Publications by authors named "Peter E Urwin"

44 Publications

The influence of competing root symbionts on below-ground plant resource allocation.

Ecol Evol 2021 Apr 2;11(7):2997-3003. Epub 2021 Mar 2.

Department of Animal and Plant Sciences University of Sheffield Sheffield UK.

Plants typically interact with multiple above- and below-ground organisms simultaneously, with their symbiotic relationships spanning a continuum ranging from mutualism, such as with arbuscular mycorrhizal fungi (AMF), to parasitism, including symbioses with plant-parasitic nematodes (PPN).Although research is revealing the patterns of plant resource allocation to mutualistic AMF partners under different host and environmental constraints, the root ecosystem, with multiple competing symbionts, is often ignored. Such competition is likely to heavily influence resource allocation to symbionts.Here, we outline and discuss the competition between AMF and PPN for the finite supply of host plant resources, highlighting the need for a more holistic understanding of the influence of below-ground interactions on plant resource allocation. Based on recent developments in our understanding of other symbiotic systems such as legume-rhizobia and AMF-aphid-plant, we propose hypotheses for the distribution of plant resources between contrasting below-ground symbionts and how such competition may affect the host.We identify relevant knowledge gaps at the physiological and molecular scales which, if resolved, will improve our understanding of the true ecological significance and potential future exploitation of AMF-PPN-plant interactions in order to optimize plant growth. To resolve these outstanding knowledge gaps, we propose the application of well-established methods in isotope tracing and nutrient budgeting to monitor the movement of nutrients between symbionts. By combining these approaches with novel time of arrival experiments and experimental systems involving multiple plant hosts interlinked by common mycelial networks, it may be possible to reveal the impact of multiple, simultaneous colonizations by competing symbionts on carbon and nutrient flows across ecologically important scales.
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http://dx.doi.org/10.1002/ece3.7292DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8019053PMC
April 2021

Toward genetic modification of plant-parasitic nematodes: delivery of macromolecules to adults and expression of exogenous mRNA in second stage juveniles.

G3 (Bethesda) 2021 Feb;11(2)

Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA, UK.

Plant-parasitic nematodes are a continuing threat to food security, causing an estimated 100 billion USD in crop losses each year. The most problematic are the obligate sedentary endoparasites (primarily root knot nematodes and cyst nematodes). Progress in understanding their biology is held back by a lack of tools for functional genetics: forward genetics is largely restricted to studies of natural variation in populations and reverse genetics is entirely reliant on RNA interference. There is an expectation that the development of functional genetic tools would accelerate the progress of research on plant-parasitic nematodes, and hence the development of novel control solutions. Here, we develop some of the foundational biology required to deliver a functional genetic tool kit in plant-parasitic nematodes. We characterize the gonads of male Heterodera schachtii and Meloidogyne hapla in the context of spermatogenesis. We test and optimize various methods for the delivery, expression, and/or detection of exogenous nucleic acids in plant-parasitic nematodes. We demonstrate that delivery of macromolecules to cyst and root knot nematode male germlines is difficult, but possible. Similarly, we demonstrate the delivery of oligonucleotides to root knot nematode gametes. Finally, we develop a transient expression system in plant-parasitic nematodes by demonstrating the delivery and expression of exogenous mRNA encoding various reporter genes throughout the body of H. schachtii juveniles using lipofectamine-based transfection. We anticipate these developments to be independently useful, will expedite the development of genetic modification tools for plant-parasitic nematodes, and ultimately catalyze research on a group of nematodes that threaten global food security.
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http://dx.doi.org/10.1093/g3journal/jkaa058DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8022973PMC
February 2021

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

PLoS Pathog 2020 10 2;16(10):e1008884. Epub 2020 Oct 2.

School of Biological Sciences, University of Southampton, Southampton, United Kingdom.

Plant parasitic nematodes are microscopic pathogens that invade plant roots and cause extensive damage to crops. We have used a chemical biology approach to define mechanisms underpinning their parasitic behaviour: We discovered that reserpine, a plant alkaloid that inhibits the vesicular monoamine transporter (VMAT), potently impairs the ability of the potato cyst nematode Globodera pallida to enter the host plant root. We show this is due to an inhibition of serotonergic signalling that is essential for activation of the stylet which is used to access the host root. 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 cloned each of these molecular components and confirmed their functional identity by complementation of the corresponding C. elegans mutant thus mapping out serotonergic signalling in G. pallida. Complementary approaches testing the effect of chemical inhibitors of each of these signalling elements on discrete sub-behaviours required for parasitism and root invasion reinforce the critical role of serotonin. Thus, targeting the serotonin signalling pathway presents a promising new route to control plant parasitic nematodes.
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http://dx.doi.org/10.1371/journal.ppat.1008884DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7556481PMC
October 2020

Host-specific signatures of the cell wall changes induced by the plant parasitic nematode, Meloidogyne incognita.

Sci Rep 2018 11 23;8(1):17302. Epub 2018 Nov 23.

Centre for Plant Sciences, Faculty of Biological Sciences, University of Leeds, LS2 9JT, Leeds, United Kingdom.

Root-knot nematodes (Meloidogyne spp.) are an important group of plant parasitic nematodes that induce within host plant roots unique feeding site structures, termed giant cells, which supply nutrient flow to the nematode. A comparative in situ analysis of cell wall polysaccharides in the giant cells of three host species (Arabidopsis, maize and aduki bean) infected with Meloidogyne incognita has been carried out. Features common to giant cell walls of all three species include the presence of high-esterified pectic homogalacturonan, xyloglucan and pectic arabinan. The species-specific presence of xylan and mixed-linkage glucan (MLG) epitopes in giant cell walls of maize reflected that host's taxonomic group. The LM5 galactan and LM21 mannan epitopes were not detected in the giant cell walls of aduki bean but were detected in Arabidopsis and maize giant cell walls. The LM2 arabinogalactan-protein epitope was notable for its apparent global variations in root cell walls as a response to infection across the three host species. Additionally, a set of Arabidopsis cell wall mutants were used to determine any impacts of altered cell wall structures on M. incognita infection. Disruption of the arabinogalactan-protein 8 gene had the greatest impact and resulted in an increased infection rate.
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http://dx.doi.org/10.1038/s41598-018-35529-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6251906PMC
November 2018

Aphid Colonization Affects Potato Root Exudate Composition and the Hatching of a Soil Borne Pathogen.

