] Aghdam MSMukherjee S, Corpas FJ. Melatonin language in postharvest life of horticultural crops. Melatonin: role in plant signaling, growth and stress tolerance, 2023, Cham, Springer173215

[5] Altaf MA, Hao Y, Shu H, Jin W, Chen C, Li L, et al.. Melatonin mitigates cold-induced damage to pepper seedlings by promoting redox homeostasis and regulating antioxidant profiling. Hortic Plant J, 2024, 10: 532-544

[6] Anifowoshe YO, Lozada D, Sanogo S, Djaman K. Water management in chile peppers and plant susceptibility to phytophthora capsici and development of phytophthora blight: A review. Agronomy, 2025, 15: 2819

[7] Banjare R, Nidhi N, Sood A. Physiological aspects of fl owering, fruit setting, fruit development and fruit drop,regulation and their manipulation: a review. Int J Environ Clim Chang. 2023;13:205–24.

[8] Bhandari K, Siddique KHM, Turner NC, Kaur J, Singh S, Agrawal SK, et al.. Heat stress at reproductive stage disrupts leaf carbohydrate metabolism, impairs reproductive function, and severely reduces seed yield in lentil. J Crop Improv, 2016, 30: 118-151

[9] Bhutia LK, VK K, Meetei NG T, Dolma N. Effects of climate change on growth and development of chilli. Agrotechnology. 2018;7:2. https://doi.org/10.4172/2168-9881.1000180.

[10] Bulle M, Rahman MM, Islam MR, Abbagani S. Strategies to develop climate-resilient chili peppers: transcription factor optimization through genome editing. Planta, 2025, 262 ArticleID: 30

[11] Busk PK, Pagès M. Regulation of abscisic acid-induced transcription. Plant Mol Biol, 1998, 37: 425-435

[12] Chaffai R, Ganesan M, Cherif AChaffai R, Ganesan M, Cherif A. Transcriptional regulation of gene expression in plant abiotic stress response. Plant adaptation to abiotic stress: from signaling pathways and microbiomes to molecular mechanisms, 2024, Singapore, Springer Nature303343

[13] Chen Z, Tang D, Ni J, Li P, Wang L, Zhou J, et al.. Development of genic KASP SNP markers from RNA-Seq data for map-based cloning and marker-assisted selection in maize. BMC Plant Biol, 2021, 21 ArticleID: 157

[14] Chhapekar SS, Jaiswal V, Ahmad I, Gaur R, Ramchiary N. Progress and prospects in Capsicum breeding for biotic and abiotic Stresses. In: VatsS, editor. Biotic and abiotic stress tolerance in plants. Singapore: Springer; 2018. p. 279–322. https://doi.org/10.1007/978-981-10-9029-5_11.

[15] Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR. Abscisic acid: Emergence of a core signaling network. Annu Rev Plant Biol, 2010, 61: 651-679

[16] Davis M, Davis AS. Effects of heat treatment and chilling duration on camas growth and development. Sci Hortic, 2021, 282 ArticleID: 110048

[17] Diao P, Chen C, Zhang Y, Meng Q, Lv W, Ma N. The role of NAC transcription factor in plant cold response. Plant Signal Behav, 2020, 15: 1785668

[18] Ding Y, Shi Y, Yang S. Advances and challenges in uncovering cold tolerance regulatory mechanisms in plants. New Phytol, 2019, 222: 1690-1704

[19] Feng Y, Li Z, Kong X, Khan A, Ullah N, Zhang X, et al.. Plant coping with cold stress: Molecular and physiological adaptive mechanisms with future perspectives. Cells, 2025, 14: 110

[20] Fowler S, Thomashow MF. Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell, 2002, 14: 1675-1690

[21] Gao C, Mumtaz MA, Zhou Y, Yang Z, Shu H, Zhu J, et al.. Integrated transcriptomic and metabolomic analyses of cold-tolerant and cold-sensitive pepper species reveal key genes and essential metabolic pathways involved in response to cold stress. Int J Mol Sci, 2022, 23: 6683

[22] Ge W, Luo M, Sun H, Wei B, Zhou X, Zhou Q, et al.. The CaMYB340 transcription factor induces chilling injury in post-harvest bell pepper by inhibiting fatty acid desaturation. Plant J, 2022, 111: 800-818

