Water deficiency is one of the most significant abiotic stresses that negatively affects growth and reduces crop yields worldwide. Most research is focused on model plants and/or crops which are most agriculturally important. In this research, drought stress was applied to two drought stress contrasting varieties of Papaver somniferum (the opium poppy), a non-model plant species, during the first week of its germination, which differ in responses to drought stress. After sowing, the poppy seedlings were immediately subjected to drought stress for 7 days. We conducted a large-scale transcriptomic and proteomic analysis for drought stress response. At first, we found that the transcriptomic and proteomic profiles significantly differ. However, the most significant findings are the identification of key genes and proteins with significantly different expressions relating to drought stress, e.g., the heat-shock protein family, dehydration responsive element-binding transcription factors, ubiquitin E3 ligase, and others. In addition, metabolic pathway analysis showed that these genes and proteins were part of several biosynthetic pathways most significantly related to photosynthetic processes, and oxidative stress responses. A future study will focus on a detailed analysis of key genes and the development of selection markers for the determination of drought-resistant varieties and the breeding of new resistant lineages.

Department of Biology and Ecology Faculty of Science University of Ostrava Chittussiho 10 710 00 Ostrava Czech Republic

Department of Genetics and Agricultural Biotechnology Faculty of Agriculture University of South Bohemia Studentská 1668 370 05 České Budějovice Czech Republic

Research Institute of Oilseed Crops OSEVA PRO Ltd Purkyňova 10 764 01 Opava Czech Republic

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Rollins J.A., Habte E., Templer S.E., Colby T., Schmidt J., Von Korff M. Leaf Proteome Alterations in the Context of Physiological and Morphological Responses to Drought and Heat Stress in Barley (Hordeum vulgare L.) J. Exp. Bot. 2013;64:3201–3212. doi: 10.1093/jxb/ert158. PubMed DOI PMC

Zougmoré R.B., Partey S.T., Ouédraogo M., Torquebiau E., Campbell B.M. Facing Climate Variability in Sub-Saharan Africa: Analysis of Climate-Smart Agriculture Opportunities to Manage Climate-Related Risks. Cah. Agric. 2018;27:3400. doi: 10.1051/cagri/2018019. DOI

Neha P., Kumar M., Solankey S.S. Impact of Drought and Salinity on Vegetable Crops and Mitigation Strategies. In: Solankey S.S., Kumari M., Kumar M., editors. Advances in Research on Vegetable Production Under a Changing Climate Vol. 1. Springer International Publishing; Cham, Switzerland: 2021. pp. 235–253. Advances in Olericulture.

Singh D., Laxmi A. Transcriptional Regulation of Drought Response: A Tortuous Network of Transcriptional Factors. Front. Plant Sci. 2015;6:895. doi: 10.3389/fpls.2015.00895. PubMed DOI PMC

Xiong Q., Cao C., Shen T., Zhong L., He H., Chen X. Comprehensive Metabolomic and Proteomic Analysis in Biochemical Metabolic Pathways of Rice Spikes under Drought and Submergence Stress. Biochim. Biophys. Acta (BBA) Proteins Proteom. 2019;1867:237–247. doi: 10.1016/j.bbapap.2019.01.001. PubMed DOI

Dias M.C., Pinto D.C.G.A., Figueiredo C., Santos C., Silva A.M.S. Phenolic and Lipophilic Metabolite Adjustments in Olea Europaea (Olive) Trees during Drought Stress and Recovery. Phytochemistry. 2021;185:112695. doi: 10.1016/j.phytochem.2021.112695. PubMed DOI

Fahad S., Bajwa A.A., Nazir U., Anjum S.A., Farooq A., Zohaib A., Sadia S., Nasim W., Adkins S., Saud S. Crop Production under Drought and Heat Stress: Plant Responses and Management Options. Front. Plant Sci. 2017;8:1147. doi: 10.3389/fpls.2017.01147. PubMed DOI PMC

