SpringerLink
Log in

The Influence of Endogenous Sugar on Potato Tuberization in In Vivo Conditions

  • Published:
American Journal of Potato Research Aims and scope Submit manuscript

Abstract

Sugar (S) and nitrogen (N) play critical roles in potato tuberization and development, which determines the number, size, and yield of tubers. However, the dynamic models of endogenous sugar and nitrogen during tuberization and development are poorly understood. A pot experiment was performed with the potato cultivar Jizhangshu 12. Tuber and leaf samples were continuously taken to detect the morphological changes in stolon or tuber during tuberization and development. Sugar, starch, nitrogen content, and sucrose metabolism-related enzyme activity were measured. Results showed that the starch, fructose, and sucrose content and S/N ratio in leaves decreased significantly, while significant increases were observed in the activities of alkaline invertase (ALI), sucrose synthetase (SS), and sucrose phosphate synthase (SPS), and the ratios of glucose/sucrose and glucose/fructose from stolon hook initiation to subapical swelling. In contrast, nitrogen content and S/N ratio decreased significantly and starch and glucose content, AI (acid invertase), ALI, SS, and SPS activities, and glucose/sucrose ratio in stolons increased significantly. When the diameter from the stolon subapical swelling to the tuber reached 3.0 cm, starch content and glucose/sucrose and glucose/fructose ratios in leaves and tubers, and contents of fructose and sucrose and the activities of AI and SPS in tubers fluctuated; the S/N ratio in both leaves and tubers increased significantly; the activity of SPS in leaves, and activities of ALI and SS in tubers declined significantly. When the tuber diameter increased from 3.0 to 6.0 cm, the content of starch, sucrose, fructose, and total nitrogen, the activities of AI, ALI, and SPS, and the S/N ratio in leaves increased, while the ratios of glucose/sucrose and glucose/fructose showed an opposite trend; the changes in tubers were slight. We conclude that the content of sugar and total nitrogen and the balance of sugar and nitrogen in leaves and stolons changed significantly at tuberization and gradually thereafter. The significant increases in the ratios of glucose/fructose and glucose/sucrose in leaves could be used as indirect indicators to determine tuberization. The ratio of S/N could replace that of nonstructural carbohydrate/nitrogen to characterize potato tuberization and development.

Resumen

El azúcar (S) y el nitrógeno (N) juegan papeles críticos en la tuberización y desarrollo de la papa, lo cual determina el número, el tamaño y el rendimiento de tubérculos. No obstante, los modelos dinámicos de azúcar endógeno y de nitrógeno durante la tuberización y el desarrollo se entienden pobremente. Se desarrolló un experimento en macetas con la variedad de papa Jizhangshu 12. Se tomaron continuamente muestras de tubérculo y hoja para detectar los cambios morfológicos en estolón y tubérculos durante la tuberización y el desarrollo. Se midieron el contenido de azúcar, almidón y nitrógeno, y la actividad enzimática relacionada con el metabolismo de la sacarosa. Los resultados mostraron que los contenidos del almidón, fructosa y sacarosa, y la relación S/N en hojas disminuyó significativamente, mientras que se observaron aumentos significativos en las actividades de la invertasa alcalina (ALI), sacarosa sintetasa (SS), y sacarosa fosfato sintetasa (SPS) y las relaciones de glucosa/sacarosa y glucosa/fructosa de la iniciación del gancho del estolón hacia la hinchazón subapical. En contraste, el contenido de nitrógeno y la relación S/N disminuyó significativamente, y el contenido de almidón y glucosa, las actividades de AI (invertasa ácida), ALI, SS, y SPS, y la relación glucosa/sacarosa en los estolones, aumentó significativamente. Cuando el diámetro de la hinchazón subapical del estolón hacia tubérculo alcanzó los 3.0 cm, fluctuaron el contenido de almidón y la proporción glucosa/sacarosa y glucosa/fructosa en hojas y tubérculos, y el contenido de fructosa y sacarosa, y las actividades de AI y SPS en tubérculos; la relación S/N, tanto en hojas como en tubérculos, aumentó significativamente; la actividad de SPS en hojas, y las actividades de ALI y SS en tubérculos declinó significativamente. Cuando aumentó el diámetro del tubérculo de 3.0 a 6.0 cm, aumentaron el contenido de almidón, sacarosa, fructosa, y nitrógeno total, y las actividades de Al, ALI y APS, y la relación S/Nen hojas, mientras que las relaciones de glucosa/sacarosa y glucosa/fructosa mostraron una tendencia opuesta; los cambios en los tubérculos fueron ligeros. Concluimos que el contenido de azúcar y el nitrógeno total, y el balance de azúcar y nitrógeno en hojas y estolones cambió significativamente en la tuberización y gradualmente de ahí en adelante. Los aumentos significativos en las relaciones de glucosa/fructosa y glucosa/sacarosa en hojas pudieran usarse como indicadores indirectos para determinar la tuberización. La relación S/N pudiera reemplazar a la de carbohidrato no estructural/nitrógeno, para caracterizar la tuberización y el desarrollo de la papa.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Appeldoorn, N. 1999. Developmental changes in carbohydrate metabolism during early tuberisation of potato. Holland: Wageningen Universiteit.

