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
Frederick R. Cook A , Brendan Fahy A and Kay Trafford A B C
+ Author Affiliations
- Author Affiliations
A John Innes Centre, Norwich Research Park, Norfolk, NR4 7UH, UK.
B Present address: National Institute of Agricultural Botany, Huntingdon Road, Cambridge, CB3 0 LE, UK.
C Corresponding author. Email: kay.trafford@niab.com
Functional Plant Biology 39(12) 1068-1078 https://doi.org/10.1071/FP12186
Submitted: 26 June 2012 Accepted: 3 September 2012 Published: 23 October 2012
Abstract
A mutant of rice (Oryza sativa L.) was identified with a Tos17 insertion in Os05g50380, a gene encoding a plastidial large subunit (LSU) of ADP-glucose pyrophosphorylase (AGPase) that was previously called OsAPL3 or OsAGPL1. The insertion prevents the production of a normal transcript. Characterisation of the mutant showed that this LSU is required for 97% of the starch synthesised in the flowering stem (culm), approximately half of the AGPase activity in developing embryos and that it contributes to AGPase activity in the endosperm. Despite the near absence of starch in the culms and reduced starch content in the embryos, the mutant rice plants grow and develop normally, and show no reduction in productivity. The starch content of leaves is increased in the mutant, revealing plasticity in the distribution of photosynthates among different temporary carbohydrate storage pools within the plant.
Additional keywords: carbohydrate, flowering stem, Tos17.
References
Akihiro T, Mizuno K, Fujimura T (2005) Gene expression of ADP-glucose pyrophosphorylase and starch contents in rice cultured cells are cooperatively regulated by sucrose and ABA. Plant & Cell Physiology 46, 937–946.| Gene expression of ADP-glucose pyrophosphorylase and starch contents in rice cultured cells are cooperatively regulated by sucrose and ABA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlslCht74%3D&md5=154958f7dd0440d5cdcd1b7bc7bb78acCAS |
Andriotis VM, Pike MJ, Kular B, Rawsthorne S, Smith AM (2010) Starch turnover in developing oilseed embryos. New Phytologist 187, 791–804.
| Starch turnover in developing oilseed embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFSmu7jL&md5=3f5d336572609d94d9203a7962b7db90CAS |
Ballicora MA, Laughlin MJ, Fu Y, Okita TW, Barry GF, Preiss J (1995) Adenosine 5′-diphosphate-glucose pyrophosphorylase from potato tuber (significance of the N terminus of the small subunit for catalytic properties and heat stability). Plant Physiology 109, 245–251.
| Adenosine 5′-diphosphate-glucose pyrophosphorylase from potato tuber (significance of the N terminus of the small subunit for catalytic properties and heat stability).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXotFWmsLY%3D&md5=1b1c9965018861225dc92a8a1cc6d80bCAS |
Blum A (1998) Improving wheat grain filling under stress by stem reserve mobilisation. Euphytica 100, 77–83.
| Improving wheat grain filling under stress by stem reserve mobilisation.Crossref | GoogleScholarGoogle Scholar |
Burton RA, Jenner H, Carrangis L, Fahy B, Fincher GB, Hylton C, Laurie DA, Parker M, Waite D, van Wegen S, Verhoeven T, Denyer K (2002a) Starch granule initiation and growth are altered in barley mutants that lack isoamylase activity. The Plant Journal 31, 97–112.
| Starch granule initiation and growth are altered in barley mutants that lack isoamylase activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmsVWrs70%3D&md5=e31950911fd0e2f07b07b403841cab7bCAS |
Burton RA, Johnson PE, Beckles DM, Fincher GB, Jenner HL, Naldrett MJ, Denyer K (2002b) Characterization of the genes encoding the cytosolic and plastidial forms of ADP-glucose pyrophosphorylase in wheat endosperm. Plant Physiology 130, 1464–1475.
