Ultrastructure of symbiotic germination of the orchid Dendrobium officinale with its mycobiont, Sebacina sp.
J. Chen A C , H. Wang A C , S. S. Liu A , Y. Y. Li A and S. X. Guo A B
+ Author Affiliations
- Author Affiliations
A Institute of Medicinal Plant Development, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100193, P.R. China.
B Corresponding author. Email: sxguo1986@163.com
C These authors contributed equally to this work.
Australian Journal of Botany 62(3) 229-234 https://doi.org/10.1071/BT14017
Submitted: 30 January 2014 Accepted: 8 June 2014 Published: 2 July 2014
Abstract
Dendrobium officinale is an endangered epiphytic orchidaceous medicinal plant. Similar to other orchid plants, the seed germination of D. officinale under natural conditions depends nutritionally upon mycorrhizal fungi. The compatible fungi have been isolated from D. officinale protocorms using in situ seed baiting technique in our previous studies. However, the interaction between seed germination of D. officinale and its mycobiont is still unclear. In the present study, we investigated the morphological changes of seed and fungus during the symbiotic germination using a light microscope and transmission electron microscope. Seeds of D. officinale have no conspicuous suspensor cells. The fungus enters into the embryo cell through the posterior end of the embryo and colonises the cortical cell in the first stage of germination (Stage 1). Then, the hyphae form pelotons with the protocorm development (Stages 1–3). After protocorm formation, the reinvaded fungal hyphae conspicuously decrease. Invaded hyphae lose bioactivity, form clumps and start degeneration at Stage 4 or 5 (seedling development). When penetrating the neighbouring cortical cell, the fungal hyphae constrict to collar shape at the contacted site and follow by swelling in the apex. Our study suggested that fungi trigger protocorm development and concomitant reserve utilisation during the symbiotic germination.
Additional keywords: mycorrhizal association, orchidaceae, seed germination.
References
Arditti J (1967) Factors affecting the germination of orchid seeds. Botanical Review 33, 1–97.| Factors affecting the germination of orchid seeds.Crossref | GoogleScholarGoogle Scholar |
Burgeff H (1959) Mycorrhiza of orchids. In ‘The orchids: a scientific survey’. (Ed. CL Withner) pp. 361–395. (Ronald Press: New York)
Chen J, Wang H, Guo SX (2012) Isolation and identification of endophytic and mycorrhizal fungi from seeds and roots of Dendrobium (Orchidaceae). Mycorrhiza 22, 297–307.
| Isolation and identification of endophytic and mycorrhizal fungi from seeds and roots of Dendrobium (Orchidaceae).Crossref | GoogleScholarGoogle Scholar | 21779810PubMed |
Fan L, Guo SX, Xiao PG (2001) Interaction between Gastrodia elata (Orchidaceae) and Mycena anoectochila during seed germination. Mycosystema 20, 539–546.
Genre A, Chabaud M, Timmers T, Bonfante P, Barkerb DG (2005) Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. The Plant Cell 17, 3489–3499.
| Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlersL3P&md5=dc22d38de6968723cc06bf9592a21ac4CAS | 16284314PubMed |
Genre A, Ivanov S, Fendrych M, Faccio A, Žárskŷ V, Bisseling T, Bonfante P (2012) Multiple exocytotic markers accumulate at the sites of perifungal membrane biogenesis in arbuscular mycorrhizas. Plant & Cell Physiology 53, 244–255.
| Multiple exocytotic markers accumulate at the sites of perifungal membrane biogenesis in arbuscular mycorrhizas.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XosFGgtw%3D%3D&md5=dd518fed784ad0da7524479fadf9481eCAS |
Guo SX, Xu JT (1990a) Studies on the cell ultrastructure in the course of Gastrodia elata digesting Mycena osmundicola Lange and Armillaria mellea Fr. Acta Mycologica Sinica 9, 218–225.
Guo SX, Xu JT (1990b) Studies on the changes of cell ultrastructure in the course of seed germination of Bletilla striata under fungus infection conditions. Acta Botanica Sinica 32, 594–598.
