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M.-A. SELOSSE Muséum Nat Les orchidées et leurs mycorhizes M.-A. SELOSSE Muséum nat. d’Histoire naturelle, Paris Universités de Gdansk (Pologne) & Viçosa (Brésil) Les réseaux mycorhiziens Mycohétérotrophie et réseaux Mixotrophie et réseaux mycorhiziens La difficile transition vers l’hétérotrophie … due à un attachement fatal à la lumière ? MYCORRHIZAL SYMBIOSIS … a symbiosis between two partners ECTO- MYCORRHIZAE Asco- and Basidiomycetes on most trees in temperate regions ORCHID MYCORHIZAE Intracellular pelotons formed within root cells, usually with « rhizoctonias" (Beyrle et al. 1995) Orchid germination, usually involving rhizoctonias MYCORRHIZAL SYMBIOSIS >85% of plants associate with soil fungi Reciprocal nutrient exchanges + protection: Sugars PLANT FUNGUS Water and N, P, K Protection against soil stresses ITS BARCODING genreGenus // ordreorder NiveauTaxonomic de résolution resolution taxonomique : : espèceSpecies / / variétésub-species genetSub-species (individus) / genet ITS ITS 2 ITS 1 IGS 1 IGS 2 18 S 5.8 S 28 S 5 S 18 S Ribosomal DNA sub-unit in fungi: circa 10 kpb environ 10 kpb Les réseaux mycorhiziens Mycohétérotrophie et réseaux Mixotrophie et réseaux mycorhiziens La difficile transition vers l’hétérotrophie … due à un attachement fatal à la lumière ? Mycoheterotrophs Gentianaceae Ericaceae Polygalaceae Geosiridaceae Corsiaceae Lacandoniaceae Burmanniaceae Orchidaceae Petrosaviaceae Triuridaceae (from Brundett, 2004) Mycoheterotrophs Gentianaceae Ericaceae Polygalaceae Geosiridaceae Corsiaceae Lacandoniaceae Burmanniaceae Orchidaceae Petrosaviaceae Triuridaceae (from Brundett, 2004) Neottia nidus-avis Selosse et al., 2002, Mol. Ecol. 11, 1831 McKendrick et al., 2002, New Phytol. 145, 523 Selosse et al., 2002, New Phytol. 155, 183 ITS BARCODING genreGenus // ordreorder NiveauTaxonomic de résolution resolution taxonomique : : espèceSpecies / / variétésub-species genetSub-species (individus) / genet ITS ITS 2 ITS 1 IGS 1 IGS 2 18 S 5.8 S 28 S 5 S 18 S Ribosomal DNA sub-unit in fungi: circa 10 kpb environ 10 kpb Neottia nidus-avis associated with Sebacinales… Neottia nidus-avis associated with Sebacinales… themselves ectomycorrhizal on nearby tree roots Epipogium aphyllum … with Inocybe species Roy et al., Annals Bot., 2009. Epipogium aphyllum Epipogium aphyllum … with Inocybe species Roy et al., Annals Bot., 2009. MYCOHETEROTROPHY Exploiting the mycorrhizal network... MYCOHETERO- GREEN TROPHIC PLANT TREE FUNGUS Mycorrhizal Mycorrhizal association Carbon flow association … as reflected in their spontaneous stable isotopes (13C and 15N) abundances Mycoheterotrophs Gentianaceae Ericaceae Polygalaceae Geosiridaceae Corsiaceae Lacandoniaceae Burmanniaceae Orchidaceae Petrosaviaceae Triuridaceae (from Brundett, 2004) Mycoheterotrophic Ericaceae: Hypopitys monotropa Tedersoo et al., 2007, Oecologia Autotrophs: Arctostaphylos uva-ursi, Picea abies, Melampyrum sylvaticum Ectomycorrhizal fungi, including Tricholoma myomyces, mycorrhizal on H. monotropa Wullschlaegelia calcrata Rhizomorphs (groups of hyphae) In 14 individuals from 4 sites: only saprotrophic fungi ! Marasmius Mycena Other saprobes Gymnopus All are white rot and litter