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Institut fur Biologie, Universitat Kassel, Heinrich-Plett-Str. 40, 34109 Kassel, Germany
Department of Plant Biology, Cornell University, Ithaca, NY 14853, USA
Abstract
In 1905, the Russian biologist C. Mereschkowsky postulated that plastids (e.g., chloroplasts)
are the evolutionary descendants of endosymbiotic cyanobacteria-like organisms. In 1927,
I. Wallin explicitly postulated that mitochondria likewise evolved from once free-living bacteria.
Here, we summarize the history of these endosymbiotic concepts to their modern-day derivative,
the serial endosymbiosis theory, which collectively expound on the origin of eukaryotic cell
organelles (plastids, mitochondria) and subsequent endosymbiotic events. Additionally, we
review recent hypotheses about the origin of the nucleus. Model systems for the study of
endosymbiosis in action are also described, and the hypothesis that symbiogenesis may
contribute to the generation of new species is critically assessed with special reference to the
secondary and tertiary endosymbiosis (macroevolution) of unicellular eukaryotic algae.
r 2005 Elsevier GmbH. All rights reserved.
Keywords: Algae; Chloroplasts; Cyanobacteria; Endosymbiosis; Mitochondria; Plastid
evolution; Speciation
Introduction
In his now classic textbook Lectures on the Physiology of Plants, Sachs (1882)
stated that the chlorophyll bodies (chloroplasts) behave like independent,
Corresponding author.
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autonomous organisms that grow by division and adapt in number to the size of
expanding leaves. Eight years later, the German cytologist Altmann (1890)
demonstrated that cell granules (mitochondria) display the same staining
properties as bacteria. Thus, Sachs and Altmann explicitly concluded that
chloroplasts and mitochondria are semi-autonomous organelles displaying the
behaviour of independent forms of life. However, the actual evolutionary origins of
plastids and mitochondria remained unknown and highly contentious until a seminal
publication of the Russian botanist C. Mereschkowsky (18551921) who hypothesized that plastids are evolutionarily derived from once free-living cyanobacteria
(blue-green algae). This landmark paper, which was published one century ago in
Biologisches Centralblatt (the precursor of this journal), was followed by two
additional publications on symbiogenesis and the evolution of cells (Mereschkowsky, 1905, 1910, 1920). These papers provided profoundly important insights into the
evolution of eukaryotic organisms-insights that have been substantiated in manifold
ways by many researchers working in diverse disciplines. Additionally, the
discoveries and deductions of Sachs (1882), Altmann (1890), Mereschkowsky
(1905, 1910, 1920), and other more recent workers have been elaborated and
modied to give rise to the serial endosymbiosis hypothesis of the origin of
eukaryotes. This concept, which has been evaluated extensively by Sitte (1989,
1991, 1994, 2001), see also Taylor (1979), attempts to unify many of the insights
gained from evolutionary and cell biology in the context of repeated endosymbiotic
events involving eukaryotic as well as prokaryotic organisms.
In a previous article reviewing the modern theory of biological evolution, we
outlined the process of endosymbiosis and noted that it is pivotal to understanding
the history of life (Kutschera and Niklas, 2004). Here, we summarize in greater detail
the history of this subtheory of the expanded synthesis and we review the evidence
that has been used to verify the basic precepts of the endosymbiotic theory, with
particular reference to a series of papers authored by Sitte (1989, 1991, 1994, 2001).
We then discuss critically the more recent proposal that eukaryotic speciation has
been driven by symbiogenesis a hypothesis introduced by Wallin (1927) and
described at greater length by Margulis and Sagan (2002). However, to avoid any
ambiguity, we begin our treatment of endosymbiosis by exploring how some basic
terms and concepts are dened, both historically and currently.
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Fig. 1. Chloroplasts in the cells of the moss Funaria hygrometrica (A) and stages in chloroplast
division (B). (Adapted from Sachs, 1882.)
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Fig. 2. Stained cell granules (mitochondria) in pancreas tissue of a mouse (Mus musculus) (A)
and symbiontic bacteria in cells of a root nodule of a leguminous plant (Coronilla glauca) (B).
(Adapted from Altmann, 1890.)
Fig. 3. Title page of C. Mereschkowskys classic paper published in the journal Biologisches
Centralblatt Vol. 25, 593604, 1905. (Adapted from the original publication.)
theoretical paper that argued for the xenogenous origin of organelles (Fig. 3).
