Biological Journal ofthe Linnean Sacit& (1982), 17: 289-306 With 2 figures
The origins of plastids
T. CAVALIER-SMITH, F.L.S.
Department of Biophysics, King’s College, London University,
2&29 Drury Lane, London WC2B 5RL
Accepttd for publication S$&tnber 1981
A new theory of plastid origins is presented in which only two symbiotic events are needed to explain
the origin of the six fundamentally different types ofplastid, which all probably originated in anteriorly
biciliated phagotrophic cells. Four of them can be derived directly from a single endosymbiotic
cyanophyte by the independent loss of different cyanophyte characters and the evolution of new
characters in the immediate descendants of this primary endosymbiosis. Retention of the phagosomal
membrane as well as the prokaryotic plasma and outer membrane could produce the dinozoan and
euglenid plastids with three envelope membranes, whereas the loss of the phagosomal membrane could
produce the two-membraned envelopes characteristic of the Biliphyta and Verdiplantae*. The
phycobilins were retained essentially unaltered in the Biliphyta, but are modified or lost in the other
lines. In the ancestor of the Euglenozoa and Verdiplantae they were replaced by chlorophyll b. I n the
ancestor of algae possessing chlorophyll c they were modified to the cryptophyte type, concomitantly
with the evolution of chlorophyll cz : one line of descent from this ancestor produced the dinozoan
plastid by the complete loss of phycobilins, while the other was incorporated by endosymbiosis into
another phagotrophic bibiliate to produce the cryptophyte plastid. The latter evolved into the
chromophyte plastid by the loss of phycobilins and the evolution of chlorophyll c,. The conversion of
the endosymbiont into a plastid depended on the evolution of a system to transport proteins into it. I
argue that this occurred by the modification of the pre-existing mitochondrial transport system, and
that the major modifications needed to adjust this to plastids with more than two envelope membranes
led to evolution of a new tubular o r disc-like morphology for the mitochondrial cristae of these groups.
This new cristal morphology is maintained by stabilizing selection even in species that have secondarily
lost plastids.
KEY WORDS :-Plastids - mitochondria - coevolution - protein translocation
Euglena - dinoflagellates - Cyanophora plastid envelope - phylogeny.
-
endosymbiont
-
~
CONTENTS
Introduction . . . . . . . . . . . . . . . . . . .
Defects of existing theories for the origin of plastids with three envelope membranes . .
A prokaryotic origin for dinozoan and euglenozoan plastids . . . . . . . .
Origin of the cryptophyte and chromophyte plastids . . . . . . . . . .
The relationship between cv(Inophora, other Glaucophyceae, and the Rhodophyceae . .
The Origin of the Euglenozoa and Verdiplantae.
. . . . . . . . . .
Nature of the ancestral biciliate ‘hosts’ and the origin of mitochondrial diversity . . .
The relationship between plastids containing phycobilins and those containing chlorophyll
b or cz
Testing the theory.
. . . . . . . . . . . . . . . . .
References.
. . . . . . . . . . . . . . . . . . .
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INTRODUCTION
Only a few biologists (e.g. Uzzell & Spolsky, 1981) now dispute the theory of
Schimper ( 1883) and Mereschkowsky ( 1905, 1910) that plastids originated
endosymbiotically. A major reason for the growing acceptance of the theory since
*Author’s Note: Vcrdiplantae should read Viridiplantae throughout.
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0 1982 The Linnean Society of London
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T. CAVALIER-SMITH
it was revived by Ris (1961) is the apparently simple way it explains plastid
diversity in eukaryotes in terms of separate symbiotic events involving different
hosts and symbionts (Mereschkowsky, 1910; Sagan, 1967; Raven, 1970). Six
fundamentally different plastid types are known (Cavalier-Smith, 1981a), and
each is present in a cell with other distinctive features sufficient to justify their
classification into separate kingdoms or subkingdoms (Cavalier-Smith, 1981b). It is
widely agreed that two of these plastid types arose endosymbiotically: red algal
plastids from the prokaryotic cyanophytes (Mereschkowsky, 1905; Ris, 1961 ;
Echlin, 1966; Sagan, 1967; Margulis, 1970; Taylor, 1970; Stanier, 1974),
cryptophyte plastids by uptake of a eukaryote endosymbiont (Greenwood,
Griffiths & Santore, 1977; Whatley, John & Whatley, 1979; Gibbs & Gillott,
1980; Gibbs, 1981). So also is the idea that chromophyte plastids evolved from
cryptophyte ones autogenously by the loss of phycobilins (Cavalier-Smith, 1977,
1978; Gibbs, 1981). Thus the two groups with a double-membraned plastid
endoplasmic reticulum (plastid ER) surrounding the plastid probably did not
evolve their plastids directly from prokaryote endosymbionts.
Although few authors now go to the extreme of postulating 20 independent
endosymbioses (Sagan, 1967) to form plastids from prokaryotes, many accept the
hypothesis that chlorophyte plastids evolved from prokaryotic symbionts like
Prochloron (Lewin, 1981) independently of the origin of red algal plastids from
cyanophytes. The idea that dinozoan and euglenoid plastids had separate origins
as eukaryote endosymbionts is also widely discussed (Whatley, 1981;Gibbs, 1981).
However, too little attention has yet been given to the nature of the possible hosts
for those postulated endosymbioses for the idea of independent symbiotic origins of
these plastids to be substantiated. At first sight it would appear that the differences
in non-plastid characters between the six photosynthetic eukaryotic kingdoms
supports the idea of several independent symbioses. However, an alternative
explanation for these basic differences is that they arose after the initial
endosymbiosis that led to the formation of plastids and that all eukaryote plastids
are descended by divergent evolution from a single endosymbiotic cyanophyte.
This paper discusses aspects of the process of conversion of a cyanophyte into a
plastid, which makes such divergence highly probable, and provides a unified
phylogeny for eukaryote plastids and their hosts. As this phylogeny requires only
one symbiotic event (that producing the Cryptophyta for which the nucleomorph
(Greenwood et al., 1977) provides evidence) in addition to the primary symbiotic
uptake of a cyanophyte, for which Cjranophora provides firm evidence (Herdman &
Stanier, 1977), the attempt to ‘relate the various classes of algae directly to each
other’ is not as ‘futile’ as it once appeared (Sagan, 1967). Consideration of the
mechanism of conversion of an endosymbiont into a plastid also leads to a new
theory of the origin of mitochondria1 diversity.
