Structure, function and membrane interactions of plant annexins: An update

doi:10.1016/j.plantsci.2011.05.013

Plant Science

Volume 181, Issue 3, September 2011, Pages 230-241

https://doi.org/10.1016/j.plantsci.2011.05.013 Get rights and content

Abstract

Knowledge accumulated over the past 15 years on plant annexins clearly indicates that this disparate group of proteins builds on the common annexin function of membrane association, but possesses divergent molecular mechanisms. Functionally, the current literature agrees on a key role of plant annexins in stress response processes such as wound healing and drought tolerance. This is contrasted by only few established details of the molecular level mechanisms that are driving these activities.

In this review, we appraise the current knowledge of plant annexin molecular, functional and structural properties with a special emphasis on topics of less coverage in recent past overviews. In particular, plant annexin post-translational modification, roles in polar growth and membrane stabilisation processes are discussed.

Highlights

► Plant annexin phosphorylation as an important regulator of membrane and calcium binding. ► Fine-tuning of annexins through phosphorylation may establish infrastructure for polar growth. ► Scaffold functionality of annexins at sites where the plasma membrane is in a transformation stage. ► Glutathionylation of the S₃ cluster as a generic mechanism of stress-related response.

Introduction

Genome sequencing revealed that annexins in plants comprise a multigene family with several members, eight in Arabidopsis thaliana [1] and nine in Oryza sativa [2]. Many annexins from other plant species have been reported to date, albeit a systematic mapping of annexins in most plants is still lacking. The defining criterion of annexins is their highly conserved fold which is also observed in plant annexins. It consists of a four-fold repeat (I–IV) of a 70 amino acid sequence that constitutes the C-terminal (core) domain (see Fig. 1). Each repeat forms the characteristic five-helix (A–E) bundle with membrane binding sites situated in the AB and DE loops. Canonical calcium binding occurs in type II or type III binding sites. The former type is established through the endonexin sequence G-X-G-T-{38–40}-D/E, where the G-X-G-T motif is found in the AB loops, and the bidentate acidic side chain is located at the C-terminal end of helix D in the same repeat. The N-terminal domain is situated at the opposite side of the molecule and typically not facing the membrane. It can vary in length from 5 to 50 amino acids, and may associate with the core domain as well as confer allosteric regulation [3].

Previous overviews on plant annexins have summarised the current knowledge protein expression in plants, biochemical and structural characterisation and putative physiological roles [4], [5], [6], [7]. This review attempts an update on some less covered aspects of plant annexins, namely post-translational modification and a role in controlling differential growth. Furthermore, a new link between the recurring phenomenological observation of plant annexin roles in stress with underlying molecular mechanisms may be established through the recent discovery of vertebrate annexin roles in plasma membrane re-sealing. Lastly, an appraisal of annexin membrane interactions is conducted.

Section snippets

Molecular structure

Experimental structural information is available in the form of crystal structures of bell pepper annexin 24 (Ca32) [8], cotton annexin Anx(Gh)1 [9], [10] and Arabidopsis Anx(At)1 [11]. The main structural features separating plant from vertebrate annexins include two dysfunctional canonical calcium binding sites, direct interactions of side chain residues on the convex side for membrane binding, and the propensity for oligomer formation in case of the plant proteins.

Based on the primary

Knowledge from vertebrate annexins

Post-translational modifications may have an enormous impact on the structure of a protein, and subsequently on its function, and provide functionalities or interactions that will lead to translocation or protein–protein interactions. The N-terminal domain in vertebrate annexins, is a main source of structural and functional diversity when comparing different members of this protein family. It can undergo several post-translational modifications, including phosphorylation [18],

Differential/polar growth

Early work on animal annexins focused on their calcium-dependent membrane interactions, especially membrane aggregation and membrane fusion activities that suggested a role for annexins in mediating secretion. Indeed, annexin A7, one of the first annexins characterised, has an established role in secretion in various cell types, which has been linked to GTP- and calcium-mediated membrane fusion and channel activities [59], [60], [61]. There are now numerous examples of other individual animal

Redox processes at the plasma membrane

An annexin protein is associated with a lipid raft membrane preparation in Medicago [100]. A complete plasma membrane redox system occurs within lipid rafts, and certain plant annexins function in reactive oxygen species (ROS) signaling pathways by reducing the levels of H₂O₂ [102], [103], [104]. They may do so via association with raft localized membrane redox systems. Lipid raft polarization of the ROS signaling system is required for pollen tube tip growth [105].

