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Common symbiosis signaling pathway

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Common Symbiotic Pathway - a simplified presentation based on McLean, Bravo and Harrison 2017
Common Symbiotic Pathway - a simplified presentation based on McLean, Bravo and Harrison 2017
A LysM Domain
A LysM Domain

The common symbiotic signaling pathway (CSSP) is a signaling cascade in plants that seen to be activated in both NOD-factor perception (for nodule forming rhizobia), as well as found in MYC-factor perception that are released from Arbuscular mycorrhizal fungi. 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 [1] by Kevin Cope and colleagues shown that possibly other type of mycorrhizae may involve the CSSP components such as Myc-factor recognition.

The AMF colonization requires the following chain[2] of events that can be roughly divided into following steps - 1: The Pre-Contact Signaling,

1: The Pre-Contact Signaling,

2: The CSSP

2: A: Perception

2: B: Transmission

2: C: Transcription

3: The Accommodation program

Outline

To accurately recognize the infection thread of a different species of organism, and to establish a mutually beneficial association requires robust signaling.[3] AM fungi are also fatty acid auxotrophs;[4][2] therefore they depend on plant for supply of fatty acid supply.[5]

At the pre-symbiotic signaling; both symbionts release chemical factors in their surroundings so that the partners can find each other.[6]' Plant root exudates play role in complex microbial interaction,[7] by releasing a lot of versatile materials.[7][8][9] among which strigolactone has been identified to facilitate both AMF colonisation and pathogen infection.[8]

It is seen that phosphate starvation in plant induces strigolactone production as well as AMF colonisation.[8] Plants release strigolactone, a class of caroteinoid-based plant hormone which also attracts the fungal symbionts and stimulate the fungal oxidative metabolism and also growth and branching of the fungal partner [2] Strigolactone promotes hyphal branching in germinating AMF spores [9] It plays role in intense ramification of the AMF hyphae at the vicinity of root and then colonization [10]

The common symbiosis signalling pathway is called so because it has common components for fungal symbiosis as well as rhizobial symbiosis. The common signalling pathway probably evolved when the existing pathway for arbuscular mycorrhizae was exploited by rhizobia,.[2][11]

The perception happens when fungal Myc factor is detected by plant. Myc factors are comparable to rhizobial nod factors. The chemical nature of Myc factor has recently been revealed as lipo-chito-oligosaccharide (Myc-LCOs) and chito-oligosaccharides (Myc-COs) that work as symbiotic signal,[10][12][13]

Presence of Strigolactone enhances the production of Myc-CO production by AMF [10]

Myc factor receptor (MFR) is still putative, however However, another protein DMI2 (or SYMRK) that have prominent role in perception process and it is thought to be a co-receptor of MFR. Rice plant probably show a different mechanism using OsCERK1 and OsCEBiP which probably detect chitin oligomers[2][14][15]

The transmission happens when the signal transmitted after detection to the gene expression stage. This process is mediated by two nucleoporins NUP85 and NUP133,[11] Alternatively, another hypothesis says HMG-CoA reductase is activated on perception, which then converts HMG-CoA into mevalonate, this mevalonate acts as a second messenger and activates a nuclear K+ cation channel (DMI-1 or Pollux).[2][16] The transmission stage ends by creating a ‘calcium spike’ into the nucleus [17]

The transcription stage starts when a Calcium and Calmodulin dependent kinase (CCaMK) is activated.[2] then it stimulates a target protein CYCLOPS.[2] CCaMK and CYCLOPS probably forms a complex that along with DELLA protein, regulates the expression of RAM1 (Reduced Arbuscular Mycorrhyza1) gene expression.[2]

The accommodation process is the extensive remodelling of host cortical cells. This includes invagination of host plasmalemma, proliferation of endoplasmic reticulum, golgi apparatus, trans-golgi network and secretary vesicles. Plastids multiply and form “stromules”. Vacuoles also goes through extensive reorganization [11]

The Pre Contact Signaling

Chemical signalling starts prior to two symbionts come into contact. From the host plant's side, it synthesizes and releases a range of caroteinoid based phytohormone, called strigolactones.[2] They have a conserved tricyclic lactone structure also known as ABC rings.[18] Strigolactone biosynthesis occurs mainly in plastid,[19] where D27 (Rice DWARF 27; Arabidopsis ortholog ATD27), an Iron binding beta-carotene isomerase works at upstream of strigolactone biosynthesis [19] Then carotenoid cleavage dioxygenase enzyme CCD7 and CCD8 modifies the structure, which has following orthologs:

