Aphids are important herbivores and important pest of many field and forest crops. They have specialized long and flexible stylets which are adapted to feeding on phloem sap. To establish successful feeding on host plant, they need to counter a range of both physical and chemical defenses. The defenses employed by plants can have direct effect on the aphid species through difficulty in establishing successful feeding due to the presence of trichomes, thick cell wall, etc. or effect on their biology with lethal consequences in extreme cases (direct defenses). In contrast to this, plants can attract natural enemies of aphids through the release of volatile compounds (the so-called “cry or call for help”) (indirect defense). The information on different defense strategies employed by plants can be utilized to enhance the level of resistance (R) to develop sustainable pest management strategies.
- insect-plant interactions
- phloem feeding
- plant defense
- sieve elements
Aphids constitute a major group of crop pests that limit productivity of many crops and cause serious damage to plants both by direct feeding and indirectly as vectors of many diseases. Despite being a relatively small insect group (about 5000 known species) compared to 10,000 species of grasshoppers, 12,000 species of geometrid moths, and 60,000 species of weevils, aphids are a serious problem for agriculture [1, 2, 3]. Of the 5000 known species in family Aphididae, 450 are endemic on crop plants, and 100 have successfully exploited the agricultural environment to the extent that they are of significant economic importance . They are the specialized phloem sap feeders resulting in significant yield losses in many crops. It is their ability to rapidly exploit the ephemeral habitats that makes them serious pests, and this ability results from (i) their high reproductive potential, (ii) their dispersal capacities, and (iii) their adaptability to local survival . Unlike majority of insects, aphids exhibit parthenogenetic viviparity—phenomenon that limits the need for males to fertilize females and eliminates egg stage from their life cycle. Thus, aphids reproduce clonally and give birth to young ones, and embryonic development of an aphid begins before its mother’s birth leading to telescoping of generations. All these traits allow aphids to exploit the periods of rapid plant growth, conserve energy, and allow for short generation times; nymphs of certain aphid species can reach maturity in as little as 5 days .
The well-known parthenogenesis exhibited by aphids sets them apart from other Hemiptera and has a great influence on their biology. In addition to parthenogenesis, many species of aphids also exhibit alternation of generations. The system of alternating one bisexual generation with a succession of parthenogenetic, all-female generation evolved as far back as the Triassic  which was later coupled with evolution of viviparity. All these led to reduction in their development period allowing them to multiply at a faster rate. Further, to conserve energy and to invest it in maximizing their reproduction and survival, aphid colonies exhibit wing dimorphism to produce highly fecund wingless morphs or less prolific winged progeny that can disperse to new host plant.
2. Aphid biology and behavior
Aphids are specialized phloem sap feeders and chemists
3. Aphid mouthparts
The beak-like modification of mouthparts (labium, labrum, maxillae, and mandibles) is a distinct character of members of order Hemiptera. Generally the labium (and rarely labrum) is modified into rostrum, into the groove of which needlelike mandibular and maxillary stylets rest when not in use . These needlelike mouthparts enable insects to penetrate the plant tissue and feed on the plant sap. Mandibles constitute the outer stylets and are important in physical penetration of cell walls, while maxillae form the inner ones  and form major role in selection of host plant . Since the stylets can penetrate the individual cells due to their microstructure, this enables the aphids to puncture the symplast without wounding. This behavior is important for phloem-feeding insects which helps them to inoculate viruses into vascular and nonvascular plant cells. Recently, Uzest et al.  reported the existence of distinct anatomical structure called “acrostyle” on the tips of maxillary stylets of aphids which is an expanded part of cuticle visible in the common duct of all aphid species.
The presence of four- or five-segmented rostrum (labium) is the characteristic of the family Aphididae , and five-segmented labium does not occur in the other groups of Hemiptera. The four-segmented labium has been confirmed in members of Aphidinae, e.g.,
4. Compatible aphid-plant interactions
Aphids are specialized phloem sap feeders which insert their needle like stylets in the plant tissue avoiding/counteracting the different plant defenses and withdrawing large quantities of phloem sap while keeping the phloem cells alive. In contrast to the insects with biting and chewing mouthparts which tear the host tissues, aphids penetrate their stylets between epidermal and parenchymal cells to finally reach sieve tubes with slight physical damage to the plants, which is hardly perceived by the host plant . The long and flexible stylets mainly move intercellular in the cell wall apoplasm , although stylets also make intracellular punctures to probe the internal chemistry of a cell. The high pressure within sieve tubes helps in passive feeding . During the stylet penetration and feeding, aphids produce two types of saliva. The first type is dense and proteinaceous (including phenol oxidases, peroxidases, pectinases, β-glucosidases) that forms an intercellular-tunneled path around the stylet in the form of sheath . In addition to proteins, this gelling saliva also contains phospholipids and conjugated carbohydrates [20, 21, 22]. This stylet sheath forms a physical barrier and protects the feeding site from plant’s immune response. When the stylet comes in contact with active flow of phloem sap, the feeding aphid releases digestive enzymes in the vascular tissue in the form of second type of “watery” saliva. The injection of watery saliva (E1) prevents the coagulation of proteins in plant sieve tubes, and during feeding the watery (E2) saliva gets mixed with the ingested sap which prevents clogging of proteins inside the capillary food canal in the insect stylets . Though the actual biochemical mode of action of inhibition of protein coagulation is unknown, the calcium-binding proteins of aphid saliva are reported to interact with the calcium of plant tissues resulting in suppression of calcium-dependent occlusion of sieve tubes and subsequent delayed plant response [23, 24]. This mechanism of feeding is more specialized and precise which avoids different allelochemicals and indigestible compounds abundant in other plant tissues . In addition to this, aphid saliva also contains nonenzymatic-reducing compounds which in the presence of oxidizing enzymes inactivate different defense-related compounds produced by plants after insect attack .