Mereschkowsky postulated that plastids are reduced foreign microorganisms
(cyanobacteria or blue-green algae) that evolved as symbionts within heterotrophic host cells during the early phase of cell evolution (Mereschkowsky, 1905). In
this paper and those that followed, Mereschkowsky presented four arguments to
support his theory (Mereschkowsky, 1905, 1910, 1920): (1) According to Schimper
(1885) plastids never appear de novo, but are inherited; (2) These chlorophyll
bodies show structural, metabolic and reproductive resemblances to cyanobacteria;
(3) There are documented cases of intracellular symbioses (cytobioses): cyanobacteria invade and live in heterotrophic cells; and (4) Zoochlorellahost associations
(Amoeba viridis or Hydra viridis) are analogous to the chloroplast/plant cell
relationships. On the basis of these data, Mereschkowsky concluded that plant cells
are animal cells with invaded cyanobacteria. This basic idea serves as basis for the
endosymbiotic theory of the origin of plastids.
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Table 1. Chlorophyll and mitochondrial features, and postulated origin of plastids in major
plant lineages
Group
Chlorophylls
Mitochondrial cristae
Plastid origin
Embryophytes (272,000)
Chlorophytes (17,000)
Charophytes (3400)
Glaucophytes (13)
Rhodophytes (6000)
Euglenoids (900)
Cryptomonads (200)
Stramenopiles (14,000)
Haptophytes (300)
Dinoagellates (2000)
a and b
a and b
a and b
a and b
a and c
a and b
a and c
a and c
a and c
a, various
Flattened
Flattened
Flattened
Flattened
Flattened
Disk-shaped
Flattened
Tubular
Tubular
Tubular
Primary
Primary
Primary
Primary
Primary
Secondary (green)
Secondary (red)
Secondary (red)
Secondary (red)
Tertiary (various)
In his last two papers dealing with endosymbiosis, Mereschkowsky introduced the
hypothesis that different groups of cyanobacteria became endosymbionts such that
chloroplasts are polyphyletic (Mereschkowsky, 1910, 1920) an idea that resonates
with the two major chlorophyll compositions observed across extant algal lineages
(Chlorophyll a and b versus Chlorophyll a and c) (Table 1). Although he adopted
Altmanns (1890) erroneous concept that the nucleus is a union of bioblasts,
Mereschkowsky curiously did not accept this authors notion that mitochondria are
domesticated bacteria. This idea only gathered momentum with the publication of
a book by Wallin (1927), who recognized mitochondria as descendants of ancient
once free-living bacteria. As was the case with the ideas of Sachs, Schimper, and
Altmann, those expressed in Mereschkowskys original paper (Fig. 3) were not
generally accepted as a serious contribution to cell biology (Wilson, 1925;
Hoxtermann, 1998). For example, Famintzin (1907) argued that there is no
evidence for the occurrence of evolution in nature and vigorously attacked
Mereschkowsky by saying the claim that chloroplasts are incorporated cyanobacteria is without any empirical basis.
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Fig. 4. Updated geological time scale (Whiteeld, 2004) with key events in prokaryotic and
eukaryotic cell evolution (Tice and Lowe, 2004). The two major endosymbiotic events giving
rise to mitochondria and plastids are denoted as endosymbiosis 1 (which involved the
transition of a-proteobacteria-like organisms into proto-mitochondria) and endosymbiosis 2
(which involved the transition from cyanobacteria-like organisms into proto-plastids).
(Adapted from Kutschera and Niklas, 2004.)
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have been used to shed light on the composition of the Mesoproterozoic atmosphere
at a time when solar luminosity was signicantly lower than today. For example,
based on ion microprobe analyses of the carbon isotopes in individual Mesoproterozoic acritarchs extracted from North China, Kaufmann and Xiao (2003) conclude
that the atmospheric concentration of CO2 1400 mya was 10100 times that of
todays (ca. 400 parts per million, p.p.m.). It seems therefore that the second primary
endosymbiontic event responsible for the origin of modern-day chloroplasts may
have occurred during a CO2 peak in Earths history (Fig. 4).
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7.
8.
9.
10.
11.
11
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12. About 18% of the nuclear genes in the plant A. thaliana seem to come from
ancient cyanobacteria (Martin, 2003). In green algae and plants, the nuclearencoded chloroplast protein, Light-dependent NADPH-protochlorophyllide
oxidoreductase (LPOR), catalyses the light-mediated reduction of protochlorophyllide to chlorophyllide. Yang and Cheng (2004) conducted a genome-wide
sequence comparison, combined with a phylogenetic analysis. The authors
conclude that photosynthetic eukaryotes obtained their LPOR homologues from
ancient cyanobacteria through endosymbiotic gene transfer.
