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Palmitoylation mediates the proteolysis of seed storage proteins during the cooling process in hydrated lettuce seeds (Lactuca sativa)

Published online by Cambridge University Press:  11 September 2023

Ying Yu
Affiliation:
Institute of Biothermal Science and Technology, School of Health Science and Technology, University of Shanghai for Science and Technology, Shanghai, China
Yingying Han*
Affiliation:
Institute of Biothermal Science and Technology, School of Health Science and Technology, University of Shanghai for Science and Technology, Shanghai, China
Yujiao Ding
Affiliation:
Institute of Biothermal Science and Technology, School of Health Science and Technology, University of Shanghai for Science and Technology, Shanghai, China
Weijie Li
Affiliation:
Institute of Biothermal Science and Technology, School of Health Science and Technology, University of Shanghai for Science and Technology, Shanghai, China
Ganesh K. Jaganathan
Affiliation:
Institute of Biothermal Science and Technology, School of Health Science and Technology, University of Shanghai for Science and Technology, Shanghai, China
Baolin Liu
Affiliation:
Institute of Biothermal Science and Technology, School of Health Science and Technology, University of Shanghai for Science and Technology, Shanghai, China
*
Corresponding author: Yingying Han; Email: yyhan2007@163.com

Abstract

Palmitoyl-protein thioesterase (PPT), involved in the fatty acid synthesis and the de-palmitoylation of protein, was induced under ecological cooling treatment in hydrated lettuce seeds. However, there was no significant difference in fatty acid levels between the control and the cooled samples. To further study the function of PPT, 2-bromopalmitic acid (2-Bp), an inhibitor of protein palmitoylation, was applied during the imbibition of hydrated lettuce seeds, which was followed by slow-cooling treatment (−3°C h−1). The application of 2-Bp (1 mM) significantly increased the survival rate of seeds from 6.70% (control imbibition) to 22.67% (2-Bp imbibition) after slow cooling to −20°C. Differential scanning calorimetry (DSC) analysis indicated that 2-Bp led to earlier onset of ice crystals in the endosperm than the control group. Two-dimensional electrophoresis (2D) confirmed that 2-Bp could promote the hydrolysis of seed globulins and the accumulation of globulin peptides with small molecular weights. High-efficiency hydrolysis of globulin induced by mercaptoethanol improved the freezing tolerance of hydrated lettuce seeds and led to the accumulation of small globulin peptides, which further proved the positive function of small globulin polypeptides in enhancing the freezing tolerance of hydrated lettuce seeds. DSC of small globulin peptides showed that the smaller the molecular weight, the earlier the appearance of ice crystals and the higher the enthalpy of heat release. For the smallest peptides, the 2-Bp-4 in 2-Bp group exhibited higher enthalpy in exothermic peak than the control group (c-4). In conclusion, the hydrolysis of seed globulins and accumulation of small-molecule globulin peptides could be the major reason for improving the freezing tolerance of hydrated seeds after de-palmitoylation treatment.

Type
Research Paper
Copyright
Copyright © The Author(s), 2023. Published by Cambridge University Press

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Footnotes

These authors contributed equally to this work.

