Structuration Écologique Et Évolutive Des Symbioses Mycorhiziennes Des

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Structuration Écologique Et Évolutive Des Symbioses Mycorhiziennes Des Universit´ede La R´eunion { Ecole´ doctorale Sciences Technologie Sant´e{ Facult´edes Sciences et des Technologies Structuration ´ecologique et ´evolutive des symbioses mycorhiziennes des orchid´ees tropicales Th`ese de doctorat pr´esent´eeet soutenue publiquement le 19 novembre 2010 pour l'obtention du grade de Docteur de l'Universit´ede la R´eunion (sp´ecialit´eBiologie des Populations et Ecologie)´ par Florent Martos Composition du jury Pr´esidente: Mme Pascale Besse, Professeur `al'Universit´ede La R´eunion Rapporteurs : Mme Marie-Louise Cariou, Directrice de recherche au CNRS de Gif-sur-Yvette M. Raymond Tremblay, Professeur `al'Universit´ede Porto Rico Examinatrice : Mme Pascale Besse, Professeur `al'Universit´ede La R´eunion Directeurs : M. Thierry Pailler, Ma^ıtre de conf´erences HDR `al'Universit´ede La R´eunion M. Marc-Andr´e Selosse, Professeur `al'Universit´ede Montpellier Laboratoire d'Ecologie´ Marine Institut de Recherche pour le D´eveloppement 2 R´esum´e Les plantes n'exploitent pas seules les nutriments du sol, mais d´ependent de champignons avec lesquels elles forment des symbioses mycorhiziennes dans leurs racines. C'est en particulier vrai pour les 25 000 esp`ecesd'orchid´eesactuelles qui d´ependent toutes de champignons mycorhiziens pour accomplir leur cycle de vie. Elles produisent des graines microscopiques qui n'ont pas les ressources nutritives pour germer, mais qui d´ependent de la pr´esencede partenaires ad´equatspour nourrir l'embryon (h´et´erotrophie)jusqu’`al'apparition des feuilles (autotrophie). Les myco- rhiziens restent pr´esents dans les racines des adultes o`uils contribuent `ala nutrition, ce qui permet d'´etudierplus facilement la diversit´edes symbiotes `al'aide des ou- tils g´en´etiques.Conscients des biais des ´etudesen faveur des r´egionstemp´er´ees, nous avons ´etudi´ela diversit´edes mycorhiziens d'orchid´eestropicales `aLa R´eunion. Nous avons montr´eque (1) les orchid´eestropicales ont des partenaires semblables aux orchid´eestemp´er´eeset m´editerran´eennes(Sebacinales, Ceratobasidiaceae et sur- tout Tulasnellaceae), et que ces taxons de champignons sont largement repr´esent´es dans diff´erents biomes et dans diff´erentes plantes h^otes.Nous avons aussi d´emontr´e pour la premi`erefois que (2) les orchid´ees´epiphytes (dont les associations ´etaient peu connues) ont des cort`egesmycorhiziens diff´erents de ceux des orchid´eester- restres dans les communaut´estropicales. De plus, en d´eveloppant une approche `a l'´echelle de r´eseauxd'interactions (78 esp`ecesde La R´eunion),nous avons montr´e que (3) les esp`ecestropicales ont tendance `a^etreg´en´eralisteset que (4) le r´eseau mycorhizien des orchid´eesmontre des propri´et´essemblables `acelles des r´eseaux d'interactions mutualistes (nestedness et asym´etried'interaction), alors que la na- ture mutualiste de cette symbiose mycorhizienne fait d´ebat. Dans un second volet de la th`ese,nous avons ´etudi´eles partenaires des orchid´eesnon chlorophylliennes (mycoh´et´erotrophes)tropicales. Nous avons montr´eque (5) les esp`ecestropicales peuvent s'associer `ades champignons saprophytes qui les nourrissent en carbone issu de la d´ecomposition de la liti`eredans les for^etstropicales humides et que (6) les mod`elestropicaux (en n'´etant pas sp´ecifiques)remettent en question les id´ees re¸cuessur la mycoh´et´erotrophiedes plantes. Nous avons confirm´eque (7) la my- coh´et´erotrophied´erive d'un r´egimenutritionnel interm´ediaire(mixotrophie) mis en place dans des lign´eeschlorophylliennes. Dans un dernier volet de la th`ese,nous avons pos´ela question du d´eterminismephylog´en´etiquedes associations orchid´ees- champignons. En analysant la force du signal dans les phylog´eniesdes deux parte- naires, nous avons v´erifi´eque (8) les associations mycorhiziennes sont peu conserv´ees `al'´echelle supra-g´en´erique dans la phylog´eniedes orchid´ees,et qu'elles (9) peuvent ^etremaintenues `aune ´echelle plus r´ecente (cas de certains clades d'angraeco¨ıdes). Ces r´esultatssoulignent l'empreinte relative des processus ´ecologiqueset ´evolutifs sur les patrons d'associations actuels, et remettent en question l'id´eequ'un processus de co´evolution pourrait guider le syst`eme. Mots cl´es : symbioses mycorhiziennes ; Orchidaceae ; for^etstropicales ; ´epiphytisme ; r´eseauxd'interactions ; nestedness ; signal phylog´en´etique; co´evolution ; mycoh´et´ero- trophie ; La R´eunion; Cara¨ıbes ; Japon. 