Cold stress-induced biochemical and molecular responses in Safflower (Carthamus tinctorious L.)
DOI:
https://doi.org/10.14719/pst.4032Keywords:
cold responsiveness, differential gene expression, SafflowerAbstract
Cold stress causes substantial losses in global agricultural productivity. When exposed to cold stress, plants usually exhibit a variety of cold-induced physiological, biochemical, and molecular responses. Safflower is one of the oldest, marginalized, neglected and domesticated multipurpose oilseed crops which is uniquely affected by cold stress at different growth stages. Because of lack of systematic research on cold signalling pathways and gene regulatory networks, the underlying biochemical and molecular mechanisms of cold signal transduction in different developmental stages of safflower are poorly understood. Therefore, this study sought to detect biochemical response and identify cold responsive safflower genes expressed at the rosette and bolling stages to provide novel insight about the growth stage’s differential responses to cold stress. The results demonstrated that pseudo-marker snap genes CtAH10T0001700.1 and CtAH10T0001500.1 are the E3 ligase genes with RING finger domain while CtAH10T0000500 matched the GRAS family genes. These genes successfully exhibited similar cold responses as per their respective family. Overexpression of some E3 genes like CIP8 and HOS 1 could be associated with the cold susceptibility of plants in the bolling stage of safflower. Additionally, CtAH10T0001700.1 expression was found to be positively correlated with electrolyte leakage and proline content at the rosette stage. Meanwhile CtAH10T0001500.1, a negative cold regulator significantly correlated with electrolyte leakage and proline content. While CtAH10T0000500, a positive cold regulator significantly correlated with electrolyte leakage and proline at the rosette stage, but negatively associated with the two parameters at bolling stage. Overall, the genes were found to play a significant role in cold responsiveness of safflower plants at different growth stages.
Downloads
References
Kopecká R, Kameniarová M, Cerný M, Brzobohatý B, Novák J. Abiotic stress in crop production. Int J Mol Sci. 2023;24(7):6603. https://doi.org/10.3390/ijms24076603
United Nations. Population: The world in 2100 [Internet] [Accessed on the 19Mar 2024]. Available from: https://www.un.org>global-issues
Iizumi T, Shen Z, Furuya J, Koizumi T, Furuhashi G, Kim W, et al. Climate change adaptation cost and residual damage to global crop production. Clim Res. 2020;80:203-18. https://doi.org/10.3354/cr01605
Li D, Hu B, Wang Q, Liu H, Pan F, Wu W. Identification and evaluation of reference genes for accurate transcription normalization in Safflower under different experimental conditions. PLoS One. 2015;10(10). https://doi:10.1371/journal.pone.0140218
Emongor VE, Emongor RA. Safflower (Carthamus tinctorious L.). Chapter 24. Elsevier Inc; 2023. p. 683-731.
Johnson RC, Dajue L, Bradley V. Autumn growth and its relationship to winter survival in diverse Safflower germplasm. Can J Plant Sci. 2006;86:701-09. https://doi.org/10.4141/P05-104
Landry EJ, Fuchs SJ, Bradley VL, Johnson RC. The effect of cold acclimation on the low molecular weight carbohydrate composition of Safflower. Heliyon. 2017;3:e00402. https://doi:10.1016/j.heliyon.2017.e00402
Emongor V. Safflower (Carthamus tinctorius L.) the underutilized and neglected crop: A Review. Asian J Plant Sci. 2010;9(6):299-306. https://doi:10.3923/ajps.2010.299.306
Vaclavik L, Mishra A, Mishra KB, Hajslova J. Mass spectrometry-based metabolomic fingerprinting for screening cold tolerance in Arabidopsis thaliana accessions. Anal Bioanal Chem. 2013;405(8): 2671-83. https://doi.org/10.1007/s00216-012-6692-1
Johnson RC, Petrie SE, Franchini MC, Evans M. Yield and yield components of winter-type Safflower. Crop Sci. 2012;52:2358-64. https://doi.org/10.2135/cropsci2011.12.0659
Kolenyane MO. The influence of nitrogen and phosphorus on growth and yield components of Safflower (Carthamus tinctorious L.). Botswana University of Agriculture and Natural Resources Press; 2022. p. 46. https://moodle.buan.ac.bw/handle/13049/534
Lee BH, Henderson DA, Zhu JK. The Arabidopsis cold responsive transcriptome and its regulation by ICE1. Plant Cell. 2005;17:3155-75. https://doi.org/10.1105/tpc.105.035568
