Beata Gabryś

Phytohormonal signaling in plant responses to aphid feeding

Aphid feeding induces various defense signaling mechanisms in plants. The recognition of feeding activities by plants occurs through the use of transmembrane pattern recognition receptors (PRRS) or, acting largely inside the cell, polymorphic nucleotide-binding leucine-rich-repeat (NB-LRR) protein products, encoded by most R genes. Activation may induce defensive reactions which are the result of highly coordinated sequential changes at the cellular level comprising, among other changes, the synthesis of signaling molecules. The ensuing plant responses are followed by the transmission of defense response signal cascades. Signals are mediated by bioactive endogenous molecules, i.e. phytohormones, such as jasmonic acid (JA), salicylic acid (SA), ethylene (ET), abscisic acid (ABA), gibberellic acid (GA) and free radicals such as hydrogen peroxide (H2O2) and nitric oxide (NO) which independently provide direct chemical resistance. Plant-induced defenses are also regulated by a network of inter-connecting signaling pathways, in which JA, SA, and ET play dominant roles. Both synergistic and inhibitory aspects of the cross-talk among these pathways have been reported. This paper presents molecular mechanisms of plant response to aphid feeding, the precise activation of various endogenous bioactive molecules signaling in the response of many plant species and their participation in the regulation of numerous defense genes, which lead to a specific metabolic effect. Selected important points in signal transduction pathways were also discussed in studies on plant response to aphid feeding.

Differential induction of Pisum sativum defense signaling molecules in response to pea aphid infestation.

This study demonstrates the sequence of enhanced generation of signal molecules such as phytohormones, i.e. jasmonic acid (JA), ethylene (ET), salicylic acid (SA), and a relatively stable free radical, nitric oxide (NO), in response of Pisum sativum L. cv. Cysterski seedling leaves to the infestation of pea aphid Acyrthosiphon pisum (Harris) at a varied population size. In time from 0 to 96h after A. pisum infestation these signal molecules accumulated transiently. Moreover, the convergence of these signaling pathways occurred. JA and its methyl derivative MeJA reached the first maximum of generation at 24th hour of infestation. An increase in ET and NO generation was observed at 48th hour of infestation. The increase in SA, JA/MeJA and ET concentrations in aphid-infested leaves occurred from the 72nd to 96th hour. In parallel, an increase was demonstrated for the activities of enzymes engaged in the biosynthesis of SA, such as phenylalanine ammonia-lyase (PAL) and benzoic acid 2-hydroxylase (BA2H). Additionally, a considerable post-infestation accumulation of transcripts for PAL was observed. An increase in the activity of lipoxygenase (LOX), an important enzyme in the biosynthesis of JA was noted. This complex signaling network may contribute to the coordinated regulation of gene expression leading to specific defence responses.

Acceptability of different species of Brassicaceae as hosts for the cabbage aphid

The probing and feeding behaviour of the cabbage aphid, Brevicoryne brassicae (L.), (Homoptera, Aphididae) was studied on several plant species that represented various levels of acceptability: Sinapis alba L. (a permanent host plant), Capsella bursa‐pastoris (L.) Med., Thlaspi arvense L., Lunaria annua L., Erysimum cheiranthoides L. (accidental host plants), Vicia faba L. (a non‐host plant), using the electrical penetration graph technique (EPG). B. brassicae on V. faba did not show any patterns related to penetration of phloem vessels. Stylet penetration was deterred on L. annua and E. cheiranthoides where non‐penetration prevailed, the periods of sap ingestion were short or did not occur, the percentage of time spent in the phloem was consistently low (5–6%) and E1 salivation predominated. The pathway activities were not suppressed on C. bursa‐pastoris and T. arvense and the aphids spent an average of 3 h in the phloem during the 8‐h experiment. However, a considerable delay between finding and accepting the phloem and a substantial proportion of E1 salivation (20–30% of all phloem activities) indicated a deterrent factor in the sieve elements of these plants. Aphid probing and sap ingestion were rarely interrupted on S. alba. The results of this study suggest that the deterrent agents vary in activity and may hinder stylet penetration at different levels (epidermis, parenchymatous tissues and/or phloem elements), depending on the plant species.

