Structural basis of the interaction between ESV1 and LESV from Arabidopsis thaliana with starch glucans

Starch is the major energy storage compound in plants. Whether it is transient or stored, it is accumulated in the form of insoluble, semi-crystalline granules. The structure of these granules is related to the structure of the main component: amylopectin. Amylopectin consists of linear polymers of glucose units linked by α-1,4 bonds, forming double helices that combine to form the semi-crystalline lamellae of the granules, and α-1,6 branching points that form the amorphous lamellae. This particular structure of amylopectin is linked to the action of isoamylases, which cut the excess of branching points and allow the granules to be structured. For a long time, it was thought that the action of these enzymes was responsible for the structuring of starch granules. Recently, two new proteins, LESV and ESV1, have been characterized and are involved in the phase transition of amylopectin (LESV) or in the maintenance of the granule structure (ESV1). These proteins share a tryptophan-rich domain folded into an antiparallel β-sheet that is particularly well suited to bind amylopectin double helices. In this paper we present the structural study of these interactions using integrative structural biology approaches and show that LESV, in contrast to ESV1 can intervenes during amylopectin biosynthesis.

[1]  S. Zeeman,et al.  LIKE EARLY STARVATION 1 and EARLY STARVATION 1 promote and stabilize amylopectin phase transition in starch biosynthesis , 2023, Science advances.

[2]  J. Fettke,et al.  LIKE EARLY STARVATION alters the glucan structures at the starch granule surface and thereby influences the action of both starch-synthesizing and -degrading enzymes. , 2022, The Plant journal : for cell and molecular biology.

[3]  Oriol Vinyals,et al.  Highly accurate protein structure prediction with AlphaFold , 2021, Nature.

[4]  B. Wallace,et al.  CDtoolX, a downloadable software package for processing and analyses of circular dichroism spectroscopic data , 2018, Protein science : a publication of the Protein Society.

[5]  A. Myers,et al.  Direct Determination of the Site of Addition of Glucosyl Units to Maltooligosaccharide Acceptors Catalyzed by Maize Starch Synthase I , 2018, Front. Plant Sci..

[6]  E. Longo,et al.  UV-Denaturation Assay to Assess Protein Photostability and Ligand-Binding Interactions Using the High Photon Flux of Diamond B23 Beamline for SRCD , 2018, Molecules.

[7]  F. Brandt,et al.  EARLY STARVATION1 specifically affects the phosphorylation action of starch-related dikinases. , 2018, The Plant journal : for cell and molecular biology.

[8]  N. Szydlowski,et al.  Proteome Analysis of Potato Starch Reveals the Presence of New Starch Metabolic Proteins as Well as Multiple Protease Inhibitors , 2018, Front. Plant Sci..

[9]  P. V. Konarev,et al.  ATSAS 2.8: a comprehensive data analysis suite for small-angle scattering from macromolecular solutions , 2017, Journal of applied crystallography.

[10]  M. Trick,et al.  The Starch Granule-Associated Protein EARLY STARVATION1 Is Required for the Control of Starch Degradation in Arabidopsis thaliana Leaves[OPEN] , 2016, Plant Cell.

[11]  S. Zeeman,et al.  Formation of starch in plant cells , 2016, Cellular and Molecular Life Sciences.

[12]  Frank Wien,et al.  Accurate secondary structure prediction and fold recognition for circular dichroism spectroscopy , 2015, Proceedings of the National Academy of Sciences.

[13]  I. Tetlow,et al.  Amylopectin biosynthetic enzymes from developing rice seed form enzymatically active protein complexes , 2015, Journal of experimental botany.

[14]  Zaheer Ahmed,et al.  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. , 2015, Plant science : an international journal of experimental plant biology.

[15]  E. Suzuki,et al.  Diversity of reaction characteristics of glucan branching enzymes and the fine structure of α-glucan from various sources. , 2014, Archives of biochemistry and biophysics.

[16]  M. Réfrégiers,et al.  3D imaging of enzymes working in situ. , 2014, Analytical chemistry.

[17]  B. Lagarde,et al.  DISCO synchrotron-radiation circular-dichroism endstation at SOLEIL. , 2012, Journal of synchrotron radiation.

[18]  Johannes E. Schindelin,et al.  Fiji: an open-source platform for biological-image analysis , 2012, Nature Methods.

[19]  M. Stitt,et al.  Starch turnover: pathways, regulation and role in growth. , 2012, Current opinion in plant biology.

[20]  P. Colonna,et al.  In situ tracking of enzymatic breakdown of starch granules by synchrotron UV fluorescence microscopy. , 2011, Analytical chemistry.

[21]  Serge Pérez,et al.  The molecular structures of starch components and their contribution to the architecture of starch granules: A comprehensive review , 2010 .

[22]  G. David,et al.  Combined sampler robot and high-performance liquid chromatography: a fully automated system for biological small-angle X-ray scattering experiments at the Synchrotron SOLEIL SWING beamline , 2009 .

[23]  R. W. Janes,et al.  Light flux density threshold at which protein denaturation is induced by synchrotron radiation circular dichroism beamlines. , 2008, Journal of synchrotron radiation.

[24]  Dmitri I Svergun,et al.  Global rigid body modeling of macromolecular complexes against small-angle scattering data. , 2005, Biophysical journal.

[25]  Manash S. Chatterjee,et al.  Mutants of Arabidopsis Lacking a Chloroplastic Isoamylase Accumulate Phytoglycogen and an Abnormal Form of Amylopectin1[w] , 2005, Plant Physiology.

[26]  J. Runt,et al.  Spherulitic crystallization in starch as a model for starch granule initiation. , 2005, Biomacromolecules.

[27]  Frank Wien,et al.  Redetermination of the extinction coefficient of camphor-10-sulfonic acid, a calibration standard for circular dichroism spectroscopy. , 2004, Analytical biochemistry.

[28]  Dmitri I. Svergun,et al.  Uniqueness of ab initio shape determination in small-angle scattering , 2003 .

[29]  A. Donald,et al.  Side‐Chain Liquid‐Crystalline Model for Starch , 2000 .

[30]  S. Ball,et al.  Recent progress toward understanding biosynthesis of the amylopectin crystal. , 2000, Plant physiology.

[31]  P Colonna,et al.  Starch granules: structure and biosynthesis. , 1998, International journal of biological macromolecules.

[32]  P Willett,et al.  Development and validation of a genetic algorithm for flexible docking. , 1997, Journal of molecular biology.

[33]  P. Colonna,et al.  From Glycogen to Amylopectin: A Model for the Biogenesis of the Plant Starch Granule , 1996, Cell.

[34]  Dmitri I. Svergun,et al.  Determination of the regularization parameter in indirect-transform methods using perceptual criteria , 1992 .

[35]  A. Imberty,et al.  The double-helical nature of the crystalline part of A-starch. , 1988, Journal of molecular biology.

[36]  Chia-Yin Tsai,et al.  The function of the Waxy locus in starch synthesis in maize endosperm , 1974, Biochemical Genetics.