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Retrotransposonable regions of sunflower genome having relevance with resistance to Sclerotinia species: S. sclerotiorum and S. minor

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Abstract

Basal stem rot (BSR), caused by Sclerotinia sclerotiorum and S. minor, is one of the most important fungal diseases of sunflower (Helianthus annuus L.) causing significant yield losses worldwide. Using resistant cultivars is the most effective method to manage BSR in the field. Therefore, identification of resistant genotypes and genomic regions related to the disease resistance is necessary for employment in the field and for development of resistant cultivars. In this study, the reaction of 100 oilseed sunflower lines was investigated against three isolates from each of the S. sclerotiorum and S. minor species in controlled conditions and association analysis of resistance traits was performed using retrotransposon-based DNA markers. The sunflower germplasm exhibited various reactions against the fungal isolates as the mean necrosis percentage in basal stem of the lines ranged from 30.67 to 100. The genotypes H156A/H543R, 110 and 8A×/LC1064C were resistant to the isolates of both species. Population structure analysis subdivided the genotypes into two subpopulations. Association analysis using general and mixed linear models identified 15 and 14 loci, respectively, which were significantly (P ≤ 0.01) associated with resistant traits. Phenotypic variance explained by QTLs (R2) ranged from 1 to 23%. The markers UF1, LTR1064-A13, LTR1061-UBC818 and LTR1064–65 were commonly associated with the traits conferring resistance to more than one fungal isolate. This was the first study on QTL mapping of genomic regions responsible for resistance to S. sclerotiorum and S. minor using retrotransposon-based DNA markers in and provided an evidence for effectiveness of these markers in association analysis of sunflower. The QTLs and the markers associated with the resistance traits can be useful in marker-aided programs to develop sunflower cultivars with effective resistance to BSR caused by the two Sclerotinia species.

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References

  • Amoozadeh M, Darvishzadeh R, Davar R, Abdollahi Mandoulakani B, Haddadi P, Basirnia A (2015) Quantitative trait loci associated with isolate specific and isolate non-specific partial resistance to Sclerotinia sclerotiorum in sunflower. J Agric Sci Technol 17(1):213–226

    Google Scholar 

  • Andersen JR, Zein I, Wenzel G, Krützfeldt B, Eder J, Ouzunova M, Lübberstedt T (2007) High levels of linkage disequilibrium and associations with forage quality at a phenylalanine ammonia-Lyase locus in European maize (Zea mays L.) inbreds. Theor Appl Genet 114(2):307–319

    Article  PubMed  CAS  Google Scholar 

  • Basirnia A, Hatami Maleki H, Darvishzadeh R, Ghavami F (2014) Mixed linear model association mapping for low chloride accumulation rate in oriental-type tobacco (Nicotiana tabacum L.) germplasm. J Plant Interact 9(1):666–672

    Article  CAS  Google Scholar 

  • Basirnia A, Darvishzadeh R, Abdollahi Mandoulakani B (2016) Retrotransposon insertional polymorphism in sunflower (Helianthus annuus L.) lines revealed by IRAP and REMAP markers. Plant Biosyst 150(4):641–652

    Article  Google Scholar 

  • Bernardo R (2008) Molecular markers and selection for complex traits in plants: learning from the last 20 years. Crop Sci 48(5):1649–1664

    Article  Google Scholar 

  • Bert P-F, Jouan I, de Labrouhe TD, Serre F, Nicolas P, Vear F (2002) Comparative genetic analysis of quantitative traits in sunflower (Helianthus annuus L.) 1. QTL involved in resistance to Sclerotinia sclerotiorum and Diaporthe helianthi. Theor Appl Genet 105(6):985–993

    PubMed  CAS  Google Scholar 

  • Bert P-F, Dechamp-Guillaume G, Serre F, Jouan I, de Labrouhe DT, Nicolas P, Vear F (2004) Comparative genetic analysis of quantitative traits in sunflower (Helianthus annuus L.). Theor Appl Genet 109(4):865–874

    Article  PubMed  CAS  Google Scholar 

  • Bolton MD, Thomma BP, Nelson BD (2006) Sclerotinia sclerotiorum (lib.) de Bary: biology and molecular traits of a cosmopolitan pathogen. Mol Plant Pathol 7(1):1–16

    Article  PubMed  CAS  Google Scholar 

  • Breseghello F, Sorrells ME (2006) Association mapping of kernel size and milling quality in wheat (Triticum aestivum L.) cultivars. Genetics 172(2):1165–1177

    Article  PubMed  PubMed Central  Google Scholar 

  • Castaño F, Vear F, de Labrouhe DT (1993) Resistance of sunflower inbred lines to various forms of attack by Sclerotinia sclerotiorum and relations with some morphological characters. Euphytica 68(1–2):85–98

