Russian Journal of Genetics, Vol. 41, No. 9, 2005, pp. 957–967. Translated from Genetika, Vol. 41, No.

9, 2005, pp. 1170–1182.

Original Russian Text Copyright © 2005 by Odintsova, Yurina.

THEORETICAL PAPERS
AND REVIEWS

Genomics and Evolution of Cellular Organelles*

M. S. Odintsova and N. P. Yurina
Bach Institute of Biochemistry, Russian Academy of Sciences, Moscow, 119071 Russia;
e-mail: nyurina@inbi.ras.ru
Received December 7, 2004

Abstract—The structure, functions, and evolution of cellular organelles are reviewed. The mitochondrial
genomes of eukaryotes differ considerably in size and structural organization mainly due to the length variation
in noncoding regions and the presence of introns. The mitochondrial genomes of angiosperms are the largest
and most complicated. Gene content in eukaryotic mitochondrial genomes is similar. They usually encode all
types of rRNA, a complete or partial complement of tRNA, and a limited number of proteins essential for mito-
chondrial functions. In all eukaryotes studied, mitochondrial genomes code for two highly hydrophobic pro-
teins involved in respiration, cytochrome b and subunit 1 of cytochrome oxidase. Genome structure and gene
content in plastids, mainly in higher plant chloroplasts, are highly conserved. Plastid genomes of algae are more
variable in gene composition and contain several unique genes absent in the chloroplast DNA of higher plants.
Plastid genomes encode proteins involved in transcription and translation, as well as proteins of the photosyn-
thetic apparatus. Both types of cellular organelles are supposed to be of endosymbiotic origin. Modern plastids
originate from a cyanobacterial ancestor. Alpha-proteobacteria, especially the most mitochondrion-like rickett-
sia, gave rise to mitochondria. The origin of plastids of higher plants and green algae as a result of primary endo-
symbiosis and that of other algal lineages by secondary endosymbiosis are briefly discussed.

* MITOCHONDRION GENOMICS ecules have been described in a few unrelated organ-

Mitochondria, cellular organelles responsible for
respiration, use electron transport coupled with oxida-
tive phosphorylation to generate ATP. Although mito-
chondria play a key role in energy transduction, they
also participate in other important processes, such as
ion homeostasis and apoptosis. Mitochondria are ubiq-
uitous in eukaryotes with very few exceptions. Some
“amitochondriate” eukaryotes contain derived mito-
chondria (e.g., hydrogenosomes), which produce ATP
anaerobically. Other amitochondriate species possess
remnant mitochondrial structures of currently unknown
functions [1]. However, for mitochondrial functions not
only the components encoded by the mitochondrial
genome (mitochondrial DNA, mtDNA) are necessary.
Many mitochondrial proteins are nuclear-encoded, and
their transcripts are synthesized in cytosol and trans-
ported to the organelles.
mtDNAs of most eukaryotes are circular super-
coiled molecules. Mitochondrial genomes usually con-
sist of a single “chromosome”; however, multiple circu-
lar molecules have been reported for the chytridio-
mycete fungus Spizellomyces punctatus, the Globodera
nematodes [2], and the Dicyema mesozoan animals [3].
A complex structural organization of the mitochondrial
genome has been reported for kinetoplastid protists
(e.g., Trypanosoma) [4]. Their mitochondrion contains
a few dozen of gene-containing maxicircles and several
thousands minicircles encoding guide RNAs involved
in mRNA editing [5]. Linear monomeric mtDNA mol-
* This article was translated by the authors.
isms, such as ciliates (Paramecium and Tetrahymena),
apicomplexa (Plasmodium and related organisms),
coelenterates (Hydra), fungi (Hansenula mrakii and
Candida rhagii), and green algae (Chlamydomonas
reinhardtii) [6]. These linear molecules have specific
end-structures, such as covalently closed single-
stranded DNA termini or covalently attached proteins,
in addition, they tend to form telomere-like repeats of
various length [1]. An unusual mitochondrial genome
has been detected in the protist Amoebidium parasiti-
cum, it is a complex assemblage of several hundred lin-
ear DNA molecules, which carry at their termini similar
short sequences of about 40 bp (repx) in inverted orien-
tation followed internally by an ~100-bp repeat (repa)
at one end and a different ~65-bp repeat (repb) at the
other end [7, 8].
mtDNA structure differs essentially not only
between eukaryotic kingdoms, but also within each
kingdom (Animalia, Plantae, Fungi, and Protista) as
well. The size of mtDNA varies more than 150-fold:
from 14.3 kb in the nematode Ascaris suum to 2400 kb
in the melon Cucumis melo [9]. Among the completely
sequenced genomes, the smallest genome (6 kb) was
found in apicomplexan protists (Plasmodium sp.), the
largest (490 kb) genome, which is ~80 times larger than
that of Plasmodium, was detected in the angiosperm
Oryza sativa. A large 366.924-kb mitochondrial
genome was described for a flowering plant Arabidop-
sis thaliana [10]; it constitutes about 1/3 of the genome
size of the mitochondria-related bacterium Rickettsia
prowazekii (1111.5 kb) [9].

1022-7954/05/4109-0957 © 2005 Pleiades Publishing, Inc.

