Transcriptome Analysis of Ethylene-Related Genes in Chlorine Dioxide-Treated Fresh-Cut Cauliflower
Abstract
:1. Introduction
2. Materials and Methods
2.1. Experimental Materials and Treatment Methods
2.2. RNA-Seq Analysis
3. Results
3.1. Transcriptome Sequencing Quality Assessment
3.2. Identification and Analysis of DEGs
3.3. Go Function Analysis of DEGs
3.4. KEGG Enrichment Analysis of DEGs
3.5. DEGs Involved in Ethylene-Related Response
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Avato, P.; Argentieri, M.P. Brassicaceae: A Rich Source of Health Improving Phytochemicals. Phytochem. Rev. 2015, 14, 1019–1033. [Google Scholar] [CrossRef]
- Li, Z.; Zheng, S.; Liu, Y.; Fang, Z.; Yang, L.; Zhuang, M.; Zhang, Y.; Lv, H.; Wang, Y.; Xu, D. Characterization of Glucosinolates in 80 Broccoli Genotypes and Different Organs Using UHPLC-Triple-TOF-MS Method. Food Chem. 2021, 334, 127519. [Google Scholar] [CrossRef] [PubMed]
- Morrison, M.E.W.; Hobika, E.G.; Joseph, J.M.; Stenzel, A.E.; Mongiovi, J.M.; Tang, L.; McCann, S.E.; Marshall, J.; Fountzilas, C.; Moysich, K.B. Cruciferous Vegetable Consumption and Pancreatic Cancer: A Case-Control Study. Cancer Epidemiol. 2021, 72, 101924. [Google Scholar] [CrossRef]
- Qinghang, W.; Zhang, C.; Zhang, J.; Xin, X.; Li, T.; He, C.; Zhao, S.; Liu, D. Variation in Glucosinolates and the Formation of Functional Degradation Products in Two Brassica Species during Spontaneous Fermentation. Curr. Res. Food Sci. 2023, 6, 100493. [Google Scholar] [CrossRef]
- Rasines, L.; Morera, S.; Miguel, G.S.; Artés-Hernández, F.; Aguayo, E. Environmental and Economic Sustainability of Fresh-Cut and Pre-Cooked Vegetables. Sci. Total Environ. 2023, 872, 162169. [Google Scholar] [CrossRef]
- Tawema, P.; Han, J.; Vu, K.D.; Salmieri, S.; Lacroix, M. Antimicrobial Effects of Combined UV-C or Gamma Radiation with Natural Antimicrobial Formulations against Listeria Monocytogenes, Escherichia coli O157: H7, and Total Yeasts/Molds in Fresh Cut Cauliflower. LWT-Food Sci. Technol. 2016, 65, 451–456. [Google Scholar] [CrossRef]
- Zhang, L.; Yu, X.; Yagoub, A.E.A.; Owusu-Ansah, P.; Wahia, H.; Ma, H.; Zhou, C. Effects of Low Frequency Multi-Mode Ultrasound and It’s Washing Solution’s Interface Properties on Freshly Cut Cauliflower. Food Chem. 2022, 366, 130683. [Google Scholar] [CrossRef] [PubMed]
- Vaishnav, J.; Srivastava, A.K.; Mishra, B.B.; Suprasanna, P.; Variyar, P.S. Glucosinolates Breakdown and Enhanced Nitrile Formation in Gamma Irradiated Minimally Processed Cauliflower (Brassica oleracia). Radiat. Phys. Chem. 2023, 205, 110672. [Google Scholar] [CrossRef]
- Jiang, Q.; Zhang, M.; Mujumdar, A.S.; Chen, B. Comparative Freezing Study of Broccoli and Cauliflower: Effects of Electrostatic Field and Static Magnetic Field. Food Chem. 2022, 397, 133751. [Google Scholar] [CrossRef]
