, Volume 207, Issue 2, pp 331–342 | Cite as

Large variation in mycorrhizal colonization among wild accessions, cultivars, and inbreds of sunflower (Helianthus annuus L.)

  • A. Turrini
  • T. Giordani
  • L. Avio
  • L. Natali
  • M. Giovannetti
  • A. CavalliniEmail author


Arbuscular mycorrhizal (AM) fungi (AMF) establish beneficial symbioses with the roots of the majority of land plants, including major food crops. The susceptibility of sunflower (Helianthus annuus) to AMF was studied in 26 genotypes—nine wild accessions, 11 cultivars and six inbred lines—by assessing mycorrhizal root colonization in individual plants, with the aim of gaining insights into the genetic control of this trait. The analysis of genetic diversity among sunflower wild accessions, cultivars, and inbred lines, performed by retrotransposon display (multilocus fingerprinting), showed large variability among the analysed genotypes, with wild accessions more variable than domesticated genotypes. Wild accessions were also more susceptible to mycorrhizal colonization than cultivars. Nevertheless, analyses of inbred lines revealed a low repeatability value of the mycorrhizal colonization trait, suggesting the absence of a clearcut genetic control; variability should therefore mostly reflect environmental effects.


Arbuscular mycorrhizal fungi Helianthus annuus Mycorrhizal susceptibility Sunflower inbreds Wild accessions versus cultivars 



This work was funded by the University of Pisa (Fondi di Ateneo) and by C.N.R.


