Eternal Youth, the Fate of Developing Arabidopsis Leaves uponRhodococcus fasciansInfection      

Abstract

The phytopathogenic actinomycete Rhodococcus fascians induces neoplastic shooty outgrowths on infected hosts. Upon R. fascians infection of Arabidopsis (Arabidopsis thaliana), leaves are formed with small narrow lamina and serrated margins. These symptomatic leaves exhibit reduced tissue differentiation, display more but smaller cells that do not endoreduplicate, and accumulate in the G1 phase of the cell cycle. Together, these features imply that leaf growth occurs primarily through mitotic cell division and not via cell expansion. Molecular analysis revealed that cell cycle gene expression is activated continuously throughout symptomatic leaf development, ensuring persistent mitotic cycling and inhibition of cell cycle exit. The transition at the two major cell cycle checkpoints is stimulated as a direct consequence of the R. fascians signals. The extremely reduced phenotypical response of a cyclind3;1-3 triple knockout mutant indicates that the D-type cyclin/retinoblastoma/E2F transcription factor pathway, as a major mediator of cell growth and cell cycle progression, plays a key role in symptom development and is instrumental for the sustained G1-to-S and G2-to-M transitions during symptomatic leaf growth.

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

“…Previously, the induction of CDKB1;1 and ARR5 had been shown to be approximately 10-and 6-fold lower, respectively, upon infection of the cycd3;1-3 mutant than that of wild-type plants (Depuydt et al, 2009a). Based on these results and our findings here, we postulated a loop-shaped pathway in which the bacterial cytokinins are necessary for the activation of both CYCD3 expression and Put production.…”

“…S2) place the action of Put during the interaction with R. fascians downstream of cytokinin perception. In the current model of R. fascians-induced signal transduction, CYCD3;1 is a primary target of the bacterial cytokinins (Depuydt et al, 2009a). However, the data presented above show that CYCD3;1 expression is also induced by Put, thus positioning Put action upstream or in a parallel pathway of CYCD3;1.…”

“…To confirm this finding, we analyzed the polyamine response of the cycd3;1-3 triple knockout mutant (Dewitte et al, 2007). This mutant is much less responsive to R. fascians because of the disruption of mitotic cell divisions in response to the bacterial cytokinins (Depuydt et al, 2009a). As in wild-type plants, in D188-infected cycd3;1-3 tissues, free and conjugated Put accumulated at 7 and 14 dpi (Fig.…”

“…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.…”

“…In a complementary pharmacological approach, plants were treated either with polyamine biosynthesis inhibitors or with Put prior to infection. To position polyamines within the signal transduction cascade triggered by R. fascians, we identified the bacterial signal responsible for the increased polyamine production and evaluated the polyamine and molecular response of the double cytokinin receptor mutant ahk3ahk4 that is not responsive to R. fascians infection (Pertry et al, 2009) and of the triple CYCD3 mutant cycd3;1-3 that exhibits strongly reduced symptom development (Depuydt et al, 2009a). Based on our data, we propose a model on the mode of action of polyamines in regular and pathological plant development.…”