ANNEXIN1 mediates calcium-dependent systemic defense in Arabidopsis plants upon herbivory and wounding.

Jaiana Malabarba,Sandra S Scholz,Michael Reichelt,Katie A Wilkins,Axel Mithöfer,Dorota Konopka‐Postupolska,Julia M Davies,Edgar Peiter,Ralf Oelmüller,Anja K Meents,Julia Rachowka

doi:10.1111/nph.17277

Abstract

Cellular calcium (Ca) transients are endogenous signals involved in local and systemic signaling and defense activation upon environmental stress, including wounding and herbivory. Still, not all Ca2+ channels contributing to the signaling have been identified, nor are their modes of action fully known. Plant annexins are proteins capable of binding to anionic phospholipids and can exhibit Ca channel-like activity. Arabidopsis ANNEXIN1 (ANN1) is suggested to contribute to Ca transport. Here, we report that wounding and simulated-herbivory-induced cytosolic free Ca elevation was impaired in systemic leaves in ann1 loss-of-function plants. We provide evidence for a role of ANN1 in local and systemic defense of plants attacked by herbivorous Spodoptera littoralis larvae. Bioassays identified ANN1 as a positive defense regulator. Spodoptera littoralis feeding on ann1 gained significantly more weight than larvae feeding on wild-type, whereas those feeding on ANN1-overexpressing lines gained less weight. Herbivory and wounding both induced defense-related responses on treated leaves, such as jasmonate accumulation and defense gene expression. These responses remained local and were strongly reduced in systemic leaves in ann1 plants. Our results indicate that ANN1 plays an important role in activation of systemic rather than local defense in plants attacked by herbivorous insects.

Highlights

Plants are challenged throughout their life by various abiotic and biotic stress factors
We report that wounding- and simulated herbivory-induced cytosolic free calcium elevation was impaired in systemic leaves in ann1 loss of function plants
We provide evidence for a role of ANNEXIN1 in local and systemic defense of plants attacked by herbivorous Spodoptera littoralis larvae

Summary

Introduction

Plants are challenged throughout their life by various abiotic and biotic stress factors. These changes in the environment require fast adaptation. In particular an attack by chewing insects is a combination of plant tissue wounding and application of insectspecific herbivore-associated molecular patterns (HAMPs), mainly present in their oral secretions (OS) (Mithöfer & Boland, 2008; Vadassery et al, 2012b; Kiep et al, 2015). The elevation in cytosolic free calcium, [Ca2+]cyt, is one of the earliest signaling events initiated upon the plant’s interaction with feeding insects (Maffei et al, 2004; Kiep et al, 2015; Toyota et al, 2018). The connection between jasmonates and [Ca2+]cyt is likely mediated by Ca2+-sensing proteins. In Arabidopsis, ligand-gated channels such as glutamate receptor-like channels (GLR) and cyclic nucleotide-gated channels (CNGC) plus potentially stretch-activated Ca2+ channels OSCA (reduced hyperosmolality-induced Ca2+ increase) and MCA (MID1-complementing activity) are the four main families of plasma membrane Ca2+-

Objectives

Methods

Results

Discussion

Conclusion