- Nasrin, T.A.A.; Yasmin, L.; Arfin, M.S.; Rahman, A.; Molla, M.M.; Sabuz, A.A.; Afroz, M. Preservation of Postharvest Quality of Fresh Cut Cauliflower through Simple and Easy Packaging Techniques. Appl. Food Res. 2022, 2, 100125. [Google Scholar] [CrossRef]
- Chen, Z. Application of Chlorine Dioxide-Based Hurdle Technology to Improve Microbial Food Safety–A Review. Int. J. Food Microbiol. 2022, 379, 109848. [Google Scholar] [CrossRef]
- Deng, L.-Z.; Mujumdar, A.S.; Pan, Z.; Vidyarthi, S.K.; Xu, J.; Zielinska, M.; Xiao, H.-W. Emerging Chemical and Physical Disinfection Technologies of Fruits and Vegetables: A Comprehensive Review. Crit. Rev. Food Sci. Nutr. 2020, 60, 2481–2508. [Google Scholar] [CrossRef]
- Malka, S.K.; Park, M.-H. Fresh Produce Safety and Quality: Chlorine Dioxide’s Role. Front. Plant Sci. 2022, 12, 775629. [Google Scholar] [CrossRef]
- Jiang, L.; Chen, Z.; Liu, L.; Wang, M.; Liu, Y.; Yu, Z. Effect of Chlorine Dioxide on Decontamination of Fresh-cut Coriander and Identification of Bacterial Species in Fresh-cutting Process. J. Food Process Preserv. 2018, 42, e13465. [Google Scholar] [CrossRef]
- Zhu, X.; Hui, S.; Huang, H.; Liu, R.; Wang, S.; Huang, C. Antimicrobial Mechanism of Chlorine Dioxide and Its Impacts on Postharvest Management in Horticultural Produce: A Review. Postharvest Biol. Technol. 2024, 213, 112921. [Google Scholar] [CrossRef]
- Chen, Z.; Zhu, C.; Zhang, Y.; Niu, D.; Du, J. Effects of Aqueous Chlorine Dioxide Treatment on Enzymatic Browning and Shelf-Life of Fresh-Cut Asparagus Lettuce (Lactuca sativa L.). Postharvest Biol. Technol. 2010, 58, 232–238. [Google Scholar] [CrossRef]
- Yang, H.; Zheng, J.; Huang, C.; Zhao, X.; Chen, H.; Sun, Z. Effects of Combined Aqueous Chlorine Dioxide and Chitosan Coatings on Microbial Growth and Quality Maintenance of Fresh-Cut Bamboo Shoots (Phyllostachys praecox f. prevernalis.) during Storage. Food Bioprocess. Technol. 2015, 8, 1011–1019. [Google Scholar] [CrossRef]
- Lin, Q.; Luo, Z.; Jiang, Y.; Li, D.; Lin, X.; Jiang, Y.; Li, L. Role of Chlorine Dioxide and Chloroxyanions Residue in Yellowing Alleviation of Ready-to-Eat Broccoli: Insights from Transcriptomic Evidence. Postharvest Biol. Technol. 2022, 194, 112103. [Google Scholar] [CrossRef]
- McMurchie, E.J.; McGlasson, W.B.; Eaks, I.L. Treatment of Fruit with Propylene Gives Information about the Biogenesis of Ethylene. Nature 1972, 237, 235–236. [Google Scholar] [CrossRef]
- Gu, S.; Xie, L.; Guan, Q.; Sheng, X.; Fang, Y.; Wang, X. Effect of Ethylene Production by Four Pathogenic Fungi on the Postharvest Diseases of Green Pepper (Capsicum annuum L.). Int. J. Food Microbiol. 2024, 418, 110729. [Google Scholar] [CrossRef]
- Huang, J.; Zhao, X.; Bürger, M.; Wang, Y.; Chory, J. Two Interacting Ethylene Response Factors Regulate Heat Stress Response. Plant Cell 2021, 33, 338–357. [Google Scholar] [CrossRef] [PubMed]
