Book Chapters and Reviews:
- MacNeill, G.J., Mehrpouyan, S., Minow, M.A.A., Patterson, J.A., Tetlow, I.J. and Emes, M.J. (2017) Starch as a Source, Starch as a Sink: the Bifunctional Role of Starch in Carbon Allocation. J. Experimental Botany 68, 4433-53.
- Patterson, J. A., Emes, M.J. and Tetlow, I.J. (2017) Seed development – starch synthesis. In “Encyclopedia of Applied Plant Sciences” edited by Thomas, B., Murray B.G. & Murphy, D. Vol. 1, Waltham, MA: Academic Press, 2017, pp. 570–576.
- I. J. Tetlow, F. Liu and M. J. Emes (2015) Protein-protein interactions during starch biosynthesis. In “Starch. Metabolism and Structure”, Nakamura, Y., (ed.). Springer. pp 291-313.
- I.J.Tetlow and M.J.Emes (2014) A review of starch branching enzymes and their role in amylopectin biosynthesis. IUBMB Life 66, 546-558. http://dx.doi.org/10.1002/iub.1297
- Michael J. Emes and Ian J. Tetlow (2012) The role of heteromeric protein complexes in starch synthesis. In Starch: origins, structure and metabolism, SEB Publishing (I.J.Tetlow Editor) Vol 5, pp 255-278.
- I. J. Tetlow, F. Liu, A. Makhmoudova and M.J. Emes (2011) Biochemical, Genetic and Molecular Insights on Starch Biosynthesis in Cereals: A Means to Quality Improvement. In “Wheat. Science Dynamics: Challenges and Opportunities”, Eds R. N. Chibaar and J. Dexter. Agrobios (International). pp 509 – 525.
- I. J. Tetlow and M. J. Emes (2011) Plant Systems. Starch Biosynthesis in Higher Plants: The Starch Granule. In: Murray Moo-Young (ed.), Comprehensive Biotechnology, Second Edition, Vol 4, pp 37-45. Elsevier.
- I. J. Tetlow and M. J. Emes (2011) Plant Systems. Starch Biosynthesis in Higher Plants: The Enzymes of Starch Synthesis. In: Murray Moo-Young(ed.), Comprehensive Biotechnology, Second Edition, Vol 4, pp 47-65. Elsevier.
The selection of papers listed below build on the discovery made in our lab and first published in the Plant Cell (2004) 16, 694-708, showing that enzymes of starch synthesis form heteromeric protein complexes (see below). This paper has now been cited more than 150 times and the following are indicative of further advances we have made in more recent work.
- Liu, F., Zhao, Q., Mano, N., Ahmed, Z., Nitschke, F., Cai, Y., Chapman, K.D., Steup, M., Tetlow, I.J., and Emes, M.J. (2016) Modification of starch metabolism in transgenic Arabidopsis thaliana increases plant biomass and triples oilseed production. Plant Biotechnology Journal. 14, 976-985. doi:10.1111/pbi.12453.
This paper demonstrated significant, unexpected effects of modifying starch metabolism on flowering and the production of oilseeds. Work is underway to transfer this technology into other oilseeds such as canola.
- Boyer, L., Roussel, X., Courseaux, A., Ndjindji, O.M., Lancelon-Pin, C., Putaux, J-L., Tetlow, I., Emes, M.J., Pontoire, B., D’Hulst, C., and Wattebled, F. (2016) Expression of E. coli glycogen branching enzyme in an Arabidopsis mutant devoid of endogenous starch branching enzymes induces the synthesis of starch-like polyglucans. Plant Cell and Environment 39, 1432-1447. doi: 10.1111/pce.12702
Working with our French collaborators, this work demonstrated that a high molecular weight, glucan polymer can still be made when substituting a bacterial enzyme for the endogenous plant enzymes, although the structure of the polymer formed is quite different from starch.
- Sarah A. Dainty, S.A., Klingel, S.L., Pilkey, S.E., McDonald, E., McKeown, B., Emes, M.J. and Duncan, A.M. (2016) Resistant starch bagels reduce fasting and postprandial insulin in adults at risk for type 2 diabetes. J. Nutr. 146, 2252-2259.
