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Article: Unveiling the Slippery Secrets of Saliva: Effector Proteins of Phloem-Feeding Insects.

Bleau, Jade R / Gaur, Namami / Fu, Yao / Bos, Jorunn I B

Molecular plant-microbe interactions : MPMI

2024 Volume 37, Issue 3, Page(s) 211–219

Abstract: Phloem-feeding insects include many important agricultural pests that cause crop damage globally, either through feeding-related damage or upon transmission of viruses and microbes that cause plant diseases. With genetic crop resistances being limited to ...

Abstract	Phloem-feeding insects include many important agricultural pests that cause crop damage globally, either through feeding-related damage or upon transmission of viruses and microbes that cause plant diseases. With genetic crop resistances being limited to most of these pests, control relies on insecticides, which are costly and damaging to the environment and to which insects can develop resistance. Like other plant parasites, phloem-feeding insects deliver effectors inside their host plants to promote susceptibility, most likely by a combination of suppressing immunity and promoting nutrient availability. The recent emergence of the effector paradigm in plant-insect interactions is highlighted by increasing availability of effector repertoires for a range of species and a broadening of our knowledge concerning effector functions. Here, we focus on recent progress made toward identification of effector repertoires from phloem-feeding insects and developments in effector biology that will advance functional characterization studies. Importantly, identification of effector activities from herbivorous insects promises to provide new avenues toward development of crop protection strategies. [Formula: see text] Copyright © 2024 The Author(s). This is an open access article distributed under the CC BY 4.0 International license.
MeSH term(s)	Animals ; Saliva/metabolism ; Phloem/metabolism ; Insecta ; Plants ; Herbivory
Language	English
Publishing date	2024-03-18
Publishing country	United States
Document type	Journal Article
ZDB-ID	743331-1
ISSN	1943-7706 ; 0894-0282
ISSN (online)	1943-7706
ISSN	0894-0282
DOI	10.1094/MPMI-10-23-0167-FI
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Article: Computational Prediction of Structure, Function, and Interaction of

Waksman, Thomas / Astin, Edmund / Fisher, S Ronan / Hunter, William N / Bos, Jorunn I B

Molecular plant-microbe interactions : MPMI

2024 Volume 37, Issue 3, Page(s) 338–346

Abstract: Similar to plant pathogens, phloem-feeding insects such as aphids deliver effector proteins inside their hosts that act to promote host susceptibility and enable feeding and infestation. Despite exciting progress toward identifying and characterizing ... ...

Abstract	Similar to plant pathogens, phloem-feeding insects such as aphids deliver effector proteins inside their hosts that act to promote host susceptibility and enable feeding and infestation. Despite exciting progress toward identifying and characterizing effector proteins from these insects, their functions remain largely unknown. The recent groundbreaking development in protein structure prediction algorithms, combined with the availability of proteomics and transcriptomic datasets for agriculturally important pests, provides new opportunities to explore the structural and functional diversity of effector repertoires. In this study, we sought to gain insight into the infection strategy used by the
MeSH term(s)	Animals ; Aphids ; Transcriptome ; Gene Expression Profiling ; Plant Proteins/genetics
Chemical Substances	Plant Proteins
Language	English
Publishing date	2024-03-18
Publishing country	United States
Document type	Journal Article
ZDB-ID	743331-1
ISSN	1943-7706 ; 0894-0282
ISSN (online)	1943-7706
ISSN	0894-0282
DOI	10.1094/MPMI-10-23-0154-FI
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Article: Plant resistance in different cell layers affects aphid probing and feeding behaviour during non-host and poor-host interactions

Escudero-Martinez, Carmen / Leybourne, Daniel J / Bos, Jorunn I.B

Bulletin of entomological research. 2021 Feb., v. 111, no. 1

2021

Abstract: Aphids are phloem-feeding insects that cause economic losses to crops globally. Whilst aphid interactions with susceptible plants and partially resistant genotypes have been well characterized, the interactions between aphids and non-host species are not ...