4 Abstract Plants generally do not exploit soil nutrients themselves, but they depend upon mycorrhizal symbioses with root-associating fungi. This is the case for the current 25,000 orchid species that depend on the development of a mycorrhizal association to germinate and establish. They produce minute seeds lacking nutritional ressources required to germinate, so that they depend on the presence of suitable fungal part- ners to obtain carbon (heterotrophy) until the development of leaves (autotrophy). Mycorrhizal fungi remain present in the roots of adult plants where they contribute to the plant nutrition, which makes the molecular identification of fungal partners easier. Given the fact that most studies have been conducted in temperate regions, we have studied the diversity of mycorrhizal fungi in tropical orchids of La R´eunion. We have found that (i) tropical orchids have the same partners as temperate and me- diterranean orchids (Sebacinales, Ceratobasidiaceae, and above all Tulasnellaceae), and that these fungi are widespread in biomes and host plants. We have also showed for the first time that (ii) epiphytic orchids|that have hardly been studied|have partners that differ from terrestrial orchids' in tropical plant communities. Moreover, by developing an interaction network approach (78 species of La R´eunion),we have found that (iii) most tropical species are generalists and that (iv) the mycorrhizal network shows the same properties as the mutualistic interaction networks' (nes- tedness and interaction asymmetry), whereas the mutualistic nature of the orchid symbiosis is still a current issue. In the second part of our thesis, we have studied the fungal partners of achlorophyllous (i.e. mycoheterotrophic) tropical orchids. We have found that (v) tropical species often associate with saprophytic fungi that pro- vide carbon extracted from decaying wood or leaves in tropical soils, and that (vi) tropical models, because of their lack of specificity, challenge the rule drawn from temperate models. We have also confirmed in tropical models that (vii) mycohete- rotrophy evolved from mixotrophic ancestors (i.e. intermediate nutritional mode). In the last part of our thesis, we have dealt with the influence of orchid and fungal phylogenies in explaining the structure of the observed networks. By measuring the phylogenetic signals in both orchid and fungal phylogenies, we have checked that (viii) mycorrhizal interactions are not explained by the phylogenetic placements of either orchid genera or fungal taxa. However, we have noticed that (ix) a phyloge- netic signal can occur in recent clades of orchid species (but not in fungal species). These results provide insights in the relative imprint of ecological and evolutionnary processes on the current patterns of fungus-orchid associations, and challenge the idea that the coevolutionary process could drive the system. Keywords : mycorrhizal symbioses ; Orchidaceae ; tropical forests ; epiphytism ; inter- action networks ; nestedness ; phylogenetic signal ; coevolution ; mycoheterotrophy ; La R´eunion; West Indies ; Japan. 6 Remerciements Cette th`esesur les symbioses mycorhiziennes des orchid´eesde La R´eunionest n´ee d'une collaboration r´ecente entre deux ´equipes de recherches : l'UMR C53 Peuple- ments V´eg´etauxet Bioagresseurs en Milieu Tropical (PVBMT) de l'Universit´ede La R´eunionet l'UMR CNRS 5175 Centre d'Ecologie´ Fonctionnelle et Evolutive´ (CEFE) de Montpellier. Je tiens avant tout `aremercier les personnes qui ont contribu´e`ala mise en place de cette collaboration, en particulier Bernard Reynaud (Directeur de l'UMR PVBMT), Dominique Strasberg (Directeur adjoint de l'UMR PVBMT), et Martine Hossaert-McKey (Responsable de l'´equipe Interactions Biotiques de l'UMR CEFE). Je remercie la R´egionR´eunionqui m'a apport´eun soutien financier durant mes trois premi`eresann´eesde doctorat, ainsi que l'Universit´ede La R´eunionet le d´epartement de Biologie qui m'ont donn´el'opportunit´ede me former `al'enseignement sup´erieur durant ces quatre ann´eescons´ecutives. Je remercie les membres du jury qui ont accept´ed'examiner la th`eseet qui ont fait le d´eplacement jusqu’`aLa R´eunion. J'adresserais enfin des remerciements `atitre personnel `atous ceux qui ont contribu´e de pr`escomme de loin `ala r´ealisationde ce travail, `asavoir : { Thierry Pailler, mon directeur de th`ese,qui m'a incit´e`apoursuivre ma forma- tion dans la recherche en ´ecologieen Master 2 puis en Doctorat. Pour m'avoir appris `areconna^ıtreles plantes de La R´eunion,pour nos ´echanges sur la biolo- gie et l'´ecologiedes orchid´ees,et pour notre mission inoubliable `aMadagascar. J'esp`ereque nous aurons encore l'occasion de collaborer sur les orchid´eesde la zone Oc´eanIndien ; { Marc-Andr´eSelosse, mon co-directeur de th`ese,qui m'a fait confiance en ac- ceptant de co-encadrer ce travail depuis Montpellier. Pour m'avoir transmis ta passion pour les symbioses, les champignons et les orchid´ees\moches" ! Pour m'avoir accueilli chez toi lors de mes passages `aMontpellier, et pour les nom- breuses fois o`utu as su te rendre disponible malgr´ela
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