    Article  Google Scholar 

  • Collard B, Jahufer M, Brouwer J, Pang E (2005) An introduction to markers, quantitative trait loci (QTL) mapping and marker-assisted selection for crop improvement: the basic concepts. Euphytica 142(1–2):169–196

    Article  CAS  Google Scholar 

  • Dadras AR, Sabouri H, Nejad GM, Sabouri A, Shoai-Deylami M (2014) Association analysis, genetic diversity and structure analysis of tobacco based on AFLP markers. Mol Biol Rep 41(5):3317–3329

    Article  PubMed  CAS  Google Scholar 

  • Darvishzadeh R (2012) Association of SSR markers with partial resistance to Sclerotinia sclerotiorum isolates in sunflower (Helianthus annuus L.). Aust J. Crop Sci 6(2):276

    CAS  Google Scholar 

  • Darvishzadeh R (2016) Population structure, linkage disequilibrium and association mapping for morphological traits in sunflower (Helianthus annuus L.). Biotechnol Biotechnol Equip 30(2):236–246

    Article  CAS  Google Scholar 

  • Davar R, Darvishzadeh R, Ahmad M, Ghosta Y, Sarrafi A (2011) QTL mapping of partial resistance to basal stem rot in sunflower using recombinant inbred lines. Phytopathol Mediterr 49(3):330–341

    Google Scholar 

  • Ebrahimi R, Rahmanpour S, Ghoosta Y, Ghaffari M (2014) Reaction and survival of four types of sunflowers against Sclerotinia sclerotiorum under controlled conditions. Arch Phytopathol Plant Protect 47(16):2033–2042

    Article  CAS  Google Scholar 

  • Ershad D (1977) Fungi of Iran. Dept. of Botany, Tehran, pp 277

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14(8):2611–2620

    Article  PubMed  CAS  Google Scholar 

  • Flint Garcia SA, Thuillet AC, Yu J, Pressoir G, Romero SM, Mitchell SE, Doebley J, Kresovich S, Goodman MM, Buckler ES (2005) Maize association population: a high resolution platform for quantitative trait locus dissection. Plant J 44(6):1054–1064

    Article  PubMed  CAS  Google Scholar 

  • Fusari CM, Di Rienzo JA, Troglia C, Nishinakamasu V, Moreno MV, Maringolo C, Quiroz F, Álvarez D, Escande A, Hopp E (2012) Association mapping in sunflower for sclerotinia head rot resistance. BMC Plant Biol 12(1):93

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gentzbittel L, Mouzeyar S, Badaoui S, Mestries E, Vear F, De Labrouhe DT, Nicolas P (1998) Cloning of molecular markers for disease resistance in sunflower (Helianthus annuus L.). Theor Appl Genet 96(3–4):519–525

    Article  PubMed  CAS  Google Scholar 

  • Ghavami F, Elias EM, Mamidi S, Ansari O, Sargolzaei M, Adhikari T, Mergoum M, Kianian SF (2011) Mixed model association mapping for fusarium head blight resistance in Tunisian-derived durum wheat populations. G3 1(3):209–218

    Article  PubMed  CAS  Google Scholar 

  • Gilmore B, Myers JR, Kean D (2002) Completion of testing of Phaseolus coccineus plant introduction (PIs) for white mold, Sclerotinia sclerotiorum resistance. Annu Rep Bean Improv Coop 45:64–65

    Google Scholar 

  • Godoy M, Castaño F, Ré J, Rodríguez R (2005) Sclerotinia resistance in sunflower: I. Genotypic variations of hybrids in three environments of Argentina. Euphytica 145(1):147–154

    Article  CAS  Google Scholar 

  • GulyaTM, Rashid KY, Masirevic SM (1997) Sunflower diseases. In: Schneiter AA (ed) Sunflower technology and production. Agronomy Monograph 35. ASA, CSSA, and SSSA, Madison, p 263–379

  • Gupta PK, Rustgi S, Kulwal PL (2005) Linkage disequilibrium and association studies in higher plants: present status and future prospects. Plant Mol Biol 57(4):461–485

    Article  PubMed  CAS  Google Scholar 

  • Hahn V (2002) Genetic variation for resistance to Sclerotinia head rot in sunflower inbred lines. Field Crop Res 77(2):153–159

    Article  Google Scholar 

  • Hall D, Tegström C, Ingvarsson PK (2010) Using association mapping to dissect the genetic basis of complex traits in plants. Brief Funct Genomics 9(2):157–165

    Article  PubMed  CAS  Google Scholar 

  • Hartman G, Gardner M, Hymowitz T, Naidoo G (2000) Evaluation of perennial species for resistance to soybean fungal pathogens that cause Sclerotinia stem rot and sudden death syndrome. Crop Sci 40(2):545–549