[23] Guan YL, Hwarari D, Mateko KH, Baseer A, Cao YW, Movahedi A, et al.. Low temperature stress-induced perception and molecular signaling pathways in plants. Environ Exp Bot, 2023, 207 ArticleID: 105190

[24] Hou XM, Zhang HF, Liu SY, Wang XK, Zhang YM, Meng YC, et al.. The NAC transcription factor CaNAC064 is a regulator of cold stress tolerance in peppers. Plant Sci, 2020, 291 ArticleID: 110346

[25] Hussain MA, Luo D, Zeng L, Ding X, Cheng Y, Zou X, et al.. Genome-wide transcriptome profiling revealed biological macromolecules respond to low temperature stress in Brassica napus L. Front Plant Sci, 2022, 13: 1050995

[26] Hwarari D, Guan Y, Ahmad B, Movahedi A, Min T, Hao Z, et al.. ICE-CBF-COR signaling cascade and its regulation in plants responding to cold stress. Int J Mol Sci, 2022, 23: 1549

[27] Jakutis G, Stainier DYR. Genotype–phenotype relationships in the context of transcriptional adaptation and genetic robustness. Annu Rev Genet, 2021, 55: 71-91

[28] Javed T, Shabbir R, Ali A, Afzal I, Zaheer U, Gao SJ. Transcription factors in plant stress responses: challenges and potential for sugarcane improvement. Plants (Basel), 2020, 9 ArticleID: 491

[29] Ji L, Li P, Su Z, Li M, Guo S. Cold-tolerant introgression line construction and low-temperature stress response analysis for bell pepper. Plant Signal Behav, 2020, 15: 1773097

[30] John Martin JJ, Song Y, Hou M, Zhou L, Liu X, Li X, et al.. Multi-omics approaches in oil palm research: A comprehensive review of metabolomics, proteomics, and transcriptomics based on low-temperature stress. Int J Mol Sci, 2024, 25: 7695

[31] Jones IR. Three-dimensional epigenomic characterization of human brain development [doctoral dissertation]. San Francisco: University of California; 2025. https://orcid.org/0009-0001-2227-9618.

[32] Kang H, Thomas HR, Xia X, Shi H, Zhang L, Hong J, et al.. An integrative overview of cold response and regulatory pathways in horticultural crops. J Integr Plant Biol, 2025, 67: 1028-1059

[33] Kang WH, Kim S, Lee HA, Choi D, Yeom SI. Genome-wide analysis of Dof transcription factors reveals functional characteristics during development and response to biotic stresses in pepper. Sci Rep, 2016, 6 ArticleID: 33332

[34] Kaya C. Molecular crosstalk of transcription factors and hormones in drought tolerance genes in plants. Turk J Bot. 2025;49:145–64. https://doi.org/10.55730/1300-008X.2852.

[35] Kaya C, Uğurlar F, Adamakis IS. Molecular mechanisms of CBL-CIPK signaling pathway in plant abiotic stress tolerance and hormone crosstalk. Int J Mol Sci, 2024, 25: 5043

[36] Khaitov B, Umurzokov M, Cho KM, Lee YJ, Park KW, Sung J. Importance and production of chilli pepper; heat tolerance and efficient nutrient use under climate change conditions. Korean J Agric Sci, 2019, 46: 769-779

[37] Kim TH, Böhmer M, Hu H, Nishimura N, Schroeder JI. Guard cell signal transduction network: Advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu Rev Plant Biol, 2010, 61: 561-591

[38] Kizis D, Pagès M. Maize DRE-binding proteins DBF1 and DBF2 are involved in rab17 regulation through the drought-responsive element in an ABA-dependent pathway. Plant J, 2002, 30: 679-689

[39] Kong XM, Zhou Q, Zhou X, Wei BD, Ji SJ. Transcription factor CaNAC1 regulates low-temperature-induced phospholipid degradation in green bell pepper. J Exp Bot, 2020, 71: 1078-1091

[40] Kumari K, Gusain S, Joshi R. Engineering cold resilience: Implementing gene editing tools for plant cold stress tolerance. Planta, 2024, 261: 2