| Characterization of the genes encoding the cytosolic and plastidial forms of ADP-glucose pyrophosphorylase in wheat endosperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovVOmsLc%3D&md5=28311147bded216315a3740e8447d052CAS |
Chen C, Gao M, Liu J, Zhu H (2007) Fungal symbiosis in rice requires an ortholog of a legume common symbiosis gene encoding a Ca2+/calmodulin-dependent protein kinase. Plant Physiology 145, 1619–1628.
| Fungal symbiosis in rice requires an ortholog of a legume common symbiosis gene encoding a Ca2+/calmodulin-dependent protein kinase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVCntb3O&md5=03a2357e8631a4d57e6ff1a2be3182d7CAS |
Comparot-Moss S, Denyer K (2009) The evolution of the starch biosynthetic pathway in cereals and other grasses. Journal of Experimental Botany 60, 2481–2492.
| The evolution of the starch biosynthetic pathway in cereals and other grasses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXntlGisbw%3D&md5=f442a967c612e5f9c4168502b9285d11CAS |
Coxon DT, Wright DJ (1985) Analysis of pea lipid content by gas chromatographic and microgravimetric methods. Genotype variation in lipid content and fatty acid composition. Journal of Agricultural and Food Chemistry 36, 847–856.
| Analysis of pea lipid content by gas chromatographic and microgravimetric methods. Genotype variation in lipid content and fatty acid composition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XhvVOguw%3D%3D&md5=18bb67c164964b6839aedc48dc370afbCAS |
Denyer K, Dunlap F, Thorbjornsen T, Keeling P, Smith AM (1996) The major form of ADP-glucose pyrophosphorylase in maize endosperm is extra-plastidial. Plant Physiology 112, 779–785.
| The major form of ADP-glucose pyrophosphorylase in maize endosperm is extra-plastidial.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmsFKkt7k%3D&md5=0febd88063533994777a05cd34398cc3CAS |
Dickinson DB, Preiss J (1969) ADP glucose pyrophosphorylase from maize endosperm. Archives of Biochemistry and Biophysics 130, 119–128.
| ADP glucose pyrophosphorylase from maize endosperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF1MXptleltQ%3D%3D&md5=7a905b0c0392ce51722489b196279201CAS |
Doan DNP, Rudi H, Olsen O-A (1999) The allosterically unregulated isoform of ADP-glucose pyrophosphorylase from barley endosperm is the most likely source of ADP-glucose incorporated into endosperm starch. Plant Physiology 121, 965–975.
| The allosterically unregulated isoform of ADP-glucose pyrophosphorylase from barley endosperm is the most likely source of ADP-glucose incorporated into endosperm starch.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXns12ntbg%3D&md5=2bb712456c14af80f28b25ebaf5ad7deCAS |
Giroux MJ, Hannah LC (1994) ADP-glucose pyrophosphorylase in shrunken-2 and brittle-2 mutants of maize. Molecular & General Genetics 243, 400–408.
Giroux MJ, Boyer C, Feix G, Hannah LC (1994) Coordinated transcriptional regulation of storage product genes in the maize endosperm. Plant Physiology 106, 713–722.
Hirochika H (1997) Retrotransposons of rice: their regulation and use for genome analysis. Plant Molecular Biology 35, 231–240.
| Retrotransposons of rice: their regulation and use for genome analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlvVGlurk%3D&md5=3cbae672ad79dcc5024f15a68b7517caCAS |
Hirose T, Ohdan T, Nakamura Y, Terao T (2006) Expression profiling of genes related to starch synthesis in rice leaf sheaths during the heading period. Physiologia Plantarum 128, 425–435.
| Expression profiling of genes related to starch synthesis in rice leaf sheaths during the heading period.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1Grt73I&md5=a5dac5adac57657a172b368ac8462470CAS |
Ishimaru K, Togawa E, Ookawa T, Kashiwagi T, Madoka Y, Hirotsu N (2008) New target for rice lodging resistance and its effect in a typhoon. Planta 227, 601–609.