    Article  Google Scholar 

  • Hittalmani S, Huang N, Courtois B, Venuprasad R, Shashidhar H, Zhuang J, Zheng K, Liu G, Wang G, Sidhu J (2003) Identification of QTL for growth-and grain yield-related traits in rice across nine locations of Asia. Theor Appl Genet 107(4):679–690

    Article  PubMed  Google Scholar 

  • Jannatdoust M, Darvishzadeh R, Ziaeifard R, Azizi H, Gholinezhad E (2015) Association mapping for grain quality related traits in confectionery sunflower (Helianthus annuus L.) using retro transposon markers under normal and drought stress conditions. Journal of Crop Biotechnology 9(4):15–28

    Google Scholar 

  • Jun T-H, Van K, Kim MY, Lee S-H, Walker DR (2008) Association analysis using SSR markers to find QTL for seed protein content in soybean. Euphytica 162(2):179–191

    Article  CAS  Google Scholar 

  • Kole C, Henry RJ (2010) Genetics, genomics and breeding of crop plants. Science Publishers

  • Liu L, Wang L, Yao J, Zheng Y, Zhao C (2010) Association mapping of six agronomic traits on chromosome 4A of wheat (Triticum aestivum L.). Molecular Plant Breeding 1(5):1–10

  • Mackay I, Powell W (2007) Methods for linkage disequilibrium mapping in crops. Trends Plant Sci 12(2):57–63

    Article  PubMed  CAS  Google Scholar 

  • Mestries E, Gentzbittel L, de Labrouhe DT, Nicolas P, Vear F (1998) Analyses of quantitative trait loci associated with resistance to shape Sclerotinia sclerotiorum in sunflowers (shape Helianthus annuus L.) using molecular markers. Mol Breed 4(3):215–226

    Article  CAS  Google Scholar 

  • Micic Z, Hahn V, Bauer E, Schön C, Knapp S, Tang S, Melchinger A (2004) QTL mapping of Sclerotinia midstalk-rot resistance in sunflower. Theor Appl Genet 109(7):1474–1484

    Article  PubMed  CAS  Google Scholar 

  • Micic Z, Hahn V, Bauer E, Melchinger A, Knapp S, Tang S, Schön C (2005a) Identification and validation of QTL for Sclerotinia midstalk rot resistance in sunflower by selective genotyping. Theor Appl Genet 111(2):233–242

    Article  PubMed  CAS  Google Scholar 

  • Micic Z, Hahn V, Bauer E, Schön C, Melchinger A (2005b) QTL mapping of resistance to Sclerotinia midstalk rot in RIL of sunflower population NDBLOSsel× CM625. Theor Appl Genet 110(8):1490–1498

    Article  PubMed  CAS  Google Scholar 

  • Paniego N, Heinz R, Fernandez P, Talia P, Nishinakamasu V, Hopp HE (2007) Sunflower. In: Oilseeds. Springer, pp 153–177

  • Pereyra VR, Escande AR (1994) Enfermedades del girasol guía para productores del sudeste bonaerense. Balcarce, Argentina: Unidad Integrada Instituto Nacional de Tecnología Agropecuaria-Universidad Nacional de Mar del Plata

  • Porter L, Hoheisel G, Coffman V (2009) Resistance of peas to Sclerotinia sclerotiorum in the Pisum core collection. Plant Pathol 58(1):52–60

    Article  Google Scholar 

  • Pritchard JK, Donnelly P (2001) Case–control studies of association in structured or admixed populations. Theor Popul Biol 60(3):227–237

    Article  PubMed  CAS  Google Scholar 

  • Pritchard JK, Stephens M, Rosenberg NA, Donnelly P (2000) Association mapping in structured populations. Am J Hum Genet 67(1):170–181

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rönicke S, Hahn V, Horn R, Grone I, Brahm L, Schnabl H, Friedt W (2004) Interspecific hybrids of sunflower as a source of Sclerotinia resistance. Plant Breed 123(2):152–157

    Article  Google Scholar 

  • Rönicke S, Hahn V, Vogler A, Friedt W (2005) Quantitative trait loci analysis of resistance to Sclerotinia sclerotiorum in sunflower. Phytopathology 95(7):834–839

    Article  PubMed  CAS  Google Scholar 

  • Ross-Ibarra J, Morrell PL, Gaut BS (2007) Plant domestication, a unique opportunity to identify the genetic basis of adaptation. Proc Natl Acad Sci 104(suppl 1):8641–8648

    Article  PubMed  CAS  Google Scholar 

  • Rostoks N, Ramsay L, MacKenzie K, Cardle L, Bhat PR, Roose ML, Svensson JT, Stein N, Varshney RK, Marshall DF (2006) Recent history of artificial outcrossing facilitates whole-genome association mapping in elite inbred crop varieties. Proc Natl Acad Sci 103(49):18656–18661