Abstract	Aphids are phloem-feeding insects that cause economic losses to crops globally. Whilst aphid interactions with susceptible plants and partially resistant genotypes have been well characterized, the interactions between aphids and non-host species are not well understood. Unravelling these non-host interactions can identify the mechanisms which contribute to plant resistance. Using contrasting aphid-host plant systems, including the broad host range pest Myzus persicae (host: Arabidopsis; poor-host: barley) and the cereal pest Rhopalosiphum padi (host: barley; non-host: Arabidopsis), we conducted a range of physiological experiments and compared aphid settling and probing behaviour on a host plant vs either a non-host or poor-host. In choice experiments, we observed that around 10% of aphids selected a non-host or poor-host plant species after 24 h. Using the Electrical Penetration Graph technique, we showed that feeding and probing behaviours differ during non-host and poor-host interactions when compared with a host interaction. In the Arabidopsis non-host interaction with the cereal pest R. padi aphids were unable to reach and feed on the phloem, with resistance likely residing in the mesophyll cell layer. In the barley poor-host interaction with M. persicae, resistance is likely phloem-based as phloem ingestion was reduced compared with the host interaction. Overall, our data suggest that plant resistance to aphids in non-host and poor-host interactions with these aphid species likely resides in different plant cell layers. Future work will take into account specific cell layers where resistances are based to dissect the underlying mechanisms and gain a better understanding of how we may improve crop resistance to aphids.
Keywords	Arabidopsis ; Myzus persicae ; Rhopalosiphum padi ; barley ; host plants ; host range ; ingestion ; mesophyll ; phloem ; research
Language	English
Dates of publication	2021-02
Size	p. 31-38.
Publishing place	Cambridge University Press
Document type	Article
Note	NAL-AP-2-clean
ZDB-ID	280516-9
ISSN	1475-2670 ; 0007-4853
ISSN (online)	1475-2670
ISSN	0007-4853
DOI	10.1017/S0007485320000231
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Article ; Online: Plant resistance in different cell layers affects aphid probing and feeding behaviour during non-host and poor-host interactions.

Escudero-Martinez, Carmen / Leybourne, Daniel J / Bos, Jorunn I B

Bulletin of entomological research

2020 Volume 111, Issue 1, Page(s) 31–38

Abstract	Aphids are phloem-feeding insects that cause economic losses to crops globally. Whilst aphid interactions with susceptible plants and partially resistant genotypes have been well characterized, the interactions between aphids and non-host species are not well understood. Unravelling these non-host interactions can identify the mechanisms which contribute to plant resistance. Using contrasting aphid-host plant systems, including the broad host range pest Myzus persicae (host: Arabidopsis; poor-host: barley) and the cereal pest Rhopalosiphum padi (host: barley; non-host: Arabidopsis), we conducted a range of physiological experiments and compared aphid settling and probing behaviour on a host plant vs either a non-host or poor-host. In choice experiments, we observed that around 10% of aphids selected a non-host or poor-host plant species after 24 h. Using the Electrical Penetration Graph technique, we showed that feeding and probing behaviours differ during non-host and poor-host interactions when compared with a host interaction. In the Arabidopsis non-host interaction with the cereal pest R. padi aphids were unable to reach and feed on the phloem, with resistance likely residing in the mesophyll cell layer. In the barley poor-host interaction with M. persicae, resistance is likely phloem-based as phloem ingestion was reduced compared with the host interaction. Overall, our data suggest that plant resistance to aphids in non-host and poor-host interactions with these aphid species likely resides in different plant cell layers. Future work will take into account specific cell layers where resistances are based to dissect the underlying mechanisms and gain a better understanding of how we may improve crop resistance to aphids.
MeSH term(s)	Animals ; Aphids/physiology ; Arabidopsis/physiology ; Herbivory ; Hordeum/physiology ; Plant Defense Against Herbivory
Language	English
Publishing date	2020-06-16
Publishing country	England
Document type	Journal Article
ZDB-ID	280516-9
ISSN	1475-2670 ; 0007-4853
ISSN (online)	1475-2670
ISSN	0007-4853
DOI	10.1017/S0007485320000231
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Article: Drought has negative consequences on aphid fitness and plant vigor: Insights from a meta-analysis.

