Publications by authors named "Karen J Kloth"

11 Publications

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SLI1 confers broad-spectrum resistance to phloem-feeding insects.

Plant Cell Environ 2021 Apr 10. Epub 2021 Apr 10.

Laboratory of Entomology, Wageningen University & Research, Wageningen, The Netherlands.

Resistance (R) genes usually compete in a coevolutionary arms race with reciprocal effectors to confer strain-specific resistance to pathogens or herbivorous insects. Here, we investigate the specificity of SLI1, a recently identified R gene in Arabidopsis that encodes a small heat shock-like protein involved in resistance to Myzus persicae aphids. In a panel with several aphid and whitefly species, SLI1 compromised reproductive rates of three species: the tobacco aphid M. persicae nicotianae, the cabbage aphid Brevicoryne brassicae and the cabbage whitefly Aleyrodes proletella. Electrical penetration graph recording of aphid behaviour, revealed shorter salivations and a 3-to-5-fold increase in phloem feeding on sli1 loss-of-function plants. The mustard aphid Lipaphis erysimi and Bemisia tabaci whitefly were not affected by SLI1. Unlike the other two aphid species, L. erysimi exhibited repetitive salivations preceding successful phloem feeding, indicating a role of salivary effectors in overcoming SLI1-mediated resistance. Microscopic characterization showed that SLI1 proteins localize in the sieve tubes of virtually all above- and below-ground tissues and co-localize with the aphid stylet tip after penetration of the sieve element plasma membrane. These observations reveal an unconventional R gene that escapes the paradigm of strain specificity and confers broad-spectrum quantitative resistance to phloem-feeding insects.
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http://dx.doi.org/10.1111/pce.14064DOI Listing
April 2021

Defenses against Virus and Vector: A Phloem-Biological Perspective on RTM- and SLI1-Mediated Resistance to Potyviruses and Aphids.

Viruses 2020 01 22;12(2). Epub 2020 Jan 22.

Laboratory of Virology, Wageningen University and Research, 6700 AA Wageningen, The Netherlands.

Combining plant resistance against virus and vector presents an attractive approach to reduce virus transmission and virus proliferation in crops. () genes confer resistance to potyviruses by limiting their long-distance transport. Recently, a close homologue of one of the genes, , has been discovered but this gene instead confers resistance to aphids, a vector of potyviruses. The functional connection between resistance to potyviruses and aphids, raises the question whether plants have a basic defense system in the phloem against biotic intruders. This paper provides an overview on restricted potyvirus phloem transport and restricted aphid phloem feeding and their possible interplay, followed by a discussion on various ways in which viruses and aphids gain access to the phloem sap. From a phloem-biological perspective, hypotheses are proposed on the underlying mechanisms of RTM- and SLI1-mediated resistance, and their possible efficacy to defend against systemic viruses and phloem-feeding vectors.
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http://dx.doi.org/10.3390/v12020129DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7077274PMC
January 2020

PECTIN ACETYLESTERASE9 Affects the Transcriptome and Metabolome and Delays Aphid Feeding.

Plant Physiol 2019 12 24;181(4):1704-1720. Epub 2019 Sep 24.

Department of Plant Physiology, Umeå Plant Science Centre, Umeå University, S-90187 Umea, Sweden.

The plant cell wall plays an important role in damage-associated molecular pattern-induced resistance to pathogens and herbivorous insects. Our current understanding of cell wall-mediated resistance is largely based on the degree of pectin methylesterification. However, little is known about the role of pectin acetylesterification in plant immunity. This study describes how one pectin-modifying enzyme, (), affects the Arabidopsis () transcriptome, secondary metabolome, and aphid performance. Electro-penetration graphs showed that aphids established phloem feeding earlier on mutants. Whole-genome transcriptome analysis revealed a set of 56 differentially expressed genes (DEGs) between uninfested mutants and wild-type plants. The majority of the DEGs were enriched for biotic stress responses and down-regulated in the mutant, including and , involved in camalexin and indole glucosinolate biosynthesis, respectively. Relative quantification of more than 100 secondary metabolites revealed decreased levels of several compounds, including camalexin and oxylipins, in two independent mutants. In addition, absolute quantification of phytohormones showed that jasmonic acid (JA), jasmonoyl-Ile, salicylic acid, abscisic acid, and indole-3-acetic acid were compromised due to PAE9 loss of function. After aphid infestation, however, mutants increased their levels of camalexin, glucosinolates, and JA, and no long-term effects were observed on aphid fitness. Overall, these data show that PAE9 is required for constitutive up-regulation of defense-related compounds, but that it is not required for aphid-induced defenses. The signatures of phenolic antioxidants, phytoprostanes, and oxidative stress-related transcripts indicate that the processes underlying PAE9 activity involve oxidation-reduction reactions.
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http://dx.doi.org/10.1104/pp.19.00635DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6878011PMC
December 2019

