{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T05:02:15Z","timestamp":1787029335387,"version":"build-2736575974"},"reference-count":66,"publisher":"MDPI AG","issue":"19","license":[{"start":{"date-parts":[[2024,9,25]],"date-time":"2024-09-25T00:00:00Z","timestamp":1727222400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"project of \u201cKunpeng Plan\u201d in Zhaotong City","award":["20211124"],"award-info":[{"award-number":["20211124"]}]},{"name":"project of \u201cKunpeng Plan\u201d in Zhaotong City","award":["20190703"],"award-info":[{"award-number":["20190703"]}]},{"name":"universities of Yunnan Province","award":["20211124"],"award-info":[{"award-number":["20211124"]}]},{"name":"universities of Yunnan Province","award":["20190703"],"award-info":[{"award-number":["20190703"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Plants"],"abstract":"<jats:p>The Defective in Induced Resistance 1 (DIR1) gene, a member of the lipid transferase proteins (LTPs), plays a crucial role in plant defense against pathogens. While previous transcriptomic studies have highlighted the significant expression of citrus LTPs during biotic stress, functional annotations of LTPs in the Citrus genera remain limited. In this study, we cloned the Murraya paniculata DIR1 (MpDIR1(t)) gene and overexpressed it in Arabidopsis thaliana to evaluate its stress response mechanisms against biotic stress. The transgenic Arabidopsis lines showed fewer disease symptoms in response to Pseudomonas syringae (Pst DC3000) compared to wild-type Arabidopsis. Defense and pathogenesis-responsive genes such as PR1, PR4, PR5, and WRKY12 were significantly induced, showing a 2- to 12-fold increase in all transgenic lines compared to the wild type. In addition, the Pst DC3000-infected transgenic Arabidopsis lines demonstrated elevated levels of flavonoids and salicylic acid (SA), along with higher expression of SA-related genes, compared to the wild type. Moreover, all transgenic lines possessed lower reactive oxygen species levels and higher activity of antioxidant defense enzymes such as superoxide dismutase, peroxidase, and catalase under Pst DC3000 stress compared to the wild type. The up-regulation of defense genes, activation of the SA pathway, accumulation of flavonoids, and reinforcement of antioxidant defense mechanisms in transgenic Arabidopsis lines in response to Pst DC3000 underscore the critical role of MpDIR1(t) in fortifying plant immunity. Thus, MpDIR1(t) constitutes a promising candidate gene for improving bacterial disease resistance in commercial citrus cultivars.<\/jats:p>","DOI":"10.3390\/plants13192692","type":"journal-article","created":{"date-parts":[[2024,9,26]],"date-time":"2024-09-26T04:05:46Z","timestamp":1727323546000},"page":"2692","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":14,"title":["The Ectopic Expression of the MpDIR1(t) Gene Enhances the Response of Plants from Arabidopsis thaliana to Biotic Stress by Regulating the Defense Genes and Antioxidant Flavonoids"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-3486-024X","authenticated-orcid":false,"given":"Mingzheng","family":"Duan","sequence":"first","affiliation":[{"name":"College of Agronomy and Life Sciences, Zhaotong University, Zhaotong 657000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Liuyuan","family":"Bao","sequence":"additional","affiliation":[{"name":"College of Agronomy and Life Sciences, Zhaotong University, Zhaotong 657000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Momina","family":"Eman","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Subtropical Silviculture, College of Forestry and Biotechnology, Zhejiang A & F University, Hangzhou 311300, China"},{"name":"Institute of Pure & Applied Biology (IP&AB), Bahauddin Zakariya University, Multan 60800, Punjab, Pakistan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Duo","family":"Han","sequence":"additional","affiliation":[{"name":"College of Agronomy and Life Sciences, Zhaotong University, Zhaotong 657000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yongzhi","family":"Zhang","sequence":"additional","affiliation":[{"name":"College of Agronomy and Life Sciences, Zhaotong