- Yu, W.; Shen, L.; Sheng, J. Synergistic Effects of SlCBF1 and Ethylene Signaling on the Maintenance of Tomatoes Quality during Long-Term Cold Storage. Postharvest Biol. Technol. 2024, 217, 113090. [Google Scholar] [CrossRef]
- Huang, J.; Zhao, X.; Bürger, M.; Chory, J.; Wang, X. The Role of Ethylene in Plant Temperature Stress Response. Trends Plant Sci. 2023, 28, 808–824. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Y.; Qiu, J.; Yang, K.; Lu, Y.; Xu, Z.; Yang, H.; Xu, Y.; Wang, L.; Lin, Y.; Tong, X.; et al. Generation, Mechanisms, Kinetics, and Effects of Gaseous Chlorine Dioxide in Food Preservation. Comp. Rev. Food Sci. Food Safe 2023, 22, 3105–3129. [Google Scholar] [CrossRef]
- Praeger, U.; Herppich, W.B.; Hassenberg, K. Aqueous Chlorine Dioxide Treatment of Horticultural Produce: Effects on Microbial Safety and Produce Quality—A Review. Crit. Rev. Food Sci. Nutr. 2018, 58, 318–333. [Google Scholar] [CrossRef] [PubMed]
- Ran, Y.; Qingmin, C.; Maorun, F. Chlorine Dioxide Generation Method and Its Action Mechanism for Removing Harmful Substances and Maintaining Quality Attributes of Agricultural Products. Food Bioprocess. Technol. 2019, 12, 1110–1122. [Google Scholar] [CrossRef]
- Mu, Y.; Feng, Y.; Wei, L.; Li, C.; Cai, G.; Zhu, T. Combined Effects of Ultrasound and Aqueous Chlorine Dioxide Treatments on Nitrate Content during Storage and Postharvest Storage Quality of Spinach (Spinacia oleracea L.). Food Chem. 2020, 333, 127500. [Google Scholar] [CrossRef] [PubMed]
- Sadeghi, K.; Kasi, G.; Ketsuk, P.; Thanakkasaranee, S.; Bahadar Khan, S.; Seo, J. A Polymeric Chlorine Dioxide Self-Releasing Sheet to Prolong Postharvest Life of Cherry Tomatoes. Postharvest Biol. Technol. 2020, 161, 111040. [Google Scholar] [CrossRef]
- Sumimoto, H. Structure, Regulation and Evolution of Nox-family NADPH Oxidases That Produce Reactive Oxygen Species. FEBS J. 2008, 275, 3249–3277. [Google Scholar] [CrossRef]
- Yang, S.; Wang, J.; Tang, Z.; Li, Y.; Zhang, J.; Guo, F.; Meng, J.; Cui, F.; Li, X.; Wan, S. Calcium/Calmodulin Modulates Salt Responses by Binding a Novel Interacting Protein SAMS1 in Peanut (Arachis hypogaea L.). Crop J. 2023, 11, 21–32. [Google Scholar] [CrossRef]
- Koo, J.C.; Lee, I.C.; Dai, C.; Lee, Y.; Cho, H.K.; Kim, Y.; Phee, B.-K.; Kim, H.; Lee, I.H.; Choi, S.H.; et al. The Protein Trio RPK1–CaM4–RbohF Mediates Transient Superoxide Production to Trigger Age-Dependent Cell Death in Arabidopsis. Cell Rep. 2017, 21, 3373–3380. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.; Wei, Y.; Jiang, S.; Ye, J.; Chen, Y.; Xu, F.; Shao, X. Transcriptome Analysis Reveals That Trehalose Alleviates Chilling Injury of Peach Fruit by Regulating ROS Signaling Pathway and Enhancing Antioxidant Capacity. Food Res. Int. 2024, 186, 114331. [Google Scholar] [CrossRef] [PubMed]
