Distinct immune sensor systems for fungal endopolygalacturonases in closely related Brassicaceae

Zhang, Lisha; Hua, Chenlei; Pruitt, Rory; Qin, Si; Wang, Lei; Albert, Isabell; Albert, Markus; Kan, Jan A.L. van; Nuernberger, Thorsten

doi:10.1038/s41477-021-00982-2

Cited by 51 publications

(55 citation statements)

References 32 publications

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“…Distribution of LRR-RP-type PRRs is remarkably restricted to individual plant genera. Functional homologs of Arabidopsis RLP1, RLP23, and RLP42 are only found in this genus as well as in a few related Brassicaceae 17,40,41 . Likewise, a tomato receptor for fungal xylanase (EIX2), N. benthamiana sensors for CspA (CSPR, CORE), and a fungal hydrolase (RXEG1) exhibit genusspecific distribution 21,22,42,43 .…”

Section: Discussionmentioning

confidence: 99%

Genotyping-by-sequencing-based identification of Arabidopsis pattern recognition receptor RLP32 recognizing proteobacterial translation initiation factor IF1

et al. 2022

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Activation of plant pattern-triggered immunity (PTI) relies on the recognition of microbe-derived structures, termed patterns, through plant-encoded surface-resident pattern recognition receptors (PRRs). We show that proteobacterial translation initiation factor 1 (IF1) triggers PTI in Arabidopsis thaliana and related Brassicaceae species. Unlike for most other immunogenic patterns, IF1 elicitor activity cannot be assigned to a small peptide epitope, suggesting that tertiary fold features are required for IF1 receptor activation. We have deployed natural variation in IF1 sensitivity to identify Arabidopsis leucine-rich repeat (LRR) receptor-like protein 32 (RLP32) as IF1 receptor using a restriction site-associated DNA sequencing approach. RLP32 confers IF1 sensitivity to rlp32 mutants, IF1-insensitive Arabidopsis accessions and IF1-insensitive Nicotiana benthamiana, binds IF1 specifically and forms complexes with LRR receptor kinases SOBIR1 and BAK1 to mediate signaling. Similar to other PRRs, RLP32 confers resistance to Pseudomonas syringae, highlighting an unexpectedly complex array of bacterial pattern sensors within a single plant species.

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Section: Discussionmentioning

confidence: 99%

Genotyping-by-sequencing-based identification of Arabidopsis pattern recognition receptor RLP32 recognizing proteobacterial translation initiation factor IF1

et al. 2022

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“…Remarkably, LbGH28 knockdown mutants of L. bicolor were found to be deficient in their ability to form Haritg nets ( Zhang et al, 2021b ). As LbGH28A was shown to be an active endopolygalacturonase with pectinase activity, Zhang et al (2021b) suggest that LbGH28 may be involved in remodeling the middle lamella through pectin hydrolysis, thus playing an essential role in plant-fungal symbiosis.…”

Section: Secreted Gh Proteins From Plant-associated Fungi and Oomycet...mentioning

confidence: 99%

“…One such example is a GH28-encoding gene from the ectomycorrhizal fungus Laccaria bicolor, LbGH28A, which was found to be induced during the formation of ectomycorrhiza in Populus trichocarpa ( Veneault-Fourrey et al, 2014) and P. tremula x alba (Zhang et al, 2021b). Immunocytolocalisation of LbGH28A demonstrated that the protein was present at hyphal tips within the Hartig net (Zhang et al, 2021b), which is formed by a network of hyphae growing between the rhizodermal cells of the plant to create a symbiotic interface through which nutrients are exchanged (Becquer et al, 2019). Remarkably, LbGH28 knockdown mutants of L. bicolor were found to be deficient in their ability to form Haritg nets (Zhang et al, 2021b).…”

Section: Secreted Glycoside Hydrolase Family 28 (Gh28) Proteinsmentioning

confidence: 99%

“…Immunocytolocalisation of LbGH28A demonstrated that the protein was present at hyphal tips within the Hartig net (Zhang et al, 2021b), which is formed by a network of hyphae growing between the rhizodermal cells of the plant to create a symbiotic interface through which nutrients are exchanged (Becquer et al, 2019). Remarkably, LbGH28 knockdown mutants of L. bicolor were found to be deficient in their ability to form Haritg nets (Zhang et al, 2021b). As LbGH28A was shown to be an active endopolygalacturonase with pectinase activity, Zhang et al (2021b) suggest that LbGH28 may be involved in remodeling the middle lamella through pectin hydrolysis, thus playing an essential role in plant-fungal symbiosis.…”

