Abstract
At present, there is no relevant information on arbuscular mycorrhiza and the effect of the symbiosis on the growth of wild populations of cyclamens. To fill this gap, two populations of Cyclamen purpurascens subsp. immaculatum, endemic in Nízke Tatry (NT) mountains and Veľká Fatra (VF) mountains, Slovakia, were studied in situ as well as in a greenhouse pot experiment. For both populations, mycorrhizal root colonization of native plants was assessed, and mycorrhizal inoculation potential (MIP) of the soils at the two sites was determined in 3 consecutive years. In the greenhouse experiment, the growth response of cyclamens to cross-inoculation with arbuscular mycorrhizal fungi (AMF) was tested: plants from both sites were grown in their native soils and inoculated with a Septoglomus constrictum isolate originating either from the same or from the other plant locality. Although the MIP of soil at the NT site was significantly higher than at the VF site, the level of AMF root colonization of C. purpurascens subsp. immaculatum plants in the field did not significantly differ between the two localities. In the greenhouse experiment, inoculation with AMF generally accelerated cyclamen growth and significantly increased all growth parameters (shoot dry weight, leaf number and area, number of flowers, tuber, and root dry weight) and P uptake. The two populations of C. purpurascens subsp. immaculatum grown in their native soils, however, differed in their response to inoculation. The mycorrhizal growth response of NT plants was one-order higher compared to VF plants, and all their measured growth parameters were stimulated regardless of the fungal isolates’ origin. In the VF plants, only the non-native (NT originating) isolate showed a significant positive effect on several growth traits. It can be concluded that mycorrhiza significantly increased fitness of C. purpurascens subsp. immaculatum, despite the differences between plant populations, implying that AMF symbionts should be taken into account in conservation programs of this endemic plant.
Similar content being viewed by others
References
Affre L, Thompson JD, Debussche M (1995) The reproductive biology of the Mediterranean endemic Cyclamen balearicum Willk (Primulaceae). Bot J Linn Soc 118:309–330
Allen MF, Moore TS, Christensen M (1982) Phytohormone changes in Bouteloua gracilis infected by vesicular arbuscular mycorrhizae. 2. Altered levels of gibberellin-like substances and abscisic acid in the host plant and abscisic-acid in the host plant. Can J Bot 60:468–471
Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Avio L, Pellegrino E, Bonari E, Giovannetti M (2006) Functional diversity of arbuscular mycorrhizal fungal isolates in relation to extraradical mycelial networks. New Phytol 172:347–357
Bennett AE, Daniell TJ, Opik M, Davison J, Moora M, Zobel M, Selosse MA, Evans D (2013) Arbuscular mycorrhizal fungal networks vary throughout the growing season and between successional stages. PLoS ONE 8(12):e83241
Bürün B, Sahin O (2009) In vitro and in vivo germination of Cyclamen alpinum seeds. Turk J Bot 33:277–283
Compton JA, Clennett JCB, Culham A (2004) Nomenclature in the dock. Overclassification leads to instability: a case study in the horticulturally important genus Cyclamen (Myrsinaceae). Bot J Linn Soc 146:339–349
Corbineau F, Neveur N, Come D (1989) Seed germination and seedling development in Cyclamen persicum. Ann Bot-London 63:87–96
Davison J, Öpik M, Zobel M, Vasar M, Metsis M, Moora M (2012) Communities of arbuscular mycorrhizal fungi detected in forest soil are spatially heterogeneous but do not vary throughout the growing season. PLoS ONE 7(8):e41938