decaying fungi No strict specificity at individual level d15N ‰ 2 0 W. aphylla Green Leaf- plant decaying -2 fungi -4 -6 -34 -32 -30 -28 -26 -24 -22 13 d C ‰ Martos et al., 2009 New Phytologist 184: 668-681 Les réseaux mycorhiziens Mycohétérotrophie et réseaux Mixotrophie et réseaux mycorhiziens La difficile transition vers l’hétérotrophie … due à un attachement fatal à la lumière ? Green orchids related to Epipactis helleborine mycoheterotrophs Epipactis helleborinedistans Epipactis distansatrorubens Epipactis atrorubensmicrophylla Epipactis microphyllapalustris EpipactisAphyllorchis palustriscaudata E.g. the Neottieae tribe, Aphyllorchis caudatamontana AphyllorchisLimodorum abortivum montana mycoheterotrophy LimodorumNeottia nidus abortivum-avis arose repeatedly, by Neottia ovatanidus-avis convergent evolution NeottiaCephalanthera ovata exigua Cephalanthera austinaeexigua among green species Cephalanthera longifoliaaustinae Cephalanthera damasoniumlongifolia Roy et al., BMC Biol. 2009 … that associate with Cephalanthera rubradamasonium CephalantheraThaia saprophytica rubra ectomycorrhizal fungi ThaiaPalmorchis saprophyticasp. Palmorchis Limodorum abortivum Russula delica group Girlanda et al., Mol. Ecol., 2006 Ph. P. Pernot Cephalanthera damasonium & Cephalanthera longifolia Cephalanthera damasonium & Cephalanthera longifolia C. longifolia C. damasonium Julou et al., 2005 Abadie et al., 2006 2 3 2 5 10 5 34 19 6 11 19 « Rhizoctonias » Ectomycorhizal fungi Saprophytes Plant endophytes or parasites Epipactis microphylla Diverse ectomycorrhizal fungi, mainly truffles spp. Pernot Selosse et al., Microb. Ph. P. Ph. P. Ecol., 2006 Epipactis microphylla associates with truffles x 800 Microscopy and antibodies demon- strate that truffles are mycorrhizal (Selosse et al., 2006 x 1 700 Microbial. Ecol.) Tedersoo et al., 2007, Oecologia « Green » orchids: Listera ovata, Platanthera bifolia, Epipactis atrorubens MIXOTROPHY Exploiting both the mycorrhizal network & photosynthesis... MYCOHETERO- GREEN TROPHIC PLANT TREE FUNGUS Mycorrhizal Mycorrhizal association Carbon flow association … as reflected in their 13C &15N abundances Limodorum abortivum A green orchid photosynthesizing below the compensation point light dark 0 1 2 CO2 produced 3 mol.m -2.s-1 Girlanda et al., Mol. Ecol., 2006 In mixotrophic orchid species, achlophyllous variants, the albinos, … survive as mycoheterotrophs! Cephalanthera damasonium (P. Pernot & F. Dusak) Epipactis purpurata (A. Hasenfratz) A. Soulié M. Roy J.C. Claessens S. Acker Gas exchange in C. damasonium Net CO2 exchange green albino PAR = photosynthetic active radiations Julou et al. 2005, New Phytol. IsotopesC. longifolia in (C.Abadie longifolia et al., 2006) green albino green Green autotrophic plants Abadie et al. 2006, Botany Some green plants - are mixotrophic and use mycorrhizal networks - are predisposed to evolve mycohetero- trophy - … with albinos as transitions? Gebauer & Meyer, 2003 Bidartondo et al., 2005 Selosse & Roy, 2009 Some green plants - are mixotrophic and use mycorrhizal networks - are predisposed to evolve mycohetero- trophy - … with albinos as transitions? Selosse & Roy, 2009 Some green plants - are mixotrophic and use mycorrhizal networks - are