University, Zhaotong 657000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6185-5641","authenticated-orcid":false,"given":"Bingsong","family":"Zheng","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Subtropical Silviculture, College of Forestry and Biotechnology, Zhejiang A & F University, Hangzhou 311300, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shunqiang","family":"Yang","sequence":"additional","affiliation":[{"name":"College of Agronomy and Life Sciences, Zhaotong University, Zhaotong 657000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4911-9451","authenticated-orcid":false,"given":"Muhammad Junaid","family":"Rao","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Subtropical Silviculture, College of Forestry and Biotechnology, Zhejiang A & F University, Hangzhou 311300, China"},{"name":"State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Agriculture, Guangxi University, 100 Daxue Rd., Nanning 530004, China"},{"name":"Key Laboratory of Horticultural Plant Biology (Ministry of Education), Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (Ministry of Agriculture), Huazhong Agricultural University, Wuhan 430070, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,9,25]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"\u00c1d\u00e1m, A.L., Nagy, Z.\u00c1., K\u00e1tay, G., Mergenthaler, E., and Viczi\u00e1n, O. (2018). Signals of systemic immunity in plants: Progress and open questions. Int. J. Mol. Sci., 19.","DOI":"10.3390\/ijms19041146"},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Champigny, M.J., Isaacs, M., Carella, P., Faubert, J., Fobert, P.R., and Cameron, R.K. (2013). Long distance movement of DIR1 and investigation of the role of DIR1-like during systemic acquired resistance in Arabidopsis. Front. Plant Sci., 4.","DOI":"10.3389\/fpls.2013.00230"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1016\/j.pmpp.2016.12.005","article-title":"Exploring the role of DIR1, DIR1-like and other lipid transfer proteins during systemic immunity in Arabidopsis","volume":"97","author":"Carella","year":"2017","journal-title":"Physiol. Mol. Plant Pathol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"399","DOI":"10.1038\/nature00962","article-title":"A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis","volume":"419","author":"Maldonado","year":"2002","journal-title":"Nature"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1762","DOI":"10.1104\/pp.110.171694","article-title":"Interconnection between methyl salicylate and lipid-based long-distance signaling during the development of systemic acquired resistance in Arabidopsis and tobacco","volume":"155","author":"Liu","year":"2011","journal-title":"Plant Physiol."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Isaacs, M., Carella, P., Faubert, J., Champigny, M.J., Rose, J.K.C., and Cameron, R.K. (2016). Orthology analysis and in vivo complementation studies to elucidate the role of DIR1 during systemic acquired resistance in Arabidopsis thaliana and Cucumis sativus. Front. Plant Sci., 7.","DOI":"10.3389\/fpls.2016.00566"},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Wang, Y., Zhou, L., Yu, X., Stover, E., Luo, F., and Duan, Y. (2016). Transcriptome profiling of Huanglongbing (HLB) tolerant and susceptible citrus plants reveals the role of basal resistance in HLB tolerance. Front. Plant Sci., 7.","DOI":"10.3389\/fpls.2016.00933"},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Champigny, M.J., Shearer, H., Mohammad, A., Haines, K., Neumann, M., Thilmony, R., He, S.Y., Fobert, P., Dengler, N., and Cameron, R.K. (2011). Localization of DIR1 at the tissue, cellular and subcellular levels during systemic acquired resistance in Arabidopsis using DIR1: GUS and DIR1: EGFP reporters. BMC Plant Biol., 11.","DOI":"10.1186\/1471-2229-11-125"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1093\/jxb\/erh025","article-title":"Signals for local and systemic responses of plants to pathogen attack","volume":"55","author":"Suzuki","year":"2004","journal-title":"J. Exp. Bot."