  1. An GH, Kobayashi S, Enoki H, Sonobe K, Muraki M, Karasawa T, Ezawa T (2010) How does arbuscular mycorrhizal colonization vary with host plant genotype? An example based on maize (Zea mays) germplasms. Plant Soil 327:441–453CrossRefGoogle Scholar
  2. Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42CrossRefGoogle Scholar
  3. Avio L, Pellegrino E, Bonari E, Giovannetti M (2006) Functional diversity of arbuscular mycorrhizal fungal isolates in relation to extraradical mycelia networks. New Phytol 172:347–357CrossRefGoogle Scholar
  4. Avio L, Cristani C, Strani P, Giovannetti M (2009) Genetic and phenotypic diversity of geographically different isolates of Glomus mosseae. Can J Microbiol 55:242–253CrossRefGoogle Scholar
  5. Azcon R, Ocampo JA (1981) Factors affecting the vesicular-arbuscular infection and mycorrhizal dependency of thirteen wheat cultivars. New Phytol 87:677–685CrossRefGoogle Scholar
  6. Bittman S, Kowalenko CG, Hunt DE, Forge TA, Wu X (2006) Starter phosphorus and broadcast nutrients on corn with contrasting colonization by mycorrhizae. Agron J 98:394–401CrossRefGoogle Scholar
  7. Bryla DR, Koide RT (1990) Role of mycorrhizal infection in the growth and reproduction of wild vs. cultivated plants. II. Eight wild accessions and two cultivars of Lycopersicon esculentum Mill. Oecologia 84:82–92CrossRefGoogle Scholar
  8. Buti M, Giordani T, Vukich M, Pugliesi C, Natali L, Cavallini A (2013) Retrotransposon-related genetic distance and hybrid performance in sunflower (Helianthus annuus L.). Euphytica 192:289–303CrossRefGoogle Scholar
  9. Chandrashekara CP, Patil VC, Sreenivasa MN (1995) VA-mycorrhiza mediated P effect on growth and yield of sunflower (Helianthus annuus L.) at different P levels. Plant Soil 176:325–328CrossRefGoogle Scholar
  10. Cheres MT, Knapp SJ (1998) Ancestral origins and genetic diversity of cultivated sunflower: analysis of the pedigrees of public germplasm. Crop Sci 38:1476–1482CrossRefGoogle Scholar
  11. Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280CrossRefGoogle Scholar
  12. Falconer DS (1981) Introduction to quantitative genetics, 2nd edn. Longman, New YorkGoogle Scholar
  13. Gallaud I (1905) Études sur les mycorrhizes endotrophes. Rev Gén Bot 17:5–48, 66–83, 123–136, 223–239, 313–325, 425–433, 479–500Google Scholar
  14. Gianinazzi S, Gollotte A, Binet MN, van Tuinen D, Redecker D, Wipf D (2010) Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20:519–530CrossRefGoogle Scholar
  15. Giovannetti M, Gianinazzi-Pearson V (1994) Biodiversity in arbuscular mycorrhizal fungi. Mycol Res 98:705–715CrossRefGoogle Scholar
  16. Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500CrossRefGoogle Scholar
  17. Graham JH, Abbott LK (2000) Wheat responses to aggressive and non-aggressive arbuscular mycorrhizal fungi. Plant Soil 220:207–218CrossRefGoogle Scholar
  18. Harter AV, Gardner KA, Falush D, Lentz DL, Bye RA, Rieseberg LH (2004) Origin of extant domesticated sunflowers in eastern North America. Nature 430:201–205CrossRefGoogle Scholar
  19. Hetrick BAD, Wilson GWT, Cox TS (1992) Mycorrhizal dependence of modern wheat varieties, landraces, and ancestors. Can J Bot 70:2032–2040CrossRefGoogle Scholar
  20. Hetrick BAD, Wilson GWT, Gill BS, Cox TS (1995) Chromosomal location of mycorrhizal responsive genes in wheat. Can J Bot 73:891–897CrossRefGoogle Scholar
  21. Hetrick BAD, Wilson GWT, Cox TS (1996) Mycorrhizal response in wheat cultivars: relationship to phosphorus. Can J Bot 74:19–25CrossRefGoogle Scholar
  22. Jaccard P (1908) Nouvelles recherches sur la distribution florale. Bull Soc Vaud Sci Nat 44:223–270Google Scholar
  23. Kaeppler SM, Parke JL, Mueller SM, Senior L, Stuber C, Tracy WF (2000) Variation among maize inbred lines and detection of quantitative trait loci for growth at low phosphorus and responsiveness to arbuscular mycorrhizal fungi. Crop Sci 40:358–364CrossRefGoogle Scholar
  24. Kalendar R, Schulman AH (2006) IRAP and REMAP for retrotransposon-based genotyping and fingerprinting. Nat Protoc 1:2478–2484CrossRefGoogle Scholar
  25. Ker K, Charest C (2010) Nickel remediation by AM-colonized sunflower. Mycorrhiza 20:399–406CrossRefGoogle Scholar
  26. Kirkegaard JA, Ryan MH (2014) Magnitude and mechanisms of persistent crop sequence effects on wheat. Field Crops Res 164:154–165CrossRefGoogle Scholar
  27. Koide RT, Schreiner RP (1992) Regulation of the vesicular-arbuscular mycorrhizal symbiosis. Annu Rev Plant Physiol Plant Mol Biol 43:557–581CrossRefGoogle Scholar
  28. Koide R, Li M, Lewis J, Irby C (1988) Role of mycorrhizal infection in the growth and reproduction of wild vs. cultivated plants. I. Wild vs. cultivated oats. Oecologia 77:537–543CrossRefGoogle Scholar
  29. Lehmann A, Barto EK, Powell JR, Rillig MC (2012) Mycorrhizal responsiveness trends in annual crop plants and their wild relatives—a meta-analysis on studies from 1981 to 2010. Plant Soil 355:231–250CrossRefGoogle Scholar
  30. Leiser W, Olatoye M, Rattunde HF, Neumann G, Weltzien E, Haussmann BG (2015) No need to breed for enhanced colonization by arbuscular mycorrhizal fungi to improve low-P adaptation of West African sorghums. Plant Soil. doi: 10.1007/s11104-015-2437-1 CrossRefGoogle Scholar
  31. Lekberg Y, Koide RT (2005) Is plant performance limited by abundance of arbuscular mycorrhizal fungi? A meta-analysis of studies published between 1988 and 2003. New Phytol 168:189–204CrossRefGoogle Scholar
  32. Lentz DL, Pohl MD, Alvarado JL, Tarighat S, Bye R (2008) Sunflower (Helianthus annuus L.) as a pre-Columbian domesticate in Mexico. Proc Natl Acad Sci USA 105:6232–6237CrossRefGoogle Scholar