Ren C, Li H, Wang Z, Dai Z, Lecourieux F, Kuang Y, et al. Characterization of chromatin accessibility and gene expression upon cold stress reveals that the RAV1 transcription factor functions in cold response in Vitis amurensis. Plant Cell Physiol. 2021;62(10):1615-29. https://doi.org/10.1093/pcp/pcab115
Ritonga FN, Chen S. Physiological and molecular mechanism involved in cold stress tolerance in plants. Review Plants. 2020;9(560):1-13. https://doi.org/10.3390/plants9050560
Chai F, Liu W, Xiang Y, Meng X, Sun X, Cheng C, et al. Comparative metabolic profiling of Vitis amurensis and Vitis vinifera during cold acclimation. Hortic Res. 2019;6:8. https://doi.org/10.1038/s41438-018-0083-5
Hasanuzzaman M, Nahar K, Alam MM, Roychowdhary R. Physiological, biochemical and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci. 2013;14:9643-84. https://doi.org/10.3390/ijms14059643
Leuendorf JE, Frank M, Schmülling T. Acclimation, priming and memory in the response of Arabidopsis thaliana seedlings to cold stress. Sci Rep. 2020;10(1):689. https://doi.org/10.1038/s41598-019-56797-x
Aazami MA, Asghari-Aruq M, Hassanpouraghdam MB, Ercisli S, Baron M, Sochor J. Low temperature stress mediates the antioxidants pool and chlorophyll fluorescence in Vitis vinifera L. cultivars. Plants. 2021;10:1877. https://doi.org/10.3390/plants10091877
Kovaleski PA, Gossman JJ. Standardization of electrolyte leakage data and novel liquid nitrogen control improve measurement of cold hardiness in woody tissues. Plant Methods. 2021;17:53. https://doi.org/10.1186/s13007-021-00755-0
Liu W, Yu K, He T, Li F, Zhang D, Lui J. The low temperature induced physiological responses of Avena nuda L, a cold-tolerant plant species. Sci World J. 2013;658793:1-7. https://doi.org/10.1155/2013/658793
Carillo P, Gibon Y. Protocol: extraction and determination of proline. [Internet]. Prometheuswiki. Researchgate Net; 2011 [cited 2024 June 23]. Available from: https://www.researchgate.net
Zhang Z, Huang R. Analysis of malondialdehyde, chlorophyll proline, soluble sugar and glutathione content in Arabidopsis seedling. Bio Protoc. 2013;3(14):e817. https://doi.org/10.21769/BioProtoc.817
The genome Database of Carthamus tinctorious repository [Internet] [Cited 2024 March 3]. Available from: https://www.safflower.scuec.edu
Lu S, Wang J, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, et al. CDD/SPARCLE: The Conserved Domain Database in 2020. Nucleic Acids Res. 2020;48:D265-68. https://doi.org/10.1093/nar/gkz991
Wang J, Chitsaz F, Derbyshire MK, Noreen R, Gonzales NR, Marc-Gwadz Lu S, et al. "The Conserved Domain Database in 2023". Nucleic Acids Res. 2023;51:D384-88. https://doi.org/10.1093/nar/gkac1096
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using Real-Time Quantitative PCR and the 2-??CT Method. Methods. 2001;25:402-08. https://doi.org/10.1006.meth.2001.1262
Hatsugai N, Katagiri F. Quantification of plant cell death by electrolyte leakage assay. Bio Protoc. 20188(5):e2758. https://doi.org/10.21769/BioProc.2758
Amala E, Singh KP, Panwar S, Namita B, Neelu J, Kumar S, et al. Physiological and morphological responses of marigold (Tagetes erecta) genotypes under cold stress. Indian J of Agric Sci. 2022;92(7):923-27. https://doi.org/10.56093/ijas.v92i7.119495
Rani A, Kiran A, Sharma KD, Prasad PVV, Jha UC, Siddique KHM, et al. Cold tolerance during the reproductive phase in chickpea (Cicer arietinum L.) is associated with superior cold acclimation ability involving antioxidants and cryoprotective solutes in anthers and ovules. Antioxidants. 2021;10(11):1693. https://doi.org/10.3390/antiox10111693
Verbruggen N, Hermans C. Proline accumulation in plants; A review. Amino Acids. 2008;35(4):753-59. https://doi.org/10.1007/s00726-0080061-6
Tatar O, Ozalkan C, Atasoy GD. Partitioning of dry matter, proline accumulation, chlorophyll content and antioxidant activity of chickpea (Cicer arietinum L.) plants under chilling stress. Bulg J Agric Sci. 2013;19(2):260-65. Available from: https://www.researchgate.net/publication/269987702
Kereilwe D, Emongor VE, Malambane G. Temperature and duration of exposure on chilling injury of safflower. EJFOOD. 2023;5(2):23-26. http://dx.doi.org/10.24018/ejfood.2023.5.2.660
Urdiales-Flores D, Zittis G, Hadjinicolaou P, Cherchi A, Alessandri A, Peleg N, et al. A global analysis of historical and future changes in mediterranean climate-type regions. Int J Climatol. 2024;0:1-14. https://doi.org/10.1002/joc.8655
Mosupiemang M, Emongor VE, Malambane G. A review of drought tolerance in safflower. IJPSS. 2022;34(10):140-49. https://doi.org/10.9734/IJPSS/2022/v34i1030930