Front Plant Sci 2018 6;9:1278. Epub 2018 Sep 6.

Centre for Plant Sciences, University of Leeds, Leeds, United Kingdom.

Plants suffer multiple, simultaneous biotic threats from both above and below ground. These pests and/or pathogens are commonly studied on an individual basis and the effects of above-ground pests on below-ground pathogens are poorly defined. Root exudates from potato plants ( L.) were analyzed to characterize the top-down plant-mediated interactions between a phloem-sucking herbivore () and a sedentary, endoparasitic nematode (). Increasing inocula of the aphid, , reduced the root mass of potato plants. Exudates collected from these roots induced significantly lower hatching of second-stage juveniles from eggs over a 28-day period, than those from uninfested control plants. Inhibition of hatch was significantly positively correlated with size of aphid inoculum. Diminished hatching was partially recovered after treatment with root exudate from uninfested potato plants indicating that the effect on hatching is reversible but cannot be fully recovered. Glucose and fructose content was reduced in root exudates from aphid-infested potato plants compared to controls and these sugars were found to induce hatching of , but not to the same degree as potato root exudates (PRE). Supplementing aphid-infested PRE with sugars did not recover the hatching potential of the treatment, suggesting that additional compounds play an important role in egg hatch. The first gene upregulated in the closely related potato cyst nematode post-exposure to host root exudate, , was confirmed to be upregulated in cysts after exposure to PRE and was also upregulated by the sugar treatments. Significantly reduced upregulation of was observed in cysts treated with root exudates from potato plants infested with greater numbers of aphids. Our data suggest that aphid infestation of potato plants affects the composition of root exudates, with consequential effects on the hatching and gene expression of eggs. This work shows that an above-ground pest can indirectly impact the rhizosphere and reveals secondary effects for control of an economically important below-ground pathogen.
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http://dx.doi.org/10.3389/fpls.2018.01278DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6136236PMC
September 2018

Duplication of hsp-110 Is Implicated in Differential Success of Globodera Species under Climate Change.

Mol Biol Evol 2018 10;35(10):2401-2413

Center for Plant Sciences, Faculty of Biological Sciences, University of Leeds, Leeds, UK.

Managing the emergence and spread of crop pests and pathogens is essential for global food security. Understanding how organisms have adapted to their native climate is key to predicting the impact of climate change. The potato cyst nematodes Globodera pallida and G. rostochiensis are economically important plant pathogens that cause yield losses of up to 50% in potato. The two species have different thermal optima that may relate to differences in the altitude of their regions of origin in the Andes. Here, we demonstrate that juveniles of G. pallida are less able to recover from heat stress than those of G. rostochiensis. Genome-wide analysis revealed that while both Globodera species respond to heat stress by induction of various protective heat-inducible genes, G. pallida experiences heat stress at lower temperatures. We use C. elegans as a model to demonstrate the dependence of the heat stress response on expression of Heat Shock Factor-1 (HSF-1). Moreover, we show that hsp-110 is induced by heat stress in G. rostochiensis, but not in the less thermotolerant G. pallida. Sequence analysis revealed that this gene and its promoter was duplicated in G. rostochiensis and acquired thermoregulatory properties. We show that hsp-110 is required for recovery from acute thermal stress in both C. elegans and in G. rostochiensis. Our findings point towards an underlying molecular mechanism that allows the differential expansion of one species relative to another closely related species under current climate change scenarios. Similar mechanisms may be true of other invertebrate species with pest status.
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http://dx.doi.org/10.1093/molbev/msy132DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6188557PMC
October 2018

Effector gene birth in plant parasitic nematodes: Neofunctionalization of a housekeeping glutathione synthetase gene.

PLoS Genet 2018 04 11;14(4):e1007310. Epub 2018 Apr 11.

Dept. of Biological Chemistry, John Innes Centre, Norwich Research Park, Norwich, United Kingdom.

Plant pathogens and parasites are a major threat to global food security. Plant parasitism has arisen four times independently within the phylum Nematoda, resulting in at least one parasite of every major food crop in the world. Some species within the most economically important order (Tylenchida) secrete proteins termed effectors into their host during infection to re-programme host development and immunity. The precise detail of how nematodes evolve new effectors is not clear. Here we reconstruct the evolutionary history of a novel effector gene family. We show that during the evolution of plant parasitism in the Tylenchida, the housekeeping glutathione synthetase (GS) gene was extensively replicated. New GS paralogues acquired multiple dorsal gland promoter elements, altered spatial expression to the secretory dorsal gland, altered temporal expression to primarily parasitic stages, and gained a signal peptide for secretion. The gene products are delivered into the host plant cell during infection, giving rise to "GS-like effectors". Remarkably, by solving the structure of GS-like effectors we show that during this process they have also diversified in biochemical activity, and likely represent the founding members of a novel class of GS-like enzyme. Our results demonstrate the re-purposing of an endogenous housekeeping gene to form a family of effectors with modified functions. We anticipate that our discovery will be a blueprint to understand the evolution of other plant-parasitic nematode effectors, and the foundation to uncover a novel enzymatic function.
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http://dx.doi.org/10.1371/journal.pgen.1007310DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5919673PMC
April 2018

A Plant-Feeding Nematode Indirectly Increases the Fitness of an Aphid.

Front Plant Sci 2017 3;8:1897. Epub 2017 Nov 3.

Centre for Plant Sciences, University of Leeds, Leeds, United Kingdom.

