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The single, ancient origin of chromist plastids
Abstract
Abstract Algae include a diverse array of photosynthetic eukaryotes excluding land plants. Explaining the origin of algal plastids continues to be a major challenge in evolutionary biology. Current knowledge suggests that plastid primary endosymbiosis, in which a single-celled protist engulfs and “enslaves” a cyanobacterium, likely occurred once and resulted in the primordial alga. This eukaryote then gave rise through vertical evolution to the red, green, and glaucophyte algae. However, some modern algal lineages have a more complicated evolutionary history involving a secondary endosymbiotic event, in which a protist engulfed an existing eukaryotic alga (rather than a cyanobacterium), which was then reduced to a secondary plastid. Secondary endosymbiosis explains the majority of algal biodiversity, yet the number and timing of these events is unresolved. Here we analyzed a five-gene plastid data set to show that a taxonomically diverse group of chlorophyll c2-containing protists comprising cryptophyte, haptophyte, and stramenopiles algae (Chromista) share a common plastid that most likely arose from a single, ancient (≈1,260 million years ago) secondary endosymbiosis involving a red alga. This finding is consistent with Chromista monophyly and implicates secondary endosymbiosis as an important force in generating eukaryotic biodiversity.
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  • References (2)
  • Cited By (283)
  • References (2)
  • Cited By (283)
Michael W. Gray65
Estimated H-index: 65
(Dalhousie University)
Publisher Summary This chapter highlights endosymbiont hypothesis. All contemporary genomes (including those of plastids and mitochondria) ultimately derive from a single genome—the genome of a single, presumably cellular, entity which was the ancestor of all surviving forms of live. The construction and interpretation of phylogenetic trees based on small subunit (SSU, or 16S-like) and large subunit (LSU, or 23S-like) rRNA sequences have proven especially informative in instances where morpholog...
461 Citations Source Cite
1997
Debashish Bhattacharya63
Estimated H-index: 63
D. Bhattacharya, An introduction to algal phylogeny and phylogenetic methods * S. Turner, Molecular systematics of oxygenic photosynthetic bacteria * C.F. Delwiche, J.D. Palmer, The origin of plastids and their spread via secondary symbiosis * T. Friedl, The evolution of the Green Algae * V.A.R. Huss, H.D. Kranz, Charophyte evolution and the origin of land plants * G.W. Saunders, G.T. Kraft, A molecular perspective on red algal evolution: focus on the Florideophycidae * D. Bhattacharya, H.A. Sch...
77 Citations Source Cite
1998 in NatureIF: 41.58
William Martin79
Estimated H-index: 79
(University of Düsseldorf),
Bettina Stoebe6
Estimated H-index: 6
(Braunschweig University of Technology)
+ 3 AuthorsKlaus V. Kowallik17
Estimated H-index: 17
(Braunschweig University of Technology)
Photosynthetic eukaryotes, particularly unicellular forms, possess a fossil record that is either wrought with gaps or difficult to interpret, or both. Attempts to reconstruct their evolution have focused on plastid phylogeny, but were limited by the amount and type of phylogenetic information contained within single genes1, 2, 3, 4, 5. Among the 210 different protein-coding genes contained in the completely sequenced chloroplast genomes from a glaucocystophyte, a rhodophyte, a diatom, a eugleno...
604 Citations Source Cite
1999 in NatureIF: 41.58
Zhaoduo Zhang5
Estimated H-index: 5
,
Beverley R. Green39
Estimated H-index: 39
,
Thomas Cavalier-Smith68
Estimated H-index: 68
Photosynthetic dinoflagellates are important aquatic primary producers and notorious causes of toxic 'red tides', Typical dinoflagellate chloroplasts differ from all other plastids in having a combination of three envelope membranes' and peridinin-chlorophyll a/c light-harvesting pigments 2 . Despite evidence of a dinoflagellete satellite DNA containing chloroplast genes 3 , previous attempts to obtain chloroplast gene sequences have been uniformly unsuccessful. Here we show that the dinoflagell...
270 Citations Source Cite
1997 in BioEssaysIF: 4.42
Paul R. Gilson19
Estimated H-index: 19
(University of Melbourne),
Geoffrey I. McFadden59
Estimated H-index: 59
(University of Melbourne)
Chlorarachniophytes are amoeboflagellate, marine protists that have acquired photosynthetic capacity by engulfing and retaining a green alga. These green algal endosymbionts are severely reduced, retaining only the chloroplast, nucleus, cytoplasm and plasma membrane. The vestigial nucleus of the endosymbiont, called the nucleomorph, contains only three small linear chromosomes and has a haploid genome size of just 380 kb - the smallest eukaryotic genome known. Initial characterisation of nucleom...
