Transcriptome analysis reveals pathways facilitating the growth of tobacco powdery mildew in Arabidopsis

Ran Li,Shunyuan Xiao,Yan Li,Xian-Feng Ma,Jing Fan,Ling-Li Zhang,Xue-Mei Yang,Ying-Ge Wang,Jing Shang,Wen-Ming Wang,Hui Yang,Viswanathan Chandran,Ji-Qun Zhao,Xiao-Long Cao

doi:10.1186/s42483-019-0012-z

Ran Li, Shunyuan Xiao + Show 12 more

Open Access

https://doi.org/10.1186/s42483-019-0012-z

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Abstract

Powdery mildew (PM) fungi are biotrophic pathogens that rely on living hosts to survive and thrive. However, their colonization is restricted by host defenses at both the penetration and post-penetration stages. The tobacco PM strain Golovinomyces cichoracearum (Gc) SICAU1 has overcome penetration resistance of Arabidopsis but its growth is arrested by post-penetration resistance. While Gc SICAU1 only poorly grows in Arabidopsis Col-0 wild-type plants, it can sustainably grow for more than 20 days on the same infected leaves of the double mutant pad4–1 sid2–1 that is defective in both the synthesis and signaling of salicylic acid (SA). To understand the underlying molecular mechanisms, we conducted a comparative transcriptome analysis between Col-0 and pad4–1 sid2–1 in response to Gc SICAU1. We found that 4811 genes were differentially expressed more than four-fold between any two of the measured seven time points (0, 1, 3, 6, 8, 10 and 12 days post-inoculation). Gene expression pattern analysis suggests that differential expression of 348 genes and 190 genes may explain resistance in Col-0 and susceptibility in pad4–1 sid2–1, respectively. Gene Ontology (GO) analysis suggests that Gc SICAU1 might be arrested in Col-0 by both pattern-triggered immunity and SA-dependent defense. By contrast, its sustained growth in pad4–1 sid2–1 may be attributable to the activation of a detoxification pathway that is normally repressed by the SA-signaling pathway. Taken together, our results suggest that multiple distinct, yet interconnected pathways control the growth of tobacco powdery mildew in Arabidopsis.

Highlights

Powdery mildew (PM) diseases epidemically occur in nearly 10,000 plant species including many economically and agriculturally important crops (Kuhn et al 2016)
The number of genes responsive to tobacco powdery mildew is quite different between Col-0 and pad4–1 sid2–1 Previously, we isolated a tobacco powdery mildew strain, Golovinomyces cichoracearum (Gc) SICAU1, which poorly sporulated in Arabidopsis ecotype Col-0 (Zhang et al 2015)
Through transcriptome analysis on a time course of infection, we found that 3 dpi was important for activation of post-penetration defense in Col-0 and 6 dpi was crucial for activation of the detoxification pathway for the sustained growth in pad4–1 sid2–1

Summary

Introduction

Powdery mildew (PM) diseases epidemically occur in nearly 10,000 plant species including many economically and agriculturally important crops (Kuhn et al 2016). The formation of a callose encasement of the haustorium complex (EHC) was observed in some invaded epidermal cells of Col-0, an Arabidopsis accession susceptible to an adapted PM (Wang et al 2009), but the frequency of EHC formation is much higher in plants challenged with a non-adapted PM (Wen et al 2011), implying that adapted PM pathogen can suppress callose deposition and more effectively break penetration resistance to establish colonization. The frequency of EHC is significantly increased in plants expressing RESISTANCE TO POWDERY MILDEW8 genes (including RPW8.1 and RPW8.2). RPW8.2 activates EHM-based, post-penetration resistance including enhanced EHC formation against adapted PM (Kuhn et al 2016)

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