doi: 10.15389/agrobiology.2018.3.450eng

UDC 635.21:631.522/.524:577.21

Acknowledgments: 
Supported financially by the Complex Research Program for potato breeding and seed production

 

THE USE OF CARBOHYDRATE METABOLISM GENES FOR POTATO (Solanum tuberosum L.) IMPROVEMENT (review)

M.A. Slugina, E.Z. Kochieva

Research Center of Biotechnology RAS, Federal Agency for Scientific Organizations, 33/2, Leninskii prospect, Moscow, 119071 Russia, e-mail mashinmail@mail.ru (✉ corresponding author), ekochieva@yandex.ru

ORCID:
Slugina M.A. orcid.org/0000-0003-1281-3837
Kochieva E.Z. orcid.org/0000-0002-6091-0765

Received February 2, 2018

 

Potato (Solanum tuberosum L.) is one of the most important crop species in the world. Its nutritional and industrial qualities depend on starch content in tubers. Starch consists of linear (amylose) and branched (amylopectin) glucose polymers. Three main goals of modern potato breeding programs include increment of tuber starch yield, development of potato cultivars with improved amylose or amylopectin content and prevention of cold-induced sweetening. Nowadays some molecular and biotechnological approaches to vary plant characteristics have been developed. Among them the most popular are marker-assisted selection, transgenic technologies, genome editing. But, regardless of the chosen approach, the fundamental stage of successful work is the proper choice of the target gene, which in turn requires detailed understanding of the metabolic pathways for the synthesis and degradation of carbohydrates in plant tissues. Starch metabolism includes rather big number of reactions and requires synergetic work of a great number of enzymes. Moreover, it should be mentioned that in starch formation and degradation participate not only carbohydrates modifying proteins, but some regulatory proteins that are also involved in such pathways. Taking into account the previously published review (V.K. Khlestkin et al., 2017), in which attention is paid to genes that determine the specific physical, chemical and technological starch properties, in the present review the emphasis is made on the current understanding of the starch biosynthesis and degradation processes and the key genes of carbohydrate metabolism enzymes in potato tubers. In the present review, among proteins involved in plant carbohydrate metabolism we have chosen those that play the key roles in potato tubers starch formation and retention. The key proteins are sucrose synthases, starch-phosphorilases, granule-bound starch synthase, α- and β-amylases, acid vacuolar invertase, as well as invertase and amylase inhibitors. The main candidate genes that may influence potato agronomical traits are described. The future work requires analysis of allelic polymorphism of the candidate genes in a wide range of potato species, cultivars and lines, looking for associations with desired agronomic traits. It will allow us to use these genes for marker-assisted selection and as target genes for gene editing.

Keywords: potato, starch, amylose, amylopectin, cold-induced sweetening, starch metabolism.

 

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REFERENCES

 