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pointed out by Falkowski et al. (2004), this genome encodes for both the small and
large subunits of the important enzyme ribulose-1,5-bisphosphate carboxylase/
oxygenase (Rubisco). In contrast, the genes encoding for the small subunit of this
enzyme were transferred to the nucleus of the host cells with green plastids.
That the barriers to lateral gene transfers from plastids to nuclei have been
breached repeatedly is attested to by tertiary as well as secondary endosymbiotic
events, which are best exemplied by the dinoagellates (Table 1, Fig. 7). Although
many dinoagellates are plastid-free, a large number of species has acquired plastids
from phyletically diverse endosymbiotic eukaryotic donors whose plastids were
themselves of secondary endosymbiotic origin, e.g., cryptomonad and chlorophyte
endosymbionts that were reduced functionally to mere plastids (Douglas, 1998;
Moreira and Philippe, 2001). Repeated endosymbiosis is further illustrated by those
dinoagellates living within the gastrointestinal cells of scleractinian corals. These
endosymbionts or zooxanthellae can provide as much as 100% of the
carbohydrates and low-molecular weight lipids required to sustain their cnidarian
hosts whose growth is limited primarily by nitrogen availability. In this regard, a
recent electron and epiuorescence microscopy study of the coral Montastraea
cavernosa indicates that this limitation to growth can be reduced or wholly
eliminated by the presence of endosymbiotic cyanobacteria living within their coral
host cells side by side with endosymbiotic dinoagellates (Lesser et al., 2004). In a
very real sense, M. cavernosa is a community of extraordinarily diverse pro- and
eukaryotic partners.
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A number of studies have shown that this clam species depends on these symbiotic
bacteria for its nutrition. Importantly, these bacteria are transmitted like
mitochondria via the eggs of the animal (Yaffe, 1999; Logan, 2003). Hurtado et
al. (2003) analysed the association between vesicomyid clams and their vertically
transmitted endosymbiotic bacteria and conclude that the bacteria have lost their
ability to live freely in the marine environment. This complete animalbacteria
interdependence may parallel ancient evolutionary processes by which eukaryotic
cells acquired mitochondria and plastids. In a series of studies, Kuznetsov and
Lebkova (2002) report electron microscopic and histochemical ndings that
document the apparent transition of symbiotic bacteria into mitochondria-like
organelles in near-hydrothermal inhabitants (bivalves) of the underwater MidAtlantic ridge. These investigators analysed gill tissues of bivalves of the genera
Nucula, Conchocele and Calyptogena and obtained similar results: the molluscs
depend strictly on endosymbiotic bacteria that show an ultrastructure very similar to
that of the mitochondria in ordinary eukaryotic cells.
Many endosymbiotic relationships exist between specic bacteria and invertebrate
hosts (Insecta) that appear to be the result of ancient infections followed by vertical
transmission within host lineages. The best-characterized insect endosymbiont is the
bacterium Buchnera amphidicola, a mutualist of aphids (Insecta: Homoptera)
(Moran and Baumann, 2000). Aphids suck phloem sap that is rich in many nutrients
but decient in amino acids that are provided by Buchnera, which are intracellular
and restricted to the cytoplasm of one insect cell type. As in other previous examples,
these endosymbionts are maternally inherited via the aphid ovary. Thus, the
insectbacteria association is essential for both partners. The Buchneraaphid
mutualism is obligatory. Douglas and Raven (2003) point out that the intracellular
Buchnera resemble endosymbiotic bacteria at the proto-organelle grade of
evolution and may aid in understanding how ancient proteobacteria became
mitochondria as residents of eukaryotic cells (see Fig. 4).
Perhaps the most impressive model system for the study of the origin and
evolution of eukaryotic organelles was described in 1876, just 2 years before the
publication of the rst formal denition for symbiosis (de Bary, 1878): the
discovery that the green pigment in many marine hermaphroditic sea slugs in the
ophistobranch order of Gastropods (Ascoglossa) was indistinguishable from
chlorophyll (see Muscatine and Greene, 1973). Although this nding led to the
erroneous conclusion that the sea slugs contained entire algal symbionts, we now
know that these animals feed by evacuating the cellular contents of siphonaceous
algae (Vaucheria litorea), transfer metabolically active chloroplasts into their bodies,
and engulf them phagocytotically into a specic layer of cells surrounding the
digestive tract (Figs. 6A and B). The chloroplasts are then distributed throughout the
animals body and become lodged only one cell layer beneath the epidermis. By these
means, the animals become green and capable of light-dependent photoautotrophic
CO2 xation. The chloroplasts remain active for a limited amount of time (Rumpho
et al., 2000). Repeated feedings on algae therefore are required to maintain a
population of living chloroplasts within the animals body. Nevertheless,
laboratory studies indicate that the solar-powered sea slugs were able to live
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Fig. 6. Dorsal view of the green slug Elysia chlorotica, feeding on the green siphonous alga
Vaucheria litorea (A). Electron micrograph (B) of an endosymbiontic chloroplast within a
host cell of the digestive tract of the animal. (Adapted from Rumpho et al., 2000).
