Plant metabolism of nematode pheromones mediates plant-nematode interactions

Manohar, Murli; Tenjo-Castano, Francisco J; Chen, Shiyan; Zhang, Ying K.; Kumari, Anshu; Williamson, Valerie M.; Wang, Xiaohong; Klessig, Daniel F.; Schroeder, Frank C.

doi:10.1038/s41467-019-14104-2

Cited by 65 publications

(49 citation statements)

References 56 publications

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“…We focused on ascr#18 because it is widespread among both free-living and parasitic nematodes. It is the most abundantly excreted ascaroside of all plantparasitic nematodes analyzed so far (60,61) and it is the most abundant in several entomopathogenic nematodes (62). Ascaroside #18 was synthesized as reported (63) and was of greater than 98% purity.…”

Section: Methodsmentioning

confidence: 99%

Natural diversity in the predatory behavior facilitates the establishment of a robust model strain for nematode-trapping fungi

Yang

Ulzurrun

Gonçalves

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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Nematode-trapping fungi (NTF) are a group of specialized microbial predators that consume nematodes when food sources are limited. Predation is initiated when conserved nematode ascaroside pheromones are sensed, followed by the development of complex trapping devices. To gain insights into the coevolution of this interkingdom predator–prey relationship, we investigated natural populations of nematodes and NTF that we found to be ubiquitous in soils.Arthrobotrysspecies were sympatric with various nematode species and behaved as generalist predators. The ability to sense prey among wild isolates ofArthrobotrys oligosporavaried greatly, as determined by the number of traps after exposure toCaenorhabditis elegans. While some strains were highly sensitive toC. elegansand the nematode pheromone ascarosides, others responded only weakly. Furthermore, strains that were highly sensitive to the nematode prey also developed traps faster. The polymorphic nature of trap formation correlated with competency in prey killing, as well as with the phylogeny ofA. oligosporanatural strains, calculated after assembly and annotation of the genomes of 20 isolates. A chromosome-level genome assembly and annotation were established for one of the most sensitive wild isolates, and deletion of the only G-protein β-subunit–encoding gene ofA. oligosporanearly abolished trap formation. In summary, our study establishes a highly responsiveA. oligosporawild isolate as a model strain for the study of fungus–nematode interactions and demonstrates that trap formation is a fitness character in generalist predators of the nematode-trapping fungus family.

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Section: Methodsmentioning

confidence: 99%

Natural diversity in the predatory behavior facilitates the establishment of a robust model strain for nematode-trapping fungi

Yang

Ulzurrun

Gonçalves

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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“…Cellulose or xylan from host plants upregulated the level of β-1,4-endoglucanase or β-1,4-endoxylanase genes, respectively. Plants can interfere with PPN signaling (Manohar et al, 2020), and it is likely that also microbial activities modulate and mediate plant-nematode communication. Blocking plant cues or nematode chemoreceptors results in nematode repellence from the roots (Zuckerman, 1983).…”

Section: Importance Of the Rhizosphere Microbiota In Plant-nematode Imentioning

confidence: 99%

Plants and Associated Soil Microbiota Cooperatively Suppress Plant-Parasitic Nematodes

