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Parthenolide reduces the freezing tolerance of hydrated lettuce seeds by inhibiting the proteolysis of seed storage globulins

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Abstract

Moisture content is a key factor affecting success of both field seed survival and seed cryobanks. Studying the freezing tolerance of hydrated seeds can provide information for above issues. Our previous study indicated that the ubiquitin-mediated proteolysis pathway was involved in the freezing tolerance of hydrated lettuce seeds. In this study, parthenolide, a repressor of ring-finger-type ubiquitin E3 ligase, was found to significantly reduce the freezing tolerance of lettuce seeds in slow cooling treatment. Differential scanning calorimeter (DSC) proved that parthenolide led to earlier and more ice crystal formation in the embryo of hydrated seeds in slow cooling, compared with control treatment. Real time PCR analysis showed that parthenolide changed the transcription rhythm of the RING-type E3 ligase COP1 and cold-induced gene ICE1 (Inducer of CBF Expression 1). Results of RNA-seq and real time PCR indicated that parthenolide affected the function of endoplasmic reticulum associated degradation (ERAD) pathway, in which Hsp90 was significantly up-regulated and Hsp20 down-regulated after slow cooling. Two-dimensional electrophoresis of total proteins and SDS-PAGE of soluble proteins found that parthenolide inhibited the proteolysis of seed storage globulins in slow cooling treatment. The inhibition of proteolysis for seed storage globulins and the reduction of small molecular chaperons that can prevented aggregation of misfolded proteins in parthenolide-treated seeds may be responsible for the reduction of freezing tolerance of the hydrated seeds.

Key message

Parthenolide can disrupt the expression pattern of COP1 and cold responsive genes, reduce the level of small molecular chaperons and the proteolysis of seed globulins, which makes hydrated seeds freezing-sensitive.

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Abbreviations

ERAD:

Endoplasmic reticulum associated degradation

Hsp:

Heat shock protein

DSC:

Differential scanning calorimeter

PCR:

Polymerase chain reaction

SDS–PAGE:

SDS–polyacrylamide gel electrophoresis

COP1:

Constitutively photomorphogenic 1

ICE1:

Inducer of CBF expression

2-D analysis:

Two-dimensional electrophoresis

MDM2:

Mouse double minute 2

References

  • Ardley HC, Robinson PA (2005) E3 ubiquitin ligases. Essays Biochem 41:15–30

    Article  CAS  Google Scholar 

  • Bai Y, Booth DT, Romo JT (1998) Winterfat (Eurotia lanata (Pursh) Moq.) seedbed ecology: low temperature exotherms and cold hardiness in hydrated seeds as influenced by imbibition temperature. Ann Bot 81:595–602

    Article  Google Scholar 

  • Breton G, Danyluk J, Charron JB, Sarhan F (2003) Expression profiling and bioinformatic analyses of a novel stress-regulated multispanning transmembrane protein family from cereals and Arabidopsis. Plant Physiol 132:64–74

    Article  CAS  Google Scholar 

  • Brodsky JL (2007) The protective and destructive roles played by molecular chaperones during ERAD (endoplasmic-reticulum-associated degradation). Biochem J 404:353–363

    Article  CAS  Google Scholar 

  • Chinnusamy V, Zhu J, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12:444–451

    Article  CAS  Google Scholar 

  • Dong CH, Agarwal M, Zhang Y, Xie Q, Zhu JK (2006) The negative regulator of plant cold responses, HOS1, is a RING E3 ligase that mediates the ubiquitination and degradation of ICE1. PNAS USA 103:8281–8286

    Article  CAS  Google Scholar 

  • Ellis RH, Hong TD, Roberts EH (1990) An intermediate category of seed storage behavior. J Exp Bot 41:1167–1174

    Article  Google Scholar 

  • Fowler SG, Cook D, Thomashow MF (2005) Low temperature induction of Arabidopsis CBF1, 2, and 3 is gated by the circadian clock. Plant Physiol 137:961–968

    Article  CAS  Google Scholar 

  • Galland M, Huguet R, Arc E, Cueff G, Job D, Rajjou L (2014) Dynamic proteomics emphasizes the importance of selective mRNA translation and protein turnover during Arabidopsis seed germination. Mol Cell Proteomics 13:252–268

    Article  CAS  Google Scholar 

  • Gopal YN, Chanchorn E, Van Dyke MW (2009) Parthenolide promotes the ubiquitination of MDM2 and activates p53 cellular functions. Mol Cancer Ther 8:552–562

    Article  CAS  Google Scholar 

  • Grabherr G, Gottfried M, Paull H (1994) Climate effects on mountain plants. Nature 369:448