  1. Khestkin V.K., Pel'tek S.E., Kolchanov N.A. Target genes for development of potato (Solanum tuberosum L.) cultivars with desired starch properties (review). Selskokhozyaistvennaya biologiya [Agricultural Biology], 2017, 52(1): 25-36 CrossRef
  2. Li L., Tacke E., Hofferbert H., Lübeck J., Strahwald J., Draffehn A. Validation of candidate gene markers for marker-assisted selection of potato cultivars with improved tuber quality. Theor. Appl. Genet., 2013, 126(4): 1039-1052 CrossRef
  3. Van Harsselaar J., Lorenz J., Senning M., Sonnewald U., Sonnewald  S. Genome-wide analysis of starch metabolism genes in potato (Solanum tuberosum L.) BMC Genomics, 2017, 18: 37 CrossRef
  4. Duarte-Delgado D., Juyó D., Gebhardt C., Sarmiento F., Mosquera-Vásquez T. Novel SNP markers in InvGE and SssI genes are associated with natural variation of sugar contents and frying color in Solanum tuberosum Group Phureja. BMC Genet., 2017, 18: 23 CrossRef
  5. Frommer W., Sonnewald U. Molecular analysis of carbon partitioning in solanaceous species. J. Exp Bot., 1995, 46: 587-607.
  6. Pfister B., Zeeman S.  Formation of starch in plant cells. Cell. Mol. Life Sci., 2016, 73(14): 2781-2807 CrossRef 
  7. Martin C., Smith A. Starch biosynthesis. Plant Cell, 1995, 7(7): 971-985 CrossRef
  8. Bahaji A., Li J., Sánchez-López Á., Baroja-Fernández E., Muñoz F., Ovecka M., Almagro G., Montero M., Ezquer I., Etxeberria E., Pozueta-Romero J. Starch biosynthesis, its regulation and biotechnological approaches to improve crop yields. Biotechnol Adv., 2014, 32(1): 87-106 CrossRef
  9. Zeeman S., Kossmann J., Smith A. Starch: its metabolism, evolution, and biotechnological modification in plants. Annu. Rev. Plant Biol., 2010, 61: 209-234 CrossRef
  10. Naeem M., Tetlow I., Emes M. Starch synthesis in amyloplasts purified from developing potato tubers. The Plant Journal, 1997, 11(5): 1095-1103 CrossRef
  11. Smith A., Zeeman S., Thorneycroft D., Smith S. Starch mobilization in leaves. J. Exp. Bot., 2003, 54(382): 577-583 CrossRef
  12. Smith A., Zeeman S., Smith S. Starch degradation. Annu. Rev. Plant Biol., 2005, 56: 73–98 CrossRef
  13. Zeeman S., Smith S., Smith A. The diurnal metabolism of leaf starch. Biochem. J., 2007, 401(1): 13-28 CrossRef
  14. Orzechowski S. Starch metabolism in leaves. Acta Biochim. Pol., 2008, 55(3): 435-445.
  15. Dauvillée D., Chochois V., Steup M., Haebel S., Eckermann N., Ritte G., Ral J., Colleoni C., Hicks G., Wattebled F. Plastidial phosphorylase is required for normal starch synthesis in Chlamydomonas reinhardtii. Plant J., 2006, 48(2): 274-285 (doi: 10.1111/j.1365-313X.2006.02870.x).
  16. Fettke J., Albrecht T., Hejazi M., Mahlow S., Nakamura Y., Steup M. Glucose 1-phosphate is efficiently taken up by potato (Solanum tuberosum) tuber parenchyma cells and converted to reserve starch granules. New Phytol., 2010, 185(3): 663-675 CrossRef
  17. Yu T., Kofler H., Häusler R., Hille D., Flügge U., Zeeman S., Smith A., Kossmann J., Lloyd J., Ritte G. The Arabidopsis sex1 mutant is defective in the R1 protein, a general regulator of starch degradation in plants, and not in the chloroplast hexose transporter. Plant Cell, 2001, 13(8): 1907-1918 CrossRef
  18. Hejazi M., Fettke J., Haebel S., Edner C., Paris O., Frohberg C., Steup M., Ritte G. Glucan, water dikinase phosphorylates crystalline maltodextrins and thereby initiates solubilization. The Plant Journal, 2008, 55(2): 323-334 CrossRef
  19. Zeeman, S., Smith, S., Smith A. The breakdown of starch in leaves. New Phytol., 2004, 163(2): 247-261 CrossRef
  20. Liu X., Song B., Zhang H., Li X.Q., Xie C., Liu J. Cloning and molecular characterization of putative invertase inhibitor genes and their possible contributions to cold-induced sweetening of potato tubers. Mol. Genet. Genomics, 2010, 284(3): 147-159 CrossRef
  21. 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 Biotechnol. J., 2014, 12(7): 984-993 CrossRef
