Phytoplasma effector SAP54 induces indeterminate leaf-like flower development in Arabidopsis plants.

Allyson M Maclean,Kim C Findlay,Saskia A Hogenhout,Réka Tóth,Akiko Sugio,Mogens Nicolaisen,Victoria M Grieve,Olga V Makarova

doi:10.1104/pp.111.181586

Abstract

Phytoplasmas are insect-transmitted bacterial plant pathogens that cause considerable damage to a diverse range of agricultural crops globally. Symptoms induced in infected plants suggest that these phytopathogens may modulate developmental processes within the plant host. We report herein that Aster Yellows phytoplasma strain Witches' Broom (AY-WB) readily infects the model plant Arabidopsis (Arabidopsis thaliana) ecotype Columbia, inducing symptoms that are characteristic of phytoplasma infection, such as the production of green leaf-like flowers (virescence and phyllody) and increased formation of stems and branches (witches' broom). We found that the majority of genes encoding secreted AY-WB proteins (SAPs), which are candidate effector proteins, are expressed in Arabidopsis and the AY-WB insect vector Macrosteles quadrilineatus (Hemiptera; Cicadellidae). To identify which of these effector proteins induce symptoms of phyllody and virescence, we individually expressed the effector genes in Arabidopsis. From this screen, we have identified a novel AY-WB effector protein, SAP54, that alters floral development, resulting in the production of leaf-like flowers that are similar to those produced by plants infected with this phytoplasma. This study offers novel insight into the effector profile of an insect-transmitted plant pathogen and reports to our knowledge the first example of a microbial pathogen effector protein that targets flower development in a host.

Highlights

Phytoplasmas are insect-transmitted bacterial plant pathogens that cause considerable damage to a diverse range of agricultural crops globally
To better define the symptoms that Aster Yellows phytoplasma strain Witches’ Broom (AY-WB) induces in Arabidopsis, we exposed 4-week-old Arabidopsis ecotype Columbia (Col-0) plants to noncarrier and AY-WB-carrying M. quadrilineatus to allow inoculation of the bacterial pathogen
We have frequently hypothesized that phytoplasmas such as AY-WB produce effectors that manipulate the phenotype of their hosts to their own benefit (Hogenhout and Loria, 2008; Hogenhout et al, 2008; Bai et al, 2009; Sugio et al, 2011)

Summary

Introduction

Phytoplasmas are insect-transmitted bacterial plant pathogens that cause considerable damage to a diverse range of agricultural crops globally. Aster Yellows phytoplasma strain Witches’ Broom (AY-WB; Candidatus Phytoplasma asteris) is vectored by the polyphagous aster leafhopper Macrosteles quadrilineatus, which readily transmits this pathogen to a wide range of plants, including members of the Solanaceae and Brassicaceae families (Sugio et al, 2011) Phytoplasmas such as AYWB induce a variety of symptoms in plants that are indicative of an abnormal development of host tissues, including the formation of witches’ broom (a dense mass of shoots originating from a single point), phyllody (conversion of floral organs into leaves), virescence (green pigmentation of tissues such as flower petals), and bolting (growth of elongated stalks). Effectors that modulate flower development have not yet been identified

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