Skip to main content
Log in

Genetic variation and association mapping of aphid (Macrosiphoniella sanbourni) resistance in chrysanthemum (Chrysanthemum morifolium Ramat.)

  • Published:
Euphytica Aims and scope Submit manuscript

Abstract

Aphid, Macrosiphoniella sanbourni, is a major insect pest that adversely affects ornamental quality and production of chrysanthemum, thus it is critical to develop new cultivars resistant to aphid. However, the genetic mechanism governing aphid resistance is thus far not thoroughly investigated in chrysanthemum. This study aimed to characterize the genetic variation of the aphid resistance in a global collection of 80 chrysanthemum entries, during summer and autumn under greenhouse condition, and to identify the molecular markers for aphid resistance by association mapping. The performances of aphid resistance, quantified by the average damage index of aphid, was significantly correlated (r = 0.93, P < 0.01) between two seasons. The coefficients phenotypic and genetic variation was calculated around 26–27%; and a high magnitude (0.93) of broad-sense heritability, together with a moderate relative genetic advance (~ 68%), was estimated for aphid resistance. By using the MLM model that integrates population structure and kinship matrix as covariates association mapping identified 11 markers related to aphid resistance, with the individually explained phenotypic variation ranging from ~ 11 to ~ 57%. Of the three markers predicted in both seasons, SSR184-1 and E1M5-1were identified as favorable alleles for aphid resistance. Seven cultivars harboring the two favorable alleles were identified as potential donor parents for future improvement of resistance against aphid. These findings add further understanding of the genetic determination of aphid resistance, and the identified favorable alleles and donor parents open a possibility to produce chrysanthemums with enhanced aphid resistance in future.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abbasi Z, Majidi MM, Arzani A, Rajabi A, Mashayekhi P, Bocianowski J (2015) Association of SSR markers and mopho-physiological traits associated with salinity tolerance in sugar beet (Beta vulgaris L.). Euphytica 205:785–797

    Article  CAS  Google Scholar 

  • Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23(19):2633–2635

    Article  CAS  PubMed  Google Scholar 

  • Breseghello F, Sorrells ME (2006) Association analysis as a strategy for improvement of quantitative traits in plants. Crop Sci 46(3):1323–1330

    Article  Google Scholar 

  • Cheng J, He Y, Yang B, Lai Y, Wang Z, Zhang H (2015) Association mapping of seed germination and seedling growth at three condition in indica rice (Oryza sativa L.). Euphytica 206:103–115

    Article  CAS  Google Scholar 

  • Chong X, Zhang F, Wu Y, Yang X, Zhao N, Wang H, Guan Z, Fang W, Chen F (2016) A SNP-Enabled assessment of genetic diversity, evolutionary relationships and the identification of candidate genes in chrysanthemum. Genome Biol Evol 8:3661–3671

    PubMed  PubMed Central  Google Scholar 

  • Davies FT, He C, Chau A, Heinz KM, Cartmill AD (2004) Fertility affects susceptibility of chrysanthemum to cotton aphids: influence on plant growth, photosynthesis, ethylene evolution, and herbivore abundance. J Am Soc Hortic Sci 129(3):344–353

    CAS  Google Scholar 

  • Deng Y, Chen S, Lu A, Chen F, Tang F, Guan Z, Teng N (2010) Production and characterization of the interneneric hybrids between Dendranthema morifolium and Artemisia vulgaris exhibiting enhanced resistance to chrysanthemum aphid (Macrosiphoniella sanbourni). Planta 231(3):693–703

    Article  CAS  PubMed  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCUTRE: a simulation study. Mol Ecol 14(8):2611–2629

    Article  CAS  PubMed  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2(4):618–620

    Article  Google Scholar 

  • He J, Chen F, Chen S, Fang W (2010) Aphid-resistance of chrysanthemum cultivars. Chinese J Ecol 29(7):1382–1386

    Google Scholar 

  • He J, Chen F, Chen S, Lv G, Deng Y, Fang W, Liu Z, Guan Z, He C (2011) Chrysanthemum leaf epidermal surface morphology and antioxidant and defense enzyme activity in response to aphid infestation. J Plant Physiol 168(7):687–693

    Article  CAS  PubMed  Google Scholar 

  • Joukhadar R, El-Bouhssini M, Jighly A, Ogbonnaya F (2013) Genome-wide association mapping for five major pest resistances in wheat. Mol Breeding 32(4):943–960

    Article  CAS  Google Scholar 

  • Jun TH, Mian MAF, Michel AP (2013) Genetic mapping of three quantitative trait loci for soybean aphid resistance in PI 567324. Heredity 111(1):16–22

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kan G, Zhang W, Yang W, Ma D, Zhang D, Hao D, Hu Z, Yu D (2015) Association mapping of soybean seed germination under salt stress. Mol Genet Genomics 290(6):2147–2162

    Article  CAS  PubMed  Google Scholar 

  • Khan MA, Korban SS (2012) Association mapping in forest trees and fruit crops. J Exp Bot 63(11):4045–4060

