ER bodies in plants of the Brassicales order: biogenesis and association with innate immunity

Ryohei T Nakano,Ikuko Hara-Nishimura,Mikio Nishimura,Kenji Yamada,Paweå‚ Bednarek

doi:10.3389/fpls.2014.00073

Abstract

The endoplasmic reticulum (ER) forms highly organized network structures composed of tubules and cisternae. Many plant species develop additional ER-derived structures, most of which are specific for certain groups of species. In particular, a rod-shaped structure designated as the ER body is produced by plants of the Brassicales order, which includes Arabidopsis thaliana. Genetic analyses and characterization of A. thaliana mutants possessing a disorganized ER morphology or lacking ER bodies have provided insights into the highly organized mechanisms responsible for the formation of these unique ER structures. The accumulation of proteins specific for the ER body within the ER plays an important role in the formation of ER bodies. However, a mutant that exhibits morphological defects of both the ER and ER bodies has not been identified. This suggests that plants in the Brassicales order have evolved novel mechanisms for the development of this unique organelle, which are distinct from those used to maintain generic ER structures. In A. thaliana, ER bodies are ubiquitous in seedlings and roots, but rare in rosette leaves. Wounding of rosette leaves induces de novo formation of ER bodies, suggesting that these structures are associated with resistance against pathogens and/or herbivores. ER bodies accumulate a large amount of β-glucosidases, which can produce substances that potentially protect against invading pests. Biochemical studies have determined that the enzymatic activities of these β-glucosidases are enhanced during cell collapse. These results suggest that ER bodies are involved in plant immunity, although there is no direct evidence of this. In this review, we provide recent perspectives of ER and ER body formation in A. thaliana, and discuss clues for the functions of ER bodies. We highlight defense strategies against biotic stress that are unique for the Brassicales order, and discuss how ER structures could contribute to these strategies.

Highlights

The endoplasmic reticulum (ER) forms highly organized network structures composed of ER tubules and ER cisternae
The constitutive presence of ER bodies in A. thaliana is strictly limited to roots in adult plants; they are absent in most cells in rosette leaves
The ER body is observed as a structure that is connected with ER tubules and/or ER cisternae in electron micrographs (Gunning, 1998; Hayashi et al, 2001). These results indicate that the ER body is continuous to the whole ER network; it is suggested to be a subdomain of the ER that has specific functions

Summary

INTRODUCTION

The endoplasmic reticulum (ER) forms highly organized network structures composed of ER tubules and ER cisternae. Many of the ER-derived compartments accumulate specific types of proteins, such as the protein bodies (PBs) in maize and rice, which contain prolamin and zein, respectively (Herman and Larkins, 1999), the KDEL-tailed protease-accumulating vesicles (KVs) in mungbean (Toyooka et al, 2000), and the ricinosomes in castor bean that accumulate papain-type proteases (Schmid et al, 2001) These structures are thought to function as repositories of particular proteins until they are required. The constitutive presence of ER bodies in A. thaliana is strictly limited to roots in adult plants; they are absent in most cells in rosette leaves Both wounding and jasmonic acid treatment induce de novo formation of ER bodies in rosette leaves. It is known that Brassicales plants have unique defense strategies against biotic stresses, which may lead to an interesting evolutionary story that includes ER bodies

MOLECULAR MECHANISMS UNDERLYING ER BODY FORMATION

Stems and maturing seeds