Enhancing aphid resistance in horticultural crops: a breeding prospective

Abstract

Increasing agricultural losses caused by insect infestations are a significant problem, so it is important to generate pest-resistant crop varieties to address this issue. Several reviews have examined aphid-plant interactions from an entomological perspective. However, few have specifically focused on plant resistance mechanisms to aphids and their applications in breeding for aphid resistance. In this review, we first outline the types of resistance to aphids in plants, namely antixenosis, tolerance (cell wall lignification, resistance proteins), and antibiosis, and we discuss strategies based on each of these resistance mechanisms to generate plant varieties with improved resistance. We then outline research on the complex interactions amongst plants, viruses, and aphids, and discuss how aspects of these interactions can be exploited to improve aphid resistance. A deeper understanding of the epigenetic mechanisms related to induced resistance, i.e. the phenomenon where plants become more resistant to a stress they have encountered previously, may allow for its exploitation in breeding for aphid resistance. Wild relatives of crop plants serve as important sources of resistance traits. Genes related to these traits can be introduced into cultivated crop varieties by breeding or genetic modification, and de novo domestication of wild varieties can be used to exploit multiple excellent characteristics, including aphid resistance. Finally, we discuss the use of molecular design breeding, genomic data, and gene editing to generate new aphid-resistant, high-quality crop varieties.

Figure 1

Three defence mechanisms of plants against aphids: antixenosis, tolerance, and antibiosis. Fig. A and B tells the aphid’s antixenosis mechanism, Fig. B tells the aphid’s tolerance mechanism, and Fig. C tells the aphid’s antibiotic mechanism. (A–B) Plants attacks by aphids emit (E)-β-farnesene (EβF), which can be sensed by neurons of adults of aphid predator hoverfly E. corollae. The specific sensing mechanism is that the odourant receptor EcorOR3 in adult worms binds to the odourant-binding protein EcorOBP15 and accurately identifies aphid-infested plants by sensing the odour of EβF. Adults of aphid predator hoverfly E. corollae will fly to the surface of an aphid-infested plant to eat aphids and improve the plant’s ability to avoid aphids [17]. MeSA releases by plants can be sensed by the SABP2 receptor in plants and converts to SA, which triggers the NAC2-SAMT1 mechanism to synthesize more MeSA. When aphids sense MeSA, they will escape the plant [16]. (C) CsTM interacts with the water channel protein CsTIP1;1 to regulate trichome morphology and reduce aphid attractiveness and fitness by modulating hydrogen peroxide. CathB3, an inducible protein in the saliva of peach aphid, is secreted into tobacco and interacts with plant EDR1-like proteins, triggering a burst of ROS in the phloem and inhibiting phloem feeding and colonization by aphid [23]. (D) Overexpression of CsPP2-A1 in cucumber increased the levels of secondary metabolites (PAL, PPO, the phenols, and flavonoids), proline, and the soluble proteins, leading to aphid death. The PpCYP716A1 gene in peach regulates the synthesis of the metabolite betulin, which is directly toxic to green peach aphids [33].

Figure 2

Interaction mechanism between viruses, aphids, and plants. (A) Aphids carrying a single TuMV protein, nuclear inclusion a-protease domain (Nla-Pro) transmit the virus to the plant via stylet when they ingest Arabidopsis or tobacco. Moreover, the TuMV protein Nla-Pro induces the production of ET, which is necessary for TuMV to inhibit the resistance of Arabidopsis to green peach aphids by suppressing callose deposition. When aphids act as vectors for TuMV and PVY transmission and transmit the virus to the host plant, changes in protein localization occur, i.e. when the TuMV protein Nla-Pro locates in the vacuole, it increases the proliferation of the vector aphids on the plant and suppresses callose deposition [49]. (B) When aphids carrying CMV virus feed on plants, the 2b protein of the virus enters the plant, binds to JA inhibitory protein JAZs, inhibits the binding of JAZs to JA signal receptor COI1, inhibits the ubiquitination degradation of JAZs, and thus inhibits JA signalling pathway, making the plant more attractive to aphids and conducive to aphid reproduction compared to aphids settling on plants that are not infected with the virus (dotted line of the change in aphid behaviour). The virus 2b protein can also directly bind to and inhibit AGO1, which positively regulates CYP81f2 expression. CYP81f2 catalyses the synthesis of 4MI3M from the aphid deterrent I3M, which promotes aphid dispersal and facilitates virus transmission compared to aphids settling on plants that are not infected with the virus (dotted line of the change in aphid behaviour) [52, 53]. (C) PLRV-carrying aphids infected plants, weakened the plant’s defence response of JA and ET, and increased the aphids’ ability to reproduce. When aphids carrying PRSV virus infect plants, it increases the accumulation of free amino acids and soluble sugars in the plant, which provide nutrients for the growth and reproduction of aphids; thus it prolongs the feeding time of aphids and enhances the adaptability of aphids to plants. The behaviour of aphids on plants infected with PLRV and PRSV changed as shown in dotted lines, compared to aphids settling on plants that were not infected with the virus [54, 55]. (D) The plant is infected with the above five viruses, including PVY, TuMV, CMV, PLRV, and PRSV. After the aphid sucks the plant, it will move the virus to other plants, which will become infected with these five viruses and develop the symptom of yellow and wilt [36–38]. TuMV: turnip mosaic virus; PVY: potato virus Y; CMV: cucumber mosaic virus; PLRV: potato leafroll virus, PRSV: papaya ringspot virus.

Figure 3

Process of de novo domestication of horticultural crops. Wild resources contain resistance genes to aphids. The figure shows the process of domesticating wild resources into conventional cultivars. (1) Select appropriate wild resource materials. (2) Gene annotation. Because most wild resource materials are very different from conventional cultivated species, their genomic information is unknown. Therefore, it is necessary to re-annotate the genomes of wild resources before domestication. (3) Editing of genes related to domestication. An effective editing system for wild resources was established to edit the genes of unfavourable traits in some wild resources. (4) Integrate favourable traits of the successfully edited lines and eventually use them in field breeding. (5) Assessment of plants planted in the field, including growth potential, aphid resistance, and yield-related traits. The solid line in the figure represents a protein-coding gene identified from the wild crucifer R. indica, which has been confirmed to have anti-aphid effects when introduced into B. juncea. In contrast, the dotted line indicates candidate genes with potential anti-aphid properties identified from a de novo transcriptome analysis. These candidate genes include RiD (R. indica defensin)[71], RiHSPRO2 (R. indica glutathione S-transferase) [70], glutaredoxin [73], EDM2 (Enhanced Downy Mildew 2) [73], and TCP4 (TCP family transcription factor 4) [73].