Defence priming in Arabidopsis - a Meta-Analysis.

Sci Rep 2019 09 16;9(1):13309. Epub 2019 Sep 16.

Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, Umeå Plant Science Centre, Umeå, Sweden.

Defence priming by organismal and non-organismal stimulants can reduce effects of biotic stress in plants. Thus, it could help efforts to enhance the sustainability of agricultural production by reducing use of agrochemicals in protection of crops from pests and diseases. We have explored effects of applying this approach to both Arabidopsis plants and seeds of various crops in meta-analyses. The results show that its effects on Arabidopsis plants depend on both the priming agent and antagonist. Fungi and vitamins can have strong priming effects, and priming is usually more effective against bacterial pathogens than against herbivores. Moreover, application of bio-stimulants (particularly vitamins and plant defence elicitors) to seeds can have promising defence priming effects. However, the published evidence is scattered, does not include Arabidopsis, and additional studies are required before we can draw general conclusions and understand the molecular mechanisms involved in priming of seeds' defences. In conclusion, defence priming of plants has clear potential and application of bio-stimulants to seeds may protect plants from an early age, promises to be both labour- and resource-efficient, poses very little environmental risk, and is thus both economically and ecologically promising.
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http://dx.doi.org/10.1038/s41598-019-49811-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6746867PMC
September 2019

SIEVE ELEMENT-LINING CHAPERONE1 Restricts Aphid Feeding on Arabidopsis during Heat Stress.

Plant Cell 2017 Oct 28;29(10):2450-2464. Epub 2017 Sep 28.

Bioscience, Wageningen University & Research, 6708 PB Wageningen, The Netherlands.

The role of phloem proteins in plant resistance to aphids is still largely elusive. By genome-wide association mapping of aphid behavior on 350 natural accessions, we identified the small heat shock-like (). Detailed behavioral studies on near-isogenic and knockout lines showed that SLI1 impairs phloem feeding. Depending on the haplotype, aphids displayed a different duration of salivation in the phloem. On mutants, aphids prolonged their feeding sessions and ingested phloem at a higher rate than on wild-type plants. The largest phenotypic effects were observed at 26°C, when expression is upregulated. At this moderately high temperature, mutants suffered from retarded elongation of the inflorescence and impaired silique development. Fluorescent reporter fusions showed that SLI1 is confined to the margins of sieve elements where it lines the parietal layer and colocalizes in spherical bodies around mitochondria. This localization pattern is reminiscent of the clamp-like structures observed in previous ultrastructural studies of the phloem and shows that the parietal phloem layer plays an important role in plant resistance to aphids and heat stress.
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http://dx.doi.org/10.1105/tpc.16.00424DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5774557PMC
October 2017

Natural variation in life history strategy of Arabidopsis thaliana determines stress responses to drought and insects of different feeding guilds.

Mol Ecol 2017 Jun 6;26(11):2959-2977. Epub 2017 Apr 6.

Laboratory of Entomology, Wageningen University, Wageningen, The Netherlands.