Anjum S.A., Ashraf U., Tanveer M., Khan I., Hussain S., Shahzad B., Zohaib A., Abbas F., Saleem M.F., Ali I. Drought Induced Changes in Growth, Osmolyte Accumulation and Antioxidant Metabolism of Three Maize Hybrids. Front. Plant Sci. 2017;8:69. doi: 10.3389/fpls.2017.00069. PubMed DOI PMC

Halliwell B. Reactive Species and Antioxidants. Redox Biology Is a Fundamental Theme of Aerobic Life. Plant Physiol. 2006;141:312–322. doi: 10.1104/pp.106.077073. PubMed DOI PMC

Shinozaki K., Yamaguchi-Shinozaki K. Gene Networks Involved in Drought Stress Response and Tolerance. J. Exp. Bot. 2007;58:221–227. doi: 10.1093/jxb/erl164. PubMed DOI

Mahmood T., Khalid S., Abdullah M., Ahmed Z., Shah M.K.N., Ghafoor A., Du X. Insights into Drought Stress Signaling in Plants and the Molecular Genetic Basis of Cotton Drought Tolerance. Cells. 2020;9:105. doi: 10.3390/cells9010105. PubMed DOI PMC

Pour-Benab S.M., Fabriki-Ourang S., Mehrabi A.-A. Expression of Dehydrin and Antioxidant Genes and Enzymatic Antioxidant Defense under Drought Stress in Wild Relatives of Wheat. Biotechnol. Biotechnol. Equip. 2019;33:1063–1073. doi: 10.1080/13102818.2019.1638300. DOI

Ennajeh M., Vadel A.M., Khemira H. Osmoregulation and Osmoprotection in the Leaf Cells of Two Olive Cultivars Subjected to Severe Water Deficit. Acta Physiol. Plant. 2009;31:711–721. doi: 10.1007/s11738-009-0283-6. DOI

Cuevas-Velazquez C.L., Reyes J.L., Covarrubias A.A. Group 4 Late Embryogenesis Abundant Proteins as a Model to Study Intrinsically Disordered Proteins in Plants. Plant Signal. Behav. 2017;12:e1343777. doi: 10.1080/15592324.2017.1343777. PubMed DOI PMC

Rodziewicz P., Swarcewicz B., Chmielewska K., Wojakowska A., Stobiecki M. Influence of Abiotic Stresses on Plant Proteome and Metabolome Changes. Acta Physiol. Plant. 2014;36:1–19. doi: 10.1007/s11738-013-1402-y. DOI

Liu H., Yang Y., Liu D., Wang X., Zhang L. Transcription Factor TabHLH49 Positively Regulates Dehydrin WZY2 Gene Expression and Enhances Drought Stress Tolerance in Wheat. BMC Plant Biol. 2020;20:259. doi: 10.1186/s12870-020-02474-5. PubMed DOI PMC

Abedini R., GhaneGolmohammadi F., PishkamRad R., Pourabed E., Jafarnezhad A., Shobbar Z.-S., Shahbazi M. Plant Dehydrins: Shedding Light on Structure and Expression Patterns of Dehydrin Gene Family in Barley. J. Plant Res. 2017;130:747–763. doi: 10.1007/s10265-017-0941-5. PubMed DOI

Kumar T., Tiwari N., Bharadwaj C., Sarker A., Pappula S.P.R., Singh S., Singh M. Identification of Allelic Variation in Drought Responsive Dehydrin Gene Based on Sequence Similarity in Chickpea (Cicer arietinum L.) Front. Genet. 2020;11:1579. doi: 10.3389/fgene.2020.584527. PubMed DOI PMC

Čepl J., Stejskal J., Korecký J., Hejtmánek J., Faltinová Z., Lstibůrek M., Gezan S. The Dehydrins Gene Expression Differs across Ecotypes in Norway Spruce and Relates to Weather Fluctuations. Sci. Rep. 2020;10:20789. doi: 10.1038/s41598-020-76900-x. PubMed DOI PMC

