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.

Acknowledgements

This work was supported by the National Natural Science Foundation of China (grant Nos. 32341043, 32302534), The ‘JBGS’ Project of Seed Industry Revitalization in Jiangsu Province (grant No. JBGS [2021]018), and the Natural Science Foundation of Jiangsu Province (grant No. BK20230574).

Author contributions

X.Y. and X.C. proposed a general idea for the review. L.Z., C.C., X.L., Y.D., and Z.L. gathered the literature to write the manuscript. X.Y. and L.Z. wrote and revised the manuscript with contributions from F.L., Y.L., and H.S. W.Z. and C.S. drew the figures.

Data availability

Not applicable.

Conflict of interest statement

The authors declare that they have no conflicts of interest.

References

[1] Deutsch CA, Tewksbury JJ, Tigchelaar M. et al. Increase in crop losses to insect pests in a warming climate. Science. 2018; 361: 916-9

[2] Therezan R, Kortbeek R, Vendemiatti E. et al. Introgression of the sesquiterpene biosynthesis from Solanum habrochaites to cultivated tomato offers insights into trichome morphology and arthropod resistance. Planta. 2021; 254:11

[3] Ninkovic V, Glinwood R, Ünlü AG. et al. Effects of methyl salicylate on host plant acceptance and feeding by the aphid Rhopalosiphum padi. Front Plant Sci. 2021; 12:710268

[4] Wang J, Li Y, Wang X. et al. Betulin, synthesized by Ppcyp716a1, is a key endogenous defensive metabolite of peach against aphids. J Agric Food Chem. 2022; 70:12865-77

[5] De Kesel J, Conrath U, Flors V. et al. The induced resistance lexicon: do’s and don’ts. Trends Plant Sci. 2021; 26:685-91

[6] Moose SP, Mumm RH. Molecular plant breeding as the foundation for 21st century crop improvement. Plant Physiol. 2008; 147:969-77

[7] Bhoi TK, Samal I, Majhi PK. et al. Insight into aphid mediated potato virus Y transmission: a molecular to bioinformatics prospective. Front Microbiol. 2022; 13:1001454

[8] Wang T, Wang K, Wang C. et al. Combining quantitative trait locus mapping with multiomics profiling reveals genetic control of corn leaf aphid (Rhopalosiphum maidis) resistance in maize. J Exp Bot. 2023; 74:3749-64

[9] Zhang S, Zhang Z, Bales C. et al. Mapping novel aphid resistance Qtl from wild soybean, glycine Soja 85-32. Theor Appl Genet. 2017; 130:1941-52

[10] Ji H, Cheon KS, Shin Y. et al. Map-based cloning and characterization of a major Qtl gene, Ffr1, which confers resistance to rice bakanae disease. Int J Mol Sci. 2024; 25:6214

[11] Khalil F, Yueyu X, Naiyan X. et al. Genome characterization of sugarcane yellow leaf virus with special reference to Rnai based molecular breeding. Microb Pathog. 2018; 120:187-97

[12] Naqqash MN. Chapter 8 - Insect-pests of potato:importance and management. In: Çalişkan ME, Bakhsh A, Jabran K, eds. Potato Production Worldwide. Academic Press, 2023,133-44

[13] Kim RJ, Lee SB, Pandey G. et al. Functional conservation of an Ap2/erf transcription factor in cuticle formation suggests an important role in the terrestrialization of early land plants. J Exp Bot. 2022; 73:7450-66

[14] Karalija E, Šamec D, Dahija S. et al. Plants strike back: plant volatiles and their role in indirect defence against aphids. Physiol Plant. 2023; 175:e13850

[15] Wang F, Park YL, Gutensohn M. Glandular trichome-derived mono- and sesquiterpenes of tomato have contrasting roles in the interaction with the potato aphid Macrosiphum euphorbiae. J Chem Ecol. 2021; 47:204-14

[16] Gong Q, Wang Y, He L. et al. Molecular basis of methyl-salicylate-mediated plant airborne defence. Nature. 2023; 622:139-48

[17] Wang B, Dong W, Li H. et al. Molecular basis of (E)-B-farnesene-mediated aphid location in the predator Eupeodes corollae. Curr Biol. 2022; 32:951-62.e7

