Abstract
Nitrogen (N) is the most important nutrient for potato growth. N fertilizer has an important effect on the tuber yield and starch content in potatoes. In this study, taking the high-starch cultivar Kexin 22 and the low-starch cultivar Kexin 19 as experimental materials, three N fertilizer application rates—0, 150 and 300 kg/ha—were used to investigate the effects of different N application rates on starch accumulation and the expression of starch synthase genes in potato tubers with different starch contents. In the cultivar Kexin 22, the accumulations of amylose, amylopectin and total starch showed a ranking of N150 > N300 > N0 for the entire growth period. The cultivar Kexin 19 showed an accumulation pattern of N0 > N150 > N300 in the early growth period, N150 > N300 > N0 in the middle growth period and N300 > N150 > N0 in the late growth period. Compared with those in Kexin 19, the expressions of the glucose-1-phosphate adenyltransferase (AGPP-L), granule-bound starch synthase (GBSSI), starch-branching enzyme I (SBEI) and soluble starch synthase III (SSIII) genes in Kexin 22 were upregulated, whereas no obvious difference existed in the expression of the alkylglycerone phosphate synthase (AGPP-S) and soluble starch synthase II (SSII) genes between the two cultivars. In Kexin 22, the different N application rates had a significant effect on the peak expression levels of AGPP-L, GBSSI, SBEI and SSIII but had a small effect on the peak expression time for these genes. Among these genes, most showed a ranking of N150 > N300 > N0 in the early and middle growth periods, and all showed a ranking of N300 > N150 > N0 in the late growth period; most showed a peak expression time on the 65th day after emergence (DAE 65). In Kexin 19, the different N application rates had a significant effect on the peak expression levels and peak expression times of the AGPP-L, GBSSI, SBEI and SSIII genes. Among these genes, all showed a ranking of N0 > N150 > N300 in the early growth period, whereas most showed a ranking of N150 > N300 > N0 in the middle growth period, and all showed a ranking of N300 > N150 > N0 in the late growth period. In Kexin 19, the peak gene expression was shifted to an earlier date under the low N levels, and it was delayed under the high N levels. The effects of the N application rate on the activities of starch synthases AGPP, GBSS, SSS and SBE showed largely the same trends as those in the expression levels of the related genes. Therefore, to obtain a high harvest of starch yield, different N application rates should be recommended for different cultivars.
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References
Doan DN, Rudi H, Olsen OA (1999) The allosterically unregulated isoform of ADP-glucose pyrophosphorylase from barley endosperm is the most likely source of ADP-glucose incorporate into endosperm starch. Plant Physiol 121:965–975
Edwards A, Fulton DC, Hylton CM, Jobling SA, Gidley M, Rossner U, Martin C, Smith AM (1999) A combined reduction in activity of starch synthase II and III of potato has novel effects on the starch of tubers. Plant J 17:251–261
Emes MJ, Neuhaus HE (1997) Metabolism and transport in non-photosynthetic plastids. J Exp Bot 48:1995–2005
Fernie AR, Willmitzer L, Trethewey RN (2002) Sucrose to starch: a transition in molecular plant physiology. Trends Plant Sci 7:35–41
Fulton DC, Edwards A, Pilling E, Robinson HL, Fahy B, Seale R, Kato L, Donald AM, Geigenberger P, Martin C, Smith AM (2002) Role of granule bound starch synthase in determination of amylopectin structure and starch granule morphology in potato. J Biol Chem 277:10834–10841
