The common symbiosis signaling pathway (CSSP) is a highly conserved signaling cascade in plants that allows them to interact with symbiotic microbes. It corresponds to an ancestral pathway that plants use to interact with arbuscular mycorrhizal fungi (AMF). It is known as "common" because different evolutionary younger symbioses also use this pathway, notably the root nodule symbiosis with nitrogen-fixing rhizobia bacteria. The pathway is activated by both Nod-factor perception (for nodule forming rhizobia), as well as by Myc-factor perception that are released from AMF. The pathway is distinguished from the pathogen recognition pathways, but may have some common receptors involved in both pathogen recognition as well as CSSP. A recent work by Kevin Cope and colleagues showed that ectomycorrhizae (a different type of mycorrhizae) also uses CSSP components such as Myc-factor recognition.

The AMF colonization requires the following chain of events that can be roughly divided into the following steps:

1: Pre-Contact Signaling 2: The CSSP2: A: Perception 2: B: Transmission 2: C: Transcription3: The Accommodation program

Overview of the pathway The common symbiosis signaling pathway occurs within plant root cells. It links the perception of fungal or bacterial signals to plant transcriptional responses required for accommodation of the symbiont via arbuscule or nodule formation.

Myc factors or Nod factors are perceived by LysM receptor-like kinases at the plant plasma membrane, triggering downstream signaling through additional proteins such as SYMRK. The signal is then transduced to the nucleus, where it generates nuclear calcium oscillations via ion channels and nucleoporins. These calcium signals are decoded by the calcium- and calmodulin-dependent protein kinase CCaMK, which activates transcription factors such as CYCLOPS.

CYCLOPS is generally considered the final component of the canonical CSSP. At this point in nodulation or AMF colonisation, downstream responses diverge depending on the symbiosis, with CYCLOPS regulating genes that control the formation of either arbuscules or nodules.

+Rhizobial bacteria and Arbuscular mycorrhizal fungi: two different kinds of symbionts elicit a similar signaling pathway

Pre-Contact Signaling Chemical signaling between plants and symbiotic microorganisms begins prior to physical contact. In arbuscular mycorrhizal symbiosis, host plants synthesize and secrete strigolactones into the rhizosphere, which stimulate hyphal branching and directional growth of fungi towards the root.

Strigolactones are carotenoid-derived signalling molecules that have a conserved tricyclic lactone structure also known as ABC rings. Strigolactone biosynthesis occurs mainly in plastids, through the action of enzymes including D27 (Rice DWARF 27; Arabidopsis ortholog ATD27), an iron-binding beta-carotene isomerase, and carotenoid cleavage dioxygenases (CCD7 and CCD8).

In addition to strigolactones, other signaling molecules contribute to pre-contact communication in AMF symbiosis. The transporter protein NOPE1 ('NO PERCEPTION 1') is also required for AMF colonisation in rice and maize, and appears to function as part of a parallel signaling mechanism. NOPE1 is a member of the major facilitator superfamily of transport proteins. It imports N-acetylglucosamine (GlcNAc), a fungal-derived molecule, into plant cells, allowing them to detect the presence of nearby fungi. NOPE1 is involved in the production of root exudates that induce fungal transcription, but whether it directly exports signaling molecules or acts indirectly via GlcNAc uptake and downstream signaling remains unresolved.

Internal plant signaling pathways upstream of the CSSP are also important for symbiosis. D14L/KAI2 is an α/β-hydrolase receptor which perceives endogenous karrikin-like molecules (KLs). KLs, associated with phosphate starvation responses, trigger D14L and D3-mediated degradation of SMAX1. Removal of SMAX1 derepresses genes required for the CSSP, including the LysM receptor-like kinases (RLKs) that detect the fungal/bacterial signal and initiate the CSSP.

Pre-contact signaling ultimately enables the perception of fungal or bacterial signals by plant receptor-like kinases, leading to activation of the common symbiosis signaling pathway.

