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Journal of Plant Research

, Volume 131, Issue 4, pp 589–597 | Cite as

Comparative morphological analysis of two parallel mycoheterotrophic transitions reveals divergent and convergent traits in the genus Pyrola (Pyroleae, Ericaceae)

  • Kohtaroh Shutoh
  • Kenji Suetsugu
  • Shingo Kaneko
  • Takahide Kurosawa
Regular Paper
  • 185 Downloads

Abstract

The genus Pyrola includes species with different degree of mycoheterotrophy; some species possess individuals that rely on all carbon through their associations with fungi (full mycoheterotrophy, FM), whereas some species obtain carbon through both fungi and photosynthesis by itself (partial mycoheterotrophy, PM). To investigate how plant functional traits of photosynthesis and reproduction are related to the degree of mycoheterotrophy in the initial stage of the transition from PM to FM, we determined morphological traits in FM (or nearly FM) and PM species in two independent lineages, P. picta and P. japonica complexes. We used herbarium specimens and examined leaf number, leaf area, flower number, and scape length in FM or nearly FM species (P. aphylla and P. subaphylla) and PM species (P. picta s.l. and P. japonica). We found a leaf area reduction in FM (or nearly FM) species in both lineages, suggesting that this is a convergent trait. The number of flowers was not significantly different between FM (or nearly FM) and PM species in both lineages. On the other hand, differences in the variation between FM (or nearly FM) and PM species were found in some traits between the two lineages. The FM (or nearly FM) species in one lineage only possessed rudimentary leaves, whereas that in the other linage possessed a few small, ordinary leaves in addition to those with only rudimentary leaves. The scape length of the FM (or nearly FM) species was significantly longer than that of PM species in one lineage, whereas it was shorter in the other lineage. The different and common variations are divergent and convergent traits, respectively, that could be associated with the transition to FM in Pylora. In addition, shoots of both PM species occasionally lacked ordinary leaves, possibly indicating possession of these shoots is preadaptation for the transition to FM in Pyrola.

Keywords

Ericaceae Herbarium specimens Full mycoheterotrophy Partial mycoheterotrophy Pyrola aphylla Pyrola subaphylla 

Notes

Acknowledgements

We are grateful to M. Briggs and S. Dawson (K), A. Ebihara (TNS), M. Maki and K. Yonekura (TUS), C. Pendry and M. F. Watson (E), N. Murakami (MAK), and H. Nagamasu (KYO) for facilitating the examination of herbarium specimens. This work was supported by the Research Project of Fukushima University for Regeneration of Harmonies between Human Activity and Nature in Bandai-Asahi National Park, the Nichirei Corporation, and a Grant-in-Aid from Japan Society for the Promotion of Science Research Fellowship [No. 15J12267].

Supplementary material

10265_2018_1040_MOESM1_ESM.pdf (348 kb)
Supplementary material 1 (PDF 347 KB)