958 ODINTSOVA, YURINA
Animal mtDNAs are small circular molecules
(about 13–19 kb) representing a population of
covalently linked circular monomers, concatameric
dimers, and oligomers. Large mtDNA molecules (20–
42 kb) were detected in mollusks, nematodes, and
insects. Angiosperms possess the largest and most com-
plex mitochondrial genomes, with the smallest mtDNA
of 208 kb in Brassica hirta. This value exceeds the larg-
est of Agaricus bitorquis (176 kb) and the size of most
chloroplast DNAs (cpDNAs). The size of the mito-
chondrial genome in different plant species differs
more than ten fold and may differ four fold even within
the same family. Plant mtDNA has many noncoding
sequences (>80% in mtDNA of Arabidopsis and <10%
in mtDNA of protists) [11] and possesses direct recom-
binationally active repeats and multiple short dispersed
repeats. Genes are dispersed throughout the genome
and usually do not form clusters. Only in rare cases, the
coding sequences are located close to each other and
are probably cotranscribed.
In summary, significant differences in mtDNA size
in different groups of eukaryotes are mostly caused by
the presence or absence of introns and variations in the
length of intergenic regions, which in some instances,
consist of multiple tandem-repeat arrays or stem–loop
motifs. Some of the repeat elements are supposed to be
mobile [12]. A characteristic feature of the plant mito-
chondrial genome is the presence of nucleotide
sequences of other cellular genomes, especially those
of chloroplasts. The length of cpDNA stretches and
their nucleotide composition may differ among plant
species. The occurrence of split genes contributes con-
siderably to the size of mtDNA. The size of introns in
mtDNA varies from 0.15 to 4.0 kb. The number of
introns is also variable: from 0 to >30. In the filamen-
tous fungus Podospora anserine, introns account for
about 75% of the overall size of mtDNA [1].
Another feature of the mitochondrial genomes is
gene fusion. In two amoeboid protists, Acanthamoeba
castellannii and Dictyostelium discoideum, the genes
encoding subunits 1 and 2 of cytochrome oxidase (cox1
and cox2, respectively) are immediately adjacent to one
another and form a single ORF. Another example of
unusual gene structure, genes that exist in pieces, was
first described for the ciliate protozoan Tetrahymena
pyriformis and the green alga Chlamydomonas rein-
hardtii. These genes exist as fragments dispersed over
the genome and interspersed with other genes and are
located on both strands of the mtDNA. Separate tran-
scription of subgenic fragments leads to the formation
of discrete rRNA segments that are held together by
base pairing of the complementary sequences. Pieces of
rRNA genes were found in Plasmodium falciparum. In
mtDNA, some protein-coding genes also occur in
pieces. In two ciliate species, Tetrahymena pyriformis
and Paramecium aurelia, the nad1 gene is split into two
fragments that are transcribed into two mRNAs and
translated into two polypeptides. Posttranslational
fusion of these polypeptides was suggested [13]. In the
RUSSIAN JOURNAL OF GENETICS
green alga Scenedesmus obliquus, subunit 2 of cyto-
chrome oxidase is encoded by two gene fragments: the
sequence coding for the N-terminal part is located on
the mtDNA, while the C-terminal part of the protein is
supposed to be nuclear-encoded. In the green algae
Chlamydomonas and Polytomella, two portions of the
protein are encoded by different nuclear genes, synthe-
sized in the cytoplasm, and imported into the mitochon-
dria. The rpl2 gene of flowering plants is another exam-
ple of split genes: one portion of the gene is located on
the mtDNA, and the other one, on the nuclear DNA. In
mtDNAs of some animals, protists, and fungi, trun-
cated genes (e.g., tRNA, rRNA, RNAse P, and some
protein-coding genes) were discovered. Thus, in the
Harpochytrium fungus, the protein-encoding genes are
often shortened in the C-terminal part of the molecule
[1, 14, 15].
Gene transfer to the nucleus that is quite common in
flowering plants, the loss of introns, and the elimination
of intergenic spacers reduce the size of mitochondrial
genomes.
The number of mtDNA copies per cell varies from
ten to several thousands. There is no correlation
between genome size and the number of mitochondrial
genes. Animal mtDNA genes are densely located usu-
ally on both DNA strands. Spacers are short and usually
consist of several base pairs. In rare instances, genes
overlap. In multicellular animals (Metazoa), the com-
plements of mitochondrial genes are nearly identical.
The animal mitochondrial genes usually lack introns.
The members of Cnidaria are the only exception. Thus,
in the class Anthozoa including marine anemones and
some coral species, one or two group I introns have
been discovered. In human mtDNA, densely “packed”
genes have no introns, while nuclear genes are rich in
introns separated by long intergenic spacers. Con-
versely, yeast mtDNA genes are rich in introns and sep-
arated by long spacers, while the yeast nuclear DNA is
compact and lack introns. This observation means that
the coding capacity and gene density in nuclear and
mitochondrial genomes of the same organism evolved
independently [8]. Unicellular organisms related to ani-
mals, such as the colonial flagellate Monosiga brevicol-
lis and the protist Amoebidium parasiticum, which
belongs to Cnidosporidia, have large mitochondrial
genomes and carry much more genes than mtDNA of
multicellular animals. This means that compaction of
mitochondrial genomes in multicellular organisms
appeared not in protists but simultaneously with the origin
of the multicellular body plan in the animal lineage [8].
The uniformity of animal mitochondrial genomes is
in contrast with the situation in plants, fungi, and pro-
tists (amoebae, flagellates and algae). mtDNAs of
plants and protists are usually considerably larger and
code for much more proteins than animal mtDNA.
Among mtDNAs studied, the mitochondrial genome of
the flagellate Reclinomonas americana is especially
gene-rich. Its circular mtDNA molecule consists of
Vol. 41 No. 9 2005
 GENOMICS AND EVOLUTION OF CELLULAR ORGANELLES
70 kb and contains approximately 100 genes, which is
several orders of magnitude higher than in animal
mtDNA. Only five genes were identified in the mito-
chondrial genome of P. falciparum. On average, the
eukaryotic mtDNA contains from 40 to 50 genes, and
from 12 to 20 of them are protein-coding. The least
number of proteins (2) is encoded by the mitochondrial
genome of P. falciparum, and the largest number (67) is
specified by the R. americana mitochondrial genome.
mtDNA of multicellular animals codes for 12 or 13 pro-
teins. The mitochondrial genome of yeasts Saccharomy-
ces cerevisiae (87.779 kb) codes for 30 proteins [16].
The mitochondrial genomes always code for the large
and small subunit rRNAs and a full or partial comple-
ment of tRNAs necessary for translation. In a limited
number of eukaryotes, mtDNA encodes 5S rRNA. In
mtDNA of plants and protists (but not in animals and
most fungi), the genes for several ribosomal proteins are
located. The eukaryotic mitochondrial genomes code for
a limited number of proteins involved in the formation of
functional mitochondria. On the whole, mtDNA-speci-
fied proteins are the components of respiratory com-
plexes I (NADH: ubiquinone oxidoreductase encoded by
the nad genes), II (succinate: ubiquinone oxidoreduc-
tase; sdh), III (ubiquinol: cytochrome c oxidoreductase;
cob), and IV (cytochrome c oxidase; cox) of the electron
transport chain, as well as complex V (ATP synthase;
atp) [8]. Yeast mitochondrial genome is atypical in this
respect, since in addition to protein-coding genes specific
to mitochondria, it bears ten genes for endonucleases,
reverse transcriptases, and mRNA maturases [16].
In summary, in all eukaryotes, mtDNA encodes a
limited number of RNA species and proteins essential
for mitochondrion functioning. Table 1 presents some
characteristics of eukaryotic mitochondrial genomes.
CHLOROPLAST GENOMICS
Chloroplasts, centers of photosynthesis in plant
cells, are a well-studied class of plastids. Chloroplasts
of higher plants and algae possess their own genome,
whose size varies from 120 to 160 kb. Three exceptions
are currently known: the 171-kb genome of the Brasil-
ien tobacco (Nicotiana acuminati, Solanaceae), the
180-kb genome of duckweed (Lemna L., Lemnaceae),
and the 217-kb genome of crane’s-bill (Pelargonium L.,
Geraniaceae). The chloroplast genome is represented by
circular DNA molecules and contains about 120 genes.
Repeated elements are usually short (<100 bp). In addi-
tion to short repeats, cpDNA has a single large inverted
repeat (IR) ranging in size from 10 to 76 kb, in most
species, its length varies from 22 to 26 kb. The legumes
lack the IR. It has been suggested that the IR was
present in the common ancestor of higher plants. In
some species, one IR segment was lost during evolu-
tion, in some cases, the IR was only partially lost, and
the chloroplast genome retained a remnant of the large
IR (such as a 495-bp fragment in black pine). The IR
always carries rRNA and usually tRNA genes; their
RUSSIAN JOURNAL OF GENETICS Vol. 41 No. 9
959
order is as follows: 16S rRNA–tRNAIle—tRNAAla—
23S rRNA—5S rRNA. As a result, the IR-located genes
in the chloroplast genome are duplicated. The structural
organization of cpDNA in higher plants is conserved.
The IR is the most conserved region, while the large
unique sequence is the most variable [17]. cpDNA mol-
ecules are capable of isomerization. In some species
(spinach, corn, tomato, and pea), they may form multi-
mers. The distribution of different cpDNA forms is as
follows: 67.5% monomers, 22.5% dimers, 7.5% trim-
ers, and 2.5% tetramers [18].
Algal plastid genomes are more diverse in size,
structural organization, and gene content than those of
higher plants. Their size averages 140 kb with about
110 genes. Within phylogenetic groups, genome size is
rather constant. Thus, the size of the red algal cpDNA
varies from 150 to 191 kb [19]. The chloroplast genome
size in green algae is similar (100–200 kb), except for
the large genomes of some Ulvophyceae species. In
Acetabularia mediterranea, a member of this group, a
uninucleate 10-cm cell has hundreds of chloroplasts
with the cpDNA size of 1500 kb. It is only by a factor
of 2.4 less than the cyanobacterial Synechocystis sp.
PCC 6803 genome [20]. It is of interest that although
Codium fragile belongs to the same Ulvophyceae fam-
ily, its genome size is only 89 kb. Apicomplexan para-
sites carry vestigial, biosynthetically active plastids
(apicoplasts) [21, 22] with a small 35-kb genome carry-
ing about 60 genes. Sequencing of the apicoplast
genomes showed its similarity to the chloroplast
genomes of green algae and higher plants [23]. In api-
complexan species, such as Plasmodium spp., Toxo-
plasma, and Eimeria that cause malaria, toxoplasmosis,
and coccidiosis, respectively, the plastid genome is
conserved and shows considerable homology in gene
content and order [23, 24]. In contrast, the unicellular
eukaryotic parasites, which belong to the order of Kine-
toplastidae and cause leishmaniasis, sleeping sickness,
and Chagas’ disease in humans did not retain plastid
remnants, but carry several plastid-derived genes [25].
Dinoflagellates have a unique chloroplast genome
structure. A detailed analysis of several peridinine-con-
taining species (Heterocapsa triquetra, Amphidinium
operculatum, and A. carterae) showed that instead of a
typical plastid genome, they possess several small cir-
cular DNA molecules of about 2–3 kb in length con-
taining a single gene [26]. The plasmid-like DNA also
occurs in plastids of some green algae, however, in this
case, they are additional to the main chloroplast
genome and bear no functional genes. In dinoflagel-
lates, minicircle genes encode products that are of the
plastid origin in other higher plants and algae. It is note-
worthy that in minicircles, only a few genes were iden-
tified. In dinoflagellates, the following genes are
located on minicircles: atpA, atpB, petB, petD, psaA,
psaB, psbA, psbB, psbD, psbE, 16S rRNA, and 23S
rRNA. However, the genes for RNA polymerase sub-
units and ribosomal proteins, as well as tRNA genes
were not found in minicircles. Sometimes minicirles
2005
960 ODINTSOVA, YURINA