López-Anido F, Martin E. Globe artichoke (Cynara cardunculus var. scolymus L.) breeding: In: Al-Khayri JM, Mohan-Jain S, Johnson DV, editors. Advances in plant breeding strategies: Vegetable crops, Volume 10; Leaves, Flowerheads, Green pods, Mushrooms and truffles; 2021. p. 303-04. https://doi.org/10.1007/978-3-030-66969-08
Cannon SB, Mitra A, Baumgarten A, Young ND, May GJB. The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol. 2004;4(10):1-21. https://doi.org/10.1186/1471-2229-4-10
Han G, Qiao Z, Li Y, Yang Z, Wang C, Zhang Y, et al. RING zinc finger proteins in plant abiotic stress tolerance. Front Plant Sci. 2022;13:877011. https://doi.org/10.3389/fpls.2022.877011
Wang S, Lv X, Zhang J, Chen D, Chen S, Fan G, et al. Roles of E3 ubiquitin ligases in plant responses to abiotic stresses. Int J Mol Sci. 2022;23:230. https://doi.org/10.3390/ijms23042308
Wang P, Zhu L, Li Z, Cheng M, Chen X, Wang A, et al. Genome-wide identification of the U-Box E3 ubiquitin ligase gene family in cabbage (Brassica oleracea var. capitata) and its expression analysis in response to cold stress and pathogen infection. Plants. 2023;12(7):1437. https://doi.org/10.3390/plants12071437
Liu K, Wang L, Xu Y, Chen N, Ma Q, Li F, et al. Overexpression of OsCOIN, a putative cold inducible zinc finger protein, increased tolerance to chilling, salt and drought, and enhanced proline level in rice. Planta. 2007;226(4):1007-16. https://doi.org/10.1007/s00425-007-0548-5
Sun J, Sun Y, Imtiaz-Ahmed R, Ren A, Xie M. Research progress on plant RING finger proteins. Genes. 2019;10(12):973. https://doi.org/10.3390/gene10120973
Lourenço T, Sapeta H, Figueiredo DD, Rodrigues M, Cordeiro A, Abreu IA, et al. Isolation and characterization of rice (Oryza sativa L.) E3-ubiquitin ligase OsHOS1 gene in the modulation of cold stress response. Plant Mol Biol. 2013;83,351-63. https://doi.org/10.1007/s11103-013-0092-6
Al-Saharin R, Hellmann H, Mooney S. Plant E3 ligases and their role in abiotic stress response. Cells. 2022;11:890. https://doi.org/10.3390/cells11050890
Lu X, Liu W, Xiang C, Li X, Wang Q, Wang T, et al. Genome-wide characterization of GRAS family and their potential roles in cold tolerance of cucumber (Cucumis sativus L.). Int J Mol Sci. 2020;21(11):3857. https://doi.org/10.3390/ijms21113857
Tong N, Li D, Zhang S, Tang M, Chen Y, Zhang Z, et al. Genome-wide identification and expression analysis of the GRAS family under low-temperature stress in bananas. Front Plant Sci. 2023;14:1216070. https://doi.org/10.3389/fpls.2023.1216070
Peng G, Xin X, Hua J, Yan D. Cloning and functional studies of maize ZmSCL7. Chin Agric Sci. 2013;46(12):2584-91. https://doi.org/10.3864/i.issn.0578-1752.2013.12.020
Li LL, Zeng WJ, Li YH, Ge FW, Lu H, Lei W, et al. Analysis of GRAS transcription factors and Lascl18 gene cloning and cold correlation. Mol Plant Breed. 2017;15(9):3428-37. https://doi.org/10.13271/j.mpb.015.003428
Ye JJ. Cold temperature stress response and promoter sequence analysis of ERF 6 and GRAS genes in citrus plants. Hang Zhou: Zhejiang Normal University; 2013.
Yan JQ, Wang J, Li QT, Hwang JR, Patterson C, Zhang H, et al. AtCHIP, A U-box-containing E3 ubiquitin ligase, plays a critical role in temperature stress tolerance in Arabidopsis. Plant Physiol. 2003;132(2):861-69. https://doi.org/10.1104/pp.103.020800
Fang H, Meng Q, Zhang H, Huang J. Knockdown of a RING finger gene confers cold tolerance. Bioengineered. 2016;7(1):39-45. https://doi.org/10.1007/s11103-015-0294-1
Li J, Yang Y, Iqbal A, Qadri R, Shi P, Wang Y, et al. Correlation analysis of cold related gene expression with physiological and biochemical indicators under cold stress in oil palm. PLoS One. 2019;14(11):e0225768. https://doi.org/10.1371/journal.pone.0225768
Downloads
Published
Versions
- 28-01-2025 (2)
- 27-01-2025 (1)
How to Cite
Issue
Section
License
Copyright (c) 2025 D Kereilwe, G Malambane, V E Emongor, U Batlang
This work is licensed under a Creative Commons Attribution 4.0 International License.
Copyright and Licence details of published articles
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
Open Access Policy
Plant Science Today is an open access journal. There is no registration required to read any article. All published articles are distributed under the terms of the Creative Commons Attribution License (CC Attribution 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited (https://creativecommons.org/licenses/by/4.0/). Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).
