Skip to main content
SpringerLink
Log in

Improvement in Submergence Tolerance of Cherry Through Regulation of Carbohydrate Metabolism and Plant Growth by PsERF and PsCIPK

  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Cherry is an important fruit tree with delicious taste and high economic value, which have been planted worldwide. However, this species cannot withstand the presence of excessive amount of water; submergence injury sometimes occurs during cultivation of cherry and results in severe economic losses. By using a submergence-tolerant germplasm Prunus serrulata “Yimeng” and a submergence-sensitive germplasm Prunus pseudocerasus “Aihua” as test materials, this study cloned PsERF and PsCIPK, which are related to submergence tolerance in cherry, and analyzed the expression of PsERF and PsCIPK in submergence-tolerant and submergence-sensitive germplasms under submergence stress; moreover, the consistency and correlation of such expression with carbohydrate metabolism and plant growth-related genes (PsPDC, PsSUS, PsRAMY, and PsEXP) were analyzed. The results showed that PsERF and PsCIPK influence the expression of PsPDC, PsSUS, PsRAMY, and PsEXP at different extents under submergence and during recovery to systematically improve the submergence resistance of P. serrulata “Yimeng”. This study lays the important theoretical and practical foundation for molecular improvement and germplasm innovation in submergence tolerance in cherry through genetic engineering.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

AP2/ERF:

APETALA2/Ethylene responsive factor

SUB1:

Submergence 1

HRE:

Hypoxia responsive ERF

CIPK:

Calcineurin B-like–interacting protein kinase

RAMY:

α-Amylase

SUS:

Sucrose Synthase

ADH:

Alcohol dehydrogenase

PDC:

Pyruvate decarboxylase

EXP:

Expansin

GA:

Gibberellin

ABA:

Abscisic acid

References

  1. Kumutha, D., Sairam, R. K., Ezhilmathi, K., Chinnusamy, V., & Meena, R. C. (2008). Effect of waterlogging on carbohydrate metabolism in pigeon pea (Cajanus cajan L.): Upregulation of sucrose synthase and alcohol dehydrogenase. Plant Science, 175, 706–716.

    Article  CAS  Google Scholar 

  2. Liao, H. B., Meng, X. L., & Guo, W. D. (2011). Effects of different rootstocks on the flood resistance of sweet cherries. J. Anhui Agri. Sci., 39(22), 13335–13339.

    CAS  Google Scholar 

  3. Zhang, Z. X., Zou, X. L., Tang, W. H., & Zheng, Y. L. (2006). Revelation on early response and molecular mechanism of submergence tolerance in maize roots by microarray and suppression subtractive hybridization. Environmental and experimental botany, 58(1–3), 53–63.

    Article  CAS  Google Scholar 

  4. Pedersen, O., Malik, A. I., & Colmer, T. D. (2010). Submergence tolerance in Hordeum marinum: dissolved CO2 determines underwater photosynthesis and growth. Funct. Plant Bio., 37(6), 524–531.

    Article  CAS  Google Scholar 

  5. Pena-Castro, J. M., van Zanten, M., Lee, S. C., Patel, M. R., Voesenek, L. A. J. C., Fukao, T., & Bailey-Serres, J. (2011). Expression of rice SUB1A and SUB1C transcription factors in Arabidopsis uncovers flowering inhibition as a submergence tolerance mechanism. The plant journal, 67(3), 434–446.

    Article  CAS  PubMed  Google Scholar 

  6. Xu, K., Xu, X., Fukao, T., Canlas, P., Maghirang-Rodriguez, R., Heuer, S., Ismail, A. M., Bailey-Serres, J., Ronald, P. C., & Mackill, D. J. (2006). Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature, 442(7103), 705–708.

    Article  CAS  PubMed  Google Scholar 

  7. Lee, K. W., Chen, P. W., Lu, C. A., Chen, S., Ho, T. H., & Yu, S. M. (2009). Coordinated responses to oxygen and sugar defficiency allow rice seedlings to tolerate flooding. Science Signaling, 2(91), ra61.

    Article  PubMed  Google Scholar 

  8. Yang, C. Y., Hsu, F. C., Li, J. P., Wang, N. N., & Shih, M. C. (2011). The AP2/ERF transcription factor AtERF73/HRE1 modulates ethylene responses during hypoxia in Arabidopsis. Plant physiology, 156, 202–212.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Hess, N., Klode, M., Anders, M., & Sauter, M. (2011). The hypoxia responsive transcription factor genes ERF71/HRE2 and ERF73/HRE1 of Arabidopsis are differentially regulated by ethylene. Physiologia Plantarum, 143(1), 41–49.

    Article  CAS  PubMed  Google Scholar 

  10. Insausti, P., Grimoldi, A. A., Chaneton, E. J., & Vasellati, V. (2001). Flooding induces a suite of adaptive plastic responses in the grass Paspalum dilatatum. New Phytol., 152, 291–299.