Table 1. Features of eukaryotic mitochondrial genomes [8]

No. of tRNAs
Genes coding for No. of

portion, %
Taxon

Size, kb

Coding
respiratory ribosomal
rRNAs other ORFs introns
chain subunits proteins

Protists
Amoebidium >200 ≈20 ≥25(47) rnl, rns atp6,8,9, cob, rps3,4,13 – ≥24 ≥21(I)
parasiticum cox1–3,
nad1–4,4L,5,6 ≥2(II)
Monosiga 76.6 46.9 25 rnl, rns atp6,8,9, rps3,4,8,12– mttB 2 4(I)
brevicollis cob, cox1–3, 14,19,
nad1–4,4L,5,6 rpl2,5,14,16
Reclinomonas 69.0 91.3 26 rnl, rns, atp1,3,6,8,9, rps1–4,7, cox11, mttB, 3 1(II)
americana rrn5 cob, cox1–3, 8,10–14,19, rnpB, rpoA-D,
nad1–4,4L, rpl1,2,5,6,10, secY, tufA, yejR,
5–11, sdh2–4 11,14,16, 18– U,V,W, ymf39
20,27,31,32,34
Fungi 19–94 41–89 7–26 rnl, rns atp6,8,(9), (rps3) (rnpB) 0–36 0–37
cob, cox1–3
(nad1–4,4L,5,6)
Animals 13–22 62–95 2–23 rnl, rns atp6,(8), – (mutS) – 0–2
cob, cox1–3,
nad1–4,4L,5,6
Plants 187–367 46–65 22–27 rnl, rns, atp1,6,8,9, cob, rps(1,2),3,4,7, mttB, yeiR,U, ≈50–100 20–32
rrn5 cox1–3, nad1– (8,10,11), (V), ymf39
4,4L,5,6, (7), 12,13,(14,19),
9(sdh3,4) rpl(2),5,(6,16)
Note: Genes enclosed in parentheses are present only in some taxa of the particular group. Roman numerals (I and II) indicate the intron
group. Genes and corresponding gene products are: atp1–9, ATP synthase subunits; cob, cytochrome b apoprotein; cox1–3, cyto-
chrome c oxidase subunits; cox11, cytochrome oxidase assembly protein; mttB, Sec-independent protein translocase; nad1–11,
NADH dehydrogenase subunits; rnl, large subunit rRNA; rns, small subunit rRNA; rrn5, 5S rRNA; rnpB, RNAse P RNA; rpl1–34,
large subunit ribosomal proteins; rps1–19, small subunit ribosomal proteins; rpoA–D, RNA polymerase subunits and sigma factor;
sdh2–4, succinate dehydrogenase subunits; secY, SecY-type preprotein translocase subunit; tufA, elongation factor A; yejR–W. ABC
transporter involved in cytochrome c biogenesis; ymf39, conserved membrane protein of unknown function. Coding portion, the per-
centage of sequence having a coding function. ORF ≥ 60 amino acids are included in the table.

contain gene fragments or carry no genes at all. Among
other specific features of the dinoflagellate minicircle
genome are the use of the GTA initiation codon, the
absence of transcript editing, etc. [27, 28].
Similarly to mtDNA, large variations in the chloro-
plast genome size in higher plants and green algae are
mainly due to different length of intergenic regions.
Higher plant chloroplast genome contains from 14 to
18 split genes. The total number of introns averages 20.
Their size varies from 0.3 to 2.5 kb. Introns are con-
served and predominantly belong to group II. Many
chloroplast genes of higher plants possess only one
intron. With the exception of green algae, high gene
density is typical for algal chloroplast genomes. Long
noncoding regions and introns are rare. In these lin-
eages, the compact chloroplast genomes are character-
ized by short intergenic spacers and the presence of
overlapping genes. Thus, introns in chloroplast genes
have a much smaller effect on genome size than in
mitochondrial genes.
According to their functions, chloroplast genes may
be classified into three main groups: genes for the tran-
scription/translation system, genes for the photosyn-
thetic apparatus, and those related to biosyntheses of
amino acids, fatty acids, pigments, etc. The transcripts
and translation products of the latter group are poorly
studied. The genes of the first two groups are the most
conserved. High degree of homology (98–100%) is
characteristic of the rRNA genes. Table 2 shows photo-
synthesis-related proteins encoded by the chloroplast
and nuclear genomes.
In chloroplast genomes of higher plants (and green
algae), the hypothetical conserved reading frames (ycf)
coding for proteins associated with photosynthesis
were discovered. The ycf3 and ycf4 genes encode pro-
teins involved in assembly/stability of PSI; the ycf9
gene participates in PSII functions and forms a single

