In the course of evolution, plants have developed powerful strategies to evade nutrient deficiencies, such as Arbuscular mycorrhiza (AM) with phosphate-acquiring fungi and root nodule symbioses with diazotrophic bacteria. Intriguingly, both plant root symbioses rely on a shared genetic toolkit consequently named common symbiosis genes.^1-3 Lysin motif receptor kinases perceive microbe-derived factors at the plasma membrane and activate downstream signaling involving the common symbiosis gene products.^4-8 The malectin-like domain leucine-rich repeat receptor kinase SYMRK constitutes the entry point of common symbiosis signaling, which results in the activation of rhythmic calcium oscillations in and around the nuclear envelop. Subsequently, Calcium and Calmodulin dependent kinase CCaMK and its phosphorylation target and transcriptional activator CYCLOPS decode the symbiotic calcium signatures and induces the expression of symbiosis-related genes.^9-11

However, the signaling events that take place between the plasma membrane and the nucleus are completely obscure. It is our long-term goal to identify and characterize the processes and players that transduce symbiont perception at the plasma membrane via the cytosol to the nucleus and balance symbiosis signaling with general nutrient homeostasis, finally resulting in the establishment of a fully compatible plant-microbe symbiosis.

References:

1. Kistner, C. et al. Seven Lotus japonicus Genes Required for Transcriptional Reprogramming of the Root during Fungal and Bacterial Symbiosis, Plant Cell. (2005).

2. Gutjahr, C. et al. Arbuscular Mycorrhiza-Specific Signaling in Rice Transcends the Common Symbiosis Signaling Pathway, Plant Cell. (2008).

3. Delaux, P.M. et al. Evolution of the plant-microbe symbiotic “toolkit,” Trends Plant Sci. (2013).

4. Radutoiu, S. et al. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature. (2003).

5. Madsen, E.B. et al. A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature. (2003).

6. Maillet, F. et al. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature. (2011).

7. Broghammer, A. et al. Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding. Proc. Natl. Acad. Sci. (2012).

8. Genre, A. et al. Short-chain chitin oligomers from arbuscular mycorrhizal fungi trigger nuclear Ca2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytol. (2013).

9. Lévy, J. et al. A Putative Ca2+and Calmodulin-Dependent Protein Kinase Required for Bacterial and Fungal Symbioses. Science. (2004).

10. Yano, K. et al. CYCLOPS, a mediator of symbiotic intracellular accommodation. Proc. Natl. Acad. Sci. (2008).

11. Singh, S. et al. A DNA-binding transcriptional activator, orchestrates symbiotic root nodule development. Cell Host Microbe. (2014).

The malectin-like domain leucine-rich repeat receptor kinase (MLD-LRR-RK) SYMRK belongs to the LRR-I family of receptor kinases and is a key component in the successful establishment of plant root symbioses.^1-3 SYMRK is subjected to proteolytic cleavage in planta giving rise to a free MLD and a truncated and highly-unstable receptor protein, which preferentially interacts with NFR5.⁴ Overabundance of SYMRK results in the spontaneous activation of symbiosis signaling in the absence of rhizobia.⁵ Release of the MLD as well as phosphorylation in the kinase domain are crucial for proper symbiotic development in the epidermis but not in the cortex.^6-7 Taken together, these data imply a complex regulation of MLD-LRR-RKs to fine-tune receptor activation and signal attenuation. Intriguingly, MLD-LRR-RKs are not only implicated in the accommodation of beneficial microbes (SYMRK; Lotus japonicus). In Arabidopsis thaliana, SYMRK homologous receptor kinase 1 (ShRK1) and ShRK2 support the reproductive success of the obligate biotrophic oomycete Hyaloperonospora arabidopsidis (Hpa) and contribute to a proper development of the oomycete within plant cells.⁸

However, it is unknown how ShRKs impact the Arabidopsis-Hpa interaction and the underlying signaling events remain elusive. It is our long-term goal to illuminate the mechanistic details of ShRK signaling in plant-microbe interactions.

References:

1. Stracke, S. et al. A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature (2002).

2. Markmann, K., Giczey, G. & Parniske, M. Functional adaptation of a plant receptor-kinase paved the way for the evolution of intracellular root symbioses with bacteria. PLoS Biol. (2008).

3. Gherbi, H. et al. SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankiabacteria. Proc. Natl. Acad. Sci. (2008).

4. Antolín-Llovera, M., Ried, M. K. & Parniske, M. Cleavage of the symbiosis receptor-like kinase ectodomain promotes complex formation with nod factor receptor 5. Curr. Biol. (2014).

5. Ried, M. K., Antolín-Llovera, M. & Parniske, M. Spontaneous symbiotic reprogramming of plant roots triggered by receptor-like kinases. Elife. (2014).

6. Kosuta, S. et al. Lotus japonicus symRK-14 uncouples the cortical and epidermal symbiotic program. Plant J. (2011).

7. Saha, S. et al. Gatekeeper Tyrosine Phosphorylation of SYMRK Is Essential for Synchronizing the Epidermal and Cortical Responses in Root Nodule Symbiosis. Plant Physiol. (2016).

8. Ried, M. K. et al. A set of Arabidopsis genes involved in the accommodation of the downy mildew pathogen Hyaloperonospora arabidopsidis. PLoS Pathog. (2019).