Effect of Soy Leaf Flavonoids on Pea Aphid Probing Behavior

Flavonoids detected in soybean Glycine max (L.) Merr. (Fabaceae) cause various alterations in the metabolism, behavior, and development of insect herbivores. The pea aphid Acyrthosiphon pisum (Harris) (Hemiptera: Aphididae) poses potential threat to soybeans, but the effect of individual flavonoids on its feeding-associated behavior is relatively unknown. We monitored probing behavior (stylet penetration activities) of A. pisum on its preferred host plant, Pisum sativum L. untreated (control) and treated with 0.1% ethanolic solutions of flavonoids apigenin, daidzein, genistein, and kaempferol. We applied the electrical penetration graph (electropenetrography, EPG) technique, which visualizes the movements of aphid stylets within plant tissues. None of the applied flavonoids affected the propensity to probe the plants by A. pisum. However, apigenin enhanced the duration of probes in non-phloem tissues, which caused an increase in the frequency and duration of stylet mechanics derailment and xylem sap ingestion but limited the ingestion of phloem sap. Daidzein caused a delay in reaching phloem vessels and limited sap ingestion. Kaempferol caused a reduction in the frequency and duration of the phloem phase. Genistein did not affect aphid probing behavior. Our findings provide information for selective breeding programs of resistant plant cultivars to A. pisum.

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Effect of Lupin Cyclitols on Pea Aphid Probing Behaviour

Journal of Plant Protection Research ◽

10.2478/v10045-011-0030-z ◽

2011 ◽

Vol 51 (2) ◽

pp. 171-178 ◽

Cited By ~ 3

Author(s):

Bożena Kordan ◽

Lesław Lahuta ◽

Katarzyna Dancewicz ◽

Wojciech Sądej ◽

Beata Gabryś

Keyword(s):

Host Plant ◽

Acyrthosiphon Pisum ◽

Initial Period ◽

Total Duration ◽

Pea Aphid ◽

Main Stage ◽

Electrical Penetration Graph ◽

Phloem Sap ◽

Probing Behaviour ◽

Plant Treatment

Effect of Lupin Cyclitols on Pea Aphid Probing BehaviourThe cyclitols: D-pinitol, D-chiro-inositol are naturally present in the tissues ofLupinus angustifolius. The effect of these cyclitols on the behaviour of the pea associated clone ofAcyrthosiphon pisumduring various stages of probing was studied. The main stage of probing studied was the stylet penetration in mesphyll and vascular bundle. D-pinitol, D-chiro-inositol and their mixture were exogenously applied to peaPisum sativumexplants and the aphid probing behaviour was evaluated using the Electrical Penetration Graph technique (EPG). Feeding of peas with cyclitols at a concentration of 10 mM, caused a selective accumulation of D-pinitol and D-chiro-inositol in stems, leaf petioles, and leaf blades. In aphid bodies, both cyclitols were traced, respectively, to the host plant treatment. The new cyclitols in pea tissues did not significantly affect the total duration and frequency of aphid activities during probing in peripheral as well as vascular tissues. However, the aphid behaviour on cyclitol-treated plants as compared to their behaviour on the control was slightly altered. Non-probing and probing in mesophyl prevailed among aphid activities during the initial period of stylet penetration. Aphids on D-pinitol+D-chiro-inositol-treated plants reached phloem vessels relatively later than aphids on the control and D-chiro-inositol plants. There were recurrent switches between E1 (salivation) and E2 (sap ingestion) patterns in some aphids during the phloem phase on D-pinitol and D-pinitol+D-chiro-inositol - treated plants. This may reflect difficulties in the uptake of the phloem sap, and point to lupin cyclitols as being responsible, at least in part, for the rejection ofL. angustifoliusas a host plant by the pea clone ofA. pisum.

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Antixenosis in Glycine max (L.) Merr against Acyrthosiphon pisum (Harris)

Scientific Reports ◽

10.1038/s41598-021-94703-6 ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Katarzyna Stec ◽

Bożena Kordan ◽

Iwona Sergiel ◽

Magdalena Biesaga ◽

Joanna Mroczek ◽

...

