Endoplasmic reticulum-derived bodies enable a single-cell chemical defense in Brassicaceae plants

Kenji Yamada,Atsushi J Nagano,Tadashi Kunieda,Mikio Nishimura,Shino Goto-Yamada,Keiko Kuwata,Akiko Nakazaki,Ikuko Hara-Nishimura

doi:10.1038/s42003-019-0739-1

Abstract

Brassicaceae plants have a dual-cell type of chemical defense against herbivory. Here, we show a novel single-cell defense involving endoplasmic reticulum (ER)-derived organelles (ER bodies) and the vacuoles. We identify various glucosinolates as endogenous substrates of the ER-body β-glucosidases BGLU23 and BGLU21. Woodlice strongly prefer to eat seedlings of bglu23 bglu21 or a glucosinolate-deficient mutant over wild-type seedlings, confirming that the β-glucosidases have a role in chemical defense: production of toxic compounds upon organellar damage. Deficiency of the Brassicaceae-specific protein NAI2 prevents ER-body formation, which results in a loss of BGLU23 and a loss of resistance to woodlice. Hence, NAI2 that interacts with BGLU23 is essential for sequestering BGLU23 in ER bodies and preventing its degradation. Artificial expression of NAI2 and BGLU23 in non-Brassicaceae plants results in the formation of ER bodies, indicating that acquisition of NAI2 by Brassicaceae plants is a key step in developing their single-cell defense system.

Highlights

Brassicaceae plants have a dual-cell type of chemical defense against herbivory
We describe a novel single-cell type of chemical defense, in which tissue damage brings endoplasmic reticulum (ER)-body β-glucosidases into contact with substrates stored in the vacuoles, identify various glucosinolate species as endogenous substrates of BGLU23 and BGLU21 and demonstrate how the Brassicaceae-specific proteins NAI2 and BGLU23 can induce ER-body formation in non-Brassicacea plants
We identified a total of 1406 metabolites, for each of which we obtained four MS signal intensities: before and after incubation of the wild-type homogenate (IWT,[0] and IWT,[30], respectively) and before and after incubation of the bglu[23] bglu[21] homogenate (Ibglu,[0] and Ibglu,[30], respectively)

Summary

Introduction

Brassicaceae plants have a dual-cell type of chemical defense against herbivory. Woodlice strongly prefer to eat seedlings of bglu[23] bglu[21] or a glucosinolate-deficient mutant over wild-type seedlings, confirming that the β-glucosidases have a role in chemical defense: production of toxic compounds upon organellar damage. Deficiency of the Brassicaceae-specific protein NAI2 prevents ER-body formation, which results in a loss of BGLU23 and a loss of resistance to woodlice. Brassicaceae plants have a chemical herbivory defense system (called mustard-oil bomb) involving thioglucosidases ( called myrosinases) and their substrates glucosinolates. Seedlings have large amounts of another type of β-glucosidase (BGLU23, known as PYK10) that is a major component of the endoplasmic reticulum (ER)-derived organelles called ER bodies[7,8,9,10].

Methods

Results

Conclusion