| New target for rice lodging resistance and its effect in a typhoon.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXktVyjtg%3D%3D&md5=9828b5e386f07db03aa5d2e8e04d3871CAS |
Johnson PE, Patron NJ, Bottrill AR, Dinges JR, Fahy BF, Parker ML, Waite DN, Denyer K (2003) A low-starch barley mutant, Risø16, 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 Physiology 131, 684–696.
| A low-starch barley mutant, Risø16, lacking the cytosolic small subunit of ADP-glucose pyrophosphorylase, reveals the importance of the cytosolic isoform and the identity of the plastidial small subunit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtlyjs7o%3D&md5=57332c187fe93110b779c51f139249b5CAS |
Kashiwagi T, Madoka Y, Hirotsu N, Ishimaru K (2006) Locus prl5 improves lodging resistance of rice by delaying senescence and increasing carbohydrate reaccumulation. Plant Physiology and Biochemistry 44, 152–157.
| Locus prl5 improves lodging resistance of rice by delaying senescence and increasing carbohydrate reaccumulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltlGqsbs%3D&md5=cc16c30a42a73ddb7646b192a1eeca12CAS |
Lee SK, Hwang SK, Han M, Eom JS, Kang HG, Han Y, Choi SB, Cho MH, Bhoo SH, An G, Hahn TR, Okita TW, Jeon JS (2007) Identification of the ADP-glucose pyrophosphorylase isoforms essential for starch synthesis in the leaf and seed endosperm of rice (Oryza sativa L.). Plant Molecular Biology 65, 531–546.
| Identification of the ADP-glucose pyrophosphorylase isoforms essential for starch synthesis in the leaf and seed endosperm of rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtF2itbfL&md5=559d46189ee760e5923827cff107af61CAS |
Nakano H, Makino A, Mae T (1995) Effects of panicle removal on the photosynthetic characteristics of the flag leaf of rice plants during the ripening stage. Plant & Cell Physiology 36, 653–659.
Nakano H, Makino A, Mae T (1997) The effect of elevated partial pressures of CO2 on the relationship between photosynthetic capacity and N content in rice leaves. Plant Physiology 115, 191–198.
Ohdan T, Francisco PB, Sawada T, Hirose T, Terao T, Satoh H, Nakamura Y (2005) Expression profiling of genes involved in starch synthesis in sink and source organs of rice. Journal of Experimental Botany 56, 3229–3244.
| Expression profiling of genes involved in starch synthesis in sink and source organs of rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1GlsbnJ&md5=79497c6d3baf069725179a36a82356acCAS |
Perez CM, Palmiano EP, Baun LC, Juliano BO (1971) Starch metabolism in the leaf sheaths and culms of rice. Plant Physiology 47, 404–408.
| Starch metabolism in the leaf sheaths and culms of rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3MXhtVyitb0%3D&md5=9a86fd1aab127bc0c01919706ef63546CAS |
Rösti S, Denyer K (2007) Two paralogous genes encoding small subunits of ADP-glucose pyrophosphorylase in maize, Bt2 and L2, replace the single alternatively spliced gene found in other cereal species. Journal of Molecular Evolution 65, 316–327.
| Two paralogous genes encoding small subunits of ADP-glucose pyrophosphorylase in maize, Bt2 and L2, replace the single alternatively spliced gene found in other cereal species.Crossref | GoogleScholarGoogle Scholar |
Rösti S, Rudi H, Rudi K, Opsahl-Sorteberg H-G, Fahy B, Denyer K (2006) The gene encoding the cytosolic small subunit of ADP-glucose pyrophosphorylase in barley endosperm also encodes the major plastidial small subunit in the leaves. Journal of Experimental Botany 57, 3619–3626.
| The gene encoding the cytosolic small subunit of ADP-glucose pyrophosphorylase in barley endosperm also encodes the major plastidial small subunit in the leaves.Crossref | GoogleScholarGoogle Scholar |
Rösti S, Fahy B, Denyer K (2007) A mutant of rice lacking the leaf large subunit of ADP-glucose pyrophosphorylase has drastically reduced leaf starch content but grows normally. Functional Plant Biology 34, 480–489.
