Mycoheterotrophic seedling growth of Gentiana zollingeri, a photosynthetic Gentianaceae plant species, in symbioses with arbuscular mycorrhizal fungi.

Arbuscular mycorrhiza Gentiana zollingeri Gentianaceae Glomeraceae Mycoheterotrophy Paris-type AM SSU rDNA Seed packets

Journal

Journal of plant research
ISSN: 1618-0860
Titre abrégé: J Plant Res
Pays: Japan
ID NLM: 9887853

Informations de publication

Date de publication:
Sep 2021
Historique:
received: 25 01 2021
accepted: 27 04 2021
pubmed: 17 5 2021
medline: 18 8 2021
entrez: 16 5 2021
Statut: ppublish

Résumé

We found mycoheterotrophic seedling growth (initial mycoheterotrophy) of Gentiana zollingeri, a spring-flowering photosynthetic species of Gentianaceae family. Small seeds (about 300 µm in length) were buried in a habitat by using seed packets, and development of the subterranean seedlings to form shoots, more than 3 cm in length, was observed in symbiosis with arbuscular mycorrhizal (AM) fungi in the dark (i.e., underground of a field). Hyphal coils and their degenerations were observed in the root cortical cells of the subterranean seedlings as well as those of adult plants. Among the mycobionts identified on the basis of partial small subunit rDNA sequences, it was found that AM fungi of a lineage in Glomeraceae dominantly colonized, and the AM fungi were also dominant in adult individuals of G. zollingeri in three habitats separated one another by 17.2, 34.7, and 49.6 km. Though initial mycoheterotrophy in symbioses with AM fungi has been observed in some pteridophytes, this is the first study to demonstrate this type of symbiosis in a photosynthetic seed plant. The mycoheterotrophy means that an energy distribution occurs through the hyphal bridges of AM fungi among different photosynthetic seed plants, which may be important in constructing plant species diversity in some ecosystems.

Identifiants

pubmed: 33993398
doi: 10.1007/s10265-021-01311-6
pii: 10.1007/s10265-021-01311-6
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

921-931

Subventions

Organisme : Japan Society for the Promotion of Science
ID : 18H02500

Informations de copyright

© 2021. The Botanical Society of Japan.