Bars 1 cm (A), 2 mm (B).)
over 910 months like plants without uptake of organic substances. It has
been suggested that the unique chloroplast symbiosis may represent tertiary
endosymbiosis (i.e., macroevolution) in action (Rumpho et al., 2000), but many
questions as to the interaction between the chloroplast and the host tissue are
unanswered.
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separated the most ancient eukaryotic heterotrophic lineages from their photoautotrophic counterparts. That these primary endosymbiotic events cast a long
shadow and continued to play an important role in lifes history is evident from the
subsequent (and in some case very recent) appearance of novel unicellular eukaryotic
lineages resulting from secondary and tertiary endosymbiotic events (Table 1,
Fig. 7). For example, molecular clock studies indicate that diatoms (a
stramenopile lineage that is given divisional status by some workers and belongs
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Conclusions
Primary endosymbiotic events between archaeal-like host cells and a-proteobacteria are responsible for the appearance of the most ancient eukaryotic heterotrophic
lineages (e.g., diplomonads and microsporidians, kingdom protoctista) (Fig. 4).
Three lines of evidence provide the strongest support for this hypothesis. First,
mitochondria possess eubacterial-like DNA and transcription/translation systems
(e.g., ribosomes similar in size to those of prokaryotes); second, proteobacteria
possess infolded membranes similar to the cristae of mitochondria; and, third, strong
molecular sequence similarities, particularly those of 16S rRNA genes, between
mitochondria and a-proteobacteria genomes. Nevertheless, the genomes of mitochondria vary widely across eukaryotic lineages and they possess features that make it
extremely difcult to trace the evolutionary history of this organelle (Lang et al.,
1999). Subsequent endosymbiotic events involving the incorporation of coccoid
cyanobacteria-like endosymbionts within ancient eukaryotic host cells (Fig. 4) gave
rise to the most ancient photoautotropic lineages (e.g., chlorophytes and rhodophytes). Some of the lines of evidence for this hypothesis include the similarities in
cyanobacterial and plastid gene sequences, similarities in 16S rDNA and various
protein-coding sequences, and the presence of a self-splicing Group I intron in a
leucine transfer RNA gene of the cyanobacterium Anabaena, which has a similar
sequence and position to an intron found in the plastid genome (Xu et al., 1990).
Secondary and tertiary endosymbiotic events gave rise to evolutionarily more
recent algal lineages (e.g., euglenoids, cryptomonads, and dinoagellates) (Fig. 7).
Evidence for this hypothesis comes from the pigment compositions of the various
algal groups, the presence of additional membranes surrounding their plastids, and
the presence of nucleomorphs (nucleus-like structures) between the two outer
membranes. Among these recent algal lineages, those with red predominate,
perhaps because the red plastid genome is more self-sufcient in terms of
photosynthetic functionality. Lateral gene transfer from the mitochondrial and
plastid genomes to the nuclear genome occurred during primary, secondary, and
tertiary endosymbiotic events. For example, the gene tufA, which encodes for Tu (a
chloroplast-specic protein-synthesis elongation factor) resides in charophycean
nuclei and those of all embryophytes (i.e., members of the green lineage, see
Niklas, 2000; Scherp et al., 2001), but it remains encoded in the plastid genomes of
other groups of algae (Baldauf and Palmer, 1990). Lateral gene transfer is likely
responsible for the widespread phyletic distribution of the capacity to synthesize
cellulose (e.g., in chlorophytes, tunicates, oomycetes, and dinoagellates) as well as
chitin (e.g., in oomycetes, diatoms, and some chlorophytes). The integration of
endosymbiotic and host cell genomes into one functional unit is therefore responsible
for many macroevolutionary events and phenomena, not the least of which was the
division between pro- and eukaryotic organisms and the division between heteroand photoautotrophic eukaryotic lineages.