2020

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Disease suppressive soils with specific suppression of soil-borne pathogens and parasites have been long studied and are most often of microbiological origin. As for the plant-parasitic nematodes (PPN), which represent a huge threat to agricultural crops and which successfully defy many conventional control methods, soil progression from conducive to suppressive state is accompanied by the enrichment of specific antagonistic microbial consortia. However, a few microbial groups have come to the fore in diminishing PPN in disease suppressive soils using culture-dependent methods. Studies with cultured strains resulted in understanding the mechanisms by which nematodes are antagonized by microorganisms. Recent culture-independent studies on the microbiome associated with soil, plant roots, and PPN contributed to a better understanding of the functional potential of disease suppressive microbial cohort. Plant root exudation is an important pathway determining host-microbe communication and plays a key role in selection and enrichment of a specific set of microbial antagonists in the rhizosphere as first line of defense against crop pathogens or parasites. Root exudates comprising primary metabolites such as amino acids, sugars, organic acids, and secondary metabolites can also cause modifications in the nematode surface and subsequently affect microbial attachment. A positive interaction between hosts and their beneficial root microbiota is correlated with a low nematode performance on the host. In this review, we first summarized the historical records of nematodesuppressive soils and then focused on more recent studies in this aspect, emphasizing the advances in studying nematode-microbe interactions over time. We highlighted nematode biocontrol mechanisms, especially parasitism, induced systemic resistance, and volatile organic compounds using microbial consortia, or bacterial strains of the genera Pasteuria, Bacillus, Pseudomonas, Rhizobium, Streptomyces, Arthrobacter, and Variovorax, or fungal isolates of Pochonia, Dactylella, Nematophthora, Purpureocillium, Trichoderma, Hirsutella, Arthrobotrys, and Mortierella. We discussed the importance of root exudates in plant communication with PPN and soil microorganisms, emphasizing their role in microbial attachment to the nematode surface and subsequent events of

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“…Many plant-parasitic nematodes have been shown to produce ascarosides, a class of glycolipid-based signaling molecules synthesized almost exclusively by nematodes ( Manosalva et al, 2015 ). Depending on the types and compositions, ascarosides can regulate the aggregation/dispersion of conspecifics or even other nematodes ( Manohar et al, 2020 ). On the other hand, other compounds have also been documented to influence nematode behavior such as carbon dioxide; the amino acids arginine and lysine; phenolic acids; the plant hormones salicylic acid and gibberellic acid; the growth supplement ethephon; 6-dimethylallylaminopurine; and nitrate analogues ( Pline and Dusenbery, 1987 ; Wang et al, 2009 ; Wang et al, 2010 ; Fleming et al, 2017 ; Hosoi et al, 2017 ; Table 2 ).…”

Section: Endoparasitic Nematodesmentioning

confidence: 99%

Chemotactic Host-Finding Strategies of Plant Endoparasites and Endophytes

2020

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Plants interact with microorganisms in the environment during all stages of their development and in most of their organs. These interactions can be either beneficial or detrimental for the plant and may be transient or long-term. In extreme cases, microorganisms become endoparastic or endophytic and permanently reside within a plant, while the host plant undergoes developmental reprogramming and produces new tissues or organs as a response to the invasion. Events at the cellular and molecular level following infection have been extensively described, however the mechanisms of how these microorganisms locate their plant hosts via chemotaxis remain largely unknown. In this review, we summarize recent findings concerning the signalling molecules that regulate chemotaxis of endoparasitic/endophytic bacteria, fungi, and nematodes. In particular, we will focus on the molecules secreted by plants that are most likely to act as guidance cues for microorganisms. These compounds are found in a wide range of plant species and show a variety of secondary effects. Interestingly, these compounds show different attraction potencies depending on the species of the invading organism, suggesting that cues perceived in the soil may be more complex than anticipated. However, what the cognate receptors are for these attractants, as well as the mechanism of how these attractants influence these organisms, remain important outstanding questions. Host-targeting marks the first step of plant-microorganism interactions, therefore understanding the signalling molecules involved in this step plays a key role in understanding these interactions as a whole.

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Plant metabolism of nematode pheromones mediates plant-nematode interactions

Cited by 65 publications

References 56 publications

Natural diversity in the predatory behavior facilitates the establishment of a robust model strain for nematode-trapping fungi

Natural diversity in the predatory behavior facilitates the establishment of a robust model strain for nematode-trapping fungi

Plants and Associated Soil Microbiota Cooperatively Suppress Plant-Parasitic Nematodes

Chemotactic Host-Finding Strategies of Plant Endoparasites and Endophytes

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