Receptor-like kinases sustain symbiotic scrutiny · 24 relationships where symbiosis is...

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Receptor-like kinases sustain symbiotic scrutiny 1

Chai Hao Chiu* and Uta Paszkowski 2

Department of Plant Sciences, University of Cambridge, Downing Street, Cambridge, CB2 3EA, 3

United Kingdom 4

* Author for correspondence: [email protected] 5

Author Contributions: C.H.C. wrote the manuscript and drew the figures, U.P. edited the 6

manuscript. 7

ORC-ID: 0000-0002-2840-0407 (C.H.C.); 0000-0002-7279-7632 (U.P.) 8

Abstract 9

Plant receptor-like kinases (RLKs) control the initiation, development and maintenance of symbioses 10

with beneficial mycorrhizal fungi and nitrogen-fixing bacteria. Carbohydrate perception activates 11

symbiosis signalling via Lysin-motif (LysM) RLKs and subsequently the common symbiosis signalling 12

pathway. As the receptors activated are often also immune receptors in multiple species, exactly 13

how carbohydrate identities avoid immune activation and drive symbiotic outcome is still not fully 14

understood. This may involve the coincident detection of additional signalling molecules that 15

provide specificity. Because of the metabolic costs of supporting symbionts, the level of symbiosis 16

development is fine-tuned by a range of local and mobile signals that are activated by various RLKs. 17

Beyond early, pre-contact symbiotic signalling, signal exchanges ensue throughout infection, 18

nutrient exchange and turnover of symbiosis. Here, we review the latest understanding on plant 19

symbiosis signalling from the perspective of RLK-mediated pathways. 20

Introduction 21

Plants interact with a plethora of other organisms, and these symbioses range from detrimental to 22

beneficial in outcomes; and from transient to persistent in terms of stability. For durable 23

relationships where symbiosis is re-established every generation, the ability to recruit, maintain and 24

terminate symbiotic relationships involve genetically encoded components that sense and 25

orchestrate signalling, metabolic and developmental changes in both parties to achieve mutually 26

beneficial outcomes. Among these components, receptor-like kinases (RLKs) transduce external and 27

endogenous signals and activate the corresponding signalling processes. 28

Here, we focus on the roles of plant RLKs in initiating, establishing, limiting and maintaining distinct 29

steps of symbiotic interactions, specifically in root endosymbioses where the genetic underpinnings 30

are well-understood. Box 1 provides a primer on the functions and stages of the two plant 31

symbioses with arbuscular mycorrhizal fungi (AMF) and with nitrogen-fixing bacteria. At each stage, 32

we highlight emerging themes and the range of pathways identified. With this, we aim to 33

complement the suite of recent reviews of plant symbioses from the perspective of transcriptional 34

regulation (Diédhiou and Diouf, 2018; Pimprikar and Gutjahr, 2018), phytohormone regulation 35

(Fonouni-Farde et al., 2016; Liu et al., 2018; Müller and Harrison, 2019), nutrient exchange (Udvardi 36

and Poole, 2013; Chiu and Paszkowski, 2019) and evolution (Martin et al., 2017; Strullu-Derrien et 37

al., 2018). 38

The Common Symbiosis Signalling Pathway 39

Plant Physiology Preview. Published on February 13, 2020, as DOI:10.1104/pp.19.01341

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From the diverse micro-organisms in the soil, plant hosts are able to recruit beneficial symbionts into 40

the root. Both AMF and nitrogen-fixing bacteria require a core signalling pathway that orchestrates 41

the signalling and developmental changes necessary for symbiont accommodation. Elucidation of 42

plant symbiotic signalling pathways began with forward genetic screens in model legumes such as 43

Medicago truncatula and Lotus japonicus. Several mutants defective in nodulation were also 44

defective in AM symbiosis (AMS), leading to the concept of a Common Symbiosis Signalling Pathway 45

(CSSP, also ‘Common SYM’). RLK activation upon ligand recognition converge on the CSSP to activate 46

symbiosis signalling. This ancient toolkit evolved for AM symbiosis (AMS), and was hypothesized to 47

be co-opted by the nodulating clade for Root Nodule Symbiosis (RNS)(Parniske, 2000; Parniske, 48

2008; Oldroyd, 2013). The CSSP begins with SYMBIOSIS RECEPTOR KINASE (SYMRK/DMI2/NORK), a 49

Malectin Domain-Leucine Rich Repeat (MLD-LRR)-RLK that activates perinuclear calcium oscillations 50

(hereafter Ca2+-oscillations) involving Ca2+-channels on the nuclear envelope (e.g. DOESN’T MAKE 51

INFECTION1, DMI1/CASTOR/POLLUX) (Kim et al., 2019). These Ca2+-oscillations activate a CALCIUM 52

AND CALMODULIN-DEPENDENT KINASE (CCaMK/DMI3) which interacts with and phosphorylates 53

CYCLOPS/INTERACTING PROTEIN OF DMI3 (IPD3), a transcriptional regulator, launching symbiosis 54

signalling. In addition, the nuclear pore complex components of NUCLEOPORIN85 (NUP85), NUP133 55

and NENA in Lotus are also CSSP components upstream of Ca2+-oscillations, but their symbiotic 56

defects are temperature-sensitive (permissive at lower temperatures). Readers are directed to 57

(Parniske, 2008; Oldroyd, 2013; MacLean et al., 2017) for comprehensive reviews of the CSSP. 58

Nonetheless, it is important to point out that compared to strong nodulation defects, intra-radical 59

colonisation, as well as arbuscule development is possible in CSSP mutants, as is observed in Lotus 60

symrk, ccamk mutants (Demchenko et al., 2004; Parniske, 2008); that CSSP-independent signalling 61

pathways occur (Kosuta et al., 2003; Kistner et al., 2005; Gutjahr et al., 2008; Camps et al., 2015), 62

and that species-specific differences exist for mutant phenotypes. CYCLOPS is a case-in-point, where 63

strong AM phenotypes in Lotus and Rice contrast starkly against reduced but successful arbuscule 64

development in Medicago ipd3/ipd3-like double mutants (Lindsay et al., 2019). Collectively, these 65

and other data show that CYCLOPS is sufficient but not necessary for symbiosis signalling (Pimprikar 66

et al., 2016). The clearest demonstration of CSSP-independent pathway comes from Lotus LACK OF 67

SYMBIONT ACCOMODATION (LjLAN), which encodes for a MEDIATOR Complex protein and regulates 68

both AMS and RNS while displaying normal Ca2+-oscillations to NF. Ljlan is impaired in infection 69

thread formation but low numbers of intercellular infection leads to some nodule development, 70

whereas Ljlan/cyclops was completely defective in nodule formation (Suzaki et al., 2019). 71