Leybourne, Daniel J / Preedy, Katharine F / Valentine, Tracy A / Bos, Jorunn I B / Karley, Alison J

Ecology and evolution

2021 Volume 11, Issue 17, Page(s) 11915–11929

Abstract: Aphids are abundant in natural and managed vegetation, supporting a diverse community of organisms and causing damage to agricultural crops. Due to a changing climate, periods of drought are anticipated to increase, and the potential consequences of this ...

Abstract	Aphids are abundant in natural and managed vegetation, supporting a diverse community of organisms and causing damage to agricultural crops. Due to a changing climate, periods of drought are anticipated to increase, and the potential consequences of this for aphid-plant interactions are unclear.Using a meta-analysis and synthesis approach, we aimed to advance understanding of how increased drought incidence will affect this ecologically and economically important insect group and to characterize any potential underlying mechanisms. We used qualitative and quantitative synthesis techniques to determine whether drought stress has a negative, positive, or null effect on aphid fitness and examined these effects in relation to (a) aphid biology, (b) geographical region, and (c) host plant biology.Across all studies, aphid fitness is typically reduced under drought. Subgroup analysis detected no difference in relation to aphid biology, geographical region, or the aphid-plant combination, indicating the negative effect of drought on aphids is potentially universal. Furthermore, drought stress had a negative impact on plant vigor and increased plant concentrations of defensive chemicals, suggesting the observed response of aphids is associated with reduced plant vigor and increased chemical defense in drought-stressed plants.We propose a conceptual model to predict drought effects on aphid fitness in relation to plant vigor and defense to stimulate further research.
Language	English
Publishing date	2021-07-28
Publishing country	England
Document type	Journal Article
ZDB-ID	2635675-2
ISSN	2045-7758
ISSN	2045-7758
DOI	10.1002/ece3.7957
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Article: The price of protection: a defensive endosymbiont impairs nymph growth in the bird cherry‐oat aphid, Rhopalosiphum padi

Leybourne, Daniel J / Bos, Jorunn I. B / Karley, Alison J / Valentine, Tracy A

Insect science. 2020 Feb., v. 27, no. 1

2020

Abstract: Bacterial endosymbionts have enabled aphids to adapt to a range of stressors, but their effects in many aphid species remain to be established. The bird cherry‐oat aphid, Rhopalosiphum padi (Linnaeus), is an important pest of cereals worldwide and has ... ...

Abstract	Bacterial endosymbionts have enabled aphids to adapt to a range of stressors, but their effects in many aphid species remain to be established. The bird cherry‐oat aphid, Rhopalosiphum padi (Linnaeus), is an important pest of cereals worldwide and has been reported to form symbiotic associations with Serratia symbiotica and Sitobion miscanthi L‐type symbiont endobacteria, although the resulting aphid phenotype has not been described. This study presents the first report of R. padi infection with the facultative bacterial endosymbiont Hamiltonella defensa. Individuals of R. padi were sampled from populations in Eastern Scotland, UK, and shown to represent seven R. padi genotypes based on the size of polymorphic microsatellite markers; two of these genotypes harbored H. defensa. In parasitism assays, survival of H. defensa‐infected nymphs following attack by the parasitoid wasp Aphidius colemani (Viereck) was 5 fold higher than for uninfected nymphs. Aphid genotype was a major determinant of aphid performance on two Hordeum species, a modern cultivar of barley H. vulgare and a wild relative H. spontaneum, although aphids infected with H. defensa showed 16% lower nymph mass gain on the partially resistant wild relative compared with uninfected individuals. These findings suggest that deploying resistance traits in barley will favor the fittest R. padi genotypes, but symbiont‐infected individuals will be favored when parasitoids are abundant, although these aphids will not achieve optimal performance on a poor quality host plant.
Keywords	Aphidius colemani ; barley ; cultivars ; endosymbionts ; genetic markers ; genotype ; Hordeum vulgare subsp. spontaneum ; host plants ; insect diseases ; microsymbionts ; nymphs ; parasitic wasps ; parasitism ; phenotype ; Rhopalosiphum padi ; Serratia ; Sitobion ; wild relatives ; Scotland
Language	English
Dates of publication	2020-02
Size	p. 69-85.
Publishing place	John Wiley & Sons, Ltd
Document type	Article
Note	JOURNAL ARTICLE
ZDB-ID	2179775-4
ISSN	1744-7917 ; 1672-9609
ISSN (online)	1744-7917
ISSN	1672-9609
DOI	10.1111/1744-7917.12606
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Article ; Online: Drought stress increases the expression of barley defence genes with negative consequences for infesting cereal aphids.