RUSSIAN JOURNAL OF GENETICS Vol. 41 No. 9 2005

 GENOMICS AND EVOLUTION OF CELLULAR ORGANELLES
transcriptional unit with the psbC and psbD genes. The
transcript of this gene is located in chloroplast thyla-
koid membranes [29]. In the green alga Chlamydomo-
nas reinhardtii, the ycf8 gene presumably encodes PSII
subunit PsbT, while the ycf9 gene is involved in the
attachment of the antenna to the PSII reaction center
[29, 30]. The transcripts of these genes have not been
identified so far. The chloroplast DNA encodes from 19
to 60 ribosomal proteins, translation factors, RNA
polymerase subunits, tRNA and rRNA. The list of chlo-
roplast genes identified in 12 completely sequenced
chloroplast genomes of higher plants [31] was pub-
lished earlier [17].
Similarly to cpDNA of higher plants, algal chloro-
plast genomes mostly possess the same gene groups.
However, in many algal lineages, especially nongreen
algae, the plastid DNA often carries unique genes.
Thus, in the sequenced plastid genomes of the red algae
Cyanidium caldarium and Porphyra purpurea, more
than 30 unique genes were identified [32]. Unique
genes are characteristic of the mitochondrial genomes
of some algal lineages and protists. For example, in the
mtDNA of the flagellate Reclinomonas americana, 18
unique genes were identified. The compact apicoplast
genome carries the genes involved in gene expression
in these organelles. They include genes for rRNA, ribo-
somal proteins (rpl2, rpl14, and rps2), tRNA, RNA
polymerase, and the elongation factor. The clpC and
sufB earlier known as ORF470 and ycf24 are the only
apicoplast genes unrelated to the transcription/transla-
tion apparatus. The clpC gene specifies a molecular
chaperone involved in protein targeting to the apico-
plast and/or folding of the imported proteins. The sufB
(ycf24) is homologous to the gene found in cyanobacte-
rial and red algal plastid genomes. Comparison of the
bacterial operons carrying the sufB gene with the Plas-
modium genome sequences revealed five proteins
(SufA, C, D, S, and NifU) homologous to the bacterial
SufB. By analogy with bacterial Nifs and Sufs, it was
suggested that SufB together with other proteins of the
malaria parasite participate in iron metabolism, the for-
mation of the Fe–S cluster, and/or oxidative stress resis-
tance. It was hypothesized that protein synthesis was
retained in apicoplasts to provide SufB and chaperone
Clp expression [23].
EVOLUTION OF CELLULAR ORGANELLES
The endosymbiotic origin of organelles in eukary-
otic cells has been widely accepted. According to this
hypothesis, the energy-transforming organelles of
eukaryotes (plastids and mitochondria) arose from
independent endosymbiotic events involving a free-liv-
ing cyanobacterium and α-proteobacteria, respectively,
which were captured by the eukaryotic host and
evolved into highly specialized machineries of photo-
synthesis and respiration [33]. A large body of cytolog-
ical and molecular biological evidence point to the
endosymbiotic origin of cell organelles. One of the
RUSSIAN JOURNAL OF GENETICS Vol. 41 No. 9
961
Table 2. Involvement of nuclear and chloroplast genomes
in the synthesis of photosynthesis-related proteins
Photosynthesis Protein Gene location
Dark reactions RUBISCO small subunit Nucleus
RUBISCO large subunit Chloroplasts
Light reactions Apoproteins ″
of PSI and PSII
Cytochrome b6 ″
Cytochrome f ″
6 ATPase subunits ″
3 ATPase subunits Nucleus
Light-harvesting complex ″
Plastocyanin ″
Ferredoxin ″
main arguments in favor of this hypothesis is the find-
ing that chloroplasts and mitochondria are formed only
from the preexisting organelles. They cannot appear de
novo because nuclear genes encode only part of the
proteins necessary for their functions. In addition, the
organellar genes show more similarity to the prokary-
otic than to eukaryotic genes. Similarly to prokaryotic
genomes, organelle genomes are represented by circu-
lar DNA molecules. Chloroplasts and mitochondria
have their own protein-synthesizing apparatus. The
structure of their ribosomes and rRNA, as well as rRNA
and ribosomal protein operons is similar to that of
prokaryotes [34].
A Russian botanist Mereschkowsky was the first
who advanced a hypothesis for the endosymbiotic ori-
gin of plastids from cyanobacteria early in the 20th cen-
tury. Its first version was published in the German jour-
nal Biologisches Centralblatt (Zentralblatt) in 1905 and
was received with profound skepticism by the scientific
community. Only half a century later, an enormous
body of evidence proved its validity. To acknowledge
the role of Mereschkowsky as the author of the endo-
symbiotic theory, an English version of his article was
published in the European Physiological Journal in
1999 [35].
According to present-day concepts of the origin of
plastids, at the early evolutionary stages, a cyanobacte-
rium was captured by a eukaryotic cell with subsequent
establishment inside the host cell and reduction of the
cyanobacterial genome to the size of the organelle
genome.
Mitochondria originated before the emergence of
plastids [1]. The hypothesis postulating the endosymbi-
otic origin of mitochondria was first put forward by the
American scientist Wallin more than a century ago [9].
According to this hypothesis, mitochondria are the
direct descendants of a bacterial endosymbiont that
appeared early in the evolution in a nucleus-containing
host cell that lacked mitochondria (Fig. 1a). The mono-
2005
962 ODINTSOVA, YURINA

Eukaryote (mitochondria–)

Archaeobacterium a a + α-Proteobacterium

‡
+
b
a
b
Proteobacterium

Eukaryote (mitochondria+)

Fig. 1. Hypotheses describing the origin of a eukaryotic cell [9]. (a) Two-stage process initially involving formation of an amito-
chondriate eukaryote by fusion of an archaeobacterium with a proteobacterium followed by acquisition of the mitochondrion
through endosymbiosis with alpha-proteobacterium; (b) simultaneous creation of the eukaryotic nucleus and mitochondrion by
fusion of a hydrogen-requiring, methanogenic archaeobacterium (host) with an alpha-proteobacterium (symbiont).