References

Batistic, O, Sorek, N, Schultke, S, Yalovsky, S and Kudla, J (2008) Dual fatty acyl modification determines the localization and plasma membrane targeting of CBL/CIPK Ca2+ signaling complexes in Arabidopsis. The Plant Cell 20, 13461362.CrossRefGoogle ScholarPubMed
Batistic, O, Rehers, M, Akerman, A, Schlücking, K, Steinhorst, L, Yalovsky, S and Kudla, J (2012) S-acylation-dependent association of the calcium sensor CBL2 with the vacuolar membrane is essential for proper abscisic acid responses. Cell Research 22, 11551168.CrossRefGoogle ScholarPubMed
Benson, EE (2008) Cryopreservation of phytodiversity: a critical appraisal of theory & practice. Critical Reviews in Plant Sciences 27, 141219.CrossRefGoogle Scholar
Berjak, P and Pammenter, NW (2008) From Avicennia to Zizania: seed recalcitrance in perspective. Annals of Botany 101, 213228.CrossRefGoogle Scholar
Blaskovic, S, Blanc, M and van der Goot, FG (2013) What does S-palmitoylation do to membrane proteins? The FEBS Journal 280, 27662774.CrossRefGoogle ScholarPubMed
Capraro, J, Benedetti, SD, Heinzl, GC, Scarafoni, A and Magni, C (2021) Bioactivities of pseudocereal fractionated seed proteins and derived peptides relevant for maintaining human well-being. International Journal of Molecular Sciences 22, 3543.CrossRefGoogle ScholarPubMed
Chen, S and Schopfer, P (1999) Hydroxyl-radical production in physiological reactions: a novel function of peroxidase. European Journal of Biochemistry 260, 726735.CrossRefGoogle ScholarPubMed
Ellis, RH and Roberts, EH (1980) Improved equations for the prediction of seed longevity. Annals of Botany 45, 1330.CrossRefGoogle Scholar
Ellis, RH, Hong, TD and Roberts, EH (1990) An intermediate category of seed storage behaviour? I. Coffee. Journal of Experimental Botany 41, 11671174.CrossRefGoogle Scholar
Galland, M, Huguet, R, Arc, E, Cueff, G, Job, D and Rajjou, L (2014) Dynamic proteomics emphasizes the importance of selective mRNA translation and protein turnover during Arabidopsis seed germination. Molecular & Cellular Proteomics 13, 252268.CrossRefGoogle ScholarPubMed
Hornemann, T (2015) Palmitoylation and depalmitoylation defects. Journal of Inherited Metabolic Disease 38, 179186.CrossRefGoogle ScholarPubMed
Imin, N, Kerim, T, Rolfe, BG and Weinman, JJ (2004) Effect of early cold stress on the maturation of rice anthers. Proteomics 4, 18731882.CrossRefGoogle ScholarPubMed
Jaganathan, GK and Liu, B (2014) Effects of dimethyl sulfoxide concentration, pre-cooling and cooling rate on cryopreservation of hydrated lettuce seeds. Seed Science and Technology 42, 214226.CrossRefGoogle Scholar
Jaganathan, GK, Han, Y, Wu, G and Liu, B (2016) Freezing tolerance in hydrated lettuce (Lactuca sativa) seeds is dependent on cooling rate but not imbibition temperature. Acta Physiologiae Plantarum 38, 17.CrossRefGoogle Scholar
Jaganathan, GK, Han, Y, Li, W, Song, D, Song, X, Shen, M, Zhou, Q, Zhang, C and Liu, B (2017) Physiological mechanisms only tell half story: multiple biological processes are involved in regulating freezing tolerance of imbibed Lactuca sativa seeds. Scientific Reports 7, 114.CrossRefGoogle ScholarPubMed
Jiang, H, Zhang, X, Chen, X, Aramsangtienchai, P, Tong, Z and Lin, H (2018) Protein lipidation: occurrence, mechanisms, biological functions, and enabling technologies. Chemical Reviews 118, 919988.CrossRefGoogle ScholarPubMed
Juntillla, O and Strushnoff, C (1977) Freezing avoidance by deep supercooling in hydrated lettuce seeds. Nature 269, 325327.CrossRefGoogle Scholar
Keefe, PD and Moore, KG (1981) Freeze desiccation: a second mechanism for the survival of hydrated lettuce {Lactuca sativa L.) seed at sub-zero temperatures. Annals of Botany 47, 635645.CrossRefGoogle Scholar
Keefe, PD and Moore, KG (1983) Freezing tolerance in hydrated Lactuca sativa (L) seed: a model to explain observed variation between seed lots. Annals of Botany 51, 373383.CrossRefGoogle Scholar
Kesari, P, Sharma, A, Katiki, M, Kumar, P, Gurjar, BR, Tomar, S, Sharma, AK and Kumar, P (2017) Structural, functional and evolutionary aspects of seed globulins. Protein and Peptide Letters 24, 267277.CrossRefGoogle ScholarPubMed