    Article  CAS  PubMed  Google Scholar 

  • Khan MSK, Saeed M, Iqbal J (2016) Association mapping validates previously identified quantitative trait loci for salt tolerance in rice (Oryza sativa L.). Mol Breed 36:172

    Article  Google Scholar 

  • Klie M, Menz I, Linde M, Debener T (2016) Strigolactone pathway genes and plant architecture: association analysis and QTL detection for horticultural traits in chrysanthemum. Mol Genet Genomics 291(2):957–969

    Article  CAS  PubMed  Google Scholar 

  • Kloth KJ, Thoen MP, Bouwmeester HJ, Jongsma MA, Dicke M (2012) Association mapping of plant resistance to insects. Trends Plant Sci 17(5):311–319

    Article  CAS  PubMed  Google Scholar 

  • Li F, Peng J (2014) Genetic and association mapping study of English grain aphid resistance and tolerance in bread wheat germplasm. J Integr Agric 13(1):40–53

    Article  Google Scholar 

  • Li P, Song A, Gao C, Jiang J, Chen S, Fang W, Zhang F, Chen F (2015) The over-expression of a chrysanthemum WRKY transcription factor enhances aphid resistance. Plant Physiol Biochem 95:26–34

    Article  CAS  PubMed  Google Scholar 

  • Li P, Zhang F, Chen S, Jiang J, Wang H, Su J, Fang W, Guan Z, Chen F (2016) Genetic diversity, population structure and association analysis in cut chrysanthemum (Chrysanthemum morifolium Ramat.). Mol Genet Genomics 291:1117–1125

    Article  CAS  PubMed  Google Scholar 

  • Liang D, Chen M, Qi X, Xu Q, Zhou F, Chen X (2016) QTL mapping by SLAF-seq and expression analysis of candidate genes for aphid resistance in cucumber. Front Plant Sci 7:1000

    PubMed  PubMed Central  Google Scholar 

  • Meihls LN, Handrick V, Glauser G, Barbier H, Kaur H, Haribal MM, Lipka AE, Gershenzon J, Buckler ES, Erb M, Köllner TG, Jander G (2013) Natural variation in maize aphid resistance is associated with 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one glucoside methyltransferase activity. Plant Cell 25(6):2341–2355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palloix A, Ayme V, Moury B (2009) Durability of plant major resistance genes to pathogens depends on the genetic background, experimental evidence and consequences for breeding strategies. New Phytol 183(1):190–199

    Article  CAS  PubMed  Google Scholar 

  • Peng J, Bai Y, Haley S, Lapitan N (2009) Microsatellite-based molecular diversity of bread wheat germplasm and association mapping of wheat resistance to the Russian wheat aphid. Genetica 135(1):95–122

    Article  CAS  PubMed  Google Scholar 

  • Pritchard JK, Falus D (2009) Documentation for STRUCTURE software: version 2.3. The University of Chicago Press, Chicago

    Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Qin J, Shi A, Mou B, Bhattarai G, Yang W, Weng Y, Motes D (2017) Association mapping of aphid resistance in USDA cowpea (Vigna unguiculata L. Walp.) core collection using SNPs. Euphytica 213(2):36

    Article  Google Scholar 

  • Resende RT, Resende MDV, Silva FF, Azevedo CF, Takahashi EK, Silva-Junior OB, Grattapaglia D (2016) Regional heritability mapping and genome-wide association identify loci for complex growth, wood and disease resistance trait in Eucalyptus. New Phytol 213(3):1287–1300

    Article  PubMed  Google Scholar 

  • Su J, Zhang F, Li P, Guan Z, Fang W, Chen F (2016) Genetic variation and association mapping of waterlogging tolerance in chrysanthemum. Planta 244:1241–1252

    Article  CAS  PubMed  Google Scholar 

  • Sun Y, Guan Z, Chen S, Fang W, Chen F (2012) Identification of aphid resistance in eleven species from Dendranthema and Artemisia at seedling stage. Acta Ecol Sin 32(1):319–325

    Article  Google Scholar 

  • Sun Y, Xia X, Jiang J, Chen S, Chen F, Lv G (2016) Salicylic acid-induced changes in physiological parameters and genes of the flavonoid biosynthesis pathway in Artemisia vulgaris and Dendranthema nankingense during aphid feeding. Genet Mol Res 15(1):gmr.15017546

    Google Scholar 

  • Suvija NV, Suresh J (2016) Evaluation of chrysanthemum (Chrysanthemum morifolium Ramat.) genotypes for loose flower, cut flower and pot mums. Int j innov res adv stud (IJIRAS) 3(4):100–104

    Google Scholar 

  • Turner MK, Kolmer JA, Pumphrey MO, Bulli P, Chao S, Anderson JA (2017) Association mapping of leaf rust resistance loci in a spring wheat core collection. Theor Appl Genet 130(2):345–361