Clearly, the hypothesis of Mereschkowsky published one century ago in this
journal (Fig. 3) has evolved over the past decades into a solid scientic theory (sensu
Mahner and Bunge, 1997) that is supported by a large body of empirical data (Sitte,
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1989, 1991, 1994, 2001). In spite of the importance of endosymbiosis in the history of
life (Kutschera and Niklas, 2004), the relevance of symbiogenesis in the generation
of new species in the eukaryotic world of macroorganisms has been grossly
overestimated by some scientists. The currently popular book of Margulis and Sagan
(2002), which is quoted by many anti-evolutionists around the world, delivers the
basic message that genomic variation and natural selection are of subordinate
importance in the process of speciation. This erroneous conclusion is not based on
solid empirical evidence and it has provided cannon fodder to an anti-Darwinian
ideology that has no place in modern science.
Acknowledgements
This review article is dedicated to Prof. Dr. Dr. h.c. P. Sitte on the occasion of his
75th birthday. The cooperation of the authors was initiated by the Alexander von
Humboldt-Stiftung (AvH, Bonn, Germany).
References
Altmann, R., 1890. Die Elementarorganismen und ihre Beziehungen zu den Zellen. Verlag von Veit &
Comp., Leipzig.
Armbrust, E.V., Berges, J.A., Bowler, C., et al., 2004. The genome of the diatom Thalassiosira pseudonana:
ecology, evolution, and metabolism. Science 306, 7986.
Baldauf, S.L., Palmer, J.D., 1990. Evolutionary transfer of the chloroplast TufA gene to the nucleus.
Nature 344, 262265.
Baluska, F., Volkmann, D., Barlow, P.W., 2004. Eucaryotic cells and their cell bodies: cell theory revised.
Ann. Bot. 94, 932.
de Bary, A.H., 1878. Vortrag: Uber Symbiose. Tagblatt der 51. Versammlung Deutscher Naturforscher
und Aerzte in Cassel. Baier & Lewalter, Kassel, pp. 121126.
Bekker, A., Holland, H.D., Wang, P.-L., Rumble, D., Stein, H.J., Hanna, J.L., Coetzee, L.L., Beukes,
N.J., 2004. Dating the rise of atmospheric oxygen. Nature 427, 117120.
Ben-Shem, A., Frolow, F., Nelson, N., 2003. Crystal structure of plant photosystem I. Nature 426,
530635.
Bhattacharya, D., Yoon, H.S., Hackett, J.D., 2003. Photosynthetic eukaryotes unite: endosymbiosis
connects the dots. BioEssays 26, 5060.
Cavalier-Smith, T., 1975. The origin of nuclei and of eukaryotic cells. Nature 256, 463468.
Cavalier-Smith, T., 2000. Membrane heredity and early chloroplast evolution. Trends Plant Sci. 5,
174182.
Cowen, R., 2000. History of Life, third ed. Blackwell Science, Oxford.
Coyne, J.A., Orr, H.A., 2004. Speciation. Sinauer, Sunderland, MA.
de Duve, C., 1996. The birth of complex cells. Sci. Am. 274 (4), 3845.
Douglas, S., 1998. Plastid evolution: origins, diversity, trends. Curr. Opin. Genet. Dev. 8, 655661.
Douglas, A.E., Raven, J.A., 2003. Genomes at the interface between bacteria and organelles. Phil. Trans.
R. Soc. Lond. B 358, 518.
Douglas, S., Zauner, S., Fraunholz, M., et al., 2001. The highly reduced genome of an enslaved algal
nucleus. Nature 410, 10911096.
Dyall, S.D., Brown, M.T., Johnson, P.J., 2004. Ancient invasions: from endosymbionts to organelles.
Science 304, 253257.
Falkowski, P.G., Katz, M.E., Knoll, A.H., Quigg, A., Raven, J.A., Schoeld, O., Taylor, F.J.R., 2004.
The evolution of modern eukaryotic phytoplankton. Science 305, 354360.
Famintzin, A., 1907. Die Symbiose als Mittel der Synthese von Organismen. Biol. Centralbl. 27, 353363.
Friedl, T., Bhattacharya, D., 2001. Origin and evolution of green lichen algae. Symbiosis 27, 341357.
ARTICLE IN PRESS
22
Frohlich, M., Kutschera, U., 1994. Chloroplast development in rye coleoptiles. Bot. Acta 107, 1217.
Graham, L.E., Wilcox, L.W., 2000. Algae. Prentice Hall, New Jersey.