Plants suffer multiple, simultaneous assaults from above and below ground. In the laboratory, pests and/or pathogen attack are commonly studied on an individual basis. The molecular response of the plant to attack from multiple organisms and the interaction of different defense pathways is unclear. The inducible systemic responses of the potato ( L.) host plant were analyzed to characterize the plant-mediated indirect interactions between a sedentary, endoparasitic nematode (), and a phloem-sucking herbivore (). The reproductive success of was greater on potato plants pre-infected with compared to control plants. Salicylic acid (SA) increased systemically in the leaves of potato plants following nematode and aphid infection singly with a corresponding increase in expression of SA-mediated marker genes. An increase in jasmonic acid associated with aphid infection was suppressed when plants were co-infected with nematodes. Our data suggests a positive, asymmetric interaction between a sedentary endoparasitic nematode and a sap-sucking insect. The systemic response of the potato plant following infection with indirectly influences the performance of . This work reveals additional secondary benefits of controlling individual crop pests.
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http://dx.doi.org/10.3389/fpls.2017.01897DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5701616PMC
November 2017

Rational design of biosafe crop resistance to a range of nematodes using RNA interference.

Plant Biotechnol J 2018 02 22;16(2):520-529. Epub 2017 Aug 22.

Centre for Plant Sciences, University of Leeds, Leeds, UK.

Double-stranded RNA (dsRNA) molecules targeting two genes have been identified that suppress economically important parasitic nematode species of banana. Proteasomal alpha subunit 4 (pas-4) and Actin-4 (act-4) were identified from a survey of sequence databases and cloned sequences for genes conserved across four pests of banana, Radopholus similis, Pratylenchus coffeae, Meloidogyne incognita and Helicotylenchus multicinctus. These four species were targeted with dsRNAs containing exact 21 nucleotide matches to the conserved regions. Potential off-target effects were limited by comparison with Caenorhabditis, Drosophila, rat, rice and Arabidopsis genomes. In vitro act-4 dsRNA treatment of R. similis suppressed target gene expression by 2.3-fold, nematode locomotion by 66 ± 4% and nematode multiplication on carrot discs by 49 ± 5%. The best transgenic carrot hairy root lines expressing act-4 or pas-4 dsRNA reduced transcript message abundance of target genes in R. similis by 7.9-fold and fourfold and nematode multiplication by 94 ± 2% and 69 ± 3%, respectively. The same act-4 and pas-4 lines reduced P. coffeae target transcripts by 1.7- and twofold and multiplication by 50 ± 6% and 73 ± 8%. Multiplication of M. incognita on the pas-4 lines was reduced by 97 ± 1% and 99 ± 1% while target transcript abundance was suppressed 4.9- and 5.6-fold. There was no detectable RNAi effect on nontarget nematodes exposed to dsRNAs targeting parasitic nematodes. This work defines a framework for development of a range of nonprotein defences to provide broad resistance to pests and pathogens of crops.
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http://dx.doi.org/10.1111/pbi.12792DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5787825PMC
February 2018

The Complex Cell Wall Composition of Syncytia Induced by Plant Parasitic Cyst Nematodes Reflects Both Function and Host Plant.

Front Plant Sci 2017 21;8:1087. Epub 2017 Jun 21.

Faculty of Biological Sciences, University of LeedsLeeds, United Kingdom.

Plant-parasitic cyst nematodes induce the formation of specialized feeding structures, syncytia, within their host roots. These unique plant organs serve as the sole nutrient resource for development and reproduction throughout the biotrophic interaction. The multinucleate syncytium, which arises through local dissolution of cell walls and protoplast fusion of multiple adjacent cells, has dense cytoplasm containing numerous organelles, surrounded by thickened outer cell walls that must withstand high turgor pressure. However, little is known about how the constituents of the syncytial cell wall and their conformation support its role during nematode parasitism. We used a set of monoclonal antibodies, targeted to a range of plant cell wall components, to reveal the microstructures of syncytial cell walls induced by four of the most economically important cyst nematode species, , , and , in their respective potato, soybean, and spring wheat host roots. fluorescence analysis revealed highly similar cell wall composition of syncytia induced by and . Both consisted of abundant xyloglucan, methyl-esterified homogalacturonan and pectic arabinan. In contrast, the walls of syncytia induced in wheat roots by and contain little xyloglucan but are rich in feruloylated xylan and arabinan residues, with variable levels of mixed-linkage glucan. The overall chemical composition of syncytial cell walls reflected the general features of root cell walls of the different host plants. We relate specific components of syncytial cell walls, such as abundant arabinan, methyl-esterification status of pectic homogalacturonan and feruloylation of xylan, to their potential roles in forming a network to support both the strength and flexibility required for syncytium function.
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http://dx.doi.org/10.3389/fpls.2017.01087DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5478703PMC
June 2017

Climate change is predicted to alter the current pest status of Globodera pallida and G. rostochiensis in the United Kingdom.

Glob Chang Biol 2017 11 30;23(11):4497-4507. Epub 2017 Mar 30.

School of Biology, University of Leeds, Leeds, UK.

The potato cyst nematodes Globodera pallida and G. rostochiensis are economically important plant pathogens causing losses to UK potato harvests estimated at £50 m/ year. Implications of climate change on their future pest status have not been fully considered. Here, we report growth of female G. pallida and G. rostochiensis over the range 15 to 25°C. Females per plant and their fecundity declined progressively with temperatures above 17.5°C for G. pallida, whilst females per plant were optimal between 17.5 and 22.5°C for G. rostochiensis. Relative reproductive success with temperature was confirmed on two potato cultivars infected with either species at 15, 22.5 and 25°C. The reduced reproductive success of G. pallida at 22.5°C relative to 15°C was also recorded for a further seven host cultivars studied. The differences in optimal temperatures for reproductive success may relate to known differences in the altitude of their regions of origin in the Andes. Exposure of G. pallida to a diurnal temperature stress for one week during female growth significantly suppressed subsequent growth for one week at 17.5°C but had no effect on G. rostochiensis. However, after two weeks of recovery, female size was not significantly different from that for the control treatment. Future soil temperatures were simulated for medium- and high-emission scenarios and combined with nematode growth data to project future implications of climate change for the two species. Increased soil temperatures associated with climate change may reduce the pest status of G. pallida but benefit G. rostochiensis especially in the southern United Kingdom. We conclude that plant breeders may be able to exploit the thermal limits of G. pallida by developing potato cultivars able to grow under future warm summer conditions. Existing widely deployed resistance to G. rostochiensis is an important characteristic to retain for new potato cultivars.
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http://dx.doi.org/10.1111/gcb.13676DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5655772PMC
November 2017

Expression of a Cystatin Transgene in Eggplant Provides Resistance to Root-knot Nematode, Meloidogyne incognita.