Vaseva I., Akiscan Y., Demirevska K., Anders I., Feller U. Drought Stress Tolerance of Red and White Clover–Comparative Analysis of Some Chaperonins and Dehydrins. Sci. Hortic. 2011;130:653–659. doi: 10.1016/j.scienta.2011.08.021. DOI

Beaudoin G.A., Facchini P.J. Benzylisoquinoline Alkaloid Biosynthesis in Opium Poppy. Planta. 2014;240:19–32. doi: 10.1007/s00425-014-2056-8. PubMed DOI

Marciano M.A., Panicker S.X., Liddil G.D., Lindgren D., Sweder K.S. Development of a Method to Extract Opium Poppy (Papaver somniferum L.) DNA from Heroin. Sci. Rep. 2018;8:2509. PubMed PMC

Zhang Z., Li C., Zhang J., Chen F., Gong Y., Li Y., Su Y., Wei Y., Zhao Y. Selection of the Reference Gene for Expression Normalization in Papaver Somniferum L. under Abiotic Stress and Hormone Treatment. Genes. 2020;11:124. doi: 10.3390/genes11020124. PubMed DOI PMC

Dąbrowski G., Czaplicki S., Konopka I. Composition and Quality of Poppy (Papaver somniferum L.) Seed Oil Depending on the Extraction Method. LWT. 2020;134:110167. doi: 10.1016/j.lwt.2020.110167. DOI

Solanki G., Dodiya N.S., Kunwar R., Bisen P., Kumar R., Singh J.S. Character Association and Path Coefficient Analysis for Seed Yield and Latex Yield in Opium Poppy (Papaver somniferum L.) Int. J. Curr. Microbiol. Appl. Sci. 2017;6:1116–1123. doi: 10.20546/ijcmas.2017.608.138. DOI

Özcan M.M., Atalay Ç. Determination of Seed and Oil Properties of Some Poppy (Papaver somniferum L.) Varieties. Grasas Y Aceites. 2006;57:169–174.

Prochazka P., Smutka L. Czech Republic as an Important Producer of Poppy Seed. Agris-Line Pap. Econ. Inform. 2012;4:35–47.

Zhao Y., Gao C., Shi F., Yun L., Jia Y., Wen J. Transcriptomic and Proteomic Analyses of Drought Responsive Genes and Proteins in Agropyron Mongolicum Keng. Curr. Plant Biol. 2018;14:19–29. doi: 10.1016/j.cpb.2018.09.005. DOI

Li C., Wang Z., Nong Q., Lin L., Xie J., Mo Z., Huang X., Song X., Malviya M.K., Solanki M.K., et al. Physiological Changes and Transcriptome Profiling in Saccharum Spontaneum L. Leaf under Water Stress and Re-Watering Conditions. Sci. Rep. 2021;11:5525. doi: 10.1038/s41598-021-85072-1. PubMed DOI PMC

Peng Z., Wang M., Li F., Lv H., Li C., Xia G. A Proteomic Study of the Response to Salinity and Drought Stress in an Introgression Strain of Bread Wheat. Mol. Cell. Proteom. 2009;8:2676–2686. doi: 10.1074/mcp.M900052-MCP200. PubMed DOI PMC

Li J., Wang Y., Wang L., Zhu J., Deng J., Tang R., Chen G. Integration of Transcriptomic and Proteomic Analyses for Finger Millet [Eleusine Coracana (L.) Gaertn.] in Response to Drought Stress. PLoS ONE. 2021;16:e0247181. doi: 10.1371/journal.pone.0247181. PubMed DOI PMC

Andersen S.B. Plant Breeding from Laboratories to Fields. University of Copenhagen; Copenhagen, Denmark: 2013.

