Enhancement of Apple Stress Resistance via Proline Elevation by Sugar Substitutes
Abstract
:1. Introduction
2. Results
2.1. Low Concentration of Sugar Substitutes Promote Proline Accumulation
2.2. Low Concentration of Sugar Substitutes Improves Salt Resistance
2.3. Low Concentration of Sugar Substitutes Enhances Cold Tolerance in Plants
2.4. Low Concentration of Sugar Substitutes Enhances Drought Tolerance in Plants
2.5. Low Concentration of Sugar Substitutes Enhances Plant Disease Resistance
2.6. The Effect of Sugar Substitutes on the Quality of Apple Fruits
3. Discussions
4. Materials and Methods
4.1. Plant Materials and Growth Conditions
4.2. Fresh Weight
4.3. Proline Content
4.4. Malondialdehyde Content
4.5. Hydrogen Peroxide Content
4.6. Superoxide Anion Radical Content
4.7. Extraction of Plant Genomic RNA
4.8. Photosynthetic Rate and Chlorophyll Fluorescence
4.9. Relative Leaf Water Content
4.10. Sugar Content
4.11. Data Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Qin, H.; Li, Y.; Huang, R. Advances and Challenges in the Breeding of Salt-Tolerant Rice. Int. J. Mol. Sci. 2020, 21, 8385. [Google Scholar] [CrossRef] [PubMed]
- Wang, N.; Qian, Z.; Luo, M.; Fan, S.; Zhang, X.; Zhang, L. Identification of Salt Stress Responding Genes Using Transcriptome Analysis in Green Alga Chlamydomonas Reinhardtii. Int. J. Mol. Sci. 2018, 19, 3359. [Google Scholar] [CrossRef] [PubMed]
- Miao, R.; Yuan, W.; Wang, Y.; Garcia-Maquilon, I.; Dang, X.; Li, Y.; Zhang, J.; Zhu, Y.; Rodriguez, P.L.; Xu, W. Low ABA Concentration Promotes Root Growth and Hydrotropism through Relief of ABA INSENSITIVE 1-Mediated Inhibition of Plasma Membrane H+-ATPase 2. Sci. Adv. 2021, 7, eabd4113. [Google Scholar] [CrossRef] [PubMed]
- Shao, H.-B.; Chu, L.-Y.; Jaleel, C.A.; Manivannan, P.; Panneerselvam, R.; Shao, M.-A. Understanding Water Deficit Stress-Induced Changes in the Basic Metabolism of Higher Plants–Biotechnologically and Sustainably Improving Agriculture and the Ecoenvironment in Arid Regions of the Globe. Crit. Rev. Biotechnol. 2009, 29, 131–151. [Google Scholar] [CrossRef] [PubMed]
- Zhang, F.; Xin, M.; Yu, S.; Liu, D.; Zhou, X.; Qin, Z. Expression and Functional Analysis of the Propamocarb-Related Gene CsMCF in Cucumber. Front. Plant Sci. 2019, 10, 871. [Google Scholar] [CrossRef]
- Huan, X.; Wang, X.; Zou, S.; Zhao, K.; Han, Y.; Wang, S. Transcription Factor ERF194 Modulates the Stress-Related Physiology to Enhance Drought Tolerance of Poplar. Int. J. Mol. Sci. 2023, 24, 788. [Google Scholar] [CrossRef]
- Wang, D.-R.; Zhang, X.-W.; Xu, R.-R.; Wang, G.-L.; You, C.-X.; An, J.-P. Apple U-Box-Type E3 Ubiquitin Ligase MdPUB23 Reduces Cold-Stress Tolerance by Degrading the Cold-Stress Regulatory Protein MdICE1. Hortic. Res. 2022, 9, uhac171. [Google Scholar] [CrossRef]