- Beaugelin, I.; Chevalier, A.; D’Alessandro, S.; Ksas, B.; Novák, O.; Strnad, M.; Forzani, C.; Hirt, H.; Havaux, M.; Monnet, F. OXI1 and DAD Regulate Light-Induced Cell Death Antagonistically through Jasmonate and Salicylate Levels. Plant Physiol. 2019, 180, 1691–1708. [Google Scholar] [CrossRef]
- Rawat, A.A.; Hartmann, M.; Harzen, A.; Lugan, R.; Stolze, S.C.; Forzani, C.; Abts, L.; Reißenweber, S.; Rayapuram, N.; Nakagami, H.; et al. OXIDATIVE SIGNAL-INDUCIBLE1 Induces Immunity by Coordinating N-hydroxypipecolic Acid, Salicylic Acid, and Camalexin Synthesis. New Phytol. 2023, 237, 1285–1301. [Google Scholar] [CrossRef]
- Chen, L.; Li, X.; He, T.; Li, P.; Liu, Y.; Zhou, S.; Wu, Q.; Chen, T.; Lu, Y.; Hou, Y. Comparative Biochemical and Transcriptome Analyses in Tomato and Eggplant Reveal Their Differential Responses to Tuta absoluta Infestation. Genomics 2021, 113, 2108–2121. [Google Scholar] [CrossRef]
- Hailemariam, S.; Liao, C.-J.; Mengiste, T. Receptor-like Cytoplasmic Kinases: Orchestrating Plant Cellular Communication. Trends Plant Sci. 2024, in press. [CrossRef]
- Li, C.; Wang, K.; Tan, M.; Lei, C.; Cao, S. Involvement of a Receptor-like Kinase Complex of FvFLS2 and FvBAK1 in Brassinosteroids-Induced Immunity in Postharvest Strawberry Fruit. Postharvest Biol. Technol. 2023, 198, 112266. [Google Scholar] [CrossRef]
- Zhao, Q.; Bao, J.; Li, H.; Hu, W.; Kong, Y.; Zhong, Y.; Fu, Q.; Xu, G.; Liu, F.; Jiao, X.; et al. Structural and Biochemical Basis of FLS2-Mediated Signal Activation and Transduction in Rice. Plant Commun. 2024, 5, 100785. [Google Scholar] [CrossRef]
- He, X.; Wang, L.; Tao, J.; Han, L.; Wang, H.; Zhao, X.; Zuo, J.; Zheng, Y. High-oxygen-Modified Atmospheric Packaging Delays Flavor and Quality Deterioration in Fresh-Cut Broccoli. Food Chem. 2024, 450, 139517. [Google Scholar] [CrossRef] [PubMed]
- Wang, T.; Sun, Z.; Wang, S.; Feng, S.; Wang, R.; Zhu, C.; Zhong, L.; Cheng, Y.; Bao, M.; Zhang, F. DcWRKY33 Promotes Petal Senescence in Carnation (Dianthus caryophyllus L.) by Activating Genes Involved in the Biosynthesis of Ethylene and Abscisic Acid and Accumulation of Reactive Oxygen Species. Plant J. 2023, 113, 698–715. [Google Scholar] [CrossRef]
- Yang, L.; Ye, C.; Zhao, Y.; Cheng, X.; Wang, Y.; Jiang, Y.-Q.; Yang, B. An Oilseed Rape WRKY-Type Transcription Factor Regulates ROS Accumulation and Leaf Senescence in Nicotiana Benthamiana and Arabidopsis through Modulating Transcription of RbohD and RbohF. Planta 2018, 247, 1323–1338. [Google Scholar] [CrossRef]
- Guo, Q.; Wu, B.; Peng, X.; Wang, J.; Li, Q.; Jin, J.; Ha, Y. Effects of Chlorine Dioxide Treatment on Respiration Rate and Ethylene Synthesis of Postharvest Tomato Fruit. Postharvest Biol. Technol. 2014, 93, 9–14. [Google Scholar] [CrossRef]