Transferring our understanding of starch biosynthesis to studies of human health, enabled production of baked food products which, when used in a randomised study, were shown to have long term health benefits for the reduction of Type 2 Diabetes.
- Z. Ahmed, I. J. Tetlow, D. E. Falk, Q. Liu and M. J. Emes (2016) Resistant starch content is related to granule size in barley. Cereal Chemistry 93, 618-630.
- Z. Ahmed, A. Regina, M. K. Morell, I .J. Tetlow and M. J. Emes (2015) Protein–protein interactions among enzymes of starch biosynthesis in high-amylose barley genotypes reveal differential roles of heteromeric enzyme complexes in the synthesis of A and B granules). Plant Science, 233, 95-106.
High amylose starches are of importance as sources of resistant starch with concomitant health benefits for Type2 Diabetes and colorectal cancer. This paper demonstrates the presence of different protein complexes in the synthesis of such starches and that these are differentially distributed between different granule types in barley.
- CroftsN., Abe N., Oitome, N.F., Matsushima, R., Hayashi, M., Tetlow, I.J., Emes, M.J., Nakamura, Y., and Fujita, N. (2015) Amylopectin biosynthetic enzymes from developing rice seed form enzymatically active protein complexes. J. Exp. Botany.
This paper, with our collaborators in Japan, shows that heteromeric protein complexes of starch biosynthetic enzymes are widely found in cereals and also describes new complexes, not previously observed.
- Luo, J., Ahmed, R., Kosar-Hashemi, B., Larroque, O., Butardo Jr., V.M., Tanner, G.J., Colgrave, M.L., Upadhyaya, N.M., Tetlow, I.J., Emes, M.J., Millar, A., Jobling, S.A., Morell, M.K. and Li, Z. (2015) The different effects of starch synthase IIa mutations or variation on endosperm amylose content of barley, wheat and rice are determined by the distribution of starch synthase I and starch branching enzyme IIb between the starch granule and amyloplast stroma. Theor. Appl. Genet.
This paper with our Australian collaborators reinforces the centrality of SSIIa in the formation of multi-enzyme complexes which influence starch structure by affecting interactions with other key enzymes and their partitioning between soluble stroma and starch granules.
- F. Zhua, E. Bertoft, Y. Wang, M. Emes, I. Tetlow, and K Seetharaman (2015). Structure of Arabidopsis leaf starch is markedly altered following nocturnal degradation. Carbohydrate Polymers 117, 1002-1013
- A. Makhmoudova, D. Williams, D. Brewer, S. Massey, J. Patterson, A. Silva, K. A. Vassall, F. Liu, S. Subedi, G. Harauz, K.W. M. Siu, I. J. Tetlow and M. J. Emes (2014) Identification of Multiple Phosphorylation Sites on Maize Endosperm Starch Branching Enzyme IIb, a Key Enzyme in Amylopectin Biosynthesis. J. Biol. Chem. 289, 9233-46.
This paper is the first to identify the sites of protein phosphorylation on any enzyme of starch biosynthesis and the characterization of two protein kinases involved.
- R. M. Subasinghe, F. Liu, U. C. Polack, E. A. Lee, M. J. Emes and I. J. Tetlow (2014) Multimeric states of starch phosphorylase determine protein-protein interactions with starch biosynthetic enzymes in amyloplasts. Plant Physiology and Biochemistry 83, 168-179.
- Cisek, R., D. Tokarz, S. Krouglov, M. Steup, M. J. Emes, I. J. Tetlow and V. Barzda (2014). Second Harmonic Generation Mediated by Aligned Water in Starch Granules. The Journal of Physical Chemistry B., 118, 14785-14794. DOI:10.1021/jp508751s. Link
- MacNeil, S., Rebry, R.,Tetlow, I.J., M. J. Emes, M.J., McKeown, B. and Graham, T.E. (2013) Resistant Starch Intake at Breakfast Affects Postprandial Responses in Type 2 Diabetics, and Enhances Insulin Secretion Following a Second Meal.Applied Physiology, Nutrition and Metabolism, 38, 1187-1195.
This paper demonstrates the health benefits of including resistant starch in baked products in a human health trial, reducing blood glucose levels and enhancing insulin secretion.