The strigolactone signalling machinery comprises through a bunch of nuclear proteins [18]
Gene name Localization function Rice ortholog Pea ortholog Petunia ortholog Arabidopsis ortholog
CCD7 Plastid proteins involved in strigolactone biosynthesis D17/ HTD1 RMS5 DAD3 MAX3
CCD8 Plastid proteins involved in strigolactone biosynthesis D10 RMS1 DAD4 MAX4
Alpha/Beta fold hydrolase Nuclear proteins involved in strigolactone perception D14 RMS3 DAD2 ?

The alpha/beta fold hydrolase D3 and also D14L (D14-Like) (Later one has Arabidopsis ortholog KAI2, or KARRIKIN INSENSITIVE-2) is reported to have important roles in mycorrhizal symbiosis [3], notably, D3, D14 and D14L are localised in nucleus.[2]

NOPE1 or 'NO PERCEPTION 1', newly discovered transporter protein in Rice (Oryza sativa) and Maize (Zea mays), also required for the priming stage for colonisation by the fungus. NOPE1 is a member of Major Facilitator Super family of transport proteins, capable of N-acetylglucosamine transport. Since nope1 mutant's root exudates fail to elicited transcriptional responses in fungi, it strongly seems NOPE1 secretes something (not yet characterised) that promotes fungal response [2]

Perception

chemical structure of a LipoChitoOligosaccharide molecule
The chemical structure of MycRi-IV (C16:0,S), a Myc factor of Rhizophagus irregularis as indicated in Maillet, F et al. (2011) "Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza." Nature 469:58–63.The factor was first identified by Fabienne Maillet and coworkers  in a groundbreaking work published in Nature, where they have extracted three hundred litre mycorrhized carrot roots and exudates from 40 million germinating spores of Rhizophagus irregularis and purified the active fraction. They demonstrated this active principle is lipo-chito-oligosaccharide in nature.

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.[20] these key common components, form the Common Symbiosis pathway (CSP or CSSP).[20] It has been proposed that, RN symbiosis has originated from AM symbiosis.[11] The perception of presence of 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 [2][21]

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 kind of secreted materials 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 [21]

Short chain chitin oligomers (Myc-COs)

AM host plants show symbiotic-like calcium wave upon exposure to short chain chitin oligomers. It has been reported that production of these molecules by AM fungus Rhizophagus irregularis, gets strongly stimulated upon exposure to strigolactones [2] This gives hint to a model that plants secrete strigolactones and as a reply to it, this fungus increases short chain chitin oligomer, which in turns elicits the plant response to accommodate the fungus. The lysine motif OsCERK1 and OsCEBiP is thought to be involved with perception of short chain chitin oligomers.[2]

N-Acetylglucosamine.

NOPE-1 transporter has been described already. NOPE-1 also shows a strong N-acetylglucosamine uptake activity, and is thought to be associated with recognition of presence of fungal symbiont.[2]

Some plant proteins suspected to recognise Myc-factors, Rice OsCERK1 Lysin motif (LysM) receptor-like kinase, is one of them.[15]

Cell Surface Receptors

Different families of LYSM Receptors
Different families of LYSM Receptors
Some SYM genes respond to both RN and AM symbiosis. Some variants exclusively respond to any 1 type of the symbioses.
Some SYM genes respond to both RN and AM symbiosis. Some variants exclusively respond to any 1 type of the symbioses.

