Tuber-specific silencing of asparagine synthetase-1 reduces the acrylamide-forming potential of potatoes grown in the field without affecting tuber shape and yield

Plant Biotechnology Journal

Volumn 10, Issue 8, 2012, Pages 913-924

  Chawla, Rekha ^a   Shakya, Roshani ^a   Rommens, Caius M ^a  

^a J R SIMPLOT COMPANY   (United States)

Author keywords

Acrylamide; Asparagine synthetase; Metabolic engineering; Potato; Tubers

Indexed keywords

ACRYLAMIDE; ASPARAGINE; ASPARTATE AMMONIA LIGASE;

ARTICLE; CHEMISTRY; DOWN REGULATION; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC ENGINEERING; GENETICS; HISTOLOGY; METABOLISM; PHENOTYPE; PLANT GENE; PLANT TUBER; POTATO; TRANSGENIC PLANT;

ACRYLAMIDE; ASPARAGINE; ASPARTATE-AMMONIA LIGASE; DOWN-REGULATION; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; GENES, PLANT; GENETIC ENGINEERING; PHENOTYPE; PLANT TUBERS; PLANTS, GENETICALLY MODIFIED; SOLANUM TUBEROSUM;

SOLANUM TUBEROSUM;

EID: 84865744675     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/j.1467-7652.2012.00720.x     Document Type: Article

References (53)