Plants are sessile organisms and, consequently, are exposed to a plethora of stresses in their local habitat. As a result, different populations of a species are subject to different selection pressures leading to adaptation to local conditions and intraspecific divergence. The annual brassicaceous plant Arabidopsis thaliana is an attractive model for ecologists and evolutionary biologists due to the availability of a large collection of resequenced natural accessions. Accessions of A. thaliana display one of two different life cycle strategies: summer and winter annuals. We exposed a collection of 308 European Arabidopsis accessions, that have been genotyped for 250K SNPs, to a range of stresses: one abiotic stress (drought), four biotic stresses (Pieris rapae caterpillars, Plutella xylostella caterpillars, Frankliniella occidentalis thrips and Myzus persicae aphids) and two combined stresses (drought plus P. rapae and Botrytis cinerea fungus plus P. rapae). We identified heritable genetic variation for responses to the different stresses, estimated by narrow-sense heritability. We found that accessions displaying different life cycle strategies differ in their response to stresses. Winter annuals are more resistant to drought, aphids and thrips and summer annuals are more resistant to P. rapae and P. xylostella caterpillars. Summer annuals are also more resistant to the combined stresses of drought plus P. rapae and infection by the fungus Botryris cinerea plus herbivory by P. rapae. Adaptation to drought displayed a longitudinal gradient. Finally, trade-offs were recorded between the response to drought and responses to herbivory by caterpillars of the specialist herbivore P. rapae.
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http://dx.doi.org/10.1111/mec.14100DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5485070PMC
June 2017

Genetic architecture of plant stress resistance: multi-trait genome-wide association mapping.

New Phytol 2017 Feb 4;213(3):1346-1362. Epub 2016 Oct 4.

Wageningen University and Research Plant Breeding, Wageningen University and Research, PO Box 386, 6700 AJ, Wageningen, the Netherlands.

Plants are exposed to combinations of various biotic and abiotic stresses, but stress responses are usually investigated for single stresses only. Here, we investigated the genetic architecture underlying plant responses to 11 single stresses and several of their combinations by phenotyping 350 Arabidopsis thaliana accessions. A set of 214 000 single nucleotide polymorphisms (SNPs) was screened for marker-trait associations in genome-wide association (GWA) analyses using tailored multi-trait mixed models. Stress responses that share phytohormonal signaling pathways also share genetic architecture underlying these responses. After removing the effects of general robustness, for the 30 most significant SNPs, average quantitative trait locus (QTL) effect sizes were larger for dual stresses than for single stresses. Plants appear to deploy broad-spectrum defensive mechanisms influencing multiple traits in response to combined stresses. Association analyses identified QTLs with contrasting and with similar responses to biotic vs abiotic stresses, and below-ground vs above-ground stresses. Our approach allowed for an unprecedented comprehensive genetic analysis of how plants deal with a wide spectrum of stress conditions.
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http://dx.doi.org/10.1111/nph.14220DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5248600PMC
February 2017

AtWRKY22 promotes susceptibility to aphids and modulates salicylic acid and jasmonic acid signalling.

J Exp Bot 2016 05 23;67(11):3383-96. Epub 2016 Apr 23.

Plant Research International, Business Unit Bioscience, Wageningen University and Research Centre, PO Box 16, 6700 AA Wageningen, The Netherlands.

Aphids induce many transcriptional perturbations in their host plants, but the signalling cascades responsible and the effects on plant resistance are largely unknown. Through a genome-wide association (GWA) mapping study in Arabidopsis thaliana, we identified WRKY22 as a candidate gene associated with feeding behaviour of the green peach aphid, Myzus persicae The transcription factor WRKY22 is known to be involved in pathogen-triggered immunity, and WRKY22 gene expression has been shown to be induced by aphids. Assessment of aphid population development and feeding behaviour on knockout mutants and overexpression lines showed that WRKY22 increases susceptibility to M. persicae via a mesophyll-located mechanism. mRNA sequencing analysis of aphid-infested wrky22 knockout plants revealed the up-regulation of genes involved in salicylic acid (SA) signalling and down-regulation of genes involved in plant growth and cell-wall loosening. In addition, mechanostimulation of knockout plants by clip cages up-regulated jasmonic acid (JA)-responsive genes, resulting in substantial negative JA-SA crosstalk. Based on this and previous studies, WRKY22 is considered to modulate the interplay between the SA and JA pathways in response to a wide range of biotic and abiotic stimuli. Its induction by aphids and its role in suppressing SA and JA signalling make WRKY22 a potential target for aphids to manipulate host plant defences.
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http://dx.doi.org/10.1093/jxb/erw159DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4892728PMC
May 2016

Automated video tracking of thrips behavior to assess host-plant resistance in multiple parallel two-choice setups.

