Belowground Chemical Interactions: An Insight Into Host-Specific Behavior of Globodera spp. Hatched in Root Exudates From Potato and Its Wild Relative, Solanum sisymbriifolium

Understanding belowground chemical interactions between plant roots and plant-parasitic nematodes is immensely important for sustainable crop production and soilborne pest management. Due to metabolic diversity and ever-changing dynamics of root exudate composition, the impact of only certain molecules, such as nematode hatching factors, repellents, and attractants, has been examined in detail. Root exudates are a rich source of biologically active compounds, which plants use to shape their ecological interactions. However, the impact of these compounds on nematode parasitic behavior is poorly understood. In this study, we specifically address this knowledge gap in two cyst nematodes, Globodera pallida, a potato cyst nematode and the newly described species, Globodera ellingtonae. Globodera pallida is a devastating pest of potato (Solanum tuberosum) worldwide, whereas potato is a host for G. ellingtonae, but its pathogenicity remains to be determined. We compared the behavior of juveniles (J2s) hatched in response to root exudates from a susceptible potato cv. Desirée, a resistant potato cv. Innovator, and an immune trap crop Solanum sisymbriifolium (litchi tomato – a wild potato relative). Root secretions from S. sisymbriifolium greatly reduced the infection rate on a susceptible host for both Globodera spp. Juvenile motility was also significantly influenced in a host-dependent manner. However, reproduction on a susceptible host from juveniles hatched in S. sisymbriifolium root exudates was not affected, nor was the number of encysted eggs from progeny cysts. Transcriptome analysis by using RNA-sequencing (RNA-seq) revealed the molecular basis of root exudate-mediated modulation of nematode behavior. Differentially expressed genes are grouped into two major categories: genes showing characteristics of effectors and genes involved in stress responses and xenobiotic metabolism. To our knowledge, this is the first study that shows genome-wide root exudate-specific transcriptional changes in hatched preparasitic juveniles of plant-parasitic nematodes. This research provides a better understanding of the correlation between exudates from different plants and their impact on nematode behavior prior to the root invasion and supports the hypothesis that root exudates play an important role in plant-nematode interactions.

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The impact of management strategies on the development and status of potato cyst nematode populations in Switzerland: An overview from 1958 to present

Plant Disease ◽

10.1094/pdis-04-21-0800-sr ◽

2021 ◽

Author(s):

Andrea Caroline Ruthes ◽

Paul Dahlin

Keyword(s):

Integrated Management ◽

Abiotic Factors ◽

Management Strategies ◽

Monitoring Program ◽

Cyst Nematode ◽

Globodera Pallida ◽

Parasitic Nematodes ◽

Plant Parasitic Nematodes ◽

The Impact ◽

Plant Parasitic

Globodera rostochiensis and Globodera pallida are some of the most successful and highly specialized plant-parasitic nematodes, and appear among the most regulated quarantine pests globally. In Switzerland, they have been monitored by annual surveys since their first detection in Swiss soil, in 1958. The dataset created was reviewed to give an overview of the development and actual status of PCN in Switzerland. Positive fields represent 0.2% of all the samples analyzed, and currently their distribution is limited to central-west and western Switzerland, suggesting that new introduction of PCN and the spread of the initial introduced PCN populations did not occur. In this way, the integrated management used in Switzerland appears to be effective. However, the increasing availability of potato varieties with resistance to G. rostochiensis and the limited availability of varieties with resistance to G. pallida, together with other biotic and abiotic factors promoted changes in the dominance of either species. Consequently, an extended monitoring program would be of interest to Swiss farmers, to avoid favoring virulent traits that could be present within Swiss Globodera populations.

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ETHYLENE RESPONSE FACTOR (ERF) genes modulate plant root exudate composition and the attraction of plant parasitic nematodes

10.1101/652321 ◽

2019 ◽

Author(s):

Steven Dyer ◽

Ryan T Weir ◽

Deborah Cox ◽

Xavier Cheseto ◽

Baldwyn Torto ◽

...

Keyword(s):

Root Exudates ◽

Root Exudate ◽

Plant Root ◽

Parasitic Nematodes ◽

Ethylene Response Factor ◽

Response Factor ◽

Plant Parasitic Nematodes ◽

Ethylene Response ◽

Plant Root Exudate ◽

Plant Parasitic

Plant root exudates are compositionally diverse, plastic and adaptive. Ethylene signalling influences the attraction of plant parasitic nematodes (PPNs), presumably through the modulation of root exudate composition. Understanding this pathway could lead to new sources of crop parasite resistance. Here we have used Virus-Induced Gene Silencing (VIGS) to knockdown the expression of two ETHYLENE RESPONSE FACTOR (ERF) genes, ERF-E2 and ERF-E3 in tomato. Root exudates are significantly more attractive to the PPNs Meloidogyne incognita, and Globodera pallida following knockdown of ERF-E2, which has no impact on the attraction of Meloidogyne javanica. Knockdown of ERF-E3 has no impact on the attraction of Meloidogyne or Globodera spp. GC-MS analysis revealed substantial changes in root exudate composition relative to controls. However, these changes do not alter the attraction of rhizosphere microbes Bacillus subtilis or Agrobacterium tumefaciens. This study further supports the potential of engineering plant root exudate for parasite control, through the modulation of plant genes.