[18] Wang X, Gao Y, Chen Z. et al. (E)-B-farnesene synthase gene affects aphid behavior in transgenic Medicago sativa. Pest Manag Sci. 2019; 75:622-31

[19] Divekar PA, Narayana S, Divekar BA. et al. Plant secondary metabolites as defense tools against herbivores for sustainable crop protection. Int J Mol Sci. 2022; 23:2690

[20] Xiao R, Zhang C, Guo X. et al. Myb transcription factors and its regulation in secondary cell wall formation and lignin biosynthesis during xylem development. Int J Mol Sci. 2021; 22:3560

[21] Liu X, Du C, Yue C. et al. Exogenously applied melatonin alleviates the damage in cucumber plants caused by Aphis goosypii through altering the insect behavior and inducing host plant resistance. Pest Manag Sci. 2023; 79:140-51

[22] Silva-Sanzana C, Zavala D, Moraga F. et al. Oligogalacturonides enhance resistance against aphids through pattern-triggered immunity and activation of salicylic acid signaling. Int J Mol Sci. 2022; 23:9753

[23] Yang S, Xue S, Shan L. et al. The Cstm alters multicellular trichome morphology and enhances resistance against aphid by interacting with Cstip1;1 in cucumber. J Adv Res. 2024; S2090-1232:00151-6

[24] Le Boulch P, Poëssel JL, Roux D. et al. Molecular mechanisms of resistance to Myzus persicae conferred by the peach Rm 2 gene: a multi-omics view. Front Plant Sci. 2022; 13:992544

[25] Guo H, Zhang Y, Tong J. et al. An aphid-secreted salivary protease activates plant defense in phloem. Curr Biol. 2020; 30:4826-36.e7

[26] Kloth KJ, Shah P, Broekgaarden C. et al. Sli1 confers broad-spectrum resistance to phloem-feeding insects. Plant Cell Environ. 2021; 44:2765-76

[27] Boissot N. Nlrs are highly relevant resistance genes for aphid pests. Curr Opin Insect Sci. 2023; 56:101008

[28] Gong Z, Luo Y, Zhang W. et al. A Slmyb75-centred transcriptional cascade regulates trichome formation and sesquiterpene accumulation in tomato. J Exp Bot. 2021; 72:3806-20

[29] Peng HC, Mantelin S, Hicks GR. et al. The conformation of a plasma membrane-localized somatic embryogenesis receptor kinase complex is altered by a potato aphid-derived effector. Plant Physiol. 2016; 171:2211-22

[30] Zhou H, Jian Y, Shao Q. et al. Development of sustainable insecticide candidates for protecting pollinators: insight into the bioactivities, selective mechanism of action and Qsar of natural coumarin derivatives against aphids. J Agric Food Chem. 2023; 71:18359-74

[31] Bakhtiari M, Rasmann S. Variation in below-to aboveground systemic induction of glucosinolates mediates plant fitness consequences under herbivore attack. J Chem Ecol. 2020; 46:317-29

[32] Florencio-Ortiz V, Sellés-Marchart S, Casas JL. Proteome changes in pepper (Capsicum annuum L.) leaves induced by the green peach aphid (Myzus persicae Sulzer). BMC Plant Biol. 2021; 21:12

[33] Li Y, Fan H, Si Y. et al. The phloem lectin Pp2-A1 enhances aphid resistance by affecting aphid behavior and maintaining Ros homeostasis in cucumber plants. Int J Biol Macromol. 2023; 229:432-42

[34] He P, Jia H, Xue H. et al. Expression of modified snowdrop lectin (Galanthus nivalis Agglutinin) protein confers aphids and Plutella xylostella resistance in Arabidopsis and cotton. Genes (Basel). 2022; 13:1169

[35] Li Y, Cui H, Cui X. et al. The altered photosynthetic machinery during compatible virus infection. Curr Opin Virol. 2016; 17:19-24

[36] Shen C, Wei C, Li J. et al. Barley yellow dwarf virus-Gav-derived Vsirnas are involved in the production of wheat leaf yellowing symptoms by targeting chlorophyll synthase. Virol J. 2020; 17:158

