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Antagonist effects of the leek Allium porrum as a companion plant on aphid host plant colonization.

ABSTRACT: Combining a non-host plant (companion plant or CP) with a target cultivated plant is considered as a promising strategy to reduce pest pressure. Among the companion plants (CP) commonly used in integrated systems, those belonging to the Amaryllidaceae family (chives, garlic, onion, leek) exhibit characteristics related to certain volatile organic compounds (VOCs) with promising repellent potentialities. The aim of this work was to investigate the potential disruption of sweet pepper (host plant) colonization by the green peach aphid (Myzus persicae) when exposed to leek (Allium porrum) as a CP. Retention/dispersion, EPG and clip-cage/Petri dish laboratory experiments were thus performed to study the effect of leek VOCs on aphid settlement/migration, feeding behavior and life history traits parameters, respectively. This work revealed that leek as a CP had a negative effect on aphid feeding behavior, by disturbing the balance between phloem and xylem sap ingestion, but had no influence concerning aphid settlement. Surprisingly, leek as a CP triggered some unexpected probiotic effects on certain life history traits such as aphid survival, biomass, and fecundity, suggesting a possible hormetic effect of leek VOCs on aphid physiology. The possibility of experience-induced preference of aphids for leek VOCs was also discussed.

SUBMITTER: Baudry X

PROVIDER: S-EPMC7889937 | biostudies-literature | 2021 Feb

REPOSITORIES: biostudies-literature

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Antagonist effects of the leek Allium porrum as a companion plant on aphid host plant colonization.

Baudry Xavier X Doury Géraldine G Couty Aude A Fourdrain Yvelise Y van Havermaet Robin R Lateur Marc M Ameline Arnaud A

Scientific reports 20210217 1

Combining a non-host plant (companion plant or CP) with a target cultivated plant is considered as a promising strategy to reduce pest pressure. Among the companion plants (CP) commonly used in integrated systems, those belonging to the Amaryllidaceae family (chives, garlic, onion, leek) exhibit characteristics related to certain volatile organic compounds (VOCs) with promising repellent potentialities. The aim of this work was to investigate the potential disruption of sweet pepper (host plant) ...[more]

PMID: 33597636

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Project description:Host adaptation plays a crucial role in virus evolution and is a consequence of long-term interactions between virus and host in a complex arms race between host RNA silencing and viral RNA silencing suppressor (RSS) as counterdefense. Leek yellow stripe virus (LYSV), a potyvirus causing yield loss of garlic, infects several species of Allium plants. The unexpected discovery of an interspecific hybrid of garlic, leek, and great-headed (GH) garlic motivated us to explore the host-adaptive evolution of LYSV. Here, using Bayesian phylogenetic comparative methods and a functional assay of viral RSS activity, we show that the evolutionary context of LYSV has been shaped by the host adaptation of the virus during its coevolution with Allium plants. Our phylogenetic analysis revealed that LYSV isolates from leek and their taxonomic relatives (Allium ampeloprasum complex; AAC) formed a distinct monophyletic clade separate from garlic isolates and are likely to be uniquely adapted to AAC. Our comparative studies on viral accumulation indicated that LYSV accumulated at a low level in leek, whereas LYSVs were abundant in other Allium species such as garlic and its relatives. When RSS activity of the viral P1 and HC-Pro of leek LYSV isolate was analyzed, significant synergism in RSS activity between the two proteins was observed in leek but not in other species, suggesting that viral RSS activity may be important for the viral host-specific adaptation. We thus consider that LYSV may have undergone host-specific evolution at least in leek, which must be driven by speciation of its Allium hosts. IMPORTANCE Potyviruses are the most abundant plant RNA viruses and are extremely diversified in terms of their wide host range. Due to frequent host switching during their evolution, host-specific adaptation of potyviruses may have been shaped by numerous host factors. However, any critical determinants for viral host range remain largely unknown, possibly because of the repeated gain and loss of virus infectivity of plants. Leek yellow stripe virus (LYSV) is a species of the genus Potyvirus, which has a relatively narrow host range, generally limited to hosts in the genus Allium. Our investigations on leek and leek relatives (Allium ampeloprasum complex), which must have been generated through interspecies hybridization, revealed that LYSV accumulation remained low in leek as a result of viral host adaptation in competition with host resistance such as RNA silencing. This study presents LYSV as an ideal model to study the process of host-adaptive evolution and virus-host coevolution.