The existence of CSSP puts symbiosis evolution into perspective and offers the tantalising possibility 72

of engineering nitrogen-fixing symbiosis into crops by identifying components and regulatory 73

mechanisms that evolved to enable RNS (Mus et al., 2016). Yet the CSSP also raises an unresolved 74

conundrum: how do rhizobia bacteria and AMF both activate CSSP but yet specify different 75

symbiotic outcomes in their host? Bifurcating downstream transcriptional regulation, e.g. by 76

transcription factors NODULATION SIGNALLING PROTEIN1 (NSP1)/ REQUIRED FOR ARBUSCULAR 77

MYCORRHIZA1 (RAM1) previously suggested to specify RNS/AMS respectively (Oldroyd, 2013) is now 78

revised with evidence demonstrating a role for NSP1 in AMS (Liu et al., 2011; Delaux et al., 2013; 79

Takeda et al., 2013; van Zeijl et al., 2015; Floss et al., 2017), leaving the specificity determinants 80

unresolved. 81

LysM-RLKs activate the CSSP 82



3

Symbiosis signalling initiates with microbial carbohydrate perception by plant plasma membrane 83

(PM)-localised RLKs – the very first step of symbiotic scrutiny. In the symbiosis between rhizobia 84

bacteria and legumes or Parasponia, this step is especially stringent, as lipochito-oligosaccharides 85

(LCOs, also known as ‘Nod-factors’) from compatible rhizobia bind to and activate their cognate 86

RLKs. These Lysin-motif RLKs (LysM-RLKs) contain three LysM domains in the extra-cellular domain 87

(ECD) capable of binding oligosaccharides containing β1–4 glycosidic bonds. Forward genetic screens 88

for nodulation-defective mutants and subsequent biochemical characterisation identified Lotus 89

japonicus NOD FACTOR RECEPTOR1 (LjNFR1) and LjNFR5 to be necessary for directly binding and 90

perceiving Mesorhizobium loti Nod-factors and activating the downstream signalling cascades for 91

infection and nodule organogenesis (Madsen et al., 2003; Radutoiu et al., 2003; Broghammer et al., 92

2012). LjNFR1 and LjNFR5 bind Nod-factors at nM ranges, concentrations at which physiological 93

responses are triggered. Loss of either LjNFR1 or LjNFR5 abolished infection or nodule 94

organogenesis. Medicago LYSM DOMAIN RECEPTOR KINASE3 (MtLYK3) and NOD FACTOR 95

PERCEPTION (MtNFP) are similarly required for nodulation. However, Mtlyk3-RNAi or mutants still 96

retain some Nod-factor responses, notably Ca2+-oscillations. MtLYK3 therefore has been proposed to 97

be an ‘entry receptor’ that regulates rhizobia infection (Catoira et al., 2000; Wais et al., 2000; Amor 98

et al., 2003; Limpens et al., 2003; Smit et al., 2007). This model also holds true for pea, where 99

PsSYM10 (LjNFR5/MtNFP homologue)(Madsen et al., 2003) as well as PsSYM37 and PsK1 (MtLYK3 100

homologues)(Zhukov et al., 2008; Kirienko et al., 2018; Kirienko et al., 2019) are involved in 101

perception of Rhizobium leguminosarum. Figure 1 highlight the roles of LysM-RLKs involved, as well 102

as a phylogenetic relationship of some of these receptors with their most recent gene names. 103

Importantly, the transfer of LjNFR1 and LjNFR5 into Medicago truncatula enabled the Lotus 104

symbiont M. loti to infect and develop nodules on M. truncatula (a non-host) (Radutoiu et al., 2007), 105

demonstrating that perception of specifically-decorated LCOs by its cognate LysM-RLKs in a receptor 106

complex may determine symbiosis specificity in RNS. 107

In addition to LjNFR1/5, a new Nod-factor receptor was recently described. LjNFRe is closely related 108

to LjNFR1, and is hypothesized to ensure robust epidermal Nod-factor signalling at the susceptible 109

zone of Lotus roots (Murakami et al., 2018). Ljnfre mutants develop fewer nodules, consistent with 110

its role in inducing NODULE INCEPTION (LjNIN) expression in the epidermis. Like LjNFR1, LjNFRe has 111

an active kinase domain, binding affinity for LCOs, and also phosphorylates and require NFR5 for 112

activating epidermal NIN expression. Furthermore, replacing the kinase domain activation segments 113

of LjNFRe with that of LjNFR1 is sufficient to change the signalling output to that of NFR1, enabling 114

cortical NIN induction and nodule development; showing that the activation segment determines 115

signalling specificity between NFR1/e (Murakami et al., 2018). 116

Together, these Nod-factor signalling components present a paradigm whereby an LysM-RLK with 117

functional, active kinase domain (LjNFR1/MtLYK3) forms a complex with an RLK with an inactive, 118

pseudokinase domain (LjNFR5/MtNFP), probably requiring the former to transphosphorylate the 119

latter to generate a signalling response (Madsen et al., 2011; Antolín-Llovera et al., 2014; Murakami 120

et al., 2018). These two types also correspond to the two LysM-RLK clades present in land plants. 121

Why a pseudokinase is necessary for signalling remains to be fully appreciated, but the additional 122

involvement of LjSYMRK in phosphorylating LjNFR5 may point to the formation of heterotypic 123

complexes or different separable, distinct receptor complexes during RNS as well as AMS. 124



4

In contrast to RNS where Nod-factor perception explains most of host-symbiont specificity, the 125

nature, range and exact suite of ligand(s) for AMS is hitherto elusive. AMF produce simple LCOs and 126

short chain chitin oligomers (CO4-5), both of which elicit ‘symbiotic outputs’ via the CSSP, often 127

shown by activation of Ca2+-oscillations and increased lateral root formation (Maillet et al., 2011; 128

Genre et al., 2013; Sun et al., 2015). Exogenous application of LCOs increased root length 129

colonisation by AMF, consistent with its role as a positive regulator of symbiosis (Maillet et al., 130

2011). However, apart from LCOs and CO4-5, the elicitors capable of activating Ca2+-oscillations and 131

symbiotic gene expression may be wider than expected. (Feng et al., 2019) demonstrated that CO8 132

and Peptidoglycan (PGN) – typically considered pathogen associated molecular patterns (PAMPs) are 133

also capable of eliciting ‘symbiotic’ signalling outputs. Coordinated perception of LCO and CO8/PGN 134

attenuated the ‘immunity’ outputs of ROS production and MAPK activation and synergistically 135

boosted symbiotic gene expression, thereby suggesting that AMS might involve coordinated 136

perception of microbe-associated molecular patterns (MAMPs) via LysM-RLKs and activating 137

symbiosis signalling via SYMRK. Thus redundancy at both ligand and receptors could explain (i) the 138

lack of LysM-RLK mutants where symbiosis with AMF is abolished, and (ii) the broad host range of 139