de Novais CB, Borges WL, Jesus ED, Saggin OJ, Siqueira JO (2014) Inter- and intraspecific functional variability of tropical arbuscular mycorrhizal fungi isolates colonizing corn plants. Appl Soil Ecol 76:78–86
Debussche M, Grandjanny M, Debussche G, Affre L (1996) The ecology of an endemic and rare species with a fragmented distribution: Cyclamen balearicum Willk in France. Acta Bot Gallica 143:65–84
Debussche M, Debussche G, Grandjanny M (2000) Distribution of Cyclamen repandum Sibth. & Sm. subsp. repandum and ecology in Corsica and continental France. Acta Bot Gallica 147:123–142
Demars BG, Boerner REJ (1995) Mycorrhizal dynamics of 3 woodland herbs of contrasting phenology along topographic gradients. Am J Bot 82:1426–1431
Dickson S (2004) The Arum-Paris continuum of mycorrhizal symbioses. New Phytol 163 (1):187–200
Dubský M, Šrámek F, Vosátka M (2002) Inoculation of cyclamen (Cyclamen persicum) and poinsettia (Euphorbia pulcherrima) with arbuscular mycorrhizal fungi and Trichoderma harzianum. Rost Vyroba 48:63–68
Dugassa GD, vonAlten H, Schonbeck F (1996) Effects of arbuscular mycorrhiza (AM) on health of Linum usitatissimum L. infected by fungal pathogens. Plant Soil 185:173–182
Enkhtuya B, Rydlová J, Vosátka M (2000) Effectiveness of indigenous and non-indigenous isolates of arbuscular mycorrhizal fungi in soils from degraded ecosystems and man-made habitats. Appl Soil Ecol 14:201–211
Erdelská O, Turis P (1995) Biology of Daphne arbuscula Celak (Thymelaeaceae). Biologia 50:333–346
Gange AC, Ayres RL (1999) On the relation between arbuscular mycorrhizal colonization and plant ‘benefit’. Oikos 87:615–621
Garmendia I, Mangas VJ (2012) Application of arbuscular mycorrhizal fungi on the production of cut flower roses under commercial-like conditions. Span J Agric Res 10:166–174
Gerdemann JW, Nicolson TH (1963) Spores of mycorrhizal Endogone species extracted from soil by wet sieving and decanting. Trans Br Mycol Soc 46:235–244
Giovannetti M, Mosse B (1980) Evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500
Gouy M, Guindon S, Gascuel O (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27:221–224
Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321
Johnson D, Vandenkoornhuyse PJ, Leake JR, Gilbert L, Booth RE, Grime JP, Young JPW, Read DJ (2004) Plant communities affect arbuscular mycorrhizal fungal diversity and community composition in grassland microcosms. New Phytol 161:503–515
Kanka R, Turis P, Chilová V (2008) Phytosociological characteristic of the plant communities with the occurrence of endemic species Cyclamen fatrense. Hacquetia 7:21–31
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780
Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301
Kohout P, Sudová R, Janoušková M, Čtvrtlíková M, Hejda M, Pánková H, Slavíková R, Štajerová K, Vosátka M, Sýkorová Z (2014) Comparison of commonly used primer sets for evaluating arbuscular mycorrhizal fungal communities: is there a universal solution? Soil Biol Biochem 68:482–493
Koide RT (2010) Mycorrhizal symbiosis and plant reproduction. In: Koltai H, Kapulnik Y (eds) Arbuscular mycorrhizas: physiology and function. Springer Science + Business Media B.V, Dordrecht, pp 297–320
Kopáček J, Hejzlar J (1995) Semi-micro determination of total phosphorus in soils, sediments, and organic materials—a simplified perchloric-acid digestion procedure. Commun Soil Sci Plant 26:1935–1946
Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect VA mycorrhizas. Mycol Res 92:486–505
Krüger M, Stockinger H, Krüger C, Schüssler A (2009) DNA-based species level detection of Glomeromycota: one PCR primer set for all arbuscular mycorrhizal fungi. New Phytol 183:212–223
Kučera J, Turis P, Zozomová-Lihová J, Slovák M (2013) Cyclamen fatrense, myth or true Western Carpathian endemic? Genetic and morphological evidence. Preslia 85:133–158
