An immune receptor complex evolved in soybean to perceive a polymorphic bacterial flagellin

Wei, Yali; Balaceanu, Alexandra; Rufián, José S.; Segonzac, Cécile; Zhao, Achen; Morcillo, Rafael J. L.; Macho, Alberto P.

doi:10.1038/s41467-020-17573-y

Cited by 64 publications

(55 citation statements)

References 65 publications

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“…The number of upregulated heat shock proteins sequentially increases in the treatment order from low- (SJ4M = 1) to medium- (SS1M = 4; SF2M = 4) to high-efficiency strains (SF4M = 7; SF8M = 11). More components at early steps of the MAPK pathway initiated by MAMP (microbe-associated molecular patterns) ( 76 ) are downregulated in the treatment of SJ4M, such as the cell surface immune receptor FLS2 recognizing bacterial flagellin ( 77 , 78 ), seven RLCKs (receptor-like cytoplasmic kinases), and three MAPKs including a GmMEKK1 homolog (Gm.14G165700) negatively regulating defense responses ( 79 ). The thiol tripeptide glutathione is a well-known antioxidant and redox buffer ( 80 ), and glutathione S -transferase can conjugate target molecules to glutathione and act as a glutathione peroxidase to scavenge peroxides such as H 2 O 2 ( 80 ).…”

Section: Resultsmentioning

confidence: 99%

Lineage-Specific Rewiring of Core Pathways Predating Innovation of Legume Nodules Shapes Symbiotic Efficiency

et al. 2021

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The interkingdom coevolution innovated the rhizobium-legume symbiosis. The application of this nitrogen-fixing system in sustainable agriculture is usually impeded by incompatible interactions between partners. However, the progressive evolution of rhizobium-legume compatibility remains elusive. In this work, deletions of rhcV encoding a structural component of the type three secretion system allow related Sinorhizobium strains to nodulate a previously incompatible soybean cultivar (Glycine max). These rhcV mutants show low to medium to high symbiotic efficiency on the same cultivated soybean while being indistinguishable on wild soybean plants (Glycine soja). The dual pantranscriptomics reveals nodule-specific activation of core symbiosis genes of Sinorhizobium and Glycine genes associated with genome duplication events along the chronogram. Unexpectedly, symbiotic efficiency is in line with lineage-dependent transcriptional profiles of core pathways which predate the diversification of Fabaceae and Sinorhizobium. This is supported by further physiological and biochemical experiments. Particularly, low-efficiency nodules show disordered antioxidant activity and low-energy status, which restrict nitrogen fixation activity. Collectively, the ancient core pathways play a crucial role in optimizing the function of later-evolved mutualistic arsenals in the rhizobium-legume coevolution. IMPORTANCE Significant roles of complex extracellular microbiota in environmental adaptation of eukaryotes in ever-changing circumstances have been revealed. Given the intracellular infection ability, facultative endosymbionts can be considered pioneers within complex extracellular microbiota and are ideal organisms for understanding the early stage of interkingdom adaptation. This work reveals that the later innovation of key symbiotic arsenals and the lineage-specific network rewiring in ancient core pathways, predating the divergence of legumes and rhizobia, underline the progressive evolution of rhizobium-legume compatibility. This insight not only is significant for improving the application benefits of rhizobial inoculants in sustainable agriculture but also advances our general understanding of the interkingdom coevolution which is theoretically explored by all host-microbiota interactions.

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Section: Resultsmentioning

confidence: 99%

Lineage-Specific Rewiring of Core Pathways Predating Innovation of Legume Nodules Shapes Symbiotic Efficiency

et al. 2021

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“…This process yielded 2,404 peptides, encompassing 1,059 distinct peptide sequences. As an initial prediction of which flg22 epitopes might be highly immunogenic to A. thaliana , we queried the sequences for the motif 11 [ST]xx[DN][DN]xAGxxI 21 , which includes amino acids important for activation of the FLS2 - BRASSINOSTEROID INSENSITIVE1-ASSOCIATED KINASE1 (BAK1) immune signaling complex (Felix et al 1999; Sun et al 2013; Wei et al 2020). We allowed for Ser or Thr at residue 11 as these amino acids have similar properties, while the flexibility of Asp or Asn at residues 14 and 15 was based on their functional interchangeability at residue 14 in the flg22 epitope of X. campestris (Sun et al 2006).…”

Section: Main Textmentioning

confidence: 99%

“…In a particularly notable example, the FLS2 XL protein of Vitis riparia (riverbank grape) triggers a strong immune response following perception of the flg22 epitope of A. tumefaciens (Fürst et al 2020), which is similar in sequence to flg22-α and is a classical example of a “non-immunogenic” flg22 epitope based on studies with A. thaliana and tomato (Felix et al 1999). Similarly, the FLS2 protein of Glycine max (soybean) can trigger an immune response upon exposure to the flg22 epitope of R. solanacearum (Wei et al 2020), despite this epitope being non-immunogenic in A. thaliana and tomato (Pfund et al 2004; Mueller et al 2012). As such, it would be interesting to examine if the five flg22 peptides tested here trigger stronger immune responses in other plant species, and whether there is a relationship between flg22-FLS2 specificity and the host range of the microbes.…”