AMF. 140

While the exact nature of signalling molecules remain to be identified, it is clear that carbohydrate 141

perception by LysM-RLKs activates symbiosis signalling in AMS. The requirement for LysM-RLKs has 142

recently been elucidated in various plant species. First demonstrated in rice, similar work in pea, 143

Medicago, tomato and banana all revealed that the LysM-RLK CHITIN ELICITOR RECEPTOR KINASE1 144

(CERK1; or equivalent homologues) is involved in signal perception of AMF-derived chitinaceous 145

ligands since cerk1 null and/or cerk1-RNAi had reduced colonisation (Miyata et al., 2014; Zhang et 146

al., 2015; Leppyanen et al., 2017; Chiu et al., 2018; Liao et al., 2018; Feng et al., 2019; Gibelin-Viala et 147

al., 2019; Zhang et al., 2019). Importantly, symbiosis is not abolished, showing that CERK1 is 148

necessary but not essential for AM symbiosis. In all cases (except for pea where microscopy data is 149

lacking), arbuscule development appears normal. 150

Furthermore, in rice where the LysM-RLK family is less expanded vis-à-vis 151

the Fabaceae, Oscerk1 mutants lack detectable epidermal Ca2+-oscillations in response to CO4 and 152

Germinated Spore Exudates (GSE), a cocktail of signal molecules from naïve AMF spores (Carotenuto 153

et al., 2017). Nevertheless, intra-radical colonisation and arbuscule formation in Oscerk1 mutants 154

(Miyata et al., 2014; Zhang et al., 2015; Chiu et al., 2018) suggests that either symbiosis 155

development can be achieved independent of Ca2+-oscillations, or that yet unobserved oscillations 156

occur under prolonged signal exchange employing redundant LysM-RLKs or SYMRK. 157

As such, in contrast to their essential role for symbiotic scrutiny in most RNS, the role of LCOs in AM 158

symbiosis is at present equivocal. Null mutants of Ljnfr5, Mtnfp displayed wild-type levels of 159

colonisation (Maillet et al., 2011; Zhang et al., 2015; Feng et al., 2019). Contradictory observations 160

were made for Ljnfr1 or Mtlyk3 (hcl) mutants which either showed transiently reduced colonisation 161

(Zhang et al., 2015), or no difference relative to wild type (Takeda et al., 2011; Feng et al., 2019). 162

Normal colonisation in mutants of LCO receptors may be due to the genetic redundancy present in 163

the Fabaceae where the receptors have expanded. For instance, LjLYS11 encodes a LCO receptor 164

closely-related to LjNFR5 that is induced during AM colonisation. Yet, even triple mutants of Ljnfr1 165

nfr5 lys11 in Lotus had no observable defects in AM colonisation (Rasmussen et al., 2016). Also, 166

whereas silencing Parasponia andersonii (PaNFP) did not prevent fungal colonisation, it blocked 167



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arbuscule development, and decreased nodulation frequency (Op den Camp et al., 2011). However, 168

it cannot be excluded that closely related LysM-RLKs may be silenced as well. Whether PaNFP 169

directly bind to or mediate LCO perception is yet to be shown. In rice where the LysM-RLK family is 170

not neofunctionalised for RNS, knockout of the LjNFR5/MtNFP orthologue, OsNFR5/RLK2/MYR1, 171

produced contrasting phenotypes. Homologous recombination mutants showed normal AM 172

symbiosis or Ca2+-spiking responses to GSE (Miyata et al., 2016; Carotenuto et al., 2017). However, 173

CRISPR-edited mutants of the same gene had reduced colonisation levels under low spore inoculum 174

strength. Under high inoculation strength, osnfr5/rlk2/myr1 have wild-type like colonisation levels 175

(He et al., 2019), suggesting that the CO4-binding ability of OsNFR5/MYR1 is dispensable for 176

symbiosis. 177

On the other hand, LCO receptors of two Solanaceaeous species, petunia and tomato, have been 178

recently identified to be involved in AM symbiosis. Virus-induced gene silencing (VIGS) of the 179

tomato orthologue (SlLYK10) delayed fungal colonisation and resulted in abnormal arbuscule 180

development (Buendia et al., 2016). Similarly, in a missense allele of Sllyk10-1, and in Phlyk10-1, a 181

transposon-insertion mutant, the mutation/loss of LCO receptor quantitatively reduced AM 182

colonisation and full arbuscule development in both species(Girardin et al., 2019). Importantly, both 183

SlLYK10 and PhLYK10 can restore RNS in Mtnfp and Ljnfr5 mutants (Girardin et al., 2019). This is 184

consistent with the notion that the evolution of RNS recruited existing components involved in AMS. 185

Therefore, evidence so far suggest that LCO perception by LysM-RLKs contributes to, but may not be 186

essential for AMS. This is supported by the observation that reduction in AM colonisation is further 187

diminished in mtcerk1 nfp double mutant relative to mtcerk1 mutants (Feng et al., 2019). Whether 188

LCO perception by LysM-RLKs is necessary, or fully dispensable for AM symbiosis remains to be 189

ascertained. 190

Overall, carbohydrate signalling during AMS appears to be more complex than expected, as 191

symbiont-encoded proteins can also affect ligand-binding and receptor activation. Fungal-secreted 192

LysM effectors previously described to be involved in subverting host defence responses during 193

chitin-triggered immunity have been recently identified in AMF as well (Schmitz et al., 2019; Zeng et 194

al., 2020). Rhizophagus irregularis SECRETED LYSM EFFECTOR (RiSLM) was capable of binding both 195

COs and LCOs. Recombinant RiSLM reduced chitin-triggered ROS production but allowed activation 196

of symbiosis signalling. Consistent with its role as a positive regulator, host-induced gene silencing 197

(HIGS) of RiSLM reduced AM colonisation; although over-expression of RiSLM in Medicago did not 198

increase colonisation (Zeng et al., 2020). 199

Whereas mutants of LysM-RLK show reduced symbiosis, AMS is fully abolished when the alpha/beta 200

hydrolase receptor DWARF14-LIKE (D14L) is mutated (Gutjahr et al., 2015; Liu et al., 2019). How 201

D14L, the ancient paralog of the strigolactone receptor D14, fits with the CSSP in AM signalling 202

remains to be demonstrated. Also unknown is the identity of the karrikin-like D14L ligand, of plant or 203

fungal origin. Nonetheless, the essential function of D14L for AMS in rice is conserved in Petunia 204

(Gutjahr et al., 2015; Liu et al., 2019), suggesting that the critical role of D14L in symbiotic scrutiny is 205

similar in monocotyledonous and dicotyledonous plant species. 206

Multifaceted LysM Receptors have roles beyond symbiosis 207

An enigma with the chitin receptor is its role in activating both defence and symbiotic responses in 208

response to fungal elicitors. This is the case in rice, Medicago and pea (Miyata et al., 2014; 209