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The role of plant-parasitic nematodes in reducing yield of sugarcane in fine-textured soils in Queensland, Australia

Australian Journal of Experimental Agriculture ◽

10.1071/ea05287 ◽

2007 ◽

Vol 47 (5) ◽

pp. 620 ◽

Cited By ~ 22

Author(s):

B. L. Blair ◽

G. R. Stirling

Keyword(s):

Growth And Yield ◽

Parasitic Nematodes ◽

Plant Parasitic Nematodes ◽

Root Knot Nematode ◽

Population Densities ◽

Lesion Nematode ◽

Yield Responses ◽

The Impact ◽

Stalk Length ◽

Plant Parasitic

Damage to sugarcane caused by root-knot nematode (Meloidogyne spp.) is well documented in infertile coarse-textured soils, but crop losses have never been assessed in the fine-textured soils on which more than 95% of Australia’s sugarcane is grown. The impact of nematodes in these more fertile soils was assessed by repeatedly applying nematicides (aldicarb and fenamiphos) to plant and ratoon crops in 16 fields, and measuring their effects on nematode populations, sugarcane growth and yield. In untreated plant crops, mid-season population densities of lesion nematode (Pratylenchus zeae), root-knot nematode (M. javanica), stunt nematode (Tylenchorhynchus annulatus), spiral nematode (Helicotylenchus dihystera) and stubby-root nematode (Paratrichodorus minor) averaged 1065, 214, 535, 217 and 103 nematodes/200 mL soil, respectively. Lower mean nematode population densities were recorded in the first ratoon, particularly for root-knot nematode. Nematicides reduced populations of lesion nematode by 66–99% in both plant and ratoon crops, but control of root-knot nematode was inconsistent, particularly in ratoons. Nematicide treatment had a greater impact on shoot and stalk length than on shoot and stalk number. The entire community of pest nematodes appeared to be contributing to lost productivity, but stalk length and final yield responses correlated most consistently with the number of lesion nematodes controlled. Fine roots in nematicide-treated plots were healthier and more numerous than in untreated plots, and this was indicative of the reduced impact of lesion nematode. Yield responses averaged 15.3% in plant crops and 11.6% in ratoons, indicating that nematodes are subtle but significant pests of sugarcane in fine-textured soils. On the basis of these results, plant-parasitic nematodes are conservatively estimated to cost the Australian sugar industry about AU$82 million/annum.

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The Influence of Root Exudates on the Activity of Some Plant-parasitic Nematodes

Root Diseases and Soil-Borne Pathogens ◽

10.1525/9780520339941-030 ◽

1970 ◽

pp. 134-138

Author(s):

Audrey M. Shepherd

Keyword(s):

Root Exudates ◽

Parasitic Nematodes ◽

Plant Parasitic Nematodes ◽

Plant Parasitic

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Plant-parasitic nematodes respond to root exudate signals with host-specific gene expression patterns

PLoS Pathogens ◽

10.1371/journal.ppat.1007503 ◽

2019 ◽

Vol 15 (2) ◽

pp. e1007503 ◽

Cited By ~ 9

Author(s):

Christopher A. Bell ◽

Catherine J. Lilley ◽

James McCarthy ◽

Howard J. Atkinson ◽

P. E. Urwin

Keyword(s):

Gene Expression ◽

Root Exudate ◽

Expression Patterns ◽

Parasitic Nematodes ◽

Gene Expression Patterns ◽

Specific Gene ◽

Plant Parasitic Nematodes ◽

Specific Gene Expression ◽

Plant Parasitic

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Differential Response of Meloidogyne, Pratylenchus, Globodera, and Xiphinema Species to the Nematicide Fluazaindolizine

Phytopathology ◽

10.1094/phyto-05-20-0189-r ◽

2020 ◽

Vol 110 (12) ◽

pp. 2003-2009

Author(s):

Catherine L. Wram ◽

Inga Zasada

Keyword(s):

