LCO Receptors Involved in Arbuscular Mycorrhiza Are Functional for Rhizobia Perception in Legumes.

Bacterial lipo-chitooligosaccharides (LCOs) are key mediators of the nitrogen-fixing root nodule symbiosis (RNS) in legumes. The isolation of LCOs from arbuscular mycorrhizal fungi suggested that LCOs are also signaling molecules in arbuscular mycorrhiza (AM). However, the corresponding plant receptors have remained uncharacterized. Here we show that petunia and tomato mutants in the LysM receptor-like kinases LYK10 are impaired in AM formation. Petunia and tomato LYK10 proteins have a high affinity for LCOs (Kd in the nM range) comparable to that previously reported for a legume LCO receptor essential for the RNS. Interestingly, the tomato and petunia LYK10 promoters, when introduced into a legume, were active in nodules similarly to the promoter of the legume orthologous gene. Moreover, tomato and petunia LYK10 coding sequences restored nodulation in legumes mutated in their orthologs. This combination of genetic and biochemical data clearly pinpoints Solanaceous LYK10 as part of an ancestral LCO perception system involved in AM establishment, which has been directly recruited during evolution of the RNS in legumes.

A set of Arabidopsis genes involved in the accommodation of the downy mildew pathogen Hyaloperonospora arabidopsidis.

The intracellular accommodation structures formed by plant cells to host arbuscular mycorrhiza fungi and biotrophic hyphal pathogens are cytologically similar. Therefore we investigated whether these interactions build on an overlapping genetic framework. In legumes, the malectin-like domain leucine-rich repeat receptor kinase SYMRK, the cation channel POLLUX and members of the nuclear pore NUP107-160 subcomplex are essential for symbiotic signal transduction and arbuscular mycorrhiza development. We identified members of these three groups in Arabidopsis thaliana and explored their impact on the interaction with the oomycete downy mildew pathogen Hyaloperonospora arabidopsidis (Hpa). We report that mutations in the corresponding genes reduced the reproductive success of Hpa as determined by sporangiophore and spore counts. We discovered that a developmental transition of haustorial shape occurred significantly earlier and at higher frequency in the mutants. Analysis of the multiplication of extracellular bacterial pathogens, Hpa-induced cell death or callose accumulation, as well as Hpa- or flg22-induced defence marker gene expression, did not reveal any traces of constitutive or exacerbated defence responses. These findings point towards an overlap between the plant genetic toolboxes involved in the interaction with biotrophic intracellular hyphal symbionts and pathogens in terms of the gene families involved.

Spontaneous symbiotic reprogramming of plant roots triggered by receptor-like kinases.

Symbiosis Receptor-like Kinase (SYMRK) is indispensable for the development of phosphate-acquiring arbuscular mycorrhiza (AM) as well as nitrogen-fixing root nodule symbiosis, but the mechanisms that discriminate between the two distinct symbiotic developmental fates have been enigmatic. In this study, we show that upon ectopic expression, the receptor-like kinase genes Nod Factor Receptor 1 (NFR1), NFR5, and SYMRK initiate spontaneous nodule organogenesis and nodulation-related gene expression in the absence of rhizobia. Furthermore, overexpressed NFR1 or NFR5 associated with endogenous SYMRK in roots of the legume Lotus japonicus. Epistasis tests revealed that the dominant active SYMRK allele initiates signalling independently of either the NFR1 or NFR5 gene and upstream of a set of genes required for the generation or decoding of calcium-spiking in both symbioses. Only SYMRK but not NFR overexpression triggered the expression of AM-related genes, indicating that the receptors play a key role in the decision between AM- or root nodule symbiosis-development.

Like all plants, crop plants need nutrients such as nitrogen and phosphate to grow. Often these essential elements are in short supply, and so millions of tons of fertiliser are applied to agricultural land each year to maintain crop yields. Another way for plants to gain access to scarce nutrients is to form symbiotic relationships with microorganisms that live in the soil. Plants pass on carbon-containing compounds­such as sugars­to the microbes and, in return, certain fungi provide minerals­such as phosphates­to the plants. Some plants called legumes (such as peas, beans, and clovers) can also form relationships with bacteria that convert nitrogen from the air into ammonia, which the plants then use to make molecules such as DNA and proteins. To establish these symbiotic relationships with plants, nitrogen-fixing bacteria release chemical signals that are recognized via receptor proteins, called NFR1 and NFR5, found on the surface of the plant root cells. These signals trigger a cascade of events that ultimately lead to the plant forming an organ called 'root nodule' to house and nourish the nitrogen-fixing bacteria. A similar signalling mechanism is thought to take place during the establishment of symbiotic relationships between plants and certain soil fungi. A plant protein called Symbiosis Receptor-like Kinase (or SYMRK for short) that is also located on the root cell surface is required for both bacteria­plant and fungi­plant associations to occur. However, the exact role of this protein in these processes was unclear. Ried et al. have now investigated this by taking advantage of a property of cell surface receptor proteins: if some of these proteins are made in excessive amounts they activate their signalling cascades even when the initial signal is not present. Ried et al. engineered plants called Lotus japonicus to produce high levels of SYMRK, NFR1, or NFR5. Each of these changes was sufficient to trigger the plants to develop root nodules in the absence of microbes. Genes associated with the activation of the signalling cascade involved the formation of root nodules were also switched on when each of the three proteins was produced in large amounts. In contrast, only an excess of SYMRK could activate genes related to fungi­plant associations. Ried et al. also found that, while SYMRK can function in the absence of the NFRs, NFR1 and NFR5 need each other to function. These data suggest that the receptor proteins play a key role in the decision between the establishment of an association with a bacterium or a fungus. As an excess of symbiotic receptors caused plants to form symbiotic structures, Ried et al. propose that this strategy could be used to persuade plants that usually do not form symbioses with nitrogen-fixing bacteria to do so. If this is possible, it might lead us to engineer crop plants to form symbiotic interactions with nitrogen-fixing bacteria; this would help increase crop yields and enable crops to be grown in nitrogen-poor environments without the addition of extra fertiliser.

Knowing your friends and foes--plant receptor-like kinases as initiators of symbiosis or defence.

The decision between defence and symbiosis signalling in plants involves alternative and modular plasma membrane-localized receptor complexes. A critical step in their activation is ligand-induced homo- or hetero-oligomerization of leucine-rich repeat (LRR)- and/or lysin motif (LysM) receptor-like kinases (RLKs). In defence signalling, receptor complexes form upon binding of pathogen-associated molecular patterns (PAMPs), including the bacterial flagellin-derived peptide flg22, or chitin. Similar mechanisms are likely to operate during the perception of microbial symbiont-derived (lipo)-chitooligosaccharides. The structurally related chitin-oligomer ligands chitooctaose and chitotetraose trigger defence and symbiosis signalling, respectively, and their discrimination involves closely related, if not identical, LysM-RLKs. This illustrates the demand for and the challenges imposed on decision mechanisms that ensure appropriate signal initiation. Appropriate signalling critically depends on abundance and localization of RLKs at the cell surface. This is regulated by internalization, which also provides a mechanism for the removal of activated signalling RLKs. Abundance of the malectin-like domain (MLD)-LRR-RLK Symbiosis Receptor-like Kinase (SYMRK) is additionally controlled by cleavage of its modular ectodomain, which generates a truncated and rapidly degraded RLK fragment. This review explores LRR- and LysM-mediated signalling, the involvement of MLD-LRR-RLKs in symbiosis and defence, and the role of endocytosis in RLK function.