- Wang, L.; Qian, B.; Zhao, L.; Liang, M.-H.; Zhan, X.; Zhu, J. Two Triacylglycerol Lipases Are Negative Regulators of Chilling Stress Tolerance in Arabidopsis. Int. J. Mol. Sci. 2022, 23, 3380. [Google Scholar] [CrossRef]
- Beirinckx, S.; Viaene, T.; Haegeman, A.; Debode, J.; Amery, F.; Vandenabeele, S.; Nelissen, H.; Inzé, D.; Tito, R.; Raes, J.; et al. Tapping into the Maize Root Microbiome to Identify Bacteria That Promote Growth under Chilling Conditions. Microbiome 2020, 8, 54. [Google Scholar] [CrossRef]
- Nevyl, S.F.; Battaglia, M.E. Developmental Plasticity in Arabidopsis Thaliana under Combined Cold and Water Deficit Stresses during Flowering Stage. Planta 2021, 253, 50. [Google Scholar] [CrossRef]
- Zhang, Y.; Dai, T.; Liu, Y.; Wang, J.; Wang, Q.; Zhu, W. Effect of Exogenous Glycine Betaine on the Germination of Tomato Seeds under Cold Stress. Int. J. Mol. Sci. 2022, 23, 10474. [Google Scholar] [CrossRef] [PubMed]
- Orzechowski, S.; Sitnicka, D.; Grabowska, A.; Compart, J.; Fettke, J.; Zdunek-Zastocka, E. Effect of Short-Term Cold Treatment on Carbohydrate Metabolism in Potato Leaves. Int. J. Mol. Sci. 2021, 22, 7203. [Google Scholar] [CrossRef]
- Liu, A.; Hu, Z.; Bi, A.; Fan, J.; Gitau, M.M.; Amombo, E.; Chen, L.; Fu, J. Photosynthesis, Antioxidant System and Gene Expression of Bermudagrass in Response to Low Temperature and Salt Stress. Ecotoxicology 2016, 25, 1445–1457. [Google Scholar] [CrossRef]
- Li, H.; Li, Y.; Ke, Q.; Kwak, S.-S.; Zhang, S.; Deng, X. Physiological and Differential Proteomic Analyses of Imitation Drought Stress Response in Sorghum Bicolor Root at the Seedling Stage. Int. J. Mol. Sci. 2020, 21, 9174. [Google Scholar] [CrossRef] [PubMed]
- Li, S.; Jiang, H.; Wang, J.; Wang, Y.; Pan, S.; Tian, H.; Duan, M.; Wang, S.; Tang, X.; Mo, Z. Responses of Plant Growth, Physiological, Gas Exchange Parameters of Super and Non-Super Rice to Rhizosphere Temperature at the Tillering Stage. Sci. Rep. 2019, 9, 10618. [Google Scholar] [CrossRef] [PubMed]
- Ma, H.; Li, P.; Liu, X.; Li, C.; Zhang, S.; Wang, X.; Tao, X. Poly-γ-Glutamic Acid Enhanced the Drought Resistance of Maize by Improving Photosynthesis and Affecting the Rhizosphere Microbial Community. BMC Plant Biol. 2022, 22, 11. [Google Scholar] [CrossRef]
- Farhangi-Abriz, S.; Torabian, S. Antioxidant Enzyme and Osmotic Adjustment Changes in Bean Seedlings as Affected by Biochar under Salt Stress. Ecotoxicol. Environ. Saf. 2017, 137, 64–70. [Google Scholar] [CrossRef]
- Per, T.S.; Khan, N.A.; Reddy, P.S.; Masood, A.; Hasanuzzaman, M.; Khan, M.I.R.; Anjum, N.A. Approaches in modulating proline metabolism in plants for salt and drought stress tolerance: Phytohormones, mineral nutrients and transgenics. Plant Physiol. Biochem. 2017, 115, 126–140. [Google Scholar] [CrossRef]
- Czarnecka, K.; Pilarz, A.; Rogut, A.; Maj, P.; Szymańska, J.; Olejnik, Ł.; Szymański, P. Aspartame—True or False? Narrative Review of Safety Analysis of General Use in Products. Nutrients 2021, 13, 1957. [Google Scholar] [CrossRef]
