Evolutionary, Structural and Expression Analysis of Core Genes Involved in Starch Synthesis

Overview

Journal Sci Rep

Specialty Science

Date 2018 Aug 26

PMID 30143668

Citations 34

Authors

Jianzhou Qu

Shutu Xu

Zhengquan Zhang

Guangzhou Chen

Yuyue Zhong

Linsan Liu

Renhe Zhang

Jiquan Xue

Dongwei Guo

Affiliations

Soon will be listed here.

Abstract

Starch is the main storage carbohydrate in plants and an important natural resource for food, feed and industrial raw materials. However, the details regarding the pathway for starch biosynthesis and the diversity of biosynthetic enzymes involved in this process are poorly understood. This study uses a comprehensive phylogenetic analysis of 74 sequenced plant genomes to revisit the evolutionary history of the genes encoding ADP-glucose pyrophosphorylase (AGPase), starch synthase (SS), starch branching enzyme (SBE) and starch de-branching enzyme (DBE). Additionally, the protein structures and expression patterns of these four core genes in starch biosynthesis were studied to determine their functional differences. The results showed that AGPase, SS, SBE and DBE have undergone complicated evolutionary processes in plants and that gene/genome duplications are responsible for the observed differences in isoform numbers. A structure analysis of these proteins suggested that the deletion/mutation of amino acids in some active sites resulted in not only structural variation but also sub-functionalization or neo-functionalization. Expression profiling indicated that AGPase-, SS-, SBE- and DBE-encoding genes exhibit spatio-temporally divergent expression patterns related to the composition of functional complexes in starch biosynthesis. This study provides a comprehensive atlas of the starch biosynthetic pathway, and these data should support future studies aimed at increasing understanding of starch biosynthesis and the functional evolutionary divergence of AGPase, SS, SBE, and DBE in plants.

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References

Streb S, Delatte T, Umhang M, Eicke S, Schorderet M, Reinhardt D . Starch granule biosynthesis in Arabidopsis is abolished by removal of all debranching enzymes but restored by the subsequent removal of an endoamylase. Plant Cell. 2008; 20(12):3448-66. PMC: 2630441. DOI: 10.1105/tpc.108.063487. View

Buschiazzo A, Ugalde J, Guerin M, Shepard W, Ugalde R, Alzari P . Crystal structure of glycogen synthase: homologous enzymes catalyze glycogen synthesis and degradation. EMBO J. 2004; 23(16):3196-205. PMC: 514502. DOI: 10.1038/sj.emboj.7600324. View

Shannon P, Markiel A, Ozier O, Baliga N, Wang J, Ramage D . Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003; 13(11):2498-504. PMC: 403769. DOI: 10.1101/gr.1239303. View

Finn R, Bateman A, Clements J, Coggill P, Eberhardt R, Eddy S . Pfam: the protein families database. Nucleic Acids Res. 2013; 42(Database issue):D222-30. PMC: 3965110. DOI: 10.1093/nar/gkt1223. View

Denyer K, Waite D, Motawia S, Moller B, Smith A . Granule-bound starch synthase I in isolated starch granules elongates malto-oligosaccharides processively. Biochem J. 1999; 340 ( Pt 1):183-91. PMC: 1220236. View

Ross J, Li Y, Lim E, Bowles D . Higher plant glycosyltransferases. Genome Biol. 2001; 2(2):REVIEWS3004. PMC: 138907. DOI: 10.1186/gb-2001-2-2-reviews3004. View

Bateman A, Coggill P, Finn R . DUFs: families in search of function. Acta Crystallogr Sect F Struct Biol Cryst Commun. 2010; 66(Pt 10):1148-52. PMC: 2954198. DOI: 10.1107/S1744309110001685. View

Nakamura Y, Francisco Jr P, Hosaka Y, Sato A, Sawada T, Kubo A . Essential amino acids of starch synthase IIa differentiate amylopectin structure and starch quality between japonica and indica rice varieties. Plant Mol Biol. 2005; 58(2):213-27. DOI: 10.1007/s11103-005-6507-2. View

Zhang X, Szydlowski N, Delvalle D, DHulst C, James M, Myers A . Overlapping functions of the starch synthases SSII and SSIII in amylopectin biosynthesis in Arabidopsis. BMC Plant Biol. 2008; 8:96. PMC: 2566982. DOI: 10.1186/1471-2229-8-96. View

10.

Pfister B, Zeeman S . Formation of starch in plant cells. Cell Mol Life Sci. 2016; 73(14):2781-807. PMC: 4919380. DOI: 10.1007/s00018-016-2250-x. View

11.

Letunic I, Bork P . Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res. 2016; 44(W1):W242-5. PMC: 4987883. DOI: 10.1093/nar/gkw290. View

12.

Moreira D, Le Guyader H, Philippe H . The origin of red algae and the evolution of chloroplasts. Nature. 2000; 405(6782):69-72. DOI: 10.1038/35011054. View

13.

LARKIN M, Blackshields G, Brown N, Chenna R, McGettigan P, McWilliam H . Clustal W and Clustal X version 2.0. Bioinformatics. 2007; 23(21):2947-8. DOI: 10.1093/bioinformatics/btm404. View

14.

Subasinghe R, Liu F, Polack U, Lee E, Emes M, Tetlow I . Multimeric states of starch phosphorylase determine protein-protein interactions with starch biosynthetic enzymes in amyloplasts. Plant Physiol Biochem. 2014; 83:168-79. DOI: 10.1016/j.plaphy.2014.07.016. View

15.

Jeon J, Ryoo N, Hahn T, Walia H, Nakamura Y . Starch biosynthesis in cereal endosperm. Plant Physiol Biochem. 2010; 48(6):383-92. DOI: 10.1016/j.plaphy.2010.03.006. View

16.

Ballicora M, Iglesias A, Preiss J . ADP-Glucose Pyrophosphorylase: A Regulatory Enzyme for Plant Starch Synthesis. Photosynth Res. 2005; 79(1):1-24. DOI: 10.1023/B:PRES.0000011916.67519.58. View

17.

Vester-Christensen M, Hachem M, Svensson B, Henriksen A . Crystal structure of an essential enzyme in seed starch degradation: barley limit dextrinase in complex with cyclodextrins. J Mol Biol. 2010; 403(5):739-50. DOI: 10.1016/j.jmb.2010.09.031. View

18.

Liu H, Yu G, Wei B, Wang Y, Zhang J, Hu Y . Identification and Phylogenetic Analysis of a Novel Starch Synthase in Maize. Front Plant Sci. 2015; 6:1013. PMC: 4653816. DOI: 10.3389/fpls.2015.01013. View

19.

Abe N, Asai H, Yago H, Oitome N, Itoh R, Crofts N . Relationships between starch synthase I and branching enzyme isozymes determined using double mutant rice lines. BMC Plant Biol. 2014; 14:80. PMC: 3976638. DOI: 10.1186/1471-2229-14-80. View

20.

Qu J, Ma C, Feng J, Xu S, Wang L, Li F . Transcriptome Dynamics during Maize Endosperm Development. PLoS One. 2016; 11(10):e0163814. PMC: 5047526. DOI: 10.1371/journal.pone.0163814. View