Abstract
Compatibility between plants and obligate biotrophic fungi requires fungal mechanisms for efficiently obtaining nutrients and counteracting plant defenses under conditions that are expected to induce changes in the host transcriptome. A key step in the proliferation of biotrophic fungi is haustorium differentiation. Here we analyzed global gene expression patterns in Arabidopsis thaliana leaves during the formation of haustoria by Golovinomyces cichoracearum. At this time, the endogenous levels of salicylic acid (SA) and jasmonic acid (JA) were found to be enhanced. The responses of wild-type, npr1-1, and jar1-1 plants were used to categorize the sensitivity of gene expression changes to NPR1 and JAR1, which are components of the SA and JA signaling pathways, respectively. We found that the infection process was the major source of variation, with 70 genes identified as having similarly altered expression patterns regardless of plant genotype. In addition, principal component analysis (PCA) identified genes responding both to infection and to lack of functional JAR1 (17 genes) or NPR1 (18 genes), indicating that the JA and SA signaling pathways function as secondary sources of variation. Participation of these genes in the SA or JA pathways had not been described previously. We found that some of these genes may be sensitive to the balance between the SA and JA pathways, representing novel markers for the elucidation of cross-talk points between these signaling cascades. Conserved putative regulatory motifs were found in the promoter regions of each subset of genes. Collectively, our results indicate that gene expression changes in response to infection by obligate biotrophic fungi may support fungal nutrition by promoting alterations in host metabolism. In addition, these studies provide novel markers for the characterization of defense pathways and susceptibility features under this infection condition.
Highlights
Obligate fungal biotrophs must establish compatible interactions with their hosts in order to survive
Experimental system We used microarray analysis to characterize global transcriptional changes occurring in Arabidopsis leaf tissues infected with G. cichoracearum at early stages of haustorium formation
To test the impact of NPR1- and JAR1-defense signaling pathways at this infection step, we examined gene expression changes in wild-type, npr1-1 and jar1-1 plants treated with the virulent fungal isolate UCSC1 (Adam et al, 1999)
Summary
Obligate fungal biotrophs must establish compatible interactions with their hosts in order to survive These organisms have evolved unique strategies to extract nutrients from infected living cells, including the assembly of specialized structures located in intimate contact with host cells. High-throughput transcriptome analyses have helped define the responses triggered in plant tissues upon recognition of these fungal pathogens These studies were performed under conditions promoting activation of defenses involving either host resistance (Euglem et al, 2004; Caldo et al, 2004; Eckey et al, 2004; Zierold et al, 2005; Michel et al, 2006) or non-host resistance (Zimmerli et al, 2004, Bruggmann et al, 2005). Except for these reports, few studies have examined plant defense programs and global host metabolic features leading to the establishment of compatibility
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