The early response of plants to feeding by insects or infection by pathogens shares some common events such as protein phosphorylation, membrane depolarization, calcium influx, and release of reactive oxygen species (ROS, such as hydrogen peroxide) , which leads to the activation of phytohormone-dependent pathways. In response to infestation/infection, different phytohormone-dependent pathways are activated. The ethylene (ET) and jasmonate (JA) pathways are activated by different necrotrophic pathogens  and grazing insects , while salicylate (SA)-dependent responses are activated by biotrophic pathogens . These responses lead to the production of various defense-related proteins and secondary metabolites with antixenotic or antibiotic properties. In the case of infestation by aphids, a SA-dependent response appears to be activated, while the expression of JA-dependent genes is repressed [29, 30, 31, 32]. All these responses lead to the manipulation of the plant metabolism to ensure compatible aphid-plant interactions.
5. Aphid endosymbionts
The plant phloem sap is a highly unbalanced diet composed principally of sugars and amino acids with high C:N content. To cope with excess of sugars in their diet, aphids have evolved modification in their intestinal tract and filter out excess of sugars and water in the form of honeydew . The most of amino acids are present at very low concentrations. Despite their nutritionally poor diet, aphids exhibit high growth and reproduction rates. Since aphids directly feed on the sugars and amino acids, they need not spend extra energy to digest complex nutrients such as proteins which remarkably increases their assimilation efficiency. In addition to this, the essential amino acids required by their growth and development are synthesized by symbiotic bacteria present in their body. Generally two types of symbiotic bacteria are known to be present in aphids: the primary (obligate) symbionts and secondary (facultative) symbionts.
6. Response of aphids to plant characters
The decision for suitability of the plant as a host is made in the very first phase of the host selection.
In addition to trichomes, plants possess other constitutive defenses such as thorns and thick cell walls that provide direct resistance to plants against aphid feeding. Though these mechanical barriers are constitutive defenses, they can also be produced in response to aphid feeding (directly induced defenses).
In addition to these structural defenses, constitutive defenses can also be chemical. For example, glandular trichomes of
The depth of the sieve elements is an important factor determining successful feeding. The length of the aphid stylets must be compatible with the depth of sieve elements. In addition, thickness at the tip of stylets is also crucial for successful feeding . The movement of stylets through plant tissue is mostly intercellular, and aphids probe all the cells that they encounter during probing. Sensorial structures located at the back of the mouth characterize the plant sap, and aphids recognize the substrate as host or nonhost. On nonhost plants, aphids retract the stylets and leaves in search of suitable host unless the plant produces toxins . Many plant species possess toxic compounds that can be either constitutive or induced that have detrimental effect on insects. The well-known examples include plants in the family Brassicaceae and Solanaceae.
