PLANT BIOLOGY
ANIMAL BIOLOGY
SUBSCRIPTION
E-SUBSCRIPTION
 
MAP
MAIN PAGE

 

 

 

 

doi: 10.15389/agrobiology.2021.5.899eng

UDC: 635.21/.24:575.15:577.2

Acknowledgments:
Supported financially from the Federal Program for the Development of Agriculture of the Russian Federation for 2017-2025 (subprogram “Development of potato breeding and seed production in the Russian Federation”).

 

EXPRESSION OF THE α-AMYLASE GENE StAmy23 IN PHOTOSYNTHETIC AND NON-PHOTOSYNTHETIC TISSUES OF POTATO (Solanum tuberosum L.) CULTIVARS

A.V. Kulakova1 , A.A. Meleshin2, A.V. Shchennikova1, E.Z. Kochieva1

1Institute of Bioengineering, Federal Research Center Fundamentals of Biotechnology RAS, 33/2, Leninskii prospect, Moscow, 119071 Russia, e-mail kulakova_97@mail.ru (✉ corresponding author), shchennikova@yandex.ru, ekochieva@yandex.ru;
2Lorkha Russian Potato Research Centre, 23-B, ul. Lorkha, pos. Korenevo, Lyuberetsky District, Moscow Province, 140051 Russia, e-mail a-mela@mail.ru

ORCID:
Kulakova A.V. orcid.org/0000-0002-3124-525X
Shchennikova A.V. orcid.org/0000-0003-4692-3727
Meleshin A.A. orcid.org/0000-0002-6018-3676
Kochieva E.Z. orcid.org/0000-0002-6091-0765

Received June 26, 2021

 

Potato (Solanum tuberosum L.) is the fourth most important agricultural crop after cereals. Almost every tissue of a potato plant contains starch, the regulation of metabolism and the physiological role of which depends on the type of tissue, the stage of plant development and external factors. Starch hydrolysis is catalyzed by α- (AMY) and β- (BAM) amylases. By degradation of cytosolic phytoglycogen, StAmy23 amylase regulates tuber cold-induced sweetening and physiological dormancy. Few available studies on StAmy23 have focused on gene activity in potato tubers, including in response to cold stress. In this study, StAmy23 expression pattern in photosynthetic and non-photosynthetic tissues of potato plants of three cultivars, differing in starch content in tubers, was determined for the first time. Structural and phylogenetic analyses revealed that the closest homologs of StAmy23 are the α-amylases of various potato and tomato cultivars. Analysis of the carbohydrate content in freshly harvested tubers of the studied potato cultivars showed a similar high starch content for cv. Gala and cv. Saturna and almost 2 times lower for cv. Barin (6.3 vs.11.34 mg/g of tissue). The largest amount of reducing sugars was found in tubers of cv. Saturna; cv. Gala tubers contained 4.5 and 24.5 times less of glucose/fructose than cv. Barin and cv. Saturna tubers, respectively (0.016/0.000 vs. 0.056/0.016 and 0.217/0.175 mg/g of tissue). For the first time, the expression profile of StAmy23 was determined not only in tubers, leaves and stems, but also in other organs and tissues of the potato plant. A high level of gene expression in stems and fruits was shown. In non-photosynthetic roots and stolons, StAmy23 transcription level either corresponded (cv. Saturna) or significantly exceeded (cv. Barin, cv. Gala) that in tubers. In stems, the highest and lowest StAmy23 transcription levels were observed in cv. Gala and cv. Saturna, respectively (0.58 and 0.13). Leaves and tuber peels showed similar, relatively low levels of StAmy23 expression. In fruits, the highest StAmy23 expression was found in cv. Barin (0.29), in the roots and tubers — in cv. Gala (0.55 and 0.17), and in the stolons — in cv. Barin and cv. Gala (0.31 and 0.33). A positive association was proposed between the level of StAmy23 transcription and the starch content (but not the content of reducing sugars) in tubers. The transcriptional activity of the StAmy23 gene in photosynthetic tissues of potato plants suggests the participation of encoded α-amylase in starch hydrolysis not only in storage organs, but also in vegetative organs to maintain physiological growth processes and plant stress response.

Keywords: Solanum tuberosum, potato, α-amylase StAmy23, starch content, reducing sugars, gene expression.