Gray, M.W., 1992. The endosymbiont hypothesis revisited. Int. Rev. Cytol. 141, 233357.
Gray, M.W., Burger, G., Lang, B.F., 1999. Mitochondrial evolution. Science 283, 14761481.
Hartman, H., Fedorov, A., 2002. The origin of the eukaryotic cell: a genomic investigation. Proc. Natl.
Acad. Sci. USA 99, 14201425.
Hentschel, U., Steinert, M., Hacker, J., 2000. Common molecular mechanisms of symbiosis and
pathenogenesis. Trends Microbiol. 8, 226231.
Hornschuh, M., Grotha, R., Kutschera, U., 2002. Epiphytic bacteria associated with the bryophyte
Funaria hygrometrica: effects of Methylobacterium strains and protonema development. Plant Biol. 4,
682687.
Hoxtermann, E., 1998. Konstantin S. Merezkovskij und die Symbiogenesetheorie der Zellevolution. In:
Geus, A. (Ed.), Bakterienlicht & Wurzelpilz. Endosymbiosen in Forschung und Geschichte.
Basiliskenpresse, Marburg, pp. 1129.
Hurtado, L.A., Mateos, M., Lutz, R.A., Vrijenhoek, R.C., 2003. Coupling of bacterial endosymbiont and
host mitochondrial genomes in the hydrothermal vent clam Calyptogena magnifica. Appl. Environ.
Microbiol. 69, 20582064.
Kaufmann, A.J., Xiao, S., 2003. High CO2 levels in the Proterozoic atmosphere estimated from analyses of
individual microfossils. Nature 425, 279282.
Keeling, P.J., 2004. Diversity and evolutionary history of plastids and their hosts. Am. J. Bot. 91,
14811493.
Knoll, A.H., 2003. Life on a Young Planet: The First Billion Years of Evolution on Earth. Princeton
University Press, Princeton, NJ.
Koositra, W.H.C.F., De Stefano, M., Mann, D.G., Medlin, L., 2002. The phylogeny of diatoms. Progr.
Mol. Subcell. Biol. 33, 5997.
Kuhlbrandt, W., 2003. Dual approach to a light problem. Nature 426, 399400.
Kutschera, U., 2001. Evolutionsbiologie. Eine allgemeine Einfuhrung. Parey Buchverlag, Berlin.
Kutschera, U., 2002. Bacterial colonization of sunower cotyledons during seed germination. J. Appl. Bot.
76, 9698.
Kutschera, U., 2003. A comparative analysis of the DarwinWallace papers and the development of the
concept of natural selection. Theory Biosci. 122, 343359.
Kutschera, U., Hoss, R., 1995. Mobilization of starch after submergence of air-grown rice coleoptiles.
Implications for growth and gravitropism. Bot. Acta 108, 266269.
Kutschera, U., Niklas, K.J., 2004. The modern theory of biological evolution: an expanded synthesis.
Naturwissenschaften 91, 255276.
Kutschera, U., Siebert, C., Masuda, Y., Sievers, A., 1990. Effects of submergence on development and
gravitropism in the coleoptile of Oryza sativa L. Planta 183, 112119.
Kuznetsov, A.P., Lebkova, N.P., 2002. On bacterial origin of mitochondria in Eukaryotes in light of
current ideas of evolution of the organic world. Biol. Bull. 29, 501507.
Lang, B.F., Gray, M.W., Burger, G., 1999. Mitochondrial genome evolution and the origin of eukaryotes.
Annu. Rev. Genet. 33, 351397.
Lesser, M.P., Mazel, C.H., Gorbunov, M.Y., Falkowski, P.G., 2004. Discovery of symbiotic nitrogrenxing cyanobacteria in corals. Science 305, 9971000.
Lloyd, D., 1974. The Mitochondria of Microorganisms. Academic Press, London.
Logan, D.C., 2003. Mitochondrial dynamics. New Phytol. 160, 463478.
Lopez-Garcia, P., Moreira, D., 1999. Metabolic symbiosis and the origin of eukaryotes. Trends Biochem.
Sci. 24, 8893.
Mahner, M., Bunge, M., 1997. Foundations of Biophilosophy. Springer, Berlin, Heidelberg, New York.
Maier, U.-G., Douglas, S.E., Cavalier-Smith, T., 2000. The nucleomorph genomes of Cryptophytes and
Chlorarachinophytes. Protist 151, 103109.
Margulis, L., 1970. Origin of Eukaryotic Cells. Yale University Press, New Haven.
Margulis, L., 1990. Words as battle cries symbiogenesis and the new eld of endocytobiology. BioScience
40, 673677.