Hadley G (1982) Orchid mycorrhiza. In ‘Orchid biology: review and perspectives II’. (Ed. J Arditti) pp. 81–118. (Cornell University Press: New York)
Hadley G, Williamson B (1971) Analysis of the post-infection growth stimulus in orchid mycorrhiza. New Phytologist 70, 445–455.
| Analysis of the post-infection growth stimulus in orchid mycorrhiza.Crossref | GoogleScholarGoogle Scholar |
Harrison M (1999) Molecular and cellular aspects of the arbuscular mycorrhizal symbiosis. Annual Review of Plant Physiology and Plant Molecular Biology 50, 361–389.
| Molecular and cellular aspects of the arbuscular mycorrhizal symbiosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkt1yksbs%3D&md5=2cd7af88eff6dcc313ef71221a5ad4a8CAS | 15012214PubMed |
Hashimoto Y, Fukukawa S, Kunishi A, Suga H, Richard F, Sauve M, Selosse MA (2012) Mycoheterotrophic germination of Pyrola asarifolia dust seeds reveals convergences with germination in orchids. New Phytologist 195, 620–630.
| Mycoheterotrophic germination of Pyrola asarifolia dust seeds reveals convergences with germination in orchids.Crossref | GoogleScholarGoogle Scholar | 22642263PubMed |
Martos F, Munoz F, Pailler T, Kottke I, Gonneau C, Selosse M (2012) The role of epiphytism in architecture and evolutionary constraint within mycorrhizal networks of tropical orchid. Molecular Ecology 21, 5098–5109.
| The role of epiphytism in architecture and evolutionary constraint within mycorrhizal networks of tropical orchid.Crossref | GoogleScholarGoogle Scholar | 22765763PubMed |
Peterson RL, Currah RS (1990) Synthesis of mycorrhizae between protocorms of Goodyera repens (Orchidaceae) and Ceratobasidium cereale. Canadian Journal of Botany 68, 1117–1125.
| Synthesis of mycorrhizae between protocorms of Goodyera repens (Orchidaceae) and Ceratobasidium cereale.Crossref | GoogleScholarGoogle Scholar |
Peterson RL, Bonfante P, Faccio A, Uetake Y (1996) The interface between fungal hyphae and orchid protocorm cells. Canadian Journal of Botany 74, 1861–1870.
| The interface between fungal hyphae and orchid protocorm cells.Crossref | GoogleScholarGoogle Scholar |
Peterson RL, Uetake Y, Zelmer C (1998) Fungal symbioses with orchid protocorms. Symbiosis 25, 29–55.
Pharmacopoeia Committee of the P.R. China (2005) ‘Pharmacopoeia of the People’s Republic of China. Vol. 1.’ (People’s Medical Publishing House: Beijing)
Purves S, Hadley G (1976) The physiology of symbiosis in Goodyera repent. New Phytologist 77, 689–696.
| The physiology of symbiosis in Goodyera repent.Crossref | GoogleScholarGoogle Scholar |
Rasmussen HN (1995) ‘Terrestrial orchids, from seed to mycotrophic plant.’ (Cambridge University Press: Cambridge, UK)
Rasmussen HN, Rasmussen FN (2009) Orchid mycorrhiza: implications of mycophagous life style. Oikos 118, 334–345.
| Orchid mycorrhiza: implications of mycophagous life style.Crossref | GoogleScholarGoogle Scholar |
Richardson KA, Peterson RL, Currah RS (1992) Seed reserves and early symbiotic protocorm development of Platanthera hyperborea (orchidaceae). Canadian Journal of Botany 70, 291–300.
| Seed reserves and early symbiotic protocorm development of Platanthera hyperborea (orchidaceae).Crossref | GoogleScholarGoogle Scholar |
Selosse MA, Boullard B, Richardson D (2011) Noël Bernard (1874–1911): orchids to symbiosis in a dozen years, one century ago. Symbiosis 54, 61–68.