DEFECTS OF EXISTING THEORIES FOR THE ORIGIN OF PLASTIDS WITH THREE ENVELOPE
MEMBRANES
The direct derivation of Dinozoa* and Euglenozoa* from a eukaryote ancestor
with two plastid envelope membranes, as in the Biliphyta* and Chromophyta*,
would involve the arbitrary acquisition of a third envelope membrane for no
*These and other names of major taxa are those explained in Cavalier-Smith (1981b).
THE ORIGINS OF PLASTIDS
29 I
obvious reason and from no obvious source. Therefore, autogenous theories must
assume that they were derived from species with a plastid ER by the loss of one of
the four membranes around the plastid. It was initially proposed that this occurred
by the lateral fusion of two of the membranes (Gibbs, 1970), but such a process is
entirely without precedent, and would pose severe and perhaps insuperable
biophysical problems. A much more plausible way of reducing the number of
membranes is by the loss of the outer, ribosome-bearing, membrane of the plastid
ER, leaving three smooth envelope membranes and no remaining connection to
the nuclear envelope (Lee, 1977; Cavalier-Smith, 1978). The Dinozoa could be
directly derived in this way from the Chromophyta, but no suitable chlorophyll-bcontaining ancestor is available for this mode of origin for the Euglenozoa.
Two non-autogenous theories have therefore been proposed. One is that the
euglenozoan and dinozoan plastids originated by the endosymbiotic uptake of
whole eukaryote cells (Gibbs, 1978, 1981), and that the third membrane
corresponds with the plasma membrane of the preserved symbiont. This theory is
reasonably plausible for the Euglenozoa, where the Chlorophyta provide possible
ancestors for the symbiont, even though it involves the loss not only of the
phagosome membrane, but of every trace of the symbiont except its plastid and
plasma membrane-this degree of reduction is much greater than in other known
cases involving eukaryote endosymbiosis. For the Dinozoa, however, the theory is
much less plausible, because no eukaryotes exist with plastids of the required type
(chlorophyll c,, no phycobilins, two envelope membranes and no plastid ER).
Moreover, the existence of a few dinoflagellates with only two envelope
membranes (Gibbs, 1981) makes a prokaryotic origin of their plastids more likely,
as discussed below.
The second symbiotic theory (Whatley et ul., 1979; Whatley, 1981) proposes that
euglenozoan and dinozoan plastids evolved from eukaryote plastids taken
up symbiotically from other eukaryotes (the possibility of a similar origin for
glaucophyte plastids has also been mentioned, Cavalier-Smith, 1978).This theory
also lacks a suitable plastid ancestor for the dinozoan ancestor. It has the serious
additional defect, also emphasized by Gibbs (1981), that eukaryote plastids lack
many of the genes coding for their own synthesis. Because of this incomplete
autonomy, endosymbiosis of isolated eukaryote plastids can only be a temporary
phenomenon, as occurs for the chloroplasts of Codium frugile in the seaslug ECysia
(Trench, 1981). Even though such plastids may be able to replicate their DNA and
divide once (or even more), their indefinitely continued propagation would not be
possible in the absence of their necessary nuclear genes.
A PROKARYOTIC ORIGIN FOR DINOZOAN AND EUGLENOZOAN PLASTIDS
It is usually assumed that uptake ofa prokaryote endosymbiont into a phagosome
could only produce a plastid with two envelope membranes: an inner one deriving
from the symbiont’s plasma membrane, and an outer one deriving from the
phagosome membrane. But this assumption neglects the fact that gram-negative
bacteria all have a second ‘outer’ lipoprotein membrane in the cell wall outside the
peptidoglycan layer (Braun, 1978). Since all prokaryotes with oxygenic
photosynthesis are gram-negative and have an outer membrane, it is perfectly
possible that this outer membrane could be retained following an endosymbiotic
292
T. CAVALIER-SMITH
event to form a third membrane in the plastid envelope in between the former
plasma and phagosome membranes. I propose that this is how the triple envelope
membrane of the Dinozoa and Euglenozoa evolved. In the case of the Euglenozoa,
the endosymbiont could have been a prochlorophyte possessing chlorophyll b like
Prochloron (Leedale, 1978); whereas in the case of the Dinozoa it could have been a
chlorophyll-c,-containing prokaryote like that hypothesized by Raven ( 1970).
Even though such a prokaryote is not known, it might have become extinct as a
result of competition with its photosynthetic eukaryote descendants. If the
chlorophyll-c,-containing prokaryote was a planktonic relative of the Cyanophyta,
having gas vacuoles but no flagella, and the adaptive zone it occupied is now filled
by the chlorophyll-c-containingphytoplankton, notably the Dinozoa, Haptophyta,
Bacillariophyceaeand Chrysophyceae, then these latter groups might just possibly
have supplanted it because of the advantages of having cilia, mitochondria,
phagotrophy and/or efficient saprotrophy. A more economical hypothesis,
however, is that the symbiont was a cyanophyte, and that chlorophyll c, evolved
during its conversion into the dinozoan plastid. The few Dinozoa with only two
envelope membranes could have evolved by the loss of the prokaryotic outer
membrane (i.e. the middle membrane in other Dinozoa), as is usually assumed to
be the case for the chlorophyte and biliphyte plastids. However, if, as I argue, the
outer membrane of the endosymbiont can be retained doing the conversion to a
plastid, then one must consider the possibility that it is the phagosome membrane
that was lost, not only in these exceptional dinoflagellates but also in other cases
and that the outer envelope membrane in the Chlorophyta and Biliphyta may be
homologous with the prokaryote outer membrane rather than the phagosome
membrane. The origin of its special permeability properties might be easiest to
explain by this idea. It is well known that the phagosome membrane has been lost
in several cellular endosymbionts which are free in the cytoplasm (Whatley et al.,
1979; Gibbs, 1981; Trench, 1981), but there is not a single proven case of the loss
of the outer membrane ofa gram-negative endosymbiont. Therefore, I suggest that
in all plastids, both the plasma and outer wall membrane of the prokaryotic
endosymbiont are retained. If the phagosome membrane also is retained, one has a
triple, if not a double envelope (Fig. 1 A-D).
One advantage of postulating a direct origin of the dinozoan plastid from a
prokaryote endosymbiont is that the great diversity of eyespots in the phylum can
be readily understood as the result of independent origin in different species. O n
the more conventional theory of a chromophyte origin for the dinoflagellate
plastid, one might have expected then to have simply inherited one of the
chromophyte eyespot types.