Riyazuddin R., Nisha N., Singh K., Verma R., Gupta R. Involvement of Dehydrin Proteins in Mitigating the Negative Effects of Drought Stress in Plants. Plant Cell Rep. 2021 doi: 10.1007/s00299-021-02720-6. PubMed DOI

Davik J., Koehler G., From B., Torp T., Rohloff J., Eidem P., Wilson R.C., Sønsteby A., Randall S.K., Alsheikh M. Dehydrin, Alcohol Dehydrogenase, and Central Metabolite Levels Are Associated with Cold Tolerance in Diploid Strawberry (Fragaria Spp.) Planta. 2013;237:265–277. doi: 10.1007/s00425-012-1771-2. PubMed DOI

Kim S.Y., Nam K.H. Physiological Roles of ERD10 in Abiotic Stresses and Seed Germination of Arabidopsis. Plant Cell Rep. 2010;29:203–209. doi: 10.1007/s00299-009-0813-0. PubMed DOI

Šunderlíková V., Wilhelm E. High Accumulation of Legumin and Lea-like MRNAs during Maturation Is Associated with Increased Conversion Frequency of Somatic Embryos from Pedunculate Oak (Quercus robur L.) Protoplasma. 2002;220:97–103. doi: 10.1007/s00709-002-0025-8. PubMed DOI

Wang R.Y., Wang H.G., Liu X.Y., Lian S., Chen L., Qiao Z.J., McInerney C.E., Wang L. Drought-Induced Transcription of Resistant and Sensitive Common Millet Varieties. J. Anim. Plant Sci. 2017;27:1303–1314.

Morales-Merida B.E., Villicaña C., Perales-Torres A.L., Martínez-Montoya H., Castillo-Ruiz O., León-Chan R., Lighbourn-Rojas L.A., Heredia J.B., León-Félix J. Transcriptomic Analysis in Response to Combined Stress by UV-B Radiation and Cold in Belle Pepper (Capsicum annuum) Int. J. Agric. Biol. 2021;25:1–12.

Bettencourt B.R., Hogan C.C., Nimali M., Drohan B.W. Inducible and Constitutive Heat Shock Gene Expression Responds to Modification of Hsp70 Copy Number in Drosophila Melanogaster but Does Not Compensate for Loss of Thermotolerance in Hsp70 Null Flies. BMC Biol. 2008;6:5. doi: 10.1186/1741-7007-6-5. PubMed DOI PMC

Ge S.X., Jung D., Yao R. ShinyGO: A Graphical Gene-Set Enrichment Tool for Animals and Plants. Bioinformatics. 2020;36:2628–2629. doi: 10.1093/bioinformatics/btz931. PubMed DOI PMC

Department of Primary Industries, Parks, Water and Environment Best Practice Poppy Growing Guide. [(accessed on 10 August 2021)];2019 Available online: https://dpipwe.tas.gov.au/agriculture/plant-industries/best-practice-poppy-growing-guide.

Verma G., Srivastava D., Tiwari P., Chakrabarty D. Reactive Oxygen, Nitrogen and Sulfur Species in Plants. John Wiley & Sons, Ltd.; Hoboken, NJ, USA: 2019. ROS Modulation in Crop Plants Under Drought Stress; pp. 311–336.

Deeba F., Pandey A.K., Ranjan S., Mishra A., Singh R., Sharma Y.K., Shirke P.A., Pandey V. Physiological and Proteomic Responses of Cotton (Gossypium herbaceum L.) to Drought Stress. Plant Physiol. Biochem. 2012;53:6–18. doi: 10.1016/j.plaphy.2012.01.002. PubMed DOI

Sharma S., Villamor J.G., Verslues P.E. Essential Role of Tissue-Specific Proline Synthesis and Catabolism in Growth and Redox Balance at Low Water Potential. Plant Physiol. 2011;157:292–304. doi: 10.1104/pp.111.183210. PubMed DOI PMC

Blum A. Osmotic Adjustment Is a Prime Drought Stress Adaptive Engine in Support of Plant Production. Plant Cell Environ. 2017;40:4–10. doi: 10.1111/pce.12800. PubMed DOI

Graether S.P., Boddington K.F. Disorder and Function: A Review of the Dehydrin Protein Family. Front. Plant Sci. 2014;5:576. doi: 10.3389/fpls.2014.00576. PubMed DOI PMC

