Origin and spread of chlorophyll-c containing plastids, and the early

Dans le document A phylogenomic contribution to the eukaryotic tree of life (Page 133-136)

A recurrent issue of our work concerns the evolution of plastids. Although we have not investigated plastid evolution per se, the new phylogenetic relationships we described have important implications. In particular, we discussed the role that Rhizaria, telonemids, and centrohelids have now to play for untangling the much debated question of the spread of chlorophyll-c containing plastids (almost amusingly, in fact, as such plastids have never been reported in either groups). Central to this debate is the chromalveolate hypothesis [Cavalier-Smith 1999], and passionate discussions about whether chromalveolate plastids do have a common origin through a single endosymbiotic event will go on until unifying evi-dences are provided (see for instance the recent exchange [Bodyl et al. 2009; Lane and Archibald 2009]). A crucial point is that the consequences of plastid loss versus plastid gain for a cell are generally not well understood, yet the chromalveolate hypothesis requires a large number of losses. New data are thus needed, and only a combined effort of many forces is likely to help in evaluating further these questions. Genomics will be crucial, for example by looking for traces of an ancient photosynthetic activity (identification of plastid derived relict genes, possible evidence for plastid targeting or even a plastid genome) in modern-day non-photosynthetic lineages related to autotrophic ones. The improbable dis-covery of new key species, such as the recently characterized Chromera velia [Moore et al. 2008], could also bring decisive answers by filling evolutionary gaps. Finally, advanced biochemical and ultrastructural analyses of similarities and differences of plastid features will be of primary interest to better define the origin(s) of red plastids. In this context, robust phylogenetic trees provide evolutionary frameworks that are essential to rule out incompatible hypotheses.

Hence, it should be stressed that, for the time being, no one really knows how the plastids of red-algal origin spread among eukaryotes. A unique secondary endosymbiosis followed by numerous losses (what is postulated by the chromalveolate hypothesis) could be correct, of course, but we believe it should not be taken as the a priori correct sce-nario. Figure 1-ch.7 describes a new framework for eukaryote evolution, summarizing our work and also taking into account results of others (e.g., [Hackett et al. 2007]). This tree is compatible with the chromalveolate hypothesis because it represents the phylogenetic rela-tionships among the host cells and all species with chlorophyll-c containing plastids share a common ancestor, although, differently from the original description [Cavalier-Smith 1999], our tree displays a much expanded assemblage also containing Rhizaria, telonemids,

cen-is correct, it does not necessarily imply that the chromalveolate scheme cen-is the true scenario for red plastid evolution and other valid alternatives are totally possible.

Figure 1-ch.7. The new tree of eukaryotes, resulting from a consensus of our and other’s work. The position of the root is unknown, but between Unikonts and the rest of the major groups (here called

“bikonts” for simplicity), as shown on this tree, is a reasonable possibility. Within bikonts excavates are probably early diverging, followed by a megagroup composed of Plantae and two groups that could be most closely related to each other: CCTH (centrohelids, cryptomonads, telonemids, hapto-phytes, but also katablepharids and biliphytes) and SAR (stramenopiles, alveolates and Rhizaria).

CCTH and SAR are colored to emphasise our contribution to the emergence of these assemblages, but also to stress the importance of this new evolutionary framework to understand the evolution of plas-tids. Colored branches correspond to photosynthetic groups (or mostly photosynthetic), and are color-coded according to plastid pigmentation. Broken colored branches means that cryptic plastids were found in these lineages, but photosynthesis was lost. Numbers in grey circles represent possible events of primary, secondary, and tertiary endosymbioses (dinoflagellates apart). Mapped on this tree are two hypotheses that both explain the current distribution of chlorophyll-c containing plastids: the chromalveolate hypothesis [Cavalier-Smith 1999] and the hypothesis of Sanchez-Puerta and Delwiche [Sanchez-Puerta and Delwiche 2008], represented by the red and blue curved dashed arrows, respec-tively. Other scenarios have been proposed but are not shown here [Bodyl et al. 2009]. Spread of sec-ondary plastids of green algal origin is not shown. Question marks in grey circles correspond to possi-ble timings for our proposition of ancestral “capacitation” to establish plastids: the shopping bag model for plastid origin [Howe et al. 2008] could have taken place very early on.

