Plant-Microbe Symbiosis

The Arbuscular Mycorrhizal (AM) symbiosis is a ubiquitous relationship established in terrestrial ecosystems between the roots of most plants and fungi of the Glomeromycota. AM fungi occur amongst many other inhabitants of the soil, and successful development of AM symbioses relies on a pre-symbiotic signal exchange that allows mutual recognition and reprogramming for the anticipated physical interaction. The nature of some of the signals has been discovered in recent years, providing a first insight into the type of chemical language spoken between the two symbiotic partners. Importantly, these discoveries suggest that the dialogue is complex and that additional factors and corresponding receptors remain to be unveiled. Here, we explore the latest advances in this pre-symbiotic plant–fungal signal exchange and present the resulting current understanding of rhizosphere communication in AM symbioses.

Receptor(-like) kinases with Lysin Motif (LysM) domains in their extracellular region play crucial roles during plant interactions with microorganisms; e.g. Arabidopsis thaliana CERK1 activates innate immunity upon perception of fungal chitin/chitooligosaccharides, whereas Medicago truncatula NFP and LYK3 mediate signalling upon perception of bacterial lipo-chitooligosaccharides, termed Nod factors, during the establishment of mutualism with nitrogen-fixing rhizobia. However, little is still known about the exact activation and signalling mechanisms of MtNFP and MtLYK3. We aimed at investigating putative molecular interactions of MtNFP and MtLYK3 produced in Nicotiana benthamiana. Surprisingly, heterologous co-production of these proteins resulted in an induction of defence-like responses, which included defence-related gene expression, accumulation of phenolic compounds, and cell death. Similar defence-like responses were observed upon production of AtCERK1 in N. benthamiana leaves. Production of either MtNFP or MtLYK3 alone or their co-production with other unrelated receptor(-like) kinases did not induce cell death in N. benthamiana, indicating that a functional interaction between these LysM receptor-like kinases is required for triggering this response. Importantly, structure-function studies revealed that the MtNFP intracellular region, specific features of the MtLYK3 intracellular region (including several putative phosphorylation sites), and MtLYK3 and AtCERK1 kinase activity were indispensable for cell death induction, thereby mimicking the structural requirements of nodulation or chitin-induced signalling. The observed similarity of N. benthamiana response to MtNFP and MtLYK3 co-production and AtCERK1 production suggests the existence of parallels between Nod factor-induced and chitin-induced signalling mediated by the respective LysM receptor(-like) kinases. Notably, the conserved structural requirements for MtNFP and MtLYK3 biological activity in M. truncatula (nodulation) and in N. benthamiana (cell death induction) indicates the relevance of the latter system for studies on these, and potentially other symbiotic LysM receptor-like kinases.

Plants constantly engage in interactions with microbial organisms. These interactions can either be detrimental such as those with the economically relevant fungus-like oomycete Phytophthora infestans, the causal agent of the Irish Potato Famine or beneficial to supply phosphate such as in symbiotic interactions with mycorrhizal fungi that occur in most plant species.

Both, pathogenic and mutualistic symbioses follow structurally similar developmental processes to establish intracellular interfaces. It is generally accepted that both, plants and microorganisms contribute to the formation of dedicated accommodation structures. However, we know little about the underlying molecular mechanisms that drive differentiation of host cells and tissues to form intracellular interfaces. 

The Schornack group aims to characterize the extent to which beneficial and detrimental microorganisms employ similar plant developmental processes for colonization. To this end we plan to assess the overlap between Mycorrhiza processes and root infection by the biotrophic pathogenPhytophthora palmivora and will characterize genetic elements with common functions. Furthermore, we will elucidate the role of microbial effectors for development of plant cells into intracellular accommodation structures. This work will reveal the boundaries between symbiosis and pathogenesis and will provide novel insights into plant development driven by biotic cues.

The vast majority of vascular plants are capable of forming
an arbuscular mycorrhizal symbiosis, and only 18% cannot
(Brundrett 2009). It is widely accepted that all ancestors
of vascular plant species were arbuscular mycorrhizal
(Pirozynski & Malloch 1975; Wang et al. 2010). Nonmycorrhizal
species presumably lost or suppressed their
ability to establish an arbuscular mycorrhizal symbiosis
because its benefits did not outweigh its costs, but the mechanism
explaining a high cost to benefit relationship may have
been very different in distant plant lineages, as explored
below.

Only species belonging to the Fabid clade, limited to four classes and ten families of Angiosperms, are able to form nitrogen-fixing root nodule symbioses (RNS) with soil bacteria. This concerns plants of the legume family (Fabaceae) and Parasponia (Cannabaceae)associated with the Gram-negative proteobacteria collectively called rhizobia and actinorhizal plants associated with the Gram-positive actinomycetes of the genus Frankia. Calcium and calmodulin-dependent protein kinase (CCaMK) is a key component of the common signaling pathway leading to both rhizobial and arbuscular mycorrhizal symbioses (AM) and plays a central role in cross-signaling between root nodule organogenesis and infection processes. Here, we show that CCaMK is also needed for successful actinorhiza formation and interaction with AM fungi in the actinorhizal tree Casuarina glauca and is also able to restore both nodulation and AM symbioses in a Medicago truncatula ccamk mutant. Besides, we expressed auto-active CgCCaMK lacking the auto-inhibitory/CaM domain in two actinorhizal species: C. glauca (Casuarinaceae), which develops an intracellular infection pathway, andDiscaria trinervis (Rhamnaceae) which is characterized by an ancestral intercellular infection mechanism. In both species, we found induction of nodulation independent of Frankia similar to response to the activation of CCaMK in the rhizobia-legume symbiosis and conclude that the regulation of actinorhiza organogenesis is conserved regardless of the infection mode. It has been suggested that rhizobial and actinorhizal symbioses originated from a common ancestor with several independent evolutionary origins. Our findings are consistent with the recruitment of a similar genetic pathway governing rhizobial and Frankia nodule organogenesis.

A new study has demonstrated that plants can use an underground network of fungi to warn each other about incoming insect attacks.