Hara M., Shinoda Y., Tanaka Y., Kuboi T. DNA Binding of Citrus Dehydrin Promoted by Zinc Ion. Plant Cell Environ. 2009;32:532–541. doi: 10.1111/j.1365-3040.2009.01947.x. PubMed DOI

Saucedo A.L., Hernández-Domínguez E.E., de Luna-Valdez L.A., Guevara-García A.A., Escobedo-Moratilla A., Bojorquéz-Velázquez E., Del Río-Portilla F., Fernández-Velasco D.A., Barba de la Rosa A.P. Insights on Structure and Function of a Late Embryogenesis Abundant Protein from Amaranthus Cruentus: An Intrinsically Disordered Protein Involved in Protection against Desiccation, Oxidant Conditions, and Osmotic Stress. Front. Plant Sci. 2017;8:497. doi: 10.3389/fpls.2017.00497. PubMed DOI PMC

Jing H., Li C., Ma F., Ma J.-H., Khan A., Wang X., Zhao L.-Y., Gong Z.-H., Chen R.-G. Genome-Wide Identification, Expression Diversication of Dehydrin Gene Family and Characterization of CaDHN3 in Pepper (Capsicum annuum L.) PLoS ONE. 2016;11:e0161073. doi: 10.1371/journal.pone.0161073. PubMed DOI PMC

Egerton-Warburton L.M., Balsamo R.A., Close T.J. Temporal Accumulation and Ultrastructural Localization of Dehydrins in Zea Mays. Physiol. Plant. 1997;101:545–555. doi: 10.1111/j.1399-3054.1997.tb01036.x. DOI

Verma G., Dhar Y.V., Srivastava D., Kidwai M., Chauhan P.S., Bag S.K., Asif M.H., Chakrabarty D. Genome-Wide Analysis of Rice Dehydrin Gene Family: Its Evolutionary Conservedness and Expression Pattern in Response to PEG Induced Dehydration Stress. PLoS ONE. 2017;12:e0176399. doi: 10.1371/journal.pone.0176399. PubMed DOI PMC

Ruan J., Zhou Y., Zhou M., Yan J., Khurshid M., Weng W., Cheng J., Zhang K. Jasmonic Acid Signaling Pathway in Plants. Int. J. Mol. Sci. 2019;20:2479. doi: 10.3390/ijms20102479. PubMed DOI PMC

Liu J., Wang R., Liu W., Zhang H., Guo Y., Wen R. Genome-Wide Characterization of Heat-Shock Protein 70s from Chenopodium Quinoa and Expression Analyses of Cqhsp70s in Response to Drought Stress. Genes. 2018;9:35. doi: 10.3390/genes9020035. PubMed DOI PMC

Sato Y., Yokoya S. Enhanced Tolerance to Drought Stress in Transgenic Rice Plants Overexpressing a Small Heat-Shock Protein, SHSP17.7. Plant Cell Rep. 2008;27:329–334. doi: 10.1007/s00299-007-0470-0. PubMed DOI

Jacob P., Hirt H., Bendahmane A. The Heat-Shock Protein/Chaperone Network and Multiple Stress Resistance. Plant Biotechnol. J. 2017;15:405–414. doi: 10.1111/pbi.12659. PubMed DOI PMC

Ye S., Yu S., Shu L., Wu J., Wu A., Luo L. Expression Profile Analysis of 9 Heat Shock Protein Genes throughout the Life Cycle and under Abiotic Stress in Rice. Chin. Sci. Bull. 2012;57:336–343. doi: 10.1007/s11434-011-4863-7. DOI

Wang G., Cai G., Kong F., Deng Y., Ma N., Meng Q. Overexpression of Tomato Chloroplast-Targeted DnaJ Protein Enhances Tolerance to Drought Stress and Resistance to Pseudomonas Solanacearum in Transgenic Tobacco. Plant Physiol. Biochem. 2014;82:95–104. doi: 10.1016/j.plaphy.2014.05.011. PubMed DOI