Leybourne, Daniel J / Valentine, Tracy A / Binnie, Kirsty / Taylor, Anna / Karley, Alison J / Bos, Jorunn I B

Journal of experimental botany

2022 Volume 73, Issue 7, Page(s) 2238–2250

Abstract: Crops are exposed to myriad abiotic and biotic stressors with negative consequences. Two stressors that are expected to increase under climate change are drought and infestation with herbivorous insects, including important aphid species. Expanding our ... ...

Abstract	Crops are exposed to myriad abiotic and biotic stressors with negative consequences. Two stressors that are expected to increase under climate change are drought and infestation with herbivorous insects, including important aphid species. Expanding our understanding of the impact drought has on the plant-aphid relationship will become increasingly important under future climate scenarios. Here we use a previously characterized plant-aphid system comprising a susceptible variety of barley, a wild relative of barley with partial aphid resistance, and the bird cherry-oat aphid to examine the drought-plant-aphid relationship. We show that drought has a negative effect on plant physiology and aphid fitness, and provide evidence to suggest that plant resistance influences aphid responses to drought stress. Furthermore, we show that the expression of thionin genes, plant defensive compounds that contribute to aphid resistance, increase in susceptible plants exposed to drought stress but remain at constant levels in the partially resistant plant, suggesting that they play an important role in determining the success of aphid populations. This study highlights the role of plant defensive processes in mediating the interactions between the environment, plants, and herbivorous insects.
MeSH term(s)	Animals ; Aphids/physiology ; Droughts ; Edible Grain ; Herbivory ; Hordeum/genetics ; Hordeum/metabolism
Language	English
Publishing date	2022-01-28
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2976-2
ISSN	1460-2431 ; 0022-0957
ISSN (online)	1460-2431
ISSN	0022-0957
DOI	10.1093/jxb/erac010
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Article ; Online: Virulence strategies of an insect herbivore and oomycete plant pathogen converge on host E3 SUMO ligase SIZ1.

Liu, Shan / Lenoir, Camille J G / Amaro, Tiago M M M / Rodriguez, Patricia A / Huitema, Edgar / Bos, Jorunn I B

The New phytologist

2022 Volume 235, Issue 4, Page(s) 1599–1614

Abstract: Pathogens and pests secrete proteins (effectors) to interfere with plant immunity through modification of host target functions and disruption of immune signalling networks. The extent of convergence between pathogen and herbivorous insect virulence ... ...

Abstract	Pathogens and pests secrete proteins (effectors) to interfere with plant immunity through modification of host target functions and disruption of immune signalling networks. The extent of convergence between pathogen and herbivorous insect virulence strategies is largely unexplored. We found that effectors from the oomycete pathogen, Phytophthora capsici, and the major aphid pest, Myzus persicae target the host immune regulator SIZ1, an E3 SUMO ligase. We used transient expression assays in Nicotiana benthamiana as well as Arabidopsis mutants to further characterize biological role of effector-SIZ1 interactions in planta. We show that the oomycete and aphid effector, which both contribute to virulence, feature different activities towards SIZ1. While M. persicae effector Mp64 increases SIZ1 protein levels in transient assays, P. capsici effector CRN83_152 enhances SIZ1-E3 SUMO ligase activity in vivo. SIZ1 contributes to host susceptibility to aphids and an oomycete pathogen. Knockout of SIZ1 in Arabidopsis decreased susceptibility to aphids, independent of SNC1, PAD4 and EDS1. Similarly SIZ1 knockdown in N. benthamiana led to reduced P. capsici infection. Our results suggest convergence of distinct pathogen and pest virulence strategies on an E3 SUMO ligase to enhance host susceptibility.
MeSH term(s)	Animals ; Aphids/metabolism ; Arabidopsis/metabolism ; Arabidopsis Proteins/genetics ; Arabidopsis Proteins/metabolism ; Gene Expression Regulation, Plant ; Herbivory ; Ligases/metabolism ; Phytophthora/metabolism ; Ubiquitin-Protein Ligases/metabolism ; Virulence
Chemical Substances	Arabidopsis Proteins ; SNC1 protein, Arabidopsis ; Ubiquitin-Protein Ligases (EC 2.3.2.27) ; Ligases (EC 6.-) ; SIZ1 protein, Arabidopsis (EC 6.3.2.-)
Language	English
Publishing date	2022-05-28
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	208885-x
ISSN	1469-8137 ; 0028-646X
ISSN (online)	1469-8137
ISSN	0028-646X
DOI	10.1111/nph.18184
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Article: Virulence strategies of an insect herbivore and oomycete plant pathogen converge on host E3 SUMO ligase SIZ1