Front Plant Sci 2016 28;7:1122. Epub 2016 Jul 28.

Division of Nematology, ICAR-Indian Agricultural Research Institute New Delhi, India.

Root-knot nematodes (RKN) cause substantial yield decline in eggplant and sustainable management options to minimize crop damage due to nematodes are still limited. A number of genetic engineering strategies have been developed to disrupt the successful plant-nematode interactions. Among them, delivery of proteinase inhibitors from the plant to perturb nematode development and reproduction is arguably the most effective strategy. In the present study, transgenic eggplant expressing a modified rice cystatin (OC-IΔD86) gene under the control of the root-specific promoter, TUB-1, was generated to evaluate the genetically modified nematode resistance. Five putative transformants were selected through PCR and genomic Southern blot analysis. Expression of the cystatin transgene was confirmed in all the events using western blotting, ELISA and qPCR assay. Upon challenge inoculation, all the transgenic events exhibited a detrimental effect on RKN development and reproduction. The best transgenic line (a single copy event) showed 78.3% inhibition in reproductive success of RKN. Our results suggest that cystatins can play an important role for improving nematode resistance in eggplant and their deployment in gene pyramiding strategies with other proteinase inhibitors could ultimately enhance crop yield.
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http://dx.doi.org/10.3389/fpls.2016.01122DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4963396PMC
August 2016

The genome of the yellow potato cyst nematode, Globodera rostochiensis, reveals insights into the basis of parasitism and virulence.

Genome Biol 2016 Jun 10;17(1):124. Epub 2016 Jun 10.

USDA-ARS Horticultural Crops Research Laboratory, Corvallis, OR, USA.

Background: The yellow potato cyst nematode, Globodera rostochiensis, is a devastating plant pathogen of global economic importance. This biotrophic parasite secretes effectors from pharyngeal glands, some of which were acquired by horizontal gene transfer, to manipulate host processes and promote parasitism. G. rostochiensis is classified into pathotypes with different plant resistance-breaking phenotypes.

Results: We generate a high quality genome assembly for G. rostochiensis pathotype Ro1, identify putative effectors and horizontal gene transfer events, map gene expression through the life cycle focusing on key parasitic transitions and sequence the genomes of eight populations including four additional pathotypes to identify variation. Horizontal gene transfer contributes 3.5 % of the predicted genes, of which approximately 8.5 % are deployed as effectors. Over one-third of all effector genes are clustered in 21 putative 'effector islands' in the genome. We identify a dorsal gland promoter element motif (termed DOG Box) present upstream in representatives from 26 out of 28 dorsal gland effector families, and predict a putative effector superset associated with this motif. We validate gland cell expression in two novel genes by in situ hybridisation and catalogue dorsal gland promoter element-containing effectors from available cyst nematode genomes. Comparison of effector diversity between pathotypes highlights correlation with plant resistance-breaking.

Conclusions: These G. rostochiensis genome resources will facilitate major advances in understanding nematode plant-parasitism. Dorsal gland promoter element-containing effectors are at the front line of the evolutionary arms race between plant and parasite and the ability to predict gland cell expression a priori promises rapid advances in understanding their roles and mechanisms of action.
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http://dx.doi.org/10.1186/s13059-016-0985-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4901422PMC
June 2016

Functional C-TERMINALLY ENCODED PEPTIDE (CEP) plant hormone domains evolved de novo in the plant parasite Rotylenchulus reniformis.

Mol Plant Pathol 2016 Oct 6;17(8):1265-75. Epub 2016 Jun 6.

Centre for Plant Sciences, University of Leeds, Leeds, LS2 9JT, UK.

Sedentary plant-parasitic nematodes (PPNs) induce and maintain an intimate relationship with their host, stimulating cells adjacent to root vascular tissue to re-differentiate into unique and metabolically active 'feeding sites'. The interaction between PPNs and their host is mediated by nematode effectors. We describe the discovery of a large and diverse family of effector genes, encoding C-TERMINALLY ENCODED PEPTIDE (CEP) plant hormone mimics (RrCEPs), in the syncytia-forming plant parasite Rotylenchulus reniformis. The particular attributes of RrCEPs distinguish them from all other CEPs, regardless of origin. Together with the distant phylogenetic relationship of R. reniformis to the only other CEP-encoding nematode genus identified to date (Meloidogyne), this suggests that CEPs probably evolved de novo in R. reniformis. We have characterized the first member of this large gene family (RrCEP1), demonstrating its significant up-regulation during the plant-nematode interaction and expression in the effector-producing pharyngeal gland cell. All internal CEP domains of multi-domain RrCEPs are followed by di-basic residues, suggesting a mechanism for cleavage. A synthetic peptide corresponding to RrCEP1 domain 1 is biologically active and capable of up-regulating plant nitrate transporter (AtNRT2.1) expression, whilst simultaneously reducing primary root elongation. When a non-CEP-containing, syncytia-forming PPN species (Heterodera schachtii) infects Arabidopsis in a CEP-rich environment, a smaller feeding site is produced. We hypothesize that CEPs of R. reniformis represent a two-fold adaptation to sustained biotrophy in this species: (i) increasing host nitrate uptake, whilst (ii) limiting the size of the syncytial feeding site produced.
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http://dx.doi.org/10.1111/mpp.12402DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5103176PMC
October 2016

A metagenetic approach to determine the diversity and distribution of cyst nematodes at the level of the country, the field and the individual.