Liu Y, He L, An LZ, Helgason T, Feng HY (2009) Arbuscular mycorrhizal dynamics in a chronosequence of Caragana korshinskii plantations. FEMS Microbiol Ecol 67:81–92
Maya MA, Matsubara Y (2013a) Influence of arbuscular mycorrhiza on the growth and antioxidative activity in cyclamen under heat stress. Mycorrhiza 23:381–390
Maya MA, Matsubara Y (2013b) Tolerance to Fusarium wilt and anthracnose diseases and changes of antioxidative activity in mycorrhizal cyclamen. Crop Prot 47:41–48
Meadow JF, Zabinski CA (2012) Linking symbiont community structures in a model arbuscular mycorrhizal system. New Phytol 194:800–809
Munkvold L, Kjoller R, Vestberg M, Rosendahl S, Jakobsen I (2004) High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol 164:357–364
Nowak J (2004) Effects of arbuscular mycorrhizal fungi and organic fertilization on growth, flowering, nutrient uptake, photosynthesis and transpiration of geranium (Pelargonium hortorum L.H. Bailey ‘Tango Orange’). Symbiosis 37:259–266
Pánková H, Münzbergová Z, Rydlová J, Vosátka M (2008) Differences in AM fungal root colonization between populations of perennial Aster species have genetic reasons. Oecologia 157:211–220
Pánková H, Münzbergová Z, Rydlová J, Vosátka M (2011) The response of Aster amellus (Asteraceae) to mycorrhiza depends on the origins of both the soil and the fungi. Am J Bot 98:850–858
Pánková H, Münzbergová Z, Rydlová J, Vosátka M (2014) Co-adaptation of plants and communities of arbuscular mycorrhizal fungi to their soil conditions. Folia Geobot 49:521–540
Perner H, Schwarz D, Bruns C, Mader P, George E (2007) Effect of arbuscular mycorrhizal colonization and two levels of compost supply on nutrient uptake and flowering of pelargonium plants. Mycorrhiza 17:469–474
Rambaut A, Suchard MA, Xie D, Drummond AJ (2013) Tracer v1.5, Available from http://beast.bio.ed.ac.uk/Tracer
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Schultz PA, Miller RM, Jastrow JD, Rivetta CV, Bever JD (2001) Evidence of a mycorrhizal mechanism for the adaptation of Andropogon gerardii (Poaceae) to high- and low-nutrient prairies. Am J Bot 88:1650–1656
Schwartz-Tzachor R, Dafni A, Potts SG, Elsikowitch D (2006) An ancient pollinator of a contemporary plant (Cyclamen persicum): when pollination syndromes break down. Flora 201:370–373
Senés-Guerrero C, Torres-Cortés G, Pfeiffer S, Rojas M, Schüssler A (2014) Potato-associated arbuscular mycorrhizal fungal communities in the Peruvian Andes. Mycorrhiza 24(6):405–417
Sensoy S, Demir S, Turkmen O, Erdinc C, Savur OB (2007) Responses of some different pepper (Capsicum annuum L.) genotypes to inoculation with two different arbuscular mycorrhizal fungi. Sci Hortic 113:92–95
Slovák M, Kučera J, Turis P, Zozomová-Lihová J (2013) Phylogeography of the alpine violet (Cyclamen purpurascens Mill.) northernmost glacial refugia and an endemic subspecies in the Western Carpathians? Acta Biol Cracov Bot 55:33
Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, London
Sohn BK, Kim KY, Chung SJ, Kim WS, Park SM, Kang JG, Rim YS, Cho JS, Kim TH, Lee JH (2003) Effect of the different timing of AMF inoculation on plant growth and flower quality of chrysanthemum. Sci Hortic 98:173–183
Streitwolf-Engel R, van der Heijden MGA, Wiemken A, Sanders IR (2001) The ecological significance of arbuscular mycorrhizal fungal effects on clonal reproduction in plants. Ecology 82:2846–2859
Sudová R, Doubková P, Vosátka M (2008) Mycorrhizal association of Agrostis capillaris and Glomus intraradices under heavy metal stress: combination of plant clones and fungal isolates from contaminated and uncontaminated substrates. Appl Soil Ecol 40:19–29