Margulis, L., 1993. Symbiosis in Cell Evolution. Microbial Communities in the Archean and Proterozoic
Eons, second ed. W. H. Freeman & Co., New York.
Margulis, L., Sagan, D., 2002. Acquiring Genomes. A Theory of the Origin of Species. Basic Books, New
York.
Martin, W., 2003. Gene transfer from organelles to the nucleus: frequent and in big chunks. Proc. Natl.
Acad. Sci. USA 100, 86128614.
ARTICLE IN PRESS
U. Kutschera, K.J. Niklas / Theory in Biosciences 124 (2005) 124
23
Martin, W., Muller, M., 1998. The hydrogen hypothesis for the rst eukaryote. Nature 392, 3741.
Martin, W., Russel, M.J., 2003. On the origins of cells: a hypothesis for the evolutionary transitions from
abiotic geochemistry to chemoautotrophic procaryotes, and from procaryotes to nucleated cells.
Philos. Trans. R. Soc. Lond. B 358, 5985.
Martin, W., Hoffmeister, M., Rotte, C., Henze, K., 2001. An overview of endosymbiotic models for the
origins of eukaryotes, their ATP-producing organelles (mitochondria and hydrogenosomes), and their
heterotrophic lifestyle. Biol. Chem. 382, 15211539.
Martin, W., Rotte, C., Hoffmeister, M., Theissen, U., Gelius-Dietrich, G., Ahr, S., Henze, K., 2003. Early
cell evolution, eukaryotes, anoxia, sulde, oxygen, fungi rst (?), and a tree of genomes revisited.
IUBMB Life 55, 193204.
Mayr, E., 2001. What Evolution Is. Basic Books, New York.
McFadden, G., Gilson, P., 1995. Something borrowed, something green: lateral transfer of chloroplasts by
secondary endosymbiosis. Trends. Ecol. Evol. 10, 1217.
Meeuson, S., McCaffery, J.M., Nunnari, J., 2004. Mitochondrial fusion intermediates revealed in vivo.
Science 305, 17471752.
Mereschkowsky, C., 1905. Uber Natur und Ursprung der Chromatophoren im Panzenreiche. Biol.
Centralbl. 25 593604, 689691.
Mereschkowsky, C., 1910. Theorie der zwei Plasmaarten als Grundlage der Symbiogenese, einer neuen
Lehre von der Entstehung der Organismen. Biol. Centralbl. 30 278303, 321347, 353367.
Mereschkowsky, C., 1920. La plante consideree comme un complexe symbiotique. Bull. Soc. Sci. Nat.
France 6, 1798.
Meyer, A., 2002. Viewing life as cooperation. Nature 418, 275276.
Moran, N.A., Baumann, P., 2000. Bacterial endosymbionts in animals. Curr. Opin. Microbiol. 3, 270275.
Morden, C.W., Sherwood, A.R., 2002. Continued evolutionary surprises among dinoagellates. Proc.
Natl. Acad. Sci. USA 99, 11,55811,560.
Moreira, D., Philippe, H., 2001. Sure facts and open questions about the origin and evolution of
photosynthetic plastids. Res. Microbiol. 152, 771787.
Muscatine, L., Greene, R.W., 1973. Chloroplasts and algae as symbionts in molluscs. Int. Rev. Cytol. 36,
137169.
Niklas, K.J., 1997. The Evolutionary Biology of Plants. The University of Chicago Press, Chicago and
London.
Niklas, K.J., 2000. The evolution of plant body plans a biomechanical perspective. Ann. Bot. 85,
411438.
Niklas, K.J., 2004. The walls that bind the tree of life. BioScience 54, 831841.
Nobles, P.R., Romanovicz, D.K., Brown, R.M., 2001. Cellulose in Cyanobacteria. origin of vascular plant
cellulose synthase? Plant Physiol. 127, 529542.
Osteryoung, K.W., Nunnari, J., 2003. The division of endosymbiotic organelles. Science 302, 16981704.
Paschen, S.A., Waizenegger, T., Stan, T., Preuss, M., Cyrklaff, M., Hell, R., Rapaport, D., Neupert, W.,
2003. Evolutionary conservation of biogenesis of beta-barrel membrane proteins. Nature 426, 862866.
Pennisi, E., 2004. The birth of the nucleus. Science 305, 766768.
Rumpho, M.E., Summer, E.J., Manhart, J.R., 2000. Solar-powered sea slugs. Mollusc/algal chloroplast
symbiosis. Plant Physiol. 123, 2938.
