Transcript Gene Loss and Organelle Genome Evolution

Gene Loss and Organelle
Genome Evolution
Level 3 Molecular Evolution and
Bioinformatics
Jim Provan
References
Race HL, Herrmann RG, Martin W (1999) “Why have
organelles retained genomes?” Trends in Genetics
15: 364-370
Lang BF, Gray MW, Burger G (1999) “Mitochondrial
genome evolution and the origin of eukaryotes”
Annual Review of Genetics 33: 351-397
Gene loss in early organelle evolution
Rickettsia prowazeki
(1,111kb - 834 genes)
Synechocystis sp.
(3,573kb - 3000 genes)
Reclinomonas americana mtDNA
(69kb - 97 genes)
Porphyra purpurea cpDNA
(201kb - 250 genes)
Types of genes in organelles and
their ancestors
160
140
120
100
80
60
40
20
0
Synechocystis
Plastids
Rickettsia
Mitochondria
Genes encoded in plastid genomes
Electron transport / related processes Gene expression
PSII
Cyt b6
PSI
ATPase CO2 fix
Synechocystis
25
8
12
9
Any plastid genome
All plastid genomes
16
13
7
2
12
4
8
5
Other Total
RNA pol
rRNA
24
12
53
3025 3168
2
1
4
3
48
16
159
2
2569
46
Evolution of the spc (spectinomycin)
operon
L14
E. coli
H. influenzae
B. subtilis
Synechocystis
P. purpurea
O. sinensis
C. paradoxa
M. polymorpha
N. tabacum
L24
L5
S14
S8
L6
L18
S5
L30
L15
Where did the genes go?
Obsolete genes eliminated early on:
Nucleotide, lipid and amino acid biosynthesis genes not found in
mitochondria
Still found in some chloroplasts: ancient mitochondrial genomes
may exist which contain these genes cf. Porphyra vs. angiosperm
chloroplasts
Takeover of corresponding function by nuclear genes:
Protozoan Paramecium mtDNA contains only three tRNA genes
To translate all codons, tRNAs are imported from cytosol
The mitochondrial RNA polymerase
Most eukaryote mtDNAs
use a nucleus-encoded
single-subunit polymerase
similar to T3/T7 phages
Jakobid protists J. libera
and R. americana mtDNA
contains genes for multisubunit RNA polymerase
like that in bacteria
Original RNA polymerase
has been superseded by
phage-like enzyme
Phylogeny of green algae
Chlorophyceae
Chlorophyta
Trebouxiophyceae
Ulvophyceae
Charophyceae
Embryophyta
Charales
Streptophyta
Prasinophyceae
Closest relatives to land
plants (Embryophyta) are
Charophyceae
Complete chloroplast DNA
sequence available for
Trebouxiophyte Chlorella
Green algae chloroplast
structure highly variable
 difficult to predict
ancestral structure
Nephroselmis olivacea chloroplast
structure
Quadripartite structure:
92,126bp LSC
16,399bp SSC
46,137bp IR
IRs also found in:
Cyanophora
Odontella
Guillardia
Land plants (mostly)
but not in:
Chlorella
Porphyra
Nephroselmis olivacea gene content
Total of 127 genes: largest among green lineage:
Marchantia - 120; Chlorella - 111; Euglena - 85
May represent “primitive” green plastid
Seven genes not found in other green chloroplasts:
rnpB, trnS(cga), ftsW, rne, ycf62 found in non-green algae
ycf81 and ftsI found in bacteria
ftsW and ftsI involved in formation of peptidoglycan:
—
—
Cell wall only found in glaucocystophyte Cyanophora
May be more prevalent than first thought
Ten subunits of NADH:ubiquinone oxidoreductase:
ndh genes found in four of five land plants
Pseudogenes in Pinus - transferred to nucleus
Nephroselmis olivacea gene content
Atypical codon usage and AT-composition:
Suggests that majority of IR has been gained by lateral
transfer
Also noted in green alga Chlamydomonas
No introns cf. Porphyra, Odontella and Guillardia:
Suggests ancestral plastid genome contained very few
introns
Intron proliferation seems to be a feature of higher plants
trnL intron in Chlorella seems to have been vertically
transmitted from cyanobacteria:
—
—
Found in Cyanophora
Found in plants
Phylogenetic position of
Nephroselmis chloroplasts
Nicotiana
*
Marchantia
*
Chlamydomonas
*
Chlorella
*
Euglena
*
Nephroselmis
Porphyra
*
Guillardia
Odontella
Cyanophora
Synechocystis
Tree based on 37 cpDNA
proteins
Agrees with 18S-rRNA
(nuclear) phylogenies
Nephroselmis represents
basal branch of Chlorophyta
Euglena included in
Chlorophyta
Patterns of gene loss in chloroplast
genomes
Euglena
(85)
chlB
chlL
chlN
cysA
cysT
psaM
rpl21
ycf12
ycf66
R(ccg)
Chlorella
(111)
Nicotiana
rpl22
accD
ccsA
cemA
chlB
chlL
chlN
clpP
cysA
cysT
ftsI
ftsW
ndhA
ndhB
ndhC
ndhD
(111)
rps16
Marchantia
ftsH
infA
minD
minE
petA
petD
petL
psaI
psbM
ndhE
ndhF
ndhG
ndhH
ndhI
ndhK
rpl19
rpoA
ycf1
ycf3
I(gau)
L(gag)
S(gga)
T(ggu)
R(ccg)
rne
rmpB
ycf6
ycf62
ycf81
S(cga)
Nephroselmis
(127)
(120)
chlI
ftsI
ftsW
minD
minE
rne
rnpB
rpl5
rpl12
rpl19
rps9
tufA
ycf62
ycf81
L(gag)
S(cga)
Ancestral
Green Alga
(137)
ndhJ
rpl21
rpl33
rps15
rps16
ycf66
V(gac)
minE
psaM
rpl22
Gene partitioning
All but one genes located in single-copy regions in
Nephroselmis are found in corresponding region in
Marchantia:
Exception is trnL(UAG)
Suggests that ancestral green algal plastid genome had IR
Some genes adjacent to IR in Marchantia have been
“subsumed” into the IR in Nephroselmis
In smaller region delineated by rRNA operons (cf. SSC),
only four of thirteen genes have been transferred to
large region (cf. LSC) between “red” / “green” lineages:
Suggests that transfer between LSC and SSC regions is rare
Further evidence for single origin of all plastid genomes