References

  1. Camp WH (1940) Aphyllous forms in Pyrola. Bull Torrey Bot Club 67:453–465.  https://doi.org/10.2307/2480967 CrossRefGoogle Scholar
  2. Chen X, Gale SW, Cribb PJ (2009) Gastrodia. In: Wu Z, Raven PH, Hong D (eds) Flora of China, Orchidaceae, vol 25. Science Press, Beijing, pp 201–205Google Scholar
  3. Haber E (1987) Variability, distribution, and systematics of Pyrola picta s.l. (Ericaceae) in Western North America. Syst Bot 12:324–335.  https://doi.org/10.2307/2419328 CrossRefGoogle Scholar
  4. Holm T (1898) Pyrola aphylla: a morphological study. Bot Gaz 25:246–254CrossRefGoogle Scholar
  5. Hynson NA, Bruns TD (2009) Evidence of a myco-heterotroph in the plant family Ericaceae that lacks mycorrhizal specificity. Proc R Soc Lond B 276:4053–4059.  https://doi.org/10.1098/rspb.2009.1190 CrossRefGoogle Scholar
  6. Hynson NA, Preiss K, Gebauer G, Bruns TD (2009) Isotopic evidence of full and partial myco-heterotrophy in the plant tribe Pyroleae (Ericaceae). New Phytol 182:719–726.  https://doi.org/10.1111/j.1469-8137.2009.02781.x CrossRefPubMedGoogle Scholar
  7. Hynson NA, Mambelli S, Amend AS, Dawson TE (2012) Measuring carbon gains from fungal networks in understory plants from the tribe Pyroleae (Ericaceae): a field manipulation and stable isotope approach. Oecologia 169:307–317.  https://doi.org/10.1007/s00442-011-2198-3 CrossRefPubMedGoogle Scholar
  8. Hynson NA, Schiebold JMI, Gebauer G (2016) Plant family identity distinguishes patterns of carbon and nitrogen stable isotope abundance and nitrogen concentration in mycoheterotrophic plants associated with ectomycorrhizal fungi. Ann Bot 118:467–479.  https://doi.org/10.1093/aob/mcw119 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Jolles DD (2015) Morphometric analysis of floral variation in the Pyrola picta species complex (Ericaceae): interpretation and implications for ecological and phylogenetic differentiation. Bot J Linn Soc 177:462–480.  https://doi.org/10.1111/boj.12244 CrossRefGoogle Scholar
  10. Jolles DD, Wilson CA (2014) Pyrola crypta: A Pacific Northwest species belonging to the Pyrola picta species complex. Taxon 63:789–800.  https://doi.org/10.12705/634.15 CrossRefGoogle Scholar
  11. Jolles DD, Wolfe AD (2012) Genetic differentiation and crypsis among members of the myco-heterotrophic Pyrola picta species complex (Pyroleae: Monotropoideae: Ericaceae). Syst Bot 37:468–477.  https://doi.org/10.1600/036364412X635511 CrossRefGoogle Scholar
  12. Julou T, Burghardt B, Gebauer G, Berveiller D, Damesin C, Selosse MA (2005) Mixotrophy in orchids: insights from a comparative study of green individuals and nonphotosynthetic individuals of Cephalanthera damasonium. New Phytol 166:639–653.  https://doi.org/10.1111/j.1469-8137.2005.01364.x CrossRefPubMedGoogle Scholar
  13. Lallemand F, Gaudeul M, Lambourdière J, Matsuda Y, Hashimoto Y, Selosse MA (2016) The elusive predisposition to mycoheterotrophy in Ericaceae. New Phytol 212:314–319.  https://doi.org/10.1111/nph.14092 CrossRefPubMedGoogle Scholar
  14. Leake JR (1994) The biology of myco-heterotrophic (‘saprophytic’) plants. New Phytol 127:171–216.  https://doi.org/10.1111/j.1469-8137.1994.tb04272.x CrossRefGoogle Scholar
  15. Liu ZW, Zhou J, Liu ED, Peng H (2010) A molecular phylogeny and a new classification of Pyrola (Pyroleae, Ericaceae). Taxon 59:1690–1700.  https://doi.org/10.2307/41059866 Google Scholar
  16. Liu ZW, Jolles DD, Zhou J, Peng H, Milne RI (2014) Multiple origins of circumboreal taxa in Pyrola (Ericaceae), a group with a tertiary relict distribution. Ann Bot 114:1701–1709.  https://doi.org/10.1093/aob/mcu198 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Matsuda Y, Shimizu S, Mori M, Ito S, Selosse MA (2012) Seasonal and environmental changes of mycorrhizal associations and heterotrophy levels in mixotrophic Pyrola japonica (Ericaceae) growing under different light environments. Am J Bot 99:1177–1188.  https://doi.org/10.3732/ajb.1100546 CrossRefPubMedGoogle Scholar
  18. Maximowicz CJ (1867) Diagnoses breves plantarum novarum Japoniae et Mandshuriae, Decas tertia. Bull Acad Imp Sci Saint-Pétersbourg 11:433–439Google Scholar
  19. Merckx VSFT. (2013) Mycoheterotrophy: an introduction. In: Merckx VSFT (ed) Mycoheterotrophy the biology of plants living on fungi. Springer, New York, pp 1–17Google Scholar