    Article  PubMed  CAS  Google Scholar 

  • Roy J, Bandopadhyay R, Rustgi S, Balyan H, Gupta P (2006) Association analysis of agronomically important traits using SSR, SAMPL and AFLP markers in bread wheat. Curr Sci 90(5):683–689

    CAS  Google Scholar 

  • Saeed M, Wangzhen G, Tianzhen Z (2014) Association mapping for salinity tolerance in cotton (Gossypium hirsutum L.) germplasm from US and diverse regions of China. Aust J Crop Sci 8(3):338

    CAS  Google Scholar 

  • Saharan G, Mehta N (2008) Economic importance. Sclerotinia Diseases of Crop Plants: Biology, Ecology and Disease Management: 41–45

  • Sahranavard AF, Darvishzadeh R, Ghadimzadeh M, Azizi H, Aboulghasemi Z (2015) Identification of SSR loci related to some important agro morphological traits in different oily sunflower (Helianthus annuus L.) lines using association mapping. Journal of Crop Biotechnology 4(10):73–87

    Google Scholar 

  • Sedun FS, Brown JF (1989) Comparison of three methods to assess resistance in sunflower to basal stem rot caused by Sclerotinia sclerotiorum and S. minor. Plant Dis 73(1):52–55

    Article  Google Scholar 

  • Sharma P, Meena P, Verma P, Saharan G, Mehta N, Singh D, Kumar A (2016) Sclerotinia sclerotiorum (lib) de Bary causing Sclerotinia rot in oilseed brassicas: a review. Journal of Oilseed Brassica 1(2):1–44

  • Sorkheh K, Malysheva-Otto LV, Wirthensohn MG, Tarkesh-Esfahani S, Martínez-Gómez P (2008) Linkage disequilibrium, genetic association mapping and gene localization in crop plants. Genet Mol Biol 31(4):805–814

    Article  Google Scholar 

  • Talukder ZI, Hulke BS, Qi L, Scheffler BE, Pegadaraju V, McPhee K, Gulya TJ (2014) Candidate gene association mapping of Sclerotinia stalk rot resistance in sunflower (Helianthus annuus L.) uncovers the importance of COI1 homologs. Theor Appl Genet 127(1):193–209

    Article  PubMed  CAS  Google Scholar 

  • Tuberosa R, Salvi S, Sanguineti MC, Landi P, Maccaferri M, Conti S (2002) Mapping QTLs regulating morphophysiological traits and yield: case studies, shortcomings and perspectives in droughtstressed maize. Ann Bot 89(7):941–963

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Valera Rojas E (2014) Physiological, anatomical and molecular characterization of partial resistance against Sclerotinia sclerotiorum in soybean. Dissertation, University of Guelph

  • Van Becelaere G, Miller JF (2004) Combining ability for resistance to Sclerotinia head rot in sunflower. Crop Sci 44:1542–1545

  • Vollmann J, Rajcan I (2009) Oil crop breeding and genetics. In: Oil Crops. Springer, pp 1–30

  • Wang M, Jiang N, Jia T, Leach L, Cockram J, Waugh R, Ramsay L, Thomas B, Luo Z (2012) Genome-wide association mapping of agronomic and morphologic traits in highly structured populations of barley cultivars. Theor Appl Genet 124(2):233–246

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Yu J, Pressoir G, Briggs WH, Bi IV, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38(2):203–208

    Article  PubMed  CAS  Google Scholar 

  • Yue B, Radi S, Vick B, Cai X, Tang S, Knapp S, Gulya T, Miller J, Hu J (2008) Identifying quantitative trait loci for resistance to Sclerotinia head rot in two USDA sunflower germplasms. Phytopathology 98(8):926–931

    Article  PubMed  CAS  Google Scholar 

  • Zhang Q, Wu C, Ren F, Li Y, Zhang C (2012) Association analysis of important agronomical traits of maize inbred lines with SSRs. Aust J Crop Sci 6(6):1131–1138

    Google Scholar 

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Acknowledgements

We would like to thank Faculty of Agriculture and Institute of Biotechnology of Urmia University, and National Elites Foundation, Iran, for financial support and providing the facilities. Also, we would like to acknowledge Institute National de la Recherche Agronomique (INRA), France, for providing the seeds of studied sunflower genotypes.

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Correspondence to Reza Darvishzadeh.

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Najafzadeh, R., Darvishzadeh, R., Musa-Khalifani, K. et al. Retrotransposonable regions of sunflower genome having relevance with resistance to Sclerotinia species: S. sclerotiorum and S. minor. Australasian Plant Pathol. 47, 511–519 (2018). https://doi.org/10.1007/s13313-018-0587-3

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