An oomycete NLP cytolysin forms transient small pores in lipid membranes

Pirc, Katja; Clifton, Luke A.; Yilmaz, Neval; Saltalamacchia, Andrea; Mally, Mojca; Snoj, Tina; Žnidaršič, Nada; Srnko, Marija; Borišek, Jure; Parkkila, Petteri; Albert, Isabell; Podobnik, Marjetka; Numata, Keiji; Nürnberger, Thorsten; Derganc, Jure; Magistrato, Alessandra; Lakey, Jeremy H.; Anderluh, Gregor

doi:10.1126/sciadv.abj9406

Cited by 15 publications

(19 citation statements)

References 67 publications

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“…In the example of wounding, release of amino acids likely occurs via the loss of membrane integrity that occurs during wounding and leakage of cell contents into the apoplastic space. However, in the case of touch or osmotic stress, how amino acids are rapidly released is less clear, but possibilities include that cellular stress responses involve the rapid activation of amino acid transporters, the exocytic release of amino acid containing vesicles as in neurotransmission in animals, or possibly by transient and nanoscale ruptures in the plasma membrane that allow leakage of cell contents ( 27 , 28 ). Having observed that living cells release amino acids that signal to neighboring cells ( Fig.…”

Section: Discussionmentioning

confidence: 99%

Diffusion and bulk flow of amino acids mediate calcium waves in plants

et al. 2022

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In plants, a variety of stimuli trigger long-range calcium signals that travel rapidly along the vasculature to distal tissues via poorly understood mechanisms. Here, we use quantitative imaging and analysis to demonstrate that traveling calcium waves are mediated by diffusion and bulk flow of amino acid chemical messengers. We propose that wounding triggers release of amino acids that diffuse locally through the apoplast, activating the calcium-permeable channel GLUTAMATE RECEPTOR-LIKE 3.3 as they pass. Over long distances through the vasculature, the wound-triggered dynamics of a fluorescent tracer show that calcium waves are likely driven by bulk flow of a channel-activating chemical. We observed that multiple stimuli trigger calcium waves with similar dynamics, but calcium waves alone cannot initiate all systemic defense responses, suggesting that mobile chemical messengers are a core component of complex systemic signaling in plants.

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Section: Discussionmentioning

confidence: 99%

Diffusion and bulk flow of amino acids mediate calcium waves in plants

et al. 2022

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“…Candidate genes from six classes that have been characterised as virulence factors in other Phytophthora species ( Hua et al, 2013 ; Ma et al, 2015 ; Amaro et al, 2017 ; Chepsergon et al, 2020 ; Pirc et al, 2022 ) were selected for further investigation. These are genes encoding candidate cytoplasmic RXLR and CRN effectors, apoplastic effectors including elicitins, NLPs, CAZymes, and GPCRs involved in signaling ( Supplementary Table S2 ).…”

Section: Resultsmentioning

confidence: 99%

Chromosome-level assembly of the Phytophthora agathidicida genome reveals adaptation in effector gene families

