Acquisition of cyanobacterial genes in green/red plant genomes
http://mbe.oxfordjournals.org/cgi/content/abstract/25/4/748?etoc
Genes of Cyanobacterial Origin in Plant Nuclear Genomes Point to a
Heterocyst-Forming Plastid Ancestor
Oliver Deusch*, Giddy Landan
, Mayo Roettger*, Nicole
Gruenheit*, Klaus V. Kowallik*,
John F. Allen
, William Martin* and
Tal Dagan*
Plastids are descended from a cyanobacterial symbiosis which occurred
over 1.2 billion years ago. During the course of endosymbiosis, most
genes were lost from the cyanobacterium's genome and many were
relocated to the host nucleus through endosymbiotic gene transfer
(EGT). The issue of how many genes were acquired through EGT
in different plant lineages is unresolved. Here, we report the
genome-wide frequency of gene acquisitions from cyanobacteria in
4 photosynthetic eukaryotes—Arabidopsis, rice, Chlamydomonas,
and the red alga Cyanidioschyzon—by comparision of the
83,138 proteins encoded in their genomes with 851,607 proteins
encoded in 9 sequenced cyanobacterial genomes, 215 other reference
prokaryotic genomes, and 13 reference eukaryotic genomes. The
analyses entail 11,569 phylogenies inferred with both
maximum likelihood and Neighbor-Joining approaches. Because
each phylogenetic result is dependent not only upon the
reconstruction method but also upon the site patterns in
the underlying alignment, we investigated how the
reliability of site pattern generation via alignment
affects our results: if the site patterns in an alignment
differ depending upon the order in which amino acids are
introduced into multiple sequence alignment—N- to C-terminal
versus C- to N-terminal—then the phylogenetic result is
likely to be artifactual. Excluding unreliable alignments by
this means, we obtain a conservative estimate, wherein about 14%
of the proteins examined in each plant genome indicate a cyanobacterial
origin for the corresponding nuclear gene, with higher
proportions (17–25%) observed among the more reliable alignments.
The identification of cyanobacterial genes in plant genomes
affords access to an important question: From which type of
cyanobacterium did the ancestor of plastids arise? Among the
9 cyanobacterial genomes sampled, Nostoc sp. PCC7120 and Anabaena
variabilis ATCC29143 were found to harbor collections of
genes which are—in terms of presence/absence and sequence similarity—more
like those possessed by the plastid ancestor than those
of the other 7 cyanobacterial genomes sampled here. This
suggests that the ancestor of plastids might have been an
organism more similar to filamentous, heterocyst-forming (nitrogen-fixing)
representatives of section IV recognized in Stanier's
cyanobacterial classification. Members of section IV are
very common partners in contemporary symbiotic associations involving
endosymbiotic cyanobacteria, which generally provide nitrogen
to their host, consistent with suggestions that fixed nitrogen
supplied by the endosymbiont might have played an important role
during the origin of plastids.
Key Words: endosymbiosis • phylogenomics • multiple
sequence alignment • plastid origin • nitrogen