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Leppyanen et al., 2017; Gibelin-Viala et al., 2019). Like its Arabidopsis counterpart, CERK1 is required 210

for activating ‘immunity’ outputs (ROS production and MAPK activation) (Miya et al., 2007; Wan et 211

al., 2008) in both roots and shoots but it also mediates AM symbiosis in the roots. Nonetheless, ROS 212

and MAPK assays are limited in their specificity, as they are also triggered by damage, development 213

and early AMF perception. When exposed to pathogens, oscerk1/mtcerk1 mutants are more 214

susceptible to both fungal (rice blast, Magnaporthe oryzae)(Kouzai et al., 2014a) and also oomycete 215

pathogens (in the case of Mtcerk1) (Bozsoki et al., 2017; Gibelin-Viala et al., 2019). Yet ‘immunity’ 216

and symbiosis appear to be separable in other species instead, showing that species-specific 217

differences and sub-functionalisation of chitin receptors exist (Figure 1). For example, in Ljcerk6 218

mutants, where chitin-induced responses were abolished, AM colonisation was not affected (Bozsoki 219

et al., 2017). Similarly, in tomato, whereas silencing SlLYK12 impaired AM colonisation; silencing 220

SlLYK1/Bti9 impaired ROS production and resistance to Pseudomonas syringae (Zeng et al., 2012; 221

Liao et al., 2018). 222

Symbiosis versus immunity signalling could be determined at the level of receptor/co-receptor 223

complex(es) composition. For instance, OsCEBiP, the high affinity receptor for CO8, is not involved in 224

AM symbiosis but in basal resistance against M. oryzae (Kaku et al., 2006; Kishimoto et al., 2010; 225

Kouzai et al., 2014b). However, the fact that CO8 and CERK1-signalling can activate both defence and 226

symbiotic signalling means that while exclusively pathogenic elicitors may activate distinct immune 227

receptor complexes, other elicitors may activate overlapping pathways for immunity and symbiosis 228

via a shared co-receptor, and require other MAMP-detection and/or effector detection for signal 229

integration before a full immune or symbiosis response is mounted. This is consistent with 230

observations that AMF transiently activates early defense responses that are attenuated (Harrison 231

and Dixon, 1993; Kapulnik et al., 1996; Garcia-Garrido, 2002; Liu et al., 2003; Campos-Soriano et al., 232

2010). It has been proposed that the changing ratio of immune-modulating CO4-5/LCOs relative to 233

immunogenic CO7-8 may be relevant (Schmitz and Harrison, 2014), but the supporting evidence is 234

lacking. 235

On top of symbiosis signalling and chitin-triggered defences, OsCERK1 is also required for increased 236

root branching responses, specifically of large lateral roots, the preferred root type for AMF 237

colonisation (Chiu et al., 2018). The ultimate explanation for this response is perhaps that symbiont 238

perception elicits an overall increase in symbiotic interfaces available. LR branching has been used as 239

a biological assay for Myc/Nod factors. In rice, this developmental response is however independent 240

of CSSP, and also independent of the karrikin receptor D14L that is necessary for pre-symbiotic 241

dialogue and symbiotic accommodation (Gutjahr et al., 2009; Gutjahr et al., 2015; Chiu et al., 2018). 242

The developmental and intra-radical colonisation steps are thus genetically separable, at least in a 243

monocot. 244

LCO perception and CSSP may not be specific to endosymbiosis signalling 245

As nod-factors and potentially myc-factors, LCOs have been regarded as a non-immunogenic 246

symbiotic signal that connects membrane perception to CSSP for endosymbiont accommodation. 247

Before discussing signalling events downstream of LysM-RLKs, it is important to highlight that many 248

non-endosymbionts produce similar signalling molecules that activate CSSP. Therefore, how 249

specificity between different organisms in the rhizosphere is achieved is still unresolved. 250



7

LCO production is not an endosymbiont-exclusive trait, as they have recently been demonstrated to 251

also be produced by ectomycorrhizal (ECM) fungi, another ecologically important plant-fungal 252

symbiosis (Cope et al., 2019) but fundamentally not an endosymbiotic association. The fungus 253

Laccaria bicolor produces LCOs and elicits perinuclear Ca2+-oscillations in Poplar trichorcarpa via 254

PtCASTOR/POLLUX. Both castor/pollux-RNAi and ccamk-RNAi show slightly reduced ECM formation 255

(Cope et al., 2019). However, a cautious interpretation is that interfering with CSSP affects both LCO 256

and CO signalling, so whether ECM symbiosis requires LCO recognition is not yet demonstrated. As 257

alluded to by this and earlier work, CSSP components are missing in some host species (e.g. Norway 258

Spruce, Picea abies) and hence is likely not a conserved pathway required for ECM associations 259

(Garcia et al., 2015; Cope et al., 2019). Moreover, compounds with near-identical chemical and 260

biological properties to LCOs have been reported to be produced by nitrogen-fixing maize root 261

endophytes of Bacillus spp. (Lian et al., 2001) and nematodes (Weerasinghe et al., 2005). Finally, the 262

LCO perception machinery is involved in other biotic interactions where Mtnfp mutants were more 263

susceptible to oomycete and fungal infections (Rey et al., 2013). Collectively, it appears that LCO 264

production and perception in the rhizosphere may extend beyond AMF and rhizobia. 265

Downstream of LCO perception, Ca2+-oscillations are also not exclusively activated by fungal or 266

rhizobial symbiont, as glucan-chitosaccharide fractions from Aphanomyces euteiches were reported 267

to elicit perinuclear Ca2+-oscillations, independent of MtNFP, MtDMI1, MtDMI2 (Nars et al., 2013). 268

However, the robustness of Ca2+-oscillations in the traces, especially for the mutants appear 269

relatively low. More recently, it was demonstrated that endophytic Fusarium solani and Serendipita 270

indica, as well as pathogenic F. oxysporum are capable of eliciting Ca2+-oscillations (Skiada et al., 271

2019). Clearly, beyond symbiotic AM/ECM fungi and rhizobia, nuclear Ca2+-oscillations can also be 272

activated by other microorganisms. 273

In addition, the loss of LysM-RLK or CSSP signalling could either suppress (Skiada et al., 2019) or 274

promote colonisation by non-endosymbionts (Fernandez-Aparicio et al., 2010). There is also no 275

obvious trend whether this correlates with the intimacy of the pathogen lifestyle. However, the 276

small quantitative nature of these effects relative to those of CSSP mutations on AMS/RNS, suggests 277

that endophytes/pathogens rely less on the CSSP for host access. Further support is provided by 278

Magnaporthe oryzae, which leads an extended biotrophic lifestyle in rice roots, but is still capable of 279

proliferating in roots of rice CSSP mutants and d14l mutants (Marcel et al., 2010; Gutjahr et al., 280