  22. Clasen B., Stoddard T., Luo S, Demorest Z., Li J., Cedrone F., Tibebu R., Davison S., Ray E., Daulhac A., Coffman A., Yabandith A., Retterath A., Haun W., Baltes N., Mathis L., Voytas D., Zhang F. Improving cold storage and processing traits in potato through targeted gene knockout. Plant Biotechnol. J., 2016, 14(1): 169-176 CrossRef
  23. Kloosterman B., Vorst O., Hall R., Visser R., Bachem C. Tuber on a chip: differential gene expression during potato tuber development. Plant Biotechnol. J., 2005, 3(5): 505-519 CrossRef
  24. Appeldoorn N., de Bruijn S.,  Koot-Gronsveld E., Visser R., Vreugdenhil D., van der Plas L. Developmental changes of enzymes involved in conversion of sucrose to hexose phosphate during early tuberisation of potato. Planta, 1997, 202(2): 220-226 CrossRef
  25. Fu H., Kim S., Park W. High-leve1 tuber expression and sucrose inducibility of a potato Sus4 sucrose synthase gene require 5´ and 3´ flanking sequences and the leader intron. The Plant Cell, 1995, 7(9): 1387-1394. 
  26. Viola R., Roberts G., Haupt S., Gazzani S., Hancock R., Marmiroli N., Machray G., Oparka K. Tuberization in potato involves a switch from apoplastic to symplastic phloem unloading. Plant Cell, 2001, 13(2): 385-398 CrossRef
  27. Zrenner R., Salanoubat M., Willmitzer L., Sonnewald U. Evidence of the crucial role of sucrose synthase for sink strength using transgenic potato plants (Solanum tuberosum L.). The Plant Journal, 1995, 7(1): 97-107 CrossRef
  28. Avigad G. Sucrose and other disaccharides. In: Encyclopedia of plant physiology. T.A. Loewus, W. Tanner (eds.). Springer-Verlag, Heidelberg, 1982.
  29. Koch K. Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr. Opin. Plant Biol., 2004, 7(3): 235-246 CrossRef
  30. Baroja-Fernández E., Muñoz F., Montero M., Etxeberria E., Sesma M., Ovecka M., Bahaji A., Ezquer I., Li J., Prat S., Pozueta-Romero J. Enhancing sucrose synthase activity in transgenic potato (Solanum tuberosum L.) tubers results in increased levels of starch, ADPglucose and UDPglucose and total yield. Plant Cell Physiol., 2009, 50(9): 1651-166 CrossRef
  31. Rathore R., Garg N., Garg S., Kumar A. Starch phosphorylase: role in starch metabolism and biotechnological applications. Crit. Rev. Biotechnol., 2009, 29(3): 214-224 CrossRef
  32. Nighojkar S., Kumar A. Starch phosphorylase: biochemical, molecular and biotechnological aspects. Genet. Eng. Biotechnol., 1997, 17(4): 189-202.
  33. Sonnewald U., Basner A., Greve B., Steup M. A second L-type isozyme of potato glucan phosphorylase: cloning, antisense inhibition and expression analysis. Plant Mol. Biol., 1995, 27(3): 567-576.
  34. Albrecht T., Koch A., Lode A., Greve B., Schneider-Mergener J., Steup M. Plastidic (Pho1-type) phosphorylase isoforms in potato (Solanum tuberosum L.) plants: expression analysis and immunochemical characterization. Planta, 2001, 213(4): 602-613.
  35. Preiss J., Levi C. Starch biosynthesis and degradation. In: The biochemistry of plants. V. 3. J.B. Pridham (ed.). Academic Press, NY, 1980.
  36. Newgard C., Hwang P., Fletterick R. The family of glycogen phosphorylases: structure and function. Crit. Rev. Biochem. Mol. Biol., 1989, 24(1): 69-99 CrossRef
  37. Dai W., Deng W., Cui W., Zhao Y., Wang X. Molecular cloning and sequence of potato granule-bound starch synthase. Acta Botanica Sinica, 1996, 38(10): 777-784.
  38. Satoh H., Shibahara K., Tokunaga T., Nishi A., Tasaki M., Hwang S.K. Mutation of the plastidial a-glucan phosphorylase gene in rice affects the synthesis and structure of starch in the endosperm. Plant Cell, 2008, 20: 1833-1849 CrossRef
  39. Tetlow I., Emes M. A review of starch-branching enzymes and their role in amylopectin biosynthesis. IUBMB Life, 2014, 66(8): 546-558 CrossRef
  40. Liu H., Yu G., Wei B., Wang Y., Zhang J., Hu Y., Liu Y., Yu G., Zhang H., Huang Y. Identification and phylogenetic analysis of a novel starch synthase in maize. Front. Plant Sci., 2015, 6: 1013 CrossRef
  41. Hovenkamp-Hermelink J., Jacobsen E., Ponstein A., Visser R., Vos-Scheperkeuter G., Bijmolt E., de Vries J., Witholt B., Feenstra W. Isolation of an amylose-free starch mutant of the potato (Solanum tuberosum L.). Theor. Appl. Genet., 1987, 75(1): 217-221 CrossRef