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Rao, M.J., Wang, L., Ahmad, U., Ahmad, M.H., and Hussain, S. (2022). Citrus metabolic and antioxidant responses to high light stress. Citrus Production, CRC Press.","DOI":"10.1201\/9781003119852-12"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1111\/1574-6968.12157","article-title":"Response of tobacco to the Pseudomonas syringae pv. tomato DC3000 is mainly dependent on salicylic acid signaling pathway","volume":"344","author":"Liu","year":"2013","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Hammond-Kosack, K.E., and Jones, J.D. (1996). Resistance gene-dependent plant defense responses. Plant Cell, 8.","DOI":"10.2307\/3870229"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"439","DOI":"10.2174\/0929866054395329","article-title":"Plant serine proteinase inhibitors","volume":"12","author":"Christeller","year":"2005","journal-title":"Protein Pept. Lett."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Rao, M.J., Zuo, H., and Xu, Q. (2021). Genomic insights into citrus domestication and its important agronomic traits. Plant Commun., 2.","DOI":"10.1016\/j.xplc.2020.100138"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1016\/S1369-5266(02)00275-3","article-title":"Cross talk between signaling pathways in pathogen defense","volume":"5","author":"Kunkel","year":"2002","journal-title":"Curr. Opin. Plant Biol."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Rawat, N., Kiran, S.P., Du, D., Gmitter, F.G., and Deng, Z. (2015). Comprehensive meta-analysis, co-expression, and miRNA nested network analysis identifies gene candidates in citrus against Huanglongbing disease. BMC Plant Biol., 15.","DOI":"10.1186\/s12870-015-0568-4"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Yu, Q., Chen, C., Du, D., Huang, M., Yao, J., Yu, F., Brlansky, R.H., and Gmitter, F.G. (2017). Reprogramming of a defense signaling pathway in rough lemon and sweet orange is a critical element of the early response to \u2018Candidatus Liberibacter asiaticus\u2019. Hortic. Res., 4.","DOI":"10.1038\/hortres.2017.63"},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Hu, Y., Zhong, X., Liu, X., Lou, B., Zhou, C., and Wang, X. (2017). Comparative transcriptome analysis unveils the tolerance mechanisms of Citrus hystrix in response to \u2018Candidatus Liberibacter asiaticus\u2019 infection. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0189229"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1526","DOI":"10.1104\/pp.110.157370","article-title":"Functional analysis of the Arabidopsis PAL gene family in plant growth, development, and response to environmental stress","volume":"153","author":"Huang","year":"2010","journal-title":"Plant Physiol."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Rao, M.J., Feng, B., Ahmad, M.H., Tahir, M., Aslam, M.Z., Khalid, M.F., Hussain, S., Zhong, R., Ali, Q., and Xu, Q. (2023). LC-MS\/MS-based metabolomics approach identified novel antioxidant flavonoids associated with drought tolerance in citrus species. Front. Plant Sci., 14.","DOI":"10.3389\/fpls.2023.1150854"},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Wu, H., Hu, Y., Fu, S., Zhou, C., and Wang, X. (2020). Physiological and Molecular Plant Pathology Coordination of multiple regulation pathways contributes to the tolerance of a wild citrus species (Citrus ichangensis \u20182586\u2019) against Huanglongbing. Physiol. Mol. Plant Pathol., 109.","DOI":"10.1016\/j.pmpp.2019.101457"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"620","DOI":"10.1094\/MPMI-12-16-0257-R","article-title":"\u2018Candidatus Liberibacter asiaticus\u2019 encodes a functional salicylic acid (SA) hydroxylase that degrades SA to suppress plant defenses","volume":"30","author":"Li","year":"2017","journal-title":"Mol. Plant-Microbe Interact."