Quality Of Phloem Sap Research Articles

Aphid Resistance in Pisum Affects the Feeding Behavior of Pea-Adapted and Non-Pea-Adapted Biotypes of Acyrthosiphon pisum Differently.

Simple SummaryResistance of a Pisum fulvum and five Pisum sativum genotypes to Acyrthosiphon pisum pea and alfalfa-adapted biotypes was evaluated by measuring aphid body mass, confirming the variable resistance level of these genotypes. The feeding behavior of the aphids on the Pisum genotypes was then examined by electropenetrography (EPG). The EPG results suggested that the resistance of Pisum genotypes to non-adapted A. pisum resides in mesophyll and phloem tissues while the resistance variation of P. sativum to pea adapted aphids may be influenced by the quality of phloem sap.Resistant genotypes of crops have emerged as an alternative and sustainable solution to pesticide use against pest insects. The resistance depends on the genetic diversity of the host plant and the pest species and can cause an alteration of the insect behavior. The aim of this work was to characterize the resistance level of different Pisum genotypes (one P. fulvum and five P. sativum genotypes) to two biotypes of the aphid Acyrthosiphon pisum, respectively adapted to pea and alfalfa, by measuring the individual aphid weight and analyzing aphid feeding behavior by electropenetrography (EPG). Aphid body mass was influenced by Pisum genotypes reflecting variation in their resistance level. P. fulvum was the most resistant to the A. pisum pea biotype (ArPo28 clone) and showed intermediate resistance to the A. pisum alfalfa biotype (LSR1 clone). The resistance levels of the five P. sativum genotypes to the two aphid biotypes were variable and more pronounced for the alfalfa biotype. EPG data showed that ArPo28 on P. fulvum and LSR1 on all the Pisum genotypes spent shorter time phloem feeding compared to ArPo28 on P. sativum genotypes, indicating that the resistance of Pisum genotypes to non-adapted A. pisum resides in mesophyll and phloem cells. In the meantime, ArPo28 on P. sativum genotypes with a different level of resistance spent a similar length of time phloem feeding, indicating that the quality of phloem sap of the resistance genotypes may not be optimal for the aphid. The study indicated that the resistance of Pisum genotypes to the two A. pisum biotypes involves different genetic factors and mechanisms that affect the aphid differently.

Aphid infestation leads to plant part-specific changes in phloem sap chemistry, which may indicate niche construction.

Phloem sap quality can differ between and within plants, and affect the performance of aphids. In turn, aphid infestation may change the chemical composition and nutritional value of phloem sap. However, the effects of different aphid species on the overall phloem sap composition of distinct parts within plant individuals in relation to aphid performance remain unclear. To test the specificity of plant responses to aphids, we used two chemotypes of Tanacetum vulgare plants and placed the monophagous aphids Macrosiphoniella tanacetaria and Uroleucon tanaceti on different plant parts (stems close to the inflorescence, young and old leaves). Aphid population growth was determined and sugars, organic acids, amino acids and metabolic fingerprints of phloem exudates were analysed. Macrosiphoniella tanacetaria performed best on stems, whereas U.tanaceti performed best on old leaves, indicating differences in niche conformance. Aphid infestation led to distinct changes in the phloem exudate composition of distinct metabolite classes, differing particularly between plant parts but less between chemotypes. In summary, plant responses to aphids are highly specific for the chemotype, plant part, metabolite class and aphid species. These changes may indicate that aphids construct their own niche, optimizing the food quality on the plant parts they prefer.

Water Stress Modulates Soybean Aphid Performance, Feeding Behavior, and Virus Transmission in Soybean.

Little is known about how water stress including drought and flooding modifies the ability of plants to resist simultaneous attack by insect feeding and transmission of insect-vectored pathogen. We analyzed insect population growth, feeding behaviors, virus transmission, and plant amino acid profiles and defense gene expression to characterize mechanisms underlying the interaction between water stress, soybean aphid and aphid-transmitted, Soybean mosaic virus, on soybean plants. Population growth of non-viruliferous aphids was reduced under drought stress and saturation, likely because the aphids spent less time feeding from the sieve element on these plants compared to well-watered plants. Water stress did not impact population growth of viruliferous aphids. However, virus incidence and transmission rate was lowest under drought stress and highest under saturated conditions since viruliferous aphids took the greatest amount time to puncture cells and transmit the virus under saturated conditions and lowest time under drought stress. Petiole exudates from drought-stressed plants had the highest level of total free amino acids including asparagine and valine that are critical for aphid performance. Aphids did not benefit from improved phloem sap quality as indicated by their lower densities on drought-stressed plants. Saturation, on the other hand, resulted in low amino acid content compared to all of the other treatments. Drought and saturation had significant and opposing effects on expression of marker genes involved in abscisic acid (ABA) signaling. Drought alone significantly increased expression of ABA marker genes, which likely led to suppression of salicylic acid (SA)- and jasmonic acid (JA)-related genes. In contrast, ABA marker genes were down-regulated under saturation, while expression of SA- and JA-related genes was up-regulated. We propose that the apparent antagonism between ABA and SA/JA signaling pathways contributed to an increase in aphid densities under drought and their decrease under saturation. Taken together, our findings suggests that plant responses to water stress is complex involving changes in phloem amino acid composition and signaling pathways, which can impact aphid populations and virus transmission.

