The Cysteine-Rich Peptide Snakin-2 Negatively Regulates Tubers Sprouting through Modulating Lignin Biosynthesis and H2O2 Accumulation in Potato
Abstract
:1. Introduction
2. Results
2.1. StSN2 Expression Level and Phenotypic Characterization of StSN2 Transgenic Lines
2.2. Effect of StSN2 on Cracking and Cell Morphology of Periderm and Water Loss
2.3. Skin Metabolome in StSN2 Transgenic Potato
2.4. Proteomics Analysis of Lignin Biosynthesis
2.5. StSN2 Interacts with Three Class III Peroxidases
2.6. StSN2 Altered H2O2 Content and the Activities of Superoxide Dismutase (SOD) and Catalase (CAT)
3. Discussion
4. Materials and Methods
4.1. Plant Material and Growth Conditions
4.2. Generation of StSN2 Transgenic Potato Lines
4.3. Western Blot and Quantitative Real-Time PCR
4.4. Assessment of Sprout Growth, Periderm Morphology and Tuber Weight
4.5. Targeted Metabolomic Analysis on Metabolites in Potato Skin
4.6. Identification and Quantification of Proteins
4.7. CoIP-MS Assays
4.8. Yeast Two-Hybrid Assay
4.9. Measurement of Lignin Content and Enzyme Activities
4.10. Statistical Analysis
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Alamar, M.C.; Tosetti, R.; Landahl, S.; Bermejo, A.; Terry, L.A. Assuring potato tuber quality during storage: A future perspective. Front. Plant Sci. 2017, 8, 2034. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Morris, W.L.; Alamar, M.C.; Lopez-Cobollo, R.M.; Cañete, J.C.; Bennett, M.; Van Der Kaay, J.; Stevens, J.; Sharma, S.K.; McLean, K.; Thompson, A.J.; et al. A member of the terminal FLOWER 1/CENTRORADIALIS gene family controls sprout growth in potato tubers. J. Exp. Bot. 2018, 70, 835–843. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sonnewald, S.; Sonnewald, U. Regulation of potato tuber sprouting. Planta 2013, 239, 27–38. [Google Scholar] [CrossRef] [Green Version]
- Liu, B.; Zhao, S.; Tan, F.; Zhao, H.; Wang, D.; Si, H.; Chen, Q. Changes in ROS production and antioxidant capacity during tuber sprouting in potato. Food Chem. 2017, 237, 205–213. [Google Scholar] [CrossRef] [PubMed]
- Shukla, S.; Pandey, S.S.; Chandra, M.; Pandey, A.; Bharti, N.; Barnawal, D.; Chanotiya, C.S.; Tandon, S.; Darokar, M.P.; Kalra, A.; et al. Application of essential oils as a natural and alternate method for inhibiting and inducing the sprouting of potato tubers. Food Chem. 2019, 284, 171–179. [Google Scholar] [CrossRef]
- Li, L.-Q.; Zou, X.; Deng, M.-S.; Peng, J.; Huang, X.-L.; Lu, X.; Fang, C.-C.; Wang, X.-Y. Comparative morphology, transcription, and proteomics study revealing the key molecular mechanism of camphor on the potato tuber sprouting effect. Int. J. Mol. Sci. 2017, 18, 2280. [Google Scholar] [CrossRef] [Green Version]
- Hou, J.; Liu, T.; Reid, S.; Zhang, H.; Peng, X.; Sun, K.; Du, J.; Sonnewald, U.; Song, B. Silencing of α-amylase StAmy23 in potato tuber leads to delayed sprouting. Plant Physiol. Biochem. 2019, 139, 411–418. [Google Scholar] [CrossRef] [PubMed]