Gálvez JH, Tai HH, Lagüe M, Zebarth BJ, Strömvik MV (2016) The N responsive transcriptome in potato (Solanum tuberosum L.) reveals significant gene regulatory motifs. Sci Rep 6:1–15
Geigenberger P (2003) Regulation of sucrose to starch conversion in growing potato tubers. J Exp Bot 54:457–465
Geigenberger P, Kolbe A, Tiessen A (2005) Redox regulation of carbon storage and partitioning in response to light and sugars. J Exp Bot 56:1469–1479
He Z (1985) Quality and analysis technique for seeds of grain and oil crops. China Agric Press, Beijing
He C, Zhang J, Qiu H, Zhang C, Zhang H, Zhang W (2017) Effect of N levels on dry matter accumulation distribution and yield of ‘Qingshu 9’ with film on dry land. J Gansu Agri Univ 52:19–26
Hovenkamp-Hermelink JHM, Jacobsen E, Ponstein AS, Visser RGF, Vos-Scheperkeuter GH, Bijmolt EW, deVries JN, Witholt B, Feenstra WJ (1987) Isolation of an amylose-free starch mutant of the potato (Solanum tuberosum L.). Theor Appl Genet 75:217–221
Hu X, Feng Y, Lei Y, Liu M, Xiong X (2015) Effects of N rate on plant growth of autumn potato crop and gene expression of nitrate reductase and ammonium transporter. Acta Horticulturae Sinica 42:1974–1982
Ihemere U, Arias–Garzon D, Lawrence S, Sayre R (2006) Genetic modification of cassava for enhanced starch production. Plant Biotechnol J 4:453–465
Johnson PE, Patron NJ, Bottrill AR, Dinges JR, Fahy BF, Parker ML, Waite DN, Denyer K (2003) A low-starch barley mutant, risø 16, lacking the cytosolic small subunit of ADP-glucose pyrophosphorylase, reveals the importance of the cytosolic isoform and the identity of the plastidial small subunit. Plant Physiol 131:684–696
Kang G, Wang Y, Guo T, Zhu Y, Guan C (2006) Key enzymes in starch synthesis in plants. Hereditas (Beijing) 28:110–116
Li P (2014) Effect of N nutrition on starch accumulation in process of tuber development of autumn Solanum tuberosum L. Southwest China. J Agric Sci 27:2455–2459
Li T, Shen B, Chen N, Luo Y (1997) Effect of Q-enzyme on the chalkiness formation of rice grain. Acta Agron Sin 23:338–344
Liu K, Niu Y, Konishi M, Wu Y, Du H, Chung H, Li L, Boudsocq M, McCormack M, Maekawa S, Ishida T, Zhang C, Shokat K, Yanagisawa S, Sheen J (2017) Discovery of nitrate–CPK–NLP signaling in central nutrient–growth networks. Nature 545:311–333
Long CM, Snapp SS, Douches DS, Chase RW (2004) Tuber yield, storability, and quality of Michigan varieties in response to N management and seed piece spacing. Am J Potato Res 81:347–357
Marshall J, Sidebottom C, Debet M, Martin C, Smith AM, Edwards A (1996) Identification of the major starch synthase in the soluble fraction of potato tubers. Plant Cell 8:1121–1135
Meng G (1985) Study and formulation of national standard for the determination of grain crude starch. Heilongjiang Agri Sci 5:55–57
Muller B, Sonnewald U, Willmitzer L (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 J 11:1229–1238
Nakamura Y, Yuki K, Park SY (1989) Carbohydrate metabolism in the developing endosperm of rice grains. Plant Cell Physiol 56:833–839
Nazarian-Firouzabadia F, Visser RGF (2017) Potato starch synthases: functions and relationships. BB Reports 10:7–16
Nelson O, Pan D (1995) Starch synthesis in maize endosperms. Annu Rev Plant Physiol Plant Mol Biol 46:475–496
Nie X (2009) Study on the tuber quality and plant N status diagnosis of potato under different N levels. MS thesis, Inner Mongolia Agricultural University, China
Satoh H, Nishi A, Yamashita K, Takemoto Y, Tanaka Y, Hosaka Y, Sakurai A, Fujita N, Nakamura Y (2003) Starch-branching enzyme I-deficient mutation specifically affects the structure and properties of starch in rice endosperm. Plant Physiol 133:1111–1121