Keyword(s):

Glycine Max ◽

Acyrthosiphon Pisum ◽

Electronic Monitoring ◽

Pea Aphid ◽

Electrical Penetration Graph ◽

Peripheral Tissues ◽

Soybean Cultivars ◽

Leaf Tissues ◽

Glycine Max L ◽

Soybean Leaves

AbstractTo reveal the antixenosis potential against the pea aphid Acyrthosiphon pisum (Harris) (Hemiptera: Aphididae) we analyzed the pea aphid survival and probing behavior, and the quantitative and qualitative variation of flavonoids in the leaves of selected soybean Glycine max (L.) Merr (Fabaceae) cultivars ‘Aldana’, ‘Annushka’, ‘Augusta’, ‘Madlen’, ‘Mavka’, ‘Simona’, ‘Violetta’, and ‘Viorica’. Aphid survival was drastically impeded on all cultivars. The electronic monitoring of aphid probing using the Electrical Penetration Graph (EPG) technique revealed that on all soybean cultivars, A. pisum readily probed into leaf tissues but the probes were usually terminated before reaching vascular tissues, which demonstrates the activity of antixenosis mechanisms in peripheral tissues epidermis and/or mesophyll in soybean leaves. The potency of antixenosis factors differed among soybean cultivars, which was reflected in differences in aphid survival and frequency and duration of phloem sap ingestion. Seven flavonoids were found: apigenin, daidzein, genistein, glycitein, isorhamnetin, kaempferol, and rutin, which occurred in different amount and proportion in individual cultivars. The content of apigenin and genistein in all soybean cultivars studied probably made them relatively unacceptable to A. pisum. Kaempferol in ‘Aldana’ might be responsible for the observed strong antixenosis resistance of this cultivar to A. pisum. The results of our survey provide the first detailed data that can be used for future studies.

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Antixenosis in Glycine max (L.) Merr against Acyrthosiphon pisum (Harris)

10.21203/rs.3.rs-177193/v1 ◽

2021 ◽

Author(s):

Katarzyna Stec ◽

Bożena Kordan ◽

Iwona Sergiel ◽

Magdalena Biesaga ◽

Joanna Gasik ◽

...

Keyword(s):

Glycine Max ◽

Acyrthosiphon Pisum ◽

Electronic Monitoring ◽

Pea Aphid ◽

Electrical Penetration Graph ◽

Peripheral Tissues ◽

Soybean Cultivars ◽

Leaf Tissues ◽

Glycine Max L ◽

Soybean Leaves

Abstract To reveal the antixenosis potential against the pea aphid Acyrthosiphon pisum (Harris) (Hemiptera: Aphididae) we analyzed the pea aphid survival and probing behavior, and the quantitative and qualitative variation of flavonoids in the leaves of selected soybean Glycine max (L.) Merr (Fabaceae) cultivars ‘Aldana’, ‘Annushka’, ‘Augusta’, ‘Madlen’, ‘Mavka’, ‘Simona’, ‘Violetta’, and ‘Viorica’. Aphid survival was drastically impeded on all cultivars. The electronic monitoring of aphid probing using the Electrical Penetration Graph (EPG) technique revealed that on all soybean cultivars, A. pisum readily probed into leaf tissues but the probes were usually terminated before reaching vascular tissues, which demonstrates the activity of antixenosis mechanisms in peripheral tissues epidermis and/or mesophyll in soybean leaves. The potency of antixenosis factors differed among soybean cultivars, which was reflected in differences in aphid survival and frequency and duration of phloem sap ingestion. Seven flavonoids were found: apigenin, daidzein, genistein, glycitein, isorhamnetin, kaempferol, and rutin, which occurred in different amount and proportion in individual cultivars. The content of apigenin and genistein in all soybean cultivars studied probably made them relatively unacceptable to A. pisum. Kaempferol in ‘Aldana’ might be responsible for the observed strong antixenosis resistance of this cultivar to A. pisum.

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Susceptibility of forage legumes to infestation by the pea aphid Acyrthosiphon pisum (Harris) (Hemiptera: Aphididae)

Crop and Pasture Science ◽

10.1071/cp18065 ◽

2018 ◽

Vol 69 (8) ◽

pp. 775 ◽

Cited By ~ 1

Author(s):

Bożena Kordan ◽

Katarzyna Stec ◽

Paweł Słomiński ◽

Marian J. Giertych ◽

Anna Wróblewska-Kurdyk ◽

...