Sýkorová Z, Ineichen K, Wiemken A, Redecker D (2007) The cultivation bias: different communities of arbuscular mycorrhizal fungi detected in roots from the field, from bait plants transplanted to the field, and from a greenhouse trap experiment. Mycorrhiza 18:1–14
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Trent JD, Svejcar TJ, Blank RR (1994) Mycorrhizal colonization, hyphal lengths, and soil-moisture associated with 2 Artemisia tridentata subspecies. Great Basin Nat 54:291–300
Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorhization VA d’un systeme radiculaire. Recherche de methodes d’estimation ayant une signification fonctionnelle. In: Gianinazzi-Pearson V, Gianinazzi S (eds) Physiological and genetical aspects of mycorrhizae. INRA, Paris, pp 217–221
Turis P (2009) Ecobiology, selected population characteristics, distribution and protection of Cyclamen fatrense in the eastern part of its distribution area. PhD thesis, Bratislava
Turis P, Vidlička L (2013) Relationship of animals to the cyclamen Cyclamen fatrense Halda et Sojak: pollinators, consumers and occasional visitors. Biologia 68:517–524
Turis P, Kliment J, Feráková V, Dítě D, Eliáš P, Hrivnák R, Košťál J, Šuvada R, Mráz P, Bernátová D (2014) Red list of vascular plants of the Carpathian part of Slovakia. Thaiszia - J Bot 24:35–87
Udaiyan K, Karthikeyan A, Muthukumar T (1996) Influence of edaphic and climatic factors on dynamics of root colonization and spore density of vesicular-arbuscular mycorrhizal fungi in Acacia farnesiana Willd, and A. planifrons W et A. Trees-Struct Funct 11:65–71
van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72
van der Heijden MGA, Wiemken A, Sanders IR (2003) Different arbuscular mycorrhizal fungi alter coexistence and resource distribution between co-occurring plant. New Phytol 157:569–578
Vosátka M, Jansa J, Regvar M, Šrámek F, Malcová R (1999) Inoculation with mycorrhizal fungi—a feasible biotechnology for horticulture. Phyton-Ann Rei Bot A 39:219–224
Yang W, Zheng Y, Gao C, He XH, Ding Q, Kim Y, Rui YC, Wang SP, Guo LD (2013) The arbuscular mycorrhizal fungal community response to warming and grazing differs between soil and roots on the Qinghai-Tibetan Plateau. PLoS ONE 8(9):e76447
Yesson C, Toomey NH, Culham A (2009) Cyclamen: time, sea and speciation biogeography using a temporally calibrated phylogeny. J Biogeogr 36:1234–1252
Zubek S, Turnau K, Blaszkowski J (2005) Arbuscular mycorrhiza of plants from the Mountain Boptanical Garden in Zakopane. Acta Mycol 40:25–41
Zubek S, Turnau K, Blaszkowski J (2008) Arbuscular mycorrhiza of endemic and endangered plants from the Tatra Mts. Acta Soc Bot Pol 77:149–156
Zubek S, Turnau K, Tsimilli-Michael M, Strasser RJ (2009a) Response of endangered plant species to inoculation with arbuscular mycorrhizal fungi and soil bacteria. Mycorrhiza 19:113–123
Zubek S, Blaszkowski J, Delimat A, Turnau K (2009b) Arbuscular mycorrhizal and dark septate endophyte colonization along altitudinal gradients in the Tatra Mountains. Arct Antarct Alp Res 41:272–279
Acknowledgments
We are grateful to Pavla Doubková for the valuable comments on the text of the manuscript and to Marie Albrechtová and Hana Strusková from the Analytical Laboratories of the Institute of Botany AS CR, who performed soil chemical analyses and determined the content of phosphorus in plant biomass. Financial support for this study was provided by the long-term research development project RVO 67985939.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Rydlová, J., Sýkorová, Z., Slavíková, R. et al. The importance of arbuscular mycorrhiza for Cyclamen purpurascens subsp. immaculatum endemic in Slovakia. Mycorrhiza 25, 599–609 (2015). https://doi.org/10.1007/s00572-015-0634-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00572-015-0634-7