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. (ref)

Seemingly, different combinations of a LYK and LYR generates differential signals, such as some combinations generate a pathogen recognition signal whereas some combinations rise to the symbiotic signal [22][23][24][25]

Receptor like Kinase (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 trancatula; Lj-SYMRK in Lotus japonicas; Ps-SYM19 in Pisum sativum; OsSYMRK in Rice). OsSYMRK lacks an N terminal domain and exclusively regulate AM symbiosis, does not work for RN symbiosis.[26] Notably, it has been found that a Nodulation-factor inducible gene, MtENOD11 get activated in presence of AMF exudates; Little is known about this phenomenon.[27][28]

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 they are involved in AM symbiosis, in some plants they are not). Tomato (Solanum lycopersicum), a non-legume dicot, 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 works in a different pathway.[29][30][31]

Most of these kinases are Serine/Threonine kinase, some are Tyrosine kinase.[32] 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.[24]

Cell surface receptors may work differently in different combinations. Same receptor can perform multiple function. Such as Oryza sativa CERK1 Receptor may trigger a PTI response (Pathogen triggered immunity) with Oryza sativa CEBiP as a co-receptor; in presence of  CO8 Chitooligosaccharide. Whereas the same receptor CERK1 can play role in recognition of symbiotic signal, in presence of CO4 Chito-oligosaccharide,  using SYMRK as a Co-receptor.
Important cell surface receptots involved in molecular pattern recognition[32]
Medicago truncatula Lotus japonicus Pisum sativum

(pea)

Prunus persica Arabidopsis thalliana Brassica rapa Solanum lycopersicum

(Tomato)

Brachypodium distachyon Oryza sativa

(Rice)

Lysine Motif

Receptor-Like Kinase and Lysine Motif Receptor like Protein

LYM LYMI LYM1 PpLYM1 AtLYM1

AtLYM3

SlLYM1 BdLYM1

BdLYM3

OsLYP6

OsLYP5, OsLYP4

LYMII LYM2 PpLYM3

PpLYM2

AtLYM2 SlLYM3

SlLYM2

BdLYM2

BdLYM4

OsCEBiP

OsLYP3

LYR LYR 1 LYRIA MtNFP

MtLYR1

LjNFR5

LjLYS11

PpLYR1 SlLyk10 Bd LYR1 OsNFR5
LYRIB MtLYR8 PpLYR2 SlLYK9 Bd LYR2
LYR 2 LIRIIA MtLYR10 LjLYS16 PpLYR6 AtLYK2 SlLYK2
LYRIIB MtLYR9 LjLYS15 PpLYR7 SlLYK15
LYR 3 LYRIIIA MtLYR3 LjLYS12 PpLYR3 AtLYK4 SlLYK4 Bd LYR4 OsLYK6
LYRIIIB MtLYR2 PpLYR4 SlLYK7

SlLYK6

LYRIIIC MtLYR4

MtLYR7

LjLYS13

LjLYS14

AtLYK5 Bd LYR3 OsLYK3

OsLYK2, OsLYK4

LYR 4 LYRIV MtLYR5

MtLYR6

LjLYS20 PpLYR5
LYK LYKI LYK1, LYK4, LYK5, LYK6, LYK7, LYK2, LYK3, LYK9, LYK8 LjLYS2

LjLYS1, LjNFR1, LjLYS6, LjLYS7

PpLYK2

PpLyk1

AtLYK1/

AtCERK1

SlLYK13

SlLYK1/ SlBti9, SlLYK12, SlLYK11

BdLYK1 OsCERK1
LYKII LYK10 LjLYS3/

EPR3

PpLYK3

PpLYK4

LYKII PpLYK5 AtLYK3 SlLYK3 BdLYK3
Receptor like Kinase RLK Mt-DMI2/

Mt-NORK

Lj-SYMRK Ps-SYM19 OsSYMRK

Transmission

The transmission of signal cascades into nucleus is not well understood. However, this transmission includes carrying the message up to the nuclear membrane and generation of a calcium wave.[33] Some elements involved in this process are as follows:

Nucleoporins

Lotus japonicas Nucleoporins LjNUP85 and LjNUP133 has potential role in transmission of the signal.[34] Lj-NENA is another important nucleoporin that plays role in AM symbiosis.[35]

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.[36][37] This mevalonate acts as a second messenger, and activates a nuclear potassium channel, DMI1 or pollux.[37]

Important nuclear cation channels identified to be involved in C S S P[36]
Nuclear envelope Protein Function Rice Lotus japonicus Medicago truncatula Pisum
CNGC15 Cyclic-nucleotide gated Calcium-channel Mt-CNGC15
Castor Potassium cation   channel Os-Castor Lj-Castor
POLLUX or DMI1 Potassium cation   channel OsPOLLUX LjPOLLUX Mt-DMI1 Ps-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[36]