  33. Natali L, Cossu RM, Barghini E, Giordani T, Buti M, Mascagni F, Morgante M, Gill N, Kane NC, Rieseberg L, Cavallini A (2013) The repetitive component of the sunflower genome as shown by different procedures for assembling next generation sequencing reads. BMC Genom 14:686CrossRefGoogle Scholar
  34. Njeru ME, Avio L, Sbrana C, Turrini A, Bocci G, Barberi P, Giovannetti M (2014) First evidence for a major cover crop effect on arbuscular mycorrhizal fungi and organic maize growth. Agron Sustain Dev 34:841–848CrossRefGoogle Scholar
  35. Parke JL, Kaeppler SW (2000) Effects of genetic differences among crop species and cultivars upon the arbuscular mycorrhizal symbiosis. In: Kapulnik Y, Douds DD Jr (eds) Arbuscular mycorrhizas: physiology and function. Kluwer Academic Publishers, Dordrecht, pp 131–146CrossRefGoogle Scholar
  36. Putt ED (1978) History and present world status. In: Carter J (ed) Sunflower science and technology. Am Soc Agron, Madison, pp 1–30Google Scholar
  37. Rao PSK, Tilak BR, Arunachalam V (1990) Genetic variation for VA mycorrhiza-dependent phosphate mobilization in groundnut (Arachis hypogaea L.). Plant Soil 122:137–142CrossRefGoogle Scholar
  38. Rohlf FJ (2000) NTSys-pc: numerical taxonomy and multivariate analysis system, version 2.1. Exeter Software, New YorkGoogle Scholar
  39. Ryan MH, Kirkegaard JA (2012) The agronomic relevance of arbuscular mycorrhizas in the fertility of Australian extensive cropping systems. Agric Ecosyst Environ 163:37–53CrossRefGoogle Scholar
  40. Rychlik W, Rhoads RE (1989) A computer program for choosing optimal oligonucleotides for filter hybridization, sequencing and in vitro amplification of DNA. Nucleic Acids Res 17:8543–8551CrossRefGoogle Scholar
  41. Sawers RJH, Gutjahr C, Paszkowski U (2008) Cereal mycorrhiza: an ancient symbiosis in modern agriculture. Trends Plant Sci 13:93–97CrossRefGoogle Scholar
  42. Schulman AH, Flavell AJ, Ellis TH (2004) The application of LTR retrotransposons as molecular markers in plants. Methods Mol Biol 260:145–173PubMedGoogle Scholar
  43. Semelczi-Kovacs A (1975) Acclimatization and dissemination of the sunflower in Europe. Acta Ethnogr Acad Sci Hung 24:47–88Google Scholar
  44. Sikes BA, Kottenie K, Klironomos JN (2009) Plant and fungal identity determines pathogen protection of plant roots by arbuscular mycorrhizas. J Ecol 97:1274–1280CrossRefGoogle Scholar
  45. Singh AK, Hamel C, DePauw RM, Knox RE (2012) Genetic variability in arbuscular mycorrhizal fungi compatibility supports the selection of durum wheat genotypes for enhancing soil ecological services and cropping systems in Canada. Can J Microbiol 58:293–302CrossRefGoogle Scholar
  46. Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic Press, LondonGoogle Scholar
  47. Smith FA, Smith SE (1997) Structural diversity in (vesicular)-arbuscular mycorrhizal symbioses. New Phytol 137:373–388CrossRefGoogle Scholar
  48. Smith FA, Grace EJ, Smith SE (2009) More than a carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses. New Phytol 182:347–358CrossRefGoogle Scholar
  49. Tawaraya K (2003) Arbuscular mycorrhizal dependency of different plant species and cultivars. Soil Sci Plant Nutr 49:655–668CrossRefGoogle Scholar
  50. Thompson JP (1987) Decline of vesicular-arbuscular mycorrhizas in long fallow disorder of field crops and its expression in phosphorus deficiency in sunflower. Aust J Agric Res 38:847–867CrossRefGoogle Scholar
  51. Toth R, Page T, Castleberry R (1984) Differences in mycorrhizal colonization of maize selections for high and low ear leaf phosphorus. Crop Sci 24:994–997CrossRefGoogle Scholar
  52. Toth R, Toth D, Starke D (1990) Vesicular-arbuscular mycorrhizal colonization in Zea mays affected by breeding for resistance to fungal pathogens. Can J Bot 68:1039–1044CrossRefGoogle Scholar
  53. Turrini A, Giovannetti M (2012) Arbuscular mycorrhizal fungi in national parks, nature reserves and protected areas worldwide: a strategic perspective for their in situ conservation. Mycorrhiza 22:81–97CrossRefGoogle Scholar
  54. Ultra VU Jr, Tanaka S, Sakurai K, Iwasaki K (2007) Arbuscular mycorrhizal fungus (Glomus aggregatum) influences biotransformation of arsenic in the rhizosphere of sunflower (Helianthus annuus L.). Soil Sci Plant Nutr 53:499–508CrossRefGoogle Scholar
  55. Vukich M, Schulman AH, Giordani T, Natali L, Kalendar R, Cavallini A (2009a) Genetic variability in sunflower (Helianthus annuus L.) and in the Helianthus genus as assessed by retrotransposon-based molecular markers. Theor Appl Genet 119:1027–1038CrossRefGoogle Scholar
  56. Vukich M, Giordani T, Natali L, Cavallini A (2009b) Copia and Gypsy retrotransposons activity in sunflower (Helianthus annuus L.). BMC Plant Biol 9:150CrossRefGoogle Scholar
  57. Yao Q, Li X, Christie P (2001) Factors affecting arbuscular mycorrhizal dependency of wheat genotypes with different phosphorus efficiencies. J Plant Nutr 24:1409–1419CrossRefGoogle Scholar
  58. Yücel C, Özkan H, Ortaş I, Yağbasanlar T (2009) Screening of wild emmer wheat accessions (Triticum turgidum subsp. dicoccoides) for mycorrhizal dependency. Turk J Agric For 33:513–523Google Scholar
  59. Zhu YG, Smith SE, Barritt AR, Smith FA (2001) Phosphorus (P) efficiencies and mycorrhizal responsiveness of old and modern wheat cultivars. Plant Soil 237:249–255CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • A. Turrini
    • 1
  • T. Giordani
    • 1
  • L. Avio
    • 2
  • L. Natali
    • 1
  • M. Giovannetti
    • 1
  • A. Cavallini
    • 1
    Email author
  1. 1.Department of Agriculture, Food and EnvironmentUniversity of PisaPisaItaly
  2. 2.Institute of Agricultural Biology and Biotechnology, CNRPisaItaly

Personalised recommendations