2015) where AMF accommodation is abolished. 281

Recently, next-generation sequencing has enabled the profiling of bacterial and fungal communities 282

in the root microbiome (Zgadzaj et al., 2016; Thiergart et al., 2019; Xue et al., 2019). As 283

demonstrated for Lotus mutants, the use of microbiome profiling, especially in complex soils or 284

controlled mesocosms, may allow a more refined understanding of whether the CSSP/LysM-285

RLK/autoregulatory mutants become more, or less susceptible to pathogens/biotrophs of interest 286

when challenged in a near-native context. 287

Moving out of the model legumes, LCOs are not necessary for symbiosis signalling. In the rhizobia-288

legume symbiosis between photosynthetic Bradyrhizobia and Aeschynomene sensitiva and A. indica, 289

nodules can develop in both stems and roots of the tropical tree without involving LCOs (Giraud et 290

al., 2007) but still requiring the CSSP (Fabre et al., 2015). Similarly, in the actinorrhizal species 291

Casuarina glauca, the unknown elicitors of Nod-factor independent signalling have been 292

characterised to be heat-stable, hydrophilic and chitinase-resistant (Chabaud et al., 2016). For nod-293



8

factor independent signalling, the Type III secretion system (T3SS) of Bradyrhizobium has been 294

shown to be required for successful symbiosis development by delivering effectors that manipulate 295

host processes (Okazaki et al., 2016; Miwa and Okazaki, 2017). 296

RLK interactions downstream of ligand perception 297

After ligand-binding, downstream signalling events occur to allow symbiont infection of the host. 298

During RNS, concomitant production of lateral organs (nodules) is also required for infection and 299

functional nitrogen-fixation. Intimate association is only achieved several days after the initial signal 300

exchanges, so the spatio-temporal regulation of RLKs and their effect on transcriptional networks is 301

instrumental to understanding symbiosis. To date, a few downstream components have been 302

identified (see Figure 2), but there is yet an overarching view of how these components link the RLKs 303

to transcriptional regulation via the CSSP (see Figure 2). 304

The localisation and stability of LysM-RLKs is altered upon ligand perception, which is important for 305

allowing rhizobia infection to proceed. One of the emerging insights of receptor biology is their 306

compartmentalisation at the PM into nanodomains/microdomains (Ott, 2017). RLKs in immunity 307

signalling, such as Arabidopsis FLAGELLIN SENSING2 (FLS2) and BRASSINOSTEROID INSENSITIVE1 308

(BRI1) have been localised to sub-micron protein/lipid assemblies and are hypothesized to nucleate 309

other signalling components that change in size and composition dynamically, especially upon 310

stimuli (Bücherl et al., 2017). These membrane nanodomains therefore could partition RLKs into 311

functionally distinct signalling units. Medicago MtLYK3, MtNFP, MtDMI2 all are able to interact with 312

Mt SYMBIOTIC REMORIN1 (MtSYMREM1), a molecular scaffold protein (Tóth et al., 2012; Liang et al., 313

2018). Prior to Nod-factor or rhizobia application, MtLYK3 has high lateral mobility at the PM, after 314

which it becomes immobilised in nanodomains labelled by MtFLOTILLIN4 (MtFLOT4) (Haney et al., 315

2011). MtSYMREM1 mediates immobilization and stabilisation of MtLYK3, reduces its endocytosis 316

and increases its dwell time in the domain. This is hypothesized to recruit additional signalling 317

components that determine infection, and control symbiosis output. Genetic evidence implicates 318

MtFLOT4 and MtSYMREM1 for successful infection, and cell biology reveals MtFLOT4/2 and actin to 319

serve as a primary core of the nanodomain and MtSYMREM1 as a symbiotically-induced secondary 320

component (Liang et al., 2018). One possible member recruited for signalling downstream of LCO 321

perception may be Lotus RHIZOBIAL INFECTION RECEPTOR-LIKE KINASE1 (LjRINRK1), an atypical 322

receptor kinase first identified from a mutant screen for infection thread defects. The full induction 323

of early infection genes, including LjNIN, is independent of LjRINRK1 kinase activity, and may point to 324

a possible role in a larger receptor complex in coordinating nod-factor signalling (Li et al., 2019). 325

Downstream of LysM-RLKs, multiple signalling pathways emerge from SYMRK; ranging from the 326

activation of mevalonate pathway for a putative secondary messenger for activating Ca2+-oscillations 327

(Kevei et al., 2007; Venkateshwaran et al., 2015), inhibition of MAPKK activity (Chen et al., 2012) and 328

importantly to activation of LjNIN (Zhu et al., 2008; Wang et al., 2013), a transcriptional regulator 329

that coordinates both infection and nodule organogenesis, and recently demonstrated to have 330

recruited the lateral root development pathway for nodule development (Schiessl et al., 2019). 331

Because overexpression of LjNFR5, LjNFR1 or especially, LjSYMRK is sufficient for spontaneous 332

nodule formation in the absence of symbiont (Ried et al., 2014); it is unsurprising that there is a 333

multitude of regulatory mechanisms on the receptors to ensure appropriate activation only when 334

the symbiont is present. One notable mechanism is via the cleavage of its MLD. When expressed in 335

tobacco leaves, truncated LjSYMRK(∆MLD) had increased affinity for LjNFR5 whereas the LRR 336



9

domain regulates its turnover (Antolín-Llovera et al., 2014). Whether overexpression of 337

LjNFR1/LjNFR5/LjSYMRK, or ectodomain cleavage/turnover of LjSYMRK also affect AMS, or are 338

specific to RNS remains to be addressed. 339

Nod-factor receptors and SYMRK have also been revealed to be under tight post-translational 340

regulation by ubiquitation via Plant U-Box (PUB) proteins. There is an increasing body of work on the 341

regulation of RLKs – specifically MtLYK3, LjSYMRK/MtDMI2, LjNFR5 by various PUBs. LjSYMRK for 342

example, is targeted by Lotus SEVEN IN ABSENTIA4 (LjSINA4) for degradation, negatively regulating 343

RNS, but not AMS (Den Herder et al., 2012). LjCERBERUS, an E3 Ubiquitin ligase, as well the de-344

ubiquitinating enzyme ASSOCIATED MOLECULE WITH THE SH3 DOMAIN OF STAM (LjAMSH1) are also 345

involved in both infection and nodule organogenesis processes (Yano et al., 2009; Małolepszy et al., 346

2015). As a post-translational modification, changes in ubiquitination of RLKs or other signalling 347

components by PUBs/E3 ligases may target them for degradation by the 26S Proteasome. But as 348

seen in the case with MtPUB1, ubiquitination may not always lead to degradation, but possibly 349

altered localisation via endocytosis/vesicle trafficking or altered protein-protein interactions 350