Section: Main Textmentioning

confidence: 99%

Proteobacteria encode diverse flg22 peptides that elicit varying immune responses inArabidopsis thaliana

Cheng

Bredow

Monaghan

et al. 2020

Preprint

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Bacterial flagellin protein is a potent microbe-associated molecular pattern. Immune responses are triggered by a 22 amino acid epitope derived from flagellin, known as flg22, upon detection by the pattern recognition receptor FLAGELLIN-SENSING2 (FLS2) in multiple plant species. However, increasing evidence suggests that flg22 epitopes of several bacterial species are not universally immunogenic to plants. We investigated whether flg22 immunogenicity systematically differs between classes of the phylum Proteobacteria, using a dataset of 2,470 flg22 sequences. To predict which species encode highly immunogenic flg22 epitopes, we queried a custom motif (11[ST]xx[DN][DN]xAGxxI21) in the flg22 sequences, followed by sequence conservation analysis and protein structural modelling. These data led us to hypothesize that most flg22 epitopes of the γ- and β-Proteobacteria are highly immunogenic, whereas most flg22 epitopes of the α-, δ-, and ε-Proteobacteria are weakly to moderately immunogenic. To test this hypothesis, we generated synthetic peptides representative of the flg22 epitopes of each proteobacterial class, and we monitored their ability to elicit an immune response in Arabidopsis thaliana. Flg22 peptides of the γ- and β-Proteobacteria triggered strong oxidative bursts, whereas peptides from the ε-, δ-, and α-Proteobacteria triggered moderate, weak, or no response, respectively. These data suggest flg22 immunogenicity is not highly conserved across the phylum Proteobacteria. We postulate that sequence divergence of each taxonomic class was present prior to the evolution of FLS2, and that the ligand specificity of A. thaliana FLS2 was driven by the flg22 epitopes of the γ- and β-proteobacteria, a monophyletic group containing many common phytopathogens.

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“…Concomitantly, some bacterial wilt pathogens have evolved modifications in the sequences of their conserved patterns, so that they are no longer recognizable by cognate PRRs. This occurs in X. fastidiosa , which contains a lipopolysaccharide featuring a masking motif that evades recognition by grapevine ( Rapicavoli et al , 2018 ), or flagellin from R. solanacearum , with a polymorphic sequence that avoids perception by many host plants ( Wei et al , 2020 ).…”

Section: Introductionmentioning

confidence: 99%

Blocking intruders: inducible physico-chemical barriers against plant vascular wilt pathogens

Kashyap

Planas-Marquès

Capellades

et al. 2020

Journal of Experimental Botany

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Xylem vascular wilt pathogens cause some of the most devastating diseases in plants. Proliferation of these pathogens in the xylem tissue causes massive disruption of water and mineral transport, resulting in severe wilting and death of the infected plants. Upon reaching the xylem vascular tissue, these pathogens multiply profusely and later spread vertically within the xylem sap and horizontally between vessels and to the surrounding tissues. Plant resistance to these pathogens is very complex. One of the most effective defense responses in resistant plants is the formation of physico-chemical barriers in the xylem tissue upon pathogen perception. Vertical spread within the vessel lumen is restricted by structural barriers namely, tyloses and gels. Further, horizontal spread to the apoplast and surrounding healthy vessels and tissues is prevented by vascular coating of the colonized vessels mainly with lignin and suberin. Both vertical and horizontal barriers compartmentalize the pathogen at the site of infection and contribute to their elimination. Induction of these defenses must be tightly coordinated, both in time and space to avoid detrimental consequences for the plant such as cavitation and embolism. Here we discuss the current knowledge on mechanisms underlying plant inducible structural barriers against major xylem colonizing pathogens. This knowledge may be applied to engineering metabolic pathways of vascular coating compounds in specific cells, to produce resistant plants against xylem colonizers.

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An immune receptor complex evolved in soybean to perceive a polymorphic bacterial flagellin

Cited by 64 publications

References 65 publications

Lineage-Specific Rewiring of Core Pathways Predating Innovation of Legume Nodules Shapes Symbiotic Efficiency

Lineage-Specific Rewiring of Core Pathways Predating Innovation of Legume Nodules Shapes Symbiotic Efficiency

Proteobacteria encode diverse flg22 peptides that elicit varying immune responses inArabidopsis thaliana

Blocking intruders: inducible physico-chemical barriers against plant vascular wilt pathogens

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