Références

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
doi: 10.1093/nar/25.17.3389
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. https://doi.org/10.1038/nature01054
doi: 10.1038/nature01054 pubmed: 12353033
Dickson S, Smith FA, Smith SE (2007) Structural differences in arbuscular mycorrhizal symbioses: more than 100 years after Gallaud, where next? Mycorrhiza 17:375–393. https://doi.org/10.1007/s00572-007-0130-9
doi: 10.1007/s00572-007-0130-9 pubmed: 17476535
Eriksson O, Kainulainen K (2011) The evolutionary ecology of dust seeds. Perspect Plant Ecol 13:73–87. https://doi.org/10.1016/j.ppees.2011.02.002
doi: 10.1016/j.ppees.2011.02.002
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
doi: 10.1111/j.1558-5646.1985.tb00420.x pubmed: 28561359
Franke T, Beenken L, Döring M, Kocyan A, Agerer R (2006) Arbuscular mycorrhizal fungi of the Glomus-group A lineage (Glomerales; Glomeromycota) detected in myco-heterotrophic plants from tropical Africa. Mycol Prog 5:24–31. https://doi.org/10.1007/s11557-006-0500-2
doi: 10.1007/s11557-006-0500-2
Gallaud I (1905) Études sur les mycorrhizes endotrophes. Revue Générale De Botanique 17:5–48; 66–83; 123–135; 223–239; 313–325; 425–433; 479–500
Giesemann P, Rasmussen HN, Liebel HT, Gebauer G (2020) Discreet heterotrophs: green plants that receive fungal carbon through Paris-type arbuscular mycorrhiza. New Phytol 226:960–966. https://doi.org/10.1111/nph.16367
doi: 10.1111/nph.16367 pubmed: 31837155
Giesemann P, Rasmussen HN, Gebauer G (2021) Partial mycoheterotrophy is common among chlorophyllous plants with Paris-type arbuscular mycorrhiza. Ann Bot 127:645–653.  https://doi.org/10.1093/aob/mcab003
doi: 10.1093/aob/mcab003 pubmed: 33547798
Gomes SIF, Merckx VSFT, Kehl J, Gebauer G (2020) Mycoheterotrophic plants living on arbuscular mycorrhizal fungi are generally enriched in
doi: 10.1111/1365-2745.13381
Imhof S (1999) Root morphology, anatomy and mycotrophy of the achlorophyllous Voyria aphylla (Jacq.) Pers. (Gentianaceae). Mycorrhiza 9:33–39. https://doi.org/10.1007/s005720050260
doi: 10.1007/s005720050260
Imhof S, Massicotte HB, Melville LH, Peterson RL (2013) Subterranean morphology and mycorrhizal structures. In: Merckx V (ed) Mycoheterotrophy. Springer, New York, pp 157–214
doi: 10.1007/978-1-4614-5209-6_4
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
doi: 10.1093/molbev/msy096 pubmed: 29722887 pmcid: 5967553
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
doi: 10.1111/j.1469-8137.1994.tb04272.x pubmed: 33874520
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. https://doi.org/10.1111/j.1574-6941.2008.00531.x
doi: 10.1111/j.1574-6941.2008.00531.x pubmed: 18631176
McGee PA (1985) Lack of spread of endomycorrhizas of Centaurium (Gentianaceae). New Phytol 101:451–458. https://doi.org/10.1111/j.1469-8137.1985.tb02851.x
doi: 10.1111/j.1469-8137.1985.tb02851.x pubmed: 33874227
McKendrick SL, Leake JR, Taylor DL, Read DJ (2000) Symbiotic germination and development of mycoheterotrophic plants in nature: ontogeny of Corallorhiza trifida and characterization of its mycorrhizal fungi. New Phytol 145:523–537. https://doi.org/10.1046/j.1469-8137.2000.00603.x
doi: 10.1046/j.1469-8137.2000.00603.x pubmed: 33862904
Merckx V (2013) Mycoheterotrophy: an introduction. In: Merckx V (ed) Mycoheterotrophy. Springer, New York, pp 1–17
doi: 10.1007/978-1-4614-5209-6
Merckx V, Stöckel M, Fleischmann A, Bruns TD, Gebauer G (2010)
doi: 10.1111/j.1469-8137.2010.03365.x pubmed: 20618915
Merckx V, Freudenstein JV, Kissling J, Christenhusz MJM, Stotler RE, Crandall-Stotler B, Wickett N, Rudall PJ, Maas-van de Kamer H, Mass PJM (2013a) Taxonomy and classification. In: Merckx V (ed) Mycoheterotrophy. Springer, New York, pp 19–101
doi: 10.1007/978-1-4614-5209-6_2
Merckx V, Kissling J, Hentrich H, Janssens SB, Mennes CB, Specht CD, Smet EF (2013b) Phylogenetic relationships of the mycoheterotrophic genus Voyria and the implications for the biogeographic history of Gentianaceae. Am J Bot 100:712–721. https://doi.org/10.3732/ajb.1200330
doi: 10.3732/ajb.1200330 pubmed: 23535773
Mishiba K, Yamane K, Nakatsuka T, Nakano Y, Yamamura S, Abe J, Kawamura H, Takahata Y, Nishihara M (2009) Genetic relationships in the genus Gentiana based on chloroplast DNA sequence data and nuclear DNA content. Breed Sci 59:119–127. https://doi.org/10.1270/jsbbs.59.119
doi: 10.1270/jsbbs.59.119
