Abstract

Jujube witches’ broom (JWB) is caused by infection with a phytoplasma. A multi-omics approach was taken during graft infection of jujube by JWB-infected scion through the analysis of the plant transcriptome, proteome and phytohormone levels. A high number of differentially expressed genes (DEGs) were identified 37 weeks after grafting (WAG), followed by observation of typical symptoms of JWB at 48 WAG. At 37 WAG, the majority of the upregulated DEGs and differentially expressed proteins (DEPs) were related to flavonoid biosynthesis, phenylalanine metabolism and phenylpropanoid biosynthesis. Two of the four upregulated proteins were similar to jasmonate-induced protein-like. Among the downregulated genes, the two most populated GO terms were plant–pathogen interaction and plant hormone signal transduction (mainly for tryptophan metabolism). Moreover, phytoplasma infection resulted in reduced auxin content and increased jasmonate content, indicating that auxin and jasmonic acid have important roles in regulating jujube responses during the first and second stages of phytoplasma infection. At 48 WAG, the two largest groups of upregulated genes were involved in phenylpropanoid biosynthesis and flavonoid biosynthesis. Both genes and proteins involved in carbon metabolism and carbon fixation in photosynthetic organisms were downregulated, indicating that photosynthesis was affected by the third stage of phytoplasma infection.

Highlights

  • Jujube (Ziziphus jujuba Mill.) is a major fruit crop cultivated in India, Russia, the Middle East, southern Europe and, especially, China.[1]

  • Fourteen differentially expressed gene (DEG)/differentially expressed protein (DEP) showed similar expression trends, and most of these were involved in flavonoid biosynthesis, phenylalanine metabolism and phenylpropanoid biosynthesis (Figure 3a)

  • The results indicated that phytoplasma infection resulted in reduced auxin content and increased JA content at the early stage of jujube witches’ broom (JWB) disease (Figure 4)

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Summary

Introduction

Jujube (Ziziphus jujuba Mill.) is a major fruit crop cultivated in India, Russia, the Middle East, southern Europe and, especially, China.[1]. The typical symptoms of a phytoplasmainfected jujube include excessive stem production from a single point (witches’ broom), yellowing and floral organs turning into leaf-like structures (phyllody).[2]. Phytoplasmas are important agricultural pathogens[4] and have been found in over 1000 plant species worldwide.[5] Recently, phytoplasma effector proteins have been shown to target transcription factors, phytohormone receptors and other components of phytohormone signaling in the host plant in order to modulate plant development.[6,7,8,9,10,11] For example, overexpression of the phytoplasma effector SAP54 induces indeterminate leaf-like flower development in Arabidopsis plants.[6] The effector SAP11 from Aster Yellows Witches’ Broom (AY-WB) Phytoplasma alters Arabidopsis morphology, destabilizes Arabidopsis CINCINNATA (CIN)-related TEOSINTE BRANCHED1, CYCLOIDEA and the PRO-

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