[41] Li C, Ng CKY, Fan LM. MYB transcription factors, active players in abiotic stress signaling. Environ Exp Bot, 2015, 114: 80-91

[42] Li C, Pan Y, Cui J, Lu X, Yu W. Mechanism of ABA in plants exposed to cold stress. Agronomy, 2025, 15: 403

[43] Li J, Yang P, Fu H, Li J, Wang Y, Zhu K, et al.. Transcriptome analysis reveals key regulatory networks and genes involved in the acquisition of cold stress memory in pepper seedlings. BMC Plant Biol, 2024, 24: 959

[44] Li Q, Zhang H, Yang Y, Tang K, Yang Y, Ouyang W, et al.. Genome-wide identification of NAC family genes and their expression analyses in response to osmotic stress in Cannabis sativa L. Int J Mol Sci, 2024, 25: 9466

[45] Li Y, Yang Z, Zhang Y, Guo J, Liu L, Wang C, et al.. The roles of HD-ZIP proteins in plant abiotic stress tolerance. Front Plant Sci, 2022, 13: 1027071

[46] Li ZY, Ma N, Zhang FJ, Li LZ, Li HJ, Wang XF, et al.. Functions of phytochrome interacting factors (PIFs) in adapting plants to biotic and abiotic stresses. Int J Mol Sci, 2024, 25: 2198

[47] Liu HY, Kao PH, Baiya S, Kao CF. A multi-layered systems biology framework reveals dual-phased regulators and hormonal crosstalk underlying soybean cold tolerance. Plant Cell Rep, 2025, 44: 263

[48] Liu J, Osbourn A, Ma P. MYB transcription factors as regulators of phenylpropanoid metabolism in plants. Mol Plant, 2015, 8: 689-708

[49] Liu S, Xing M, Yin X. MAPK regulates secondary metabolism and abiotic stress in horticultural and medicinal plants. Hortic Res. 2025b;13:uhaf350. https://doi.org/10.1093/hr/uhaf350.

[50] Liu X, Zhou Y, Xiao J, Bao F. Effects of chilling on the structure, function and development of chloroplasts. Front Plant Sci, 2018, 9: 1715

[51] Liu Y, Li X, Li K, Liu H, Lin C. Multiple bHLH proteins form heterodimers to mediate CRY2-dependent regulation of flowering-time in Arabidopsis. PLoS Genet, 2013, 9 ArticleID: e1003861

[52] Liu Y, Tang Y, Tan X, Ding W. NtRNF217, encoding a putative RBR E3 ligase protein of Nicotiana tabacum, plays an important role in the regulation of resistance to Ralstonia solanacearum infection. Int J Mol Sci, 2021, 22: 5507

[53] Liu Y, Zhao C, Tang X, Wang L, Guo R. Transcriptomic and metabolomic insights into ABA-related genes in Cerasus humilis under drought stress. Int J Mol Sci, 2024, 25 ArticleID: 7635

[54] Lukatkin, AS. Contribution of oxidative stress to the development of cold-induced damage to leaves of chilling-sensitive plants: 3. Injury of cell membranes by chilling temperatures. Russ J Plant Physiol. 2003;50:243–6. https://doi.org/10.1023/A:1022985500733.

[55] Ma J, Wang LY, Dai JX, Wang Y, Lin D. The NAC-type transcription factor CaNAC46 regulates the salt and drought tolerance of transgenic Arabidopsis thaliana. BMC Plant Biol, 2021, 21 ArticleID: 11

[56] Ma S, Zhang Y. Profiling chromatin regulatory landscape: insights into the development of ChIP-seq and ATAC-seq. Mol Cells, 2020, 1 ArticleID: 9

[57] Ma X, Gai WX, Li Y, Yu YN, Ali M, Gong ZH. The CBL-interacting protein kinase CaCIPK13 positively regulates defence mechanisms against cold stress in pepper. J Exp Bot, 2022, 73: 1655-1667

[58] Ma X, Yu YN, Jia JH, Li QH, Gong ZH. The pepper MYB transcription factor CaMYB306 accelerates fruit coloration and negatively regulates cold resistance. Sci Hortic, 2022, 295 ArticleID: 110892