    Google Scholar 

  • Botjes, J.G. Oortwijn. 1927. Ontijdige knolvorming bij aardappelen. Tijdschrift Over Plantenziekten 33: 1–13.

    Google Scholar 

  • Cao, B.B. 2017. Effects of different cultivars and cultivations on leaf senescence and C/N of wheat. Master thesis: Northwest Sci-Tech University of Agriculture and Forestry, China.

    Google Scholar 

  • Chen, D., S. Wang, B. **ong, B. Cao, and X. Deng. 2015. Carbon/nitrogen imbalance associated with drought-induced leaf senescence in sorghum bicolor. PLoS One 10 (8): e0137026.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cui, N., W.P. Wang, F. Lin, L.P. Bai, and Y.L. Zhang. 2010. Update on fructokinase in higher plants. Chinese Agricultural Science Bullentin 26 (14): 41–47.

    Google Scholar 

  • Dai, M.H., J.R. Zhao, G.H. Yang, R.H. Wang, and G.P. Chen. 2011. Source-sink relationship and carbon-nitrogen metabolism of maize in different ecological regions and varieties. Scientia Agricultura Sinica 44 (8): 1585–1595.

  • Davies, H.V. 1984. Sugar metabolism in stolon tips of potato during early tuberisation. Zeitschrift für Pflanzenphysiologie 113 (5): 377–381.

    Article  CAS  Google Scholar 

  • Dick, Vreugdenhil, Yvonne Boogaard, G.F. Visser Richard, and M. de Bruijn Steef. 1998. Comparison of tuber and shoot formation from in vitro cultured potato explants. Plant Cell, Tissue and Organ Culture 53: 197–204.

    Article  Google Scholar 

  • Duan, C.Q., Y.Z. Wang, Q.H. Pan, L.Y. Zhang, and D.P. Zhang. 2003. Negative regulation of amylase activity by fructose and glucose in growing apple fruits. Acta Horticulturae Sinica 30 (1): 74–76.

    Google Scholar 

  • Eckert, D.J., and E.O. Mclean. 1981. Dry matter production and nitrogen utilization by six potato cultivars. Agronomy Journal 73 (5): 799–802.

    Article  Google Scholar 

  • Fang, J.G., X.D. Zhu, H.F. Jia, and C. Wang. 2017. Research advances on physiological function of plant sucrose synthase. Journal of Nan**g Agricultural University 40 (5): 759–768.

    Google Scholar 

  • Fernie, A.R., and L. Willmitzer. 2001. Molecular and biochemical triggers of potato tuber development. Plant Physiology 127 (4): 1459–1465.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao, J.F. 2006. Plant physiology experiment guidance, 105–108. Bei**g: Higher Education Press.

    Google Scholar 

  • Hana Ševčíková, Mašková Petra, Tarkowská Danuše, Mašek Tomáš, and Lipavská Helena. 2017. Carbohydrates and gibberellins relationship in potato tuberization. Journal of Plant Physiology 214: 53–63.

  • Horacio, P., and G. Martinez-Noel. 2013. Sucrose signaling in plants: A world yet to be explored. Plant Signaling & Behavior 8 (3): e23316.

    Article  CAS  Google Scholar 

  • Huber, S.C., and J.L. Huber. 1996. Role and regulation of sucrose-phosphate synthase in highter plants. Physiology and Molecular Biology of Plants 47: 431–444.

    Article  CAS  Google Scholar 

  • Im, V.D.M., M. Ebskamp, R. Visser, P. Weisbeek, and S. Smeekens. 1994. Fructan as a new carbohydrate sink in transgenic potato plants. Plant Cell 6 (4): 561–570.

    Article  Google Scholar 

  • Ivins, J., and P. Bremner. 1965. Growth, development and yield in the potato. Outlook on Agriculture 4: 211–217.