ORIGIN OF THE CRYPTOPHYTE AND CHROMOPHYTE PLASTIDS
An essential corollary of the above hypothesis is that the cryptophyte and
chromophyte plastids which also contain chlorophyll-c, evolved from dinozoan
plastids. This can only be the case if the cryptophyte phycobilins are derived not
directly from those of the Biliphyta as often supposed (Gibbs, 1981; Whatley et al.,
1979), but arose either de mu0 or from the Dinozoa. Since the Dinozoa have no
phycobilins, and since the cryptophyte phycobilins are very different from the
biliphyte ones, a de mu0 origin is superficially plausible. Recent studies of
T H E ORIGINS OF PLASTIDS
293
Figure I . The origin of the characteristic topology of plastid envelopes in eukaryotes. A phagotrophic
biciliate (A) with a single nucleus (n) engulfed a gram-negative photosynthetic prokaryote (B) with a
plasma membrane and an outer membrane to yield a photosynthetic biciliate (C) with three
membranes surrounding its plastid (p) as in the Euglenozoa and most Dinozoa. The third outermost
membrane is the phagosome membrane. Lou of the phagosome membrane can produce a plastid with
two bounding membranes (D) as in the Biliphyta, Verdiplantae, and a very few Dinozoa. Symbiotic
uptake of such a eukaryote (E) by a non-photosynthetic phagotroph (A) followed by fusion of the
phagosome membrane with the nuclear envelope produces a cryptophyte arrangement (F) with a
plastid endoplasrnic reticulum (per) surrounding the eukaryote endosymbiont’s vestigial cytoplasm
and nucleus (now represented by the nucleomorph, labelled arrow). The outer membrane of the
plastid ER is derived by fusion of phagosome and outer nuclear envelope membranes and has
ribosomes on it like the nuclear envelope: the three-membraned envelope of the Euglenozoa and
Dinozoa (C) never fused with the nuclear envelope so never acquired ribosome binding sites. Theinner
membrane of the PER is the former plasma membrane of the eukaryote endosymbiont (D). Loss of the
contents of the nucleomorph-containing compartment gave the arrangement of four concentric
membranes seen in the Chromophyta (G). The outer membrane of the prokaryote was retained in all
plastids, but the thin peptidoglycan layer (not shown here) lying between it and the prokaryotic
plasma membrane was lost in all except Cyanophora. A minimum of two endosymbioses are therefore
needed to explain the origins of plastids.
cryptophyte sequences, however, show strong sequence homology between one
cryptophyte and one biliphyte phycobiliprotein (MacColl & Berns, 1979), which
firmly rules out de novo origin. However, a second biliprotein shows almost no
sequence homology between the two groups, which also make improbable a direct
derivation of the cryptophyte plastid from those of red algae as has often been
proposed (Dodge, 1979; Gibbs, 1981). Therefore, two other possibilities must be
considered.
One is that there once existed a free-living prokaryote, which had thylakoids
fundamentally the same as in the cryptophyte, i.e. arranged in pairs with
biliproteins inside the thylakoids rather than on their surface as in cyanophytes and
294
T. CAVALIER-SMITH
biliphytes, and with chlorophyll c, (but not c , ) . I call this hypothetical prokaryote
a procryptophyte. If the organism that ultimately became the difiozoan plastid was
a procryptophyte with cryptophytic phycobilins, rather than a prokaryote
possessing only chlorophyll c,, then its endosymbiotic uptake by a dinozoan host
could lead, by the differential loss of different symbiont properties, to three
separate evolutionary lines. (1) A line that lost the phycobilins to yield the majority
of the modern Dinozoa; (2) a line that also lost the phagosome membrane leading
to the Dinozoa with double-membraned envelopes; and (3)a line that retained the
phycobilins but lost the phagosome membrane to yield an organism with
cryptophyte phycobilins and chlorophyll c, but no plastid ER. This third organism
is now extinct in its free living form but ‘survives’as a much reduced endosymbiont
in the lumen of the plastid ER of the Cryptophyta (Fig. 1F). The presence of starch
in the compartment containing the cryptophyte cryptonucleus indicates that the
symbiont that gave rise to the cryptophyte plastid and cryptonucleus must have
stored starch in its cytoplasm; this is usually seen as support for the idea that it was
a red alga-but as dinozoa also store starch in the cytoplasm and unlike red algae
process chlorophyll c,, and red algal phycobilins differ from those of cryptophytes,
a dinoflagellate that had not yet lost the phycobilins from its procryptophyte
endosymbiont is a far more suitable candidate.
As in previous theories, the chromophyte plastid can readily be derived from the
cryptophyte one by the loss of phycobilins and the nucleomorph compartment
(Fig. lF, G) and the origin of chlorophyll c,, which significantly is absent in both
the Dinozoa and the Cryptophyta. The unique occurrence of the carotenoid
peridinin in the Dinozoa is readily explained if it was present in the
procryptophyte but was lost during or prior to the formation of the cryptophyte
plastid. I therefore predict that if a procryptophyte is ever found in some remote
part of the world it will have the following characters: (1 gram negative wall; (2)
paired thylakoids containing phycobilins homologous wit those of cryptophytes ;
(3) chlorophyll c, but not c , ; (4)peridinin; and (5) gas vacuoles. Such an
organism could, like Prochloron, be a specialized offshoot of the Cyanophyta.
The second possibility, which I prefer, is that a free-living procryptophyte never
existed but only evolved from a cyanophyte ancestor after it became an
endosymbiont and was well on its way towards becoming a plastid (see later
section).