For example, an alternative model of plastid evolution that have been recently pro-posed is mapped on the schematized tree in Figure 1-ch.7 [Sanchez-Puerta and Delwiche 2008]. This model accommodates several new pieces of information such as the existence of the SAR group (i.e. Rhizaria are within the chromalveolates, yet they do not have red plastids) [Burki et al. 2007; Hackett et al. 2007] or the HGT of the rpl36 gene [Rice and

Palmer 2006]. It involves a single secondary endosymbiosis with a red alga during the evo-lution of cryptomonads and haptophytes, and one or two tertiary endosymbioses (some dinoflagellate lineages aside) during the evolution of stramenopiles and alveolates. However, given the uncertainties of the phylogenetic relationships we now showed within the CCTH group, and the numerous uninvestigated early diverging stramenopile and alveolate linea-ges, it is not possible for the moment to be more precise on the timing of plastid acquisi-tions in such scenarios. Multiple tertiary endosymbioses are also invoked in another model that explain the distribution of red algal-derived plastids by serial transfers, the authors insisting that plastid losses should not be favored over plastid gains [Bodyl et al. 2009].

In order to eliminate hypotheses that are inconsistent with a robust phylogeny, a cru-cial point that remains to be strongly demonstrated for understanding the current distribu-tion of red plastids is the posidistribu-tion of the CCTH group. Our lastest results showed a sister relationship to SAR (chapter 6), but this group has proven unstable, in particular several studies recovered a close relationship with the Plantae [Patron et al. 2007; Burki et al.

2008; Hampl et al. 2009]. If the latter position gets convincing support in future studies, even when all potential artifacts are demonstrably removed, it would indeed invalidate the chromalveolate scenario because a secondary red algal plastid would then need to have been present before red algae ever originated.

More generally, the association of the SAR and CCTH groups with Plantae into a

“megagroup” of eukaryotes, regardless of the relationships among these assemblages, con-tributes to the debate on the origin and evolution of eukaryotic photosynthesis. In chapter 5, we have speculated that the last common ancestor of this clade could have transmitted an increased capability to its descendants to establish plastids (no photosynthetic species are found within unikonts), resulting in an early split in eukaryote evolution with funda-mentally different properties in each part of the tree (Figure 1-ch.7). In that sense our view is quite consistent with the shopping bag model for the origin of plastids [Howe et al.

2008]. It seems indeed possible that in this last common ancestor (or even earlier, in the ancestor that also gave rise to excavates), the early stages of establishment of a durable endosymbiosis involved a process of unsuccessful attempts, where the stable symbiont ul-timately acquired by the host cell was not the first one it ever acquired; it could have been preceded by the continuous uptake of photosynthetic organisms that, for some at least, persisted for some time within the host (kleptoplasty could be an example of such an evolutionary stage). During this process, endosymbiont DNA could have been transferred and integrated into the nuclear genome, providing a pool of sequences of symbiont origin

occasions (following models that have yet to be clarified, see above). Importantly, these plastid acquisitions would have been facilitated by the earlier transferred genes from the former endosymbionts (those that preceded primary plastid gain). Alternatively, primary plastids could have been established even earlier, lost and later replaced by secondary and tertiary plastids (except in Plantae which preserved primary plastids). Dinoflagellates could be a much more recent example that follows the same evolutionary pattern, with an ap-parent “facility” in replacing plastids, providing evidence in support of this hypothetical scheme [Tengs et al. 2000; Nosenko et al. 2006; Gould et al. 2008].

7.3 A molecular time-scale for eukaryote evolution: combining

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