A receptor required for chitin perception facilitates arbuscular mycorrhizal associations and distinguishes root symbiosis from immunity.

Plants establish symbiotic associations with arbuscular mycorrhizal fungi (AMF) to facilitate nutrient uptake, particularly in nutrient-limited conditions. This partnership is rooted in the plant's ability to recognize fungal signaling molecules, such as chitooligosaccharides (chitin) and lipo-chitooligosaccharides. In the legume Medicago truncatula, chitooligosaccharides trigger both symbiotic and immune responses via the same lysin-motif-receptor-like kinases (LysM-RLKs), notably CERK1 and LYR4. The nature of plant-fungal engagement is opposite according to the outcomes of immunity or symbiosis signaling, and as such, discrimination is necessary, which is challenged by the dual roles of CERK1/LYR4 in both processes. Here, we describe a LysM-RLK, LYK8, that is functionally redundant with CERK1 for mycorrhizal colonization but is not involved in chitooligosaccharides-induced immunity. Genetic mutation of both LYK8 and CERK1 blocks chitooligosaccharides-triggered symbiosis signaling, as well as mycorrhizal colonization, but shows no further impact on immunity signaling triggered by chitooligosaccharides, compared with the mutation of CERK1 alone. LYK8 interacts with CERK1 and forms a receptor complex that appears essential for chitooligosaccharides activation of symbiosis signaling, with the lyk8/cerk1 double mutant recapitulating the impact of mutations in the symbiosis signaling pathway. We conclude that this novel receptor complex allows chitooligosaccharides activation specifically of symbiosis signaling and helps the plant to differentiate between activation of these opposing signaling processes.

Nutrient regulation of lipochitooligosaccharide recognition in plants via NSP1 and NSP2.

Many plants associate with arbuscular mycorrhizal fungi for nutrient acquisition, while legumes also associate with nitrogen-fixing rhizobial bacteria. Both associations rely on symbiosis signaling and here we show that cereals can perceive lipochitooligosaccharides (LCOs) for activation of symbiosis signaling, surprisingly including Nod factors produced by nitrogen-fixing bacteria. However, legumes show stringent perception of specifically decorated LCOs, that is absent in cereals. LCO perception in plants is activated by nutrient starvation, through transcriptional regulation of Nodulation Signaling Pathway (NSP)1 and NSP2. These transcription factors induce expression of an LCO receptor and act through the control of strigolactone biosynthesis and the karrikin-like receptor DWARF14-LIKE. We conclude that LCO production and perception is coordinately regulated by nutrient starvation to promote engagement with mycorrhizal fungi. Our work has implications for the use of both mycorrhizal and rhizobial associations for sustainable productivity in cereals.

Arbuscular mycorrhizal fungi induce lateral root development in angiosperms via a conserved set of MAMP receptors.

Root systems regulate their branching patterns in response to environmental stimuli. Lateral root development in both monocotyledons and dicotyledons is enhanced in response to inoculation with arbuscular mycorrhizal (AM) fungi, which has been interpreted as a developmental response to specific, symbiosis-activating chitinaceous signals. Here, we report that generic instead of symbiosis-specific, chitin-derived molecules trigger lateral root formation. We demonstrate that this developmental response requires the well-known microbe-associated molecular pattern (MAMP) receptor, Chitin Elicitor Receptor Kinase 1 (CERK1), in rice, Medicago truncatula, and Lotus japonicus, as well as the non-host of AM fungi, Arabidopsis thaliana, lending further support for a broadly conserved signal transduction mechanism across angiosperms. Using rice mutants impaired in strigolactone biosynthesis and signaling, we show that strigolactone signaling is necessary to regulate this developmental response. Rice CERK1 operates together with either Chitin Elicitor Binding Protein (CEBiP) or Nod Factor Receptor 5 (NFR5) in immunity and symbiosis signaling, respectively; for the lateral root response, however, all three LysM receptors are required. Our work, therefore, reveals an overlooked but a conserved role of LysM receptors integrating MAMP perception with developmental responses in plants, an ability that might influence the interaction between roots and the rhizosphere biota.

Receptor-Like Kinases Sustain Symbiotic Scrutiny.

Plant receptor-like kinases (RLKs) control the initiation, development, and maintenance of symbioses with beneficial mycorrhizal fungi and nitrogen-fixing bacteria. Carbohydrate perception activates symbiosis signaling via Lysin-motif RLKs and subsequently the common symbiosis signaling pathway. As the receptors activated are often also immune receptors in multiple species, exactly how carbohydrate identities avoid immune activation and drive symbiotic outcome is still not fully understood. This may involve the coincident detection of additional signaling molecules that provide specificity. Because of the metabolic costs of supporting symbionts, the level of symbiosis development is fine-tuned by a range of local and mobile signals that are activated by various RLKs. Beyond early, precontact symbiotic signaling, signal exchanges ensue throughout infection, nutrient exchange, and turnover of symbiosis. Here, we review the latest understanding of plant symbiosis signaling from the perspective of RLK-mediated pathways.

Mechanisms and Impact of Symbiotic Phosphate Acquisition.

Phosphorous is important for life but often limiting for plants. The symbiotic pathway of phosphate uptake via arbuscular mycorrhizal fungi (AMF) is evolutionarily ancient and today occurs in natural and agricultural ecosystems alike. Plants capable of this symbiosis can obtain up to all of the phosphate from symbiotic fungi, and this offers potential means to develop crops less dependent on unsustainable P fertilizers. Here, we review the mechanisms and insights gleaned from the fine-tuned signal exchanges that orchestrate the intimate mutualistic symbiosis between plants and AMF. As the currency of trade, nutrients have signaling functions beyond being the nutritional goal of mutualism. We propose that such signaling roles and metabolic reprogramming may represent commitments for a mutualistic symbiosis that act across the stages of symbiosis development.

Independent signalling cues underpin arbuscular mycorrhizal symbiosis and large lateral root induction in rice.

Perception of arbuscular mycorrhizal fungi (AMF) triggers distinct plant signalling responses for parallel establishment of symbiosis and induction of lateral root formation. Rice receptor kinase CHITIN ELICITOR RECEPTOR KINASE 1 (CERK1) and α/ß-fold hydrolase DWARF14-LIKE (D14L) are involved in pre-symbiotic fungal perception. After 6 wk post-inoculation with Rhizophagus irregularis, root developmental responses, fungal colonization and transcriptional responses were monitored in two independent cerk1 null mutants; a deletion mutant lacking D14L, and with D14L complemented as well as their respective wild-type cultivars (cv Nipponbare and Nihonmasari). Here we show that although essential for symbiosis, D14L is dispensable for AMF-induced root architectural modulation, which conversely relies on CERK1. Our results demonstrate uncoupling of symbiosis and the symbiotic root developmental signalling during pre-symbiosis with CERK1 required for AMF-induced root architectural changes.