  42. Jacobsen E., Hovenkamp-Hermelink J., Krijgsheld H., Nijdam H., Pijnacker L., Witholt B., Feenstra W. Phenotypic and genotypic characterization of an amylose-free starch mutant of the potato. Euphytica, 1989, 44(1-2): 43-48 CrossRef
  43. Visser R., Somhorst I., Kuipers G., Ruys N., Feenstra W., Jacobsen E. Inhibition of the expression of the gene for granule-bound starch synthase in potato by antisense constructs. Mol. Gen. Genet., 1991, 225(2): 285-296.
  44. Van der Steege G., Nieboer M., Swaving J., Tempelaar M. Potato granule-bound starch synthase promoter-controlled GUS expression: regulation of expression after transient and stable transformation. Plant Mol. Biol., 1992, 20(1): 19-30.
  45. Rohde W., Becker D., Kull B., Salamini F. Structural and functional analysis of two waxy gene promoters from potato. Journal of Genetics & Breeding, 1990, 44: 311-315.
  46. Van de Wal M., Jacobsen E., Visser R. Multiple allelism as a control mechanism in metabolic pathways: GBSSI allelic composition affects the activity of granule-bound starch synthase I and starch composition in potato. Mol. Genet. Genomics, 2001, 265(6): 1011-1021 CrossRef
  47. Visser R., Stolte A., Jacobsen E. Expression of a chimaeric granule-bound starch synthase-GUS gene in transgenic potato plants. Plant Mol. Biol., 1991, 17(4): 691-699 CrossRef
  48. Kuipers G., Vreem J., Meyer H., Jacobsen E., Feenstra W., Visser R. Field evaluation of antisense RNA mediated inhibition of GBSS gene expression in potato. Euphytica, 1992, 59(1): 83-91 CrossRef
  49. Flipse E., Keetels C., Jacobson E., Visser R. The dosage effect of the wild type GBSS allele is linear for GBSS activity, but not for amylose content: absence of amylose has a distinct influence on the physico-chemical properties of starch. Theor. Appl. Genet., 1996, 92(1): 21-127 CrossRef
  50. Heilersig B., Loonen A., Janssen E., Wolters A., Visser R. Efficiency of transcriptional gene silencing of GBSSI in potato depends on the promoter region that is used in an inverted repeat. Mol. Genet. Genomics, 2006, 275(5): 437-449 CrossRef
  51. Haworth W., Peat S., Bourne E. Synthesis of amylopectin. Nature, 1944, 154: 236-238 CrossRef
  52. Hizukuri S. Polymodal distribution of the chain lengths of amylopectin, and its significance. Carbohyd. Res., 1986, 147(2): 342-347 CrossRef
  53. Bertoft E., Seetharaman K. Starch structure. In: Starch: origins, structure and metabolism. I.J. Tetlow (ed.). Society for Experimental Biology, London, 2002.
  54. Bhattacharyya M., Smith A., Ellis T., Hedley C., Martin C. The wrinkle-seeded character of peas described by Mendel is caused by a transposon-like insertion in a gene encoding starch branching enzyme. Cell, 1990, 60(1): 115-122 CrossRef
  55. Boyer C., Daniels R., Shannon J. Abnormal starch granule formation in Zea mays L. endosperms possessing the amylose-extender mutant. Crop Sci., 1976, 16: 298-301.
  56. Schwall G., Safford R., Westcott R., Jeffcoat R., Tayal A. Production of very-high-amylose potato starch by inhibition of SBE A and B. Nature Biotechnology, 2000, 18: 551-554 CrossRef
  57. Tareke E., Rydberg P., Karlsson P., Eriksson S., Törnqvist M. Analysis of acrylamide, a carcinogen formed in heated foodstuffs. J. Agric. Food Chem., 2002, 50(17): 4998-5006 CrossRef
  58. Shepherd L., Bradshaw J., Dale M., McNicol J., Pont S., Mottram D., Davies H. Variation in acrylamide producing potential in potato: segregation of the trait in a breeding population. Food Chem., 2010, 123(3): 568-573 CrossRef
  59. 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. J. Exp. Bot., 2017, 68(9): 2317-2331 CrossRef
  60. Xin Z., Browse J. Cold comfort farm: the acclimation of plants to freezing temperatures. Plant, Cell & Environment, 2000, 23(9): 893-902 CrossRef
  61. Mottram D., Wedzicha B., Dodson A. Food chemistry: Acrylamide is formed in the Maillard reaction. Nature, 2002, 419: 448-449 CrossRef
