FNP TEAM4 project

Project team
Kenji Yamada (PI)
Kaichiro Endo (postdoc)
Toru Maeda (postdoc)
Shayan Sarkar (postdoc)
Alwine Wilkens (PhD student)
Mohamadreza Mirzaei (PhD student)
Karolina Małek (technician)

Collaborators
Prof. Mamiko Ozaki (Kobe University)
Prof. Ikuko Hara-Nishimura (Konan University)

Introduction
Plants have developed sophisticated defence systems to adapt to changes in the environment. Animal herbivores have the potential to damage plants seriously. Therefore, plants have evolved a defence system to alleviate them, which relies on species-specific metabolites. In the Brassicaceae plants, the defence metabolites are glucosinolates, which make spicy taste like wasabi and mustard, and it is a so-called “mustard oil bomb”. The glucosinolate biosynthesis pathway has evolved from the cyanogenic glucoside synthesis pathway in the plants of the order Brassicales. Many families of Brassicaceae share glucosinolates and cyanogenic glucosides, but Brassicaceae plants completely shifted to glucosinolate synthesis from cyanogenic glucoside synthesis. Glucosinolates are the precursor form of the active defence chemicals, and β-glucosidases (BGLUs) are required to activate these glucosides. Glucosinolates and BGLUs are separately stored, coming into contact and producing toxic molecules immediately against the cell damage by the herbivores, like a “mustard oil bomb”. Brassicaceae plants have two different sites for the storage of BGLUs; one is the vacuole of myrosin cells, and another is the endoplasmic reticulum (ER) bodies of epidermal cells (Figure 1). These variations of defence metabolites and enzyme storages raise the question of how Brassicaceae plants came to use these different defence systems; are there any benefits? An overview of the mustard oil bomb-based defence system is needed for further understanding the sophisticated defence system, which is essential for the survival of Brassicaceae plants.
Mutant seedlings lacking ER bodies are more sensitive to insects that normally would not attack living plants, indicating that the β-glucosidase in ER bodies is responsible for the defence against those insects. This finding is the first example showing that Arabidopsis thaliana has specific resistance mechanisms against certain insects in the seedlings. It is proposed that the interaction of plants and herbivores causes the divergence of defence strategies; the specific herbivores develop a tolerance to plant defence chemicals, and this will induce the development of new other defence chemicals in plants. However, there is no direct evidence the plant-herbivore interaction directs the divergence of plant defence chemicals and furthermore, it is still unknown about the impact of the changes in plant defence strategies on the behaviour of insects. 

The aim of the project is to understand 1) How the plants have established chemical defence strategies and 2) How the herbivores respond and elude the plant defence. In this project, we collaborate with animal ethologists. Studies on the defence systems of plants and the feeding mechanism of animals have been performed independently. Despite much effort in each field, there is a lack of research on coevolutionary interaction between plants and herbivorous animals. Our collaboration between plant molecular biologist and animal neuroethologists will provide an innovative breakthrough to figure out the interactive development of their chemical strategies.

Figure 1. Two "mustard oil bomb" systems. A. thaliana seedlings have ER bodies in the epidermal cells. ER bodies accumulate β-glucosidase BGLU21/23 (green circle), and vacuoles accumulate the substrates (orange pentagon). In contrast, rosette leaves accumulate BGLU37/38 (yellow-green circle) in myrosin cells and glucosinolates (yellow circle) in S-cells. In both systems, glucosinolates and BGLUs come into contact and produce toxic molecules immediately against the cell damage by the herbivores.