    Article  Google Scholar 

  • Janick. 1982. Horticultural reviews. London: Palgrave Macmillan UK.

    Book  Google Scholar 

  • Khuri, S., and J. Moorby. 1995. Investigation into the role of sucrose in potato cv. Estima microtuber production in vitro. Annals of Botany 75: 295–303.

    CAS  Google Scholar 

  • Li, D., Y. Wang, L. He, X.Y. Shi, and F.M. Ma. 2009. Study on the relationship between the sucrose metabolizing enzymes and accumulation in sugar beet. Crops 25 (3): 27–31.

    Google Scholar 

  • Li, T.T., J.Q. Xue, S.L. Wang, Y.Q. Xue, F.R. Hu, and X.X. Zhang. 2018. Research advances in the metabolism and transport of non-structural carbohydrates in plants. Plant Physiology Journal 54 (1): 25–35.

    CAS  Google Scholar 

  • Liu, J., and C.H. **e. 2001. The mechanism of potato (Solanum tuberosum L.) tuber development and related gene expression. Chinese Bulletin of Botany 18 (5): 531–539.

    Google Scholar 

  • Liu, Y., X.H. Lin, Y.L. Yao, and J.B. Su.. 2012. Sucrose metabolism in higher plants. Chinese Agricultural Science Bullentin 28 (6): 145–152.

  • Liu, H.K., X.N. Liu, Y.F. Huang, and Y.L. Ye. 2014. Effect of nitrogen application on carbon metabolisms and relationship between carbon metabolism and wheat scab. Chinese Journal of Eco-Agriculture 22 (7): 782–789.

    Google Scholar 

  • Lukas, F., L. Helena, H. Jean-Francois, and O. Zdenek. 2008. Morphological and molecular characterization of a spontaneously tuberizing potato mutant: An insight into the regulatory mechanisms of tuber induction. BMC Plant Biology 8 (1): 117.

    Article  CAS  Google Scholar 

  • Luo, Y. 2004. Sugar metabolism and relation enzymes in plants. Journal of Wenshan Teacher College 17 (2): 155–159.

    Google Scholar 

  • Men, F.Y., and M.Y. Liu. 1993. Potato cultivation physiology. Bei**g: China Agricultural Publishing House.

    Google Scholar 

  • Minhas, J.S., V.K. Rai, and H.S. Saini. 2004. Carbohydrate metabolism during tuber initiation in potato:A transient surge in invertase activity marks the stolon to tuber transition. Potato Research 47 (5): 113–126.

    Article  Google Scholar 

  • Müller-Röber, B., U. Sonnewald, and L. Willmitzer. 1992. Inhibition of the ADP-glucose pyrophosphorylase in transgenic potatoes leads to sugar-storing tubers and influences tuber formation and expression of tuber storage protein genes. EMBO Journal 11 (4): 1229–1238.

    Article  PubMed  Google Scholar 

  • Pan, Q.M., G.X. Han, Y.F. Bai, and J.C. Yang. 2002. Advances in physiology and ecology studies on stored non-structure carbohydrates in plants. Chinese Bulletin of Botany 19 (1): 30–38.

    Google Scholar 

  • Ross, H.A., H.V. Davies, L.R. Burch, R. Viola, and D. Mcrae. 1994. Developmental changes in carbohydrate content and sucrose degrading enzymes in tuberising stolons of potato (solanum tuberosum). Physiologia Plantarum 90 (4): 748–756.

    Article  CAS  Google Scholar 

  • Si, L.Z., and C.C. Chu. 2003. Manipulation of sucrose synthesis in transgenic plant. Journal of Chinese biotechnology 23 (1): 11–16.

    CAS  Google Scholar 

  • Viola, R., A.G. Roberts, S. Haupt, S. Gazzani, R.D. Hancock, and N. Marmiroli. 2001. Tuberization in potato involves a switch from apoplastic to symplastic phloem unloading. Plant Cell 13 (2): 385–398.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, L.N., H.B. Tao, and M.H. Dai. 2009. Effect of coated urea on grain yield and metabolism of summer maize. Journal of Maize Sciences 17 (2): 124–129.

    Google Scholar 

  • Ward, J.M., C. Kühn, M. Tegeder, and W.B. Frommer. 1998. Sucrose transport in higher plants. International Review of Cytology 178 (335): 41–71.

    CAS  PubMed  Google Scholar 

  • Wellensiek, S.J. 1929. The physiology of tuber-formation in Solanum tuberosum L. Ede: Veenman.