i
THE RELATIONSHIP BETWEEN CYANOPHORA, OTHER GLAUCOPHYCEAE, AND THE
RHODOPHYCEAE
If, as argued above, elements of the cell wall of prokaryotic endosymbionts may
be retained in highly evolved plastids, and a single endosymbiosis may give rise to
several different lines by the loss of different prokaryotic components, it becomes
necessary to re-evaluate the position of Cyanophora and the Glaucophyceae. These
organisms are usually dismissed as mere analogies showing how the endosymbiosis
of a cyanophyte could in principle lead to the origin of a red algal plastid, and
treated as a mere ragbag of independent and rather recent endosymbioses of no
phylogenetic import. I propose that on the contrary they are all derivatives of the
very same endosymbiotic event that gave rise to the red algal plastid, and have
THE ORIGINS OF PLASTIDS
295
profound implications for eukaryote phylogeny. Apart from Paulinella, which is
clearly a thecamoeba and which may well be a recent and poorly established
symbiosis, the painstaking work of Kies (Kies, 1979; 1980) and his colleagues
(Kremer, Kies & Rostami-Rabet, 1979; Kremer, Feige & Schneider, 1978) has
clearly established that there is an evolutionary relationship between the ‘host’ cell
of four ‘cyanelk’-bearing organisms Cyanophora, Glaucocystis, Gloeochaete and
Glaucosphaera, and that these cannot be assigned to any existing non-phycobilincontaining eukaryote taxon. Therefore, the establishment of a separate taxon for
them (Skuja, 1954) is entirely justified. Kies (1979, 1980) follows Skuja in giving
them phylum status as the Glaucophyta. I prefer to emphasize their relationship to
the red algae by treating them as a class, the Glaucophyceae, grouped with the
class Rhodophyceae (red algae) in a new phylum (and kingdom) Biliphyta
(Cavalier-Smith, 1981b) . The plastids of Glaucocystis, Gloeochaete and Glaucosphaera
are indistinguishable from those of the red algae. That of Cyanophora differs only by
having retained the peptidoglycan layer of the cell wall as well as the outer
membrane (Herdman & Stanier, 1977; Aitken & Stanier, 1979). I do not accept
that this means that the Cyanophora endosymbiosis is of recent origin. If the outer
wall membrane can be retained for hundreds of millions of years, as I have argued
for the Euglenozoa and Dinozoa, why not also the peptidoglycan? The conversion
of a prokaryote into a plastid must involve a succession of steps that probably took
many cell generations. It is usually assumed that all the steps were completed prior
to any subsequent speciation. However, if, as seems a priori more reasonable, some
diversification occurred during the process, it would not be surprising to find a
number of different types of plastid arising as a result of differences in the
conversion process in different lines. All the evidence supports the idea that the
Glaucophyceae (the four genera referred to above) and the Rhodophyceae all
derive from a single symbiotic event. The Glaucophyceae and Rhodophyceae both
have starch in their cytoplasm. No existing definition of the Rhodophyceae would
exclude the non-ciliate Glaucospharea. The spectrum running from Glaucosphaera,
through Cyanidium to unicellular red algae, such as Porphyridium aerugineum and
purpureum is continuous. When it was thought that red algal plastids had an
autogenous origin but that glaucophyte plastids were endosymbionts, there was a
justification for making a sharp distinction between them. But now that it is
established that the genome of the Cyanophora cyanelle is the same size as that of
true plastids (Herdman & Stanier, 1977), there is no longer any justification for
not regarding it as a true plastid, or for giving it a systematic name like a
cyanophyte, even though it still retains its peptidoglycan. The assimilate pattern in
the Glaucophyceae and Cyanidium are similar. The only way the Glaucophyceae
and Rhodophyceae can be unequivocally distinguished is by the presence of
membranous alveoli in the cortex of the Glaucophyceae similar to those in several
Protozoa. Since three of them are anteriorly biciliated with non-tubular
mastigonemes, and two (Glaucocystis and Gloeochaete) have four microtubular roots
with a characteristic multilayered structure (MLS), and an anterior ciliary
depression, there can now be little doubt that the ancestor of the Biliphyta was a
colourless phagotrophic cell with a pellicle with underlying cortical alveoli and two
anterior flagella bearing non-tubular mastigonemes. The next section will review
evidence suggesting that the chlorophyll-b-containing algae also derive from a
single endosymbiotic event involving an anteriorly biciliated phagotroph with a
pellicle, gullet and non- tubular mastigonemes.
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T . CAVALIER-SMITH
THE ORIGIN OF THE EUGLENOZOA AND VERDIPLANTAE
If, as argued above, the Euglenozoan plastid originated by the uptake of a
prokaryotic endosymbiont, as is generally accepted for the verdiplant plastid
(Gibbs, 1981 ; Whatley 1981), the simplest hypothesis is that only one such event
occurred and that the two kingdoms diverged early on from each other during the
establishment of the green plastid from a common ancestral symbiont. The
resemblances in thylakoid stacking and organization between the two groups and
the differences from Prochloron emphasized by Gibbs (1981) support the idea of a
common origin of both plastids. Since plastid origin by endosymbiosis necessarily
involves the loss of some endosymbiont genes, the absence of starch in Euglenu can
easily be explained by the loss of the genes for the starch-making machinery. The
presence of the p- 1-3-linked paramylon in Euglena cytoplasm outside the plastids is
readily explained if the phagotrophic host used it instead of a-1-4 linked starch as
storage material, and if these host genes were lost instead in the chlorophyte line.
The phylogenetic importance of such differential loss of different characters in
different lines has been emphasized before (Cavalier-Smith, 1978) and is a
particularly likely event following endosymbiotic events that create redundancy by
placing two functionally equivalent processes in the same cell (Whatley et al.,
1979).Differential loss of the lysine synthetic pathways must also have occurred; I
proposed (Cavalier-Smith, 1980) that the host had the amino-adipic acid (AAA)
pathway and the prokaryotic symbiont the diaminopimelic acid (DAP) pathway,
and that the host pathway was lost in the chlorophyte line. In the Euglenophyceae,
the host A M pathway is retained instead. In the non-photosynthetic
Kinetoplastida, which I treat as a class of the Euglenozoa, the DAP pathway is
retained, strongly indicating that they are derived from a photosynthetic derivative
of the prochloryphyte endosymbiosis and diverged very early from the
Euglenophyceae. In the Chromophyta and Rhodophyceae, the symbiont DAP
pathway appears to be retained; it would be valuable to know the situation in the
Glaucophyceae, Cryptophyta and Dinozoa (and other Protozoa).
If the Euglenozoa and Chlorophyta diverged early on, and eyespots evolved
subsequently and entirely independently, their location inside the chlorophyte
plastid, but free in the euglenophyte cytoplasm is readily explained. Clearly
therefore, many of the fundamental differences between Euglenids and
Verdiplantae, which have appeared to contradict the evidence of their pigment
similarities, can be readily explained by the common origin for their plastids from
an ancestral chlorophyll-b-containing endosymbiont. It has long been recognized
that the ciliary rootlets of the Chlorophyta differ from those of the Euglenozoa, but
the recent discovery of an MLS in some of the most primitive Euglenids
(Moestrup, 1978) that closely resembles the similar structures in the Verdiplantae,
supports the idea that the divergences are secondary and do not conflict with a
common origin for the two kingdoms. With increasing knowledge of the
Prasinophyceae, now widely recognized as the most primitive class of the
Verdiplantae (Moestrup, 1978; Stewart & Mattox, 1978), a common origin
becomes highly plausible. This is because, unlike the higher Verdiplantae, the
Prasinophyceae like the Euglenophyceae are naked and have an apical gullet-like
pit, and sometimes even trichocysts (though admittedly of a very different form).
