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Primary endosymbiosis: have cyanobacteria and Chlamydiae ever been roommates?

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Deschamps P.

Acta Societatis Botanicorum Poloniae

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2014

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tom 83

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nr 4

Eukaryotes acquired the ability to process photosynthesis by engulfing a cyanobacterium and transforming it into a genuine organelle called the plastid. This event, named primary endosymbiosis, occurred once more than a billion years ago, and allowed the emergence of the Archaeplastida, a monophyletic supergroup comprising the green algae and plants, the red algae and the glaucophytes. Of the other known cases of symbiosis between cyanobacteria and eukaryotes, none has achieved a comparable level of cell integration nor reached the same evolutionary and ecological success than primary endosymbiosis did. Reasons for this unique accomplishment are still unknown and difficult to comprehend. The exploration of plant genomes has revealed a considerable amount of genes closely related to homologs of Chlamydiae bacteria, and probably acquired by horizontal gene transfer. Several studies have proposed that these transferred genes, which are mostly involved in the functioning of the plastid, may have helped the settlement of primary endosymbiosis. Some of these studies propose that Chlamydiae and cyanobacterial symbionts coexisted in the eukaryotic host of the primary endosymbiosis, and that Chlamydiae provided solutions for the metabolic symbiosis between the cyanobacterium and the host, ensuring the success of primary endosymbiosis. In this review, I present a reevaluation of the contribution of Chlamydiae genes to the genome of Archaeplastida and discuss the strengths and weaknesses of this tripartite model for primary endosymbiosis.

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The Glaucophyta: the blue-green plants in a nutshell

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Jackson C., Clayden S., Reyes-Prieto A.

Acta Societatis Botanicorum Poloniae

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2015

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tom 84

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nr 2

The Glaucophyta is one of the three major lineages of photosynthetic eukaryotes, together with viridiplants and red algae, united in the presumed monophyletic supergroup Archaeplastida. Glaucophytes constitute a key algal lineage to investigate both the origin of primary plastids and the evolution of algae and plants. Glaucophyte plastids possess exceptional characteristics retained from their cyanobacterial ancestor: phycobilisome antennas, a vestigial peptidoglycan wall, and carboxysome-like bodies. These latter two traits are unique among the Archaeplastida and have been suggested as evidence that the glaucophytes diverged earliest during the diversification of this supergroup. Our knowledge of glaucophytes is limited compared to viridiplants and red algae, and this has restricted our capacity to untangle the early evolution of the Archaeplastida. However, in recent years novel genomic and functional data are increasing our understanding of glaucophyte biology. Diverse comparative studies using information from the nuclear genome of Cyanophora paradoxa and recent transcriptomic data from other glaucophyte species provide support for the common origin of Archaeplastida. Molecular and ultrastructural studies have revealed previously unrecognized diversity in the genera Cyanophora and Glaucocystis. Overall, a series of recent findings are modifying our perspective of glaucophyte diversity and providing fresh approaches to investigate the basic biology of this rare algal group in detail.

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Contrasting patterns in the evolution of the Rab GTPase family in Archaeplastida

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Petrzelkova R., Elias M.

Acta Societatis Botanicorum Poloniae

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2014

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tom 83

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nr 4

Rab GTPases are a vast group of proteins serving a role of master regulators in membrane trafficking in eukaryotes. Previous studies delineated some 23 Rab and Rab-like paralogs ancestral for eukaryotes and mapped their current phylogenetic distribution, but the analyses relied on a limited sampling of the eukaryotic diversity. Taking advantage of the recent growth of genome and transcriptome resources for phylogenetically diverse plants and algae, we reanalyzed the evolution of the Rab family in eukaryotes with the primary plastid, collectively constituting the presumably monophyletic supergroup Archaeplastida. Our most important novel findings are as follows: (i) the ancestral set of Rabs in Archaeplastida included not only the paralogs Rab1, Rab2, Rab5, Rab6, Rab7, Rab8, Rab11, Rab18, Rab23, Rab24, Rab28, IFT27, and RTW (=Rabl2), as suggested previously, but also Rab14 and Rab34, because Rab14 exists in glaucophytes and Rab34 is present in glaucophytes and some green algae; (ii) except in embryophytes, Rab gene duplications have been rare in Archaeplastida. Most notable is the independent emergence of divergent, possibly functionally novel, in-paralogs of Rab1 and Rab11 in several archaeplastidial lineages; (iii) recurrent gene losses have been a significant factor shaping Rab gene complements in archaeplastidial species; for example, the Rab21 paralog was lost at least six times independently within Archaeplastida, once in the lineage leading to the “core” eudicots; (iv) while the glaucophyte Cyanophora paradoxa has retained the highest number of ancestral Rab paralogs among all archaeplastidial species studied so far, rhodophytes underwent an extreme reduction of the Rab gene set along their stem lineage, resulting in only six paralogs (Rab1, Rab2, Rab6, Rab7, Rab11, and Rab18) present in modern red algae. Especially notable is the absence of Rab5, a virtually universal paralog essential for the endocytic pathway, suggesting that endocytosis has been highly reduced or rewired in rhodophytes.