 

REFERENCES

  1. Sonnewald S., Sonnewald U. Regulation of potato tuber sprouting. Planta, 2014, 239(1): 27-38 CrossRef
  2. 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 Physiology and Biochemistry, 2019, 139: 411-418 CrossRef
  3. Shepherd L.V.T., Bradshaw J.E., Dale M.F.B., McNicol J.W., Pont S.D.A., Mottram D.S., Davies H.V. Variation in acrylamide producing potential in potato: segregation of the trait in a breeding population. Food Chemistry, 2010, 123(3): 568-573 CrossRef
  4. Hou J., Zhang H., Liu J., Reid S., Liu T., Xu S., Tian Z., Sonnewald U., Song B., Xie C. Amylases StAmy23, StBAM1 and StBAM9 regulate cold-induced sweetening of potato tubers in distinct ways. Journal of Experimental Botany, 2017, 68(9): 2317-2331 CrossRef
  5. Hedhly A., Vogler H., Schmid M.W., Pazmino D., Gagliardini V., Santelia D., Grossniklaus U. Starch turnover and metabolism during flower and early embryo development. Plant Physiology, 2016, 172 (4): 2388-2402 CrossRef
  6. Tang L.Y., Nagata N., Matsushima R., Chen Y.L., Yoshioka Y., Sakamoto W. Visualization of Plastids in pollen grains: involvement of FtsZ1in pollen plastid division. Plant Cell Physiology, 2009, 50(4): 904-908 CrossRef
  7. Dong S., Beckles D.M. Dynamic changes in the starch-sugar interconversion within plant source and sink tissues promote a better abiotic stress response. Journal of Plant Physiology, 2019, 234-235: 80-93 CrossRef
  8. Zeeman S.C., Tiessen A., Pilling E., Kato K.L., Donald A.M., Smith A.M. Starch synthesis in arabidopsis. Granule synthesis, composition, and structure. Plant Physiology, 2002, 129(2): 516-529 CrossRef
  9. Zeeman S.C., Smith M.C., Smith A.M. The diurnal metabolism of leaf starch. The Biochemical Journal, 2007, 401(1): 13-28 CrossRef
  10. Benkeblia N., Alexopoulos A.A., Passam H.C. Physiology and biochemistry regulation of dormancy and sprouting in potato tuber (Solanum tuberosum L.). Fruit, Vegetable and Cereal Science and Biotechnology, 2008, 2: 54-68.
  11. Thalmann M., Santelia D. Starch as a determinant of plant fitness under abiotic stress. The New Phytologist, 2017, 214(3): 943-951 CrossRef
  12. MacNeill G.J., Mehrpouyan S., Minow M.A., Patterson J.A., Tetlow I.J., Emes M.J. Starch as a source, starch as a sink: the bifunctional role of starch in carbon allocation. Journal of Experimental Botany, 2017, 68(16): 4433-4453 CrossRef
  13. Preiss J. Regulation of the biosynthesis and degradation of starch. Annual Reviews of Plant Physiology, 1982, 33: 431-454.
  14. Solomos T., Mattoo A.K. Starch-sugar metabolism in potato (Solanum tuberosum) tubers in response to temperature variations. In: Genetic improvement of Solanaceous crops.Vol. I. M.K. Razdan, A.K. Mattoo (eds.). Science Publishers, Enfield, NH, United States, 2005: 209-234.
  15. Asatsuma S., Sawada C., Itoh K., Okito M., Kitajima A., Mitsui T. Involvement of α-amylase I-1 in starch degradation in rice chloroplasts. Plant & Cell Physiology, 2005, 46(6): 858-869 CrossRef
  16. Kitajima A., Asatsuma S., Okada H., Hamada Y., Kaneko K., Nanjo Y., Kawagoe Y., Toyooka K., Matsuoka K., Takeuchi M., Nakano A., Mitsui T. The rice α-amylase glycoprotein is targeted from the Golgi apparatus through the secretory pathway to the plastids. The Plant Cell, 2009, 21(9): 2844-2858 CrossRef
  17. Yu T.S., Zeeman S.C., Thorneycroft D., Fulton D.C., Dunstan H., Lue W-L.,  Hegemann B., Tung S-Y., Umemoto T., Chapple A., Tsai D-L., Wang  S-M.,  Smith A.M., Chen J., Smith S.M. α-Amylase is not required for breakdown of transitory starch in Arabidopsis leaves. The Journal of Biological Chemistry,2005, 280(11): 9773-9779 CrossRef
  18. Glaring M.A., Baumann M.J., Abou H.M, Nakai N., Nakai H., Santelia D., Sigurskjold B.W., Zeeman S.C., Blennow A., Svensson B. Starchbinding domains in the CBM45 family — low-affinity domains from glucan, water dikinase and α-amylase involved in plastidial starch metabolism. The FEBS Journal, 2011, 278(7): 1175-1185 CrossRef      
  19. Van Harsselaar J.K., Lorenz J., Senning M., Sonnewald U., Sonnewald S. Genome-wide analysis of starch metabolism genes in potato (Solanum tuberosum L.). BMC Genomics, 2017, 18(1): 37 CrossRef