Perception

There are two main type of root symbiosis; one is root nodule symbiosis by Rhizobia (RN-type) and another is Arbuscular Mycorrhiza (AM-type). There are common genes involved in between these two pathways. these key common components, form the Common Symbiosis pathway (CSP or CSSP). It has been proposed that, RN symbiosis has originated from AM symbiosis. The perception of the presence of the fungal symbiont takes place mainly through fungal chemical secretions generally termed as Myc-factors. Receptors for Myc-factors are yet to be identified. However, DMI2/SYMRK probably acts as a co-receptor of Myc factor receptor (MFR). The AM fungal secreted materials relevant to symbiosis are Myc-LCOs, Myc-COs, N-Acetylglucosamine

{| class="wikitable" |+ Fungal Myc-factors and the plant protein they act on |- ! Myc factor!! Plant protein it mainly act on |- | Myc-LCOs || LYS11 in Lotus japonicus |- | Short chain chitin oligomers (COs) || OsCERK1 and OsCEBiP in rice |- | N-acetylglucosamine || NOPE-1 in maize

Fungal Molecules that triggers CSSP

Myc-LCOs (lipochitooligosaccharides) Like Rhizobial LCOs (Nod factors); Myc-LCOs play important role in perception stage. They are a kind of secreted compounds from AM fungi, mainly mixtures of lipo-chito-oligosaccharides (Myc-LCOs). In Lotus japonicus, LYS11, a receptor for LCOs, was expressed in root cortex cells associated with intra-radical colonizing arbuscular mycorrhizal fungi

Short chain chitin oligomers (Myc-COs) AM host plants show symbiotic-activated calcium waves upon exposure to short chain chitin oligomers. It has been reported that production of these molecules by the AM fungus Rhizophagus irregularis, is strongly stimulated upon exposure to strigolactones. This suggests that plants secrete strigolactones and in response, the fungus increases short chain chitin oligomers, which in turns elicits the plant response to accommodate the fungus. The lysine motif domain of OsCERK1 and OsCEBiP is thought to be involved in the perception of short chain chitin oligomers.

N-Acetylglucosamine NOPE-1 is transporter (described above). NOPE-1 also shows a strong N-acetylglucosamine uptake activity, and is thought to be associated with recognition of presence of fungal symbiont.

Some plant proteins are suspected to recognise Myc-factors, and the rice OsCERK1 Lysin motif (LysM) receptor-like kinase, is one of them.

Cell Surface Receptors

There are multiple families of pattern recognition receptors and co-receptors involved in recognition of microbial pathogens and symbionts. Some of the relevant families involved in CSSP, are Membrane bound LysMs (LYM), Soluble LysM Receptor like Protein, LYK (LysM receptors with active Kinase domain), LYR (LysM proteins with inactive kinase domain), etc.

Seemingly, different combinations of a LYK and LYR receptors perceive and generate differential signals, such as some combinations generate a pathogen recognition signal whereas some combinations generate symbiotic signals.

Receptor-like Kinases (RLKs) DMI2/ SYMRK is a receptor-like kinase, an important protein in endosymbiosis signal perception, reported in several plants (Mt-DMI2 or Mt-NORK in Medicago truncatula; Lj-SYMRK in Lotus japonicas; Ps-SYM19 in Pisum sativum; OsSYMRK in Rice). OsSYMRK lacks an N-terminal domain and exclusively regulate AM symbiosis (is not involved in the RN symbiosis). Notably, it has been found that a Nod-factor inducible gene, MtENOD11, is activated in the presence of AMF exudates; little is known about this phenomenon.

LysM receptor-like kinase Lysin Motif (LysM) receptor-like kinase are a subfamily related to membrane bound Receptor-like kinase (RLKs) with an extracellular region consisting of 3 Lysine motifs. They have some important orthologs in different plants, that vary in their function. In some plant species they are involved in AM symbiosis, in others they are not. Tomato (Solanum lycopersicum), a non-legume eudicot, also have a similar LysM receptor, SlLYK10 that Promotes AM symbiosis. There are some co-receptors of Myc-factor receptor viz., OsCEBiP in Rice, a LysM membrane protein can function as a co-receptor of OsCERK1 but it participates in a different pathway.

Most of these kinases are serine/threonine kinases, some are tyrosine kinases. Also, they are type-1 transmembrane proteins, that indicates their N-terminal domain towards the outside of the cell, and the C-terminal domain is towards inside of the cell.