Keyword(s):

Acyrthosiphon Pisum ◽

Feeding Activity ◽

Pea Aphid ◽

Electrical Penetration Graph ◽

Forage Legumes ◽

Common Vetch ◽

Forage Crops ◽

Phloem Sap ◽

Experimental Time ◽

Crimson Clover

The small-seeded legumes are important forage crops for grazing animals and contribute nitrogen to succeeding crops in crop rotation systems. However, the susceptibility of several of the forage legumes to the specialist pea aphid Acyrthosiphon pisum (Harris) has never been investigated. The present study on aphid probing behaviour using the Electrical Penetration Graph technique revealed that the forage legumes studied were (i) highly acceptable (common vetch Vicia sativa L.), (ii) acceptable (wooly vetch Vicia villosa Roth), (iii) moderately acceptable (fodder galega Galega orientalis Lam., crimson clover Trifolium incarnatum L., Persian clover Trifolium resupinatum L., white clover Trifolium repens L.), (iv) barely acceptable (common bird’s-foot-trefoil Lotus corniculatus L., yellow lucerne Medicago falcata L., alfalfa Medicago sativa L., sand lucerne Medicago × varia Martyn, common bird’s-foot Ornithopus sativus Brot., alsike clover Trifolium hybridum L., red clover Trifolium pratense L., common sainfoin Onobrychis viciifolia Scop.), and (v) unacceptable (white melilot Melilotus albus Medik.) to the pea aphid. On (i) plants, probing occupied 85% of experimental time, all aphids (100%) succeeded in feeding on phloem sap, phloem phase occupied 50% of probing time, sap ingestion periods were long (mean duration: 100.8 ± 28.2 min.) and engaged 97% of the phloem phase. On (ii) plants, probing occupied 73% of exp. time, feeding activity occurred in 66.7% of aphids, phloem phase occupied 30% of probing time, sap ingestion periods were long (mean duration: 115.5 ± 46.7 min) and engaged 80% of the phloem phase. On (iii) plants, probing ranged from 53% of exp. time on T. repens to 70% on T. incarnatum and T. resuspinatum, feeding occurred in 35.3% of aphids on T. resuspinatum up to 54.5% on T. incarnatum, phloem phase occupied 10% of exp. time on G. orientalis, T. incarnatum, and T. resuspinatum and 20% on T. repens, sap ingestion periods were from 9.8 ± 1.8 min. on G. orientalis to 51.9 ± 20.7 min. long on T. resuspinatum and engaged from 30% of phloem phase on G. orientalis to 80% on T. incarnatum. On (iv) plants, probing occupied 25% of exp. time on O. viciifolia up to 38% on O. sativus and T. hybridum, feeding occurred in 6.7% of aphids on T. hybridum to 28% on O. sativus, phloem phase occupied less than 1% of probing time on all plants except O. viciifolia (4%) and O. sativus (5%) and it consisted mainly of salivation. On M. albus (v), probing occupied 22% of experimental time, the probes were short (1.8 ± 0.3 min), and no aphid on M. albus showed feeding on phloem sap. M. albus can be recommended for intercropping, ‘push-pull’ strategies, or as a barrier crop against A. pisum in sustainable agricultural practices.

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Probing behavior of Adelges laricis Vallot (Hemiptera: Adelgidae) on Larix decidua Mill: Description and analysis of EPG waveforms

PLoS ONE ◽

10.1371/journal.pone.0251663 ◽

2021 ◽

Vol 16 (5) ◽

pp. e0251663

Author(s):

Katarzyna Dancewicz ◽

Beata Gabryś ◽

Iwona Morkunas ◽

Sławomir Samardakiewicz

Keyword(s):

Xylem Sap ◽

Sister Group ◽

Larix Decidua ◽

Plant Tissues ◽

Electrical Penetration Graph ◽

European Larch ◽

Voltage Level ◽

Phloem Sap ◽

Probing Behavior ◽

Behavioral Activities

Adelgidae are a sister group of Aphididae and Phylloxeridae within Hemiptera, Aphidoidea and occur exclusively on Pinaceae. The piercing-sucking mouthparts of Adelgidae are similar to those of aphids and it is believed that adelgids ingest sap from both the non-vascular and vascular (phloem) tissues. The aim of the present study was to identify and characterize the adelgid stylet activities during their penetration in plant tissues. The probing behavior of Adelges laricis Vallot (Hemiptera: Adelgidae) on European larch Larix decidua Mill. and sucrose diets was monitored using the DC-EPG (Electrical Penetration Graph technique = electropenetrography). The EPG waveforms were described based on amplitude, frequency, voltage level, and electrical origin of the observed traces, and associated with putative behavioral activities based on analogy with aphid activities. Waveform frequency, duration, and sequence were analysed as well. A. laricis generated EPG signals at two clearly distinct voltage levels positive and negative, suggesting extracellular and intracellular stylet penetration, respectively. The adelgid EPG patterns were ascribed to four behavioral phases, which were non-probing, pathway, phloem, and xylem phases. Non-probing referred to the position of the stylets outside the plant tissues. Pathway phase was represented by three waveform patterns that visualized extracellular stylet penetration in non-vascular tissues without potential drops (AC1), with serial short (1.2–1.5 s) potential drops (AC2), and with ‘aphid-like’ (5–10 s) potential drops (AC3). Phloem phase comprised three waveform patterns at intracellular level, which in all probability represented phloem salivation (AE1), and phloem sap passive (AE2) and active ingestion (AE3). AE3 was a newly described waveform, previously unreported from Hemiptera. Waveform AG represented the ingestion of xylem sap. The comparative analysis demonstrated that the gymnosperm-associated adelgids show certain similarities in probing behavior typical of aphids and phylloxerids on angiosperm plants. The present work is the first detailed analysis of specific adelgid stylet activities on gymnosperms.