- Li, L.; Deng, M.; Lyu, C.; Zhang, J.; Peng, J.; Cai, C.; Yang, S.; Lu, L.; Ni, S.; Liu, F.; et al. Quantitative phosphoproteomics analysis reveals that protein modification and sugar metabolism contribute to sprouting in potato after BR treatment. Food Chem. 2020, 325, 126875. [Google Scholar] [CrossRef]
- Paul, V.; Ezekiel, R.; Pandey, R. Sprout suppression on potato: Need to look beyond CIPC for more effective and safer alternatives. J. Food Sci. Technol. 2015, 53, 1–18. [Google Scholar] [CrossRef] [Green Version]
- Jin, L.; Cai, Q.; Huang, W.; Dastmalchi, K.; Rigau, J.; Molinas, M.; Figueras, M.; Serra, O.; Stark, R.E. Potato native and wound periderms are differently affected by down-regulation of FHT, a suberin feruloyl transferase. Phytochemistry 2018, 147, 30–48. [Google Scholar] [CrossRef]
- Serra, O.; Hohn, C.; Franke, R.; Prat, S.; Molinas, M.; Figueras, M. A feruloyl transferase involved in the biosynthesis of suberin and suberin-associated wax is required for maturation and sealing properties of potato periderm. Plant J. 2010, 62, 277–290. [Google Scholar] [CrossRef]
- Lashbrooke, J.; Cohen, H.; Levy-Samocha, D.; Tzfadia, O.; Panizel, I.; Zeisler, V.; Massalha, H.; Stern, A.; Trainotti, L.; Schreiber, L.; et al. MYB107 and MYB9 homologs regulate suberin deposition in angiosperms. Plant Cell 2016, 28, 2097–2116. [Google Scholar] [CrossRef] [Green Version]
- Panikashvili, D.; Shi, J.X.; Schreiber, L.; Aharoni, A. The arabidopsis DCR encoding a soluble BAHD acyltransferase is required for cutin polyester formation and seed hydration properties. Plant Physiol. 2009, 151, 1773–1789. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liao, N.; Hu, Z.; Li, Y.; Hao, J.; Chen, S.; Xue, Q.; Ma, Y.; Zhang, K.; Mahmoud, A.; Ali, A.; et al. Ethylene-responsive factor 4 is associated with the desirable rind hardness trait conferring cracking resistance in fresh fruits of watermelon. Plant Biotechnol. J. 2020, 18, 1066–1077. [Google Scholar] [CrossRef] [Green Version]
- Vulavala, V.K.R.; Fogelman, E.; Faigenboim, A.; Shoseyov, O.; Ginzberg, I. The transcriptome of potato tuber phellogen reveals cellular functions of cork cambium and genes involved in periderm formation and maturation. Sci. Rep. 2019, 9, 10216. [Google Scholar] [CrossRef] [Green Version]
- Liang, M.; Davis, E.; Gardner, D.; Cai, X.; Wu, Y. Involvement of AtLAC15 in lignin synthesis in seeds and in root elongation of Arabidopsis. Planta 2006, 224, 1185–1196. [Google Scholar] [CrossRef] [PubMed]
- Renard, J.; Martínez-Almonacid, I.; Sonntag, A.; Molina, I.; Moya-Cuevas, J.; Bissoli, G.; Muñoz-Bertomeu, J.; Faus, I.; Niñoles, R.; Shigeto, J.; et al. PRX2 and PRX25, peroxidases regulated by COG1, are involved in seed longevity in Arabidopsis. Plant Cell Environ. 2019, 43, 315–326. [Google Scholar] [CrossRef] [PubMed]
- Zhang, S.; Yang, C.; Peng, J.; Sun, S.; Wang, X. GASA5, a regulator of flowering time and stem growth in Arabidopsis thaliana. Plant Mol. Biol. 2009, 69, 745–759. [Google Scholar] [CrossRef]
- Rubinovich, L.; Weiss, D. The arabidopsis cysteine-rich protein GASA4 promotes GA responses and exhibits redox activity in bacteria and in planta. Plant J. 2010, 64, 1018–1027. [Google Scholar] [CrossRef]