Untreated Control ◽

Exposure Dose ◽

Parasitic Nematodes ◽

Plant Parasitic Nematodes ◽

Response Curves ◽

Greenhouse Study ◽

Meloidogyne Spp ◽

The Impact ◽

Plant Parasitic

This research focused on the effects of fluazaindolizine on a diversity of plant-parasitic nematodes. In microwell assays, 24-h dose-response curves were generated for several species and populations of Meloidogyne, Pratylenchus neglectus, P. penetrans, Globodera ellingtonae, and Xiphinema americanum. In a greenhouse study, the impact of fluazaindolizine on fecundity of M. incognita, M. hapla, and M. chitwoodi was tested by exposing nematodes for 24 h in solution and inoculating on tomato. The average 24-h ED50s (dose that resulted in the immobility of 50% of exposed nematodes) for M. hapla, M. chitwoodi, and M. incognita were 325.7, 223.4, and 100.7 ppm, respectively. M. hapla had the most variation among populations, with 24-h ED50s ranging from 72 to 788 ppm. G. ellingtonae had the lowest 24-h ED50 at 30 ppm. Pratylenchus spp. were unaffected by fluazaindolizine. X. americanum was the only species where effects of fluazaindolizine were reversible, but had a 24-h ED50 that fell in the range of the Meloidogyne spp. In the greenhouse study, M. chitwoodi was the least sensitive with reproduction reaching 62% of the untreated control after a pre-exposure to 47 ppm, whereas M. incognita and M. hapla at the same exposure dose had reproduction rates of 27 and 36% of the untreated control, respectively. Despite varying in in vitro responses to fluazaindolizine, reproduction of all Meloidogyne spp. was suppressed after only 24 h of exposure. This study expanded our understanding of how G. ellingtonae, P. thornei, P. penetrans, and X. americanum respond to fluazaindolizine.

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The use of Pluronic F-127 to study the development of the potato cyst nematode, Globodera pallida

Nematology ◽

10.1163/156854112x631944 ◽

2012 ◽

Vol 14 (7) ◽

pp. 869-873 ◽

Cited By ~ 5

Author(s):

Ayano Sasaki-Crawley ◽

Rosane Curtis ◽

Michael Birkett ◽

Apostolos Papadopoulos ◽

Rod Blackshaw ◽

...

Keyword(s):

Aqueous Solution ◽

Solanum Tuberosum ◽

Transgenic Plants ◽

Cyst Nematode ◽

Potato Cyst Nematode ◽

Globodera Pallida ◽

Parasitic Nematodes ◽

Plant Parasitic Nematodes ◽

Plant Parasitic

This paper demonstrates a simple novel in vitro method using Pluronic F-127 aqueous solution to study the development of the potato cyst nematode, Globodera pallida, in Solanum spp. without any need for sterilisation of either the plants or the nematodes. In this study, this method was successfully applied to comparative studies on the development of G. pallida in Solanum tuberosum (potato) or S. sisymbriifolium (sticky nightshade). The protocol described here could be useful for screening transgenic plants or different plant cultivars/species for their ability to allow development not only of G. pallida but also any other plant-parasitic nematodes.

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Identification and characterisation of serotonin signalling in the potato cyst nematode Globodera pallida reveals new targets for crop protection

10.1101/358358 ◽

2018 ◽

Cited By ~ 1

Author(s):

Anna Crisford ◽

Fernando Calahorro ◽

Elizabeth Ludlow ◽

Jessica M.C. Marvin ◽

Jennifer K. Hibbard ◽

...

Keyword(s):

Biogenic Amines ◽

Tryptophan Hydroxylase ◽

Plant Root ◽

Crop Protection ◽

Cyst Nematode ◽

Potato Cyst Nematode ◽

Globodera Pallida ◽

Parasitic Nematodes ◽

Plant Parasitic Nematodes ◽

Plant Parasitic

AbstractPlant parasitic nematodes are microscopic pests that invade plant roots and cause extensive damage to crops worldwide. To investigate mechanisms underpinning their parasitic behaviour we used a chemical biology approach: We discovered that reserpine, a plant alkaloid known for its antagonism of the mammalian vesicular monoamine transporter VMAT and ability to impart a global depletion of synaptic biogenic amines in the nervous system, potently impairs the ability of the potato cyst nematode Globodera pallida to enter the host plant root. We show that this effect of reserpine is mediated by an inhibition of serotonergic signalling that is essential for activation of the stylet, a lance-like organ that protrudes from the mouth of the worm and which is used to pierce the host root to gain access. Prompted by this we identified core molecular components of G. pallida serotonin signalling encompassing the target of reserpine, VMAT; the synthetic enzyme for serotonin, tryptophan hydroxylase; the G protein coupled receptor SER-7 and the serotonin-gated chloride channel MOD-1. We found that inhibitors of tryptophan hydroxylase, SER-7 and MOD-1 phenocopy the plant protecting action of reserpine. Thus targeting the serotonin signalling pathway presents a promising new route to control plant parasitic nematodes.SummaryIndian snakeroot, an herbal medicine prepared from the roots of the shrub Rauwolfia serpentina, has been used for centuries for its calming action. The major active constituent is reserpine which works by depleting a specific class of mood regulating chemical in the brain, the biogenic amines. We have discovered a remarkable effect of reserpine on a pest of global concern, the plant parasitic nematodes. These microscopic worms invade the roots of crops presenting a severe threat to food production. We show that reserpine disables serotonin signalling in the worm’s ‘brain’ that regulates the rhythmic thrusting of the stylet: a lance-like structure that protrudes from its mouth to pierce the plant root and which is essential to its parasitic lifecycle. Thus, reserpine joins nicotine as another intriguing example of Nature evolving its own protection against pests. We have identified key components of the serotonin signalling pathway in the potato cyst nematode Globodera pallida and show that chemicals that target these sites inhibit the ability of the nematode to invade its host plant. We conclude that biogenic amine transmitters are intimately involved in the worm’s parasitic behaviour and provide a new discrete route to crop protection.

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