phyletic origin of mitochondria from an eubacterial
ancestor related to extant α-proteobacteria was further
confirmed by sequence analysis of mitochondrial
genes.
Recent analysis of the protist genome and proteome
and evolutionary studies of the enzymes of anaerobic
metabolism (oxygen-independent ATP synthesis) in
three major groups of heterotrophic eukaryotes: amito-
chondriate eukaryotes (that lack organelles and synthe-
size ATP), eukaryotes with mitochondria, and eukary-
otes containing hydrogenosomes, have provided
insights that challenge the traditional endosymbiotic
theories [36, 37]. Several models for the origin of
eukaryotic cell (and mitochondria) are described in the
literature [38]. An alternative endosymbiotic hypothe-
sis called a “hydrogen hypothesis” deserves special
attention. It postulates that mitochondria arose from the
symbiosis of a hydrogen-dependent methanogenic
archaebacterium that utilized hydrogen and carbon
dioxide to generate methane (host cell) with α-proteo-
bacterium (symbiont), for which these compounds
served as by-products of anaerobic metabolism [39].
The host dependence from hydrogen produced by the
symbiont fixed the established symbiosis in the evolu-
tion. The hydrogen hypothesis explains the origin of
heterotrophy and compartmentation of the processes of
anaerobic metabolism in eukaryotes. It suggests con-
current origin of the ancestral eukaryotic cell and mito-
chondria and postulates transfer of a portion of the α-
eubacterial genome into the eukaryotic nucleus with
simultaneous transformation of its reduced form into
the mitochondrial genome (Fig. 1b). Both symbioses,
the symbiotic association of a cyanobacterial ancestor
with a eukaryotic cell that led to the birth of all pho-
totrophic eukaryotes and the symbiosis that gave rise to
mitochondria, play a pivotal role in the evolution of the
eukaryotic cell [40]. As part of the nucleus-containing
host cell, cellular organelles remained semiautono-
mous: having preserved their own genome capable of
replication and expression, they lost their free-living
lifestyle. Genes of the contemporary organelles carry
the genetic information of the ancestral endosymbionts.
During the evolution, a massive gene transfer to the
nucleus and/or loss of the genetic information by the
endosymbiotic genome occurred (due to transfer of
some functions from the endosymbiont to the nucleus
and in case when an endosymbiotic gene was already
present in the host cell genome) [41–47]. In Arabidop-
sis thaliana, a copy of the whole mitochondrial genome
(367 kb) with 99% similarity to the organelle copy is
located on chromosome 2 [48]; in rice, a fragment of
the chloroplast genome (33 kb) with 99.7% homology
to the organelle copy is located on chromosome 10.
mtDNA fragments were discovered in nuclear genomes
of different yeast races [49]. The nuclear genomes of
primates carry many insertions of mtDNA [50]. Func-
tional gene transfer from the organelles to the nucleus
of the host cells that started more than a billion years
ago is an ongoing process (e.g., in flowering plants)
[51]. A recent transfer of the cox2 gene encoding cyto-

RUSSIAN JOURNAL OF GENETICS Vol. 41 No. 9 2005

 GENOMICS AND EVOLUTION OF CELLULAR ORGANELLES
chrome oxidase subunit 2 from mitochondria to the
nucleus has been much studied in legumes [45]. While
in most plants, the cox2 gene is mitochondrion-
encoded, in many legumes, an actively transcribed copy
of the gene was found in the nucleus. In several species,
both copies of the gene (nuclear and mitochondrial) are
transcribed [45].
Functional gene transfer from organelles to the
nucleus usually involves an RNA intermediate. It is
common knowledge that in mitochondria and chloro-
plasts, posttranscriptional RNA editing occurs [5].
Gene transport from the organelles to the nucleus sug-
gests reimport of the gene product to the organelle and
therefore, must include duplication of the organelle
gene, conversion of the nuclear copy into the active
form, acquisition of a nuclear promoter and other regu-
latory elements conferring properly regulated expres-
sion together with a targeting sequence to direct the
gene product to a particular cell compartment. It was
speculated that in evolution of eukaryotes, unidirec-
tional organelle-to-nucleus gene transfer could be
driven largely by mechanistic forces and chance muta-
tions [45]. In different phylogenetic groups, different
genes were transferred to the nucleus. As a result, the
organelle genomes of present-day organisms have dif-
ferent but overlapping gene content. It is of interest that
after incorporation into the nuclear genome, the
encoded protein copies may be targeted to organelles
distinct from those, from which they were originally
transferred [25, 52]. Comparison of the nuclear genome
of Arabidopsis thaliana with three cyanobacterial
genomes (Nostoc punctiforme, Prochlorococcus mari-
nus, and Synechocystis sp. PCC 6803) showed that
approximately 4500 of Arabidopsis nuclear protein-
coding genes (18%) were acquired from the cyanobac-
terial ancestor of plastids. The products of more than a
half of them are targeted to cell compartments other
than the chloroplast. Conversely, protein products of
many nuclear noncyanobacterial genes are imported
into the plastids [46].
Together with gene transfer from the organelles to
the nucleus, a horizontal gene transfer between differ-
ent organelles occurred in the evolution. There is exper-
imental body of evidence in favor of the horizontal gene
transfer from chloroplasts to mitochondria and between
mitochondrial genomes. Gene transfer between mito-
chondrial genomes is supported by the presence of sim-
ilar introns at identical positions in homologous mito-
chondrial genomes of evolutionarily divergent species.
A transfer of the gene encoding subunit 6 of the ATPase
complex between mitochondria of two fungal classes
resulting in the hybrid atp6 gene was described. A hor-
izontal gene transfer of the mitochondrial genes for the
respiratory chain and ribosomal proteins between dis-
tantly related angiosperms, even between dicotyledons
and monocotyledons was reported [53]. This transfer is
not obvious in other higher plants and algae [53, 54].
The genomic consequences of mtDNA–mtDNA gene
transfer include gene duplication, recapture of genes
RUSSIAN JOURNAL OF GENETICS Vol. 41 No. 9
963
previously lost through transfer to the nucleus, and the
formation of chimeric genes, such as the rps11 gene:
one part of the gene has a counterpart in monocotyle-
dons, and the other half is homologous to rps11 of
dicotyledons.
Comparative genomics proves a monophyletic ori-
gin of cellular organelles. Thus, mitochondrial genome
sequences in protists, a phylogenetically diverse group
of unicellular eukaryotes (such as amoebae, flagellates,
and algae), reveal considerable homology [11]. This
indicates that contemporary mtDNAs originated from a
single ancestral, protomitochondrial genome. Studies
of mtDNA and its expression support eubacterial ori-
gin. Among the existing organisms, the purple bacteria
from the division of α-proteobacteria are the most
closely related to mitochondria. Rickettsia, which
belong to the subdivision of α-proteobacteria including
such genera as Rickettsia, Anaplasma, and Ehrlichia,
are a group of obligate intracellular parasites that show
the highest homology to mitochondria. In gene number
and content, the mitochondrial genome of the flagellate
protist R. americana is the most bacteria-like [11], and
the genome of eubacterium Rickettsia prowazekii is the
most mitochondrion-like. These two organisms mark the
current boundaries of the evolutionary divide between
mitochondria and their eubacterial relatives [9].
As mentioned above, plastids arose from the symbi-
osis of a primitive cyanobacterium with a eukaryotic
host cell that followed the acquisition of mitochondria.
Plastids of higher plants, red and green algae, as well as
plastids of glaucocystophytes arose from the primary
endosymbiosis; the remaining eukaryotic algae carry
plastids derived from the secondary endosymbiosis
[40, 55, 56]. The secondary endosymbiotic event con-
sisted of the engulfment, but not digestion of a photo-
synthesizing cell (red, green algae, or glaucocysto-
phytes) by a nonphotosynthesizing (heterotrophic)
eukaryotic cell. Whereas plastids derived from primary
endosymbiosis are surrounded by a double membrane
corresponding to the membranes of the cyanobacterial
endosymbiont, secondary plastids have three or four
membranes; the outermost derived from the host pha-
gosomal membrane. In most cases, secondary plastids
may be recognized only by the presence of more than
two surrounding membranes. All other traces of the
captured phytotrophic cell disappeared in the evolution.
It appears that secondary endosymbiosis occurred more
than once, thus providing an extreme diversity of
present-day algae [40, 56]. In some algal lineages
(cryptomonads and chlorarachniophytes), the second-
ary endosymbiont has retained a vestigial cytoplasm
and nucleus. Secondary endosymbiosis was first dis-
covered in cryptomonads (Guillardia theta), where a
small nucleus-like organelle called “nucleomorph”
derived from the endosymbiotic nucleus was found.
From this tiny nucleus, DNA was isolated and
sequenced. The obtained sequence revealed similarity
to the nuclear DNA of red algae. Complete sequencing
showed that cryptomonads represent an intermediate
2005
964 ODINTSOVA, YURINA