    Article  Google Scholar 

  11. Aschi-Smiti, S., Chaïbi, W., Brouquisse, R., Ricard, B., & Saglio, P. (2003). Assessment of enzyme induction and aerenchyma formation as mechanisms for flooding tolerance in Trifolium subterraneum ‘park’. Annals of botany, 91, 195–204.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Ashraf, M., & Habib-ur-Rehman. (1999). Interactive effects of nitrate and long-term waterlogging on growth, water relations and gaseous exchange properties of maize (Zea mays L.) Plant science, 144(1), 35–43.

    Article  CAS  Google Scholar 

  13. Shiono, K., Takahashi, H., Colmer, T. D., & Nakazono, M. (2008). Role of ethylene in acclimations to promote oxygen transport in roots of plants in waterlogged soils. Plant Science, 175, 52–58.

    Article  CAS  Google Scholar 

  14. Santosa, I. E., Ram, P. C., Boamfa, E. I., Laarhoven, L. J. J., Reuss, J., Jackson, M. B., & Harren, F. J. M. (2007). Patterns of peroxidative ethane emission from submerged rice seedlings indicate that damage from reactive oxygen species takes place during submergence and is not necessarily a post-anoxic phenomenon. Planta, 226(1), 193–202.

    Article  CAS  PubMed  Google Scholar 

  15. Perata, P., & Voesenek, L. A. C. J. (2007). Submergence tolerance in rice requires Sub1A, an ethylene-response-factor-like gene. Trends in Plant Sci., 12(2), 43–46.

    Article  CAS  Google Scholar 

  16. Jackson, M. B., & Ram, P. C. (2003). Physiological and molecular basis of susceptibility and tolerance of rice plants to complete submergence. Annals of Botany, 91, 227–241.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Lee, D. K., Ahn, J. H., Song, S. K., Choi, Y. D., & Lee, J. S. (2003). Expression of an expansin gene is correlated with root elongation in soybean. Plant physiology, 131(3), 985–997.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Umeda, M., & Uchimiya, H. (1994). Differential transcript levels of genes associated with glycolysis and alcohol fermentation in rice plants (Oryza sativa L.) under submergence stress. Plant physiology, 106, 1015–1022.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Sachs, M. M., Subbiah, C. C., & Saab, I. N. (1996). Anaerobic gene expression and flooding tolerance in maize. Journal of experimental botany, 47, 1–15.

    Article  CAS  Google Scholar 

  20. Chen, Q., Guo, X. W., Hu, Y. L., Li, J., Gao, X. B., Wang, C., Hao, Y. H., Zhao, L., & Mao, Z. Q. (2007). Effects of water-logging on anaerobic respiration enzymes and fermentation products in roots of two kind of sweet cherry rootstocks. Acta ecologica sinica, 27(11), 4925–4931.

    CAS  Google Scholar 

  21. Sheng, L. X., Feng, L. G., & Shu, H. R. (2008). Effect of calcium on the functions of antioxidant systems and mitochondria in cherry rootstock roots under hypoxia stress. Sci. Agr. Sin., 41(11), 3913–3919.

    CAS  Google Scholar 

  22. Hao, Y. H., Hu, Y. L., Shen, X., Mao, Z. Q., Wang, Y. Z., Su, L. T., & Yang, S. Q. (2009). Exogenous NO3 − enhanced sugar contents and sucrose correlated enzymes activity in roots of sweet cherry under waterlogging condition. Acta Hortic. Sinica., 36(7), 937–944.

    CAS  Google Scholar 

  23. Meng, X. Y. (2016). Cloning and expression analysis of genes related to waterlogging tolerance in cherry. Master Thesis. Yangzhou: Yangzhou University.

  24. Feng, L. G., Chen, C., Li, T. L., Wang, M., Tao, J., Zhao, D. Q., & Sheng, L. X. (2014). Flowery odor formation revealed by differential expression of monoterpene biosynthetic genes and monoterpene accumulation in rose (Rosa rugosa Thunb.) Plant Physiol. Bioch., 75, 80–88.

    Article  CAS  Google Scholar 

  25. Schmittgen, T. D., & Livak, K. J. (2008). Analyzing real-time PCR data by the comparative CT method. Nature protocols, 36, 1101–1108.

    Article  Google Scholar 

  26. Kudahettige, N. P., Pucciariello, C., Parlanti, S., Alpi, A., & Perata, P. (2011). Regulatory interplay of the Sub1A and CIPK15 pathways in the regulation of α-amylase production in flooded rice plants. Plant biology, 13, 611–619.