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Trehalose and glucose levels regulate feeding behavior of the phloem-feeding insect, the pea aphid Acyrthosiphon pisum Harris

Scientific Reports ◽

10.1038/s41598-021-95390-z ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Guang Wang ◽

Jing-Jiang Zhou ◽

Yan Li ◽

Yuping Gou ◽

Peter Quandahor ◽

...

Keyword(s):

Feeding Behavior ◽

Growth And Development ◽

Acyrthosiphon Pisum ◽

Pea Aphid ◽

Feeding Time ◽

Electrical Penetration Graph ◽

Glucose Content ◽

Glucose Levels ◽

Phloem Feeding ◽

Trehalose Content

AbstractTrehalose serves multifarious roles in growth and development of insects. In this study, we demonstrated that the high trehalose diet increased the glucose content, and high glucose diet increased the glucose content but decreased the trehalose content of Acyrthosiphon pisum. RNA interference (RNAi) of trehalose-6-phosphate synthase gene (ApTPS) decreased while RNAi of trehalase gene (ApTRE) increased the trehalose and glucose contents. In the electrical penetration graph experiment, RNAi of ApTPS increased the percentage of E2 waveform and decreased the percentage of F and G waveforms. The high trehalose and glucose diets increased the percentage of E2 waveform of A. pisum red biotype. The correlation between feeding behavior and sugar contents indicated that the percentage of E1 and E2 waveforms were increased but np, C, F and G waveforms were decreased in low trehalose and glucose contents. The percentage of np, E1 and E2 waveforms were reduced but C, F and G waveforms were elevated in high trehalose and glucose contents. The results suggest that the A. pisum with high trehalose and glucose contents spent less feeding time during non-probing phase and phloem feeding phase, but had an increased feeding time during probing phase, stylet work phase and xylem feeding phase.

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Bacteriocyte Reprogramming to Cope With Nutritional Stress in a Phloem Sap Feeding Hemipteran, the Pea Aphid Acyrthosiphon pisum

Frontiers in Physiology ◽

10.3389/fphys.2018.01498 ◽

2018 ◽

Vol 9 ◽

Cited By ~ 2

Author(s):

Stefano Colella ◽

Nicolas Parisot ◽

Pierre Simonet ◽

Karen Gaget ◽

Gabrielle Duport ◽

...

Keyword(s):

Acyrthosiphon Pisum ◽

Nutritional Stress ◽

Pea Aphid ◽

Phloem Sap ◽

Sap Feeding

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Changes in phytohormone levels following inoculation of two soybean lines differing in nodulation

Functional Plant Biology ◽

10.1071/pp01166 ◽

2002 ◽

Vol 29 (8) ◽

pp. 965 ◽

Cited By ~ 14

Author(s):

Asghari Bano ◽

James E. Harper ◽

Robert M. Auge ◽

Dawn S. Neuman

Keyword(s):