2 3 4

6 7 8 9 10 11 12 13

14
15
Fig. 2. A scheme for the origin and evolution of plastids [40]. A single primary endosymbiosis between an unknown heterotrophic
eukaryote and a cyanobacterium led to three primary plastid-bearing lineages (top). Two secondary endosymbiotic events involving
two different green algae and unrelated hosts led to euglenids and chlorarachniophytes. A single endosymbiosis between a red alga
and a heterotrophic host led to all remaining eukaryotic algae. In some of lineages, photosynthesis was lost; in the ciliates, the entire
lineage is non-photosynthetic. Figures denote: (1) Primary endosymbiosis; (2) Red algae; (3) Glaucocystophytes; (4) Green algae
(and plants); (5) Secondary endosymbiosis; (6) Cryptomonads; (7) Haptophytes; (8) Heterokonts; (9) Ciliates; (10) Apicomplexa;
(11) Dinoflagellates; (12) Euglenids; (13) Chlorarachniophytes; (14) Alveolates; (15) Chromalveolates

stage of the secondary plastid endosymbiosis. The
Guillardia theta nucleomorph contains 511 genes,
30 of which are protein-coding. Euglenids, chlorarach-
niophytes, cryptomonads, heterokonts, dinoflagellates,
and apicomplexa carry plastids derived from secondary
endosymbiosis (Fig. 2) [57].
A comprehensive analysis of cell organelles allows
one to trace the evolutionary history of eukaryotes [58],
help to reconstruct more accurately the origin of plas-
tids and mitochondria, and to revise the stages of their
early evolution. Diverse molecular markers used in
genomics in combination with numerous morphologi-
cal and biochemical markers complement phylogenetic
data based on the analysis of individual genes.
Sequencing of organelle genomes, in particular those of
different algal lineages that retained more traits of the
ancestral cyanobacterial genome than plastids of higher
plants, seems most promising [34, 59]. For the evolu-
tionary studies, sequencing of the mtDNA of protists,
the most phylogenetically divergent group of eukary-
otes, is especially important.
Until recently, the data concerning organization of the
mitochondrial and plastid genomes have been limited. The
human mitochondrial genome (1981) and the chloroplast