    Article  CAS  PubMed  Google Scholar 

  27. Sheng, L. X., Feng, L. G., & Shu, H. R. (2009). Effects of nitrogen on the activity of antioxidant enzymes and functions of mitochondria in cherry rootstock toots under hypoxia stress. Acta Hortic. Sinica., 36(11), 1575–1580.

    CAS  Google Scholar 

  28. Sheng, L. X., Feng, L. G., & Shu, H. R. (2011). Effects of applying calcium on the functions and nitrogen metabolism of cherry root system under hypoxia stress. Chinese J. Ecol., 30(10), 2209–2213.

    Google Scholar 

  29. Feng, L. G., Sheng, L. X., & Shu, H. R. (2010). Effects of exogenous NO3 − on cherry root function and enzyme activities related to nitrogen metabolism under hypoxia stress. Chinese J. Appl. Ecol., 21(12), 3282–3286.

    CAS  Google Scholar 

  30. Vriezen, W. H., Graaf, B. D., Mariani, C., & Voesenek, L. A. C. J. (2000). Submergence induces expansin gene expression in flooding-tolerant Rumex palustris and not in flooding-intolerant R. acetosa. Planta, 210(6), 956–963.

    Article  CAS  PubMed  Google Scholar 

  31. Fukao, T., Xu, K., Ronald, P. C., & Bailey-Serres, J. (2006). A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice. The Plant Cell, 18(8), 2021–2034.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Jung, K. H., Seo, Y. S., Walia, H., Cao, P. J., Fukao, T., Canlas, P. E., Amonpant, F., Bailey-Serresand, J., & Ronald, P. C. (2010). The submergence tolerance regulator Sub1A mediates stress-responsive expression of AP2/ERF transcription factors. Plant Physiology, 152(3), 1674–1692.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Morimoto, K., & Yamasue, Y. (2007). Differential ability of alcohol fermentation between the seeds of flooding-tolerant and flooding-susceptible varieties of Echinochloa crusgalli (L.) Beauv. Weed Biol. Manag., 7(1), 62–69.

    Article  CAS  Google Scholar 

  34. Dennis, E. S. (2000). Molecular strategies for improving waterlogging tolerance in plants. Journal of experimental botany, 51, 89–97.

    Article  CAS  PubMed  Google Scholar 

  35. Geigenberger, P. (2003). Response of plant metabolism to too little oxygen. Current opinion in plant biology, 6, 247–256.

    Article  CAS  PubMed  Google Scholar 

  36. Ruan, Y. L., & Chourey, P. S. (1998). A fiberless seed mutation in cotton is associated with lack of fiber cell initiation in ovule epidermis and alterations in sucrose synthase expression and carbon partitioning in developing seeds. Plant Physiology, 118(2), 399–406.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Huang, S. B., Colmer, T. D., & Millar, A. H. (2008). Does anoxia tolerance involve altering the energy currency towards Ppi? Trends in Plant Science, 13, 221–227.

    Article  CAS  PubMed  Google Scholar 

  38. Crawford, R. M. M., & Brndle, R. (1996). Oxygen deprivation stress in a changing environment. Journal of experimental botany, 47, 145–159.

    Article  CAS  Google Scholar 

  39. Li, J. (2008). Effects of different nitrogen types on the physiological and biochemical characteristics during recovery of waterlogging in sweet cherry. Doctoral dissertation. Tai’an: Shandong Agricultural University.

    Google Scholar 

  40. Eck, W. H. J. M. V., Steeg, H. M. V. D., Blom, C. W. P. M., & Kroon, H. D. (2004). Is tolerance to summer flooding correlated with distribution patterns in river floodplains? A comparative study of 20 terrestrial grassland species. Oikos, 107, 393–405.

    Article  Google Scholar 

Download references

Acknowledgments

This research was funded by National Natural Science Foundation of China (Grant No. 31301746).

Author information

Authors and Affiliations

  1. College of Horticulture and Plant Protection, Yangzhou University, Yangzhou, 225009, China

    Lixia Sheng, Xiangyi Meng, Meng Wang, Shu Zang & Liguo Feng

Authors
  1. Lixia Sheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiangyi Meng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Meng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shu Zang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Liguo Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

L.X. Sheng and L.G. Feng conceived and designed the experiments. X.Y. Meng and M. Wang performed the experiments. L.X. Sheng and X.Y. Meng analyzed the data and wrote the paper. S. Zang contributed reagents/materials/analysis tools.

Corresponding author

Correspondence to Liguo Feng.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Fig. S1

(DOCX 570 kb)

Fig. S2

(DOCX 108 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sheng, L., Meng, X., Wang, M. et al. Improvement in Submergence Tolerance of Cherry Through Regulation of Carbohydrate Metabolism and Plant Growth by PsERF and PsCIPK . Appl Biochem Biotechnol 184, 63–79 (2018). https://doi.org/10.1007/s12010-017-2530-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-017-2530-4

Keywords

Search

Navigation