(Mbengue et al., 2010; Vernié et al., 2016). The importance of ubiquitination as well as the signalling 351

components modified in both symbioses still require a more complete analysis. 352

Downstream of membrane perception, the phosphorylation cascades are also not well understood. 353

Recently, a Receptor-Like Cytoplasmic Kinase (RLCK) was identified biochemically to act downstream 354

of LjNFR5. Lotus NFR5-INTERACTING CYTOPLASMIC KINASE4 (LjNiCK4) phosphorylates LjNFR1 and 355

LjNFR5 in vitro and relocates to the nucleus upon Nod-factor perception to positively regulate 356

nodule organogenesis (Wong et al., 2019). LjNiCK4 adds to the growing theme of RLK-RLCK 357

combinations in other signalling contexts e.g. immunity, stress response (Liang and Zhou, 2018). 358

Overall, complex signalling activation and regulation occurs for receptors, especially for SYMRK, but 359

how this receptor functions to specify fungal and bacterial symbioses remain to be fully dissected. 360

Keeping nod-factor independent RNS in mind, the effector ErnA is delivered to activate nodule 361

development, and ectopic expression in plant roots generated numerous lateral meristem-like 362

structures along the root length (Teulet et al., 2019). This could be a result of ErnA interacting with 363

RLK/SYMRK and the CSSP, or by activating lateral organogenesis independently. 364

During RNS, symbiont recognition also activates the expression of other LysM-RLKs for additional 365

symbiotic scrutiny by the plant host. Nod-factor perception by LjNFR1/5 activates CSSP and induces 366

the expression of another LysM-RLK, Lotus EXOPOLYSACCHARIDE RECEPTOR3 (LjEPR3)(Kawaharada 367

et al., 2015; Kawaharada et al., 2017). The surface exopolysaccharides (EPS) of rhizobia have been 368

long studied for their roles in symbiosis. Like Nod-factors, EPS have strain-specific characteristics but 369

are heteropolymers of 8-9 sugar residues. LjEPR3 ECD directly binds EPS, and Ljepr3 mutants show 370

that EPS recognition is necessary for intracellular infection progression in epidermis, cortex and into 371

nodule primordia (Kawaharada et al., 2015; Kawaharada et al., 2017). 372

The continuation of both bacterial nod gene expression, and plant expression of LjNFR1/NFR5/EPR3 373

in cortex cells of developing nodule primordia (but not mature ones), observations of Ca2+-374

oscillations ahead of the growing infection thread (Sieberer et al., 2012) together suggest that Nod-375

factor perception and CSSP activation is involved beyond pre-symbiotic stages, through to infection 376

and nodule development. This insight is also demonstrated using promoters that enrich for 377

epidermal or cortical expression (Rival et al., 2012; Hayashi et al., 2014). Beyond RNS, the role of 378



10

EPR3-type LysM-RLKs remains enigmatic, as recent phylogenetic and phylogenomic surveys of LysM-379

RLKs identified LjEPR3/MtLYK10 clade to be conserved in plant species capable of engaging in AMS, 380

suggesting a possible function during AMS (Bravo et al., 2016; Buendia et al., 2018). The likely rice 381

orthologue, OsLYK1, is induced by AMF and expressed in arbusculated cells, but oslyk1 mutants 382

showed no defects in AMS (Roth et al., 2018). Thus, whether the various mechanisms of symbiotic 383

scrutiny that are described for RNS also exist in AMS remain unknown. 384

RLKs and signalling networks are required in late stages of symbiosis 385

Apart from vesicle trafficking and nutrient exchange in sustaining AM symbiosis development (as 386

reviewed in Harrison and Ivanov, 2017; Chiu and Paszkowski, 2019), we now also appreciate the 387

existence of RLK-mediated signalling in symbiosis maintenance via novel and unknown signalling 388

cascades at the peri-arbuscular membrane (PAM). Rice ARBUSCLE RLK1 (OsARK1)/ Medicago 389

KINASE3 (KIN3) encodes a serine/threonine RLK present in AM host species (Bravo et al., 2016; Roth 390

et al., 2018). Localised to the PAM, OsARK1 controls processes post arbuscule development, and is 391

required for sustaining fungal fitness during progressing symbiosis as reflected by the compromised 392

vesicle formation in Osark1 mutants (Roth et al., 2018). Vesicles emerge as lipid storage bodies and 393

could be crucial for subsequent rounds of infection affected in Osark1 mutants. Interestingly, the 394

Osark1 phenotype is rescued in the presence of a common mycorrhizal network where AMF are 395

supported by wild-type plants, suggesting that OsARK1 is required for fungal vigour (Roth et al., 396

2018). The OsARK1 signalling mechanisms are still unknown. Whether kinase activity is required for 397

its symbiotic role, and whether it is required to suppress defence signalling also remains to be 398

shown. 399

On the other hand, immune suppression is required for the full development of functional nitrogen-400

fixing symbiosis, especially when bacteria in infection threads are released into nodules. In many 401

non-fixing nodulating mutants, strong immune responses lead to white, necrotic, non-fixing nodules, 402

highlighting the need for immune suppression for continued symbiosis. Medicago SYMBIOTIC 403

CYSTEINE-RICH RLK (MtSymCRK) is the only cysteine-rich RLK known to have a symbiotic function so 404

far (Berrabah et al., 2014); whereas the other members of the RLK family have known roles in 405

defence, abiotic stress response and programmed cell death. Recently, it was demonstrated that 406

MtSymCRK works through ethylene signalling (Berrabah et al., 2018) as well as the CDPK-Rboh 407

signalling axis to regulate immune responses in nodules (Yu et al., 2018). 408

Secreted, cysteine-rich peptides provide another mechanism for exercising host-symbiont 409

compatibility, especially for symbiotic function (N-fixation). These peptides are typically regarded as 410

antimicrobial defense peptides (defensins). Nodule cysteine rich (NCR) peptides comprise an 411

expanded, large gene family in Inverted Repeat-Lacking Clade (IRLC) legumes. The small, white, non-412

fixing nodules in mutants lacking specific NCRs point to an essential function in developing functional 413

RNS (Horvath et al., 2015; Kim et al., 2015). Majority of NCRs are targeted to the bacteria, where 414

they are proposed to act in ensuring terminal differentiation of the symbionts into bacteroids. At the 415

same time, rhizobia bacteria are capable of degrading NCRs, illustrating a molecular dialogue at late 416

symbiotic stages (Price et al., 2015). Excessive levels of NCRs are detrimental to RNS; thus quantity, 417

combination of NCRs and bacterial strains are important determinants of symbiotic outcome (Pan 418

and Wang, 2017). However, other mechanisms of scrutiny at the stage of N-fixation probably exist, 419

as NCRs appear to have arisen in IRLC legumes with indeterminate nodules (where meristem is 420

maintained and bacteroids terminally differentiated), independently in dalbergoid legumes (e.g. 421