+Important cell surface receptots involved in molecular pattern recognitionMedicago truncatulaLotus japonicusPisum sativum (pea)Prunus persicaArabidopsis thallianaBrassica rapaSolanum lycopersicum (Tomato)Brachypodium distachyonOryza sativa (Rice)Lysine Motif Receptor-Like Kinase and Lysine Motif Receptor like ProteinLYMLYMILYM1PpLYM1AtLYM1 AtLYM3SlLYM1BdLYM1 BdLYM3OsLYP6 OsLYP5, OsLYP4LYMIILYM2PpLYM3 PpLYM2AtLYM2SlLYM3 SlLYM2BdLYM2 BdLYM4OsCEBiP OsLYP3LYRLYR 1LYRIAMtNFP MtLYR1LjNFR5 LjLYS11PpLYR1SlLyk10Bd LYR1OsNFR5LYRIBMtLYR8PpLYR2SlLYK9Bd LYR2LYR 2LIRIIAMtLYR10LjLYS16PpLYR6AtLYK2SlLYK2LYRIIBMtLYR9LjLYS15PpLYR7SlLYK15LYR 3LYRIIIAMtLYR3LjLYS12PpLYR3AtLYK4SlLYK4Bd LYR4OsLYK6LYRIIIBMtLYR2PpLYR4SlLYK7 SlLYK6LYRIIICMtLYR4 MtLYR7LjLYS13 LjLYS14AtLYK5Bd LYR3OsLYK3 OsLYK2, OsLYK4LYR 4LYRIVMtLYR5 MtLYR6LjLYS20PpLYR5LYKLYKILYK1, LYK4, LYK5, LYK6, LYK7, LYK2, LYK3, LYK9, LYK8LjLYS2 LjLYS1, LjNFR1, LjLYS6, LjLYS7PpLYK2 PpLyk1AtLYK1/ AtCERK1SlLYK13 SlLYK1/ SlBti9, SlLYK12, SlLYK11BdLYK1OsCERK1LYKIILYK10LjLYS3/ EPR3PpLYK3 PpLYK4LYKIIPpLYK5AtLYK3SlLYK3BdLYK3Receptor like KinaseRLKMt-DMI2/ Mt-NORKLj-SYMRKPs-SYM19OsSYMRK

Transmission

The transmission of signal cascades into the nucleus is not well understood. However, this transmission includes carrying the message up to the nuclear membrane and generation of a calcium wave.3. MacLean AM, Bravo A, Harrison MJ. Plant signaling and metabolic pathways enabling arbuscularmycorrhizal symbiosis. The Plant Cell. 2017; 29(10):2319-2335. https://doi.org/10.1105/tpc.17.00555 Some elements involved in this process are:

Nucleoporins Lotus japonicus Nucleoporins LjNUP85 and LjNUP133 has potential role in transmission of the signal. Lj-NENA is another important nucleoporin that plays role in AM symbiosis.

HMGR and Mevalonate.  It has been proposed that the enzyme 3-hydroxy-3-methylglutaryl-CoA reductase (HMG CoA reductase or HMGR) has potential role in the transmission stage. The enzyme is activated by SYMRK/DMI2, and forms mevalonate. This mevalonate acts as a second messenger, and activates a nuclear potassium channel, DMI1 or POLLUX. +Important nuclear cation channels identified to be involved in C S S PNuclear envelope ProteinFunctionRiceLotus japonicusMedicago truncatulaPisumCNGC15Cyclic-nucleotide gated Calcium-channelMt-CNGC15CastorPotassium cation channelOs-CastorLj-CastorPOLLUX or DMI1Potassium cation channelOsPOLLUXLjPOLLUXMt-DMI1Ps-SYM8

Nuclear membrane cation channels.  The nuclear calcium channel CNGC15, which is cyclic nucleotide gated ion channel; mediates the symbiotic nuclear Ca2+ influx, and it is countered by K+ efflux by DMI1.

Transcription +Some component of signalling cascade involved in transcription stage of the common symbiosis signalling ProteinFunctionName of the PlantRiceLotus japonicusMedicago TruncatulaPisum sativumCCamKCalcium calmodulin-dependent kinase with role in AMF symbiosisOs-DMI3 or

Os-CCaMKLj-CCaMKMt-DMI3Ps-SYM9CYCLOPSCoiled coil domain containing proteins that respond to CCamK and promote AMF symbiosisOs-CYCLOPSLj-CYCLOPSMt-IPD3Ps-SYM33DELLAPromote AMF symbiosisOs-SLR1 Mt-DELLA1

Mt-DELLA2Ps-LA

Ps-CRY