Sachs, J., 1882. Vorlesungen uber Panzen-Physiologie. Verlag W. Engelmann, Leipzig.
Saffo, M.B., 1992. Invertebrates in endosymbiotic associations. Am. Zool. 32, 557565.
Scherp, P., Grotha, R., Kutschera, U., 2001. Occurrence and phylogenetic signicance of cytokinesisrelated callose in green algae, bryophytes, ferns and seed plants. Plant Cell Rep. 20, 143149.
Schilthuizen, M., 2001. Frogs, Flies and Dandelions. The Making of Species. Oxford University Press,
Oxford.
Schimper, A.F.W., 1885. Untersuchungen uber die Chlorophyllkorper und die ihnen homologen Gebilde.
Jahrb. f. wiss. Botanik 16, 1247.
Schopf, J.W., 1999. Cradle of Life. The Discovery of Earths Earliest Fossils. Princeton University Press,
Princeton, NJ.
Schwemmler, W., Schenk, H.E.A. (Eds.), 1980. Endocytobiology. Endosymbiosis and Cell Biology.
Walter de Gruyter & Co., Berlin, New York.
Sitte, P., 1989. Phylogenetische Aspekte der Zellevolution. Biol. Rundsch. 28, 118.
Sitte, P., 1991. Die Zelle in der Evolution des Lebens. Biol. in unserer Zeit 21, 8592.
Sitte, P., 1994. Die Evolution von Zellen: Innovation durch Symbiogenese. In: Wieser, W. (Ed.), Die
Evolution der Evolutionstheorie. Von Darwin zur DNA. Spektrum Akademischer Verlag, Berlin,
Heidelberg, pp. 77108.
ARTICLE IN PRESS
24
Sitte, P., 2001. Symbiogenese in der Zell- und Lebensevolution. In: Storch, V., Welsch, U., Wink, M.
(Eds.), Evolutionsbiologie. Springer, Berlin, Heidelberg, pp. 196208.
Stoebe, B., Maier, U.-G., 2002. One, two, three: natures tool box for building plastids. Protoplasma 219,
123130.
Taylor, F.J.R., 1979. Symbionticism revisited: a discussion of the evolutionary impact of intracellular
symbioses. Proc. R. Soc. Lond. B 204, 267286.
Thompson, J.N., 1987. Symbiont-induced speciation. Biol. J. Linn. Soc. 32, 385393.
Tice, M.M., Lowe, D.R., 2004. Photosynthetic microbial mats in the 3416-Myr-old ocean. Nature 431,
549552.
Timmis, J.N., Ayliffe, M.A., Huang, C.Y., Martin, W., 2004. Endosymbiotic gene transfer: organelle
genomes forge eukaryotic chromosomes. Nat. Rev. Genet. 5, 123135.
Vargas, W., Cumino, A., Salerno, G.L., 2003. Cyanobacterial alkaline/neutral invertases. Origin of
sucrose hydrolysis in the plant cytosol? Planta 216, 951960.
Walden, W.E., 2002. From bacteria to mitochondria: aconitase yields surprises. Proc. Natl. Acad. Sci.
USA 99, 41384140.
Wallin, I.E., 1927. Symbionticism and the Origin of Species. Bailliere, Tindall & Cox, London.
Whiteeld, J., 2004. News feature: time lords. Nature 429, 124125.
Whitehead, L.F., Day, D.A., 1997. The peribacteroid membrane. Physiol. Plant 100, 3044.
Wilkinson, D.M., 2001. At cross purposes. Nature 412, 485.
Wilson, E.B., 1925. The Cell in Development and Heredity, third ed. McMillan Co., New York.
Woese, C.R., 2002. On the evolution of cells. Proc. Natl. Acad. Sci. USA 99, 87428747.
Xu, M.-Q., Kathe, S.D., Coodrich-Blair, H., Nierzwicki-Bauer, S.A., Shub, D.A., 1990. Bacterial origin of
a chloroplast intron: conserved self-splicing Group I introns in cyanobacteria. Science 250, 15661572.
Yaffe, M.P., 1999. The machinery of mitochondrial inheritance and behavior. Science 283, 14931497.
Yang, J., Cheng, Q., 2004. Origin and evolution of the light-dependent Protochlorophyllide
Oxidoreductase (LPOR) genes. Plant Biol. 6, 537544.
Zhang, M., Mileykovskaya, W., Dowhan, X., 2002. Glueing the respiratory chain together. J. Biol. Chem.
277, 4355343556.