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ROS Produced via BsRBOHD Plays an Important Role in Low Temperature-Induced Anthocyanin Biosynthesis in Begonia semperflorens

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Abstract

Low temperature (LT) is an important elicitor that triggers anthocyanin biosynthesis. To investigate whether the reactive oxygen species (ROS) produced via RBOH are involved in this process, we analysed the function and mechanism of ROS produced via RBOH during LT-induced anthocyanin biosynthesis in Begonia semperflorens Link & Otto. The results showed that BsRBOHD transcription was upregulated in LT-grown seedlings at the 3rd hour, which was followed by the upregulation of anthocyanin-biosynthesis genes at the 5–9th hour, leading to anthocyanin accumulation on the 2nd day. The LT-induced increases in ROS production, BsRBOHD and anthocyanin-biosynthesis gene transcription, and anthocyanin content were abolished by the pre-treatment of seedlings with DPI [an inhibitor of nicotinamide adenine nucleoside phosphorylase (NADPH) oxidase or DMTU (a H2O2 scavenger)], but were promoted by pre-treatment with NADPH (a substrate of NADPH oxidase). Changes in the chlorophyll fluorescence parameters showed that pre-treatment of DPI or DMTU alleviated the LT-induced decrease in the seedling chlorophyll content and a/b ratio, which subsequently alleviated the LT-induced decreases in the ABS/CSm, TRo/CSm, RC/CSm, ETo/CSm and REo/CSm values. In contrast, NAPDH pre-treatment intensified these changes. Therefore, we suggest that ROS produced via BsRBOHD may be involved in the LT-induced anthocyanin biosynthesis by strengthening the overaccumulation of ROS produced by the overexcitation of PSII reaction centres and overflux from \({\text{Q}}_{{\text{A}}}^{ - }\) to NADP+ in B. semperflorens.

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REFERENCES

  1. Hughes, N.M., Winter leaf reddening in 'evergreen' species, New Phytol., 2011, vol. 190, p. 573.

    Article  Google Scholar 

  2. Schaberg, P.G., Murakami, P.F., Butnor, J.R., and Hawley, G.J., Experimental branch cooling increases foliar sugar and anthocyanin concentrations in sugar maple at the end of the growing season, Can. J. Forest Res., 2017, vol. 47, p. 696.

    Article  CAS  Google Scholar 

  3. Ensminger, I., Busch, F., and Huner, N.P.A., Photostasis and cold acclimation: sensing low temperature through photosynthesis, Physiol. Plant., 2010, vol. 126, p. 28.

    Article  Google Scholar 

  4. Zhang, K.M., Li, Z., Li, Y., Li, Y.H., Kong, D.Z., and Wu, R.H., Carbohydrate accumulation may be the proximate trigger of anthocyanin biosynthesis under autumn conditions in Begonia semperflorens,Plant Biol., 2013, vol. 15, p. 991.

    Article  CAS  Google Scholar 

  5. Choudhury, F.K., Rivero, R.M., Blumwald, E., and Mittler, R., Reactive oxygen species, abiotic stress and stress combination, Plant J., 2017, vol. 90, p. 856.

    Article  CAS  Google Scholar 

  6. Qu, Y., Bai, X., Zhu, Y., Qi, R., Tian, G., Wang, Y., Li, Y., and Zhang, K., Reactive oxygen species acts as an important inducer in low-temperature-induced anthocyanin biosynthesis in Begonia semperflorens,J. Am. Soc. Hortic. Sci., 2018, vol. 143, p. 486.

    Article  Google Scholar 

  7. Xu, Z. and Rothstein, S.J., ROS-induced anthocyanin production provides feedback protection by scavenging ROS and maintaining photosynthetic capacity in Arabidopsis, Plant Signal. Behav., 2018, vol. 13: e1451708.

    Article  Google Scholar 

  8. Brandes, R.P., Weissmann, N., and Schröder, K., Nox family NADPH oxidases: molecular mechanisms of activation, Free Radic. Biol. Med., 2014, vol. 76, p. 208.