  20. Zhang H., Hou J., Liu J., Xie C., Song B. Amylase analysis in potato starch degradation during cold storage and sprouting. Potato Research, 2014, 57: 47-58 CrossRef
  21. Wegrzyn T., Reilly K., Cipriani G., Murphy P., Newcomb R., Gardner R., MacRae E. A novel α-amylase gene is transiently upregulated during low temperature exposure in apple fruit. European Journal of Biochemistry, 2000, 267(5): 1313-1322 CrossRef
  22. Lopez-Pardo R., de Galarreta J.I.R., Ritter E. Selection of housekeeping genes for qRT-PCR analysis in potato tubers under cold stress. Molecular Breeding, 2013, 31(1): 39-45 CrossRef
  23. Tang X., Zhang N., Si H., Calderón-Urrea A. Selection and validation of reference genes for RT-qPCR analysis in potato under abiotic stress. Plant Methods, 2017, 13: 85 CrossRef
  24. Slugina M.A., Shchennikova A.V., Kochieva E.Z. The expression pattern of the Pho1a genes encoding plastidic starch phosphorylase correlates with the degradation of starch during fruit ripening in green-fruited and red-fruited tomato species. Functional Plant Biology, 2019, 46(12): 1146-1157 CrossRef
  25. Slugina M.A., Filyushin M.A., Meleshin A.A., Shchennikova A.V., Kochieva E.Z. Genetika, 2020, 56(3): 361-365 CrossRef (in Russ.).
  26. Liu X., Cheng S., Liu J., Oua Y., Song B., Zhang C., Lin Y., Li X.-Q., Xie C. The potato protease inhibitor gene, St-Inh, plays roles in the cold-induced sweetening of potato tubers by modulating invertase activity. Postharvest Biology and Technology, 2013, 86: 265-271 CrossRef
  27. Mckenzie M.J., Chen R.K., Harris J.C., Ashworth M.J., Brummell D.A. Post-translational regulation of acid invertase activity by vacuolar invertase inhibitor affects resistance to cold-induced sweetening of potato tubers. Plant, Cell & Environment, 2013, 36(1): 176-185 CrossRef
  28. Zhang H., Liu J., Hou J., Yao Y., Lin Y., Ou Y., Song B., Xie C. The potato amylase inhibitor gene SbAI regulates cold-induced sweetening in potato tubers by modulating amylase activity. Plant Biotechnology Journal, 2014, 12(7): 984-993 CrossRef
  29. Slugina M.A., Shchennikova A.V., Kochieva E.Z. TAI vacuolar invertase orthologs: the interspecific variability in tomato plants (Solanum section Lycopersicon). Molecular Genetics and Genomics, 2017, 292(5): 1123-1138 CrossRef
  30. Peyrot des Gachons C., Breslin P.A. Salivary amylase: digestion and metabolic syndrome. Current Diabetes Reports, 2016, 16(10): 102 CrossRef
  31. Braun D.M., Wang L., Ruan Y.L. Understanding and manipulating sucrose phloem loading, unloading, metabolism, and signalling to enhance crop yield and food security. Journal of Experimental Botany, 2014, 65(7): 1713-1735 CrossRef
  32. Slugina M.A., Shchennikova A.V., Meleshin A.A., Kochieva E.Z. Homologs of vacuolar invertase inhibitor INH2 in tuber-bearing wild potato species and Solanum tuberosum: gene polymorphism and co-expression with saccharolytic enzyme genes in response to cold stress. Scientia Horticulturae, 2020, 269: 109425 CrossRef
  33. Slugina M.A., Shchennikova A.V., Kochieva, E.Z. Differences in the sucrose synthase gene SUS1 expression pattern between Solanum lycopersicum and wild tomato species. Theoretical and Experimental Plant Physiology, 2019, 31: 455-462 CrossRef
  34. Cook F.R., Fahy B., Trafford K. A rice mutant lacking a large subunit of ADP-glucose pyrophosphorylase has drastically reduced starch content in the culm but normal plant morphology and yield. Functional Plant Biology, 2012, 39(12): 1068-1078 CrossRef
  35. Okamura M., Hirose T., Hashida Y., Ohsugi R., Aoki N. Suppression of starch synthesis in rice stems splays tiller angle due to gravitropic insensitivity but does not affect yield. Functional Plant Biology, 2015, 42(1): 31-41 CrossRef
  36. Graf A., Smith A.M. Starch and the clock: the dark side of plant productivity. Trends in Plant Science, 2011, 16(3): 169-175 CrossRef
  37. Sulpice R., Pyl E.T., Ishihara H., Trenkamp S., Steinfath M., Witucka-Wall H., Gibon Y., Usadel B., Poree F., Piques M.C., Von Korff M., Steinhauser M.C., Keurentjes J.J.B., Guenther M., Hoehne M., Selbig J., Fernie A.R., Altmann T., Stitt M. Starch as a major integrator in the regulation of plant growth. Proceedings of the National Academy of Sciences of the United States of America, 2009, 106(25): 10348-10353 CrossRef

 

back