[37] Shimura H, Pantaleo V, Ishihara T. et al. A viral satellite Rna induces yellow symptoms on tobacco by targeting a gene involved in chlorophyll biosynthesis using the Rna silencing machinery. PLoS Pathog. 2011; 7:e1002021

[38] Hodge S, Powell G. Do plant viruses facilitate their aphid vectors by inducing symptoms that alter behavior and performance? Environ Entomol. 2008; 37:1573-81

[39] Santos RCD, Penaflor MFGV, Sanches PA. et al. The effects of Gibberella zeae, barley yellow dwarf virus, and co-infection on Rhopalosiphum padi olfactory preference and performance. Phytoparasitica. 2015; 43:1-8

[40] Eigenbrode SD, Ding H, Shiel P. et al. Volatiles from potato plants infected with potato leafroll virus attract and arrest the virus vector, Myzus persicae (Homoptera: Aphididae). Proc Biol Sci. 2002; 269:455-60

[41] Mauck KE. Variation in virus effects on host plant phenotypes and insect vector behavior: what can it teach us about virus evolution? Curr Opin Virol. 2016; 21:114-23

[42] Eigenbrode SD, Bosque-Pérez NA, Davis TS. Insect-borne plant pathogens and their vectors: ecology, evolution, and complex interactions. Annu Rev Entomol. 2018; 63:169-91

[43] Luan JB, Yao DM, Zhang T. et al. Suppression of terpenoid synthesis in plants by a virus promotes its mutualism with vectors. Ecol Lett. 2013; 16:390-8

[44] Raspberry viruses manipulate the behaviour of their insect vectors. Entomol Exp Appl. 2012; 144:56-68

[45] Mauck KE, De Moraes CM, Mescher MC. Deceptive chemical signals induced by a plant virus attract insect vectors to inferior hosts. Proc Natl Acad Sci USA. 2010; 107:3600-5

[46] Groen SC, Jiang S, Murphy AM. et al. Virus infection of plants alters pollinator preference: a payback for susceptible hosts? PLoS Pathog. 2016; 12:e1005790

[47] Milonas PG, Anastasaki E, Psoma A. et al. Plant viruses induce plant volatiles that are detected by aphid parasitoids. Sci Rep. 2023; 13:8721

[48] Casteel CL, Yang C, Nanduri AC. et al. The Nia-pro protein of turnip mosaic virus improves growth and reproduction of the aphid vector, Myzus persicae (green peach aphid). Plant J. 2014; 77:653-63

[49] Bak A, Cheung AL, Yang C. et al. A viral protease relocalizes in the presence of the vector to promote vector performance. Nat Commun. 2017; 8:14493

[50] Wu D, Qi T, Li WX. et al. Viral effector protein manipulates host hormone signaling to attract insect vectors. Cell Res. 2017; 27:402-15

[51] Ziebell H, Murphy AM, Groen SC. et al. Cucumber mosaic virus and its 2b Rna silencing suppressor modify plant-aphid interactions in tobacco. Sci Rep. 2011; 1:187

[52] Zhang X, Yuan YR, Pei Y. et al. Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis argonaute1 cleavage activity to counter plant defense. Genes Dev. 2006; 20:3255-68

[53] Kim JH, Lee BW, Schroeder FC. et al. Identification of indole glucosinolate breakdown products with antifeedant effects on Myzus persicae (green peach aphid). Plant J. 2008; 54:1015-26

[54] Patton MF, Bak A, Sayre JM. et al. A polerovirus, potato leafroll virus,alters plant-vector interactions using three viral proteins. Plant Cell Environ. 2020; 43:387-99

[55] Gadhave KR, Dutta B, Coolong T. et al. A non-persistent aphid-transmitted potyvirus differentially alters the vector and non-vector biology through host plant quality manipulation. Sci Rep. 2019; 9:2503

[56] Kashyap A, Garg P, Tanwar K. et al. Strategies for utilization of crop wild relatives in plant breeding programs. Theor Appl Genet. 2022; 135:4151-67

[57] Deng Y, Jiang J, Chen S. et al. Combination of multiple resistance traits from wild relative species in chrysanthemum via trigeneric hybridization. PLoS One. 2012; 7:e44337

[58] Zhong J, Guo Y, Shi H. et al. Volatiles mediated an eco-friendly aphid control strategy of Chrysanthemum genus. Ind Crop Prod. 2022; 180:114734