Section: Secreted Glycoside Hydrolase Family 28 (Gh28) Proteinsmentioning

confidence: 99%

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Secreted Glycoside Hydrolase Proteins as Effectors and Invasion Patterns of Plant-Associated Fungi and Oomycetes

et al. 2022

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During host colonization, plant-associated microbes, including fungi and oomycetes, deliver a collection of glycoside hydrolases (GHs) to their cell surfaces and surrounding extracellular environments. The number and type of GHs secreted by each organism is typically associated with their lifestyle or mode of nutrient acquisition. Secreted GHs of plant-associated fungi and oomycetes serve a number of different functions, with many of them acting as virulence factors (effectors) to promote microbial host colonization. Specific functions involve, for example, nutrient acquisition, the detoxification of antimicrobial compounds, the manipulation of plant microbiota, and the suppression or prevention of plant immune responses. In contrast, secreted GHs of plant-associated fungi and oomycetes can also activate the plant immune system, either by acting as microbe-associated molecular patterns (MAMPs), or through the release of damage-associated molecular patterns (DAMPs) as a consequence of their enzymatic activity. In this review, we highlight the critical roles that secreted GHs from plant-associated fungi and oomycetes play in plant–microbe interactions, provide an overview of existing knowledge gaps and summarize future directions.

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“…Finally, the inceptin receptor (INR) appears to be specific to the legume tribe Phaseoleae and recognizes inceptin (In11), a HAMP found in the oral secretion of multiple caterpillars [31][32][33][34] . Notably, all the above examples of LRR-RLPs are family-specific, restricted to the Solanaceae (Cf-2, Cf-4, Cf-9 and CuRe1), Brassicaceae (RLP23, RLP42, ReMAX) or Leguminosae (tribe Phaseoleae) (INR) 17,26 . However, despite clear signatures of lineage-specific functions, specific evolutionary steps leading to novel PRR functions across multiple species have not been described.…”

Section: Introductionmentioning

confidence: 99%

Evolutionary gain and loss of a plant pattern-recognition receptor for HAMP recognition

Snoeck

Abramson

Garcia

et al. 2022

Preprint

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Pattern recognition receptors (PRR) recognize distinct pathogen and herbivore-associated molecular patterns (PAMPs and HAMPs) and mediate activation of immune responses, but the evolution of new PRR sensing functions is not well understood. We employed comparative genomics and functional analysis to define evolutionary events leading to the sensing of the peptide HAMP inceptin (In11) by the PRR Inceptin Receptor (INR). Existing and de novo genome assemblies revealed that the presence of a functional INR gene corresponded with In11 response across 55 million years (my) of legume evolution, and that In11 recognition is unique to the clade of Phaseoloid legumes. The INR loci of certain Phaseoloid and non-Phaseoloid species also contain diverse INR-like homologues, suggesting that the evolution of INR receptor function ~28 mya occurred after an ancestral gene insertion ~32 mya. Functional analysis of chimeric and ancestrally reconstructed receptors revealed that specific AA differences in the C1 leucine-rich repeat (LRR) domain and C2 intervening motif likely mediated gain of In11 recognition. In summary, we present a conceptual model for the evolution of a defined PRR function based on patterns of INR variation in legumes.

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Distinct immune sensor systems for fungal endopolygalacturonases in closely related Brassicaceae

Cited by 51 publications

References 32 publications

Genotyping-by-sequencing-based identification of Arabidopsis pattern recognition receptor RLP32 recognizing proteobacterial translation initiation factor IF1

Genotyping-by-sequencing-based identification of Arabidopsis pattern recognition receptor RLP32 recognizing proteobacterial translation initiation factor IF1

Secreted Glycoside Hydrolase Proteins as Effectors and Invasion Patterns of Plant-Associated Fungi and Oomycetes

Evolutionary gain and loss of a plant pattern-recognition receptor for HAMP recognition

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