Phenological synchrony between Scaphoideus titanus (Hemiptera: Cicadellidae) hatchings and grapevine bud break: could this explain the insect's expansion?

Scaphoideus titanus is the invasive vector of the phytoplasma causing the Flavescence dorée in European vineyards. This epidemic is a serious threat to viticulture that has been increasing for more than 60 years in Europe. We studied the effect of synchrony with the plant phenology and the effect of plant-sap quality on the individual fitness. Thus, we conducted laboratory experiments to determine if insect hatchings were synchronized with grapevine bud break. We used two natural populations: one from a cold winter vineyard and one from a mild winter vineyard. In both cases, egg hatching was synchronized with bud break and leaf appearance. The phloem quality of the young and old leaves as a food source was analysed by high-performance liquid chromatography, and the effects on S. titanus growth were evaluated. Phloem composition varied with the grapevine cutting's age but also varied between leaves of different ages from the same plant. The older leaves were less nutritious because they had the highest carbon-to-nitrogen ratio and the lowest content of essential amino acids. Despite diverse phloem qualities, no fitness difference was observed. We found that the synchronization of egg hatchings with bud break is well regulated. However, the nymphs are not affected by the phloem-sap quality, suggesting that S. titanus may accept different food qualities and that egg hatching synchrony could contribute to population expansion in vineyards.

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.

Water Stress and Aphid Feeding Differentially Influence Metabolite Composition in Arabidopsis thaliana (L.)

Little is known about how drought stress influences plant secondary metabolite accumulation and how this affects plant defense against different aphids. We therefore cultivated Arabidopsis thaliana (L.) plants under well-watered, drought, and water-logged conditions. Two aphid species were selected for this study: the generalist Myzus persicae (Sulzer) and the crucifer specialist Brevicoryne brassicae (L.). Metabolite concentrations in the phloem sap, which influence aphid growth, changed particularly under drought stress. Levels of sucrose and several amino acids, such as glutamic acid, proline, isoleucine, and lysine increased, while concentrations of 4-methoxyindol-3-ylmethyl glucosinolate decreased. M. persicae population growth was highest on plants under drought stress conditions. However, B. brassicae did not profit from improved phloem sap quality under drought stress and performed equally in all water treatments. Water stress and aphids generally had an opposite effect on the accumulation of secondary metabolites in the plant rosettes. Drought stress and water-logging led to increased aliphatic glucosinolate and flavonoid levels. Conversely, aphid feeding, especially of M. persicae, reduced levels of flavonoids and glucosinolates in the plants. Correspondingly, transcript levels of aliphatic biosynthetic genes decreased after feeding of both aphid species. Contrary to M. persicae, drought stress did not promote population growth of B. brassicae on these plants. The specialist aphid induced expression of CYP79B2, CYP79B3, and PAD3 with corresponding accumulation of indolyl glucosinolates and camalexin. This was distinct from M. persicae, which did not elicit similarly strong camalexin accumulation, which led to the hypothesis of a specific defense adaptations against the specialist aphid.

Phloem sap intricacy and interplay with aphid feeding

Aphididae feed upon the plant sieve elements (SE), where they ingest sugars, nitrogen compounds and other nutrients. For ingestion, aphid stylets penetrate SE, and because of the high hydrostatic pressure in SE, phloem sap exudes out into the stylets. Severing stylets to sample phloem exudates (i.e. stylectomy) has been used extensively for the study of phloem contents. Alternative sampling techniques are spontaneous exudation upon wounding that only works in a few plant species, and the popular EDTA-facilitated exudation technique. These approaches have allowed fundamental advances on the understanding of phloem sap composition and sieve tube physiology, which are surveyed in this review. A more complete picture of metabolites, ions, proteins and RNAs present in phloem sap is now available, which has provided large evidence for the phloem role as a signalling network in addition to its primary role in partitioning of photo-assimilates. Thus, phloem sap sampling methods can have remarkable applications to analyse plant nutrition, physiology and defence responses. Since aphid behaviour is suspected to be affected by phloem sap quality, attempts to manipulate phloem sap content were recently undertaken based on deregulation in mutant plants of genes controlling amino acid or sugar content of phloem sap. This opens up new strategies to control aphid settlement on a plant host.