Although the nuclear division of most Verdiplantae differs from that of the
Euglenophyceae, one or two species (Heath, 1980) show no significant differences :
THE ORIGINS OF PLASTIDS
29 1
the differences can therefore be attributed to subsequent divergence. The absence
of the nine-pointed star in Euglenophyceae is also compatible with a common
origin, since this is the ancestral condition found in all eukaryotes except the
Verdiplantae: the star must have evolved in the Verdiplantae after their
divergence from the Euglenozoa. Although the narrow-necked disc shape of
euglenozoan mitochondria1cristae is unique, it would not be hard to derive it from
the ancestral plate-like condition after the divergence from the chlorophyte.
We may therefore conclude that the Euglenozoa and the Verdiplantae both
arose from a common ancestral naked phagotroph with plate-like cristae, an
anterior gullet, and two anterior cilia lacking tubular mastigonemes and a ninefold star, shortly after it began to convert a chlorophyll-b-containing endosymbiont
into a plastid. The Euglenozoa remained mainly biciliates, though many lost
phagocytosis, whereas the Prasinophyceae lost phagotrophy and gave rise to three
lines of walled algae, each of which evolved non-motile descendants (Stewart &
Mattox, 1975, 1978).
NATURE OF THE ANCESTRAL BICILIATE ‘HOSTS’ AND THE ORIGIN OF MITOCHONDRIAL
DIVERSITY
Stewart & Mattox (1980) have cogently argued that all phytoflagellates evolved
from asymmetrical non-photosynthetic phagotrophs with a gullet, pellicle and
anterior cilia, and which phagocytosed photosynthetic prokaryotes and converted
them into plastids. My detailed analysis of plastid origins in the preceding sections,
and the new seven-kingdom classification (Cavalier-Smith, 1981b), strongly
supports their argument. There now seems little doubt that all six of the eukaryote
kingdoms with photosynthetic members (i.e. Verdiplantae, Euglenozoa, Protozoa,
Biliphyta, Cryptophyta and Chromophyta) evolved from non-photosynthetic
phagotrophs with two anterior cilia. The nature and origin of these phagotrophs
therefore becomes of great importance, and here my interpretations differ
profoundly from Stewart & Mattox (1980).They propose that the most primitive
ciliates are the Dinozoa but do not explain how they, or cilia evolved. Their
suggestion is based primarily on the view that dinozoan mitosis is primitive. In my
view, detailed elsewhere (Cavalier-Smith, in prep.), dinozoan mitosis is advanced
and derived, and the most primitive mitoses resemble those of the hemiascomyete
yeasts. I have also argued that no biciliate organism is really primitive (CavalierSmith, 1982), and that the biciliate condition evolved only after the origin of
phagocytosis, before which only eukaryotes with a single posterior cilium existed,
i.e. the Ciliofungi. According to this interpretation, the first biciliates had platelike cristae like the Glaucophyceae and Verdiplantae and not tubular ones as
found in the Dinozoa.
The evidence discussed above suggests that the biciliate ancestor of the
Biliphyta, Chlorophyta and Euglenozoa all had plate-like cristae and MLS
rootlets. However, the Dinozoa have tubular cristae and no MLS. This might
suggest that two very different groups acted as hosts for the endosymbiotic origin of
plastids. However, the presence of an alveolate pellicle in the Glaucophyceae and
Euglenozoa as well as the Dinozoa suggests that they may have been quite closely
related. In support of this is the occurrence of MLS rootlets in the proteromonad
Karatonympha which, like Dinozoa and other Protozoa, has tubular cristae
(Brugerolle & Joyon, 1975). The widespread presence of the distinctive MLS in
298
T. CAVALIER-SMITH
such different groups marks it strongly as a primitive character that was present in
their common ancestor but has been lost independently in different lines, e.g. in the
Dinozoa and most Euglenozoa. The presence of a dense rod beside the ciliary
axoneme of Dinozoa and Euglenozoa also indicates a close relationship, despite the
differences in cristal morphology. The varied mitotic mechanisms of the present
day descendants’ different biciliate hosts can as, argued elsewhere (Cavalier-Smith,
in prep.), reasonably be supposed to have arisen after the establishment of plastids.
The only major aspect of cell structure that argues against a very close
relationship between the different biciliate hosts, are the differences in cristal
morphology. Each plastid type is associated with a characteristic and distinct
cristal morphology. The differences in cristal morphology go beyond the simple
tubular/plate-like dichotomy (Taylor, 1976, 1978). Typical plate-like cristae are
found only in the two kingdoms (Biliphyta and Verdiplantae) with two
membranes in the plastid envelopes and no plastid ER. The Euglenozoa have discshaped cristae with narrow necks (Taylor, 1976), the Cryptophyta have flattened
tubular cristae (Santore and Greenwood, 1977), the Chromophyta have
unflattened tubular cristae of relatively large diameter, the Dinozoa (and most
non-photosynthetic Protozoa) have narrower more highly curved tubular cristae
(Taylor 1976, 1978). Did these differences arise before, during or after the
acquisition of plastids? The simplest explanation of this remarkable association of
the five cristal types with different plastid morphologies, is that the differences
originated during the establishment of plastids and have conservatively been
maintained ever since by stabilizing selection. On this hypothesis all the different
non-photosynthetic hosts had the same cristal morphology, which I suggest was the
conventional plate-like kind because this is the morphology found in the Ciliofungi
which I have argued were the first organisms to evolve cilia (Cavalier-Smith,
1982). On this hypothesis, mitochondrial and plastid morphology are
fundamentally coadapted and unable to evolve independently of each other.
I propose that the mechanistic basis for this coadaptation is the possession of
related mechanisms for the transport of cytoplasmically synthesized proteins across
their envelope into the mitochondrial and plastid matrices. Mitochondria and
chlorophyte plastids have similar methods of post-translational transport of
proteins across their envelopes (Blobel et al., 1979; Neupert & Shatz, 1981). In
both cases, transport is mediated by receptor proteins embedded in the.envelope,
perhaps in regions where the inner and outer membranes are in contact (Blobel et
al., 1979), and is accompanied by the cleavage of a signal peptide from the
precursor protein. I have pointed out (Cavalier-Smith, 1980) that the
establishment of transenvelope protein transport would have been a key step in the
conversion of an endosymbiont into a plastid, and proposed that the mechanism
evolved first in mitochondria and was then simply adapted for plastids (CavalierSmith, 1980). If the proteins that mediated protein transport across the
mitochondrial envelope in the non-photosynthetic hosts were coded by nonrepeated nuclear genes, as is highly probable, it follows that the process could not
be modified to suit it to an endosymbiont undergoing conversion to a plastid
without at the same time affecting mitochondrial transport. Mutations in the
nuclear genes would have a pleiotropic effect on both plastid and mitochondrial
transport : changes selected because they allowed the transport mediating proteins
to interact better with plastid envelopes could affect their interactions with the
mitochondrial envelope. Other envelope components that interact with this
THE ORIGINS OF PLASTIDS
299
transport machinery will therefore also coevolve in plastids and mitochondria.