Brassica plants possess a well-studied class of sulfur-containing secondary metabolites—glucosinolates—that defend them from insects. However, during the course of evolution, some (though only a few) insects have been specialized to feed even on these plants. The examples include the turnip aphid,
Similarly, members of family Solanaceae, e.g., potato and tomato, possess glycosidic alkaloids (tomatine, solanine) that defend them from not only insect pests but bacteria and fungi as well. However, some of the species have evolved to overcome this defense, for example,
The resistance gene present in resistant plant provides protection against avirulent strains of insects. To date, one R gene (
The defense-signaling mechanism in plants after aphid attack is similar to incompatible responses in plant-pathogen interactions. Aphid feeding triggers SA-dependent response similar to that triggered by biotrophic pathogens and/or
7. Response of host plants to aphid infestation
Plants respond in a variety of ways to attack by aphid herbivores. Simple feeding by aphids leads to withdrawal of large quantities of plant sap leading to local chlorosis, weakening of the plant, and increase in susceptibility to other insects or pathogens. The well-known examples include infestation of Brassica plants by
Unlike other herbivores that only cause direct feeding damage, aphids also cause indirect damage to plants. The honeydew drops deposited on the leaves act as magnifying lenses that may burn the leaf tissue beneath on sunny days. In addition, black sooty mold develops on the honeydew that interferes with normal photosynthetic activity and blocks the stomata which interferes with gas exchange leading to leaf fall. Some of the aphid species also act as vectors of phytopathogenic viruses, and the association is of advantage to both the aphid vector and the phytopathogenic virus. Aphids serve as an important mean of dispersion, and some species of viruses (replicative) even use aphids as favorable host for replication. Once inside the aphid body, both replicative and circulative viruses make aphids infective for the rest of its life. When aphid density increases on a virus-infected plant due to it being more nutritious than healthy plant, they produce
8. Aphid-plant-natural enemy tritrophic interaction: the “cry or call for help”
In response to aphid feeding, plants release a number of volatile compounds which are perceived by aphid natural enemies. Since plants employ these natural enemies to defend themselves, the release of volatile compounds is analogous to “cry or call for help” by plants. This type of defense is referred to as indirect defense. A number of insects are associated with natural suppression of aphid population which includes predators such as ladybird beetles (e.g.,
The feeding by aphids triggers the release of volatile compounds from infested plants making them more attractive to parasitoids. For example,
9. Potential applications for aphid management
The current understanding of these interactions can help find ways to improve plant resistance to aphids. Since aphids cause serious damage to many agricultural crops, there is a need to find sustainable solution for the management as an effective alternative strategy to synthetic insecticides. There are accelerated global research efforts to search for source(s) of aphid resistance especially in crop wild relatives (CWRs) [4, 73, 74, 75]. There is a growing body of literature that suggests that almost all the variations necessary for crop improvement can be found in their CWRs that were lost over the course of domestication [76, 77, 78, 79, 80]. The use of CWRs is continuously increasing over the years for a range of beneficial traits including pest and disease resistance [81, 82, 83]. In a comprehensive survey by Hajjar and Hodgkin  about the use of CWRs in crop improvement for the period 1986–2005, over 80% of the beneficial traits involved pest and disease resistance. The present knowledge of genomics and availability of tools of biotechnology have erased the boundaries of crossing the species from different gene pools, and there has been a significant increase in the number of wild species in gene banks. Despite this, the use of CWRs in their contributions in providing useful genes for improvement of crop plants has been less than expected. In addition to this, the external application of analogues of jasmonic acid and salicylic acid can also be used to further enhance the level of resistance in crop plants .
In recent years, there has been an increase in the knowledge on resistance genes, but only a few
The attractiveness of the crop plants to aphids and subsequently to their parasitoids can also be augmented to increase effectiveness of parasitoids/natural enemies provided aphids do not act as vector of the phytopathogenic virus. This strategy is especially important as it does not exert any ecological pressure on the aphids. Germplasm screening can be targeted for genotypes that are good at defending themselves from aphid attack and simultaneously attractive to aphid natural enemies. For example,
Another area of potential application in aphid control is the development of transgenic plants expressing resistance against aphids. Modern breeding techniques can be of great help in transferring target trait to the cultivated plant compared to traditional breeding methods. The commercial insect-resistant GM crops that express
Another potential area in aphid management is the exploitation of RNAi technology, which is posttranslational RNA-mediated gene silencing. Plants can be genetically engineered to produce dsRNA to provide protection against a target pest. Transgenic maize plants that produce dsRNA significantly reduced feeding damage by Western corn rootworm,
All the organisms synthesize small 12–50 amino acid long peptides which have antibiotic activity and are termed antimicrobial peptides. They are generally synthesized ribosomally but are also produced enzymatically in fungi and bacteria. They are known to possess antibiotic activity against both gram-positive and gram-negative bacteria and provide immunity against microbial infection. Many insect species are known to produce AMPs [100, 101]. On the contrary aphids do not produce AMPs  as they have mutual relationship with endosymbiotic bacteria such as
Production of volatile compounds by plants is another area that can be explored. Aphids respond to plant volatiles and use them for long-range orientation as recorded in
The aphid-plant coevolution is a continuous arms race that helps to improve defense strategies employed by plants to ward off aphids and counter defense mechanisms employed by aphid herbivores. For a compatible aphid-plant interaction, aphids not only need to alter local and systemic events but also need to modify resource allocation to suit phloem sap to their requirements. Generally, the JA-mediated defenses are employed by plants to control aphids. But aphids through the use of specific effectors are able to modify the JA-mediated defense response of plant and are able to establish successful feeding. Plants, on the other hand, have evolved to use aphid salivary components as elicitors of defense response. The phloem sealing mechanism is one such response observed in resistant plants. In addition, plants have also evolved a plethora of plant secondary metabolites (PSMs) that have defensive functions. But some specialist aphids have learned to use these compounds to their own advantage and use them as cues for feeding and colonization and even sequester them for their advantage.
The current knowledge on aphid-plant interactions is still in its infancy. But the recent studies have provided insights into such interactions which will have far-reaching implications at different levels including development of novel aphid management strategies.
Conflict of interest
The author declares that he has no conflict of interest.