[59] Manasa SL, Panigrahy M, Panigrahi KCS, Rout GR. Overview of cold stress regulation in plants. Bot Rev, 2022, 88: 359-387

[60] Mercado JA, Reid MS, Valpuesta V, Quesada MA. Metabolic changes and susceptibility to chilling stress in Capsicum annuum plants grown at suboptimal temperature. Aust J Plant Physiol, 1998, 24: 759-767

[61] Nakashima K, Ito Y, Yamaguchi-Shinozaki K. Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol, 2009, 149: 88-95

[62] Orvar BL, Sangwan V, Omann F, Dhindsa RS. Early steps in cold sensing by plant cells: The role of actin cytoskeleton and membrane fluidity. Plant J, 2000, 23: 785-794

[63] Ou L, Wei G, Zhang Z, Dai X, Zou X. Effects of low temperature and low irradiance on the physiological characteristics and related gene expression of different pepper species. Photosynthetica, 2015, 53: 85-94

[64] Pandey H, Misra V, Mall AK, Sharma A, Edwin Hillary V, Ceasar SA. Enhancing sugar crop resilience to abiotic stress using CRISPR/Cas tools. Sugar Tech, 2025, 27: 985-1002

[65] Peng C, Hua W, Liu J. Unraveling the signaling pathways of plant cold stress: Current insights and future directions. Front Plant Sci, 2025, 16: 1666852

[66] Polowick PL, Sawhney VK. Temperature effects on male fertility and flower and fruit development in Capsicum annuum L. Sci Hortic, 1985, 25: 117-127

[67] Pressman E, Moshkovitch H, Rosenfeld K, Shaked R, Gamliel B, Aloni B. Influence of low night temperatures on sweet pepper flower quality and the effect of repeated pollinations, with viable pollen, on fruit setting. J Hortic Sci Biotechnol, 1998, 73: 131-136

[68] Pressman E, Shaked R, Firon N. Exposing pepper plants to high day temperatures prevents the adverse low night temperature symptoms. Physiol Plantarum, 2006, 126: 618-626

[69] Priya Dharshini LC, Vishnupriya S, Sakthivel KM, Rasmi RR. Oxidative stress responsive transcription factors in cellular signalling transduction mechanisms. Cell Signal, 2020, 72 ArticleID: 109670

[70] Qari SH, Tarbiyyah I. The genetic regulation of secondary metabolic pathways in response to salinity and drought as abiotic stresses. Appl Sci (Basel), 2021, 11 ArticleID: 6668

[71] Qian Z, He L, Li F. Understanding cold stress response mechanisms in plants: An overview. Front Plant Sci, 2024, 15: 1443317

[72] Qu J, Xiao P, Zhao ZQ, Wang YL, Zeng YK, Zeng X, et al.. Genome-wide identification, expression analysis of WRKY transcription factors in Citrus ichangensis and functional validation of CiWRKY31 in response to cold stress. BMC Plant Biol, 2024, 24: 617

[73] Rajametov SN, Lee K, Jeong HB, Cho MC, Nam CW, Yang EY. The effect of night low temperature on the agronomical traits of thirtynine pepper accessions (Capsicum annuum L.). Agronomy. 2021;11:1986. https://doi.org/10.3390/agronomy11101986.

[74] Razzaq MK, Aleem M, Mansoor S, Khan MA, Rauf S, Iqbal S, et al.. Omics and CRISPR-Cas9 approaches for molecular insight, functional gene analysis, and stress tolerance development in crops. Int J Mol Sci, 2021, 22: 1292

[75] Reimer JJ, Shaaban B, Drummen N, Sanjeev Ambady S, Genzel F, Poschet G, et al.. Capsicum leaves under stress: using multi-omics analysis to detect abiotic stress network of secondary metabolism in two species. Antioxidants (Basel), 2022, 11 ArticleID: 671

[76] Ren H, Ou Q, Pu Q, Lou Y, Yang X, Han Y, et al.. Comprehensive review on bimolecular fluorescence complementation and its application in deciphering protein–protein interactions in cell signaling pathways. Biomolecules, 2024, 14 ArticleID: 859

[77] Riechmann JL, Heard J, Martin G, Reuber L, Jiang C, Keddie J, et al.. Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science, 2000, 290: 2105-2110

[78] Rutayisire A, Mukayiranga A, Habineza JC, Avosa M, Edema R, Lubadde G. Effect of low temperature stress on field performance of highland sorghum (Sorghum bicolor (l.) Moench) at flowering stages. J Plant Breed Crop Sci. 2020;12:25–33. https://doi.org/10.5897/JPBCS2019.0844.

