Effect of low and high-saponin lines of alfalfa on pea aphid

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Abstract

Pea aphid fed on a high-saponin line of alfalfa showed reduction of reproduction and survival, and disturbance in development of its population. This line negatively influenced aphid probing behaviour, particularly prolonging the non-probing period and probing of the peripheral tissues (epidermis and mesophyll) and shortening the period of phloem sap ingestion. The high-saponin line of alfalfa differed from the low-saponin one by the presence of zanhic acid tridesmoside and a higher level of 3-GlcA,28-AraRhaXyl medicagenic acid glycoside. The saponins incorporated into sucrose–agarose gels significantly reduced number of the aphid probes into the gels and extended their duration in comparison to the control gels (without tested compounds). Role of zanhic acid tridesmoside and 3-GlcA,28-AraRhaXyl medicagenic acid glycoside as potential factors for partial resistance of alfalfa towards the pea aphid is discussed.

Introduction

Secondary plant metabolites are involved in plant–herbivorous insect chemical interactions. Many of them including phenolics, hydroxamic acids, indole alkaloids, glucosinolates, cyanogenic glycosides and surface waxes are known as natural resistance factors against various species of aphids (Argandona et al., 1983; Leszczynski et al., 1989; Ciepiela and Chrzanowski, 1999; Leszczynski et al., 2003; Ridsdill-Smith et al., 2004; Urbanska et al., 2004; Wójcicka et al., 2004). They seriously affect aphid behaviour, physiology and metabolism and as a result reduce aphid populations on resistant plants. Quite often a synergistic effect of plant allelochemicals strongly influences herbivorous pests and natural plant resistance is observed (Berenbaum, 1985). Such partial (moderate) resistance is valuable since it controls phytophagous insect populations and does not reduce the plant value as food. Plant allelochemicals usually play an important role in such resistance mechanisms as antixenosis and antibiosis (Lowe, 1981; Beck et al., 1983; Bennett and Wallsgrove, 1994).

Pea aphid, Acyrthosiphon pisum (Harris) is an oligophagous aphid species. It is one of the most important insect pests of Fabaceae including alfalfa (Medicago sativa L.) where it feeds in phloem sieve tubes. Aphids have sucking–piercing mouthparts (stylets) and are able to feed by taking sap directly from the sieve tubes of plants. Behavioural studies of the aphid on the plant surface suggest that host preference is chemically mediated and involves chemoreception, which is likely due to secondary compounds located in the epidermal or mesophyll cells. Pea aphids do not distinguish between hosts and non-hosts at a distance but determine whether the plant is suitable or not after short probes (Caillaud, 1999). Previous studies suggest that aphid feeding causes foliar damage and an increase in coumestrol content within the infested alfalfa plants (Loser, 1968; Kain and Biggs, 1980).

Saponins were also suggested as possible chemicals involved in defence of alfalfa against phytophagous insect pests (Horber, 1972). High saponin content in some cultivars of alfalfa is related to their resistance to the pea aphid and other polyphagous insects (Pedersen et al., 1976). Alfalfa saponins contain soyasapogenins A–F, and such aglycones as medicagenic acid, hederagenin and lucernic acid (Shany et al., 1972). Oleszek et al. (1992) has identified the latter one as a zanhic acid tridesmoside. The naturally occurring zanhic acid glycosides are present in alfalfa tops and in some varieties are the main saponin compounds. The greater polarity of the medicagenic acid (two carboxylic acid groups) results in greater biological activity and antinutritional properties.

Saponins are also reported to be important in varietal resistance of alfalfa to the pea aphid as well and were suggested to be useful in alfalfa resistance breeding programs (Horber et al., 1974). However, no detailed information considering level, composition and structure of these compounds was provided. Since the varietal resistance of alfalfa resistance to the aphid might be also conditioned by other allelochemicals we performed experiments on homogenous lines of the same cultivar of alfalfa that varied only in the level of saponins.

The present paper reports the effect of high and low-saponin lines of alfalfa on pea aphid performance. Moreover, differences in saponins within the studied lines were determined and an influence of some isolated compounds on the pea aphid probing behaviour was estimated.