- Guo, Q.; Lv, X.; Xu, F.; Zhang, Y.; Wang, J.; Lin, H.; Wu, B. Chlorine Dioxide Treatment Decreases Respiration and Ethylene Synthesis in Fresh-cut ‘ H Ami’ Melon Fruit. Int. J. Food Sci. Tech. 2013, 48, 1775–1782. [Google Scholar] [CrossRef]
- Yang, S.; Zhou, J.; Watkins, C.B.; Wu, C.; Feng, Y.; Zhao, X.; Xue, Z.; Kou, X. NAC Transcription Factors SNAC4 and SNAC9 Synergistically Regulate Tomato Fruit Ripening by Affecting Expression of Genes Involved in Ethylene and Abscisic Acid Metabolism and Signal Transduction. Postharvest Biol. Technol. 2021, 178, 111555. [Google Scholar] [CrossRef]
- He, Y.; Xue, J.; Li, H.; Han, S.; Jiao, J.; Rao, J. Ethylene Response Factors Regulate Ethylene Biosynthesis and Cell Wall Modification in Persimmon (Diospyros kaki L.) Fruit during Ripening. Postharvest Biol. Technol. 2020, 168, 111255. [Google Scholar] [CrossRef]
- Wu, W.; Wang, M.; Gong, H.; Liu, X.; Guo, D.; Sun, N.; Huang, J.; Zhu, Q.; Chen, K.; Yin, X. High CO2/Hypoxia-Induced Softening of Persimmon Fruit Is Modulated by DkERF8/16 and DkNAC9 Complexes. J. Exp. Bot. 2020, 71, 2690–2700. [Google Scholar] [CrossRef] [PubMed]
- Ghimire, U.; Abeli, P.; Brecht, J.K.; Pliakoni, E.; Liu, T. Unique Molecular Mechanisms Revealed for the Effects of Temperature, CA, Ethylene Exposure, and 1-MCP on Postharvest Senescence of Broccoli. Postharvest Biol. Technol. 2024, 213, 112919. [Google Scholar] [CrossRef]
- Mata, C.I.; Van De Poel, B.; Hertog, M.L.A.T.M.; Tran, D.; Nicolai, B.M. Transcription Analysis of the Ethylene Receptor and CTR Genes in Tomato: The Effects of on and off-Vine Ripening and 1-MCP. Postharvest Biol. Technol. 2018, 140, 67–75. [Google Scholar] [CrossRef]
- Wang, X.; Meng, H.; Tang, Y.; Zhang, Y.; He, Y.; Zhou, J.; Meng, X. Phosphorylation of an Ethylene Response Factor by MPK3/MPK6 Mediates Negative Feedback Regulation of Pathogen-Induced Ethylene Biosynthesis in Arabidopsis. J. Genet. Genom. 2022, 49, 810–822. [Google Scholar] [CrossRef]
Sample_ID | Clean Reads | % > Q30 | GC Content | Mapped Reads | Multiple Mapped Reads | Unique Mapped Reads |
---|---|---|---|---|---|---|
D0_CK_1 | 48256708 | 96.52 | 46.55% | 90.45% | 4.75% | 85.7% |
D0_CK_2 | 47668452 | 96.65 | 46.4% | 90.34% | 4.33% | 86.01% |
D0_CK_3 | 49227078 | 96.67 | 46.67% | 90.48% | 4.23% | 86.25% |
D0_T_1 | 43902798 | 96.71 | 46.22% | 90.2% | 3.81% | 86.39% |
D0_T_2 | 52426856 | 96.75 | 46.21% | 90.27% | 4.49% | 85.78% |
D0_T_3 | 55188122 | 96.63 | 46.17% | 90.19% | 4.51% | 85.68% |
D4_CK_1 | 57183564 | 96.56 | 46.18% | 89.8% | 3.09% | 86.71% |
D4_CK_2 | 50121392 | 96.59 | 46.15% | 89.76% | 2.95% | 86.8% |
D4_CK_3 | 47448964 | 96.62 | 46.09% | 89.84% | 3.29% | 86.55% |
D4_T_1 | 51790312 | 96.53 | 46.39% | 90.15% | 4.36% | 85.79% |
D4_T_2 | 55035510 | 96.61 | 46.29% | 90.0% | 4.49% | 85.51% |
D4_T_3 | 46029862 | 96.42 | 46.26% | 90.07% | 4.16% | 85.92% |
D8_CK_1 | 56371558 | 96.68 | 46.14% | 89.67% | 3.34% | 86.33% |
D8_CK_2 | 46888498 | 96.61 | 45.98% | 89.7% | 3.1% | 86.6% |