    Article  CAS  PubMed  Google Scholar 

  • Wang C, Zhang F, Guan Z, Chen S, Jiang J, Fang W, Chen F (2014) Inheritance and molecular markers for aphid (Macrosiphoniella sanbourni) resistance in chrysanthemum (Chrysanthemum morifolium Ramat.). Sci Hortic 180:220–226

    Article  CAS  Google Scholar 

  • Wang Y, Sheng L, Zhang H, Du X, An C, Xia X, Chen F, Jiang J, Chen S (2017) CmMYB19 over-expression improves aphid tolerance in chrysanthemum by promoting lignin synthesis. Int J Mol Sci 18(3):619

    Article  PubMed Central  Google Scholar 

  • Waugh R, Jannink JL, Muehlbauer GJ, Ramsay L (2009) The emergence of whole genome association scans in barley. Curr Opin Plant Biol 12(2):218–222

    Article  CAS  PubMed  Google Scholar 

  • Wiarda SL, Fehr WR, O’Neal ME (2012) Soybean aphid (Hemiptera: Aphididae) development on soybean with Rag1 alone, Rag2 alone, and both genes combined. J Econ Entomol 105(1):252–258

    Article  CAS  PubMed  Google Scholar 

  • Xia X, Shao Y, Jiang J, Ren L, Chen F, Fang W, Guan Z, Chen S (2014) Gene expression profiles responses to aphid feeding in chrysanthemum (Chrysanthemum morifolium). BMC Genomics 15(1):1050

    Article  PubMed  PubMed Central  Google Scholar 

  • Xiao L, Hu Y, Wang B, Wu T (2013) Genetic mapping of a novel gene for soybean aphid resistance in soybean (Glycine max [L.] Merr.) line P203 from China. Theor Appl Genet 126(9):2279–2287

    Article  CAS  PubMed  Google Scholar 

  • Yu J, Buckler ES (2006) Genetic association mapping and genome organization of maize. Curr Opin Biotechnol 17(2):155–160

    Article  CAS  PubMed  Google Scholar 

  • Yu J, Pressoir G, Briggs WH, Bi IV, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB, Kresovich S, Buckler ES (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208

    Article  CAS  PubMed  Google Scholar 

  • Zhang G, Gu C, Wang D (2013) Mapping and validation of a gene for soybean aphid resistance in PI 567537. Mol Breed 32(1):131–138

    Article  CAS  Google Scholar 

  • Zhao K, Aranzana MJ, Kim S, Lister C, Shindo C, Tang C, Toomajian C, Zheng H, Dean C, Marjoram P, Nordborg M (2007) An Arabidopsis example of association mapping in structured samples. PLoS Genet 3(1):71–82

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (Grant Nos. 31471900 and 31672192). Germplasm Resources Protection (crop) project of Ministry of Agriculture (Grant No. 1120162130135252031).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zhiyong Guan.

Electronic supplementary material

Below is the link to the electronic supplementary material.

10681_2017_2085_MOESM1_ESM.tif

Supplementary material 1 (TIFF 25521 kb). Fig. S1 Planting design of the aphid-induced rows and the investigated accessions

10681_2017_2085_MOESM2_ESM.tif

Supplementary material 2 (TIFF 287 kb). Fig. S2 The structure of the AM set of 80 chrysanthemums based on an admixture model with K = 2. Pop 1 and Pop 2 represent the two sub-populations defined by a Q threshold of 0.8

10681_2017_2085_MOESM3_ESM.tif

Supplementary material 3 (TIFF 653 kb). Fig. S3 The distribution of pair-wise kinship coefficients in the AM set of 80 chrysanthemums

10681_2017_2085_MOESM4_ESM.tif

Supplementary material 4 (TIFF 2219 kb). Fig. S4 Quantile–quantile (Q–Q) probability plot for I* value obtained from the application of MLM model taking population structure and kinship matrix into account. Each dot represents a marker

10681_2017_2085_MOESM5_ESM.tif

Supplementary material 5 (TIFF 51017 kb). Fig. S5 Non-choice test on the aphid resistance of each five resistant and susceptive chrysanthemum cultivars using artificial inoculation method. A, a sample of ten wingless adult aphids (second instar nymphs) placed in a plastic clip cage on the underside of the full leaf; B, different aphid densities of susceptive and resistant genotypes at 7d after inoculation; C, the average aphid damage index (I*) of each five resistant and susceptive chrysanthemum genotypes between the non-choice (artificial inoculation) and choice (simulated field evaluation) tests

Supplementary material 6 (XLSX 15 kb)

Supplementary material 7 (XLSX 10 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fu, X., Su, J., Yu, K. et al. Genetic variation and association mapping of aphid (Macrosiphoniella sanbourni) resistance in chrysanthemum (Chrysanthemum morifolium Ramat.). Euphytica 214, 21 (2018). https://doi.org/10.1007/s10681-017-2085-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10681-017-2085-z

Keywords

Navigation