- Chattopadhyay, S.; Raychaudhuri, U.; Chakraborty, R. Artificial Sweeteners—A Review. J. Food Sci. Technol. 2011, 51, 611–621. [Google Scholar] [CrossRef]
- Zhu, Z.; Wu, M.; Cai, J.; Li, S.; Marszałek, K.; Lorenzo, J.M.; Barba, F.J. Optimization of Spray-Drying Process of Jerusalem Artichoke Extract for Inulin Production. Molecules 2019, 24, 1674. [Google Scholar] [CrossRef] [PubMed]
- van Zelm, E.; Zhang, Y.; Testerink, C. Salt Tolerance Mechanisms of Plants. Annu. Rev. Plant Biol. 2020, 71, 403–433. [Google Scholar] [CrossRef] [PubMed]
- Wang, L.; Zhou, Y.; Ding, Y.; Chen, C.; Chen, X.; Su, N.; Zhang, X.; Pan, Y.; Li, J. Novel Flavin-Containing Monooxygenase Protein FMO1 Interacts with CAT2 to Negatively Regulate Drought Tolerance through ROS Homeostasis and ABA Signaling Pathway in Tomato. Hortic. Res. 2023, 10, uhad037. [Google Scholar] [CrossRef] [PubMed]
- Sarkate, A.; Saini, S.; Teotia, D.; Gaid, M.; Mir, J.; Roy, P.; Agrawal, P.; Sircar, D. Comparative metabolomics of scab-resistant and susceptible apple cell cultures in response to scab fungus elicitor treatment. Sci. Rep. 2018, 8, 17844. [Google Scholar] [CrossRef]
- Ba, F.; Ji, X.; Huang, S.; Zhang, Y.; Liu, W.; Liu, Y.; Ling, S.; Li, J. Engineering Escherichia coli to Utilize Erythritol as Sole Carbon Source. Adv. Sci. 2023, 10, 2207008. [Google Scholar] [CrossRef]
- Kushi, L.; Doyle, C.; McCullough, M.; Rock, C.; Demark-Wahnefried, W.; Bandera, E.; Gapstur, S.; Patel, A.; Andrews, K.; Gansler, T.; et al. American Cancer Society Guidelines on Nutrition and Physical Activity for Cancer Prevention Reducing the Risk of Cancer with Healthy Food Choices and Physical Activity. CA Cancer J. Clin. 2012, 62, 30–67. [Google Scholar] [CrossRef]
- Malbert, C.; Horowitz, M.; Young, R. Low-calorie sweeteners augment tissue-specific insulin sensitivity in a large animal model of obesity. Eur. J. Nucl. Med. Mol. Imaging 2019, 46, 2380–2391. [Google Scholar] [CrossRef]
- Muley, A.; Shingote, P.; Patil, A.; Dalvi, S.; Suprasanna, P. Gamma radiation degradation of chitosan for application in growth promotion and induction of stress tolerance in potato (Solanum tuberosum L.). Carbohydr. Polym. 2019, 210, 289–301. [Google Scholar] [CrossRef]
- Gu, J.; Xia, Z.; Luo, Y.; Jiang, X.; Qian, B.; Xie, H.; Zhu, J.-K.; Xiong, L.; Zhu, J.; Wang, Z.-Y. Spliceosomal Protein U1A Is Involved in Alternative Splicing and Salt Stress Tolerance in Arabidopsis Thaliana. Nucleic Acids Res. 2017, 46, 1777–1792. [Google Scholar] [CrossRef]
- Cheng, G.; Wang, M.; Zhang, L.; Wei, H.; Wang, H.; Lu, J.; Yu, S. Overexpression of a Cotton Aquaporin Gene GhTIP1;1-like Confers Cold Tolerance in Transgenic Arabidopsis. Int. J. Mol. Sci. 2022, 23, 1361. [Google Scholar] [CrossRef]