- F. Liu, N. Romanova, E.A. Lee, R. Ahmed, E. Gilbert, M. Evans, M. K. Morell, M. J. Emes, and Ian J. Tetlow (2012) Glucan affinity of starch synthase IIa determines binding of starch synthase I and starch branching enzyme IIb to starch granules Biochemical Journal, 448, 373-387.
This paper highlights the centrality of heteromeric protein complexes to the formation of organised glucan clusters in normal starch. Here we defined a model for the interactions between 3 enzymes, demonstrating that starch synthase IIa forms the core of a protein-complex to which the other two enzymes are recruited. Using a novel maize mutant, developed over several years of back-crossing, we showed that a single point mutation in starch synthase IIa prevents it from binding to the starch granule. As a consequence, the other two enzymes with which it forms a functional protein-complex are also not able to bind to starch, and do not become incorporated into granules.
- F. Liu, Z. Ahmed, E. A. Lee, E. Weber, Q. Liu, R. Ahmed, M. K. Morell, M. J. Emes and I. J. Tetlow (2012) Allelic variants of the amylose extender mutation of maize demonstrate phenotypic variation in starch structure resulting from modified protein-protein interactions J. Exp. Bot. 63, 1167-1183.
This paper investigated a genetic variant of a starch branching enzyme IIb mutant in which an inactive enzyme is expressed, and was compared with the effects of a null mutation of the same gene. As a result, different heteromeric enzyme complexes are formed in the two mutants in vivo, leading to marked alterations in the size of starch granules and the amylose content. This is critical to an understanding of how variation in protein complexes, rather than just loss of an enzyme activity, influences phenotype.
- F. Liu, A. Makhmoudova, E.A. Lee,R. Wait, M.J. Emes and I.J. Tetlow (2009) The amylose extender mutant of maize conditions novel protein-protein interactions between starch biosynthetic enzymes in amyloplasts. J. Exp. Bot 60, 4423-4440
This paper was the first to demonstrate that in a high amylose mutant of maize, lacking branching enzyme IIb, novel stromal protein complexes are formed between starch biosynthetic enzymes. These complexes contribute to the altered starch phenotype and, as a consequence, become incorporated into starch granules. Significantly, this paper combined a genetic approach with powerful biochemical and molecular assays which many groups from around the world have visited our lab to learn. The discovery that the formation of soluble, multi-enzyme complexes in the amyloplast stroma is reflected in the granule composition provides an additional tool to look for genetic variation in the process of starch biosynthesis.
- I.J. Tetlow, K.G. Beisel, S. Cameron, A. Makhmoudova, F. Liu, N.S. Bresolin, R. Wait, M.K. Morell, and M. J. Emes (2008) Analysis of Protein Complexes in Wheat Amyloplasts Reveals Functional Interactions among Starch Biosynthetic Enzymes. Plant Physiology 146, 1878-1891: and
- T.A. Hennen-Bierwagen, F. Liu, R.S. Marsh, S. Kim, Q. Gan, I.J. Tetlow, M.J. Emes, M.G. James, and A.M. Myers (2008) Multiple Starch Biosynthetic Enzymes from Developing Zea mays Endosperm Associate in Multisubunit Complexes. Plant Physiology 146, 1892-1908
These papers showed for the first time that soluble starch synthases and starch branching enzymes form functional protein complexes in the stroma of amyloplasts. The association of SSI, SSII and SBEII isoforms was shown to be phosphorylation-dependent and has led to much of our recent work on the discovery of the protein kinases involved. These two papers were published back-to-back, and established that the novel regulatory mechanisms discovered in wheat are common within different species of cereal endosperm. Each has been cited about 100 times.
- I.J. Tetlow, R. Wait, Z. Lu, R. Akkasaeng, C.G. Bowsher, S. Esposito, B. Kosar- Hashemi, M.K. Morell and M.J. Emes (2004) Protein Phosphorylation in Amyloplasts Regulates Starch Branching Enzyme Activity and Protein-Protein Interactions. The Plant Cell: 16, 694-708.
This was the first publication to demonstrate that the pathway of starch synthesis in plants is regulated by protein phosphorylation and that this process can catalyse the formation of multi-enzyme complexes involved in the biosynthesis of starch.