Changes would also be selected to give the mitochondrial and plastid systems
distinct specificities, so as to prevent transport of mitochondrial proteins into
plastids or vice versa.
During the establishment of plastids there would, therefore, necessarily have
been marked changes in some aspects of mitochondrial envelope structure until the
optimal coadaptation of plastid and mitochondrial protein transport was
achieved. Thereafter, any changes in either would be highly disadvantageous and
selected against ever after ; mitochondrial and plastid structure would be
evolutionarily frozen. Therefore, this hypothesis for the first time gives a rational
explanation not only for the origin. of the different mitochondrial morphologies,
but also for their characteristic association with particular plastid types, and for the
great evolutionary stability, and therefore phylogenetic value, of both
mitochondrial and plastid envelope morphology. I shall not be surprised if
comparative study of the molecular basis of transenvelope protein transport in the
different kingdoms eventually proves its correctness. Even now one can give
additional arguments for it.
It is highly significant that the only biciliate photosynthetic kingdoms with the
ancestral type of plate-like cristae found in Eufungi, Ciliofungi and animals,
namely the Verdiplantae and Biliphyta, are also the only photosynthetic
kingdoms which have plastids with only two surrounding membranes. Since
mitochondria also have two envelope membranes, it can be argued that the
adaptation of the mitochondrial protein-transport system to this kind of plastid
would not require alterations large enough to alter significantly the mitochondrial
inner membrane morphology. For plastids with three or four surrounding
membranes much larger modification of the mitochondrial transport system would
be needed to adapt it to plastids, which would have correspondingly larger
repercussions on cristal structure. Since this process must have occurred
independently in each of the four kingdoms lacking standard plate-like cristae, it is
not surprising that the detailed changes and resulting cristal morphology are
different in each case. The nature of the changes would depend in part on the
nature of the plastid envelope membranes into which the transport system had to
become embedded.
The exact nature of the molecular changes must await future study, but it is
reasonable to argue that changes in inner mitochondrial membrane structure,
dictated by changes in the transenvelope protein transport system, would have led
to concomitant coadaptive changes in respiratory chain proteins embedded in it, or
bound to its surface like cytochrome c. Indeed, the cytochrome phenetic tree
(Dayhoff & Schwartz, 1981) strongly supports the present interpretation. The
verdiplant, animal, and eufungal cytochromes are most similar to each other, but
the euglenozoan cytochromes are considerably removed from this cluster. The
cytochromes of the Infusoria (=Ciliophora) are even more different, which is
expected if they evolved from dinozoan ancestry. A useful test of the present
interpretation would be to obtain mitochondrial cytochrome c sequences from the
four kingdoms for which they are not available (Chromophyta, Cryptophyta,
Biliphyta and Ciliofungi) and for the seven protozoan phyla not yet studied. I
predict that the biliphyte and ciliofungal cytochromes will be close to the verdiplant,
animal and Eufungi cluster (but form distinct lines within it), whereas the
chromophyte and cryptophyte cytochromes should form distinct lines in a cluster
300
T.CAVALIER-SMITH
near the protozoan ones, The other protozoan phyla should be close to the
Infusoria.
A corollary of my interpretation of cristal diversity is that all the nonphotosynthetic members of the kingdom Protozoa, as well as the kingdoms
Chromophyta, Cryptophyta and Euglenozoa, are derived from the single
photosynthetic ancestor for each of these kingdoms that first evolved their
characteristic plastid and mitochondrial morphology. The most prominent
colourless groups in the Chromophyta and Euglenozoa are the Phycomycotina
(Cavalier-Smith, 1981b) and Kinetoplastida, respectively, both of which have the
DAP lysine pathway which gives independent support for a photosynthetic
ancestry (Cavalier-Smith, 1980, 1981a). In the Protozoa, such independent
evidence is so far lacking, but the explanatory power of the coadaptational
hypothesis for the origin of mitochondrial diversity is so strong that it seems
reasonable to suppose that all Protozoa with tubular cristae-the vast majoritymust have photosynthetic ancestors with plastids like those of the Dinozoa, which
places the Dinozoa in a pivotal position for interpretation of protozoan phylogeny.
The fact that the Phycomycotina, Kinetoplastida, colourless Chrysophyceae, and
large numbers of Protozoa have retained the cristal morphology of their
photosynthetic ancestors despite the loss of plastids, probably hundreds of millions
of years ago, demonstrates that plastid/mitochondrion coadaptation is not the
fundamental explanation of the stability of cristal morphology, even though it may
be essential to explain its origins. The origin of the vesicular cristae of some
amoebae and gregarines is not explained by the present theory. However,
stabilizing selection acting on mitochondrial envelopes alone may be a less potent
stabilizing force than if it is acting simultaneously on mitochondria and plastids ;
maybe in a group like the Sarcodina, that may have split off from the
photosynthetic biciliate ancestor at a very early stage, later changes in cristal
morphology were possible. However, the possibility should also be considered that
the Protozoa with vesicular cristae are derived from an extinct photosynthetic
ancestor that had evolved a different type of plastid from any now extant, and that
the origin of vesicular cristae was therefore by the same mechanism as for the other
five non-plate-like types.
The present coadaptational theory of the origin of mitochondrial diversity has
much more explanatory power than the theory of several separate endosymbiotic
origins for mitochondria (Dayhoff & Schwartz, 1980, 1981 ; Stewart & Mattox,
1980). On the multiple symbiosis theory, the association between the five cristal
and plastid types must either be dismissed as a coincidence or ‘explained’ by
postulating an unknown factor determining which mitochondrial symbionts could
become established in which hosts. Moreover, although there are purple-nonsulphur bacteria with vesicular respiratory membranes and ones with plate-like
ones, there are none with disc-shaped euglenozoan-like, or flattened tubular
cryptophyte types; nor does the morphology of the few species with limited tubular
membranes closely resemble the protozoan or chromophyte tubules. Thus, the
required diversity of morphology does not exist in the most likely group of potential
symbionts. Moreover, the purple-non-sulphur bacteria with cytochrome c, most
closely resembling mitochondrial cytochrome c (including that of species with
tubular cristae) are all budding species with plate-like membranes. A symbiotic
theory of mitochondrial origin is entirely unnecessary now that one can explain in
great detail the origin of the whole eukaryote cell by the conversion of a colourless
THE ORIGINS OF PLASTIDS
30 1
derivative of a budding purple-non-sulphur bacterium with plate-like respiratory
cisternae into a budding yeast with plate-like mitochondrial cristae (CavalierSmith, in prep.).