  20. Merckx V, Schols P, Maas-van de Kamer H, Maas P, Huysmans S, Smets E (2006) Phylogeny and evolution of Burmanniaceae (Dioscoreales) based on nuclear and mitochondrial data. Am J Bot 93:1684–1698.  https://doi.org/10.3732/ajb.93.11.1684 CrossRefPubMedGoogle Scholar
  21. Merckx VSFT., Mennes CB, Peay KG, Geml J (2013) Evolution and diversification. In: Merckx VSFT (ed) Mycoheterotrophy the biology of plants living on fungi. Springer, New York, pp 215–244Google Scholar
  22. Motomura H, Selosse MA, Martos F, Kagawa A, Yukawa T (2010) Mycoheterotrophy evolved from mixotrophic ancestors: evidence in Cymbidium (Orchidaceae). Ann Bot 106:573–581.  https://doi.org/10.1093/aob/mcq156 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Ohwi J, Meyer FG, Walker EH (1965) Flora of Japan (in English). Smithsonian Institution, WashingtonGoogle Scholar
  24. Preiss K, Adam IKU, Gebauer G (2010) Irradiance governs exploitation of fungi: fine-tuning of carbon gain by two partially myco-heterotrophic orchids. Proc R Soc Lond B 277:1333–1336.  https://doi.org/10.1098/rspb.2009.1966 CrossRefGoogle Scholar
  25. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna: http://www.r-project.org/. Accessed 11 May 2018
  26. Selosse MA, Roy M (2009) Green plants that feed on fungi: facts and questions about mixotrophy. Trends Plant Sci 14:64–70.  https://doi.org/10.1016/j.tplants.2008.11.004 CrossRefPubMedGoogle Scholar
  27. Shutoh K, Kaneko S, Suetsugu K, Naito YI, Kurosawa T (2016) Variation in vegetative morphology tracks the complex genetic diversification of the mycoheterotrophic species Pyrola japonica sensu lato. Am J Bot 103:1618–1629.  https://doi.org/10.3732/ajb.1600091 CrossRefPubMedGoogle Scholar
  28. Shutoh K, Izuno A, Isagi Y, Kurosawa T, Kaneko S (2017a) Development of microsatellite markers for partially and putative fully mycoheterotrophic varieties of Pyrola japonica sensu lato (Ericaceae). Genes Genet Syst 92:99–103.  https://doi.org/10.1266/ggs.16-00048 CrossRefPubMedGoogle Scholar
  29. Shutoh K, Kaneko S, Kurosawa T (2017b) Taxonomy and distribution of Pyrola subaphylla Maxim. (Pyroleae, Ericaceae). Acta Phytotaxon Geobot 68:181–192.  https://doi.org/10.18942/apg.201707 Google Scholar
  30. Suetsugu K (2017) Two new species of Gastrodia (Gastrodieae, Epidendroideae, Orchidaceae) from Okinawa Island, Ryukyu Islands, Japan. Phytotaxa 302:251–258.  https://doi.org/10.11646/phytotaxa.302.3.4 CrossRefGoogle Scholar
  31. Takahashi H (1986) Pollen morphology of Pyrola and its taxonomic significance. Bot Mag Tokyo 99:137–154.  https://doi.org/10.1007/BF02488816 CrossRefGoogle Scholar
  32. Takahashi H (1993) Pyrolaceae. In: Iwatsuki K, Yamazaki T, Bouffod DE, Ohba H (eds) Flora of Japan, vol. IIIa: Angiospermae dicotyledoneae sympetalae (a). Kodansha, Tokyo, pp 64–70Google Scholar
  33. Tonkova NA (2013) The morphology of flowers and method of pollination representatives of the subfamily Pyroloidea feps. family Ericaceae Jus. Bull Bot Gard-Inst FEB RAS 10:27–34 (in Russian with English abstract).Google Scholar
  34. Wallace GD (2009) Pterospora. In: Flora of North America Editorial Committee (ed) Flora of North America, vol 8 Magnoliophyta: Paeoniaceae to Ericaceae. Oxford University Press, New York, pp 389–390Google Scholar
  35. Wickham H (2009) ggplot2: Elegant graphics for data analysis. Springer, New YorkCrossRefGoogle Scholar
  36. Zimmer K, Hynson NA, Gebauer G, Allen EB, Allen MF, Read DJ (2007) Wide geographical and ecological distribution of nitrogen and carbon gains from fungi in pyroloids and monotropoids (Ericaceae) and in orchids. New Phytol 175:166–175.  https://doi.org/10.1111/j.1469-8137.2007.02065.x CrossRefPubMedGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  • Kohtaroh Shutoh
    • 1
    • 2
  • Kenji Suetsugu
    • 3
  • Shingo Kaneko
    • 4
  • Takahide Kurosawa
    • 4
  1. 1.Graduate School of Symbiotic Systems Science and TechnologyFukushima UniversityFukushimaJapan
  2. 2.Faculty of EducationNiigata UniversityNiigataJapan
  3. 3.Graduate School of ScienceKobe UniversityKobeJapan
  4. 4.Faculty of Symbiotic Systems ScienceFukushima UniversityFukushimaJapan

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