  62. Halford N., Curtis T., Muttucumaru N., Postles J., Elmore J., Mottram D. The acrylamide problem: a plant and agronomic science issue. J. Exp. Bot., 2012, 63(8): 2841-2751 CrossRef
  63. Zhang H., Hou J., Liu J., Xie C., Song B. Amylase analysis in potato starch degradation during cold storage and sprouting. Potato Res., 2014, 57(1): 47-58, CrossRef
  64. Weise S., Kim K., Stewart R., Sharkey T. β-Maltose is the metabolically active anomer of maltose during transitory starch degradation. Plant Physiol., 2005, 137(2): 756-761 CrossRef
  65. Cottrell J., Duffus C., Paterson L., Mackay G., Allison M., Bain H. The effect of storage temperature on reducing sugar concentration and the activities of three amylolytic enzymes in tubers of the cultivated potato, Solanum tuberosum L. Potato Res., 1993, 36(2): 107-117 CrossRef
  66. Wiberley-Bradford A., Busse J., Bethke P. Temperature-dependent regulation of sugar metabolism in wild-type and low-invertase transgenic chipping potatoes during and after cooling for low-temperature storage. Postharvest Biol. Tec., 2016, 115: 60-71 CrossRef
  67. Bhaskar P., Wu L., Busse J., Whitty B., Hamernik A., Jansky S., Buell C., Bethke P.,  Jiang J. Suppression of the vacuolar invertase gene prevents cold-induced sweetening in potato. Plant Physiol., 2010, 154(2): 939-948 CrossRef
  68. Ye J., Shakya R., Shrestha P., Rommens C. Tuber-specific silencing of the acid invertase gene substantially lowers the acrylamide-forming potential of potato. J. Agric. Food Chem., 2010, 58(23): 12162-12167 CrossRef
  69. Liu X., Zhang C., Ou Y., Lin Y., Song B., Xie C., Liu J., Li X.Q. Systematic analysis of potato acid invertase genes reveals that a cold-responsive member, StvacINV1, regulates cold-induced sweetening of tubers. Mol. Genet. Genomics, 2011, 286(2): 109-118 CrossRef
  70. Wu L., Bhaskar P., Busse J., Zhang R., Bethke P., Jiang J. Developing cold-chipping potato varieties by silencing the vacuolar invertase gene. Crop Sci., 2011, 51(3): 981-990 CrossRef
  71. Draffehn A., Meller S., Li L., Gebhardt C. Natural diversity of potato (Solanum tuberosum) invertases. BMC Plant Biol., 2010, 10(1): 271 CrossRef
  72. Slugina M., Snigir E., Ryzhova N., Kochieva E. Structure and polymorphism of a fragment of the Pain-1 vacuolar invertase locus in Solanum species. Mol. Biol. (Russia), 2013, 7(2): 215-221 CrossRef
  73. Slugina M.A., Khrapalova I.A., Ryzhova N.N., Kochieva E.Z., Skryabin K.G. Doklady Akademii nauk, 2014, 454(1): 100 CrossRef (in Russ.).
  74. Slugina M., Shchennikova A., Kochieva E. TAI vacuolar invertase orthologs: the interspecific variability in tomato plants (Solanum section Lycopersicon). Mol. Genet. Genomics, 2017, 292(5): 1123-1138 CrossRef
  75. Rausch T., Greiner S. Plant protein inhibitors of invertases. Biochim. Biophys. Acta, 2004, 1696(2): 253-261 CrossRef
  76. Brummell D., Chen R.K.Y., Harris J.C., Zhang H., Hamiaux C., Kralicek A.V., McKenzie M.J. Induction of vacuolar invertase inhibitor mRNA in potato tubers contributes to cold-induced sweetening resistance and includes spliced hybrid mRNA variants. J. Exp. Bot., 2011, 62(10): 3519-3534 CrossRef 
  77. Glaczinski H., Heibges A., Salamini R., Gebhardt C. Members of the Kunitz-type protease inhibitor gene family of potato inhibit soluble tuber invertase in vitro. Potato Res., 2002, 45(2-4): 163-176 CrossRef
  78. Liu X., Cheng S., Liu J., Ou Y., Song B., Zhang C., Lin Y., Li X., Xie C. The potato protease inhibitor gene, St-Inh, plays roles in the cold-induced sweetening of potato tubers by modulating invertase activity. Postharvest Biol. Tec., 2013, 86: 265-271 CrossRef
  79. Liu Q., Guo Q., Akbar S., Zhi Y., El Tahchy A., Mitchell M., Li Z., Shrestha P., Vanhercke T., Ral J.P., Liang G., Wang M.B., White R., Larkin P., Singh S., Petrie J. Genetic enhancement of oil content in potato tuber (Solanum tuberosum L.) through an integrated metabolic engineering strategy. Plant Biotechnol. J., 2017, 15(1): 56-67 CrossRef

 

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