Mol Ecol 2015 Dec;24(23):5842-51

Cell and Molecular Sciences Group, Dundee Effector Consortium, The James Hutton Institute, Invergowrie, Dundee, DD2 5DA, UK.

Distinct populations of the potato cyst nematode (PCN) Globodera pallida exist in the UK that differ in their ability to overcome various sources of resistance. An efficient method for distinguishing between populations would enable pathogen-informed cultivar choice in the field. Science and Advice for Scottish Agriculture (SASA) annually undertake national DNA diagnostic tests to determine the presence of PCN in potato seed and ware land by extracting DNA from soil floats. These DNA samples provide a unique resource for monitoring the distribution of PCN and further interrogation of the diversity within species. We identify a region of mitochondrial DNA descriptive of three main groups of G. pallida present in the UK and adopt a metagenetic approach to the sequencing and analysis of all SASA samples simultaneously. Using this approach, we describe the distribution of G. pallida mitotypes across Scotland with field-scale resolution. Most fields contain a single mitotype, one-fifth contain a mix of mitotypes, and less than 3% contain all three mitotypes. Within mixed fields, we were able to quantify the relative abundance of each mitotype across an order of magnitude. Local areas within mixed fields are dominated by certain mitotypes and indicate towards a complex underlying 'pathoscape'. Finally, we assess mitotype distribution at the level of the individual cyst and provide evidence of 'hybrids'. This study provides a method for accurate, quantitative and high-throughput typing of up to one thousand fields simultaneously, while revealing novel insights into the national genetic variability of an economically important plant parasite.
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http://dx.doi.org/10.1111/mec.13434DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4981918PMC
December 2015

Field resistance of transgenic plantain to nematodes has potential for future African food security.

Sci Rep 2015 Jan 30;5:8127. Epub 2015 Jan 30.

Centre for Plant Sciences, University of Leeds, Leeds LS2 9JT, UK.

Plant parasitic nematodes impose losses of up to 70% on plantains and cooking bananas in Africa. Application of nematicides is inappropriate and resistant cultivars are unavailable. Where grown, demand for plantain is more than for other staple crops. Confined field testing demonstrated that transgenic expression of a biosafe, anti-feedant cysteine proteinase inhibitor and an anti-root invasion, non-lethal synthetic peptide confers resistance to plantain against the key nematode pests Radopholus similis and Helicotylenchus multicinctus. The best peptide transgenic line showed improved agronomic performance relative to non-transgenic controls and provided about 99% nematode resistance at harvest of the mother crop. Its yield was about 186% in comparison with the nematode challenged control non-transgenic plants based on larger bunches and diminished plant toppling in storms, due to less root damage. This is strong evidence for utilizing this resistance to support the future food security of 70 million, mainly poor Africans that depend upon plantain as a staple food.
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http://dx.doi.org/10.1038/srep08127DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4311252PMC
January 2015

NHR-176 regulates cyp-35d1 to control hydroxylation-dependent metabolism of thiabendazole in Caenorhabditis elegans.

Biochem J 2015 Feb;466(1):37-44

*School of Biology, University of Leeds, Leeds LS2 9JT, U.K.

Knowledge of how drugs are metabolized and excreted is an essential component of understanding their fate within and among target and non-target organisms. Thiabendazole (TBZ) was the first benzimidazole (BZ) to be commercially available and remains one of the most important anthelmintic drugs for medical and veterinary use. We have characterized how Caenorhabditis elegans metabolizes and excretes TBZ. We have shown that TBZ directly binds to the nuclear hormone receptor (NHR)-176 and that this receptor is required for the induction by TBZ of the cytochrome P450 (CYP) encoded by cyp-35d1. Further, RNAi inhibition of cyp-35d1 in animals exposed to TBZ causes a reduction in the quantity of a hydroxylated TBZ metabolite and its glucose conjugate that is detected in C. elegans tissue by HPLC. This final metabolite is unique to nematodes and we also identify two P-glycoproteins (PGPs) necessary for its excretion. Finally, we have shown that inhibiting the metabolism we describe increases the susceptibility of C. elegans to TBZ in wild-type and in resistant genetic backgrounds.
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http://dx.doi.org/10.1042/BJ20141296DOI Listing
February 2015

Genomic characterisation of the effector complement of the potato cyst nematode Globodera pallida.

BMC Genomics 2014 Oct 23;15:923. Epub 2014 Oct 23.

The James Hutton Institute, Dundee Effector Consortium, Invergowrie, Dundee DD2 5DA, UK.

Background: The potato cyst nematode Globodera pallida has biotrophic interactions with its host. The nematode induces a feeding structure - the syncytium - which it keeps alive for the duration of the life cycle and on which it depends for all nutrients required to develop to the adult stage. Interactions of G. pallida with the host are mediated by effectors, which are produced in two sets of gland cells. These effectors suppress host defences, facilitate migration and induce the formation of the syncytium.

Results: The recent completion of the G. pallida genome sequence has allowed us to identify the effector complement from this species. We identify 128 orthologues of effectors from other nematodes as well as 117 novel effector candidates. We have used in situ hybridisation to confirm gland cell expression of a subset of these effectors, demonstrating the validity of our effector identification approach. We have examined the expression profiles of all effector candidates using RNAseq; this analysis shows that the majority of effectors fall into one of three clusters of sequences showing conserved expression characteristics (invasive stage nematode only, parasitic stage only or invasive stage and adult male only). We demonstrate that further diversity in the effector pool is generated by alternative splicing. In addition, we show that effectors target a diverse range of structures in plant cells, including the peroxisome. This is the first identification of effectors from any plant pathogen that target this structure.

Conclusion: This is the first genome scale search for effectors, combined to a life-cycle expression analysis, for any plant-parasitic nematode. We show that, like other phylogenetically unrelated plant pathogens, plant parasitic nematodes deploy hundreds of effectors in order to parasitise plants, with different effectors required for different phases of the infection process.
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http://dx.doi.org/10.1186/1471-2164-15-923DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4213498PMC
October 2014

Identification and characterisation of a hyper-variable apoplastic effector gene family of the potato cyst nematodes.