Anomalous stylet punctures of phloem sieve elements by aphids

A deviating type of potential drop (pd), i.e. the electrically recorded intracellular punctures during the pathway phase of plant penetration by aphids, is described and discussed. This so-called repetitive pd (R-pd) has been observed in 4 aphid species, two on herbs and two on sycamore. Apart from a regular repetition with short intervals, the most characteristic feature of the R-pd is the middle intracellular part, i.e. sub-phase 2, which is extended, making the individual R-pd 2-3 times longer than the normal pd. Differences between the normal and R-pd are described, as well as differences within each pd type between species. The R-pd’s seem to reflect repeated punctures of phloem sieve elements. Their biological significance is unknown.

Sex Pheromone of Cabbage Aphid Brevicoryne brassicae: Identification and Field Trapping of Male Aphids and Parasitoids

The sex pheromone of the cabbage aphid, Brevicoryne brassicae, is shown by GC and GC-MS analysis of pheromone entrained from sexual females, and by electrophysiological studies on single cell preparations from male antennae, to comprise (4aS,7S,7aR)-nepetalactone. The compound proved to be attractive in a laboratory bioassay and release of the pheromone from glass vials placed above water traps in crops of autumn brassicaceous crops increased the catch of males of this species. The specialist parasitoid of B. brassicae, Diaeretiella rapae, and the more general aphid parasitoid Praon volucre were found in significantly larger numbers in pheromone traps as compared to the controls, under certain conditions.

European yellow lupine, Lupinus luteus, and narrow‐leaf lupine, Lupinus angustifolius, as hosts for the pea aphid, Acyrthosiphon pisum

The pea aphid, Acyrthosiphon pisum Harris (Homoptera: Aphididae), fed, developed, and reproduced on yellow lupine, Lupinus luteus L. (Fabaceae: Genisteae). No clear preferences for any variety within L. luteus were found. Acyrthosiphon pisum showed negative values of relative growth rate and no aphid completed development on any variety of narrow‐leaf lupine Lupinus angustifolius L. Aphids did not ingest phloem sap while probing on L. angustifolius and the probes were very short. All varieties of L. angustifolius were rejected by aphids during an early stage of probing in peripheral tissues, that is, epidermis or mesophyll. There were qualitative and quantitative differences in alkaloid and soluble sugar content between the two lupine species. Within species, the relative content of individual compounds differed among the varieties. Lupinus angustifolius contained four quinolizidine alkaloids (13‐hydroxylupanine, dehydrolupanine, lupanine, and angustifoline), while L. luteus contained two (lupanine and sparteine). Lupanine occurred in all varieties of both lupine species. The total content of soluble carbohydrates was similar in L. luteus and L. angustifolius. The following cyclitols were found in both lupine species: myo‐inositol, D‐ononitol, and D‐pinitol. Lupinus angustifolius also contained D‐chiro‐inositol. The study of aphid probing behaviour, development, and reproduction demonstrated that L. luteus is a suitable host plant for A. pisum while L. angustifolius is not. It is likely that the rejection of L. angustifolius by A. pisum was caused by chemical factors detected by aphids at the epidermis and mesophyll level.

Synthesis of piperitone-derived halogenated lactones and their effect on aphid probing, feeding, and settling behavior{{

Five racemic and five enantiomeric pairs of new halolactones with the p-menthane system were obtained in two or three step synthesis from racemic and optically active cis- and trans-piperitols. The key steps of the syntheses were the Claisen-Johnson rearrangement of piperitols to γ,δ-unsaturated esters and haloloctonization of γ,δ-unsaturated esters or acids. The structures of the compounds were confirmed by spectroscopic and crystallographic data. Antifeedant activity of all iodo-, bromo- and chlorolactones and racemic piperitone against Myzus persicae was examinated. The effect of these compounds on probing, feeding, and settling behavior of M. persicae in vivo was studied.

Piperitone-derived saturated lactones: synthesis and aphid behavior-modifying activity.