- Thompson, R.A.; Adams, H.D.; Breshears, D.D.; Collins, A.D.; Dickman, L.T.; Grossiord, C.; Manrique-Alba, À.; Peltier, D.M.; Ryan, M.G.; Trowbridge, A.M.; et al. No Carbon Storage in Growth-Limited Trees in a Semi-Arid Woodland. Nat. Commun. 2023, 14, 1959. [Google Scholar] [CrossRef] [PubMed]
- Volaire, F. A Unified Framework of Plant Adaptive Strategies to Drought: Crossing Scales and Disciplines. Glob. Chang. Biol. 2018, 24, 2929–2938. [Google Scholar] [CrossRef]
- Feng, Z.-Q.; Li, T.; Wang, X.; Sun, W.-J.; Zhang, T.-T.; You, C.-X.; Wang, X.-F. Identification and Characterization of Apple MdNLP7 Transcription Factor in the Nitrate Response. Plant Sci. 2022, 316, 111158. [Google Scholar] [CrossRef] [PubMed]
- Li, T.; Feng, Z.; Yang, Y.; Li, M.; Li, G.; You, C.; Gao, W.; Wang, X. Functional identification of the bHLH transcription factor MdSAT1 in the phosphate deficiency response. Fruit Res. 2023, 3, 26. [Google Scholar] [CrossRef]
- Bates, L.S.; Waldren, R.P.; Teare, I.D. Rapid Determination of Free Proline for Water-Stress Studies. Plant Soil 1973, 39, 205–207. [Google Scholar] [CrossRef]
- Heath, R.L.; Packer, L. Photoperoxidation in Isolated Chloroplasts. Arch. Biochem. Biophys. 1968, 125, 189–198. [Google Scholar] [CrossRef] [PubMed]
- Feng, Z.; Wang, X.; Li, T.; Wang, X.; Li, H.; You, C. Genome-wide identification and comparative analysis of genes encoding AAPs in apple (Malus × domestica Borkh). Gene 2022, 83, 146558. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Zhang, Z.; Liang, Y.; Han, Y.; Han, Y.; Tan, J. High Potassium Application Rate Increased Grain Yield of Shading-Stressed Winter Wheat by Improving Photosynthesis and Photosynthate Translocation. Front. Plant Sci. 2020, 11, 134. [Google Scholar] [CrossRef]
- Puscion-Jakubik, A.; Borawska, M.; Socha, K. Modern Methods for Assessing the Quality of Bee Honey and Botanical Origin Identification. Foods 2020, 9, 1028. [Google Scholar] [CrossRef]
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Feng, Z.-Q.; Li, T.; Li, X.-Y.; Luo, L.-X.; Li, Z.; Liu, C.-L.; Ge, S.-F.; Zhu, Z.-L.; Li, Y.-Y.; Jiang, H.; et al. Enhancement of Apple Stress Resistance via Proline Elevation by Sugar Substitutes. Int. J. Mol. Sci. 2024, 25, 9548. https://doi.org/10.3390/ijms25179548
Feng Z-Q, Li T, Li X-Y, Luo L-X, Li Z, Liu C-L, Ge S-F, Zhu Z-L, Li Y-Y, Jiang H, et al. Enhancement of Apple Stress Resistance via Proline Elevation by Sugar Substitutes. International Journal of Molecular Sciences. 2024; 25(17):9548. https://doi.org/10.3390/ijms25179548
Chicago/Turabian StyleFeng, Zi-Quan, Tong Li, Xin-Yi Li, Long-Xin Luo, Zhi Li, Chun-Ling Liu, Shun-Feng Ge, Zhan-Ling Zhu, Yuan-Yuan Li, Han Jiang, and et al. 2024. "Enhancement of Apple Stress Resistance via Proline Elevation by Sugar Substitutes" International Journal of Molecular Sciences 25, no. 17: 9548. https://doi.org/10.3390/ijms25179548