Glycine Max ◽

Xylem Sap ◽

Zeatin Riboside ◽

Phloem Sap ◽

Root Nodulation ◽

Hormone Transport ◽

Glycine Max L ◽

Bradyrhizobium Inoculation

Changes in the concentration of free and conjugated ABA, zeatin riboside (ZR), and IAA in response to Bradyrhizobium inoculation and subsequent nodulation were monitored in xylem sap, phloem sap, and leaves of soybean [Glycine max (L.) Merr. cv. Williams 82] and its hypernodulating mutant, NOD1-3. In this study, pre-inoculation concentrations of phloem and xylem sap ABA and ZR were lower in NOD1-3 than in Williams 82, a difference that was accentuated in phloem after inoculation. The concentration of xylem ABA increased within 6�h of inoculation, while the concentration of phloem and leaf ABA did not change until 48-96 h after inoculation. Leaf uptake of [3H]ABA and distribution to phloem sap was greater in Williams 82 than in NOD1-3 during 48-72�h after inoculation. Inoculation resulted in similar increases in phloem and leaf IAA concentrations in both cultivars. While inoculation increased xylem sap ZR in both lines, the concentration of ZR increased much earlier in NOD1-3. Of particular interest is that ratios between hormones were altered during nodulation. Leaf and phloem ABA/IAA ratios were higher in Williams 82 than in the hypernod mutant, while the phloem IAA/ZR was greater from inoculation until nodulation in the NOD1-3 hypernod mutant. The xylem ABA/ZR ratio, as well as phloem ABA/ZR ratio, decreased in Williams 82 following inoculation, and leaf ABA concentration was elevated. The most noteworthy results of this study, therefore, came from an examination of the ratios between hormones in xylem and phloem sap, and the demonstration that hormone transport may play an important role in autoregulation of root nodulation.

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Acceptance of low-saponin lines of alfalfa with varied phenolic concentrations by pea aphid (Homoptera: Aphididae)

Biologia ◽

10.2478/s11756-009-0051-5 ◽

2009 ◽

Vol 64 (2) ◽

Cited By ~ 19

Author(s):

Sylwia Goławska ◽

Iwona Łukasik

Keyword(s):

Feeding Behaviour ◽

Acyrthosiphon Pisum ◽

Rank Correlation ◽

Pea Aphid ◽

Spearman Rank Correlation ◽

Peripheral Tissues ◽

Phloem Sap ◽

Reproduction Period ◽

Aphid Feeding ◽

Low Levels

AbstractThis research aims to examine the effect of phenolics on pea aphid (Acyrthosiphon pisum) (Homoptera: Aphididae) development and feeding behaviour, on leaves of selected low-saponin lines of Radius alfalfa (Medicago sativa). There was a slight, negative correlation (Spearman rank correlation r s = −0.80) between concentrations of saponins and phenols. Lines with higher concentrations of saponins had less phenolics. Levels of phenolics in low-saponin lines of alfalfa cv. Radius were related to their acceptance by the pea aphid. Our data revealed an inverse relationship between level of phenolics and the aphid abundance and its biology on studied alfalfa lines. Larval development of the pea aphid was longer, reproduction period was shorter, and the fecundity was lower on low-saponin lines with higher level of phenolics. There were observed some tendencies in the pea aphid feeding behaviour on these lines: prolonging the probing of the peripheral tissues (epidermis and mesophyll) and shortening the period of phloem sap ingestion. The better hosts for the pea aphid were low-saponin lines with low levels of phenolic compounds.

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Quercetin and Rutin as Modifiers of Aphid Probing Behavior

Molecules ◽

10.3390/molecules26123622 ◽

2021 ◽

Vol 26 (12) ◽

pp. 3622

Author(s):

Katarzyna Stec ◽

Bożena Kordan ◽

Beata Gabryś

Keyword(s):

Acyrthosiphon Pisum ◽

Plant Protection ◽

Rhopalosiphum Padi ◽

Aphid Species ◽

Plant Tissues ◽

Electrical Penetration Graph ◽

Probing Behavior ◽

Herbivore Interactions ◽

Plant Herbivore ◽

Rutin And Quercetin

Rutin and its aglycone quercetin occur in the fruits, leaves, seeds, and grains of many plant species and are involved in plant herbivore interactions. We studied the effect of the exogenous application of rutin and quercetin on the probing behavior (= stylet penetration activities in plant tissues) of Acyrthosiphon pisum on Pisum sativum, Myzus persicae on Brassica rapa ssp. pekinensis, and Rhopalosiphum padi on Avena sativa using the electrical penetration graph technique (EPG = electropenetrography). The reaction of aphids to quercetin and rutin and the potency of the effect depended on aphid species, the flavonol, and flavonol concentration. Quercetin promoted probing activities of A. pisum within non-phloem and phloem tissues, which was demonstrated in the longer duration of probes and a trend toward longer duration of sap ingestion, respectively. M. persicae reached phloem in a shorter time on quercetin-treated B. rapa than on the control. Rutin caused a delay in reaching sieve elements by A. pisum and deterred probing activities of M. persicae within non-phloem tissues. Probing of R. padi was not affected by quercetin or rutin. The potency of behavioral effects increased as the applied concentrations of flavonols increased. The prospects of using quercetin and rutin in plant protection are discussed.

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