    Google Scholar 

  • **ong, B.L., X.Y. Wang, D.Q. Chen, S.Y. Wang, L.N. Yin, and X.P. Deng. 2016. Carbon/nitrogen balance associate with drought-induced leaf senescence in maize (zea mays) seedling. Acta Botanica Boreali-Occidentalia Sinica 36 (3): 534–541.

    Google Scholar 

  • Xu, X., André A.M. van Lammeren, and V.D. Vreugdenhil. 1998. The role of gibberellin, abscisic acid, and sucrose in the regulation of potato tuber formation in vitro. Plant Physiology 117 (2): 575–584.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang, H., and L.T. Yang. 2000. Dynamic changes of nucleic acid content of buds and leaves during flower bud differentiation in apricot trees. Acta Horticulturae Sinica 27 (2): 90–94.

    Google Scholar 

  • Zhang T.T. 2015. Effects of different nitrogen levels on carbon and nitrogen metabolism,y ield and quality of potato. Master thesis, Inner Mongolia Agricultural University, China.

  • Zhang, G.Z. 2016. Effects of sugar metabolism on stolon occurrence and tuber formation in potato. Master thesis: Heilongjiang Bayi Agricultural University, China.

    Google Scholar 

  • Zhang, Z.L., Z.W. Zhai, and X.F. LI. 2009. Plant physiology experiment guidance (fourth edition), 103–104. Bei**g: Higher Education Press.

    Google Scholar 

  • Zhang, H.Y., S.T. Dong, and R.Q. Gao. 2016. The study progress in plant starch. Joumal of the Chinese cereals and oils association 21 (1): 41–46.

    Google Scholar 

  • Zhao, J.T. 2016. Advances in research on invertase in plant development and response to abiotic and biotic stresses. Journal of Tropical and Subtropical Botany 24 (3): 352–358.

    CAS  Google Scholar 

  • Zhao, Z.Z., S.L. Zhang, C.J. Xu, K.S. Chen, and S.T. Liu. 2001. Roles of sucrose-metabolizing enzymes in accumulation of sugars in Satsuma mandarin fruit. Acta Horticulturae Sinica 28 (2): 112–118.

    Google Scholar 

  • Zheng, S.L. 2008. Effects of nourishment on the physiological character in the process of tuber formation in Solanum tuberosum L. PHD dissertation: Sichuan Agricultural University, China.

    Google Scholar 

  • Zheng, H.L., Y.N. Wang, J.Y. Zhao, X.H. Shi, Z. Ma, and M.S. Fan. 2018. Tuber formation as influenced by the C:N ratio in potato plants. Journal of Plant Nutrition and Soil Science 181 (5): 686–693.

    Article  CAS  Google Scholar 

  • Zuo, Q.H., J. Yin, G.L. Tian, and Y. Feng. 2012. Release of the new potato variety Jizhangshu 12. Chinese Potato Journal 26 (2): 127–128.

    Google Scholar 

Download references

Acknowledgements

This work was supported by Agriculture Research System of China (CARS-09-P10).

Author information

Authors and Affiliations

  1. College of Agronomy, Inner Mongolia Agricultural University, Hohhot, 010019, China

    Lili Meng, Tingting Zhang, Yingying Zhang & Meilian Meng

  2. College of Life Science, Inner Mongolia Agricultural University, Hohhot, 010018, China

    Youjun Chen

  3. Inner Mongolia Academy of Agricultural /Animal husbandry Sciences, Hohhot, 010031, China

    **aojiao Wang

  4. Chinese Academy of Agricultural Sciences / Key Laboratory of Biology and Genetic Improvement of Tuber and Root Crop, Ministry of Agriculture and Rural Affairs, Institute of Vegetables and Flowers, Bei**g, 100081, China

    Junhong Qin

Authors
  1. Lili Meng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tingting Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Youjun Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yingying Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. **aojiao Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Junhong Qin
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Meilian Meng
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

M.L. and Q.J. designed the experiment. M.L., Z.T., and Z.Y. performed the experiment with the help of W.X. and C.Y.. M.L. analyzed the data and wrote the manuscript with input from M.M. and Q.J. All authors read and approved the manuscript.

Corresponding authors

Correspondence to Junhong Qin or Meilian Meng.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Meng, L., Zhang, T., Chen, Y. et al. The Influence of Endogenous Sugar on Potato Tuberization in In Vivo Conditions. Am. J. Potato Res. 97, 297–307 (2020). https://doi.org/10.1007/s12230-020-09782-4

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12230-020-09782-4

Keywords

Search

Navigation