Schwall GP, Safford R, Westcott RJ, Jeffcoat R, Tayal A, Shi YC, Gidley MJ, Jobling SA (2000) Production of very-high-amylose potato starch by inhibition of SBE A and B. Nature Biotec 18:551–554
Šimková D, Lachman J, Hamouz K, Vokál B (2013) Effect of variety, location and year on total starch, amylose, phosphorus content and starch grain size of high starch potato varieties for food and industrial processing. Food Chem 141:3872–3880
Smith AM (2001) The biosynthesis of starch granules. Biomacromolecules 2:335–341
Stark DM, Timmerman KP, Barry GF, Preiss J, Kishore GM (1992) Regulation of the amount of starch in plant tissues by ADP glucose pyrosphosphorylase. Science 258:287–292
Tetlow IJ, Wait R, Lu Z, Akkasaeng R, Bowsher CG, Esposito S, Kosar-Hashemi B, Morell MK, Emes MJ (2004) Protein phosphorylation in amyloplasts regulates starch branching enzyme activity and protein–protein interactions. Plant Cell 16:694–708
Tiessen A, Hendriks JHM, Stitt M, Branscheid A, Gibon Y, Farré EM, Geigenberger P (2002) Starch synthesis in potato tubers is regulated by post-translational redox modification of ADP-glucose pyrophosphorylase: a novel regulatory mechanism linking starch synthesis to the sucrose supply. Plant Cell 14:2191–2213
Tiessen A, Prescha K, Branscheid A, Palacios N, McKibbin R, Halford NG, Geigenberger P (2003) Evidence that SNF1-related kinase and hexokinase are involved in separate sugar-signalling pathways modulating post-translational redox activation of ADP-glucose pyrophosphorylase in potato tubers. Plant J 35:490–500
Vrinten P, Nakamura T, Yamamori M (1999) Molecular characterization of waxy mutations in wheat. Mol Gen Genet 261:463–471
Zebarth BJ, Rosen CJ (2007) Research perspective on N BMP development for potato. Am J Potato Res 84:3–18
Zebarth BJ, Leclerc Y, Moreau G, Botha E (2004) Rate and timing of N fertilization of Russet Burbank potato: yield and processing quality. Can J Plant Sci 84:855–863
Zebarth BJ, Rochette P, Burton DL (2008) N2O emissions from spring barley production as influenced by fertilizer N rate. Can J Soil Sci 88:197–205
Zhao S, Yang J, Zhou W, Zhang P (2013) Starch biosynthesis and the key enzymes of root and tuber plants. Botanical Res 2:24–33
Zheng S, Wang X, Ma J, Yuan J, Li S (2008) Effects of nutritional level on hormones, yield and quality in the process of tuber formation in potato. Plant Nutr Fertilizer Sci 14:515–519
Acknowledgements
We extend our thanks to Prof. Hui Li and Prof. Yingqiu Du for their help in the methods of starch quality analysis, to Dr. Yingni Cao for her assistance in the enzyme activity assay for starch synthases, to Dr. Haitao Guan and Dr. Hongtao Wen for their help in the methods of fluorescence quantitative PCR and to Ms. Dandan Huo and Mr. Xudong Li for their technical assistance in the field and in the laboratory.
Funding
This study was funded by the National Natural Science Foundation of China (31501358), Collaborative Innovation System of Industry Technology in Modern Agriculture from Heilongjiang Province (HNWJZTX201701) and the Special Foundation for Innovation Capability Enhancement of Research Institutes from Heilongjiang Province (YC2015D003).
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Li, Y., Lu, W., Lyu, D. et al. Effects of Different Nitrogen Application Rates on Starch Accumulation, Starch Synthase Gene Expression and Enzyme Activity in Two Distinctive Potato Cultivars. Potato Res. 61, 309–326 (2018). https://doi.org/10.1007/s11540-018-9379-y
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DOI: https://doi.org/10.1007/s11540-018-9379-y