- Nahirñak, V.; Almasia, N.I.; Fernandez, P.V.; Hopp, H.E.; Estevez, J.M.; Carrari, F.; Vazquez-Rovere, C. Potato snakin-1 gene silencing affects cell division, primary metabolism, and cell wall composition. Plant Physiol. 2011, 158, 252–263. [Google Scholar] [CrossRef] [Green Version]
- Sun, S.; Wang, H.; Yu, H.; Zhong, C.; Zhang, X.; Peng, J.; Wang, X. GASA14 regulates leaf expansion and abiotic stress resistance by modulating reactive oxygen species accumulation. J. Exp. Bot. 2013, 64, 1637–1647. [Google Scholar] [CrossRef] [Green Version]
- Zhong, C.; Xu, H.; Ye, S.; Wang, S.; Li, L.; Zhang, S.; Wang, X. Gibberellic acid-stimulated arabidopsis6 serves as an integrator of gibberellin, abscisic acid, and glucose signaling during seed germination in arabidopsis. Plant Physiol. 2015, 169, 2288–2303. [Google Scholar] [CrossRef] [Green Version]
- Qu, J.; Kang, S.G.; Hah, C.; Jang, J.-C. Molecular and cellular characterization of GA-stimulated transcripts GASA4 and GASA6 in Arabidopsis thaliana. Plant Sci. 2016, 246, 1–10. [Google Scholar] [CrossRef]
- Nahirñak, V.; Rivarola, M.; Almasia, N.I.; Barón, M.P.B.; Hopp, H.E.; Vile, D.; Paniego, N.; Rovere, C.V. Snakin-1 affects reactive oxygen species and ascorbic acid levels and hormone balance in potato. PLoS ONE 2019, 14, e0214165. [Google Scholar] [CrossRef] [PubMed]
- Tianli, W.; Chunzhen, C.; Yun, Z.; Yuanda, L.; Yanyan, M.; Guangyan, Z. Molecular characterization of the gibberellin-stimulated transcript of GASA4 in Citrus. Plant Growth Regul. 2020, 91, 89–99. [Google Scholar]
- Rubinovich, L.; Ruthstein, S.; Weiss, D. The arabidopsis cysteine-rich GASA5 is a redox-active metalloprotein that suppresses gibberellin responses. Mol. Plant 2014, 7, 244–247. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, W.; Jiang, Y.; Wang, C.; Zhao, L.; Jin, Y.; Xing, Q.; Li, M.; Lv, T.; Qi, H. Lignin synthesized by CmCAD2 and CmCAD3 in oriental melon (Cucumis melo L.) seedlings contributes to drought tolerance. Plant Mol. Biol. 2020, 103, 689–704. [Google Scholar] [CrossRef] [PubMed]
- Ho-Yue-Kuang, S.; Alvarado, C.; Antelme, S.; Bouchet, B.; Cézard, L.; Le Bris, P.; Légée, F.; Maia-Grondard, A.; Yoshinaga, A.; Saulnier, L.; et al. Mutation in Brachypodium caffeic acid O-methyltransferase 6 alters stem and grain lignins and improves straw saccharification without deteriorating grain quality. J. Exp. Bot. 2015, 67, 227–237. [Google Scholar] [CrossRef] [Green Version]
- Fernández-Pérez, F.; Vivar, T.; Pomar, F.; Pedreño, M.A.; Novo-Uzal, E. Peroxidase 4 is involved in syringyl lignin formation in Arabidopsis thaliana. J. Plant Physiol. 2015, 175, 86–94. [Google Scholar] [CrossRef]
- Tamasloukht, B.; Wong, Q.L.M.; Martinez, Y.; Tozo, K.; Barbier, O.; Jourda, C.; Jauneau, A.; Borderies, G.; Balzergue, S.; Renou, J.P.; et al. Characterization of a cinnamoyl-CoA reductase 1 (CCR1) mutant in maize: Effects on lignification, fibre development, and global gene expression. J. Exp. Bot. 2011, 62, 3837–3848. [Google Scholar] [CrossRef]