Oostermeijer JGB, van Eijck MW, den Nijs JCM (1994) Offspring fitness in relation to population size and genetic variation in the rare perennial plant species Gentiana pneumonanthe (Gentianaceae). Oecologia 97:289–296
doi: 10.1007/BF00317317
Öpik M, Vanatoa A, Vanatoa E, Moora M, Davison J, Kalwij JM, Rejer Ü, Zobel M (2010) The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytol 188:223–241. https://doi.org/10.1111/j.1469-8137.2010.03334.x
doi: 10.1111/j.1469-8137.2010.03334.x pubmed: 20561207
Perez-Lamarque B, Selosse MA, Öpik M, Morlon H, Martos F (2020) Cheating in arbuscular mycorrhizal mutualism: a network and phylogenetic analysis of mycoheterotrophy. New Phytol 226:1822–1835. https://doi.org/10.1111/nph.16474
doi: 10.1111/nph.16474 pubmed: 32022272
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
doi: 10.1093/oxfordjournals.molbev.a040454
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
doi: 10.1016/j.tplants.2008.11.004 pubmed: 19162524
Simon LM, Lalonde TD, Bruns TD (1992) Specific amplification of 18S fungal ribosomal genes from vesicular-arbuscular endomycorrhizal fungi colonizing roots. Appl Env Microbiol 58:291–295
doi: 10.1128/aem.58.1.291-295.1992
Simpson MJA, Webb CJ (1980) Germination in some New Zealand species of Gentiana: a preliminary report. N Z J Bot 18:495–501. https://doi.org/10.1080/0028825X.1980.10425172
doi: 10.1080/0028825X.1980.10425172
Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME, Berbee ML, Bonito G, Corradi N, Grigoriev I, Gryganskyi A, James TY, O’Donnell K, Roberson RW, Taylor TN, Uehling J, Vilgalys R, White MM (2016) A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108:1028–1046. https://doi.org/10.3852/16-042
doi: 10.3852/16-042 pubmed: 27738200 pmcid: 6078412
Stevens PF (2017) Angiosperm Phylogeny Website. Version 14. [WWW document]. http://www.mobot.org/MOBOT/research/APweb/welcome.html . Accessed 14 Oct 2020.
Suetsugu K, Matsubayashi J, Ogawa NO, Murata S, Sato R, Tomimatsu H (2020a) Isotopic evidence of arbuscular mycorrhizal cheating in a grassland gentian species. Oecologia 192:929–937. https://doi.org/10.1007/s00442-020-04631-x
doi: 10.1007/s00442-020-04631-x pubmed: 32172377
Suetsugu K, Taketomi S, Tanabe AS, Haraguchi TF, Tayasu I, Toju H (2020b) Isotopic and molecular data support mixotrophy in Ophioglossum at the sporophytic stage. New Phytol 228:415–419. https://doi.org/10.1111/nph.16534
doi: 10.1111/nph.16534 pubmed: 32162317
Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17:1105–1109. https://doi.org/10.1007/BF00037152
doi: 10.1007/BF00037152 pubmed: 1932684
Winther JL, Friedman WE (2007) Arbuscular mycorrhizal symbionts in Botrychium (Ophioglossaceae). Am J Bot 94:1248–1255. https://doi.org/10.3732/ajb.94.7.1248
doi: 10.3732/ajb.94.7.1248 pubmed: 21636490
Winther JL, Friedman WE (2008) Arbuscular mycorrhizal associations in Lycopodiaceae. New Phytol 177:790–801. https://doi.org/10.1111/j.1469-8137.2007.02276.x
doi: 10.1111/j.1469-8137.2007.02276.x pubmed: 17971070
Winther JL, Friedman WE (2009) Phylogenetic affinity of arbuscular mycorrhizal symbionts in Psilotum nudum. J Plant Res 122:485–496. https://doi.org/10.1007/s10265-009-0234-8
doi: 10.1007/s10265-009-0234-8 pubmed: 19513803
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. https://doi.org/10.1007/s00572-002-0187-4
doi: 10.1007/s00572-002-0187-4 pubmed: 12466916
Yamato M, Yagame T, Iwase K (2011) Arbuscular mycorrhizal fungi in roots of non-photosynthetic plants, Sciaphila japonica and Sciaphila tosaensis (Triuridaceae). Mycoscience 52:217–223. https://doi.org/10.1007/s10267-010-0084-1
doi: 10.1007/s10267-010-0084-1

Auteurs

Masahide Yamato (M)

Faculty of Education, Chiba University, 1-33, Yayoi-cho, Inage-ku, Chiba, 263-8522, Japan. myamato@chiba-u.jp.

Takako Suzuki (T)

Graduate School of Education, Chiba University, 1-33, Yayoi-cho, Inage-ku, Chiba, 263-8522, Japan.

Mayu Matsumoto (M)

Faculty of Education, Chiba University, 1-33, Yayoi-cho, Inage-ku, Chiba, 263-8522, Japan.

Toshimi Shiraishi (T)

Faculty of Education, Chiba University, 1-33, Yayoi-cho, Inage-ku, Chiba, 263-8522, Japan.

Tomohisa Yukawa (T)

Tsukuba Botanical Garden, National Museum of Nature and Science, 4-1-1 Amakubo, Tsukuba, Ibaraki, 305-0005, Japan.

Articles similaires

Lakes Salinity Archaea Bacteria Microbiota
Rivers Turkey Biodiversity Environmental Monitoring Animals
1.00
Iran Environmental Monitoring Seasons Ecosystem Forests
1.00
Oryza Agricultural Irrigation Potassium Sodium Soil

Classifications MeSH