RUSSIAN JOURNAL OF GENETICS Vol. 41 No. 9 2005

 GENOMICS AND EVOLUTION OF CELLULAR ORGANELLES
genomes of tobacco (1986) and Marchantia (1986) were
the first to be sequenced. The nucleotide sequences of
more than 600 mainly vertebrate mtDNAs (OGMP data-
base at http://megasun.bch.umontreal.ca/ogmp/projects/
other/mt_list.html) and more than 40 plastid genomes of
higher plants, algae, and protists (http://megasun.
bch.umontreal.ca/ogmp/projects/other/cp_list.html) are
presently known.
Progress in genomics posed several questions. One
of the most challenging evolutionary problems is gene
transfer to the nucleus. Why some genes were trans-
ferred to the nucleus while others remained in cell
organelles? What were the advantages of preserving
some genes in the organelles and donating others to the
nucleus? It has been suggested that selection played a
key role in the preservation of the nuclear and elimina-
tion of the organellar copy. Presence of a gene in the
nucleus allows for crossing over during meiosis, per-
haps enabling beneficial mutations to be fixed more
rapidly than in asexual organelle genomes. Conversely,
progressive accumulation of deleterious mutations in
asexual genomes of organelles may favor transfer of
genes to the nucleus. It is also possible that nuclear
localization protects organelle genes from the damag-
ing effect of active oxygen species. Finally, there is the
possibility that some organellar protein-coding genes
may be better regulated in the nucleus [45].
Another question arises as to why a few protein
genes are retained by organelle genomes across all or
most eukaryotes genomes. One view [45, 60] is that the
products of these genes are highly hydrophobic and
cannot be imported into the organelles and properly
inserted (posttranslationally) into the inner membranes.
The mitochondrial cytochrome b, a highly hydrophobic
protein containing eight transmembrane helices and
synthesized in the cytoplasm, could not be completely
incorporated into the inner mitochondrial membrane.
Successful import was restricted to three to four trans-
membrane domains. The most hydrophobic mitochon-
drial proteins involved in respiration, cytochrome b and
subunit 1 of cytochrome oxidase, are encoded by mito-
chondrial genomes in all eukaryotes studied (cob, cox1)
[14, 61]. It has been recently shown that some plastid-
encoded thylakoid proteins are synthesized in associa-
tion with the thylakoid membranes and cotranslation-
ally inserted into the membrane protein complexes.
This refers to such proteins as D1 of PSII. Another
hypothesis for retention of certain genes in organelles is
that their products are toxic when present in the cytosol
or in some other, inappropriate cellular compartment to
which they might be misrouted after synthesis in the cyto-
sol. It cannot be excluded that the preservation of genes in
organelles facilitates immediate regulation of their expres-
sion by the redox state of the organelles [45, 60].
Originally genomics, namely genome sequencing,
provided an enormous body of fundamental data. How-
ever, functional genomics demonstrated that gene
expression in organelles is much more complicated
RUSSIAN JOURNAL OF GENETICS Vol. 41 No. 9
965
than suggested earlier. Further research in the field of
genome structure and expression of organelle genes
and nuclear factors regulating their expression will help
to elucidate phylogenetic relationships in eukaryotes.
ACKNOWLEDGMENTS
This work was supported by the Russian Foundation
for Basic Research (grant no. 03-04-49051a) and the
Program of the Presidium of the Russian Academy of
Sciences “Molecular and Cellular Biology”.
REFERENCES
1. Burger, G., Gray, M.W., and Lang, B.F., Mitochondrial
Genomes: Anything Goes, Trends Genet., 2003, vol. 19,
no. 12, pp. 709–716.
2. Armstrong, M.R., Blok, V.C., and Philips, M.S., A Mul-
tipartite Mitochondrial Genome in the Potato Cyst Nem-
atode Globodera pallida, Genetics, 2000, vol. 154, no. 1,
pp. 181–192.
3. Watanabe, K.I., Bessho, Y., Kawasaki, M., and Hori, H.,
Mitochondrial Genes Are Found on Minicircle DNA
Molecules in the Mesozoan Animal Dicyema, J. Mol.
Biol., 1999, vol. 286, no. 3, pp. 645–650.
4. Yurchenko, V.Yu. and Kolesnikov, A.A., Minicircular
Kinetoplast DNA of Trypanosomatidae, Mol. Biol.
(Moscow), 2001, vol. 35, no. 1, pp. 3–13.
5. Odintsova, M.S. and Yurina, N.P., RNA Editing in Plant
Chloroplasts and Mitochondria, Fiziol. Rast., 2000,
vol. 37, no. 2, pp. 307–320.
6. Gray, M.W., Origin and Evolution of Mitochondrial
DNA, Annu. Rev. Cell Biol., 1989, vol. 5, pp. 25–50.
7. Lang, B.F., O’Kelly, C., Nerad, T., et al., The Closest
Unicellular Relatives of Animals, Curr. Biol., 2002,
vol. 12, no. 20, pp. 1773–1778.
8. Burger, G., Forget, L., Yun Zhu, et al., Unique Mitochon-
drial Genome Architecture in Unicellular Relatives of
Animals, Proc. Natl. Acad. Sci. USA, 2003, vol. 100,
no. 3, pp. 892–897.
9. Gray, M.W., Burger, G., and Lang, B.F., Mitochondrial
Evolution, Science, 1999, vol. 283, no. 5407, pp. 1476–
1481.
10. Unseld, M., Marienfeld, J.R., Brandt, P., and Brennicke, A.,
The Mitochondrial Genome of Arabidopsis thaliana
Contains 57 Genes in 366 924 Nucleotides, Nat. Genet.,
1997, vol. 15, no. 1, pp. 57–61.
11. Odintsova, M.S. and Yurina, N.P., The Mitochondrial
Genome of Protists, Rus. J. Genet., 2002, vol. 38, no. 6,
pp. 642–655.
12. Paquin, B. and Lang, B.F., The Mitochondrial DNA of
Allomyces macrogynus: The Complete Genomic
Sequence from an Ancestral Fungus, J. Mol. Biol., 1996,
vol. 255, no. 5, pp. 688–701.
13. Edqvist, J., Burger, G., and Gray, M.W., Expression of
Mitochondrial Protein-Coding Genes in Tetrahymena
pyriformis, J. Mol. Biol., 2000, vol. 297, no. 2, pp. 381–
393.
14. Gray, M.W., Lang, B.F., Cedergren, R., et al., Genome
Structure and Gene Content in Protist Mitochondrial
2005
966 ODINTSOVA, YURINA
DNAs, Nucleic Acids Res., 1998, vol. 26, no. 4, pp. 865–
878.
15. Seif, E.R., Forget, L., Martin, N.C., and Lang, B.F.,
Mitochondrial RNase P RNAs in Ascomycete Fungi:
Lineage-Specific Variations in RNA Secondary Struc-
ture, RNA, 2003, vol. 9, no. 9, pp. 1073–1083.
16. Anderson, G.E., Karlberg, O., Canback, B., and
Kurland, Ch.G., On the Origin of Mitochondria: A
Genomics Perspective, Phil. Trans. R. Soc. London, B,
2003, vol. 358, no. 1429, pp. 165–179.
17. Odintsova, M.S. and Yurina, N.P., The Plastid Genome
of Higher Plants and Algae: Structure and Functions,
Mol. Biol. (Moscow), 2003, vol. 37, no. 5, pp. 1–16.
18. Deng, X.-W., Wing, R.A., and Gruissem, W., The Chlo-
roplast Genome Exists in Multimeric Forms, Proc. Natl.
Acad. Sci. USA, 1989, vol. 86, no. 11, pp. 4156–4160.
19. Simpson, C.L. and Stern, D.B., The Treasure Trove of
Algal Chloroplast Genomes: Surprises in Architecture
and Gene Content, and Their Functional Implications,
Plant Physiol., 2002, vol. 129, no. 3, pp. 957–966.
20. Kaneko, T., Sato, S., Kotani, H., et al., Sequence Analy-
sis of the Genome of the Unicellular Cyanobacterium
Synechocystis sp. Strain PCC 6803: II. Sequence Deter-
mination of the Entire Genome and Assignment of
Potential Protein-Coding Regions, DNA Res., 1996, vol. 3,
no. 1, pp. 109–136.
21. Kohler, S., Delwiche, C.F., Denny, P.W., et al., A Plastid
