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

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Abstract

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.

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References

  • 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 327:441–453

    Article  CAS  Google Scholar 

  • Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42

    Article  Google Scholar 

  • Avio L, Pellegrino E, Bonari E, Giovannetti M (2006) Functional diversity of arbuscular mycorrhizal fungal isolates in relation to extraradical mycelia networks. New Phytol 172:347–357

    Article  Google Scholar 

  • Avio L, Cristani C, Strani P, Giovannetti M (2009) Genetic and phenotypic diversity of geographically different isolates of Glomus mosseae. Can J Microbiol 55:242–253

    Article  CAS  Google Scholar 

  • Azcon R, Ocampo JA (1981) Factors affecting the vesicular-arbuscular infection and mycorrhizal dependency of thirteen wheat cultivars. New Phytol 87:677–685

    Article  CAS  Google Scholar 

  • 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 98:394–401

    Article  Google Scholar 

  • 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 84:82–92

    Article  Google Scholar 

  • 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 192:289–303

    Article  CAS  Google Scholar 

  • 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 176:325–328

    Article  CAS  Google Scholar 

  • Cheres MT, Knapp SJ (1998) Ancestral origins and genetic diversity of cultivated sunflower: analysis of the pedigrees of public germplasm. Crop Sci 38:1476–1482

    Article  Google Scholar 

  • Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280

    Article  CAS  Google Scholar 

  • Falconer DS (1981) Introduction to quantitative genetics, 2nd edn. Longman, New York

    Google Scholar 

  • Gallaud I (1905) Études sur les mycorrhizes endotrophes. Rev Gén Bot 17:5–48, 66–83, 123–136, 223–239, 313–325, 425–433, 479–500

  • 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 20:519–530

    Article  Google Scholar 

  • Giovannetti M, Gianinazzi-Pearson V (1994) Biodiversity in arbuscular mycorrhizal fungi. Mycol Res 98:705–715

    Article  Google Scholar 

  • Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500

    Article  Google Scholar 

  • Graham JH, Abbott LK (2000) Wheat responses to aggressive and non-aggressive arbuscular mycorrhizal fungi. Plant Soil 220:207–218

    Article  CAS  Google Scholar 

  • Harter AV, Gardner KA, Falush D, Lentz DL, Bye RA, Rieseberg LH (2004) Origin of extant domesticated sunflowers in eastern North America. Nature 430:201–205

    Article  CAS  Google Scholar 

  • Hetrick BAD, Wilson GWT, Cox TS (1992) Mycorrhizal dependence of modern wheat varieties, landraces, and ancestors. Can J Bot 70:2032–2040

    Article  Google Scholar 

  • Hetrick BAD, Wilson GWT, Gill BS, Cox TS (1995) Chromosomal location of mycorrhizal responsive genes in wheat. Can J Bot 73:891–897

    Article  Google Scholar 

  • Hetrick BAD, Wilson GWT, Cox TS (1996) Mycorrhizal response in wheat cultivars: relationship to phosphorus. Can J Bot 74:19–25

    Article  CAS  Google Scholar 

  • Jaccard P (1908) Nouvelles recherches sur la distribution florale. Bull Soc Vaud Sci Nat 44:223–270

    Google Scholar 

  • 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 40:358–364

    Article  Google Scholar 

  • Kalendar R, Schulman AH (2006) IRAP and REMAP for retrotransposon-based genotyping and fingerprinting. Nat Protoc 1:2478–2484

    Article  CAS  Google Scholar 

  • Ker K, Charest C (2010) Nickel remediation by AM-colonized sunflower. Mycorrhiza 20:399–406

    Article  CAS  Google Scholar 

  • Kirkegaard JA, Ryan MH (2014) Magnitude and mechanisms of persistent crop sequence effects on wheat. Field Crops Res 164:154–165

    Article  Google Scholar 

  • Koide RT, Schreiner RP (1992) Regulation of the vesicular-arbuscular mycorrhizal symbiosis. Annu Rev Plant Physiol Plant Mol Biol 43:557–581