Xia Z., Zhang X., Li J., Su X., Liu J. Overexpression of a Tobacco J-Domain Protein Enhances Drought Tolerance in Transgenic Arabidopsis. Plant Physiol. Biochem. 2014;83:100–106. doi: 10.1016/j.plaphy.2014.07.023. PubMed DOI

Nakashima K., Yamaguchi-Shinozaki K., Shinozaki K. The Transcriptional Regulatory Network in the Drought Response and Its Crosstalk in Abiotic Stress Responses Including Drought, Cold, and Heat. Front. Plant Sci. 2014;5:170. doi: 10.3389/fpls.2014.00170. PubMed DOI PMC

Dossa K., Wei X., Li D., Fonceka D., Zhang Y., Wang L., Yu J., Boshou L., Diouf D., Cissé N., et al. Insight into the AP2/ERF Transcription Factor Superfamily in Sesame and Expression Profiling of DREB Subfamily under Drought Stress. BMC Plant Biol. 2016;16:171. doi: 10.1186/s12870-016-0859-4. PubMed DOI PMC

Ding S., Zhang B., Qin F. Arabidopsis RZFP34/CHYR1, a Ubiquitin E3 Ligase, Regulates Stomatal Movement and Drought Tolerance via SnRK2.6-Mediated Phosphorylation. Plant Cell. 2015;27:3228–3244. doi: 10.1105/tpc.15.00321. PubMed DOI PMC

Zhou S., Li M., Guan Q., Liu F., Zhang S., Chen W., Yin L., Qin Y., Ma F. Physiological and Proteome Analysis Suggest Critical Roles for the Photosynthetic System for High Water-Use Efficiency under Drought Stress in Malus. Plant Sci. 2015;236:44–60. doi: 10.1016/j.plantsci.2015.03.017. PubMed DOI

Sarwar M.B., Ahmad Z., Rashid B., Hassan S., Gregersen P.L., Leyva M.D., Nagy I., Asp T., Husnain T. De Novo Assembly of Agave Sisalana Transcriptome in Response to Drought Stress Provides Insight into the Tolerance Mechanisms. Sci. Rep. 2019;9:396. doi: 10.1038/s41598-018-35891-6. PubMed DOI PMC

Saito K., Yonekura-Sakakibara K., Nakabayashi R., Higashi Y., Yamazaki M., Tohge T., Fernie A.R. The Flavonoid Biosynthetic Pathway in Arabidopsis: Structural and Genetic Diversity. Plant Physiol. Biochem. 2013;72:21–34. doi: 10.1016/j.plaphy.2013.02.001. PubMed DOI

Halbwirth H. The Creation and Physiological Relevance of Divergent Hydroxylation Patterns in the Flavonoid Pathway. Int. J. Mol. Sci. 2010;11:595–621. doi: 10.3390/ijms11020595. PubMed DOI PMC

Yao X., Wang T., Wang H., Liu H., Liu S., Zhao Q., Chen K., Zhang P. Identification, Characterization and Expression Analysis of the Chalcone Synthase Family in the Antarctic Moss Pohlia nutans. Antarct. Sci. 2019;31:23–33. doi: 10.1017/S0954102018000470. DOI

Jiang L., Gao Q.C., Chen Z.P., Zhang J.J., Bai X.Y., He X.L., Xu Q.X. Selenium Tolerance of an Arabidopsis Drought-Resistant Mutant Csm1-1. Russ. J. Plant Physiol. 2015;62:625–631. doi: 10.1134/S102144371505009X. DOI

Azzouz-Olden F., Hunt A.G., Dinkins R. Transcriptome Analysis of Drought-Tolerant Sorghum Genotype SC56 in Response to Water Stress Reveals an Oxidative Stress Defense Strategy. Mol. Biol. Rep. 2020;47:3291–3303. doi: 10.1007/s11033-020-05396-5. PubMed DOI PMC