- Su, X.; Zhao, Y.; Wang, H.; Li, G.; Cheng, X.; Jin, Q.; Cai, Y. Transcriptomic analysis of early fruit development in Chinese white pear (Pyrus bretschneideri Rehd.) and functional identification of PbCCR1 in lignin biosynthesis. BMC Plant Biol. 2019, 19, 417. [Google Scholar] [CrossRef] [Green Version]
- Li, J.; Wu, L.; Foster, R.; Ruan, Y.-L. Molecular regulation of sucrose catabolism and sugar transport for development, defence and phloem function. J. Integr. Plant Biol. 2017, 59, 322–335. [Google Scholar] [CrossRef] [Green Version]
- Su, G.; An, Z.; Zhang, W.; Liu, Y. Light promotes the synthesis of lignin through the production of H2O2 mediated by diamine oxidases in soybean hypocotyls. J. Plant Physiol. 2005, 162, 1297–1303. [Google Scholar] [CrossRef] [PubMed]
- Bajji, M.; M’Hamdi, M.; Gastiny, F.; Rojas-Beltran, J.A.; du Jardin, P. Catalase inhibition accelerates dormancy release and sprouting in potato (Solanum tuberosum L.) tubers. Biotechnol. Agron. Soc. 2007, 2, 121–131. [Google Scholar]
- Wojtyla, Ł.; Lechowska, K.; Kubala, S.; Garnczarska, M. Different modes of hydrogen peroxide action during seed germination. Front. Plant Sci. 2016, 7, 66. [Google Scholar] [CrossRef] [Green Version]
- Wigoda, N.; Ben-Nissan, G.; Granot, D.; Schwartz, A.; Weiss, D. The gibberellin-induced, cysteine-rich protein GIP2 from Petunia hybrida exhibits in planta antioxidant activity. Plant J. 2006, 48, 796–805. [Google Scholar] [CrossRef] [PubMed]
- Ben-Nissan, G.; Lee, J.-Y.; Borohov, A.; Weiss, D. GIP, a Petunia hybrida GA-induced cysteine-rich protein: A possible role in shoot elongation and transition to flowering. Plant J. 2003, 37, 229–238. [Google Scholar] [CrossRef] [PubMed]
- Li, X.; Shi, S.; Tao, Q.; Tao, Y.; Miao, J.; Peng, X.; Li, C.; Yang, Z.; Zhou, Y.; Liang, G. OsGASR9 positively regulates grain size and yield in rice (Oryza sativa). Plant Sci. 2019, 286, 17–27. [Google Scholar] [CrossRef]
- Liu, Z.H.; Zhu, L.; Shi, H.Y.; Chen, Y.; Zhang, J.M.; Zheng, Y.; Li, X.B. Cotton GASL genes encoding putative gibberellin-regulated proteins are involved in response to GA signaling in fiber development. Mol. Biol. Rep. 2013, 40, 4561–4570. [Google Scholar] [CrossRef]
- Oliveira-Lima, M.; Benko-Iseppon, A.M.; Neto, J.R.C.F.; Rodriguez-Decuadro, S.; Kido, E.A.; Crovella, S.; Pandolfi, V. Snakin: Structure, roles and applications of a plant antimicrobial peptide. Curr. Protein Pept. Sci. 2017, 18, 368–374. [Google Scholar] [CrossRef] [PubMed]
- Berrocal-Lobo, M.; Segura, A.; Moreno, M.; López, G.; García-Olmedo, F.; Molina, A. Snakin-2, an antimicrobial peptide from potato whose gene is locally induced by wounding and responds to pathogen infection. Plant Physiol. 2002, 128, 951–961. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, L.; Wang, Z.; Xu, Y.; Joo, S.-H.; Kim, S.-K.; Xue, Z.; Xu, Z.; Wang, Z.; Chong, K. OsGSR1is involved in crosstalk between gibberellins and brassinosteroids in rice. Plant J. 2009, 57, 498–510. [Google Scholar] [CrossRef]