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A contemplation on the secondary origin of green algal and plant plastids

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Kim E., Maruyama S.

Acta Societatis Botanicorum Poloniae

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2014

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tom 83

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nr 4

A single origin of plastids and the monophyly of three “primary” plastid-containing groups – the Chloroplastida (or Viridiplantae; green algae+land plants), Rhodophyta, and Glaucophyta – are widely accepted, mainstream hypotheses that form the basis for many comparative evolutionary studies. This “Archaeplastida” hypothesis, however, thus far has not been unambiguously confirmed by phylogenetic studies based on nucleocytoplasmic markers. In view of this as well as other lines of evidence, we suggest the testing of an alternate hypothesis that plastids of the Chloroplastida are of secondary origin. The new hypothesis is in agreement with, or perhaps better explains, existing data, including both the plastidal and nucleocytoplasmic characteristics of the Chloroplastida in comparison to those of other groups.

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Monophyly of Archaeplastida supergroup and relationships among its lineages in the light of phylogenetic and phylogenomic studies. Are we close to a consensus?

84%

Mackiewicz P., Gagat P.

Acta Societatis Botanicorum Poloniae

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2014

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tom 83

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nr 4

One of the key evolutionary events on the scale of the biosphere was an endosymbiosis between a heterotrophic eukaryote and a cyanobacterium, resulting in a primary plastid. Such an organelle is characteristic of three eukaryotic lineages, glaucophytes, red algae and green plants. The three groups are usually united under the common name Archaeplastida or Plantae in modern taxonomic classifications, which indicates they are considered monophyletic. The methods generally used to verify this monophyly are phylogenetic analyses. In this article we review up-to-date results of such analyses and discussed their inconsistencies. Although phylogenies of plastid genes suggest a single primary endosymbiosis, which is assumed to mean a common origin of the Archaeplastida, different phylogenetic trees based on nuclear markers show monophyly, paraphyly, polyphyly or unresolved topologies of Archaeplastida hosts. The difficulties in reconstructing host cell relationships could result from stochastic and systematic biases in data sets, including different substitution rates and patterns, gene paralogy and horizontal/endosymbiotic gene transfer into eukaryotic lineages, which attract Archaeplastida in phylogenetic trees. Based on results to date, it is neither possible to confirm nor refute alternative evolutionary scenarios to a single primary endosymbiosis. Nevertheless, if trees supporting monophyly are considered, relationships inferred among Archaeplastida lineages can be discussed. Phylogenetic analyses based on nuclear genes clearly show the earlier divergence of glaucophytes from red algae and green plants. Plastid genes suggest a more complicated history, but at least some studies are congruent with this concept. Additional research involving more representatives of glaucophytes and many understudied lineages of Eukaryota can improve inferring phylogenetic relationships related to the Archaeplastida. In addition, alternative approaches not directly dependent on phylogenetic methods should be developed.

Ograniczanie wyników

5 Acta Societatis Botanicorum Poloniae

1 Clayden S.

1 Deschamps P.

1 Elias M.

1 Gagat P.

1 Jackson C.

1 Kim E.

1 Mackiewicz P.

1 Maruyama S.

1 Petrzelkova R.

1 Reyes-Prieto A.

1 2015

4 2014

Primary endosymbiosis: have cyanobacteria and Chlamydiae ever been roommates?

The Glaucophyta: the blue-green plants in a nutshell

Contrasting patterns in the evolution of the Rab GTPase family in Archaeplastida

A contemplation on the secondary origin of green algal and plant plastids

Monophyly of Archaeplastida supergroup and relationships among its lineages in the light of phylogenetic and phylogenomic studies. Are we close to a consensus?