Clavibacter michiganensis Downregulates Photosynthesis and Modifies Monolignols Metabolism Revealing a Crosstalk with Tomato Immune Responses

Abstract

The gram-positive pathogenic bacterium Clavibacter michiganensis subsp. michiganensis (Cmm) causes bacterial canker disease in tomato, affecting crop yield and fruit quality. To understand how tomato plants respond, the dynamic expression profile of host genes was analyzed upon Cmm infection. Symptoms of bacterial canker became evident from the third day. As the disease progressed, the bacterial population increased in planta, reaching the highest level at six days and remained constant till the twelfth day post inoculation. These two time points were selected for transcriptomics. A progressive down-regulation of key genes encoding for components of the photosynthetic apparatus was observed. Two temporally separated defense responses were observed, which were to an extent interdependent. During the primary response, genes of the phenylpropanoid pathway were diverted towards the synthesis of monolignols away from S-lignin. In dicots, lignin polymers mainly consist of G- and S-units, playing an important role in defense. The twist towards G-lignin enrichment is consistent with previous findings, highlighting a response to generate an early protective barrier and to achieve a tight interplay between lignin recomposition and the primary defense response mechanism. Upon progression of Cmm infection, the temporal deactivation of phenylpropanoids coincided with the upregulation of genes that belong in a secondary response mechanism, supporting an elegant reprogramming of the host transcriptome to establish a robust defense apparatus and suppress pathogen invasion. This high-throughput analysis reveals a dynamic reorganization of plant defense mechanisms upon bacterial infection to implement an array of barriers preventing pathogen invasion and spread.

Transcriptome analysis of tomato plants following salicylic acid-induced immunity against <i>Clavibacter michiganensis</i> ssp. <i>michiganensis</i>

“…A total of 346 and 525 genes were downregulated after SA treatment and Cmm infection, respectively, with only 65 genes being commonly repressed after both interventions (Figure 1A). Previous studies have reported that Cmm infection suppresses photosynthesis-related gene expression in tomato, which may be associated with immunity (Tsitsekian et al 2021;Yokotani et al 2021), consistent with the results of the present study. However, the results of GO and KEGG enrichment analyses indicated that SA is not involved in the repression of photosynthesis-related gene expression (Supplementary Table S4).…”

“…Increased expression of PR, RLK, and ethylene synthesis genes has been observed in tomato stems after Cmm infection (Balaji et al 2008). In contrast, decreased expression of photosynthesis-related genes after Cmm infection in tomato stems has been shown to be potentially associated with immunity (Tsitsekian et al 2021). Transcriptome comparisons between resistant and susceptible tomato species have identified a number of candidate genes involved in immunity (Basim et al 2021;Lara-Ávila et al 2012).…”

A subset of highly responsive transcription factors upon tomato infection by pepino mosaic virus

“…Quantitative gene expression analysis was performed using gene‐specific primers (Table S1) with a PikoReal 96 Real‐Time PCR System (Thermo Fisher Scientific) using the SYBR Select Master Mix (Applied Biosystems, Waltham, MA, USA). For RT‐qPCR analysis, glyceraldehyde‐3‐phosphate dehydrogenase ( GAPDH ) was chosen as housekeeping gene and control plants were used as internal calibrators (Tsitsekian et al ., 2021). Quantification of gene expression was calculated as expression of the gene of interest relative to GAPDH expression based on the 2 −ΔCt method as previously described (Tsitsekian et al ., 2021).…”

“…For RT‐qPCR analysis, glyceraldehyde‐3‐phosphate dehydrogenase ( GAPDH ) was chosen as housekeeping gene and control plants were used as internal calibrators (Tsitsekian et al ., 2021). Quantification of gene expression was calculated as expression of the gene of interest relative to GAPDH expression based on the 2 −ΔCt method as previously described (Tsitsekian et al ., 2021). The fold change was similarly calculated with the 2 −ΔΔCt method (Ioannidi et al ., 2016).…”

Eceriferum Genes in Tomato (Solanum lycopersicum): Genome-Wide Identification and Expression Analysis Reveal Their Potential Functions during Domestication

“…In order to explore SlCERs' expression patterns under abiotic/biotic stresses, we downloaded the transcriptome sequencing data of tomato under stresses of drought, heat, salt, pathogenic bacteria [59,60] and parasitic plant [61] on the NCBI website (https://www. ncbi.nlm.nih.gov/).…”