1. Andrews, M.C. (1986) The partitioning of nitrate assimilation between the root and shoot of higher plants. Plant, Cell Environ. 9, 511-519.
2. Atkins, C.A., Pate, J.S. and Sharkey, P.J. (1975) Asparagine metabolism-key to the nitrogen nutrition of developing legume seeds. Plant Physiol. 56, 807-12.
3. Barker, A.V. (1999a) Ammonium accumulation and ethylene evolution by tomato infected with root-knot nematode and grown under different regimes of plant nutrition. Commun. Soil Sci. Plant Anal. 30, 175-182.
4. Barker, A.V. (1999b) Foliar ammonium accumulation as an index of stress in plants. Commun. Soil Sci. Plant Anal. 30, 167-174.
5. Boettcher, M.I., Schettgen, T., Kütting, B., Pischetsrieder, M. and Angerer, J. (2005) Mercapturic acids of acrylamide and glycidamide as biomarkers of the internal exposure to acrylamide in the general population. Mutat. Res. 580, 167-176.
6. + toxicity in higher plants: a critical review. J. Plant Physiol. 159, 567-584.
7. Canas, R.A., Quillere, I., Lea, P.J. and Hirel, B. (2010) Analysis of amino acid metabolism in the ear of maize mutants deficient in two cytosolic glutamine synthetase isozymes highlights the importance of asparagine for nitrogen translocation within sink organs. Plant Biotech. J. 8, 966-978.
8. Cao, W. and Tibbits, T.W. (1998) Response of potatoes to nitrogen concentrations differ with nitrogen forms. J. Plant Nutr. 21, 615-623.
9. Clayber, C.D. (1975) Insect resistance in a graft-induced periclinal chimera of tomato. HortScience, 10, 13-15.
10. Davies, A.M.C. (1977) The free amino acids of tubers of potato varieties grown in England and Ireland. Potato Res. 20, 9-21.
11. Duff, S.M.G., Qi, Q., Reich, T., Wu, X., Brown, T., Crowley, J.H. and Fabbri, B. (2011) A kinetic comparison of asparagine synthetase isozymes from higher plants. Plant Phys. Biochem. 49, 251-256.
12. Dybing, E., Farmer, P.B., Andersen, M., Fennell, T.R., Lalljie, S.P., Müller, D.J., Olin, S., Petersen, B.J., Schlatter, J., Scholz, G., Scimeca, J.A., Slimani, N., Törnqvist, M., Tuijtelaars, S. and Verger, P. (2005) Human exposure and internal dose assessments of acrylamide in food. Food Chem. Toxicol. 43, 365-410.
13. Garbarino, J.E. and Belknap, W.R. (1994) Isolation of a ubiquitin ribosomal protein gene (ubi3) from potato and expression of its promoter in transgenic plants. Plant Mol. Biol. 24, 119-127.
14. Garbarino, J.E., Oosumi, T. and Belknap, W.R. (1995) Isolation of a polyubiquitin promoter and its expression in transgenic potato plants. Plant Physiol. 109, 1371-1378.
15. Gaufichon, L., Reisdorf-Cren, M., Rothstein, S.J., Chardon, F. and Suzuki, A. (2010) Biological functions of asparagine synthetase in plants. Plant Sci. 179, 141-153.
16. Golan-Goldhirsh, A. (1986) Effect of the add-back process on the free amino acid pool of potatoes. Z. Lebensm. Unters. Forsch. 182, 29-32.
17. Golmirzaie, A.M., Bretschneider, K. and Ortiz, R. (1998) Inbreeding and true seed in tetrasomic potato. II. Selfing and sib-mating in heterogeneous hybrid populations of Solanum tuberosum. Theor. Appl. Genet. 97, 1129-1132.
18. Herrera-Rodríguez, M.B., Carrasco-Ballesteros, S., Maldonado, J.M., Pineda, M., Aguilar, M. and Pérez -Vicente, R. (2002) Three genes showing distinct regulatory patterns encode the asparagine synthetase of sunflower (Helianthus annuus). New Phytol. 155, 33-45.
19. Herrera-Rodríguez, M.B., Pérez-Vicente, R. and Maldonado, J.M. (2007) Expression of asparagine synthetase genes in sunflower (Helianthus annuus) under various environmental stresses. Plant Physiol. Biochem. 45, 33-38.
20. Hochmuth, G.J., Hutchinson, C.M., Maynard, D.N., Stall, W.M., Kucharek, T.A., Webb, S.E., Taylor, T.G., Smith, S.A. and Simonne, E.H. (2001) Potato production in Florida. In Vegetable Production Guide for Florida (Maynard, D.N. and Olson, S.M., eds), pp. 223-230. Vance Publishing, Lincolnshire.
21. Hörteinsteiner, S. and Feller, U. (2002) Nitrogen metabolism and remobilization during senescence. J. Exp. Bot. 53, 927-937.
22. Ireland, R.J. and Lea, P.J. (1999) The enzymes of glutamine, glutamate, asparagine, and aspartate metabolism. In Plant Amino Acids: Biochemistry and Biotechnology (Singh, B.K., ed.), pp. 49-109. New York: Marcel Dekker.
23. Jefferies, R.A. and Mackerron, D.K.L. (1987) Observations on the incidence of tuber growth cracking in relation to weather patterns. Potato Res. 30, 613-623.
24. Kanamori, T. and Matsumoto, H. (1974) Asparagine biosynthesis by Oryza sativa seedlings. Phytochemistry, 13, 1407-1412.
25. Karley, A.J., Douglas, A.E. and Parker, W.E. (2002) Amino acid composition and nutritional quality of potato leaf phloem sap for aphids. J. Exp. Biol. 205, 3009-3018.
26. Koch, W., Kwart, M., Laubner, M., Heineke, D., Stransky, H., Frommer, W.B. and Tegeder, M. (2003) Reduced amino acid content in transgenic potato tubers due to antisense inhibition of the leaf H+/amino acid symporter StAAP1. Plant J. 33, 211-220.
27. Lam, H.-M., Hsieh, M.-H. and Coruzzi, G. (1998) Reciprocal regulation of distinct asparagine synthetase genes by light and metabolites in Arabidopsis thaliana. Plant J. 16, 345-353.