    Article  CAS  Google Scholar 

  • 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 77:537–543

    Article  Google Scholar 

  • 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 355:231–250

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 168:189–204

    Article  CAS  Google Scholar 

  • 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 105:6232–6237

    Article  CAS  Google Scholar 

  • 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 14:686

    Article  CAS  Google Scholar 

  • 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 34:841–848

    Article  Google Scholar 

  • 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 131–146

    Chapter  Google Scholar 

  • Putt ED (1978) History and present world status. In: Carter J (ed) Sunflower science and technology. Am Soc Agron, Madison, pp 1–30

    Google Scholar 

  • Rao PSK, Tilak BR, Arunachalam V (1990) Genetic variation for VA mycorrhiza-dependent phosphate mobilization in groundnut (Arachis hypogaea L.). Plant Soil 122:137–142

    Article  CAS  Google Scholar 

  • Rohlf FJ (2000) NTSys-pc: numerical taxonomy and multivariate analysis system, version 2.1. Exeter Software, New York

    Google Scholar 

  • Ryan MH, Kirkegaard JA (2012) The agronomic relevance of arbuscular mycorrhizas in the fertility of Australian extensive cropping systems. Agric Ecosyst Environ 163:37–53

    Article  Google Scholar 

  • 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 17:8543–8551

    Article  CAS  Google Scholar 

  • Sawers RJH, Gutjahr C, Paszkowski U (2008) Cereal mycorrhiza: an ancient symbiosis in modern agriculture. Trends Plant Sci 13:93–97

    Article  CAS  Google Scholar 

  • Schulman AH, Flavell AJ, Ellis TH (2004) The application of LTR retrotransposons as molecular markers in plants. Methods Mol Biol 260:145–173

    CAS  PubMed  Google Scholar 

  • Semelczi-Kovacs A (1975) Acclimatization and dissemination of the sunflower in Europe. Acta Ethnogr Acad Sci Hung 24:47–88

    Google Scholar 

  • Sikes BA, Kottenie K, Klironomos JN (2009) Plant and fungal identity determines pathogen protection of plant roots by arbuscular mycorrhizas. J Ecol 97:1274–1280

    Article  Google Scholar 

  • 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 58:293–302

    Article  CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic Press, London

    Google Scholar 

  • Smith FA, Smith SE (1997) Structural diversity in (vesicular)-arbuscular mycorrhizal symbioses. New Phytol 137:373–388

    Article  Google Scholar 

  • Smith FA, Grace EJ, Smith SE (2009) More than a carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses. New Phytol 182:347–358

    Article  CAS  Google Scholar 

  • Tawaraya K (2003) Arbuscular mycorrhizal dependency of different plant species and cultivars. Soil Sci Plant Nutr 49:655–668

    Article  Google Scholar 

  • 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 38:847–867

    Article  CAS  Google Scholar 

  • Toth R, Page T, Castleberry R (1984) Differences in mycorrhizal colonization of maize selections for high and low ear leaf phosphorus. Crop Sci 24:994–997

    Article  Google Scholar 

  • 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 68:1039–1044

    Article  Google Scholar 

  • 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 22:81–97

    Article  Google Scholar 

  • 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 53:499–508

    Article  CAS  Google Scholar 

  • 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 119:1027–1038

    Article  CAS  Google Scholar 

  • Vukich M, Giordani T, Natali L, Cavallini A (2009b) Copia and Gypsy retrotransposons activity in sunflower (Helianthus annuus L.). BMC Plant Biol 9:150

    Article  Google Scholar 

  • Yao Q, Li X, Christie P (2001) Factors affecting arbuscular mycorrhizal dependency of wheat genotypes with different phosphorus efficiencies. J Plant Nutr 24:1409–1419

    Article  CAS  Google Scholar 

  • 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 33:513–523

    Google Scholar 

  • Zhu YG, Smith SE, Barritt AR, Smith FA (2001) Phosphorus (P) efficiencies and mycorrhizal responsiveness of old and modern wheat cultivars. Plant Soil 237:249–255

    Article  CAS  Google Scholar 

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Acknowledgments

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

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Correspondence to A. Cavallini.

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A. Turrini and T. Giordani contributed equally to this work.

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Turrini, A., Giordani, T., Avio, L. et al. Large variation in mycorrhizal colonization among wild accessions, cultivars, and inbreds of sunflower (Helianthus annuus L.). Euphytica 207, 331–342 (2016). https://doi.org/10.1007/s10681-015-1546-5

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