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Hu, B., Rao, M.J., Deng, X., Pandey, S.S., Hendrich, C., Ding, F., Wang, N., and Xu, Q. (2021). Molecular signatures between citrus and Candidatus Liberibacter asiaticus. PLoS Pathog., 17.","DOI":"10.1371\/journal.ppat.1010071"},{"key":"ref_24","first-page":"2045","article-title":"Citrus Huanglongbing (Greening Disease) in Egypt: Symptoms Documentation and Pathogen Detection","volume":"15","author":"Tolba","year":"2015","journal-title":"Am. Eurasian J. Agric. Environ. Sci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"31","DOI":"10.21273\/HORTSCI11374-16","article-title":"Apparent tolerance to Huanglongbing in Citrus and Citrus-related germplasm","volume":"52","author":"Miles","year":"2017","journal-title":"HortScience"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Killiny, N., and Hijaz, F. (2016). Amino acids implicated in plant defense are higher in Candidatus Liberibacter asiaticus-tolerant citrus varieties. Plant Signal. Behav., 11.","DOI":"10.1080\/15592324.2016.1171449"},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Hijaz, F., Nehela, Y., and Killiny, N. (2016). Possible role of plant volatiles in tolerance against huanglongbing in citrus. Plant Signal. Behav., 11.","DOI":"10.1080\/15592324.2016.1138193"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1346","DOI":"10.1094\/PHYTO-99-12-1346","article-title":"Examination of the responses of different genotypes of citrus to Huanglongbing (citrus greening) under different conditions","volume":"99","author":"Folimonova","year":"2009","journal-title":"Phytopathology"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1858","DOI":"10.1094\/PDIS-03-16-0271-RE","article-title":"Long-Term Field Evaluation Reveals Huanglongbing Resistance in Citrus Relatives","volume":"100","author":"Ramadugu","year":"2016","journal-title":"Plant Dis."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Zheng, Z.-L., and Zhao, Y. (2013). Transcriptome comparison and gene coexpression network analysis provide a systems view of citrus response to \u2018Candidatus Liberibacter asiaticus\u2019 infection. BMC Genom., 14.","DOI":"10.1186\/1471-2164-14-27"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1396","DOI":"10.1094\/MPMI-06-12-0150-R","article-title":"Comparative transcriptional and anatomical analyses of tolerant rough lemon and susceptible sweet orange in response to \u2018Candidatus Liberibacter asiaticus\u2019 infection","volume":"25","author":"Fan","year":"2012","journal-title":"Mol. Plant-Microbe Interact."},{"key":"ref_32","first-page":"31","article-title":"Detection of the bearing rate of Liberobacter asiaticum, in citrus psylla and its host plant Murraya paniculata by nested PCR","volume":"29","author":"Li","year":"2002","journal-title":"Acta Phytopathol. Sin."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"671","DOI":"10.1094\/PHYTO-04-20-0153-R","article-title":"A lipid transfer protein has antifungal and antioxidant activity and suppresses Fusarium head blight disease and DON accumulation in transgenic wheat","volume":"111","author":"McLaughlin","year":"2021","journal-title":"Phytopathology"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"915","DOI":"10.1046\/j.1365-3040.2003.01024.x","article-title":"Three pathogen-inducible genes encoding lipid transfer protein from pepper are differentially activated by pathogens, abiotic, and environmental stresses","volume":"26","author":"Jung","year":"2003","journal-title":"Plant. Cell Environ."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1016\/S1360-1385(00)01600-9","article-title":"The WRKY superfamily of plant transcription factors","volume":"5","author":"Eulgem","year":"2000","journal-title":"Trends Plant Sci."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1111\/j.1365-313X.2007.03397.x","article-title":"Interplay between JA, SA and ABA signalling during basal and induced resistance against Pseudomonas syringae and Alternaria brassicicola","volume":"54","author":"Flors","year":"2008","journal-title":"Plant J."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"47","DOI":"10.4489\/MYCO.2004.32.1.047","article-title":"Induction of defense related enzymes and pathogenesis related proteins in Pseudomonas fluorescens-treated chickpea in response to infection by Fusarium oxysporum f. sp. ciceri","volume":"32","author":"Saikia","year":"2004","journal-title":"Mycobiology"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1016\/j.postharvbio.2013.01.004","article-title":"Molecular characterization of PR and WRKY genes during SA-and MeJA-induced resistance against Colletotrichum musae in banana fruit","volume":"79","author":"Tang","year":"2013","journal-title":"Postharvest Biol. Technol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1146\/annurev-phyto-073009-114447","article-title":"Hormone crosstalk in plant disease and defense: More than just jasmonate-salicylate antagonism","volume":"49","author":"Grant","year":"2011","journal-title":"Annu. Rev. Phytopathol."