Modulation of the Hormone Setting byRhodococcus fasciansResults in EctopicKNOXActivation in Arabidopsis    

Abstract

The biotrophic actinomycete Rhodococcus fascians has a profound impact on plant development and a common aspect of the symptomatology is the deformation of infected leaves. In Arabidopsis (Arabidopsis thaliana), the serrated leaf margins formed upon infection resemble the leaf phenotype of transgenic plants with ectopic expression of KNOTTED-like homeobox (KNOX) genes. Through transcript profiling, we demonstrate that class-I KNOX genes are transcribed in symptomatic leaves. Functional analysis revealed that BREVIPEDICELLUS/KNOTTED-LIKE1 and mainly SHOOT MERISTEMLESS were essential for the observed leaf dissection. However, these results also positioned the KNOX genes downstream in the signaling cascade triggered by R. fascians infection. The much faster activation of ARABIDOPSIS RESPONSE REGULATOR5 and the establishment of homeostatic and feedback mechanisms to control cytokinin (CK) levels support the overrepresentation of this hormone in infected plants due to the secretion by the pathogen, thereby placing the CK response high up in the cascade. Hormone measurements show a net decrease of tested CKs, indicating either that secretion by the bacterium and degradation by the plant are in balance, or, as suggested by the strong reaction of 35S:CKX plants, that other CKs are at play. At early time points of the interaction, activation of gibberellin 2-oxidase presumably installs a local hormonal setting favorable for meristematic activity that provokes leaf serrations. The results are discussed in the context of symptom development, evasion of plant defense, and the establishment of a specific niche by R. fascians.

Eternal Youth, the Fate of Developing Arabidopsis Leaves uponRhodococcus fasciansInfection

“…Interestingly, the number of cells with an 8C content decreased over time and was finally half that of the controls, suggesting that the R. fascians signals can still interfere with endoreduplication in the cycd3;1-3 mutant plants. The intermediate response of cycd3;1-3 plants to R. fascians infection could also be demonstrated at the molecular level by assessing the expression of marker genes (Depuydt et al, 2008). In agreement with the absence of leaf margin serrations, no ectopic expression of SHOOT MERISTEMLESS (STM), a meristem-associated class I KNOX gene, could be observed (Table I), but cytokinin signaling was still activated, as indicated by enhanced ARABIDOPSIS RESPONSE REGULATOR5 (ARR5) expression.…”

“…The latter is accomplished by ectopic expression of meristem-associated class I KNOX genes, but the cause for the strongly reduced leaf expansion had not been addressed (Depuydt et al, 2008). Here, we determined that the small lamina size is caused by an almost 5-fold reduction in cell size that could not be compensated for by the 2-to 3-fold increase in cell number.…”

“…Hence, four different stages in leaf development were considered: outgrowing primordia and young, expanding, and mature leaves. For leaves 5 and 6, no significant differences between the two conditions were measured, which was anticipated because of the lack of morphological alterations in these leaves (Depuydt et al, 2008). In leaf 7, the increase in cells with an 8C content started later upon D188 infection, suggesting a delay in the endoreduplication onset that possibly correlated with the moderate leaf phenotype (Fig.…”

“…Typically, infection of Arabidopsis plants with the wild-type R. fascians strain D188 generates symptomatic leaves with small and narrow leaf blades and strongly serrated margins (Depuydt et al, 2008). To evaluate the leaf phenotype in greater detail, the youngest nonsymptomatic leaf (leaf 7) was compared with the first symptomatic leaf (leaf 8) of plants that were infected at developmental stage 1.05, when five leaves are visible (Boyes et al, 2001).…”

Bacterial and Plant Signal Integration via D3-Type Cyclins Enhances Symptom Development in the Arabidopsis-Rhodococcus fasciansInteraction

“…In Arabidopsis (Arabidopsis thaliana), a model plant adopted to study the molecular basis of this pathosystem, these cytokinins are perceived by the cytokinin receptors ARABI-DOPSIS HISTIDINE KINASE3 (AHK3) and AHK4. Transduction of these signals triggers mitotic cell divisions by stimulating CYCLIN D3 (CYCD3) expression, which inhibits tissue maturation and, ultimately, establishes a nutrient-rich niche (Depuydt et al, 2008a(Depuydt et al, , 2009aPertry et al, 2009). Although the quantity of secreted cytokinins is low, the impact of infection on plant development is severe.…”