Transcription

Some component of signalling cascade involved in transcription stage of the common symbiosis signalling [36][35][38]
Protein Function Name of the Plant
Rice Lotus japonicus Medicago Truncatula Pisum sativum
CCamK Calcium calmodulin-dependent kinase with role in AMF symbiosis Os-DMI3 or

Os-CCaMK

Lj-CCaMK Mt-DMI3 Ps-SYM9
CYCLOPS Coiled coil domain containing proteins that respond to CCamK and promote AMF symbiosis Os-CYCLOPS Lj-CYCLOPS Mt-IPD3 Ps-SYM33
DELLA Promote AMF symbiosis Os-SLR1 Mt-DELLA1

Mt-DELLA2

Ps-LA

Ps-CRY

Calmodulin is a widespread regulatory protein that functions along with Ca2+ in various biological processes. In AM symbiosis signalling it modulates the CCaMK.[36]  CCaMK or DMI3 is a calcium-and-calmodulin-dependent kinase (CCaMK) is thought to be a key decoder of Ca2+ oscillation and an important regulatory kinase protein. Nuclear Ca2+ spiking promotes binding of Ca2+ calmodulin with CCaMK.[36] Binding of Ca2+ calmodulin with CCaMK causes conformational change of CCaMK that stimulates a target protein CYCLOPS which has different orthologs.[36] CYCLOPS is a coiled coil domain containing protein [36] possibly form a complex with CCaMK[36] that works along with DELLA proteins. DELLA proteins are kind of GRAS-domain protein and were originally identified as repressors of Gibberellin signalling pathway, however now it is seen that DELLA provides a mechanism for crosstalk between many signalling pathways.[39]  There are two DELLA proteins in Medicago trancatula and Pisum sativum play role in symbiosis whereas in rice plant only one DELLA protein fulfils this task.[36] Reduced Arbuscular Mycorrhiza or RAM1[36] is a GRAS[40] protein whose gene is directly regulated by DELLA and CCaMK/ CYCLOPS.[36] Using Chromatin immune precipitation assay it has been shown that RAM1 binds to RAM2 gene promoter.[36] RAM1 also play role in many of the fungal accommodation genes directly or indirectly.

A bunch of GRAS proteins play role in AM symbiosis whose roles are not yet fully understood. These includes RAD1 (REQUIRED FOR ARBUSCLE DEVELOPMENT 1), MIG1 (MYCORRHIZA INDUCED GRAS1), NSP1, NSP2 etc.[36] WRKY transcription factor genes are thought to play very important roles in establishment of mycorrhizal symbiosis and they perhaps work through regulating plant defense genes.[41]

The Accommodation program

Huge reorganization of cortex cells takes place in order to make accommodation for the fungal endosymbiont. The pre-penetration apparatus (PPA) like structure and the peri-arbuscular membrane have to form and the cytoplasm have to retract,[34] so, the vacuole retract in size, the nucleus and nucleolus enlarge in size and chromatin decondense indicating heightened transcriptional activity,[34] Plastids multiply and stay connected with “stromulus”.[34] Furthermore, it was suggested that the apoplastic longitudinal hyphal growth is probably regulated by plant genes such as taci1 and CDPK1.[42]

Genes and proteins playing role in accommodation programme

Although various proteins have been identified which may play role on how this accommodation process happens, the detailed signalling cascade is not well understood. Some of the proteins and machineries involved in the deposition on peri-arbuscular membrane are EXOCYST complex, EXO70 subunit, a symbiosis-specific splice variant of SYP132, VAPYRIN, two variants of VAMP721 etc.[36] Plant enzymes FatM and RAM2[43] and ABC transporter STR/STR2 is involved in synthesis and supplying of a lipid 16:0 β-monoacylglycerol to the AM fungi.[43][44]

The protein composition of peri-arbuscular membrane is very different from plasma membrane. It includes some special transporters such as phosphate transporter (Mt-PT4, Os-PT11, Os-PT13), Ammonium transporter (Mt-AMT2 and 3) etc. and ABC transporters such as lipid transporter STR/STR2[36][45]

Evolutionary significance

AM fungi and plants co-evolved and developed a very complex interaction that allow the plant accommodate the AM-fungal host [46][47][48] It has been proposed that, RN symbiosis has originated from AM symbiosis[34][35]

See also

References

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