[79] Saibo NJ, Lourenço T, Oliveira MM. Transcription factors and regulation of photosynthetic and related metabolism under environmental stresses. Ann Bot, 2009, 103: 609-623

[80] Saita E, Albanesi D, de Mendoza D. Sensing membrane thickness: lessons learned from cold stress. Biochim Biophys Acta, 2016, 1861: 837-846

[81] Shahzad N, Nabi HG, Qiao L, Li W. The molecular mechanism of cold-stress tolerance: Cold responsive genes and their mechanisms in rice (Oryza sativa L.). Biology (Basel). 2024;13:442. https://doi.org/10.3390/biology13060442.

[82] Shaked R, Rosenfeld K, Pressman E. The effect of low night temperatures on carbohydrates metabolism in developing pollen grains of pepper in relation to their number and functioning. Sci Hortic, 2004, 102: 29-36

[83] Shi Y, Ding Y, Yang S. Molecular regulation of CBF signaling in cold acclimation. Trends Plant Sci, 2018, 23: 623-637

[84] Singh A, Sagar S, Biswas DK. Calcium dependent protein kinase, a versatile player in plant stress management and development. Crit Rev Plant Sci, 2017, 36: 336-352

[85] Song Y, Chen Y. Zhang X. Song P, Liu L, Li G. et al. The transcription factor FvbHLH130 activates flowering in Fragaria vesca. Acta Hortic Sin. 2023;50:295–306. https://doi.org/10.16420/j.issn.0513-353x.2021-1246.

[86] Sun Z, Li S, Chen W, Zhang J, Zhang L, Sun W, et al.. Plant dehydrins: Expression, regulatory networks, and protective roles in plants challenged by abiotic stress. Int J Mol Sci, 2021, 22: 12619

[87] Talukder MR, Bappy NAH, Haque MM, Molla MAH, Alam MZ, Mosharaf MK, et al.. Fluctuation of ambient day-night temperature influences morphological traits, floral characters, fruit yield and quality of summer tomato genotypes grown in hydroponics. N Z J Crop Hortic Sci, 2025, 53: 2731-2754

[88] Tang B, Xie L, Yang H, Li X, Chen Y, Zou X, et al.. Analysis of the expression and function of key genes in pepper under low-temperature stress. Front Plant Sci, 2022, 13 ArticleID: 852511

[89] Thakur P, Nayyar HTuteja N, Singh Gill S. Facing the cold stress by plants in the changing environment: sensing, signaling, and defending mechanisms. Plant acclimation to environmental stress, 2012, New York, Springer2969

[90] Theocharis A, Clément C, Barka EA. Physiological and molecular changes in plants grown at low temperatures. Planta, 2012, 235: 1091-1105

[91] Topuz A, Ozdemir F. Assessment of carotenoids, capsaicinoids and ascorbic acid composition of some selected pepper cultivars (Capsicum annuum L.) grown in Turkey. J Food Compos Anal, 2007, 20: 596-602

[92] Udvardi MK, Kakar K, Wandrey M, Montanari O, Murray J, Andriankaja A, et al.. Legume transcription factors: Global regulators of plant development and response to the environment. Plant Physiol, 2007, 144: 538-549

[93] Ullah I, Ullah I, Zhang H, Khan MR, Mateen A, Pei Y, et al.. Molecular mechanisms and genomic strategies for enhancing stress resilience in pepper crop. Sci Hortic, 2025, 352 ArticleID: 114403

[94] Umezawa T, Fujita M, Fujita Y, Yamaguchi-Shinozaki K, Shinozaki K. Engineering drought tolerance in plants: Discovering and tailoring genes to unlock the future. Curr Opin Biotechnol, 2006, 17: 113-122