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"D\u2019Maris Amick Dempsey, A.C., Vlot, M.C.W., and Daniel, F.K. (2011). Salicylic acid biosynthesis and metabolism. Arab. Book\/Am. Soc. Plant Biol., 9.","DOI":"10.1199\/tab.0156"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"496","DOI":"10.1080\/07352689.2018.1544843","article-title":"Metabolic mechanisms of host species against citrus Huanglongbing (Greening Disease)","volume":"37","author":"Rao","year":"2018","journal-title":"CRC Crit. Rev. Plant Sci."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"841","DOI":"10.1111\/1758-2229.12086","article-title":"Plant flavonoids target Pseudomonas syringae pv. tomato DC 3000 flagella and type III secretion system","volume":"5","author":"Vargas","year":"2013","journal-title":"Environ. Microbiol. Rep."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1016\/j.pmpp.2015.04.004","article-title":"Overexpression of TaUb2 enhances disease resistance to Pseudomonas syringae pv. tomato DC3000 in tobacco","volume":"90","author":"Zhang","year":"2015","journal-title":"Physiol. Mol. Plant Pathol."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Rao, M.J., Xu, Y., Huang, Y., Tang, X., Deng, X., and Xu, Q. (2019). Ectopic expression of citrus UDP-GLUCOSYL TRANSFERASE gene enhances anthocyanin and proanthocyanidins contents and confers high light tolerance in Arabidopsis. BMC Plant Biol., 19.","DOI":"10.1186\/s12870-019-2212-1"},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Rao, M.J., Xu, Y., Tang, X., Huang, Y., Liu, J., and Deng, X. (2020). CsCYT75B1, a citrus CYTOCHROME P450 gene, is involved in accumulation of antioxidant flavonoids and anduces drought tolerance in transgenic Arabidopsis. Antioxidants, 9.","DOI":"10.3390\/antiox9020161"},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Rao, M.J., Wu, S., Duan, M., and Wang, L. (2021). Antioxidant metabolites in primitive, wild, and cultivated citrus and their role in stress tolerance. Molecules, 26.","DOI":"10.3390\/molecules26195801"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"419","DOI":"10.1007\/s00299-008-0653-3","article-title":"Overexpression of lipid transfer protein (LTP) genes enhances resistance to plant pathogens and LTP functions in long-distance systemic signaling in tobacco","volume":"28","author":"Sarowar","year":"2009","journal-title":"Plant Cell Rep."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"971","DOI":"10.1007\/s00425-016-2585-4","article-title":"Lipid transfer proteins: Classification, nomenclature, structure, and function","volume":"244","author":"Salminen","year":"2016","journal-title":"Planta"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"735","DOI":"10.1046\/j.1365-313x.1998.00343.x","article-title":"Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana","volume":"16","author":"Clough","year":"1998","journal-title":"Plant J."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1016\/S1360-1385(02)02251-3","article-title":"GATEWAYTM vectors for Agrobacterium-mediated plant transformation","volume":"7","author":"Karimi","year":"2002","journal-title":"Trends Plant Sci."},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Amack, S.C., and Antunes, M.S. (2020). CaMV35S promoter\u2014A plant biology and biotechnology workhorse in the era of synthetic biology. Curr. Plant Biol., 24.","DOI":"10.1016\/j.cpb.2020.100179"},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Edwards, K., Johnstone, C., and Thompson, C. (1991). A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Res., 19.","DOI":"10.1093\/nar\/19.6.1349"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1007\/BF02773348","article-title":"A protocol for rapid DNA extraction fromArabidopsis thaliana for PCR analysis","volume":"22","author":"Kasajima","year":"2004","journal-title":"Plant Mol. Biol. Rep."