[59] Ali J, Sobhy IS, Bruce TJ. Wild potato ancestors as potential sources of resistance to the aphid Myzus persicae. Pest Manag Sci. 2022; 78:3931-8

[60] Katche E, Quezada-Martinez D, Katche EI. et al. Interspecific hybridization for Brassica crop improvement. Crop Breeding Genetics Genomics. 2019; 1:e190007

[61] Zhang L, Huang J, Su S. et al. Feronia receptor kinase-regulated reactive oxygen species mediate self-incompatibility in Brassica rapa. Curr Biol. 2021; 31:3004-16.e4

[62] Huang J, Yang L, Yang L. et al. Stigma receptors control Intraspecies and interspecies barriers in Brassicaceae. Nature. 2023; 614:303-8

[63] Du H, Qin R, Li H. et al. Genome-wide association studies reveal novel loci for herbivore resistance in wild soybean (Glycine soja). Int J Mol Sci. 2022; 23:8016

[64] Tyryshkin LG, Lysenko NS, Kolesova MA. Effective resistance to four fungal foliar diseases in samples of wild Triticum L. species from the Vir (N.I. Vavilov All-Russian Institute of Plant Genetic Resources) collection: view from Vavilov’s concepts of plant immunity. Plants (Basel). 2022; 11:3467

[65] Curtin S, Qi Y, Peres LEP. et al. Pathways to de novo domestication of crop wild relatives. Plant Physiol. 2022; 188:1746-56

[66] Kumar K, Mandal SN, Pradhan B. et al. From evolution to revolution: accelerating crop domestication through genome editing. Plant Cell Physiol. 2022; 63:1607-23

[67] Zsögön A, Cermak T, Voytas D. et al. Genome editing as a tool to achieve the crop ideotype and de novo domestication of wild relatives: case study in tomato. Plant Sci. 2017; 256:120-30

[68] Li T, Yang X, Yu Y. et al. Domestication of wild tomato is accelerated by genome editing. Nat Biotechnol. 2018; 36:1160-3

[69] Zsögön A, Čermák T, Naves ER. et al. De novo domestication of wild tomato using genome editing. Nat Biotechnol. 2018; 36:1211-6

[70] Bose S, Gangopadhyay G, Sikdar SR. Rorippa indica Hspro2 expression in transgenic Brassica juncea induces tolerance against mustard aphid Lipaphis erysimi. Plant Cell Tissue Organ Cult. 2018; 136:431-43

[71] Sarkar P, Jana K, Sikdar SR. Overexpression of biologically safe Rorippa indica defensin enhances aphid tolerance in Brassica juncea. Planta. 2017; 246:1029-44

[72] Bandopadhyay L, Basu D, Sikdar SR. De novo transcriptome assembly and global analysis of differential gene expression of aphid tolerant wild Mustardrorippa indica(L.) Hiern infested by mustard Aphidlipaphis erysimi(L.) Kaltenbach. Funct Integr Genomics. 2024; 24:43

[73] Bandopadhyay L, Basu D, Sikdar SR. Identification of genes involved in wild crucifer Rorippa indica resistance response on mustard aphid Lipaphis erysimi challenge. PLoS One. 2013; 8:e73632

[74] Yu H, Lin T, Meng X. et al. A route to de novo domestication of wild allotetraploid rice. Cell. 2021; 184:1156-70.e14

[75] Züst T, Agrawal AA. Mechanisms and evolution of plant resistance to aphids. Nat Plants. 2016; 2:15206

[76] Messina FJ, Taylor R, Karren ME. Divergent responses of two cereal aphids to previous infestation of their host plant. Entomol Exp Appl. 2002; 103:43-50

[77] Sauge MH, Mus F, Lacroze JP. et al. Genotypic variation in induced resistance and induced susceptibility in the peach-Myzus persicae aphid system. Oikos. 2006; 113:305-13

[78] Wibowo A, Becker C, Marconi G. et al. Hyperosmotic stress memory in Arabidopsis is mediated by distinct epigenetically labile sites in the genome and is restricted in the male germline by DNA glycosylase activity. elife. 2016; 5:5