11

Aeschynomene) (Czernic et al., 2015), and not in legumes with determinate nodules such as soybean 422

where phytoalexin accumulation and hypersensitive response appear to play a role (Parniske et al., 423

1990; Mergaert et al., 2003). The existence of symbiotic scrutiny up to the late stages of symbiosis is 424

perhaps driven by the need to monitor and terminate nutritional exchanges. 425

Taken together, immune modulation for symbiosis is a recurring requirement from pre-contact 426

signal exchange to intimate endosymbiotic accommodation. 427

Peptide ligands and cognate RLKs enforce host control of the extent of symbiosis development 428

Because symbiosis with micro-organisms come at a cost mostly but not limited to carbon, the extent 429

of microbial proliferation in situ needs to be balanced to the nutrient demands of the plant. To 430

achieve this, signal perception by RLKs also activates negative regulatory mechanisms, which act 431

systemically via another set of RLKs (Figure 3). 432

Autoregulatory mechanisms involve systemic peptide transport, and are common to both rhizobia-433

legume symbiosis and AMS. RWP-RK type transcriptional regulators of the NIN/NIN-like protein 434

(NLP) family, named after the conserved amino acid residues in the clade, activate the expression of 435

root-derived CLAVATA3/EMBRYO SURROUNDING REGION (CLE) peptides. Nod-factor perception 436

activates LjNIN, which transcriptionally induces LjCLE-RS1,2. In the shoot, they activate CLAVATA1-437

like LRR-RLKs Medicago SUPER NUMERIC NODULES1/ Lotus HYPERNODULATION ABERRANT ROOT1/ 438

Glycine NODULE AUTOREGULATION RECEPTOR KINASE1 (MtSUNN1/LjHAR1/GmNARK1) that repress 439

nodule formation in the roots (Krusell et al., 2002; Nishimura et al., 2002; Searle et al., 2003; Krusell 440

et al., 2011). Ligand-receptor binding of the glycosylated LjCLE-RS2 peptide to LjHAR1 has also been 441

demonstrated (Okamoto et al., 2013). Similar to the regulation of shoot apical meristem in 442

Arabidopsis, autoregulation of nodulation (AON) also require Medicago and Pea CLV2 and Medicago 443

CORYNE (MtCRN); and in Lotus, another LRR-RLK KLAVIER (LjKLV) is also involved (Miyazawa et al., 444

2010; Krusell et al., 2011; Crook et al., 2016), as summarised in Figure 3. In addition, signalling via 445

MtSUNN1/LjHAR1/GmNARK1 also integrates the plant nitrate status (Jeudy et al., 2010; Reid et al., 446

2011; Okamoto and Kawaguchi, 2015). Using a forward genetics screen for loss of nitrate-447

suppression of nodulation in Lotus or a reverse genetic screen for NLP mutants in Medicago, Lotus 448

NITRATE UNRESPONSIVE SYMBIOSIS1 (LjNRSYM1/NLP4) and MtNLP1 were identified to undergo 449

nitrate-triggered nuclear accumulation, inducing their downstream CLE-RS peptides (Lin et al., 2018; 450

Nishida et al., 2018). Together, nitrate status and rhizobia presence work via RWP-RK regulators 451

(NLPs) to induce specific and overlapping sets of CLE peptides that activate shoot CLV1-like RLKs 452

(Nishida and Suzaki, 2018). 453

One of the consequences of LjHAR1 activation is the downregulation of miR2111 production, a 454

mobile shoot-to-root signal delivered via the phloem. Over-expressing miR2111 resulted in 455

hypernodulation (Tsikou et al., 2018), as it targets Lotus TOO MUCH LOVE (TML), a Kelch F-box 456

protein that negatively regulates nodulation (Magori et al., 2009; Takahara et al., 2013). In 457

uninfected roots, low TML levels maintains susceptibility for rhizobia. In symbiotic plants, root-458

derived CLE peptides activates LjHAR1 in the shoot, which reduces miR2111 abundance in shoots 459

and roots, allowing LjTML to negatively regulate RNS (Tsikou et al., 2018). Another consequence of 460

LjHAR1 signalling is shoot-derived cytokinins, which also inhibit nodulation (Sasaki et al., 2014). 461

Meanwhile, the CLE-SUNN signalling module also regulates AMS. As in RNS, plant phosphate status 462

and AM colonisation induce root-derived CLE peptides that negatively regulate AM symbiosis. 463



12

Overexpression of Pi-induced MtCLE33, or AM-induced MtCLE53, reduced colonisation levels by 464

inhibiting expression of genes involved in SL biosynthesis and transport, leading to reduced SL levels 465

(Müller et al., 2019). Accordingly, the reduced AM colonisation could be overcome by exogenous 466

application of the synthetic SL analogue GR24. MtSUNN1 is required for CLE-mediated signalling 467

responses and is also involved in suppression of AM symbiosis under phosphate sufficiency (Müller 468

et al., 2019). Whether MtCLE33/53 directly bind to MtSUNN1 remains to be demonstrated, but a 469

common mode of systemic regulation is emerging from these recent findings (see (Kereszt et al., 470

2018; Müller and Harrison, 2019) for in depth reviews). As the CLE-SUNN/HAR mechanism for 471

autoregulation of AM colonisation (AOM) is present in Brachypodium distachyon (Müller et al., 2019) 472

and because tomato CLV2 is also involved in AOM (Wang et al., 2018), it is tempting to speculate 473

that this host-control mechanism may pre-date the evolution of RNS, and like the CSSP, this 474

signalling pathway may have been co-opted in the evolution of RNS to exert host control over the 475

extent of symbiosis. 476

Independent of LjHAR1/MtSUNN/GmNARK, another peptide-LRR-RLK pathway exists in parallel, 477

regulating nodulation and root development. C-terminally encoded peptides (CEPs) undergo 478

extensive post-translational modifications and have proposed roles in regulating plant development, 479

abiotic and biotic responses (Taleski et al., 2018). MtCEP1 inhibits lateral root emergence but 480

promotes nodule formation via separate pathways downstream of its putative receptor, Medicago 481