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1006\/meth.2001.1262","article-title":"Analysis of relative gene expression data using real-time quantitative PCR and the 2\u2212\u0394\u0394CT method","volume":"25","author":"Livak","year":"2001","journal-title":"Methods"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"410","DOI":"10.1094\/MPMI-11-17-0270-TA","article-title":"Validation of RT-qPCR approaches to monitor Pseudomonas syringae gene expression during infection and exposure to pattern-triggered immunity","volume":"31","author":"Smith","year":"2018","journal-title":"Mol. Plant-Microbe Interact."},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Jambunathan, N. (2010). Determination and detection of reactive oxygen species (ROS), lipid peroxidation, and electrolyte leakage in plants. Plant Stress Tolerance, Springer.","DOI":"10.1007\/978-1-60761-702-0_18"},{"key":"ref_57","first-page":"90","article-title":"V Estimation of salicylic acid in Eucalyptus leaves using spectrophotometric methods","volume":"3","author":"Warrier","year":"2013","journal-title":"Genet. Plant Physiol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1016\/S0168-9452(99)00197-1","article-title":"Oxidative stress and some antioxidant systems in acid rain-treated bean plants: Protective role of exogenous polyamines","volume":"151","author":"Velikova","year":"2000","journal-title":"Plant Sci."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1016\/j.plaphy.2013.11.003","article-title":"Manipulation of monoubiquitin improves chilling tolerance in transgenic tobacco (Nicotiana tabacum)","volume":"75","author":"Feng","year":"2014","journal-title":"Plant Physiol. Biochem."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"198","DOI":"10.4103\/0973-1296.66936","article-title":"Total phenolic, anthocyanin contents and antioxidant capacity of selected elderberry (Sambucus canadensis L.) accessions","volume":"6","author":"Ozgen","year":"2010","journal-title":"Pharmacogn. Mag."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"1769","DOI":"10.1093\/mp\/sst080","article-title":"A novel integrated method for large-scale detection, identification, and quantification of widely targeted metabolites: Application in the study of rice metabolomics","volume":"6","author":"Chen","year":"2013","journal-title":"Mol. Plant"},{"key":"ref_62","doi-asserted-by":"crossref","unstructured":"Rao, M.J., Duan, M., Eman, M., Yuan, H., Sharma, A., and Zheng, B. (2024). Comparative Analysis of Citrus Species\u2019 Flavonoid Metabolism, Gene Expression Profiling, and Their Antioxidant Capacity under Drought Stress. Antioxidants, 13.","DOI":"10.3390\/antiox13091149"},{"key":"ref_63","doi-asserted-by":"crossref","unstructured":"Chanana, S., Thomas, C.S., Zhang, F., Rajski, S.R., and Bugni, T.S. (2020). HCAPCA: Automated hierarchical clustering and principal component analysis of large metabolomic datasets in R. Metabolites, 10.","DOI":"10.3390\/metabo10070297"},{"key":"ref_64","unstructured":"Nicholas, K.B. (1997). GeneDoc: Analysis and visualization of genetic variation. EMBnet News, 4."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"1870","DOI":"10.1093\/molbev\/msw054","article-title":"MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets","volume":"33","author":"Kumar","year":"2016","journal-title":"Mol. Biol. Evol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1194","DOI":"10.1016\/j.molp.2020.06.009","article-title":"TBtools: An integrative toolkit developed for interactive analyses of big biological data","volume":"13","author":"Chen","year":"2020","journal-title":"Mol. Plant"}],"container-title":["Plants"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2223-7747\/13\/19\/2692\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T16:03:06Z","timestamp":1760112186000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2223-7747\/13\/19\/2692"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,9,25]]},"references-count":66,"journal-issue":{"issue":"19","published-online":{"date-parts":[[2024,10]]}},"alternative-id":["plants13192692"],"URL":"https:\/\/doi.org\/10.3390\/plants13192692","relation":{},"ISSN":["2223-7747"],"issn-type":[{"value":"2223-7747","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,9,25]]}}}