Plant Methods 2016 18;12. Epub 2016 Jan 18.

PRI-Bioscience, Wageningen University and Research Center, P.O. Box 16, 6700 AA Wageningen, The Netherlands.

Background: Piercing-sucking insects cause severe damage in crops. Breeding for host-plant resistance can significantly reduce the yield losses caused by these insects, but host-plant resistance is a complex trait that is difficult to phenotype quickly and reliably. Current phenotyping methods mainly focus on labor-intensive and time-consuming end-point measurements of plant fitness. Characterizing insect behavior as a proxy for host-plant resistance could be a promising time-saving alternative to end-point measurements.

Results: We present a phenotyping platform that allows screening for host-plant resistance against Western flower thrips (WFT, Frankliniella occidentalis (Pergande)) in a parallel two-choice setup using automated video tracking of thrips behavior. The platform was used to establish host-plant preference of WFT with a large plant population of 345 wild Arabidopsis accessions and the method was optimized with two extreme accessions from this population that differed in resistance towards WFT. To this end, the behavior of 88 WFT individuals was simultaneously tracked in 88 parallel two-choice arenas during 8 h. Host-plant preference of WFT was established both by the time thrips spent on either accession and various behavioral parameters related to movement (searching) and non-movement (feeding) events.

Conclusion: In comparison to 6-day end-point choice assays with whole plants or detached leaves, the automated video-tracking choice assay developed here delivered similar results, but with higher time- and resource efficiency. This method can therefore be a reliable and effective high throughput phenotyping tool to assess host-plant resistance to thrips in large plant populations.
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http://dx.doi.org/10.1186/s13007-016-0102-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4717623PMC
January 2016

High-throughput phenotyping of plant resistance to aphids by automated video tracking.

Plant Methods 2015 30;11. Epub 2015 Jan 30.

Plant Research International, Wageningen University and Research Center, P.O. Box 16, 6700 AA Wageningen, The Netherlands.

Background: Piercing-sucking insects are major vectors of plant viruses causing significant yield losses in crops. Functional genomics of plant resistance to these insects would greatly benefit from the availability of high-throughput, quantitative phenotyping methods.

Results: We have developed an automated video tracking platform that quantifies aphid feeding behaviour on leaf discs to assess the level of plant resistance. Through the analysis of aphid movement, the start and duration of plant penetrations by aphids were estimated. As a case study, video tracking confirmed the near-complete resistance of lettuce cultivar 'Corbana' against Nasonovia ribisnigri (Mosely), biotype Nr:0, and revealed quantitative resistance in Arabidopsis accession Co-2 against Myzus persicae (Sulzer). The video tracking platform was benchmarked against Electrical Penetration Graph (EPG) recordings and aphid population development assays. The use of leaf discs instead of intact plants reduced the intensity of the resistance effect in video tracking, but sufficiently replicated experiments resulted in similar conclusions as EPG recordings and aphid population assays. One video tracking platform could screen 100 samples in parallel.

Conclusions: Automated video tracking can be used to screen large plant populations for resistance to aphids and other piercing-sucking insects.
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http://dx.doi.org/10.1186/s13007-015-0044-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4318543PMC
February 2015

Association mapping of plant resistance to insects.

Trends Plant Sci 2012 May 8;17(5):311-9. Epub 2012 Feb 8.

Laboratory of Entomology, Wageningen University, P.O. Box 8031, 6700 EH Wageningen, The Netherlands.

Association mapping is rapidly becoming an important method to explore the genetic architecture of complex traits in plants and offers unique opportunities for studying resistance to insect herbivores. Recent studies indicate that there is a trade-off between resistance against generalist and specialist insects. Most studies, however, use a targeted approach that will easily miss important components of insect resistance. Genome-wide association mapping provides a comprehensive approach to explore the whole array of plant defense mechanisms in the context of the generalist-specialist paradigm. As association mapping involves the screening of large numbers of plant lines, specific and accurate high-throughput phenotyping (HTP) methods are needed. Here, we discuss the prospects of association mapping for insect resistance and HTP requirements.
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http://dx.doi.org/10.1016/j.tplants.2012.01.002DOI Listing
May 2012