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Structuration Écologique Et Évolutive Des Symbioses

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Structuration Écologique Et Évolutive Des Symbioses Structuration ´ecologiqueet ´evolutive des symbioses mycorhiziennes des orchid´eestropicales Florent Martos To cite this version: Florent Martos. Structuration ´ecologiqueet ´evolutive des symbioses mycorhiziennes des or- chid´eestropicales. Biologie v´eg´etale. Universit´ede la R´eunion,2010. Fran¸cais. <NNT : 2010LARE0019>. <tel-00732894> HAL Id: tel-00732894 https://tel.archives-ouvertes.fr/tel-00732894 Submitted on 17 Sep 2012 HAL is a multi-disciplinary open access L'archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destin´eeau d´ep^otet `ala diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publi´esou non, lished or not. The documents may come from ´emanant des ´etablissements d'enseignement et de teaching and research institutions in France or recherche fran¸caisou ´etrangers,des laboratoires abroad, or from public or private research centers. publics ou priv´es. 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´ee et 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, Maˆıtre de conf´erences HDR `al’Universit´ede La R´eunion M. Marc-Andr´e Selosse, Professeur `al’Universit´ede Montpellier 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`eces d’orchid´ees actuelles 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´esence de partenaires ad´equats pour nourrir l’embryon (h´et´erotrophie) jusqu’`al’apparition des feuilles (autotrophie). Les myco- rhiziens restent pr´esents dans les racines des adultes o`u ils contribuent `ala nutrition, ce qui permet d’´etudier plus facilement la diversit´edes symbiotes `al’aide des ou- tils g´en´etiques. Conscients des biais des ´etudes en faveur des r´egions temp´er´ees, nous avons ´etudi´ela diversit´edes mycorhiziens d’orchid´ees tropicales `aLa R´eunion. Nous avons montr´eque (1) les orchid´ees tropicales ont des partenaires semblables aux orchid´ees temp´er´ees et 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 hˆotes. Nous avons aussi d´emontr´e pour la premi`ere fois que (2) les orchid´ees ´epiphytes (dont les associations ´etaient peu connues) ont des cort`eges mycorhiziens diff´erents de ceux des orchid´ees ter- restres dans les communaut´es tropicales. De plus, en d´eveloppant une approche `a l’´echelle de r´eseaux d’interactions (78 esp`eces de La R´eunion), nous avons montr´e que (3) les esp`eces tropicales ont tendance `aˆetre g´en´eralistes et que (4) le r´eseau mycorhizien des orchid´ees montre des propri´et´es semblables `acelles des r´eseaux d’interactions mutualistes (nestedness et asym´etrie d’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´ees non chlorophylliennes (mycoh´et´erotrophes) tropicales. Nous avons montr´eque (5) les esp`eces tropicales peuvent s’associer `ades champignons saprophytes qui les nourrissent en carbone issu de la d´ecomposition de la liti`ere dans les forˆets tropicales humides et que (6) les mod`eles tropicaux (en n’´etant pas sp´ecifiques) remettent en question les id´ees re¸cues sur la mycoh´et´erotrophie des plantes. Nous avons confirm´eque (7) la my- coh´et´erotrophie d´erive d’un r´egime nutritionnel interm´ediaire (mixotrophie) mis en place dans des lign´ees chlorophylliennes. Dans un dernier volet de la th`ese, nous avons pos´ela question du d´eterminisme phylog´en´etique des associations orchid´ees- champignons. En analysant la force du signal dans les phylog´enies des 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´enie des orchid´ees, et qu’elles (9) peuvent ˆetre maintenues `aune ´echelle plus r´ecente (cas de certains clades d’angraeco¨ıdes). Ces r´esultats soulignent l’empreinte relative des processus ´ecologiques et ´evolutifs sur les patrons d’associations actuels, et remettent en question l’id´ee qu’un processus de co´evolution pourrait guider le syst`eme. Mots cl´es : symbioses mycorhiziennes ; Orchidaceae ; forˆets tropicales ; ´epiphytisme ; r´eseaux d’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`ese sur les symbioses mycorhiziennes des orchid´ees de La R´eunion est 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´eunion et 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´egion R´eunion qui m’a apport´eun soutien financier durant mes trois premi`eres ann´ees de doctorat, ainsi que l’Universit´ede La R´eunion et le d´epartement de Biologie qui m’ont donn´el’opportunit´ede me former `al’enseignement sup´erieur durant ces quatre ann´ees cons´ecutives. Je remercie les membres du jury qui ont accept´ed’examiner la th`ese et 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`es comme de loin `ala r´ealisation de ce travail, `asavoir : – Thierry Pailler, mon directeur de th`ese, qui m’a incit´e`a poursuivre ma forma- tion dans la recherche en ´ecologie en Master 2 puis en Doctorat. Pour m’avoir appris `areconnaˆıtre les plantes de La R´eunion, pour nos ´echanges sur la biolo- gie et l’´ecologie des orchid´ees, et pour notre mission inoubliable `aMadagascar.
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