predisposed to evolve mycohetero- trophy - … with albinos as transitions? Selosse & Roy, 2009 Les réseaux mycorhiziens Mycohétérotrophie et réseaux Mixotrophie et réseaux mycorhiziens La difficile transition vers l’hétérotrophie … due à un attachement fatal à la lumière ? Many mutation could abolish greenness, yet albinos remain very rare in mixotrophic orchid populations… Why then? Roy et al. 2013, Ecol. Monographs 83: 95–117 A 4–year monitoring of two Cephalanthera damasonium populations, with 20-70 albinos Dormancy… Year n n+1 n+2 dormancy Dormancy: more frequent! Year n n+1 n+2 % of dormant individuals in 2007 12 10 8 6 4 dormancy 2 0 n=110 n=850 n=35 n=46 Montferrier Boigneville Albinos were 16.5x more often dormant than green individuals Shoot survival… Number of shoots Apparition Flowering time of shoots Shoot survival: lower! Number of shoots % shoots dried in late June 2007 60 50 40 30 20 10 0 51% albino shoots dry in June (vs 7% for green ones) > no seeds! Seed production and quality: lower… Number of seeds % of seeds germinating in situ per fruits (x10) in seeds pockets (3 months) 100 100 *** 1400 *** 90 90 1200 80 80 70 70 1000 ns 60 60 800 50 50 600 40 40 30 30 400 20 20 200 10 10 0 0 0 n=7200nombre n=22800 de n=7200 %n=22800 fertilité %n=3960 germination% fertilité n=10800 % germination graines 3 x 3 less viable seeds in albinos! Comparison green ind. / albinos Patterns of dormancy 6.8x more Patterns of shoot survival 16.5x less Seed production 9x less = 103 x lower fitness Roy et al. 2013, Ecol. Monographs 83: 95–117 Comparison green ind. / albinos Patterns of dormancy 6.8x more Patterns of shoot survival 16.5x less Seed production 9x less = 103 x lower fitness WHY DID ALBINOS FAIL THE TRANSITION ? Les réseaux mycorhiziens Mycohétérotrophie et réseaux Mixotrophie et réseaux mycorhiziens La difficile transition vers l’hétérotrophie … due à un attachement fatal à la lumière ? Allocation of mycoheterotrophic C versus photosynthetic C in mixotrophic orchids based on δ13C (and N content) Allocation of fungal versus photosynthetic C In shoots Shoot C nutrition over the growth season in C. damasonium -22 δ13C (‰) -24 Albinos (enriched in 13C) -26 -28 C. vitalba -30 Autotrophs (depleted -32 R. peregrina in 13C) -34 Growth Mar 23 Apr 12 May 02 May 22 Jun 11 Jul 01 03/26 04/27 05/11 05/24 06/26 season First leaves All leaves First Flowers Ripen opened flowers pollinated fruits Shoot C nutrition over the growth season in C. damasonium -22 δ13C (‰) -24 Albinos -26 Green individuals -28 C. vitalba -30 Autotrophs -32 R. peregrina -34 Growth Mar 23 Apr 12 May 02 May 22 Jun 11 Jul 01 03/26 04/27 05/11 05/24 06/26 season First leaves All leaves First Flowers Ripen opened flowers pollinated fruits A shift from 80% heterotrophic to 20% at fruiting! -22 δ13C (‰) -24 Albinos -26 Green individuals -28 C. vitalba -30 Autotrophs -32 R. peregrina -34 Growth Mar 23 Apr 12 May 02 May 22 Jun 11 Jul 01 03/26 04/27 05/11 05/24 06/26 season First leaves All leaves First Flowers Ripen opened flowers pollinated fruits A shift from 100% heterotrophic to 20% in E. helleborine Albinos Hypopitys monotropa C. mayalis Green individuals Autotrophs S. virgaurea
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