Project description:Polyphagous aphids often consist of host-specialized lineages, which have greater fitness on their native hosts than on others. The underlying causes are important for understanding of the evolution of diet breadth and host shift of aphids. The cotton-melon aphid Aphis gossypii Glover is extremely polyphagous with many strict host-specialized lineages. Whether and how the lineage specialized on the primary host hibiscus shifts to the secondary host cucumber remains elusive. We found that the hibiscus-specialized lineage suffered high mortality and gave birth to very few nymphs developing into yellow dwarfs on fresh cucumber leaves, and did not inflict any damage symptoms on cucumber plants. The poor performance did not improve with prolonged exposure to cucumber; however, it did significantly improve when the cucumber leaves were pre-infected with a biotrophic phytopathogen Pseudoperonospora cubensis. More importantly, the hibiscus-specialized lineage with two-generation feeding experience on pre-infected cucumber leaves performed as well as the cucumber-specialized lineage did on fresh cucumber leaves, and inflicted typical damage symptoms on intact cucumber plants. Electrical penetration graph (EPG) indicated that the hibiscus-specialized lineage did not ingest phloem sap from fresh cucumber leaves but succeeded in ingesting phloem sap from pre-infected cucumber leaves, which explained the performance improvement of the hibiscus-specialized lineage on pre-infected cucumber leaves. This study revealed a new pathway for the hibiscus-specialized lineage to quickly acclimate to cucumber under the assistance of the phytopathogen. We considered that the short feeding experience on pre-infected cucumber may activate expression of effector genes that are related to specific host utilization. We suggest to identify host-specific effectors by comparing proteomes or/and transcriptomes of the hibiscus-specialized lineage before and after acclimating to cucumber.

Project description:Genetic variation in plants can influence the community structure of associated species, through both direct and indirect interactions. Herbivorous insects are known to feed on a restricted range of plants, and herbivore preference and performance can vary among host plants within a species due to genetically based traits of the plant (e.g., defensive compounds). In a natural system, we expect to find genetic variation within both plant and herbivore communities and we expect this variation to influence species interactions. Using a three-species plant-aphid model system, we investigated the effect of genetic diversity on genetic interactions among the community members. Our system involved a host plant (Hordeum vulgare) that was shared by an aphid (Sitobion avenae) and a hemi-parasitic plant (Rhinanthus minor). We showed that aphids cluster more tightly in a genetically diverse host-plant community than in a genetic monoculture, with host-plant genetic diversity explaining up to 24% of the variation in aphid distribution. This is driven by differing preferences of the aphids to the different plant genotypes and their resulting performance on these plants. Within the two host-plant diversity levels, aphid spatial distribution was influenced by an interaction among the aphid's own genotype, the genotype of a competing aphid, the origin of the parasitic plant population, and the host-plant genotype. Thus, the overall outcome involves both direct (i.e., host plant to aphid) and indirect (i.e., parasitic plant to aphid) interactions across all these species. These results show that a complex genetic environment influences the distribution of herbivores among host plants. Thus, in genetically diverse systems, interspecific genetic interactions between the host plant and herbivore can influence the population dynamics of the system and could also structure local communities. We suggest that direct and indirect genotypic interactions among species can influence community structure and processes.

Dataset Information

Antagonist effects of the leek Allium porrum as a companion plant on aphid host plant colonization.

Publications

Antagonist effects of the leek Allium porrum as a companion plant on aphid host plant colonization.

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