| Noël Bernard (1874–1911): orchids to symbiosis in a dozen years, one century ago.Crossref | GoogleScholarGoogle Scholar |
Smith SE, Read DJ (2008) ‘Mycorrhizal symbiosis.’ 3rd edn. (Academic Press: San Diego, CA)
Stewart SL, Zettler LW (2002) Symbiotic germination of three semiaquatic rein orchids quinqueseta, H. macroceratitis) from Florida. Aquatic Botany 72, 25–35.
| Symbiotic germination of three semiaquatic rein orchids quinqueseta, H. macroceratitis) from Florida.Crossref | GoogleScholarGoogle Scholar |
Takemoto D, Hardham A (2004) The cytoskeleton as a regulator and target of biotic interactions in plants. Plant Physiology 136, 3864–3876.
| The cytoskeleton as a regulator and target of biotic interactions in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtVamsA%3D%3D&md5=8f02612c8ca04ad83793bd2e05c1ca76CAS | 15591444PubMed |
Těšitelová T, Těšitel J, Jersáková A (2012) Symbiotic germination capability of four Epipactis species (Orchidaceae) is broader than expected from adult ecology. American Journal of Botany 99, 1020–1032.
| Symbiotic germination capability of four Epipactis species (Orchidaceae) is broader than expected from adult ecology.Crossref | GoogleScholarGoogle Scholar | 22688426PubMed |
Uetake Y, Peterson L (1998) Association between microtubules and symbiotic fungal hyphae in protocorm cells of the orchid species, Spiranthes sinensis. New Phytologist 140, 715–722.
| Association between microtubules and symbiotic fungal hyphae in protocorm cells of the orchid species, Spiranthes sinensis.Crossref | GoogleScholarGoogle Scholar |
Uetake Y, Kobayashi K, Ogoshi A (1992) Ultrastructural changes during the symbiotic development of Spiranthes sinensis (Orchidaceae) protocorms associated with binucleate Rhizoctonia anastomosis group C. Mycological Research 96, 199–209.
| Ultrastructural changes during the symbiotic development of Spiranthes sinensis (Orchidaceae) protocorms associated with binucleate Rhizoctonia anastomosis group C.Crossref | GoogleScholarGoogle Scholar |
Uetake Y, Earquhar ML, Peterson RL (1997) Changes in microtubule arrays in symbiotic orchid protocorms during fungal colonization and senescence. New Phytologist 135, 701–709.
| Changes in microtubule arrays in symbiotic orchid protocorms during fungal colonization and senescence.Crossref | GoogleScholarGoogle Scholar |
Wang H, Fang HY, Wang YQ, Duan LS, Guo SX (2011) In situ seed baiting techniques in Dendrobium officinale Kimuraet Migo and Dendrobium nobile Lindl.: the endangered Chinese endemic Dendrobium (Orchidaceae). World Journal of Microbiology & Biotechnology 27, 2051–2059.
| In situ seed baiting techniques in Dendrobium officinale Kimuraet Migo and Dendrobium nobile Lindl.: the endangered Chinese endemic Dendrobium (Orchidaceae).Crossref | GoogleScholarGoogle Scholar |
Xu JT, Mou C, Ran YZ (1990) Cytological observation on hyphae invading Mycena osmundicola in the process of seed germination of Gastrodia elata Bl. Acta Academiae Medicinae Sinicae 12, 315–317.
Yagame T, Funabiki E, Nagasawa E, Fukiharu T, Iwase K (2013) Identification and symbiotic ability of Psathyrellaceae fungi isolated from a photosynthetic orchid, Cremastra appendiculata (Orchidaceae). American Journal of Botany 100, 1823–1830.
| Identification and symbiotic ability of Psathyrellaceae fungi isolated from a photosynthetic orchid, Cremastra appendiculata (Orchidaceae).Crossref | GoogleScholarGoogle Scholar | 24026354PubMed |
Yam TW, Arditti J (2009) History of orchid propagation: a mirror of the history of biotechnology. Plant Biotechnology Report 3, 1–56.
| History of orchid propagation: a mirror of the history of biotechnology.Crossref | GoogleScholarGoogle Scholar |