    Article  CAS  Google Scholar 

  • Guo X, Shang W, Strappe P, Zhou Z, Blanchard C (2018) Peptides derived from lupin proteins confer potent protection against oxidative stress. J Sci Food Agric 98:5225–5234

    Article  CAS  Google Scholar 

  • Guo XH, Jiang J, Lin SJ, Wang BC, Wang YC, Liu GF, Yang CP (2009) A ThCAP gene from Tamarix hispida confers cold tolerance in transgenic Populus (P. davidiana × P. bolleana). Biotechnol Lett 31:1079–1087

    Article  CAS  Google Scholar 

  • Hastie T, Tibshirani R, Friedman JH (2001) The elements of statistical learning: data mining, inference, and prediction. Springer, New York

    Book  Google Scholar 

  • Jaganathan GK, Han Y, Li W, Song D, Song X, Shen M, Zhou Q, Zhang C, Liu B (2017) Physiological mechanisms only tell half story: multiple biological processes are involved in regulating freezing tolerance of imbibed Lactuca sativa seeds. Sci Rep 7:44166. https://doi.org/10.1038/srep44166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jaganathan GK, Liu B (2014) Effects of dimethyl sulfoxide concentration, pre-cooling and cooling rate on cryopreservation of hydrated lettuce seeds. Seed Sci Technol 42:214–226

    Article  Google Scholar 

  • Kami D, Kasuga J, Arakawa K, Fujikawa S (2008) Improved cryopreservation by diluted vitrification solution with supercooling-facilitating flavonol glycoside. Cryobiology 57:242–245

    Article  CAS  Google Scholar 

  • Keefe P, Moore K (1981) Freeze desiccation: a second mechanism for the survival of hydrated lettuce (Lactuca sativa L.) seed at sub-zero temperatures. Ann Bot 47:635–645

    Article  Google Scholar 

  • Körner C (2003) Alpine plant life: functional plant ecology of high mountain ecosystems. Springer, New York

    Book  Google Scholar 

  • Krishnan HB, Oehrle NW, 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 9:3174–3188

    Article  CAS  Google Scholar 

  • Lee JH, Kim WT (2011) Regulation of abiotic stress signal transduction by E3 ubiquitin ligases in Arabidopsis. Mol Cells 31:201–208

    Article  CAS  Google Scholar 

  • Levitt J (1980) Responses of plants to environmental stresses. Volume II. Water, radiation, salt, and other stresses, 2nd edn. Academic Press, New York

    Google Scholar 

  • Liu Y, Li J (2014) Endoplasmic reticulum-mediated protein quality control in Arabidopsis. Front Plant Sci 5:162. https://doi.org/10.3389/fpls.2014.00162

    Article  PubMed  PubMed Central  Google Scholar 

  • Moran Luengo T, Mayer MP, Rudiger SGD (2019) The Hsp70-Hsp90 chaperone cascade in protein folding. Trends Cell Biol 29:164–177

    Article  CAS  Google Scholar 

  • Mori S, Choi J, Devireddy RV, Bischof JC (2012) Calorimetric measurement of water transport and intracellular ice formation during freezing in cell suspensions. Cryobiology 65:242–255

    Article  CAS  Google Scholar 

  • Nguyen TP, Cueff G, Hegedus DD, Rajjou L, Bentsink L (2015) A role for seed storage proteins in Arabidopsis seed longevity. J Exp Bot 66:6399–6413

    Article  CAS  Google Scholar 

  • Niu L, Zhang H, Wu Z, Wang Y, Liu H, Wu X, Wang W (2018) Modified TCA/acetone precipitation of plant proteins for proteomic analysis. PLoS ONE 13:e0202238. https://doi.org/10.1371/journal.pone.0202238

    Article  PubMed  PubMed Central  Google Scholar 

  • Park S, Shi A, Mou B (2020) Genome-wide identification and expression analysis of the CBF/DREB1 gene family in lettuce. Sci Rep 10:5733. https://doi.org/10.1038/s41598-020-62458-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng D, Zhou B, Jiang Y, Tan X, Yuan D, Zhang L (2018) Enhancing freezing tolerance of Brassica napus L. by overexpression of a stearoyl-acyl carrier protein desaturase gene (SAD) from Sapium sebiferum (L.) Roxb. Plant Sci 272:32–41

    Article  CAS  Google Scholar 

  • Rost B, Liu J, Nair R, Wrzeszczynski KO, Ofran Y (2003) Automatic prediction of protein function. Cell Mol Life Sci 60:2637–2650

    Article  CAS  Google Scholar 

  • Rudakova AS, Cherdivara AM, Wilson KA, Shutov AD (2015) Seed Storage Globulins: Origin and evolution of primary and higher order structures. Biochemistry (Mosc) 80:1354–1361