- Verdaguer, R.; Soler, M.; Serra, O.; Garrote, A.; Fernandez, S.; Company-Arumi, D.; Antico, E.; Molinas, M.; Figueras, M. Silencing of the potato StNAC103 gene enhances the accumulation of suberin polyester and associated wax in tuber skin. J. Exp. Bot. 2016, 67, 5415–5427. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- De La Fuente, J.I.; Amaya, I.; Castillejo, C.; Sánchez-Sevilla, J.F.; Quesada, M.A.; Botella, M.Á.; Valpuesta, V. The strawberry gene FaGAST affects plant growth through inhibition of cell elongation. J. Exp. Bot. 2006, 57, 2401–2411. [Google Scholar] [CrossRef] [PubMed]
- Trapalis, M.; Li, S.F.; Parish, R.W. The Arabidopsis GASA10 gene encodes a cell wall protein strongly expressed in developing anthers and seeds. Plant Sci. 2017, 260, 71–79. [Google Scholar] [CrossRef] [PubMed]
- Li, Q.; Qin, X.; Qi, J.; Dou, W.; Dunand, C.; Chen, S.; He, Y. CsPrx25, a class III peroxidase in Citrus sinensis, confers resistance to citrus bacterial canker through the maintenance of ROS homeostasis and cell wall lignification. Hortic. Res. 2020, 7, 192. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.; Li, J.; Zou, X.; Lu, L.; Li, L.; Ni, S.; Liu, F. Ectopic expression of AtCIPK23 enhances tolerance against Low-K+ stress in transgenic potato. Am. J. Potato Res. 2010, 88, 153–159. [Google Scholar] [CrossRef] [Green Version]
- Hu, Y.; Yu, D. BRASSINOSTEROID INSENSITIVE2 interacts with ABSCISIC ACID INSENSITIVE5 to mediate the antagonism of brassinosteroids to abscisic acid during seed germination in Arabidopsis. Plant Cell 2014, 26, 4394–4408. [Google Scholar] [CrossRef] [Green Version]
- Chen, R.; Xiao, M.; Gao, H.; Chen, Y.; Li, Y.; Liu, Y.; Zhang, N. Identification of a novel mitochondrial interacting protein of C1QBP using subcellular fractionation coupled with CoIP-MS. Anal. Bioanal. Chem. 2016, 408, 1557–1564. [Google Scholar] [CrossRef]
- Guo, X.; Qin, Q.; Yan, J.; Niu, Y.; Huang, B.; Guan, L.; Li, S.-S.; Ren, D.; Liu, Y.; Hou, S. TYPE-ONE PROTEIN PHOSPHATASE4 regulates pavement cell interdigitation by modulating PIN-FORMED1 polarity and trafficking in Arabidopsis. Plant Physiol. 2015, 167, 1058–1075. [Google Scholar] [CrossRef] [Green Version]
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Deng, M.; Peng, J.; Zhang, J.; Ran, S.; Cai, C.; Yu, L.; Ni, S.; Huang, X.; Li, L.; Wang, X. The Cysteine-Rich Peptide Snakin-2 Negatively Regulates Tubers Sprouting through Modulating Lignin Biosynthesis and H2O2 Accumulation in Potato. Int. J. Mol. Sci. 2021, 22, 2287. https://doi.org/10.3390/ijms22052287
Deng M, Peng J, Zhang J, Ran S, Cai C, Yu L, Ni S, Huang X, Li L, Wang X. The Cysteine-Rich Peptide Snakin-2 Negatively Regulates Tubers Sprouting through Modulating Lignin Biosynthesis and H2O2 Accumulation in Potato. International Journal of Molecular Sciences. 2021; 22(5):2287. https://doi.org/10.3390/ijms22052287
Chicago/Turabian StyleDeng, Mengsheng, Jie Peng, Jie Zhang, Shuang Ran, Chengcheng Cai, Liping Yu, Su Ni, Xueli Huang, Liqin Li, and Xiyao Wang. 2021. "The Cysteine-Rich Peptide Snakin-2 Negatively Regulates Tubers Sprouting through Modulating Lignin Biosynthesis and H2O2 Accumulation in Potato" International Journal of Molecular Sciences 22, no. 5: 2287. https://doi.org/10.3390/ijms22052287