[95] Uritani I, Hyodo H, Kuwano M. Mechanism of cold injury in sweet potatoes. Agric Biol Chem, 2014, 35: 1248-1253

[96] van Esse HP, Reuber TL, van der Does D. Genetic modification to improve disease resistance in crops. New Phytol, 2020, 225: 70-86

[97] van Tol N, van der Zaal BJ. Artificial transcription factor-mediated regulation of gene expression. Plant Sci, 2014, 225: 58-67

[98] Villiger L, Joung J, Koblan L, Weissman J, Abudayyeh OO, Gootenberg JS. CRISPR technologies for genome, epigenome and transcriptome editing. Nat Rev Mol Cell Biol, 2024, 25: 464-487

[99] Wang H, Wang H, Shao H, Tang X. Recent advances in utilizing transcription factors to improve plant abiotic stress tolerance by transgenic technology. Front Plant Sci, 2016, 7: 67

[100] Wang X, Zhou X, Xie K, Feng X, LuLiu, Gao L, et al. Genome-wide characterization and their roles in abiotic stress responses of HD-Zip transcription factors in pepper. BMC Plant Biol. 2025;25:764. https://doi.org/10.1186/s12870-025-06798-y.

[101] Wang Y, Wang J, Sarwar R, Zhang W, Geng R, Zhu KM, et al.. Research progress on the physiological response and molecular mechanism of cold response in plants. Front Plant Sci, 2024, 15: 1334913

[102] Wang Z, Zhang Y, Hu H, Chen L, Zhang H, Chen R. CabHLH79 acts upstream of CaNAC035 to regulate cold stress in pepper. Int J Mol Sci, 2022, 23 ArticleID: 2537

[103] Woodrow P, Pontecorvo G, Ciarmiello LF, Annunziata MG, Fuggi A, Carillo PVenkateswarlu B, Shanker AK, Shanker C, Maheswari M. Transcription factors and genes in abiotic stress. Crop stress and its management: perspectives and strategies, 2012, Dordrecht, Springer317-357

[104] Wu Y, Wu S, Wang X, Mao T, Bao M, Zhang J. Genome-wide identification and characterization of the bHLH gene family in an ornamental woody plant Prunus mume. Hortic Plant J, 2022, 8: 531-544

[105] Wu Z, Cheng J, Hu F, Qin C, Xu X, Hu K. The SnRK2 family in pepper (Capsicum annuum L.): Genome-wide identification and expression analyses during fruit development and under abiotic stress. Genes Genomics. 2020;42:1117–30. https://doi.org/10.1007/s13258-020-00968-y.

[106] Xiao J, Sui X, Xu Z, Liang L, Tang W, Tang Y, et al.. CaNAC76 enhances lignin content and cold resistance in pepper by regulating CaCAD1. Int J Biol Macromol, 2025, 285 ArticleID: 138271

[107] Xiao J, Wang D, Liang L, Xie M, Tang Y, Lai YS, et al. CaMYB80 enhances the cold tolerance of pepper by directly targeting CaPOA1. Hortic Res. 2024;11:uhae219. https://doi.org/10.1093/hr/uhae219.

[108] Xiong H, He H, Chang Y, Miao B, Liu Z, Wang Q, et al.. Multiple roles of NAC transcription factors in plant development and stress responses. J Integr Plant Biol, 2025, 67: 510-538

[109] Yamaguchi-Shinozaki K, Shinozaki K. A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell, 1994, 6: 251-264

[110] Yan Z, Cao X, Bing L, Lin D, Cheng F, Wang K, et al.. Assessment of the growth and quality of pepper seedlings under the combinations of daily light integral and nitrogen concentration. Hortic Environ Biotechnol, 2025, 66: 331-346

[111] Yang Y, Guang Y, Wang F, Chen Y, Yang W, Xiao X, et al.. Characterization of Phytochrome-Interacting Factor genes in pepper and functional analysis of CaPIF8 in cold and salt stress. Front Plant Sci, 2021, 12 ArticleID: 746517