Section snippets

Plant material

Lines of alfalfa, Radius cv. varied in saponin level (high- and low-saponin lines, with previously determined saponins’ concentration) were used in the experiments. Seeds of the lines were obtained from Plant Breeding and Acclimatization Institute (IHAR) in Radzików/Błonie, near Warsaw (Poland). Seeds of the studied lines were germinated in a climatic chamber, kept at 20–25 °C under a 16 h daylight and 8 h of darkness, and 70% humidity. Plants were grown in a medium nutrient fine structure compost

Pea aphid performance on high and low-saponin lines

Previously selected lines of alfalfa, Radius cv. of high saponin level (2.5% of dry matter) and low-saponin level (below 0.2% of dry matter) were used in the performed experiments.

Pea aphid performance on the high-saponin line was clearly reduced in comparison to the low-saponin lines. Particularly, plants of the high-saponin line prolonged larval development of the pea aphid and shortened its reproduction. Statistically significant differences were found for duration of the aphid

Discussion

Saponins are well known plant allelochemicals that form a chemical barrier for feeding of the phytophagous insects (Oleszek et al., 1992; Wawrzyniak et al., 2003). Resistance mechanisms of legumes plants such as red clover (Trifilium pratense L.), white clover (Trifilium repens L.) and birdsfoot trifoil (Lotus corniculatus L.) to phytophagous insects is related on content of the saponins (Applebaum and Birk, 1979; Sutherland et al., 1982; Potter and Kimmerer, 1989; Nozzolillo et al., 1997;

Acknowledgments

We thank the Institute of Soil Science and Plant Cultivation, Pulawy, Poland, for excellent technical assistance. We wish to express sincere gratitude to Prof. Z. Stzszewski (Plant Breeding and Acclimatization Institute, Radzikow, Poland) for providing us with high and low-saponins lines of Medicago sativa.

References (39)

  • W. Oleszek et al.

    Triterpene saponins and flavonoids in the seeds of Trifolium species

    Phytochemistry

    (2002)
  • M.M. Adel et al.

    Effects of alfalfa saponins on the moth Spodoptera littoralis

    Journal of Chemical Ecology

    (2000)
  • H.J.V. Apablaza et al.

    Effects of three species of grain aphids (Homoptera: Aphididae) reared on wheat, oats or barley and transferred as adult to wheat, oats and barley

    Entomologia Experimentalis et Applicata

    (1967)
  • S.W. Applebaum et al.

    Saponins

  • V.H. Argandona et al.

    Toxicity and feeding deterrency of hydroxamic acids from Graminae in synthetic diets against the greenbug, Schizaphis graminum

    Entomologia Experimentalis et Applicata

    (1983)
  • D.L. Beck et al.

    Biochemical basis of resistance in corn leaf aphid

    Crop Science

    (1983)
  • R.N. Bennett et al.

    Secondary metabolites in plant defence mechanisms

    New Phytologist

    (1994)
  • Berenbaum, M.R., 1985. Synergistic action among allelochemicals in crop plans. Abstracts of the 190Assiciation Natural...
  • L.C. Birch

    The intrinsic rate of natural increase an insect population

    Journal of Animal Ecology

    (1948)
  • A. Bondi et al.

    Forage saponins

  • R. Bournoville et al.

    Evaluation of medics resistance to phea aphid clones of two host-races

  • R. Bournoville et al.

    Host—races of the pea aphid, Acyrthosiphon pisum: biological criteria and feeding behaviour of clones orginating from legumes

  • M.C. Caillaud

    Behavioural correlates of genetic divergence due to host specialization in the pea aphid, Acyrthosiphon pisum

    Entomologia Experimentalis et Applicata

    (1999)
  • A.P. Ciepiela et al.

    Accumulation of phenolic compounds in winter triticale of different resistance to grain aphid Sitobion avenae /F./ (Homoptera: Aphididae)

  • A.J. Herlt et al.

    Two major saponins from seeds of Barringtonia asiatica: putative antifeedants toward Epilachna sp. larvae

    Journal of Natural Products

    (2002)
  • E. Horber

    Alfalfa saponins significant in resistance to insect

  • E. Horber et al.

    Biological activities of saponin components from Dupuits and Lahontan alfalfa

    Entomologia Experimentalis et Applicata

    (1974)
  • I. Ishaaya

    Nutritional and allelochemic insect–plant interactions relating to digestion and food intake: some examples

  • W.M. Kain et al.

    Effect of pea aphid and bluegreen lucerne aphid (Acyrthosiphon spp.) on coumestrol levels in herbage of lucerne (Medicago sativa)

    New Zealand Journal of Agriculture Research

    (1980)
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