42 Citations Source Cite
Juan F. Saldarriaga11
Estimated H-index: 11
(University of British Columbia),
F.J.R. Taylor2
Estimated H-index: 2
(University of British Columbia)
+ 1 AuthorsThomas Cavalier-Smith68
Estimated H-index: 68
(University of Oxford)
Dinoflagellates are a trophically diverse group of protists with photosynthetic and non-photosynthetic members that appears to incorporate and lose endosymbionts relatively easily. To trace the gain and loss of plastids in dinoflagellates, we have sequenced the nuclear small subunit rRNA gene of 28 photosynthetic and four non-photosynthetic species, and produced phylogenetic trees with a total of 81 dinoflagellate sequences. Patterns of plastid gain, loss, and replacement were plotted onto this ...
253 Citations Download PDF Cite
Guan Zhu19
Estimated H-index: 19
,
Janet S. Keithly15
Estimated H-index: 15
(New York State Department of Health),
Hervé Philippe18
Estimated H-index: 18
(University of Paris)
The phylogenetic position of Cryptosporidium is elusive. Although previous studies based solely upon small-subunit (SSU) rRNA sequences suggested that the genus was an early emerging lineage among the Apicomplexa, bootstrap support for this placement was low. Here, the phylogenetic position of Cryptosporidium has been re-evaluated for SSU rRNA, fused SSU/large-subunit (LSU) rRNA and six protein sequences using traditional distance-based neighbour-joining, maximum-parsimony and maximum-likelihood...
80 Citations Source Cite
  • References (2)
  • Cited By (283)
Jinling Huang20
Estimated H-index: 20
(East Carolina University),
Johann Peter Gogarten19
Estimated H-index: 19
(University of Connecticut)
20 Citations Source Cite
2006 in AlgaeIF: 1.56
Reyes-Prieto Adrian1
Estimated H-index: 1
,
Hwan-Su Yoon1
Estimated H-index: 1
,
Debashish Bhattacharya63
Estimated H-index: 63
Genomic data is accumulating in public database at an unprecedented rate. Although presently dominated by the sequences of metazoan, plant, parasitic, and picoeukaryotic taxa, both expressed sequence tag (EST) and complete genomes of free-living algae are also slowly appearing. This wealth of information offers the opportunity to clarify many long-standing issues in algal and plant evolution such as the contribution of the plastid endosymbiont to nuclear genome evolution using the tools of compa...
16 Citations Source Cite
Wriddhiman Ghosh10
Estimated H-index: 10
,
Prabir Kumar Haldar1
Estimated H-index: 1
+ 3 AuthorsMasrure Alam5
Estimated H-index: 5
Source Cite
2007
J. Kenneth Hoober24
Estimated H-index: 24
(Arizona State University)
7 Citations Source Cite
2010
Azúa-Bustos Armando1
Estimated H-index: 1
(Pontifical Catholic University of Chile),
Vicuña Rafael2
Estimated H-index: 2
(Pontifical Catholic University of Chile)
Caves represent an interesting habitat for searching life in extreme environments, since they offer a stable protected environment from harsh and changing outside prevailing conditions. Here we report that in a coastal cave of the hyperarid Atacama Desert, a member of the ancient eukaryote red algae Cyanidium group was found forming a seemingly monospecific biofilm growing under extremely low photon flux levels. Our work suggests that this species, Cyanidium sp. Atacama, is a new member of a rec...
2 Citations Source Cite
Thomas Mock29
Estimated H-index: 29
(University of East Anglia),
Linda Medlin15
Estimated H-index: 15
(Centre national de la recherche scientifique)
Abstract Diatoms are unicellular eukaryotes with nano-patterned silica cell walls and they contribute about 20% of global primary production. Their beautiful shells and significance for life on our planet already caused scientific interest many centuries ago. However, the development of genetics and genomics-enabled technology about two decades ago and their application to diatom research has caused a step change in our understanding of diatom evolution, biology and ecology. In contrast to plant...
11 Citations Source Cite
2011
Linda Medlin15
Estimated H-index: 15
(Centre national de la recherche scientifique)
The diatoms are, without doubt, one of the most successful groups of unicellular algae and contribute significantly to the global carbon cycle. They arose within the heterokont lineage no earlier than 250 Ma. The radiation of the pigmented heterokonts and that of the haptophytes and dinoflagellates was likely a response to the Permian–Triassic (PT) extinction event when host cells with a red algal endosymbiont had an adaptive advantage. There are three major clades of diatoms, which have been fo...
10 Citations Source Cite
2010
Hwan Su Yoon19
Estimated H-index: 19
(Bigelow Laboratory For Ocean Sciences),
Giuseppe C. Zuccarello25
Estimated H-index: 25
(Victoria University of Wellington),
Debashish Bhattacharya63
Estimated H-index: 63
(Rutgers University)
The red algae (Rhodophyta) form a distinct photosynthetic eukaryotic lineage that consists of around 6,000 species including unicellular to large multicellular taxa (http://www.algaebase.org/). The red algae are unique among eukaryotes in lacking both flagella and centrioles during their entire life cycle (Gabrielson et al., 1990; Graham and Wilcox, 2000). Pit connections, pit plugs, and a triphasic life cycle that are mostly found in the Florideophyceae are also distinguishing characters of the...
19 Citations Download PDF Cite
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