**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, 73–75]. 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 [76–80]. The use of CWRs is continuously increasing over the years for a range of beneficial traits including pest and disease resistance [81–83]. In a comprehensive survey by Hajjar and Hodgkin [83] 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 [84].

In recent years, there has been an increase in the knowledge on resistance genes, but only a few *R* genes that confer resistance against hemipteran insects have been identified. Some of them include *Vat* that confers resistance to *Aphis gossypii* in melon [85], *Bph 14* and *Bph 26* genes in rice that confer resistance to *Nilaparvata lugens*, and *Mi-12*. gene in tomato that confers resistance to *Macrosiphum euphorbiae* [32]. The *Vat* gene in melon enhances SE wound healing and thus confers resistance to *A. gossypii* [86]*.* The cloning of *Mi-1.2* gene has been a milestone in plant resistance to aphids [54, 55, 86–88], and it has distinct resistance mechanisms against different pests. Against root-knot nematode, *M. incognita*, plants exhibit hypersensitive response, and this response is not manifested upon aphid infestation. The resistance to aphids is antibiotic and phloem based, while it is antixenotic to psyllids. On the other hand, *Mi-1.2-*mediated resistance to whiteflies deters insect settling. However, if the insect establishes a feeding site, it can develop even on the *Mi-1.2* plants. The resistant plants exhibit distinct mechanism of resistance against members of four different animal taxa; however, the biochemical basis of such resistance is not yet known.

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, *Eruca sativa* genotypes are particularly attractive to coccinellid beetles in *Brassica* systems compared to *B. juncea*, *B. napus*, *B. carinata*, or *B. rapa*.

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 *Bt* toxins are particularly effective against Lepidoptera and Coleoptera [89] with no efficacy against phloem feeders including aphids [90]. This accelerated the work on finding alternate strategies such as protease inhibitors, RNAi, antimicrobial peptides (AMPs), etc. Protease inhibitors which may be small peptides or protein molecules inhibit the activity of proteases, thus disrupting the normal protein digestion and consequent amino acid assimilation vital for insect growth. These are already present in plant storage organs and are induced upon insect feeding. Significantly high activity of PI was reported in barley infested with *Schizaphis graminum* with minor effect on its survival, while survival of *Rhopalosiphum padi* was significantly affected [91]. Oryzacystatin-I in transgenic rapeseed [92] and egg plants [93] and cysteine in *Arabidopsis thaliana* [94] from barley are known to provide protection against aphid infestation with their effect on aphid survival, growth, and reproduction. Thus, the use of PIs in aphid management has a good promise as an alternate control strategy [92–94].

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, *Diabrotica virgifera* larvae [95]. In the case of aphids, different workers have achieved RNAi-mediated gene silencing either by injecting the siRNA (short-interfering RNA) [96, 97] or dsRNA into insect hemolymph or

**167**

*Aphid-Plant Interactions: Implications for Pest Management*

feeding the insect with dsRNA [98, 99]. A temporary mRNA inhibition of about 30–40% in aphids was observed by single dose of dsRNA [96]. Similarly, 50% reduction in salivary gland protein expression was observed by Mutti et al. [97]. 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 [95] as they have mutual relationship with endosymbiotic bacteria such as *Buchnera aphidicola*, *Hamiltonella*, *Serratia*, *Rickettsia*, and *Regiella* spp. [102] which play an important role of converting nonessential amino acids in phloem sap to essential ones [103]. Thus, aphid bacterial endosymbionts can be a useful target for AMPs. Any adverse effect on aphid endosymbionts can adversely affect aphid fecundity and can prolong development period [104, 105]. So far, there is only one report on the effect of AMP (indolicidin) on aphids, ingestion of which reduces the number of bacteriocytes and number of bacteria in *M. persicae*, which have significant negative effect on aphid survival, development, and fecundity [106]. This suggests that AMPs expressed in GM plants offer a promising approach for aphid control.

Production of volatile compounds by plants is another area that can be explored.

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 coloniza-

Aphids respond to plant volatiles and use them for long-range orientation as recorded in *Aphis fabae*, *A. pisum*, *Brevicoryne brassicae*, and *M. persicae* [107–110]. Many plants synthesize E-ß-farnesene (Eßf), a well-known alarm pheromone of aphids, as aphid repellent such as wild potato species [48]. Choice experiments by these authors indicated that aphids remain at a distance of 1–3 mm from leaf surface. Apart from general avoidance, aphids also responded to Eßf by producing higher proportion of *alate* (migratory) individuals on treated plants under controlled conditions [111] as well in the field [112]. Thus, plants are exposed to reduced number of apterous (feeding) forms and high proportion of *alates* (migratory forms) that have greater tendency to leave the plant [111]. Besides a repellent effect on aphids, Eßf is also known to attract natural enemies of aphids such as ladybirds *Coccinella septempunctata* and *Harmonia axyridis*, parasitoids *Aphidius uzbekistanicus* and *A. ervi*, and syrphid fly *Episyrphus balteatus* [113–117]. Thus, production of transgenic plants expressing Eßf can have dual effect on aphids and

*DOI: http://dx.doi.org/10.5772/intechopen.84302*

can increase the benefits of Eßf production.

tion and even sequester them for their advantage.