[112] Yi SY, Kim JH, Joung YH, Lee S, Kim WT, Yu SH, et al.. The pepper transcription factor CaPF1 confers pathogen and freezing tolerance in Arabidopsis. Plant Physiol, 2004, 136: 2862-2874

[113] Zent KH, Dell’Acqua MLSaha RN, Dudek SM. Calcium signaling to the nucleus. Transcriptional regulation by neuronal activity: to the nucleus and back, 2024, Cham, Springer5184

[114] Zhang HX, Zhu WC, Feng XH, Jin JH, Wei AM, Gong ZH. Transcription factor CaSBP12 negatively regulates salt stress tolerance in pepper (Capsicum annuum L.). Int J Mol Sci. 2020a;21:444. https://doi.org/10.3390/ijms21020444.

[115] Zhang L, Jiang X, Liu Q, Ahammed GJ, Lin R, Wang L, et al.. The HY5 and MYB15 transcription factors positively regulate cold tolerance in tomato via the CBF pathway. Plant Cell Environ, 2020, 43: 2712-2726

[116] Zhang RX, Cheng GX, Liu GT, Chen SY, ul Haq S, Khan A, et al. Assessing the functional role of color-related CaMYB gene under cold stress using virus-induced gene silencing in the fruit of pepper (Capsicum annuum L.). Sci Hortic. 2020c;272:109504. https://doi.org/10.1016/j.scienta.2020.109504.

[117] Zhang H, Guo J, Chen X, Zhou Y, Pei Y, Chen L, et al.. Transcription factor CabHLH035 promotes cold resistance and homeostasis of reactive oxygen species in pepper. Hortic Plant J, 2024, 10: 823-836

[118] Zhang H, Pei Y, Zhu F, He Q, Zhou Y, Ma B, et al.. CaSnRK2. 4‐mediated phosphorylation of CaNAC035 regulates abscisic acid synthesis in pepper (Capsicum annuum L.) responding to cold stress. Plant J, 2024, 117: 1377-1391

[119] Zhang X, Ma X, Wang S, Liu S, Shi S. Physiological and genetic aspects of resistance to abiotic stresses in Capsicum species. Plants (Basel), 2024, 13 ArticleID: 3013

[120] Zhang J, Liang L, Xie Y, Zhao Z, Su L, Tang Y, et al. Transcriptome and metabolome analyses reveal molecular responses of two pepper (Capsicum annuum L.) cultivars to cold stress. Front Plant Sci. 2022;13:819630. https://doi.org/10.3389/fpls.2022.819630.

[121] Zhang J, Sohail H, Xu X, Zhang Y, Zhang Y, Chen Y. Unveiling tolerance mechanisms in pepper to combined low-temperature and low-light stress: A physiological and transcriptomic approach. BMC Plant Biol, 2025, 25: 171

[122] Zhang J, Xie M, Yu G, Wang D, Xu Z, Liang L, et al. CaSPDS, a spermidine synthase gene from pepper (Capsicum annuum L.), plays an important role in response to cold stress. Int J Mol Sci. 2023a;24:5013. https://doi.org/10.3390/ijms24055013.

[123] Zhang Z, Jiang C, Chen C, Su K, Lin H, Zhao Y, et al.. VvWRKY5 enhances white rot resistance in grape by promoting the jasmonic acid pathway. Hortic Res, 2023, 10 ArticleID: uhad172

[124] Zheng J, Liu F, Zhu C, Li X, Dai X, Yang B, et al.. Identification, expression, alternative splicing and functional analysis of pepper WRKY gene family in response to biotic and abiotic stresses. PLoS ONE, 2019, 14 ArticleID: e0219775

[125] Zheng PF, Yang YY, Zhang S, You CX, Zhang ZL, Hao YJ. Identification and functional characterization of MdPIF3 in response to cold and drought stress in Malus domestica. Plant Cell Tissue Organ Cult, 2021, 144: 435-447

Funding

National Natural Science Foundation of China(32172582)

the Agricultural Key Science and Technology Program of Shaanxi Province(2024NC-YBXM-045)

the China Postdoctoral Science Foundation(GZC20241390)

Shaanxi Province Postdoctoral Science Foundation(2024BSHSDZZ171)

RIGHTS & PERMISSIONS

The Author(s)