Two racemic and two enantiomeric pairs of new saturated lactones with the p-menthane system were obtained. The lactones were synthesized from racemic and enantiomerically enriched cis- and trans-piperitols, which were obtained from piperitone. The structures of the compounds were confirmed by spectroscopic data. The antifeedant activity of piperitone to Myzus persicae was studied, and the biological consequences of structural modifications of piperitone, that is, lactonization and chiral center configuration, were examined as well. The behavioral responses of M. persicae to piperitone and piperitone-derived saturated lactones were investigated to reveal the biological background of their deterrent activity. Piperitone appeared rather neutral or weakly deterrent to aphids. The introduction of a lactone moiety into a piperitone molecule dramatically changed its biological activity. All piperitone-derived lactones evoked negative aphid responses. However, the deterrent activity of individual compounds varied in potency, the time of expression, and the duration of the effect, depending on the spatial structure of the lactone. Lactones (1R,3S,6R)-3-isopropyl-6-methyl-9-oxabicyclo[4.3.0]nonan-8-one and trans-3-isopropyl-6-methyl-9-oxabicyclo[4.3.0]nonan-8-one showed the broadest ranges and the highest potencies and durabilities of deterrent activity to M. persicae: they acted immediately after application, caused a cessation of probing before aphids reached phloem elements, and decreased the quality of phloem sap.

Chemo-Enzymatic Synthesis of Optically Active γ- and δ-Decalactones and Their Effect on Aphid Probing, Feeding and Settling Behavior

The enantiomerically enriched γ- and δ-decalactones (4a and 4b) were prepared from corresponding racemic primary-secondary 1,4- and 1,5-diols (1a and 1b), as products of enzymatic oxidation catalyzed by different alcohol dehydrogenases. The results of biotransformations indicated that the oxidation processes catalyzed by alcohol dehydrogenase (HLADH), both isolated from horse liver and recombinant in Escherichia coli, were characterized by the highest degree of conversion with moderate enantioselectivity of the reaction. Useful, environmentally friendly extraction procedure of decalactones (4a and 4b) based on hydrodistillation using a Deryng apparatus was developed. Both racemic lactones (4a and 4b), as well as their enantiomerically enriched isomers, were tested for feeding deterrent activity against Myzus persicae. The effect of these compounds on probing, feeding and settling behavior of M. persicae was studied in vivo. The deterrent activity of decalactones (4a and 4b) against aphids depended on the size of the lactone ring and the enantiomeric purity of the compounds. δ-Decalactone (4b) appeared inactive against M. persicae while γ-decalactone (4a) restrained aphid probing at ingestional phase. Only (–)-(S)-γ-decalactone (4a) had strong and durable (i.e. lasting for at least 24 hours) limiting effect, expressed at phloem level.

Systemic deterrence of aphid probing and feeding by novel β-damascone analogues

Abstractβ-Damascone appeared a weak attractant close to not active to Myzus persicae, but modifications of its structure caused the avoidance of treated leaves by aphids during settling and reluctance to probe in simple choice- and no-choice experiments in previous studies. Here, the electrical penetration graph (EPG) technique, which allows monitoring of aphid probing within plant tissues, was applied to explore the biological background and localisation in plant tissues of the deterrent activities of β-damascone and its analogues. Activity of β-damascone and β-damascone-derived compounds depended on their substituents, which was manifested in the variation in the potency of the behavioural effect and differences in aphid probing phases that were affected. β-Damascone appeared a behaviourally inactive compound. The moderately active β-damascone ester affected aphid activities only during the phloem phase. The highly active deterrents—dihydro-β-damascol, β-damascone acetate, δ-bromo-γ-lactone, and unsaturated γ-lactone—affected pre-phloem and phloem aphid probing activities. The most effective structural modification that evoked the strongest negative response from M. persicae was the transformation of β-damascone into δ-bromo-γ-lactone. The behavioural effect of this transformation was demonstrated in frequent interruption of probing in peripheral tissues, which caused repeated failures in finding sieve elements, and reduction in the ingestion time during the phloem phase in favour of watery salivation. The inhibition of aphid probing at both the pre-phloem and phloem levels reveals the passage of the compounds studied through the plant surface and their distribution within plant tissues in a systemic way, which may reduce the risk of the transmission of non-persistent and persistent viruses.