Dr Phil Carella

Group Leader Advancing Plant Health (APH)

Unravelling the origin, evolutionary history, and diversity of plant immune systems

Since the dawn of plant evolution over 500 million years ago, pathogenic microbes have impacted plant health and survival. While much of our knowledge is centred on evolutionarily young flowering plants, emerging research in non-flowering lineages has provided new insight into the origin and evolution of plant immunity and pathogen virulence. Indeed, many plant pathogenic microbes can infect both non-flowering and flowering plants, which demonstrates that pathogens have evolved robust virulence strategies to overcome diverse host immune systems.

Research in the Carella group focuses on understanding the evolution of plant-microbe interactions from algae-to-angiosperms across full spectrum of plant evolution. In particular, we investigate plant-pathogen interactions in the model liverwort Marchantia polymorpha, a non-vascular/non-seed bryophyte that diverged from the last common ancestor of flowering plants over 450 million years ago. To challenge them, we’ve established pathosystems with broad host range oomycete (Phytophthora sp.) or bacterial (Pseudomonas syringae) pathogens that also infect flowering plants. Taking advantage of both the evolutionary and practical benefits of the Marchantia, our research aims to identify and understand core mechanisms of pathogen virulence and the conserved plant vulnerabilities they exploit. Ultimately, we aim to leverage this knowledge to generate new and broadly deployable protection strategies in plants.

Our research program focuses on two key areas underpinning plant pathogen interactions, plant immunity and pathogen virulence. Below are examples of our recent work on these topics, alongside progress on the diversity of experimental systems for further expansion of our research.

  1. Conservation and functional diversity of plant intracellular immune receptors (NLRs)

Nucleotide-binding domain and leucine-rich repeat (NLR) proteins are a prominent class of intracellular immune receptors in plants. However, our understanding of plant NLR structure and function is limited to the evolutionarily young flowering plant clade. Our group combines computational and experimental approaches to interrogate the extended spectrum of NLRs that are present across divergent plant lineages. We have demonstrated that diverse land plants encode NLRs with structurally and functionally similar N-terminal immune domains that are able to trigger common responses in distantly related land plants (Chia et al. 2024). We are particularly interested in understanding how NLRs evolved to detect pathogens across the full spectrum of plant evolution and beyond. We are continuing efforts to identify and interrogate diverse NLRs to understand their evolutionary history alongside structural and functional diversity.

Manuscript DOI: https://doi.org/10.1093/plcell/koae113

2. Necrotizing toxins enable broad host virulence of Pseudomonas syringae

We’ve taken a comparative evolutionary approach to understand how the bacterial pathogen Pseudomonas syringae infects distantly related plants. By screening diverse P. syringae pathovars, we identified broad host range isolates causing significant disease in the liverwort Marchantia polymorpha, the fern Ceratopteris richardii, and the flowering plant Nicotiana benthamiana. Broad host P. syringae belonging to the phylogroup 2 clade of the Psy species complex are particularly virulent in non-flowering plants, relying on a combination of type-III secreted effector proteins and the lipopeptide phytotoxin syringomycin. Further investigation into syringomycin activity demonstrates a role in promoting tissue necrosis that enhances in planta bacterial growth of toxin-deficient strains. Our research reveals a key role for the lipopeptide syringomycin in promoting Pseudomonas colonization, which works in concert with effectors to antagonize an exceptionally wide spectrum of land plants. Further research interrogating the interplay between toxins and effectors is required to understand the highly effective virulence program of broad host P. syringae.

Manuscript DOI: https://doi.org/10.1101/2024.07.17.603760

3. Pioneering molecular plant-microbe interactions in diverse plants

To facilitate the interrogation of key questions in evolutionary molecular plant-microbe interactions (evo-MPMI),we are establishing a diverse range of pathosystems between evolutionarily divergent plant and microbial lineages. In addition to plant-bacterial interactions, we work with oomycete pathogens like the broad host range species Phytophthora palmivora. Our group, alongside others at the JIC and TSL, keep a diverse range of plant-associated microbes that we are exploiting to answer diverse questions in the evo-MPMI field. To complement this approach, we are also beginning to identify pathogens that naturally associate with nonflowering plants to understand the molecular principals underpinning compatibility. We encourage anyone interested in using any of our established pathosystems, or those who are keen on building new pathosystems, to get in touch with us. The more the merrier.

Opportunities: Any funded opportunity to join the lab will be shared widely on social media (X/Twitter) and will be posted on the JIC vacancies page. For those interested in applying for funding through scholarships/fellowships, please e-mail Phil to discuss possibilities.

Training, Development, and Culture: The Carella group is committed to training the next generation of scientists. Interns, project students, and other incoming members at any level are trained and supported in technical, computational, theoretical, communication, and any other relevant skillset required for their success. Our goal is to support the development and career aspirations of every member in our team. We promote an open, engaging, and respectful research environment that both promotes and celebrates the diversity of our team members (much like our efforts/views on plant diversity!).

Selected Publications

See all of Dr Phil Carella's publications