The above discussion of the origin of mitochondrial diversity has been entirely in
terms of the needs for protein transport into plastids. There are, however, also
many translocators of small molecules in the plastid envelope (Wellburn &
Hampp, 1980) some of which may have been derived from mitochondrial
translocators and which may therefore have been important for the coevolution of
mitochondria and plastids. A further possibility is that some t RNA transport into
mitochondria occurs in organisms such as Tetrahymena (Chiu, Chiu & Suyama,
1975) having tubular cristae, but not in those such as yeast and animals with platelike cristae, and that tubular cristae are essential for this RNA transport. If the
reality of RNA transport into 'Tetrahymena is confirmed, it will be important to
seek it also in other Protozoa and in the Chromista.
THE RELATIONSHIP BETWEEN PLASTIDS CONTAINING PHYCOBILIN AND THOSE
CONTAINING CHLOROPHYLL B OR C ,
No one doubts that Cyunophora evolved its plastid by modification of an
endosymbiotic cyanophyte (Herdman & Stanier, 1977) : the evidence discussed
above quite strongly suggests that not only the plastids but also the host cells of the
other Glaucophyceae are related to Cyanophora and are all derived from the same
symbiotic event ; the Rhodophyceae clearly seem to have been derived from nonciliated Glaucophytes like Glaucosphaera by the loss of the pellicle and formation of
a cell wall to produce an intermediate like Cyunidium. Therefore, all the Biliphyta
probably have a single common ancestor: the phagotrophic biciliate that first
began to convert a symbiotic cyanophyte into a plastid.
I have also provided evidence that the chlorophyll-b-containing plastids of the
Euglenozoa and Verdiplantae originated in a biciliate phagotroph by the
conversion along divergent lines of a single photosynthetic prokaryote
endosymbiont into two distinct types of plastid. The arguments presented here
indicate that this host had essentially the same structure as the ancestral host of the
Biliphyta : both probably had a pellicle, anterior gullet, MLS, non-tubular
mastigonemes and plate-like cristae. This means that one should consider very
seriously the possibility that the biliphyte, euglenophyte and chlorophyte plastids
all originated endosymbiotically from a single cyanophyte, and that the origin of
chlorophyll b occurred during the process of conversion of it into a plastid in a line
that lost phycobilins. The problematic glaucophytes Cyanidium and Gluucocystis
share several features with the Rhodophyceae and Verdiplantae. Cyanidium has the
sterol ergosterol, like Verdiplantae and unlike the Rhodophyceae, and the sterol
camposterol like the Rhodophyceae and unlike the Verdiplantae; like the
Verdiplantae it lacks phycoerythrin but like the Rhodophyceae it lacks
chlorophyll b (Seckbach, Hammerman & Hanania, 1981): moreover, its starch is
like that of cyanophytes, and not Rhodophyceae or Verdiplantae. Gluucocystis on
the other hand has starch indistinguishable from that of the Verdiplantae and
unlike that of all other Biliphyta or cyanophytes.
The puzzling and varied distribution of characters in the Glaucophyceae
suggests that they may be evolutionary relics of alternative pathways of plastid
formation that never underwent extensive adaptive radiation. They may give us
302
T. CAVALIER-SMITH
powerful clues as to the nature of the host biciliate as well as the process of plastid
formation.
Detailed study of the location and sequence of the genes coding for the storage
polyglucans (Frederick, 1981) in various Biliphyta should help clarify the
relationships between the Glaucophyceae and Rhodophyceae, and to decide
whether the anomalous green thermophile Cyunidiurn is not a rhodophyte but really
a glaucophyte as several lines of evidence indicate (Kies, 1980; Seckbach,
Hammerman & Hananig, 1981) .
Prochloron may simply be a red-r
rather green-herring. Its possession of
chlorophyll b is not enough to establish it as the ancestor of chloroplasts.
chlorophyll b differs from chlorophyll a only by the replacement of two hydrogen
atoms by a n oxygen atom-a
slender thread on which to hang a weighty
argument. The absence of phycobilins in both chloroplasts and Prochloron is no
evidence of affinity. Nor is thylakoid stacking, which is found in every kind of
plastid in which phycobilisomes are absent, and so is likely to be an inevitable
evolutionary consequence of the loss of phycobilins. Gibbs (1981) has pointed out
significant differences in the thylakoid arrangement in Prochloron and eukaryote
chloroplasts. This is in marked contrast to the thylakoids of cyanophytes and
biliphyte plastids, which in many cases are completely indistinguishable.
Another objection to the prochlorophyte theory of chloroplast origin is that
Prochloron is not free-living but is itself a symbiont inhabiting a multicellular
animal. I suggest that free-living prochlorophytes never existed, and that Prochloron
itself is derived from a symbiotic cyanophyte by the loss of phycobilins and the
concomitant evolution of chlorophyll b and thylakoid stacking. It may be a case of
convergent evolution in response to a similar niche.
If the case of Prochloron is dubious, that of the completely hypothetical
procryptophyte is even worse. As emphasized earlier, major changes must
necessarily occur during the formation of plastids from a symbiont. This means
that the major changes that led to the origin of chlorophyll c, and the
cryptomonad phycobilins are more easily understood as occurring during the
conversion of a symbiotic cyanophyte into a cryptophyte type of plastid than in
free-living cyanophytes, which appear to be evolutionarily very conservative.
Therefore, since there is no evidence for the existence of a procryptophyte, the
most economical hypothesis would be that this is what happened, and that the
dinozoan plastid also is derived by divergent evolution prior to the full
establishment of the plastids from the very same cyanophyte symbiont that formed
the biliphyte plastid. In support of this, one may quote the close similarity of
plastid cytochrome cs of the brown chromophyte alga Aluriu with that of red algae
and cyanophytes (Schwartz & Dayhoff, 1981).
Therefore, I postulate that chlorophyll-b-, c,- and phycobilin-containing plastids
are all descended from the same endosymbiont and that the basic differences
between them originated because the conversion of the symbiont into plastids took
a different course in different early descendants of the initial host, as argued above
in the discussion of the origin of mitochondria1 diversity, and summarized in Fig. 2.