PLoS Pathog 2014 Sep 25;10(9):e1004391. Epub 2014 Sep 25.

Centre for Plant Sciences, University of Leeds, Leeds, United Kingdom.

Sedentary endoparasitic nematodes are obligate biotrophs that modify host root tissues, using a suite of effector proteins to create and maintain a feeding site that is their sole source of nutrition. Using assumptions about the characteristics of genes involved in plant-nematode biotrophic interactions to inform the identification strategy, we provide a description and characterisation of a novel group of hyper-variable extracellular effectors termed HYP, from the potato cyst nematode Globodera pallida. HYP effectors comprise a large gene family, with a modular structure, and have unparalleled diversity between individuals of the same population: no two nematodes tested had the same genetic complement of HYP effectors. Individuals vary in the number, size, and type of effector subfamilies. HYP effectors are expressed throughout the biotrophic stages in large secretory cells associated with the amphids of parasitic stage nematodes as confirmed by in situ hybridisation. The encoded proteins are secreted into the host roots where they are detectable by immunochemistry in the apoplasm, between the anterior end of the nematode and the feeding site. We have identified HYP effectors in three genera of plant parasitic nematodes capable of infecting a broad range of mono- and dicotyledon crop species. In planta RNAi targeted to all members of the effector family causes a reduction in successful parasitism.
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http://dx.doi.org/10.1371/journal.ppat.1004391DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4177990PMC
September 2014

The transcriptome of Nacobbus aberrans reveals insights into the evolution of sedentary endoparasitism in plant-parasitic nematodes.

Genome Biol Evol 2014 Aug 13;6(9):2181-94. Epub 2014 Aug 13.

Cell and Molecular Sciences Group, Dundee Effector Consortium, James Hutton Institute, Dundee, United Kingdom

Within the phylum Nematoda, plant-parasitism is hypothesized to have arisen independently on at least four occasions. The most economically damaging plant-parasitic nematode species, and consequently the most widely studied, are those that feed as they migrate destructively through host roots causing necrotic lesions (migratory endoparasites) and those that modify host root tissue to create a nutrient sink from which they feed (sedentary endoparasites). The false root-knot nematode Nacobbus aberrans is the only known species to have both migratory endoparasitic and sedentary endoparasitic stages within its life cycle. Moreover, its sedentary stage appears to have characteristics of both the root-knot and the cyst nematodes. We present the first large-scale genetic resource of any false-root knot nematode species. We use RNAseq to describe relative abundance changes in all expressed genes across the life cycle to provide interesting insights into the biology of this nematode as it transitions between modes of parasitism. A multigene phylogenetic analysis of N. aberrans with respect to plant-parasitic nematodes of all groups confirms its proximity to both cyst and root-knot nematodes. We present a transcriptome-wide analysis of both lateral gene transfer events and the effector complement. Comparing parasitism genes of typical root-knot and cyst nematodes to those of N. aberrans has revealed interesting similarities. Importantly, genes that were believed to be either cyst nematode, or root-knot nematode, "specific" have both been identified in N. aberrans. Our results provide insights into the characteristics of a common ancestor and the evolution of sedentary endoparasitism of plants by nematodes.
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http://dx.doi.org/10.1093/gbe/evu171DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4202313PMC
August 2014

The genome and life-stage specific transcriptomes of Globodera pallida elucidate key aspects of plant parasitism by a cyst nematode.

Genome Biol 2014 Mar 3;15(3):R43. Epub 2014 Mar 3.

Background: Globodera pallida is a devastating pathogen of potato crops, making it one of the most economically important plant parasitic nematodes. It is also an important model for the biology of cyst nematodes. Cyst nematodes and root-knot nematodes are the two most important plant parasitic nematode groups and together represent a global threat to food security.

Results: We present the complete genome sequence of G. pallida, together with transcriptomic data from most of the nematode life cycle, particularly focusing on the life cycle stages involved in root invasion and establishment of the biotrophic feeding site. Despite the relatively close phylogenetic relationship with root-knot nematodes, we describe a very different gene family content between the two groups and in particular extensive differences in the repertoire of effectors, including an enormous expansion of the SPRY domain protein family in G. pallida, which includes the SPRYSEC family of effectors. This highlights the distinct biology of cyst nematodes compared to the root-knot nematodes that were, until now, the only sedentary plant parasitic nematodes for which genome information was available. We also present in-depth descriptions of the repertoires of other genes likely to be important in understanding the unique biology of cyst nematodes and of potential drug targets and other targets for their control.

Conclusions: The data and analyses we present will be central in exploiting post-genomic approaches in the development of much-needed novel strategies for the control of G. pallida and related pathogens.
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http://dx.doi.org/10.1186/gb-2014-15-3-r43DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4054857PMC
March 2014

The feeding tube of cyst nematodes: characterisation of protein exclusion.

PLoS One 2014 28;9(1):e87289. Epub 2014 Jan 28.

Centre for Plant Sciences, University of Leeds, Leeds, United Kingdom.

Plant parasitic nematodes comprise several groups; the most economically damaging of these are the sedentary endoparasites. Sedentary endoparasitic nematodes are obligate biotrophs and modify host root tissue, using a suite of effector proteins, to create a feeding site that is their sole source of nutrition. They feed by withdrawing host cell assimilate from the feeding site though a structure known as the feeding tube. The function, composition and molecular characteristics of feeding tubes are poorly characterised. It is hypothesised that the feeding tube facilitates uptake of host cell assimilate by acting as a molecular sieve. Several studies, using molecular mass as the sole indicator of protein size, have given contradictory results about the exclusion limits of the cyst nematode feeding tube. In this study we propose a method to predict protein size, based on protein database coordinates in silico. We tested the validity of these predictions using travelling wave ion mobility spectrometry--mass spectrometry, where predictions and measured values were within approximately 6%. We used the predictions, coupled with mass spectrometry, analytical ultracentrifugation and protein electrophoresis, to resolve previous conflicts and define the exclusion characteristics of the cyst nematode feeding tube. Heterogeneity was tested in the liquid, solid and gas phase to provide a comprehensive evaluation of three proteins of particular interest to feeding tube size exclusion, GFP, mRFP and Dual PI. The data and procedures described here could be applied to the design of plant expressed defence compounds intended for uptake into cyst nematodes. We also highlight the need to assess protein heterogeneity when creating novel fusion proteins.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0087289PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3905015PMC
November 2014

Adaptive and specialised transcriptional responses to xenobiotic stress in Caenorhabditis elegans are regulated by nuclear hormone receptors.