Density‐dependent effects on the reproductive fitness of the New Zealand beech scale insect (Ultracoelostoma assimile) across multiple spatial scales

Abstract. 1. Intraspecific competition can be an important factor influencing the individual fitness of organisms. This study reports density‐dependent effects on the fecundity of the beech scale insect (Ultracoelostoma assimile, Hemiptera: Margarodidae) on naturally occurring, canopy‐dominant red beech (Nothofagus fusca, Fagaceae) trees in New Zealand. For the first time an increasing intensity of intraspecific competition at increasing spatial scales within individual host trees is demonstrated.2. Beech scale insect ‘tests’ containing adult female scale insects and eggs were collected from the trunks of 10 red beech trees [17.7–48.5 cm in diameter at breast height (1.4 m), d.b.h.] with varying densities of scale insect infestation. The relationship between individual female fecundity and scale insect density at three spatial scales: local (within 5 cm), lower trunk (below 2 m above ground level), and whole tree, was tested.3. Beech scale insect fecundity was density dependent, with total female egg load decreasing with increasing scale insect density. The strength of the density‐dependent effect increased with increasing spatial scale, suggesting that scale insects are creating a tree‐wide drain on the quality of phloem sap, rather than depleting nutrients from localised, high‐density areas within trees. These results indicate that at high densities, the New Zealand beech scale insect can have a negative effect on the nutritional quality of the phloem of red beech, thus negatively affecting conspecifics elsewhere on individual host trees. The increasing intensity of the effect with increasing spatial scale within individual trees emphasises the importance of measuring density‐dependent effects at the appropriate spatial scale.

Nutritional quality of phloem sap in relation to host plant-alternation in the bird cherry-oat aphid

Host alternation in aphids has been attributed to complementary growth of host plants, or more specifically to seasonal changes in the nitrogen quality of the phloem sap. In this report, seasonal fluctuation of free amino acids in phloem of the winter and summer host plants (Prunus padus, bird cherry and Hordeum vulgare, barley) of Rhopalosiphum padi (the bird cherry-oat aphid) were investigated in the context of aphid growth and behaviour. Phloem was collected from the cut stylets of aphids taken from plants that were grown outdoors. The total concentration of amino acids in P. padus phloem increased between bud break and late flush (spring), decreased in mature leaves (summer), and increased again in early senescent leaves (autumn). In H. vulgare, however, amino acid concentration fluctuated less from seedlings to flowering. Spring aphids from P. padus grew rapidly on this host from bud break to late flush, but died on mature and early senescent leaves. Summer aphids from H. vulgare grew as fast on this host as spring aphids did on flush leaves of P. padus. Sexual females grew more slowly than other generations and nearly as well on mature as on early senescent P. padus leaves. As judged by aphid growth and phloem nitrogen quality, P. padus during spring equals the summer host H. vulgare. However, the lower growth rates of R. padi on mature and senescent leaves of P. padus appear only loosely correlated with phloem amino acid concentrations. Therefore, factors influencing aphid nutrition, or ecology, other than seasonal changes in phloem sap amino acid concentration may explain the existence of host alternation in R. padi.

Feeding rates and carbohydrate metabolism by Bemisia tabaci (Homoptera: Aleyrodidae) on different quality phloem saps

Abstract.The effects of water stress on phloem sap quality of the melon, Cucumis melo, and how this, in turn, has an impact on the sweet potato whitefly, Bemisia tabaci were studied. Melon plants were grown under watering regimes that produced plants with or without water stress. Plants showed strong developmental responses to the treatments; water‐stressed plants were shorter, with fewer, smaller leaves than those without stress. There was, however, no effect of plant water stress on the development period of whiteflies feeding on these plants, or on the weights of male or female adults. Honeydew production was used as an indirect measure to test whether the absence of insect developmental or behavioural effects was due to differential phloem sap ingestion. Feeding rates on the stressed plants were almost half those on unstressed plants, and there was also variation in the daily pattern of honeydew production. Phloem sap and honeydew were analysed to determine why the feeding behaviours differed. Amino acid composition of the phloem sap was similar in both groups of plants, but carbohydrate concentrations were greater in water‐stressed plants, indicating that lower feeding rates may have been due either to the physical or nutritional quality of the phloem sap. The honeydew of insects that were feeding on water‐stressed plants contained a greater concentration of carbohydrate than those on unstressed plants, and was composed of a significantly greater proportion of glucose and the disaccharide, trehalulose. This isomerization of more complex sugars from those in the diet suggests that B. tabaci uses a mechanism of osmoregulation to actively maintain its internal water status. It is concluded that transient conditions of water stress in this host plant do not affect the development of B. tabaci, due to physiological and behavioural changes in response to diets with different nutritional and physical properties. The implications of this finding for the feeding biology of B. tabaci on desert‐grown crops are discussed.