| A mutant of rice lacking the leaf large subunit of ADP-glucose pyrophosphorylase has drastically reduced leaf starch content but grows normally.Crossref | GoogleScholarGoogle Scholar |
Salamone PR, Greene TW, Kavakli IH, Okita TW (2000) Isolation and characterization of a higher plant ADP-glucose pyrophosphorylase small subunit homotetramer. FEBS Letters 482, 113–118.
| Isolation and characterization of a higher plant ADP-glucose pyrophosphorylase small subunit homotetramer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXntVWhurs%3D&md5=72785f77e0c9dd121890abf051df5122CAS |
Schnyder H (1992) The role of carbohydrate storage and redistribution in the source-sink relations of wheat and barley during grain filling – a review. New Phytologist 123, 233–245.
| The role of carbohydrate storage and redistribution in the source-sink relations of wheat and barley during grain filling – a review.Crossref | GoogleScholarGoogle Scholar |
Sikka VK, Choi SB, Kavakli IH, Sakulsingharoj C, Gupta S, Ito H, Okita TW (2001) Subcellular compartmentation and allosteric regulation of the rice endosperm ADPglucose pyrophosphorylase. Plant Science 161, 461–468.
| Subcellular compartmentation and allosteric regulation of the rice endosperm ADPglucose pyrophosphorylase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXls1aquro%3D&md5=e6dd6dda961eead62b8c81094eb838caCAS |
Singletary G, Anderson PC, Coughlan SJ (2001) Patent assigned to Pioneer Hi-Bred International, Inc., Methods of producing high-oil seed by modification of starch levels. US Patent no. 6 232 529 (The United States Patent and Trademark Office: Alexandria, Virginia).
Smidansky ED, Martin JM, Hannah LC, Fischer AM, Giroux MJ (2003) Seed yield and plant biomass increases in rice are conferred by deregulation of endosperm ADP-glucose pyrophosphorylase. Planta 216, 656–664.
Smith AM, Bettey M, Bedford ID (1989) Evidence that the rb locus alters the starch content of developing pea embryos through an effect on AGP glucose pyrophosphorylase. Plant Physiology 89, 1279–1284.
| Evidence that the rb locus alters the starch content of developing pea embryos through an effect on AGP glucose pyrophosphorylase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXit1yks7Y%3D&md5=29eda7833f7f5acb16610b9a07598ed3CAS |
Thorbjørnsen T, Villand P, Denyer K, Olsen OA, Smith AM (1996) Distinct isoforms of ADPglucose pyrophosphorylase occur inside and outside the amyloplasts in barley endosperm. The Plant Journal 10, 243–250.
| Distinct isoforms of ADPglucose pyrophosphorylase occur inside and outside the amyloplasts in barley endosperm.Crossref | GoogleScholarGoogle Scholar |
Tsai CY, Nelson OE (1966) Starch-deficient maize mutant lacking adenosine diphosphate glucose pyrophosphorylase activity. Science 151, 341–343.
| Starch-deficient maize mutant lacking adenosine diphosphate glucose pyrophosphorylase activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF28XltlyhtA%3D%3D&md5=3a76e6c58bf701463f7503398930bb33CAS |
Watanabe Y, Nakamura Y, Ishii R (1997) Relationship between starch accumulation and activities of the related enzymes in the leaf sheath as a temporary sink organ in rice (Oryza sativa). Australian Journal of Plant Physiology 24, 563–569.
| Relationship between starch accumulation and activities of the related enzymes in the leaf sheath as a temporary sink organ in rice (Oryza sativa).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXotVars7Y%3D&md5=aad060007a7d129c790f5a44251698ccCAS |
Yang J, Zhang J, Wang Z, Zhu Q (2001) Activities of starch hydrolytic enzymes and sucrose-phosphate synthase in the stems of rice subjected to water stress during grain filling. Journal of Experimental Botany 52, 2169–2179.
Yoshida S (1972) Physiological aspects of grain yield. Annual Review of Plant Physiology 23, 437–464.
| Physiological aspects of grain yield.Crossref | GoogleScholarGoogle Scholar |