Kosmala, A, Bocian, A, Rapacz, M, Jurczyk, B and Zwierzykowski, Z (2009) Identification of leaf proteins differentially accumulated during cold acclimation between Festuca pratensis plants with distinct levels of frost tolerance. Journal of Experimental Botany 60, 35953609.CrossRefGoogle ScholarPubMed
Krishnan, HB, Oehrle, NW and Natarajan, SS (2009) A rapid and simple procedure for the depletion of abundant storage proteins from legume seeds to advance proteome analysis: a case study using Glycine max. Proteomics 9, 31743188.CrossRefGoogle ScholarPubMed
Li, Y, Scott, R, Doughty, J, Grant, M and Qi, B (2016) Protein S-Acyltransferase 14: a specific role for palmitoylation in leaf senescence in Arabidopsis. Plant Physiology 170, 415428.CrossRefGoogle ScholarPubMed
Mohammed, AM, Syeda, K, Hadden, T and Kowluru, A (2013) Upregulation of phagocyte-like NADPH oxidase by cytokines in pancreatic beta-cells: attenuation of oxidative and nitrosative stress by 2-bromopalmitate. Biochemical Pharmacology 85, 109114.CrossRefGoogle ScholarPubMed
Mori, S, Choi, J, Devireddy, RV and Bischof, JC (2012) Calorimetric measurement of water transport and intracellular ice formation during freezing in cell suspensions. Cryobiology 65, 242255.CrossRefGoogle ScholarPubMed
Qi, B, Doughty, J and Hooley, R (2013) A Golgi and tonoplast localized S-acyl transferase is involved in cell expansion, cell division, vascular patterning and fertility in Arabidopsis. New Phytologist 200, 444456.CrossRefGoogle ScholarPubMed
Rio, DC, Ares, M, Hannon, GJ and Nilsen, TW (2010) Purification of RNA using TRIzol (TRI reagent). Cold Spring Harbor Protocols 2010, pdb-prot5439.CrossRefGoogle ScholarPubMed
Roberts, EH (1973) Predicting the storage life of seeds. Seed Science & Technology 1, 499514.Google Scholar
Shutov, AD, Baumlein, H, Blattner, FR and Muntz, K (2003) Storage and mobilization as antagonistic functional constraints on seed storage globulin evolution. Journal of Experimental Botany 54, 16451654. doi:10.1093/jxb/erg165CrossRefGoogle ScholarPubMed
Sripichitt, A, Nawata, E and Shigenaga, S (1988) Effect of storage on changes in TTC staining pattern and germination of soybean seeds. Japanese Journal of Tropical Agriculture 32, 95103.Google Scholar
Svanella Dumas, L, Τsarmpopoulos, Ι, Marais, A, Theil, S, Faure, C, Gaudin, J and Candresse, T (2018) Complete genome sequence of lettuce chordovirus 1 isolated from cultivated lettuce in France. Archives of Virology 163, 25432545.CrossRefGoogle ScholarPubMed
Wesley Smith, J, Berjak, P, Pammenter, NW and Walters, C (2014) Intracellular ice and cell survival in cryo-exposed embryonic axes of recalcitrant seeds of Acer saccharinum: an ultrastructural study of factors affecting cell and ice structures. Annals of Botany 113, 695709.CrossRefGoogle ScholarPubMed
Wilms, H, Fanega Sleziak, N, Van der Auweraer, M, Brands, M, Verleije, M, Hardeman, D, Andre, E and Panis, B (2020) Development of a fast and user-friendly cryopreservation protocol for sweet potato genetic resources. Scientific Reports 10, 14674.CrossRefGoogle ScholarPubMed
Wyse, SV, Dickie, JB and Willis, KJ (2018) Seed banking not an option for many threatened plants. Nature Plants 4, 848850.CrossRefGoogle Scholar
Xue, L, Gollapalli, DR, Maiti, P, Jahng, WJ and Rando, RR (2004) A palmitoylation switch mechanism in the regulation of the visual cycle. Cell 117, 761771.CrossRefGoogle ScholarPubMed
Yan, S, Zhang, Q, Tang, Z, Su, W and Sun, W-N (2006) Comparative proteomic analysis provides new insights into chilling stress responses in rice. Molecular & Cellular Proteomics 5, 484496.CrossRefGoogle ScholarPubMed
Zhang, YL, Li, E, Feng, QN, Zhao, XY, Ge, FR, Zhang, Y and Li, S (2015) Protein palmitoylation is critical for the polar growth of root hairs in Arabidopsis. BMC Plant Biology 15, 50. doi:10.1186/s12870-015-0441-5CrossRefGoogle ScholarPubMed
Zhou, L, Li, S, Feng, Q, Zhang, Y-L, Zhao, X, Zeng, Y-l, Wang, H, Jiang, L and Zhang, Y (2013) Protein S-ACYL Transferase10 is critical for development and salt tolerance in Arabidopsis. The Plant Cell 25, 10931107.CrossRefGoogle ScholarPubMed
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