Salekdeh G.H., Siopongco J., Wade L.J., Ghareyazie B., Bennett J. Proteomic Analysis of Rice Leaves during Drought Stress and Recovery. Proteomics. 2002;2:1131–1145. doi: 10.1002/1615-9861(200209)2:9<1131::AID-PROT1131>3.0.CO;2-1. PubMed DOI

Shiriga K., Sharma R., Chaudhary K., Yadav S., Hossain F. Expression Pattern of Superoxide Dismutase Under Drought Stress in Maize. Int. J. Innov. Res. Sci. Eng. Technol. 2014;3:11333–11337.

Weng M., Cui L., Liu F., Zhang M., Shan L., Yang S., Deng X.-P. Effects of Drought Stress on Antioxidant Enzymes in Seedlings of Different Wheat Genotypes. Pak. J. Bot. 2015;47:49–56.

Bolwell G.P., Bozak K., Zimmerlin A. Plant Cytochrome P450. Phytochemistry. 1994;37:1491–1506. doi: 10.1016/S0031-9422(00)89567-9. PubMed DOI

Ghodke P., Khandagale K., Thangasamy A., Kulkarni A., Narwade N., Shirsat D., Randive P., Roylawar P., Singh I., Gawande S.J., et al. Comparative Transcriptome Analyses in Contrasting Onion (Allium cepa L.) Genotypes for Drought Stress. PLoS ONE. 2020;15:e0237457. doi: 10.1371/journal.pone.0237457. PubMed DOI PMC

Duan F., Ding J., Lee D., Lu X., Feng Y., Song W. Overexpression of SoCYP85A1, a Spinach Cytochrome P450 Gene in Transgenic Tobacco Enhances Root Development and Drought Stress Tolerance. Front. Plant Sci. 2017;8:1909. doi: 10.3389/fpls.2017.01909. PubMed DOI PMC

Greenbaum D., Colangelo C., Williams K., Gerstein M. Comparing Protein Abundance and MRNA Expression Levels on a Genomic Scale. Genome Biol. 2003;4:117. doi: 10.1186/gb-2003-4-9-117. PubMed DOI PMC

Koussounadis A., Langdon S.P., Um I.H., Harrison D.J., Smith V.A. Relationship between Differentially Expressed MRNA and MRNA-Protein Correlations in a Xenograft Model System. Sci. Rep. 2015;5:10775. doi: 10.1038/srep10775. PubMed DOI PMC

de Sousa Abreu R., Penalva L.O., Marcotte E.M., Vogel C. Global Signatures of Protein and MRNA Expression Levels. Mol. Biosyst. 2009;5:1512–1526. doi: 10.1039/b908315d. PubMed DOI PMC

Andrews S. FastQC: A Quality Control Tool for High Throughput Sequence Data. Babraham Bioinformatics, Babraham Institute; Cambridge, UK: 2010.

Araújo M., Prada J., Mariz-Ponte N., Santos C., Pereira J.A., Pinto D.C.G.A., Silva A.M.S., Dias M.C. Antioxidant Adjustments of Olive Trees (Olea europaea) under Field Stress Conditions. Plants. 2021;10:684. doi: 10.3390/plants10040684. PubMed DOI PMC

Bolger A.M., Lohse M., Usadel B. Trimmomatic: A Flexible Trimmer for Illumina Sequence Data. Bioinformatics. 2014;30:2114–2120. doi: 10.1093/bioinformatics/btu170. PubMed DOI PMC

Szklarczyk D., Franceschini A., Wyder S., Forslund K., Heller D., Huerta-Cepas J., Simonovic M., Roth A., Santos A., Tsafou K.P. STRING V10: Protein–Protein Interaction Networks, Integrated over the Tree of Life. Nucleic Acids Res. 2015;43:D447–D452. doi: 10.1093/nar/gku1003. PubMed DOI PMC

New Low Morphine Opium Poppy Genotype Obtained by TILLING Approach