    Article  CAS  Google Scholar 

  9. Suzuki, N., Miller, G., Morales, J., Shulaev, V., Torres, M.A., and Mittler, R., Respiratory burst oxidases: the engines of ros signaling, Curr. Opin. Plant Biol., 2011, vol. 14, p. 691.

    Article  CAS  Google Scholar 

  10. Zhou, J., Xiao, X.J., Zhou, Y.H., Shi, K., Chen, Z., and Yu, J.Q., RBOH1-dependent H2O2 production and subsequent activation of MPK1/2 play an important role in acclimation-induced cross-tolerance in tomato, J. Exp. Bot., 2015, vol. 65, p. 595.

    Article  Google Scholar 

  11. Hu, C.H., Wei, X.Y., Yuan, B., Yao, L.B., Ma, T.T., Zhang, P.P., Wang, X., Wang, P.Q., Liu, W.T., Li, W.Q., Meng, L.S., and Chen, K.M., Genome-wide identification and functional analysis of NADPH oxidase family genes in wheat during development and environmental stress responses, Front. Plant Sci., 2018, vol. 9: 906.

    Article  Google Scholar 

  12. Monshausen, G.B., Bibikova, T.N., Weisenseel, M.H., and Gilroy, S., Ca2+ regulates reactive oxygen species production and pH during mechanosensing in Arabido-psis roots, Plant Cell, 2009, vol. 21, p. 2341.

    Article  CAS  Google Scholar 

  13. Li, X.H., Zhang, H.J., Tian, L.M., Huang, L., Liu, S.X., Li, D.Y., and Song, F.M., Tomato SLRbohB, a member of the NADPH oxidase family, is required for disease resistance against Botrytis cinerea and tolerance to drought stress, Front. Plant Sci., 2015, vol. 6: 463.

    PubMed  PubMed Central  Google Scholar 

  14. Kadota, Y., Shirasu, K., and Zipfel, C., Regulation of the NADPH oxidase RBOHD during plant immunity, Plant Cell Physiol., 2015, vol. 56, p. 1472.

    Article  CAS  Google Scholar 

  15. Noctor, G., Reichheld, J.P., and Foyer, C.H., ROS-related redox regulation and signaling in plants, Semin. Cell Dev. Biol., 2018, vol. 80, p. 3.

    Article  CAS  Google Scholar 

  16. Zhou, J., Xu, X.C., Cao, J.J., Yin, L.L., Xia, X.J., Shi, K., Zhou, Y.H., Chen, Z., and Yu, J.Q., Heat shock factor HsfA1a is essential for R gene-mediated nematode resistance and triggers H2O2 production, Plant Physiol., 2018, vol. 176, p. 2456.

    Article  CAS  Google Scholar 

  17. Grondin, A., Rodrigues, O., Verdoucq, L., Merlot, S., Leonhardt, N., and Maurel, C., Aquaporins contribute to ABA-triggered stomatal closure through OST1-mediated phosphorylation, Plant Cell, 2015, vol. 27, p. 1945.

    Article  CAS  Google Scholar 

  18. Bi, H., Guo, M., Wang, J., Qu, Y., Du, W., and Zhang, K., Transcriptome analysis reveals anthocyanin acts as a protectant in Begonia semperflorens under low temperature, Acta Physiol. Plant., 2018, vol. 40, p. 10.

    Article  Google Scholar 

  19. Wang, J., Guo, M., Li, Y., Wu, R., and Zhang, K., High-throughput transcriptome sequencing reveals the role of anthocyanin metabolism in Begonia semperflorens under high light stress, Photochem. Photobiol., 2018, vol. 94, p. 105.

    Article  CAS  Google Scholar 

  20. Liao, Z., Chen, M., Guo, L., Gong, Y., Tang, F., Sun, X., and Tang, K., Rapid isolation of high-quality total RNA from taxus and ginkgo, Prep. Biochem. Biotec-h., 2004, vol. 34, p. 209.