PLoS One 2013 26;8(7):e69956. Epub 2013 Jul 26.

School of Biology, University of Leeds, Leeds, United Kingdom.

Characterisation of the pathways by which xenobiotics are metabolised and excreted in both target and non-target organisms is crucial for the rational design of effective and specific novel bioactive molecules. Consequently, we have investigated the induced responses of the model nematode Caenorhabditis elegans to a variety of xenobiotics which represent a range of putative modes of action. The majority of genes that were specifically induced in preliminary microarray analyses encoded enzymes from Phase I and II metabolism, including cytochrome P450s, short chain dehydrogenases, UDP-glucuronosyl transferases and glutathione transferases. Changes in gene expression were confirmed by quantitative PCR and GFP induction in reporter strains driven by promoters for transcription of twelve induced enzymes was investigated. The particular complement of metabolic genes induced was found to be highly contingent on the xenobiotic applied. The known regulators of responses to applied chemicals ahr-1, hif-1, mdt-15 and nhr-8 were not required for any of these inducible responses and skn-1 regulated GFP expression from only two of the promoters. Reporter strains were used in conjunction with systematic RNAi screens to identify transcription factors which drive expression of these genes under xenobiotic exposure. These transcription factors appeared to regulate specific xenobiotic responses and have no reported phenotypes under standard conditions. Focussing on nhr-176 we demonstrate the role of this transcription factor in mediating the resistance to thiabendazole.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0069956PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3724934PMC
April 2014

Identification of genes involved in the response of Arabidopsis to simultaneous biotic and abiotic stresses.

Plant Physiol 2013 Aug 25;162(4):2028-41. Epub 2013 Jun 25.

Centre for Plant Sciences, Faculty of Biological Sciences, University of Leeds, Leeds LS2 9JT, United Kingdom.

In field conditions, plants may experience numerous environmental stresses at any one time. Research suggests that the plant response to multiple stresses is different from that for individual stresses, producing nonadditive effects. In particular, the molecular signaling pathways controlling biotic and abiotic stress responses may interact and antagonize one another. The transcriptome response of Arabidopsis (Arabidopsis thaliana) to concurrent water deficit (abiotic stress) and infection with the plant-parasitic nematode Heterodera schachtii (biotic stress) was analyzed by microarray. A unique program of gene expression was activated in response to a combination of water deficit and nematode stress, with 50 specifically multiple-stress-regulated genes. Candidate genes with potential roles in controlling the response to multiple stresses were selected and functionally characterized. RAPID ALKALINIZATION FACTOR-LIKE8 (AtRALFL8) was induced in roots by joint stresses but conferred susceptibility to drought stress and nematode infection when overexpressed. Constitutively expressing plants had stunted root systems and extended root hairs. Plants may produce signal peptides such as AtRALFL8 to induce cell wall remodeling in response to multiple stresses. The methionine homeostasis gene METHIONINE GAMMA LYASE (AtMGL) was up-regulated by dual stress in leaves, conferring resistance to nematodes when overexpressed. It may regulate methionine metabolism under conditions of multiple stresses. AZELAIC ACID INDUCED1 (AZI1), involved in defense priming in systemic plant immunity, was down-regulated in leaves by joint stress and conferred drought susceptibility when overexpressed, potentially as part of abscisic acid-induced repression of pathogen response genes. The results highlight the complex nature of multiple stress responses and confirm the importance of studying plant stress factors in combination.
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http://dx.doi.org/10.1104/pp.113.222372DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3729780PMC
August 2013

The cell walls of syncytia formed by Heterodera schachtii in Arabidopsis thaliana are abundant in methyl-esterified pectin.

Plant Signal Behav 2012 Nov 7;7(11):1404-6. Epub 2012 Sep 7.

Centre for Plant Sciences, University of Leeds, Leeds, UK.

Plant-parasitic cyst nematodes form a specialized feeding site, termed a syncytium, in the roots of host plants. Monoclonal antibodies to defined glycans, in addition to a cellulose-binding module, were used to characterize the cell walls of a functioning syncytia in situ. Cell walls of syncytia were found to contain cellulose, xyloglucan and mannan. Analysis of the pectin network revealed syncytial cell walls are abundant in homogalacturonan, which was heavily methyl-esterified. Arabinan was also detected and the results suggest the cell walls of syncytia are highly flexible.
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http://dx.doi.org/10.4161/psb.21925DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3548858PMC
November 2012

The interaction of plant biotic and abiotic stresses: from genes to the field.

J Exp Bot 2012 Jun 30;63(10):3523-43. Epub 2012 Mar 30.

Centre for Plant Sciences, Faculty of Biological Sciences, University of Leeds, Leeds, UK.

Plant responses to different stresses are highly complex and involve changes at the transcriptome, cellular, and physiological levels. Recent evidence shows that plants respond to multiple stresses differently from how they do to individual stresses, activating a specific programme of gene expression relating to the exact environmental conditions encountered. Rather than being additive, the presence of an abiotic stress can have the effect of reducing or enhancing susceptibility to a biotic pest or pathogen, and vice versa. This interaction between biotic and abiotic stresses is orchestrated by hormone signalling pathways that may induce or antagonize one another, in particular that of abscisic acid. Specificity in multiple stress responses is further controlled by a range of molecular mechanisms that act together in a complex regulatory network. Transcription factors, kinase cascades, and reactive oxygen species are key components of this cross-talk, as are heat shock factors and small RNAs. This review aims to characterize the interaction between biotic and abiotic stress responses at a molecular level, focusing on regulatory mechanisms important to both pathways. Identifying master regulators that connect both biotic and abiotic stress response pathways is fundamental in providing opportunities for developing broad-spectrum stress-tolerant crop plants.
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http://dx.doi.org/10.1093/jxb/ers100DOI Listing
June 2012

Generation of transgenic plantain (Musa spp.) with resistance to plant pathogenic nematodes.