D8_CK_3 | 47708112 | 96.54 | 46.24% | 89.66% | 3.26% | 86.39% |
D8_T_1 | 52000634 | 96.65 | 46.38% | 90.13% | 4.17% | 85.96% |
D8_T_2 | 49258952 | 96.63 | 46.19% | 90.11% | 4.08% | 86.03% |
D8_T_3 | 48839766 | 96.7 | 46.19% | 90.24% | 4.06% | 86.17% |
D16_CK_1 | 55581818 | 96.53 | 46.16% | 89.7% | 2.99% | 86.7% |
D16_CK_2 | 47357874 | 96.62 | 46.11% | 89.67% | 3.31% | 86.36% |
D16_CK_3 | 59152866 | 96.7 | 46.08% | 89.79% | 3.46% | 86.33% |
D16_T_1 | 52493840 | 96.54 | 46.06% | 89.88% | 3.17% | 86.71% |
D16_T_2 | 50458528 | 96.5 | 46% | 89.73% | 3.3% | 86.42% |
D16_T_3 | 54911890 | 96.69 | 46.17% | 89.55% | 3.23% | 86.33% |
Gene ID | Gene Description/Annotation | Log2FC (4 d) |
---|---|---|
BolC5t34953H | probable NAC; positive regulation of ethylene biosynthetic process | −2.24 |
BolC1t05767H | probable NAC; positive regulation of ethylene biosynthetic process | −1.64 |
BolC2t06548H | probable ethylene-responsive transcription factor ERF113 | −1.44 |
BolC1t01080H | ethylene-responsive transcription factor 1A | 2.36 |
BolC6t38599H | ethylene-responsive transcription factor ERF073 | 4.29 |
BolC4t28768H | ethylene-responsive transcription factor ERF071 | 6.08 |
BolC3t17122H | ethylene-responsive transcription factor RAP2-3 | 1.14 |
BolC8t48489H | ethylene-responsive transcription factor 1A | 3.00 |
BolC3t14461H | ethylene-responsive transcription factor 1 | 1.29 |
BolC7t43635H | ethylene-responsive transcription factor 2 | 1.60 |
BolC9t55823H | ethylene-responsive transcription factor 2 | 1.23 |
BolC3t18401H | probable ethylene-responsive transcription factor | 1.83 |
BolC9t53913H | probable ethylene-responsive transcription factor | 7.66 |
BolC1t04038H | Ethylene receptor (ETR) | 1.81 |
BolC2t09157H | Mitogen-activated protein kinase kinase 9 (MKK9) | 1.14 |
BolC3t12569H | MPK4; ethylene-dependent systemic resistance | 3.10 |
BolC9t54716H | Receptor burst oxidase homolog (Rboh) | 1.87 |
BolC5t34361H | ethylene-activated signaling pathway | 1.11 |
BolC9t58400H | ethylene-activated signaling pathway | 5.12 |
BolC6t39722H | ethylene-activated signaling pathway | 4.63 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Jin, W.; Jiang, Q.; Zhao, H.; Su, F.; Li, Y.; Yang, S. Transcriptome Analysis of Ethylene-Related Genes in Chlorine Dioxide-Treated Fresh-Cut Cauliflower. Genes 2024, 15, 1102. https://doi.org/10.3390/genes15081102
Jin W, Jiang Q, Zhao H, Su F, Li Y, Yang S. Transcriptome Analysis of Ethylene-Related Genes in Chlorine Dioxide-Treated Fresh-Cut Cauliflower. Genes. 2024; 15(8):1102. https://doi.org/10.3390/genes15081102
Chicago/Turabian StyleJin, Weiwei, Qiaojun Jiang, Haijun Zhao, Fengxian Su, Yan Li, and Shaolan Yang. 2024. "Transcriptome Analysis of Ethylene-Related Genes in Chlorine Dioxide-Treated Fresh-Cut Cauliflower" Genes 15, no. 8: 1102. https://doi.org/10.3390/genes15081102