28. Lam, H.-M., Wong, P., Chan, H.K., Yam, K.M., Chen, L., Chow, C.M. and Coruzzi, G.M. (2003) Overexpression of the ASN1 gene enhances nitrogen status in seeds of Arabidopsis. Plant Physiol. 132, 926-935.
29. Lea, P.J., Sodek, L., Parry, M.A.J., Shewry, P.R. and Halford, N.G. (2007) Asparagine in plants. Ann. Appl. Biol. 150, 1-26.
30. Lehmann, T. and Ratajczak, L. (2008) The pivotal role of glutamine dehydrogenase (GDH) in the mobilization of N and C from storage material to asparagine in germinating seeds of yellow lupine. J. Plant Physiol. 165, 149-158.
31. Lisinska, G. and Leszczynski, W. (1989) Potato Science and Technology. Chapter 2: Potato Tubers as a Raw Material for Processing and Nutrition. London: Elsevier Applied Science, pp. 11-128.
32. Lohaus, G., Büker, M., Hubmann, M., Soave, C. and Heldt, H.W. (1998) Transport of amino acids with special emphasis on the synthesis and transport of asparagine in the Illinois Low Protein and Illinois High Protein strains of maize. Planta, 205, 181-188.
33. Marcotrigiano, M. and Gouin, F.R. (1984) Experimentally synthesized plant chimera 2. A comparison of in vitro and in vivo techniques for the production of interspecific Nicotiana chimeras. Ann. Bot. 54, 513-521.
34. Martin, A., Lee, J., Kichey, T., Gerentes, D., Zivy, M., Tatout, C., Dubois, F., Balliau, T., Valot, B., Davanture, M., Tercé-Laforgue, T., Quilleré, I., Coque, M., Gallais, A., Gonzalez-Moro, M., Bethencourt, L., Habash, D.Z., Lea, P.J., Charcosset, A., Perez, P., Murigneux, A., Sakakibara, H., Edwards, K.J. and Hirel, B. (2006) Two cytosolic glutamine synthetase isoforms of maize are specifically involved in the control of grain production. Plant Cell, 18, 3252-3274.
35. Masclaux-Daubresse, C., Reisdorf-Cren, M., Pageau, K., Lelandais, M., Grandjean, O., Kronenberger, J., Valadier, M.H., Feraud, M., Jouglet, T. and Suzuki, A. (2006) Glutamine synthetase-glutamate synthase pathway and glutamate dehydrogenase play distinct roles in the sink-source nitrogen cycle in tobacco. Plant Physiol. 140, 444-456.
36. Muller-Rober, B., La Cognata, U., Sonnewald, U. and Willmitzer, L. (1994) A truncated version of an ADP-glucose pyrophosphorylase promoter from potato specifies guard cell-selective expression in transgenic plants. Plant Cell, 6, 601-612.
37. Oaks, A. (1992) A re-evaluation of nitrogen assimilation in roots. Bioscience, 42, 103-110.
38. Parzefall, W. (2008) Minireview on the toxicity of dietary acrylamide. Food Chem. Toxicol. 46, 1360-1364.
39. Richael, C.M., Kalyaeva, M., Chretien, R.C., Yan, H., Adimulam, S., Stivison, A., Weeks, J.T. and Rommens, C.M. (2008) Cytokinin vectors mediate marker-free and backbone-free plant transformation. Transgenic Res. 5, 905-917.
40. Rommens, C.M., Humara, J.M., Ye, J., Yan, H., Richael, C., Zhang, L., Perry, R. and Swords, K. (2004) Crop improvement through modification of the plant's own genome. Plant Physiol. 135, 421-431.
41. Rommens, C.M., Bougri, O., Yan, H., Humara, J.M., Owen, J., Swords, K. and Ye, J. (2005) Plant-derived transfer DNAs. Plant Physiol. 139, 1338-1349.
42. Rommens, C.M., Yan, H., Swords, K., Richael, C. and Ye, J. (2008) Low-acrylamide French fries and potato chips. Plant Biotech. J. 6, 843-853.
43. Seebauer, J.R., Moose, S.P., Fabbri, B.J., Crossland, L.D. and Below, F.E. (2004) Amino acid metabolism in maize earshoots. Implications for assimilate preconditioning and nitrogen signaling. Plant Physiol. 136, 4326-4334.
44. Stadler, R.H. (2005) Acrylamide formation in different foods and potential strategies for reduction. Adv. Exp. Med. Biol. 561, 157-169.
45. N analysis. Anal. Biochem. 154, 564-569.
46. Tardiff, R.G., Gargas, M.L., Kirman, C.R., Carson, M.L. and Sweeney, L.M. (2010) Estimation of safe dietary intake levels of acrylamide for humans. Food Chem. Toxicol. 48, 658-667.
47. Tareke, E., Rydberg, P., Karlsson, P., Eriksson, S. and Törnqvist, M. (2002) Analysis of acrylamide, a carcinogen formed in heated foodstuffs. J. Agric. Food Chem. 50, 4998-5006.
48. Taylor, L., Nunes-Nesi, A., Parsley, K., Leiss, A., Leach, G., Coates, S., Wingler, A., Fernie, A. and Hibberd, J.M. (2010) Cytosolic pyruvate, orthophosphate dikinase functions in nitrogen remobilization during leaf senescence and limits individual seed growth and nitrogen content. Plant J. 62, 641-652.
49. Tsai, F.Y. and Coruzzi, G.M. (1991) Light represses transcription of asparagine synthetase genes in photosynthetic and non-photosynthetic organs of plants. Mol. Cell. Biol. 11, 4966-4972.
50. Visser, R.G., Stolte, A. and Jacobsen, E. (1991) Expression of a chimaeric granule-bound starch synthase-GUS gene in transgenic potato plants. Plant Mol. Biol. 17, 691-699.
51. Weiner, H., Blechschmidt-Schneider, S., Mohme, H., Eschrich, W. and Heldt, H.W. (1991) Phloem transport of amino acids. Comparison of amino acid contents of maize leaves and of the sieve tube exudates. Plant Physiol. Biochem. 29, 19-23.
52. Wong, H.K., Chan, H.K., Coruzzi, G.M. and Lam, H.M. (2004) Correlation of ASN2 gene expression with ammonium metabolism in Arabidopsis. Plant Physiol. 134, 332-338.
53. Xin, Z., Velten, J.P., Oliver, M.J. and Burke, J.J. (2003) High-throughput DNA extraction method suitable for PCR. Biotechniques, 34, 820-824.