Skip to main content
Log in

Specific arbuscular mycorrhizal fungi associated with non-photosynthetic Petrosavia sakuraii (Petrosaviaceae)

  • Original Paper
  • Published:
Mycorrhiza Aims and scope Submit manuscript

Abstract

Mycorrhizal fungi in roots of the achlorophyllous Petrosavia sakuraii (Petrosaviaceae) were identified by molecular methods. Habitats examined were plantations of the Japanese cypress Chamaecyparis obtusa in Honshu, an evergreen broad-leaved forest in Amami Island in Japan and a mixed deciduous and evergreen forest in China. Aseptate hyphal coils were observed in root cortical cells of P. sakuraii, suggesting Paris-type arbuscular mycorrhiza (AM). Furthermore, hyphal coils that had degenerated to amorphous clumps were found in various layers of the root cortex. Despite extensive sampling of P. sakuraii from various sites in Japan and China, most of the obtained AM fungal sequences of the nuclear small subunit ribosomal RNA gene were nearly identical and phylogenetic analysis revealed that they formed a single clade in the Glomus group A lineage. This suggests that the symbiotic relationship is highly specific. AM fungi of P. sakuraii were phylogenetically different from those previously detected in the roots of some mycoheterotrophic plants. In a habitat in C. obtusa plantation, approximately half of the AM fungi detected in roots of C. obtusa surrounding P. sakuraii belonged to the same clade as that of P. sakuraii. This indicates that particular AM fungi are selected by P. sakuraii from diverse indigenous AM fungi. The same AM fungi can colonize both plant species, and photosynthates of C. obtusa may be supplied to P. sakuraii through a shared AM fungal mycelial network. Although C. obtusa plantations are widely distributed throughout Japan, P. petrosavia is a rare plant species, probably because of its high specificity towards particular AM fungi.

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
Fig. 4

Similar content being viewed by others

References

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bidartondo MI, Redecker D, Hijri I, Wiemken A, Bruns TD, Domínguez L, Sérsic A, Leake JR, Read DJ (2002) Epiparasitic plants specialized on arbuscular mycorrhizal fungi. Nature 419:389–392

    Article  CAS  PubMed  Google Scholar 

  • Bonfante P, Perotto S (1995) Strategies of arbuscular mycorrhizal fungi when infecting host plants. New Phytol 130:3–21

    Article  Google Scholar 

  • Brundrett M, Bougher N, Dell B, Grove T, Malajczuk N (1996) Working with mycorrhizas in forestry and agriculture. Australian Center for International Agriculture Research, Canberra

    Google Scholar 

  • Cameron KM, Chase MW, Rudall PJ (2003) Recircumscription of the monocotyledonous family Petrosaviaceae to include Japonolirion. Brittonia 55:214–225

    Article  Google Scholar 

  • Chen X, Tamura MN (2000) Petrosavia. Flora of China 24:77. Science, Beijing

    Google Scholar 

  • Domínguez L, Sérsic A, Melville L, Peterson RL (2006) ‘Prepackaged symbioses’: propagules on roots of themycoheterotrophic plant Arachnitis uniflora. New Phytol 169:191–198

    Article  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  PubMed  Google Scholar 

  • Franke T, Beenken L, Döring M, Kocyan A, Agerer R (2006) Arbuscular mycorrhizal fungi of the Glomus-group A lineage (Glomerales; Glomeromycota) detected inmycoheterotrophic plants from tropical Africa. Mycol Prog 5:24–31

    Article  Google Scholar 

  • Fuse S, Tamura MN (2000) A phylogenetic analysis of the plastid matK gene with emphasis on Melanthiaceae sensu lato. Plant Biol 2:415–427

    Article  CAS  Google Scholar 

  • Helgason T, Daniell TJ, Husband R, Fitter AH, Young JPW (1998) Ploughing up the wood-wide web? Nature 394:431

    Article  CAS  PubMed  Google Scholar 

  • Imhof S (1997) Root anatomy and mycotrophy of the achlorophyllous Voyria tenella Hooker (Gentianaceae). Bot Acta 110:298–305

    Article  Google Scholar 

  • Imhof S (1998) Subterranean structures and mycotrophy of the achlorophyllous Triuris hyaline Miers (Triuridaceae). Can J Bot 76:2011–2019