**10. Conclusion**

### *Aphid-Plant Interactions: Implications for Pest Management DOI: http://dx.doi.org/10.5772/intechopen.84302*

*Plant Communities and Their Environment*

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 [84]. In recent years, there has been an increase in the knowledge on resistance genes, but only a few *R* genes that confer resistance against hemipteran insects have been identified. Some of them include *Vat* that confers resistance to *Aphis gossypii* in melon [85], *Bph 14* and *Bph 26* genes in rice that confer resistance to *Nilaparvata lugens*, and *Mi-12*. gene in tomato that confers resistance to *Macrosiphum euphorbiae* [32]. The *Vat* gene in melon enhances SE wound healing and thus confers resistance to *A. gossypii* [86]*.* The cloning of *Mi-1.2* gene has been a milestone in plant resistance to aphids [54, 55, 86–88], and it has distinct resistance mechanisms against different pests. Against root-knot nematode, *M. incognita*, plants exhibit hypersensitive response, and this response is not manifested upon aphid infestation. The resistance to aphids is antibiotic and phloem based, while it is antixenotic to psyllids. On the other hand, *Mi-1.2-*mediated resistance to whiteflies deters insect settling. However, if the insect establishes a feeding site, it can develop even on the *Mi-1.2* plants. The resistant plants exhibit distinct mechanism of resistance against members of four different animal

taxa; however, the biochemical basis of such resistance is not yet known.

promise as an alternate control strategy [92–94].

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, *Eruca sativa* genotypes are particularly attractive to coccinellid beetles in *Brassica* systems compared to *B. juncea*, *B. napus*, *B. carinata*, or *B. rapa*. 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 *Bt* toxins are particularly effective against Lepidoptera and Coleoptera [89] with no efficacy against phloem feeders including aphids [90]. This accelerated the work on finding alternate strategies such as protease inhibitors, RNAi, antimicrobial peptides (AMPs), etc. Protease inhibitors which may be small peptides or protein molecules inhibit the activity of proteases, thus disrupting the normal protein digestion and consequent amino acid assimilation vital for insect growth. These are already present in plant storage organs and are induced upon insect feeding. Significantly high activity of PI was reported in barley infested with *Schizaphis graminum* with minor effect on its survival, while survival of *Rhopalosiphum padi* was significantly affected [91]. Oryzacystatin-I in transgenic rapeseed [92] and egg plants [93] and cysteine in *Arabidopsis thaliana* [94] from barley are known to provide protection against aphid infestation with their effect on aphid survival, growth, and reproduction. Thus, the use of PIs in aphid management has a good

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, *Diabrotica virgifera* larvae [95]. In the case of aphids, different workers have achieved RNAi-mediated gene silencing either by injecting the siRNA (short-interfering RNA) [96, 97] or dsRNA into insect hemolymph or

**166**

feeding the insect with dsRNA [98, 99]. A temporary mRNA inhibition of about 30–40% in aphids was observed by single dose of dsRNA [96]. Similarly, 50% reduction in salivary gland protein expression was observed by Mutti et al. [97].

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 [95] as they have mutual relationship with endosymbiotic bacteria such as *Buchnera aphidicola*, *Hamiltonella*, *Serratia*, *Rickettsia*, and *Regiella* spp. [102] which play an important role of converting nonessential amino acids in phloem sap to essential ones [103]. Thus, aphid bacterial endosymbionts can be a useful target for AMPs. Any adverse effect on aphid endosymbionts can adversely affect aphid fecundity and can prolong development period [104, 105]. So far, there is only one report on the effect of AMP (indolicidin) on aphids, ingestion of which reduces the number of bacteriocytes and number of bacteria in *M. persicae*, which have significant negative effect on aphid survival, development, and fecundity [106]. This suggests that AMPs expressed in GM plants offer a promising approach for aphid control.

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 *Aphis fabae*, *A. pisum*, *Brevicoryne brassicae*, and *M. persicae* [107–110]. Many plants synthesize E-ß-farnesene (Eßf), a well-known alarm pheromone of aphids, as aphid repellent such as wild potato species [48]. Choice experiments by these authors indicated that aphids remain at a distance of 1–3 mm from leaf surface. Apart from general avoidance, aphids also responded to Eßf by producing higher proportion of *alate* (migratory) individuals on treated plants under controlled conditions [111] as well in the field [112]. Thus, plants are exposed to reduced number of apterous (feeding) forms and high proportion of *alates* (migratory forms) that have greater tendency to leave the plant [111]. Besides a repellent effect on aphids, Eßf is also known to attract natural enemies of aphids such as ladybirds *Coccinella septempunctata* and *Harmonia axyridis*, parasitoids *Aphidius uzbekistanicus* and *A. ervi*, and syrphid fly *Episyrphus balteatus* [113–117]. Thus, production of transgenic plants expressing Eßf can have dual effect on aphids and can increase the benefits of Eßf production.