    Article  CAS  Google Scholar 

  • Shen MQ, Han Y, Zhou Q, Li W, Liu B (2016) Effects of parthenolide and decending speed of temperature on chilling resistance of imbibed seeds of Lactuca sativa. Subtropical Plant Sci 45:308–314

    Google Scholar 

  • Shi Y, Ding Y, Yang S (2018) Molecular regulation of CBF signaling in cold acclimation. Trends Plant Sci 23:623–637

    Article  CAS  Google Scholar 

  • Stromer T, Ehrnsperger M, Gaestel M, Buchner J (2003) Analysis of the interaction of small heat shock proteins with unfolding proteins. J Biol Chem 278:18015–18021

    Article  CAS  Google Scholar 

  • Tuteja N, Ahmad P, Panda BB, Tuteja R (2009) Genotoxic stress in plants: shedding light on DNA damage, repair and DNA repair helicases. Mutat Res 681:134–149

    Article  CAS  Google Scholar 

  • Villalobos AS, Wiese J, Imhoff JF, Dorador C, Keller A, Hentschel U (2019) Systematic affiliation and genome analysis of Subtercola vilae DB165(T) with particular emphasis on cold adaptation of an isolate from a high-altitude cold volcano lake. Microorganisms 7: https://doi.org/10.3390/microorganisms7040107

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Liang E, Lu X, Zhu H, Piao S, Zhu L (2017) Are treelines advancing in response to climate warming on the Tibetan Plateau? Chin J Nat 39:179–183

    Google Scholar 

  • Wen C, Zhang J, Zhang H, Duan Y, Ma H (2019) Effects of divergent ultrasound pretreatment on the structure of watermelon seed protein and the antioxidant activity of its hydrolysates. Food Chem 299:125165. https://doi.org/10.1016/j.foodchem.2019.125165

    Article  CAS  PubMed  Google Scholar 

  • Wyse SV, Dickie JB, Willis KJ (2018) Seed banking not an option for many threatened plants. Nat Plants 4:848–850

    Article  Google Scholar 

  • Zhang Y, Yang C, Li Y, Zheng N, Chen H, Zhao Q, Gao T, Guo H, Xie Q (2007) SDIR1 is a RING finger E3 ligase that positively regulates stress-responsive abscisic acid signaling in Arabidopsis. Plant Cell 19:1912–1929

    Article  CAS  Google Scholar 

  • Zhang Z, Li J, Li F, Liu H, Yang W, Chong K, Xu Y (2017) OsMAPK3 Phosphorylates OsbHLH002/OsICE1 and Inhibits Its Ubiquitination to Activate OsTPP1 and Enhances Rice Chilling Tolerance. Dev Cell 43:731–743

    Article  CAS  Google Scholar 

  • Zhou Y, Jiang Y, Shi R, Chen Z, Li Z, Wei Y, Zhou X (2020) Structural and antioxidant analysis of Tartary buckwheat (Fagopyrum tartaricum Gaertn.) 13S globulin. J Sci Food Agric 100:1220–1229

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by the Research Fund for International Young Scientists of National Natural Science Fundation of China (3171101125). We thank Robbie Lewis, MSc, from Liwen Bianji, Edanz Group China (www.liwenbianji.cn/ac), for editing a draft of this manuscript.

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Authors and Affiliations

  1. Institute of Biothermal Science and Technology, School of Mecical Instrument and Food Engineering, University of Shanghai for Science and Technology, 516 Jungong Road, Shanghai, 200093, China

    Yingying Han, Ying Yu, Jingwen Zhou, Ganesh K. Jaganathan, Mengqi Shen, Qiang Zhou, Danping Song & Baolin Liu

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  1. Yingying Han
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  2. Ying Yu
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  3. Jingwen Zhou
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  4. Ganesh K. Jaganathan
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  5. Mengqi Shen
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  6. Qiang Zhou
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  7. Danping Song
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  8. Baolin Liu
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Contributions

Han YY designed the experiments and wrote the article. Yu Y performed the SDS-PAGE, RNA-seq and Real time PCR of Hsps. Zhou JW performed 2-D analysis. Jaganathan GK revised the article. Shen MQ and Zhou Q performed the real time PCR of E3 ligases. Song DP performed the cooling treatment. Liu BL designed the study and revised the article.

Corresponding authors

Correspondence to Yingying Han or Baolin Liu.

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Communicated by Qiao-Chun Wang.

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Han, Y., Yu, Y., Zhou, J. et al. Parthenolide reduces the freezing tolerance of hydrated lettuce seeds by inhibiting the proteolysis of seed storage globulins. Plant Cell Tiss Organ Cult 144, 247–259 (2021). https://doi.org/10.1007/s11240-020-01836-z

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  • DOI: https://doi.org/10.1007/s11240-020-01836-z

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