    Google Scholar 

  • Imhof S (1999a) Root morphology, anatomy and mycotrophy of the achlorophyllous Voyria aphylla (Jacq.) Pers. (Gentianaceae). Mycorrhiza 9:33–39

    Article  Google Scholar 

  • Imhof S (1999b) Subterrranean structures and mycorrhiza of the achlorophyllous Burmannia tenella Benth. (Burmanniaceae). Can J Bot 77:637–643

    Google Scholar 

  • Imhof S (2003) A dorsivental mycorrhizal root in the achlorophyllous Sciaphila polygyna (Triuridaceae). Mycorrhiza 13:327–332

    Article  PubMed  Google Scholar 

  • Imhof S (2007) Specialized mycorrhizal colonization pattern in achlorophyllous Epirixanthes spp. (Polygalaceae). Plant Biol 9:786–792

    Article  CAS  PubMed  Google Scholar 

  • Imhof S, Weber HC (1997) Root anatomy and mycotrophy (AM) of the achlorophyllous Voyria truncate (Standl.) Standl. & Steyerm. (Gentianaceae). Bot Acta 110:127–134

    Article  Google Scholar 

  • Knöbel M, Weber HC (1988) Vergleichende Untersuchungen zur Mycotrophie bei Gentiana verna L. und Voyria truncate (Stand.) Stand. and Stey. (Gentianaceae). Beitr Biol Pflanz 63:463–477

    Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Leake JR (1994) Tansley Review No. 69. The biology of mycoheterotrophic (‘saprotrophic’) plants. New Phytol 127:171–216

    Article  Google Scholar 

  • Lee J, Lee S, Young JPW (2008) Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 65:339–349

    Article  CAS  PubMed  Google Scholar 

  • Merckx V, Bidartondo MI (2008) Breakdown and delayed cospection in the arbuscular mycorrhizal mutualism. Proc R Soc B 275:1029–1035

    Article  PubMed  PubMed Central  Google Scholar 

  • Merckx V, Stöckel M, Fleischmann A, Bruns TD, Gebauer G (2010) 15N and 13C natural abundance of two mycoheterotrophic and a putative partially mycoheterotrophic species associated with arbuscular mycorrhizal fungi. New Phytol 188:590–596

    Article  CAS  PubMed  Google Scholar 

  • Ministry of the Environment (2007) Red list. http://www.biodic.go.jp/rdb/rdb_f.html. Accessed 7 December 2010

  • Ohba H (1984) A review of Petrosavia (Liliaceae), with special reference to the floral features. J Jap Bot 59:106–110

    Google Scholar 

  • Page RDM (1996) An application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358

    CAS  PubMed  Google Scholar 

  • Peterson RL, Howarth MJ, Whittier DP (1981) Interactions between a fungal endophyte and gametophyte cells in Psilotum nudum. Can J Bot 59:711–720

    Article  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:404–425

    Google Scholar 

  • Sanders IR (2002) Specificity in the arbuscular mycorrhizal symbiosis. In: van der Heijden MGA, Sanders IR (eds) Mycorrhizal ecology. Springer, Berlin, pp 415–437

    Chapter  Google Scholar 

  • Schmid E, Oberwinkler F (1993) Mycorrhiza-like interaction between the achlorophyllous gametophyte of Lycopodium clavatum L. and its fungal endophyte studied by light and electron microscopy. New Phytol 124:69–81

    Article  Google Scholar 

  • Schüβler A (2010) Glomeromycota taxonomy. http://www.lrz.de/~schuessler/amphylo/. Accessed 13 July 2010

  • Schüβler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421

    Article  Google Scholar 

  • Schwarzott D, Schüβler A (2001) A simple and reliable method for SSU rRNA gene DNA extraction, amplification, and cloning from single AM fungal spores. Mycorrhiza 10:203–207

    Article  CAS  Google Scholar 

  • Selosse MA, Cameron DD (2010) Introduction to a virtual special issue on mycoheterotrophy: new phytologist sheds light on non-green plants. New Phytol 185:591–593

    Article  PubMed  Google Scholar 

  • Simon LM, Lalonde TD, Bruns TD (1992) Specific amplification of 18S fungal ribosomal genes from vesicular-arbuscular endomycorrhizal fungi colonizing roots. Appl Environ Microbiol 58:291–295

    CAS  PubMed  PubMed Central  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, London