et al. 2022

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Phytophthora species are notorious plant pathogens, with some causing devastating tree diseases that threaten the survival of their host species. One such example is Phytophthora agathidicida, the causal agent of kauri dieback – a root and trunk rot disease that kills the ancient, iconic and culturally significant tree species, Agathis australis (New Zealand kauri). A deeper understanding of how Phytophthora pathogens infect their hosts and cause disease is critical for the development of effective treatments. Such an understanding can be gained by interrogating pathogen genomes for effector genes, which are involved in virulence or pathogenicity. Although genome sequencing has become more affordable, the complete assembly of Phytophthora genomes has been problematic, particularly for those with a high abundance of repetitive sequences. Therefore, effector genes located in repetitive regions could be truncated or missed in a fragmented genome assembly. Using a combination of long-read PacBio sequences, chromatin conformation capture (Hi-C) and Illumina short reads, we assembled the P. agathidicida genome into ten complete chromosomes, with a genome size of 57 Mb including 34% repeats. This is the first Phytophthora genome assembled to chromosome level and it reveals a high level of syntenic conservation with the complete genome of Peronospora effusa, the only other completely assembled genome sequence of an oomycete. All P. agathidicida chromosomes have clearly defined centromeres and contain candidate effector genes such as RXLRs and CRNs, but in different proportions, reflecting the presence of gene family clusters. Candidate effector genes are predominantly found in gene-poor, repeat-rich regions of the genome, and in some cases showed a high degree of duplication. Analysis of candidate RXLR effector genes that occur in multicopy gene families indicated half of them were not expressed in planta. Candidate CRN effector gene families showed evidence of transposon-mediated recombination leading to new combinations of protein domains, both within and between chromosomes. Further analysis of this complete genome assembly will help inform new methods of disease control against P. agathidicida and other Phytophthora species, ultimately helping decipher how Phytophthora pathogens have evolved to shape their effector repertoires and how they might adapt in the future.

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“…On the basis of their impacts on host plants, NLPs are classified into two forms: cytotoxic to eudicot and monocot plants and noncytotoxic [ 59 , 65 , 76 ]. Cytotoxic NLPs are expressed when a pathogen converts from biotrophy into necrotrophy and function as pore-forming toxins (PFTs), and these NLPs bind to the terminal monomeric hexose moieties of glycosyl inositol phosphoryl ceramide (GIPC) to cause cytolysis [ 65 , 76 , 77 , 78 ]. Noncytotoxic NLPs induce an immune response without cytolysis.…”

Section: Nlpsmentioning

confidence: 99%

“…As mentioned above, cytotoxic NLPs target and bind to the terminal hexose residues of glycosylinositol phosphorylceramide (GIPC) sphingolipids, which vary in total amount and concentration among different plants, which are located at the outer leaflet of the envelope membrane in plants [ 59 , 65 ]. The binding of GIPC-NLP is driven by electrostatic interactions, which can be strengthened in the presence of sterols and results in NLP conformational changes [ 65 , 77 , 86 ]. After binding, NLPs form functional oligomers and then form shallow transient pores that leak small molecules [ 77 , 87 ].…”

Section: Nlpsmentioning

confidence: 99%

Characteristics, Roles and Applications of Proteinaceous Elicitors from Pathogens in Plant Immunity

Liu²,

Ma³

et al. 2023

Life

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In interactions between pathogens and plants, pathogens secrete many molecules that facilitate plant infection, and some of these compounds are recognized by plant pattern recognition receptors (PRRs), which induce immune responses. Molecules in both pathogens and plants that trigger immune responses in plants are termed elicitors. On the basis of their chemical content, elicitors can be classified into carbohydrates, lipopeptides, proteinaceous compounds and other types. Although many studies have focused on the involvement of elicitors in plants, especially on pathophysiological changes induced by elicitors in plants and the mechanisms mediating these changes, there is a lack of up-to-date reviews on the characteristics and functions of proteinaceous elicitors. In this mini-review, we provide an overview of the up-to-date knowledge on several important families of pathogenic proteinaceous elicitors (i.e., harpins, necrosis- and ethylene-inducing peptide 1 (nep1)-like proteins (NLPs) and elicitins), focusing mainly on their structures, characteristics and effects on plants, specifically on their roles in plant immune responses. A solid understanding of elicitors may be helpful to decrease the use of agrochemicals in agriculture and gardening, generate more resistant germplasms and increase crop yields.

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An oomycete NLP cytolysin forms transient small pores in lipid membranes

Cited by 15 publications

References 67 publications

Diffusion and bulk flow of amino acids mediate calcium waves in plants

Diffusion and bulk flow of amino acids mediate calcium waves in plants

Chromosome-level assembly of the Phytophthora agathidicida genome reveals adaptation in effector gene families

Characteristics, Roles and Applications of Proteinaceous Elicitors from Pathogens in Plant Immunity

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