    Article  CAS  Google Scholar 

  21. Mita, S., Murano, N., Akaike, M., and Nakamura, K., Mutants of Arabidopsis thaliana with pleiotropic effects on the expression of the gene for β-amylase and on the accumulation of anthocyanin that are inducible by sugars, Plant J., 1997, vol. 11, p. 841.

    Article  CAS  Google Scholar 

  22. Arnon, D.I., Copper enzymes in isolated chloroplasts. Polyphenoloxidases in Beta vulgaris,Plant Physiol., 1949, vol. 24, p. 1.

    Article  CAS  Google Scholar 

  23. Brennan, T. and Frenkel, C., Involvement of hydrogen peroxide in the regulation of senescence in pear, Plant Physiol., 1977, vol. 59, p. 411.

    Article  CAS  Google Scholar 

  24. Elstner, E.F. and Heupel, A., Inhibition of nitrite formation from hydroxylammoniumchloride: a simple assay for superoxide dismutase, Anal. Biochem., 1976, vol. 70, p. 616.

    Article  CAS  Google Scholar 

  25. Pan, C., Ahammed, G.J., Li, X., and Shi, K., Elevated CO2 improves photosynthesis under high temperature by attenuating the functional limitations to energy fluxes, electron transport and redox homeostasis in tomato leaves, Front. Plant Sci., 2018, vol. 9: 1739.

    Article  Google Scholar 

  26. Saxena, I., Srikanth, S., and Chen, Z., Cross talk between H2O2 and interacting signal molecules under plant stress response, Front. Plant Sci., 2016, vol. 7: 570.

    Article  Google Scholar 

  27. Mei, Y., Chen, H., Shen, W., Shen, W., and Huang, L., Hydrogen peroxide is involved in hydrogen sulfide-induced lateral root formation in tomato seedlings, BMC Plant Biol., 2017, vol. 17, p. 162.

    Article  Google Scholar 

  28. Tisarum, R., Theerawitaya, C., Samphumphuang, T., and Cha-um, S., Regulation of anthocyanin accumulation in rice (Oryza sativa L. subsp. indica) using MgSO4 spraying and low temperature, Arch. Agron. Soil Sci., 2018, vol. 64, p. 1663.

    Article  CAS  Google Scholar 

  29. Parvanova, D., Popova, A., Zaharieva, I., Lambrev, P., Konstantinova, T., Taneva, S., Atanassov, A., Goltsev, V., and Djilianov, D., Low temperature tolerance of tobacco plants transformed to accumulate proline, fructans, or glycine betaine. Variable chlorophyll fluorescence evidence, Photosynthetica, 2004, vol. 42, p. 179.

    Article  CAS  Google Scholar 

  30. Li, Y.T., Liang, Y., Li, Y.N., Che, X.K., Zhao, S.J., Zhang, Z.S., and Gao, H.Y., Mechanisms by which Bisphe-nol A affect the photosynthetic apparatus in cucumber (Cucumis sativus L.) leaves, Sci. Rep., 2018, vol. 8: 4253.

    Article  Google Scholar 

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Funding

This research was supported by the Natural Science Foundation of Henan Province (project no. 182300410091) and the Key Scientific Research Project of High Education in Henan Province (project no. 18B220004).

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This information is published at the request of the authors to determine the contribution of each author to the study.

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Correspondence to P. F. Wang.

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This article does not contain any studies involving animals or human participants performed by any of the authors. The authors declare no conflicts of interest.

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Abbreviations: DMTU—N,N'-dimethylthiourea; DPI—diphenyleneiodonium chloride; LT—low temperature; RBOHs—plant respiratory burst oxidase homologues.

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Zhang, K.M., Tian, G., Li, X.H. et al. ROS Produced via BsRBOHD Plays an Important Role in Low Temperature-Induced Anthocyanin Biosynthesis in Begonia semperflorens. Russ J Plant Physiol 67, 250–258 (2020). https://doi.org/10.1134/S1021443720020181

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