Liu, Shan / Lenoir, Camille J. G. / Amaro, Tiago M. M. M. / Rodriguez, Patricia A. / Huitema, Edgar / Bos, Jorunn I. B.

The new phytologist. 2022 Aug., v. 235, no. 4

2022

Abstract	Pathogens and pests secrete proteins (effectors) to interfere with plant immunity through modification of host target functions and disruption of immune signalling networks. The extent of convergence between pathogen and herbivorous insect virulence strategies is largely unexplored. We found that effectors from the oomycete pathogen, Phytophthora capsici, and the major aphid pest, Myzus persicae target the host immune regulator SIZ1, an E3 SUMO ligase. We used transient expression assays in Nicotiana benthamiana as well as Arabidopsis mutants to further characterize biological role of effector–SIZ1 interactions in planta. We show that the oomycete and aphid effector, which both contribute to virulence, feature different activities towards SIZ1. While M. persicae effector Mp64 increases SIZ1 protein levels in transient assays, P. capsici effector CRN83_152 enhances SIZ1‐E3 SUMO ligase activity in vivo. SIZ1 contributes to host susceptibility to aphids and an oomycete pathogen. Knockout of SIZ1 in Arabidopsis decreased susceptibility to aphids, independent of SNC1, PAD4 and EDS1. Similarly SIZ1 knockdown in N. benthamiana led to reduced P. capsici infection. Our results suggest convergence of distinct pathogen and pest virulence strategies on an E3 SUMO ligase to enhance host susceptibility.
Keywords	Arabidopsis ; Myzus persicae ; Nicotiana benthamiana ; Phytophthora capsici ; immunity ; ligases ; phytophagous insects ; plant pathogens ; virulence
Language	English
Dates of publication	2022-08
Size	p. 1599-1614.
Publishing place	John Wiley & Sons, Ltd
Document type	Article
Note	JOURNAL ARTICLE
ZDB-ID	208885-x
ISSN	1469-8137 ; 0028-646X
ISSN (online)	1469-8137
ISSN	0028-646X
DOI	10.1111/nph.18184
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Article ; Online: A fitness cost resulting from

Leybourne, Daniel J / Valentine, Tracy A / Bos, Jorunn I B / Karley, Alison J

The Journal of experimental biology

2020 Volume 223, Issue Pt 1

Abstract: Many herbivorous arthropods, including aphids, frequently associate with facultative endosymbiotic bacteria, which influence arthropod physiology and fitness. In aphids, endosymbionts can increase resistance against natural enemies, enhance aphid ... ...

Abstract	Many herbivorous arthropods, including aphids, frequently associate with facultative endosymbiotic bacteria, which influence arthropod physiology and fitness. In aphids, endosymbionts can increase resistance against natural enemies, enhance aphid virulence and alter aphid fitness. Here, we used the electrical penetration graph technique to uncover physiological processes at the insect-plant interface affected by endosymbiont infection. We monitored the feeding and probing behaviour of four independent clonal lines of the cereal-feeding aphid
MeSH term(s)	Animals ; Aphids/genetics ; Aphids/growth & development ; Aphids/physiology ; Enterobacteriaceae/physiology ; Feeding Behavior ; Genetic Fitness ; Nymph/genetics ; Nymph/growth & development ; Nymph/physiology ; Symbiosis
Language	English
Publishing date	2020-01-02
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	218085-6
ISSN	1477-9145 ; 0022-0949
ISSN (online)	1477-9145
ISSN	0022-0949
DOI	10.1242/jeb.207936
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