of Probable Green Algal Origin in Apicomplexan Para-
sites, Science, 1997, vol. 275, no. 5305, pp. 1485–1489.
22. Ralph, S.A., Foth, B.J., Hall, N., and McFadden, G.I.,
Evolutionary Pressures on Apicoplast Transit Peptides,
Mol. Biol. Evol., 2004, vol. 21, no. 12, pp. 2183–2194.
23. Foth, B.J. and McFadden, G.I., The Apicoplast: A Plastid
in Plasmodium falciparum and Other Apicomplexan
Parasites, Int. Rev. Cytol., 2003, vol. 224, pp. 57–110.
24. Wilson, R.J.M., (Iain), Rangachari, K., Saldanha, J.W.,
et al., Parasite Plastids: Maintenance and Functions,
Phil. Trans. R. Soc. London, B, 2003, vol. 358, no. 1429,
pp. 155–164.
25. Martin, W. and Borst, P., Secondary Loss of Chloroplasts
in Trypanosomes, Proc. Natl. Acad. Sci. USA, 2003,
vol. 100, no. 3, pp. 765–767.
26. Zhang, Z., Green, B.R., and Cavalier-Smith, T., Single
Gene Circles in Dinoflagellate Chloroplast Genomes,
Nature, 1999, vol. 400, no. 6740, pp. 155–159.
27. Howe, Ch.J., Barbrook, A.C., Koumandou, V.L., et al.,
Evolution of the Chloroplast Genome, Phil. Trans. R.
Soc. London, B, 2003, vol. 358, no. 1429, pp. 99–107.
28. Koumandou, V.L., Nisbet, R.E.R., Barbrook, A.C., and
Howe, Ch.J., Dinoflagellate Chloroplasts—Where Have
All the Genes Gone?, Trends Genet., 2004, vol. 20, no. 5,
pp. 261–267.
29. Maenpaa, P., Gonzalez, E.B., Chen, L., et al., The ycf9
(orf62) Gene in the Plant Chloroplast Genome Encodes
a Hydrophobic Protein of Stromal Thylakoid Mem-
branes, J. Exp. Bot., 2000, spec. issue, pp. 375–382.
30. Rochaix, J.-D., The Three Genomes of Chlamydomonas,
Photosynth. Res., 2002, vol. 73, pp. 285–293.
31. Wakasugi, T., Tsudzuki, T., and Sugiura, M., The
Genomics of Land Plant Chloroplasts: Gene Content and
RUSSIAN JOURNAL OF GENETICS
Alteration of Genomic Information by RNA Editing,
Photosynth. Res., 2001, vol. 70, pp. 107–118.
32. Glockner, G., Rosenthal, A., and Valentin, K., The Struc-
ture and Gene Repertoire of an Ancient Red Algal Plas-
tid Genome, J. Mol. Evol., 2000, vol. 51, no. 4, pp. 382–
390.
33. Miyagishima, S., Nishida, K., and Kuroiwa, T., An Evo-
lutionary Puzzle: Chloroplast and Mitochondrial Divi-
sion Rings, Trends Plant Sci., 2003, vol. 8, no. 9,
pp. 432–438.
34. Odintsova, M.S. and Yurina, N.P., Common Features in
the Structural Organization of the Chloroplast Genome:
Comparison with Prokaryotic and Eukaryotic Genomes,
Mol. Biol. (Moscow), 1992, vol. 26, no. 4, pp. 757–771.
35. Martin, W. and Kowallik, K.V., Annotated English
Translation of Mereschkowsky’s 1905 Paper “Ueber
Natur und Ursprung der Chromatophoren im Pflanzenre-
iche”, Eur. J. Phycol., 1999, vol. 34, no. 3, pp. 287–295.
36. Kurland, C.G. and Andersson, S.G., Origin and Evolu-
tion of the Mitochondrial Proteome, Microbiol. Mol.
Biol. Rev., 2000, vol. 64, no. 4, pp. 786–820.
37. Martin, W., Hoffmeister, M., Rotte, C., and Henze, K.,
An Overview of Endosymbiotic Models for the Origins
of Eukaryotes, Their ATP-Producing Organelles (Mito-
chondria and Hydrogenosomes), and Their Het-
erotrophic Lifestyle, Biol. Chem., 2001, vol. 382, no. 11,
pp. 1521–1539.
38. Shestakov, S.V., On the Early Steps of Biological Evolu-
tion from the Genomics Viewpoint, Paleontol. Zh., 2003,
no. 6, pp. 50–57.
39. Martin, W. and Muller, M., The Hydrogen Hypothesis
for the First Eukaryote, Nature, 1998, vol. 392, no. 11,
pp. 1521–1539.
40. Archibald, J.M. and Keeling, P.J., Recycled Plastids: A
“Green Movement” in Eukaryotic Evolution, Trends
Genet., 2002, vol. 18, no. 11, pp. 577–584.
41. Martin, W. and Herrmann, R.G., Gene Transfer from
Organelles to the Nucleus: How Much, What Happens,
and Why?, Plant Physiol., 1998, vol. 118, pp. 9–17.
42. Martin, W., Stoebe, B., Goremykin, V., et al., Gene
Transfer to the Nucleus and the Evolution of Chloro-
plasts, Nature, 1998, vol. 393, pp. 162–165.
43. Stoebe, B., Hansmann, S., Goremykin, V., et al., Proteins
Encoded in Sequenced Chloroplast Genomes: An Over-
view of the Gene Content, Phylogenetic Information and
Endosymbiotic Gene Transfer to the Nucleus, Molecular
Systematics and Plant Evolution, Hollingsworth, P.M.,
Bateman, R.M., and Gornall, R.J., Eds., London: Taylor
and Francis, 1999, pp. 327–352.
44. Lang, B.F., Gray, M.W., and Burger, G., Mitochondrial
Genome Evolution and the Origin of Eukaryotes, Annu.
Rev. Genet., 1999, vol. 33, pp. 351–397.
45. Palmer, J.D., Adams, K.L., Cho, Y., et al., Dynamic Evo-
lution of Plant Mitochondrial Genomes: Mobile Genes
and Introns and Highly Variable Mutation Rates, Proc.
Natl. Acad. Sci. USA, 2000, vol. 97, no. 13, pp. 6960–
6966.
46. Martin, W., Rujan, T., Richly, E., et al., Evolutionary
Analysis of Arabidopsis, Cyanobacterial, and Chloro-
plast Genomes Reveals Plastid Phylogeny and Thou-
sands of Cyanobacterial Genes in the Nucleus, Proc.
Vol. 41 No. 9 2005
 GENOMICS AND EVOLUTION OF CELLULAR ORGANELLES
Natl. Acad. Sci. USA, 2002, vol. 99, no. 19, pp. 12 246–
12 251.
47. Sato, N., Comparative Analysis of the Genomes of
Cyanobacteria and Plants, Genome Informatics, 2002,
vol. 13, pp. 173–182.
48. Lin, X., Kaul, S., Rounslay, S., et al., Sequence and
Analysis of Chromosome 2 of the Plant Arabidopsis
thaliana, Nature, 1999, vol. 402, no. 6763, pp. 761–769.
49. Thorsness, P.E. and Fox, T.D., Escape of DNA from
Mitochondria to the Nucleus in Saccharomyces cerevi-
siae, Nature, 1990, vol. 346, pp. 376–379.
50. Woischnik, M. and Moraes, C.T., Pattern of Organiza-
tion of Human Mitochondrial Pseudogenes in the
Nuclear Genome, Genome Res., 2002, vol. 12, pp. 885–
893.
51. Stegemann, S., Hartmann, S., Ruf, S., and Bock, R.,
High-Frequency Gene Transfer from the Chloroplast
Genome to the Nucleus, Proc. Natl. Acad. Sci. USA,
2003, vol. 100, no. 15, pp. 8828–8833.
52. Archibald, J.M. and Keeling, P.J., Plant Genomes:
Cyanobacterial Genes Revealed, Heredity, 2003, vol. 90,
pp. 2–3.
53. Bergthorsson, U., Adams, K.L., Thomason, B., and
Palmer, J.D., Widespread Horizontal Transfer of Mito-
chondrial Genes in Flowering Plants, Nature, 2003,
vol. 424, no. 6945, pp. 197–201.
RUSSIAN JOURNAL OF GENETICS Vol. 41 No. 9
967
54. Marienfeld, J., Unseld, M., and Brennicke, A., The Mito-
chondrial Genome of Arabidopsis Is Composed of Both
Native and Immigrant Information, Trends Plant Sci.,
1999, vol. 4, no. 12, pp. 495–502.
55. Raven, J.A. and Allen, J.F., Genomics and Chloroplast
Evolution: What Did Cyanobacteria Do for Plants?,
Genome Biol., 2003, vol. 4, no. 3, article 209.
56. McFadden, G.I., Primary and Secondary Endosymbiosis
and the Origin of Plastids, J. Phycol., 2001, vol. 37,
no. 6, pp. 951–959.
57. Leister, D., Chloroplast Research in the Genomic Age,
Trends Genet., 2003, vol. 19, no. 1, pp. 47–56.
58. Danilenko, N.G. and Davydenko, O.G., Miry genomov
organell (Worlds of the Organellar Genomes), Minsk:
Tekhnalogiya, 2003.
59. Simpson, C.L. and Stern, D.B., The Treasure Trove of
Algal Chloroplast Genomes: Surprises in Architecture
and Gene Content, and Their Functional Implications,
Plant Physiol., 2002, vol. 129, pp. 957–966.
60. Race, H.L., Herrmann, R.G., and Martin, W., Why Have
Organelles Retained Genomes?, Trends Genet., 1999,
vol. 15, no. 9, pp. 364–370.
61. Gray, M.W., Evolution of Organellar Genomes, Curr.
Opin. Genet. Dev., 1999, vol. 9, no. 6, pp. 678–687.
2005