COMPACT ROOT ARCHITECTURE2 (MtCRA2). MtCRA2 acts locally to limit LR development, but its 482

systemic activity positively regulates nodule formation. And while MtCEP1-MtCRA2 regulation of LR 483

development is independent of CSSP and Medicago ETHYLENE INSENSITIVE2 (MtEIN2), regulation of 484

nodule development requires these signalling components, suggesting that two different pathways 485

may exist downstream of MtCRA2 (Mohd-Radzman et al., 2016; Laffont et al., 2019). Moreover, 486

expression of CEP peptides are also differentially regulated during AMS (de Bang et al., 2017), but 487

their role in regulating AMS awaits further investigation. 488

Conclusion and Perspectives 489

To perceive and engage with symbionts, plant roots recognise bacterial or fungal carbohydrate 490

molecules and orchestrate a series of signal exchanges before a mutually beneficial symbiosis is 491

established. Because of the rich understanding of the host signalling mechanisms relative to the 492

symbiont, this review focused on the roles of plant RLKs in recruiting and scrutinising endosymbionts 493

from pre-contact to termination of the association. It is still unclear how host-symbiont specificity, 494

especially for AMS, can be encoded in a rhizosphere where very similar carbohydrate molecules are 495

likely to be produced by different organisms. To date, the lack of genetically tractable AMF restricts 496

our understanding on the biosynthesis and relative importance of important fungal signalling 497

molecules, be they LCOs, COs or others. The most parsimonious hypothesis, based on the recent 498

discoveries, might be that the combinatorial and/or sequential perception of signalling molecules 499

including but not restricted to carbohydrates, activate host a set of host receptors for symbiosis 500

signalling. The present challenge (see Outstanding Questions) is to identify the range of signals for 501

AMF to explain its broad host range, and to explain how plants integrate the signals downstream of 502

perception and receptor activation. Moreover, although multiple classes of RLKs have been 503

identified to regulate various stages of symbiosis, there is a lack of understanding on their signalling 504

mechanisms. At the level of receptor complexes, membrane receptor domains and 505



13

phosphorylation/signal transduction cascade(s), we anticipate future discoveries to reveal shared 506

and diverging modes of receptor activities in the two most studied plant root endosymbioses. 507

508

509

510

Acknowledgements 511

C.H.C. is supported by a Gates Cambridge PhD Scholarship. Research in the laboratory of U.P. is 512

supported by the BBSRC Grant No. BB/P003419/1 and by the Bill & Melinda Gates Foundation as 513

OPP1028264 514

515



14

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976



ADVANCES

• Receptor-like kinases (RLKs) control different stages of symbiosis development.

• Recognition of carbohydrate molecules initiate signalling for root endosymbioses with rhizobia bacteria and arbuscular mycorrhizal fungi.

• Range of ligands that activate conserved symbiosis signalling is broader than expected, involving overlapping sets of Lysin-motif (LysM) receptors.

• RLKs in the shoot are regulated by systemically moving plant peptide hormones to enable plant control of symbiosis extent in endosymbiosis.



OUTSTANDING QUESTIONS

• What are the molecules produced by AM fungi perceived by plant RLKs/receptors for symbiosis signalling, and what are their cognate ligands?

• What are the mechanisms/ligands/receptors for achieving signalling specificities – in immunity vs symbiosis; and AM symbiosis vs nitrogen-fixing root nodule symbiosis?

• In cases where receptors are known, e.g. D14L, SYMRK, ARK1, SymCRK, what are their ligands and downstream signalling cascades?

• By understanding RLK-mediated signalling at various stages, especially symbiont compatibility in nitrogen-fixation, can we engineer more productive symbioses?



BOX 1. Overview of Plant Endosymbioses

Through symbiosis, plants may improve nutrient uptake, in particular of phosphorous and nitrogen. AM symbiosis between plants and the Glomeromycotinan fungi is evolutionarily ancient as evidenced by fossil records from the Rhynie Chert, and ecologically important for the biogeochemical fluxes and their consequences over the past 460 million years. The successful conquest of land plants is often attributed to the ability for symbiotic nutrient exchange of plant C for fungal P or N, enabled by a toolkit of receptors, kinases, transporters and transcriptional regulators that can be traced back to algal lineages. From the signalling toolkit enabling AM symbiosis arose nitrogen-fixing symbiosis c.100 million years ago, in the Fabales, Fagales, Cucurbitales and Rosales – where nitrogen-fixing diazotrophs are hosted in a lateral organ (nodule) to reduce atmospheric N2 into ammonium.

In the rhizosphere, plant roots exude a cocktail of chemical compounds – collectively known as root exudates, including sugars, amino acids, organic acids, enzymes, and other organic compounds. The concentration gradient of these chemicals provides positional information to the symbionts. In legume-rhizobia symbiosis, host-released flavonoids are perceived by rhizobia bacteria and activate the Nod operon via NodD, resulting in the activation of Nod genes for production of lipochito-oligosaccharides (LCOs) as well as changes in bacterial motility and growth. For RNS, host-symbiont specificity is relatively well-understood, with the majority of the specificity determined by specific flavonoid activating NodD of specific rhizobia species, and further by specific decorations onto LCOs that are perceived by the specific, cognate host high-affinity NF receptors.

Perception of NF activates membrane depolarisation, cytosolic calcium influx, perinuclear calcium spiking, cytoskeletal rearrangements, root hair deformation and curling. Sustained signal exchange with the rhizobial bacteria develops an infection thread; and concomitant signal exchange with the cortex and xylem pole pericycle determines whether nodule organogenesis occurs for eventual bacteria release into the nodule; or the abortion of infection thread without nodule formation.

In AM symbiosis (AMS), perception of root-released strigolactones (SL), flavonoids, hydroxy-fatty acids and and N-acetylglucosamine (GlcNAc) derivatives trigger different fungal responses and branching patterns towards the host. SL perception also induces AM fungi (AMF) to increase the production of short chain chitin oligomers (CO4-5), which are perceived by the host. AMF also produces LCOs structurally similar to NFs, with CO4-5 linked to C16:0 or C18:1 acyl groups that may or may not be sulphated on the non-reducing end. Chitooctaose (CO8), have recently been demonstrated to be capable of activating plant symbiosis signalling. Hyphopodia, a swollen, branched fungal structure forms upon fungal contact with the root surface. The fungus then invades the outer root cell layers, eventually forming arbuscules in the cortex cells. Symbiotic nutrient transfer occurs at these highly ramified but ephemeral structures. Bi-directional nutrient transfer regulates the full development of arbuscules, and their subsequent senescence coincides with the formation of fungal lipid storage vesicles and spores. In contrast to RNS, how AMF achieves broad host specificity is so far unclear.



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Figure 1: LysM-RLKs in symbiosis signalling and beyond

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Figure 2: Post-transcriptional regulation of RLKs

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Figure 3: Systemic regulation of symbiosis signalling



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https://www.ncbi.nlm.nih.gov/pubmed?term=Buendia%20L%252C%20Wang%20T%252C%20Girardin%20A%252C%20Lefebvre%20B%20%25282016%2529%20The%20LysM%20receptor%252Dlike%20kinase%20SlLYK10%20regulates%20the%20arbuscular%20mycorrhizal%20symbiosis%20in%20tomato%252E%20New%20Phytol%20210%253A%20184%2526%2523x&dopt=abstract

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Receptor-like kinases sustain symbiotic scrutiny · 24 relationships where symbiosis is...

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Transcript of Receptor-like kinases sustain symbiotic scrutiny · 24 relationships where symbiosis is...