The resemblances between the cilia and the pellicle of the Euglenozoa and
Dinozoa support the idea that they diverged from a common ancestor similar to
that of Gluucocystis, Cyunophoru and Gloeochaete.
The origin of the Cryptophyta probably also involved a related biciliate as a
host, which probably differed mainly in having tubular rather than non-tubular
T H E ORIGINS OF PLASTIDS
303
Figure 2. A phylogeny for photosynthetic eukaryotes assuming only two endosymbioses. A nonphotosynthetic phdgotrophic eukaryote (A) with a single nucleus (n), two anterior cilia bearing nontubular mastigonemes, a gullet and a pellicle engulfed a cyanophyte to produce an endosymbiotic
cyanelle with three bounding membranes (B). The cyanelle became rapidly established in the host and
stably passed on to its offspring at cell division. The conversion of the cyanelle into a plastid took many
cell generations and therefore took a different course in different descendants of the initial symbiotic
complex (B). Three main lines evolved ( I ) , (2), and (3). In that leading to the Biliphyta, the
phagosome membrane was lost (-p) but the thylakoids and pigments remained essentially unaltered;
the cyanophyte starch-making machinery was lost but that ofthe host was retained. In the second line,
phycobilins (pb) were replaced by chlorophyll b and the thylakoids consequently became stacked; this
line diverged early by the loss of the phagosome membrane (-p) to produce the Verdiplantae on the
one hand, and the loss of the starch-making machinery of both host and symbiont, on the other, to
produce the Euglenozoa; retention of the phagosome membrane in the euglenozoan line led to the
modification of the mitochondrial protein transport system and the origin of disc-shaped cristae (dc).
In the third line, the phycobilins were moved inside the thylakoids (pbi), which thus became able to
stack, chlorophyll c2 evolved and the cyanophyte starchmaking machinery was lost (C) but that of the
host was retained, and the mitochondrial cristae became tubular (tc). This line also forked: one branch
lost phycobilins ( - pb) to yield the Dinozoa (a very few of which also lost the phagosome membrane
(-PI)), while the other lost the phagosome membrane before or during its incorporation by a nonphotosynthetic phagotroph (D) to form the Cryptophyta. The cryptophyte host (D), like the host (A)
that engulfed the cyanophyte had a pellicle, trichocysts, and a gullet, but differed in having tubular
rather than non-tubular mastigonemes on its two anterior cilia. These major events probably occurred
very rapidly-perhaps even within ten years of the primary endosymbiotic uptake of a cyanophyte by
the first biciliated host ( A ) .
mastigonemes: it would have had a gullet near its two anterior cilia, a pellicle, and
trichocysts like those of the Prasinophyceae (Morrall & Greenwood, 1980).
The carotenoid and xanthophyll composition of the red algae, whose plastids are
accepted as being derived from endosymbiotic cyanophytes, has at least as many
features in common with those of the other eukaryote algae as with those of
cyanophytes (Dougherty & Allen, 1960) which supports a common origin for all
eukaryote plastids.
904
T. CAVALIER-SMITH
The phylogeny shown in Fig. 2 is much more economical than other recent ones
that postulate five to seven separate endosymbioses (Dodge, 1979; Cavalier-Smith,
1981a; Whatley, 1981), or earlier ones that postulated as many as 20 (Sagan,
1967). It assumes that only one prokaryote was ever converted into a plastid.
However, it differs radically from earlier schemes that derive all plastids from a
common ancestor, in that it argues that the transitions between the major types
occurred not between well-developed plastids with a long evolutionary history, but
during the actual process of conversion of a cyanophyte into, not one, but several
different plastid types. In the present view, the modification of an endosymbiont is
seen as the creator of plastid diversity: whereas, in the earlier idea of multiple
symbiosis of different procaryotes it simply incorporates pre-existing prokaryote
diversity (whose origin remains entirely unexplained) into the eukaryote cell
(Sagan, 1967; Raven, 1970).
This rapid origin of plastids from a single symbiont, and the concomitant
changes in mitochondria, is one of the most important examples of rapid quantum
evolution (Simpson, 1953; Stanley, 1979),since the origin of eukaryotes themselves
(Cavalier-Smith, 1975, 1981a),and the origin of cilia and phagotrophy (CavalierSmith, 1982).
TESTING THE THEORY
The best test will be to compare the detailed organization of plastid DNA in the
six kingdoms. There is already evidence of this kind bearing on the relationship
between the euglenoid and verdiplant plastids. Euglenoid plastid DNA has three
rRNA genes arranged in a tandem array as in bacteria. Verdiplant plastid DNA
has only two rRNA genes, usually arranged as inverted repeats as in Chlamydomonas
(Gillham & Boynton, 1981). Since the inverted arrangement must be derived and
the tandem arrangement in Euglena the ancestral one, this conflicts with the theory
that Euglena plastids are derived by symbiosis from chlorophyte algae (Gibbs, 1978,
1981) or plastids (Whatley, 1981), but is entirely consistent with my proposal that
they are both derived from a single endosymbiotic cyanophyte by the loss of
phycobilins and the evolution of chlorophyll b and thylakoid stacking.
Comparisons with biliphyte (both glaucophyte and rhodophyte), chromophyte,
cryptophyte, and dinozoan plastid DNA should eventually decide unambiguously
whether the hypothesis of a single, primary endoxymbiotic event involving a
cyanophyte is correct. Studies of plastid DNA in these groups is badly needed; it
has been isolated only from two such species, the glaucophyte Cyanophora
(Loffelhardt, Mucke & Bohnert, 1980) and the chromophyte (diatom) Olisthodiscus
(Aldrich & Cattolico, 1979), both of which have circular DNA in the same general
size range as the green algal plastid DNA; but there is not yet data to support or
refute the idea of an independent origin.
My theory of the origin of dinozoan and cryptophyte plastids predicts that a
dinozoan with phycobilins and chlorophyll c, once existed. Perhaps some still do:
electron microscopy and pigment analysis are needed of the few Dinozoa with blue
pigments (Taylor, 1980, 1981) to see if any have plastids like cryptophytes.
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, Vufu added in / J ~ w /Several
:
o f the tiixa here callcd kingdoms iirr probably better trcatcd as subkingdoms, ;IS in
my simplified 6-kingdom cl;issilic;ition (C;rvalier-Smir.h, 1981b). 'Ihis docs not alter any of thr arguiiic'iits
prescntcd i n this paper.