[79] Annacondia ML, Markovic D, Reig-Valiente JL. et al. Aphid feeding induces the relaxation of epigenetic control and the associated regulation of the defense response in Arabidopsis. New Phytol. 2021; 230:1185-200

[80] Liu J, Feng L, Gu X. et al. An H3k27me 3 demethylase-Hsfa2 regulatory loop orchestrates transgenerational thermomemory in Arabidopsis. Cell Res. 2019; 29:379-90

[81] Zheng X, Chen L, Xia H. et al. Transgenerational epimutations induced by multi-generation drought imposition mediate rice plant’s adaptation to drought condition. Sci Rep. 2017; 7:39843

[82] Ong-Abdullah M, Ordway JM, Jiang N. et al. Loss of karma transposon methylation underlies the mantled somaclonal variant of oil palm. Nature. 2015; 525:533-7

[83] Hannan Parker A, Wilkinson SW, Ton J. Epigenetics: a catalyst of plant immunity against pathogens. New Phytol. 2022; 233:66-83

[84] Singh B, Bhatia D, Narang D. et al. High-resolution genetic mapping of Qtl governing resistance to corn leaf aphid, Rhopalosiphum maidis (Fitch) in barley. Cereal Res Commun. 2023; 51:379-89

[85] An Q, Pan Z, Aini N. et al. Identification of candidate genes for aphid resistance in upland cotton by Qtl mapping and expression analysis. Crop Journal. 2023; 11:1600-4

[86] Sun M, Voorrips RE, Van’t Westende W. et al. Aphid resistance in capsicum maps to a locus containing Lrr-Rlk gene analogues. Theor Appl Genet. 2020; 133:227-37

[87] Liang D, Chen M, Qi X. et al. Qtl mapping by Slaf-Seq and expression analysis of candidate genes for aphid resistance in cucumber. Front Plant Sci. 2016; 7:1000

[88] Liang D, Liu M, Hu Q. et al. Identification of differentially expressed genes related to aphid resistance in cucumber (Cucumis sativus L.). Sci Rep. 2015; 5:9645

[89] Kusi F, Padi FK, Obeng-Ofori D. et al. A novel aphid resistance locus in cowpea identified by combining Ssr and Snp markers. Plant Breed. 2018; 137:203-9

[90] Dehghan A. Genome-wide association studies. Methods Mol Biol. 2018; 1793:37-49

[91] Ollivier R, Glory I, Cloteau R. et al. A major-effect genetic locus, Aprvii, controlling resistance against both adapted and non-adapted aphid biotypes in pea. Theor Appl Genet. 2022; 135:1511-28

[92] Zou C, Wang P, Xu Y. Bulked sample analysis in genetics, genomics and crop improvement. Plant Biotechnol J. 2016; 14:1941-55

[93] Pan L, Lu Z, Yan L. et al. Nlr1 is a strong candidate for the Rm3 dominant green peach aphid (Myzus persicae) resistance trait in peach. J Exp Bot. 2022; 73:1357-69

[94] Talakayala A, Katta S, Garladinne M. Genetic engineering of crops for insect resistance: an overview. J Biosci. 2020; 45:114

[95] Van Damme EJM. 35 years in plant lectin research: a journey from basic science to applications in agriculture and medicine. Glycoconj J. 2022; 39:83-97

[96] Vanti GL, Katageri IS, Inamdar SR. et al. Potent insect gut binding lectin from Sclerotium rolfsii impart resistance to sucking and chewing type insects in cotton. J Biotechnol. 2018; 278:20-7

[97] Javaid S, Naz S, Amin I. et al. Computational and biological characterization of fusion proteins of two insecticidal proteins for control of insect pests. Sci Rep. 2018; 8:4837

[98] Rani S, Sharma V, Hada A. et al. Efficient genetic transformation of Brassica juncea with lectin using cotyledons explants. Int J Adv Biotechnol Res. 2017; 7:1-12

[99] Rani S, Sharma V, Hada A. et al. Fusion gene construct preparation with lectin and protease inhibitor genes against aphids and efficient genetic transformation of Brassica juncea using cotyledons explants. Acta Physiol Plant. 2017; 39:115

[100] Li M, Guo S, Zhang J. et al. Sugar transporter Vst1 knockout reduced aphid damage in watermelon. Plant Cell Rep. 2022; 41:277-9