    Google Scholar 

  • Smith FA, Smith SE (1997) Tansley Review no. 96. Structual diversity in (vesicular)-arbuscular mycorrhizal symbioses. New Phytol 137:373–388

    Article  Google Scholar 

  • Soltis DE, Mort ME, Soltis PS, Albach DC, Zanis M, Savolainen V, Hahn WH, Hoot SB, Fay MF, Axtell M, Swensen SM, Price LM, Kress WJ, Nixon KC, Farris JS (2000) Angiosperm phylogeny inferred from 18S rDNA, rbcL, and atpB sequences. Bot J Linn Soc 133:381–461

    Article  Google Scholar 

  • Spurr AR (1969) A low viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43

    Article  CAS  PubMed  Google Scholar 

  • Stant MY (1970) Anatomy of Petrosavia stellaris Becc., a saprophytic monocotyledon. Bot J Linn Soc 63:147–161

    Google Scholar 

  • Takahashi H, Nishio E, Hayashi H (1993) Pollination biology of the saprophytic species Petrosavia sakuraii (Makino) van Steenis in central Japan. J Plant Res 106:213–217

    Article  Google Scholar 

  • Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbour-joining method. Proc Natl Acad Sci USA 101:11030–11035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetic analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Tobe H (2008) Embryology of Japonolirion (Petrosaviaceae, Petrosaviales): a comparison with other monocots. J Plant Res 121:407–416

    Article  PubMed  Google Scholar 

  • Tobe H, Takahashi H (2009) Embryology of Petrosavia (Petrosaviaceae, Petrosaviales): evidence for the distinctiness of the family from other monocots. J Plant Res 122:597–610

    Article  PubMed  Google Scholar 

  • Wang B, Qiu YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363

    Article  CAS  PubMed  Google Scholar 

  • Watanabe K (1944) Morphologisch-biologische studien über Miyoshia sakuraii Makino. J Jap Bot 20:85–93

    Google Scholar 

  • Weising K, Nybom H, Wolff K, Meyer W (1995) DNA fingerprinting in plants and fungi. CRC, Boca Raton

    Google Scholar 

  • Winther JL, Friedman WE (2007) Arbuscular mycorrhizal symbionts in Botrychium (Ophioglossaceae). Am J Bot 94:1248–1255

    Article  CAS  PubMed  Google Scholar 

  • Winther JL, Friedman WE (2008) Arbuscular mycorrhizal associations in Lycopodiaceae. New Phytol 177:790–801

    Article  CAS  PubMed  Google Scholar 

  • Winther JL, Friedman WE (2009) Phylogenetic affinity of arbuscular mycorrhizal symbionts in Psilotum nudum. J Plant Res 122:485–496

    Article  PubMed  Google Scholar 

  • Yamato M (2001) Identification of a mycorrhizal fungus in the roots of achlorophyllous Sciaphila tosaensis Makino (Triuridaceae). Mycorrhiza 11:83–88

    Article  CAS  Google Scholar 

  • Yamato M, Iwasaki M (2002) Morphological types of arbuscular mycorrhizal fungi in roots of understory plants in Japanese deciduous broadleaved forests. Mycorrhiza 12:291–296

    Article  PubMed  Google Scholar 

  • Yamato M, Yagame T, Iwase K (2010) Arbuscular mycorrhizal fungi in roots of non-photosynthetic plants, Sciaphila japonica and Sciaphila tosaensis (Triuridaceae). Mycoscience (in press)

Download references

Acknowledgements

We thank Ryozo Hayashi, Tatsuya Iwai, Masayuki Matsui, Teruo Nakajima and Hiroshi Yamashita for their kind help during the field work and Hiroko Abe and Shohei Fujimomri for technical assistance. This study was supported by the Global COE Program ‘Advanced utilization of fungus/mushroom resources for sustainable society in harmony with nature’ from the Ministry of Education, Culture, Sports, Science and Technology of Japan and by Grants-in-Aid to Scientific Research from the Japan Society for Promotion of Science (Nos. 21370038 and 21510240).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Masahide Yamato.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yamato, M., Yagame, T., Shimomura, N. et al. Specific arbuscular mycorrhizal fungi associated with non-photosynthetic Petrosavia sakuraii (Petrosaviaceae). Mycorrhiza 21, 631–639 (2011). https://doi.org/10.1007/s00572-011-0373-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-011-0373-3

Keywords

Navigation