Annexins: central regulators of plant growth and stress signaling

Abstract

Annexins are a family of multifunctional calcium-dependent and phospholipid-binding proteins that are widely distributed in the plant kingdom. They have a highly conserved evolutionary history that dates back to single-celled protists. Plant annexins, as soluble proteins, can flexibly bind to endomembranes and plasma membranes, exhibiting unique calcium-dependent and calcium-independent characteristics. Members of the annexin family have diverse functions, including binding to F-actin, participating in ATP and GTP hydrolysis, and even serving as peroxidases or cation channels. Annexins play pivotal roles in plant growth and stress signaling. They can respond sensitively to environmental, metabolic, and developmental signals, thereby affecting cytoskeleton remodeling and exocytosis mechanisms. Plant annexin gene families have been successfully identified in multiple species, and their expression and intracellular localization are precisely regulated by developmental processes and environmental factors. Although research on plant annexins has aroused great interest, their depth and breadth still need further expansion compared with those of animal annexins. This article provides a comprehensive and in-depth review of the characteristics and functions of plant annexin families, revealing their core roles in plant growth and adaptation, and yielding valuable references and insights for future research.

1. Introduction

Annexins are a multifunctional and evolutionarily conserved multigene family of Ca2+-dependent and phospholipid-binding proteins [1–3]. They are a group of primitive proteins that date back to approximately 1 to 1.5 billion years ago in the unicellular protist Giardia lamblia [4]. These proteins are widely distributed in plants, animals, and microorganisms [2,5,6]. Plant annexins were first discovered in tomatoes by Boustead et al. [7] in 1989, but research interest in plant annexins has increased. In contrast, animal annexins have been extensively studied. Animal annexins are involved in signal transduction, free cytosolic Ca2+ homeostasis, exocytosis and endocytosis, membrane organization, cytoskeletal dynamics, cell cycle control, and water permeability [8,9].

Plants can sense and respond to a range of environmental, metabolic, and developmental signals. The operation and control of interacting signal transduction pathways involve cells, endomembranes, and a range of integrated, peripheral, and soluble proteins. The downstream responses may require remodeling of the cytoskeleton and changes in the exocytosis mechanism and cell wall [1]. Plant annexins appear to function at all of these levels [8]. Research has shown that plant annexins, as ubiquitous soluble proteins, can bind to endomembranes and the plasma membrane with both calcium-dependent and calcium-independent properties. Some members of this multigene family can bind to F-actin, hydrolyze GTP and ATP, and act as peroxidases or cation channels [10–15]. Plant annexins seem to be at the center of signal transduction and adaptation, playing a role as core regulators or effectors in plant growth and stress signaling. Plant annexins can not only regulate cell activities such as cell division and tissue and organ development but also regulate abiotic stress (such as salt and drought stresses) and biotic stress processes caused by pathogens [3,16–18].