Role of phloem sap quality and exudation characteristics on performance of pea aphid grown on lucerne genotypes

AbstractThe phloem sap of two lucerne (Medicago sativa L.) genotypes inducing differences in pea aphid, Acyrthosiphon pisum Harris (Homoptera: Aphididae) performances (weight, fecundity, survival), was collected by stylectomy (radio frequency microcautery). Sugars and amino acids were assayed. No significant difference in their concentrations could be established between genotypes. It is thus unlikely that a substantial part of the varietal resistance of these lucerne genotypes to pea aphid could be related to the content in sugars or amino acids. The same conclusion was drawn for the sugar/amino acid ratio. The amino acid profiles were globally similar. They nevertheless allowed a discrimination between the two genotypes on a few amino acids (alanine, leucine, isoleucine, arginine, ornithine) only. Moreover, the degree of resistance can be related neither to GABA concentration, nor to that of sulfur amino acids, because these constituants were either absent, or in trace amounts, whatever the lucerne genotype taken into account.Stylectomy parameters revealed some interesting differences in the sap exudation of the two genotypes. Average volume of exudation by stylet and average duration of exudation were respectively 2.8 and 2.3 times higher in the susceptible genotype. These results suggest a reduced flow of phloem sap, after puncturing of the sieve‐tubes by the aphid stylets on the resistant genotype; this could result in a greater difficulty in phloem sap ingestion by aphids settled on the resistant genotype and thus in suboptimal performances.RésumeéLa sève phloémienne de deux génotypes de luzerne, sur lesquels le puceron du pois, Acyrthosiphon pisum Harris, présente des caractéristiques biologiques (poids, fécondité, survie) différentes, est collectée par stylectomie (microcautérisation à l'aide de fréquences radio). Les sucres et les acides aminés sont analysés. Les teneurs globales en sucres et en acides aminés totaux ne diffèrent pas selon l'origine de la sève phloémienne. Il semble donc que ni la concentration en sucres, ni celle en acides aminés totaux ne soient responsables des effets observés d'antibiose de la luzerne à l'égard du puceron du pois. Le rapport sucres/acides aminés ne paraît pas non plus avoir une action déterminante sur les performances aphidiennes puisqu'il est identique dans les sèves phloémiennes des deux génotypes. Si le spectre des acides aminés est globalement similaire dans les deux cas, quelques doutes subsistent quant au rôle de certains acides aminés (alanine, leucine, isoleucine, arginne, ornithine). Mais le degré de résistance ne peut être relié ni aux concentrations en GABA ni à celles en acides aminés soufrés, puisque ces constituants sont soit absents, soit à l'état de traces dans la sève phloémienne de luzerne, quel que soit le génotype considéré.Des différences plus nettes entre les deux génotypes de luzerne étudiés apparaissent, relativement aux volume et durée d'exsudation de la sève: en effet, le volume moyen récolté par stylet est 2.8 fois plus important sur le génotype sensible que sur le génotype ‘résistant’; de même, la durée moyenne de récolte par stylet est 2.3 fois plus élevée sur le génotype sensible que sur le résistant. Ces derniers résultats suggèrent un moindre écoulement de la sève phloémienne après perforation des tubes criblés par les stylets aphidiens chez le génotype résistant, entraînant ainsi une prise alimentaire plus difficile pour les pucerons installés sur ce génotype.

The nutritional quality of phloem sap utilized by natural aphid populations

Abstract. The amino acid content of phloem exudates from leaves and of aphid honeydew were adopted as indices of the nutritional quality of phloem sap for aphids. Four plant species and associated leaf‐dwelling aphids were investigated: the sycamore Acer pseudoplanatus and sycamore aphid Drepanosiphum platanoides; Prunus domestica (victoria plum) and the mealy plum aphid Hyalopterus pruni; and the spindle tree Euonymus europaeus and broad‐bean Vicia faba, both hosts of the black bean aphid Aphis fabae. The concentration of amino acids in the phloem exudates varied with: (a) plant species (greater in the herb Vicia than in the tree species), (b) season (greater in the autumn than summer for Acer and Euonymus), and (c) position (greater in flush leaves than mature leaves of Prunus). For Acer and Prunus and their aphids, the concentration of amino acids in phloem exudates was significantly correlated with the amino acid content of the aphid honeydew. The amino acids in all exudates and honeydew were dominated by non‐essential amino acids (glutamic acid, glutamine, asparagine or serine, varying with season and between plant species). The sole major discrepancy between the amino acid profiles of exudates and honeydew was the production of asparagine‐rich honeydew by aphids feeding on leaves, whose exudates were dominated by glutamic acid; this applied to both H.pruni on mature Prunus leaves and Drepanosiphum platanoides on summer‐leaves of Acer. It is suggested that EDTA‐exudation may be a useful technique to study nutritional correlates of aphid life cycles, e.g. the time of migration between primary and secondary plant hosts.