Mol Plant Pathol 2012 Oct 21;13(8):842-51. Epub 2012 Mar 21.

Centre for Plant Sciences, University of Leeds, Leeds LS2 9JT, UK.

Plant parasitic nematodes impose a severe constraint on plantain and banana productivity; however, the sterile nature of many cultivars precludes conventional breeding for resistance. Transgenic plantain cv. Gonja manjaya (Musa AAB) plants, expressing a maize cystatin that inhibits nematode digestive cysteine proteinases and a synthetic peptide that disrupts nematode chemoreception, were assessed for their ability to resist nematode infection. Lines were generated that expressed each gene singly or both together in a stacked defence. Nematode challenge with a single species or a mixed population identified 10 lines with significant resistance. The best level of resistance achieved against the major pest species Radopholus similis was 84% ± 8% for the cystatin, 66% ± 14% for the peptide and 70% ± 6% for the dual defence. In the mixed population, trial resistance was also demonstrated to Helicotylenchus multicinctus. A fluorescently labelled form of the chemodisruptive peptide underwent retrograde transport along certain sensory dendrites of R. similis as required to disrupt chemoreception. The peptide was degraded after 30 min in simulated intestinal fluid or boiling water and after 1 h in nonsterile soil. In silico sequence analysis suggests that the peptide is not a mammalian antigen. This work establishes the mode of action of a novel nematode defence, develops the evidence for its safe and effective deployment against multiple nematode species and identifies transgenic plantain lines with a high level of resistance for a proposed field trial.
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http://dx.doi.org/10.1111/j.1364-3703.2012.00792.xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6638790PMC
October 2012

Transgenic potatoes for potato cyst nematode control can replace pesticide use without impact on soil quality.

PLoS One 2012 16;7(2):e30973. Epub 2012 Feb 16.

Centre for Plant Sciences, University of Leeds, Leeds, United Kingdom.

Current and future global crop yields depend upon soil quality to which soil organisms make an important contribution. The European Union seeks to protect European soils and their biodiversity for instance by amending its Directive on pesticide usage. This poses a challenge for control of Globodera pallida (a potato cyst nematode) for which both natural resistance and rotational control are inadequate. One approach of high potential is transgenically based resistance. This work demonstrates the potential in the field of a new transgenic trait for control of G. pallida that suppresses root invasion. It also investigates its impact and that of a second transgenic trait on the non-target soil nematode community. We establish that a peptide that disrupts chemoreception of nematodes without a lethal effect provides resistance to G. pallida in both a containment and a field trial when precisely targeted under control of a root tip-specific promoter. In addition we combine DNA barcoding and quantitative PCR to recognise nematode genera from soil samples without microscope-based observation and use the method for nematode faunal analysis. This approach establishes that the peptide and a cysteine proteinase inhibitor that offer distinct bases for transgenic plant resistance to G. pallida do so without impact on the non-target nematode soil community.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0030973PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3281046PMC
August 2012

Strategies for transgenic nematode control in developed and developing world crops.

Curr Opin Biotechnol 2012 Apr 11;23(2):251-6. Epub 2011 Oct 11.

Centre for Plant Sciences, University of Leeds, Leeds LS2 9JT, UK.

Nematodes cause an estimated $118b annual losses to world crops and they are not readily controlled by pesticides or other control options. For many crops natural resistance genes are unavailable to plant breeders or progress by this approach is slow. Transgenic plants can provide nematode resistance for such crops. Two approaches have been field trialled that control a wide range of nematodes by either limiting use of their dietary protein uptake from the crop or by preventing root invasion without a direct lethality. In addition, RNA interference increasingly in tandem with genomic studies is providing a range of potential resistance traits that involve no novel protein production. Transgenic resistance can be delivered by tissue specific promoters to just root tissues where most economic nematodes invade and feed rather than the harvested yield. High efficacy and durability can be provided by stacking nematode resistance traits including any that natural resistance provides. The constraints to uptake centre on market acceptance and not the availability of appropriate biotechnology. The need to deploy nematode resistance is intensifying with loss of pesticides, an increased need to protect crop profit margins and in many developing world countries where nematodes severely damage both commodity and staple crops.
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http://dx.doi.org/10.1016/j.copbio.2011.09.004DOI Listing
April 2012

Influence of combined biotic and abiotic stress on nutritional quality parameters in tomato (Solanum lycopersicum).

J Agric Food Chem 2011 Sep 19;59(17):9673-82. Epub 2011 Aug 19.

Centre for Plant Sciences, Faculty of Biological Sciences, University of Leeds, Leeds LS2 9JT, United Kingdom.

Induction of abiotic stress in tomato plants has been proposed as a mechanism for improving the nutritional quality of fruits. However, the occurrence of biotic stress can interfere with normal abiotic stress responses. In this study, the combined effect of water stress and infection with plant-parasitic nematodes on the nutritional quality of tomato was investigated. Plants were exposed to one or both stresses, and the levels of phenolic compounds, carotenoids, and sugars in fruits were analyzed as well as physiological responses. Levels of carotenoids lycopene and β-carotene were lower in water-stressed tomatoes but exhibited a different response pattern under combined stress. Nematode stress was associated with increased flavonoid levels, albeit with reduced yields, while chlorogenic acid was increased by nematodes, water stress, and the combined stress. Sugar levels were higher only in tomatoes exposed to both stresses. These results emphasize the importance of studying plant stress factors in combination.
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http://dx.doi.org/10.1021/jf202081tDOI Listing
September 2011