Emerging Roles of Cyst Nematode Effectors in Exploiting Plant Cellular Processes

Gardner, Michael; Verma, Anju; Mitchum, Melissa G.

doi:10.1016/bs.abr.2014.12.009

Cited by 23 publications

(19 citation statements)

References 112 publications

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“…Based on data from the current study and previous literature, we concluded that nematode invasion activates PTI responses, which are suppressed during later stages of nutrient acquisition and feeding site development. Indeed, an increasing number of nematode effectors involved in suppression of PTI have been characterised during last few years [8, 10, 18, 22, 23]. …”

Section: Discussionmentioning

confidence: 99%

“…In a compatible plant-nematode interaction, plant defence responses are either down-regulated or overcome by the nematodes [4–6]. A cocktail of secreted molecules including effectors that are synthesized in the oesophageal glands of the nematodes is purportedly responsible for modulating the plant defences as well as the induction and development of the syncytium [7–10]. Whereas most root-knot nematodes reproduce parthenogenically, cyst nematodes reproduce sexually.…”

Section: Introductionmentioning

confidence: 99%

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Arabidopsis leucine-rich repeat receptor–like kinase NILR1 is required for induction of innate immunity to parasitic nematodes

et al. 2017

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Plant-parasitic nematodes are destructive pests causing losses of billions of dollars annually. An effective plant defence against pathogens relies on the recognition of pathogen-associated molecular patterns (PAMPs) by surface-localised receptors leading to the activation of PAMP-triggered immunity (PTI). Extensive studies have been conducted to characterise the role of PTI in various models of plant-pathogen interactions. However, far less is known about the role of PTI in roots in general and in plant-nematode interactions in particular. Here we show that nematode-derived proteinaceous elicitor/s is/are capable of inducing PTI in Arabidopsis in a manner dependent on the common immune co-receptor BAK1. Consistent with the role played by BAK1, we identified a leucine-rich repeat receptor-like kinase, termed NILR1 that is specifically regulated upon infection by nematodes. We show that NILR1 is essential for PTI responses initiated by nematodes and nilr1 loss-of-function mutants are hypersusceptible to a broad category of nematodes. To our knowledge, NILR1 is the first example of an immune receptor that is involved in induction of basal immunity (PTI) in plants or in animals in response to nematodes. Manipulation of NILR1 will provide new options for nematode control in crop plants in future.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Arabidopsis leucine-rich repeat receptor–like kinase NILR1 is required for induction of innate immunity to parasitic nematodes

et al. 2017

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“…Despite having independent evolutionary origins, this feeding on host cells by plant parasites of entirely different clades can induce similar responses in host cells and surrounding tissue. It is well established that effectors and other biologically active compounds in nematode secretions are required for specific host cell responses to enable prolonged feeding by the most advanced sedentary plant parasitic nematodes (Mitchum et al, 2013;Gardner et al, 2015). Perhaps, convergent evolution and horizontal gene transfers have also led to parallel adaptations in the molecular make-up of secretions of nematodes from entirely distinct lineages of plant parasites (Bird et al, 2015;Kikuchi et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

“…We will therefore not discuss components of plant innate immunity, as these have been recently covered elsewhere (Goverse and Smant, 2014;Holbein et al, 2016). Similarly, for a detailed update on various roles of nematode effectors in feeding cell formation, we refer the reader to recent review papers on this topic (Gardner et al, 2015;Truong et al, 2015;Ali et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

Parallel adaptations and common host cell responses enabling feeding of obligate and facultative plant parasitic nematodes

2018

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SUMMARYParallel adaptations enabling the use of plant cells as the primary food source have occurred multiple times in distinct nematode clades. The hallmark of all extant obligate and facultative plant-feeding nematodes is the presence of an oral stylet, which is required for penetration of plant cell walls, delivery of pharyngeal gland secretions into host cells and selective uptake of plant assimilates. Plant parasites from different clades, and even within a single clade, display a large diversity in feeding behaviours ranging from short feeding cycles on single cells to prolonged feeding on highly sophisticated host cell complexes. Despite these differences, feeding of nematodes frequently (but certainly not always) induces common responses in host cells (e.g. endopolyploidization and cellular hypertrophy). It is thought that these host cell responses are brought about by the interplay of effectors and other biological active compounds in stylet secretions of feeding nematodes, but this has only been studied for the most advanced sedentary plant parasites. In fact, these responses are thought to be fundamental for prolonged feeding of sedentary plant parasites on host cells. However, as we discuss in this review, some of these common plant responses to independent lineages of plant parasitic nematodes might also be generic reactions to cell stress and as such their onset may not require specific inputs from plant parasitic nematodes. Sedentary plant parasitic nematodes may utilize effectors and their ability to synthesize other biologically active compounds to tailor these common responses for prolonged feeding on host cells.

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“…Protein sequences of effectors reported in the root-knot and cyst nematodes [34][35][36][37] were obtained from GenBank. Blast was used to predict putative homologous effectors from D. destructor.…”

Section: (E) Expert Functional Annotationmentioning

confidence: 99%

TheDitylenchus destructorgenome provides new insights into the evolution of plant parasitic nematodes

et al. 2016

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Plant-parasitic nematodes were found in 4 of the 12 clades of phylum Nematoda. These nematodes in different clades may have originated independently from their free-living fungivorous ancestors. However, the exact evolutionary process of these parasites is unclear. Here, we sequenced the genome sequence of a migratory plant nematode, Ditylenchus destructor. We performed comparative genomics among the free-living nematode, Caenorhabditis elegans and all the plant nematodes with genome sequences available. We found that, compared with C. elegans, the core developmental control processes underwent heavy reduction, though most signal transduction pathways were conserved. We also found D. destructor contained more homologies of the key genes in the above processes than the other plant nematodes. We suggest that Ditylenchus spp. may be an intermediate evolutionary history stage from free-living nematodes that feed on fungi to obligate plantparasitic nematodes. Based on the facts that D. destructor can feed on fungi and has a relatively short life cycle, and that it has similar features to both C. elegans and sedentary plant-parasitic nematodes from clade 12, we propose it as a new model to study the biology, biocontrol of plant nematodes and the interaction between nematodes and plants.

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Emerging Roles of Cyst Nematode Effectors in Exploiting Plant Cellular Processes

Cited by 23 publications

References 112 publications

Arabidopsis leucine-rich repeat receptor–like kinase NILR1 is required for induction of innate immunity to parasitic nematodes

Arabidopsis leucine-rich repeat receptor–like kinase NILR1 is required for induction of innate immunity to parasitic nematodes

Parallel adaptations and common host cell responses enabling feeding of obligate and facultative plant parasitic nematodes

TheDitylenchus destructorgenome provides new insights into the evolution of plant parasitic nematodes

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