The finding is an interesting

Conclusions and outlook

The available data on plant annexin phosphorylation indicates modification of either the convex or the concave side of the molecule. Therefore, consequences for membrane and calcium binding can be expected, thus resulting in altered translocation. The concave side of the plant annexin molecule may also be a prime site of interaction with other proteins, subject to phosphorylation-dependent regulation.

The structural similarity of the C-terminal helix IVD with a region in 14-3-3 proteins provides

Acknowledgement

The work was partially supported by Grants N N301 567540 to DKP from the Polish Ministry of Education and Science.

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ReviewStructure, function and membrane interactions of plant annexins: An update

Abstract

Highlights

Introduction

Section snippets

Molecular structure

Knowledge from vertebrate annexins

Differential/polar growth

Redox processes at the plasma membrane

Conclusions and outlook

Acknowledgement

Plant Physiol. Biochem.

Plant Sci.

J. Biol. Chem.

J. Biol. Chem.

Structure

J. Biol. Chem.

J. Biol. Chem.

J. Biol. Chem.

J. Biol. Chem.

J. Biol. Chem.

J. Biol. Chem.

J. Biol. Chem.

J. Biol. Chem.

J. Biol. Chem.

Biochem. Biophys. Res. Commun.

Mol. Cell. Proteomics

FEBS Lett.

Cell

J. Biol. Chem.

J. Biol. Chem.

Plant Physiol. Biochem.

J. Biol. Chem.

Trends Plant Sci.

Curr. Biol.

Curr. Opin. Plant Biol.

Mol. Cell. Proteomics

The annexins

Genome Biol.

Structural conservation and functional versatility: allostery as a common annexin feature

Annexins in the plant kingdom—perspectives and potentials

Annexins

Annexins: multifunctional components of growth and adaptation

J. Exp. Bot.

Annexins

New Phytol.

The crystal structure of annexin Gh1 from Gossypium hirsutum reveals an unusual S3 cluster

Eur. J. Biochem.

Structures and functions of annexins in plants

Cell. Mol. Life Sci.

Structural determinants for plant annexin–membrane interactions

Biochemistry

Plant annexins form calcium-independent oligomers in solution

Protein Sci.

Annexin-like protein from Arabidopsis thaliana rescues delta oxyR mutant of Escherichia coli from H2O2 stress

Proc. Natl. Acad. Sci. U. S. A.

Zea mays annexins modulate cytosolic free Ca2+ and generate a Ca2+-permeable conductance

Plant Cell

The role of annexin 1 in drought stress in Arabidopsis

Plant Physiol.

Participation of annexins in protein phosphorylation

Cell. Mol. Life Sci.

A strategy for isolation of cDNAs encoding proteins affecting human intestinal epithelial cell growth and differentiation: characterization of a novel gut-specific N-myristoylated annexin

J. Cell Biol.

Annexin XIIIb: a novel epithelial specific annexin is implicated in vesicular traffic to the apical plasma membrane

J. Cell Biol.

Identification of oxidant-sensitive proteins: TNF-alpha induces protein glutathiolation

Biochemistry

Regulation of annexin I by proteolysis in rat alveolar epithelial type II cells

Biochem. Mol. Biol. Int.

Proteolytic signals in the primary structure of annexins

Mol. Cell. Biochem.

Phosphorylation mutants elucidate the mechanism of annexin IV-mediated membrane aggregation

Biochemistry

Annexins: from structure to function

Physiol. Rev.

Regulation of the chromaffin granule aggregating activity of annexin A1 by phosphorylation

Biochemistry

An annexin 2 phosphorylation switch mediates its p11-dependent translocation to the cell surface

J. Biol. Chem.

Review
Structure, function and membrane interactions of plant annexins: An update

The crystal structure of annexin Gh1 from Gossypium hirsutum reveals an unusual S₃ cluster

Annexin-like protein from Arabidopsis thaliana rescues delta oxyR mutant of Escherichia coli from H₂O₂ stress

Zea mays annexins modulate cytosolic free Ca²⁺ and generate a Ca²⁺-permeable conductance