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Utilizing diversity to decipher the role of autophagy in plant-microbe interactions

Periodic Reporting for period 3 - DIVERSIPHAGY (Utilizing diversity to decipher the role of autophagy in plant-microbe interactions)

Période du rapport: 2023-01-01 au 2024-06-30

During the course of evolution, plants have been exposed to a plethora of beneficial and pathogenic microbes. While symbionts are beneficial for the host plant by improving nutrient supply and health, pathogens are reprogramming their host only for their own benefit. At the interface of this interaction proteomes at both sides are highly flexible and require regulated protein turnover. In line with this, our previous work revealed that regulated protein degradation by autophagy is an essential player in plant immunity. Consequently, plant pathogens hijack autophagy during binary interactions though in contrasting manners. However, in a more complete scenario, plants are constantly exposed to different microbes and hence it is crucial to include the microbial diversity into this equation to obtain a holistic picture of the role of autophagy in plant-microbe interactions. The picture is getting even more complex if we look at the cellular diversity on the host side. Thus, DIVERSIPHAGY approaches the role of autophagy through bacterial and cellular diversity on the host side. We aim to address following questions:
• Identifying how the bacterial diversity impacts autophagy and vice versa
• Determining new bacteria and/or bacterial communities hijacking autophagy
• Revealing the autophagy degradome and novel autophagy factors by utilizing autophagy-modulating bacteria
• Identifying tissue and cell-type specific modulation of autophagy by diverse bacteria.
With DIVERSIPHAGY we will reveal the holistic picture of the role of autophagy in plant-microbe interactions using a mixture of state-of-the-art approaches including metabolomics, proteomics, single-cell transcriptomics and cell-type specific reverse genetic screens. As such DIVERSIPHAGY is the next generation approach to understand the role of plant autophagy in plant-microbe interactions and by translating our results into crop plants we will be able to develop more durable resistances toward destructive pathogens.
In the first reporting period we have started to work on all three work packages (WP). In WP1 we have started to characterize the impact of the root microbiome on autophagy using synthetic bacterial communities (SynCom). Preliminary results indicate that SynComs are inducing autophagy early on. We have also measured the composition of SynComs in Arabidopsis thaliana plants (including Col-0 and autophagy deficient mutants) and identified specific bacteria that are either depleted or enriched in different conditions. This indicates that autophagy might be required to maintain a certain composition of the microbiome. In WP2 we have started to characterize various autophagy targets (including RNA-binding proteins, and novel components of autophagy (e.g. a ubiquitin binding protein that acts as a ubiquitin shuttle factor). In a more unbiased approach, we generated an atlas of potential autophagy targets using the nine different isoforms of ATG8 during bacterial infection. The analysis is still ongoing. In WP3 we have started to investigate cell-type specific autophagy responses in the leaves (during infection) and in roots using a single cell RNA-seq approach. First results indicate that different cell types in the shoot as well as in the root respond in a specific manner to autophagy induction. The analysis is still ongoing and currently we are generating marker lines to validate our findings.
We expect to identify novel autophagy targets in WP2 and will validate them using different genetic, cell biological and biochemical methods. Cell-type specific autophagy responses will be evaluated using bacterial infection as well as chemical induction of autophagy in leaves and roots.