The Botanical Review 1970 v36

THE PYRENOID
D I L W Y N J. GRIFFITHS
School of Biological Sciences
La Trobe University
Bundoora, Victoria, Australia
Introduction ........................................................................................................................................................................................... 29
Structure of Pyrenoids
Gross morphology ................................................................................................................................................................... 29
Limiting membrane .............................................................................................................................................................. 31
Matrix ............................................................................................................................................................................................ 32
Inclusions ...................................................................................................................................................................................... 34
Associated Reserve Substances .............................................................................................................................................. 39
Growth and Division of Pyrenoids ................................................................................................................................. 42
Funetion of Pyrneoids
Formation of the Starch Sheath ............................................................................................................................... 44
Formation of Stromal Starch ..................................................................................................................................... 44
Formation of Other Storage Materials ............................................................................................................. 46
Role of the Pyrenoid Inclusions ................................................................................................................................ 47
Relation between the Pyrenoid and the Nucleus .................................................................................. 47
Pyrenoids under Abnormal Conditions ................................................................................................................... 48
Taxonomic Considerations ................................................................................................................................................... 49
Concluding Remarks .................................................................................................................................................................. 53
Literature Cited .................................................................................................................................................................. 54
INTRODUCTION
The pyrenoid is a feature of algal cells that has always attracted the attention"
of microscopists. Much of the earlier work was of a purely descriptive nature,
and any investigation of the physiology of pyrenoids was necessarily of very
limited scope. With the introduction of electron microscopy, however, a new
dimension was added to these studies, and the information provided gave a new
insight into the nature and functioning of the pyrenoid. In spite of the sig-
nificant body of new information now available, however, there is still much
that is not known about the pyrenoid. This article is an attempt to summarize
our present knowledge of this unique feature of algal cells and is based very
largely on work carried out using the electron microscope, although some of
the earlier contributions in this field are considered, particularly where they
form a background to the more recent studies.
STRUCTURE OF PYRENOIDS
G r o s s M o r p h o l o g y . Pyrenoid containing species are to be found within all
the major groups of algae with the exception of the Cyanophyta; the only
29
30 THE BOTANICAL REVIEW
plant outside the algae with a recognizable pyrenoid is the liverwort Anthoceros.
Although there is much variation in the type of pyrenoid present in different
algae, most of them belong to one of two basic morphological types, the em-
bedded pyrenoid and the projecting pyrenoid.
GRIFFITHS: THE PYRENO1D 31
Embedded pyrenoids are usually spherical or sub-spherical bodies set deeply

within the chloroplast, a feature that led Schmitz (1883) to liken the morpho-
logical relationship between the pyrenoid and the chloroplast to that between the
nucleolus and the cell nucleus. There may be one or more pyrenoids per chloro-
plast, depending on the species. When there is only one pyrenoid, it is usually
more or less centrally located, while in multipyrenoidal chloroplasts the pyre-
noids may be randomly distributed (Lang, 1963). The pyrenoid of Anthoceros
has a compound structure and has been described as consisting of from 25 to
30 closely aggregated disc- or spindle-shaped bodies (McAllister, 1914, 1927).
Projecting pyrenoids appear as a bulge on the inner face of the chloro-
plast, to which they may sometimes be connected by a short stalk. Projecting
pyrenoids usually occur singly, but sometimes two widely spaced pyrenoids
may arise from the same chloroplast (Bouck, 1965; Evans, 1966).
Some species have pyrenoids that do not fall into either of the above cate-
gories. The genus Carteria, for example, has a pyrenoid that is suspended in the
middle of the cell by thin arms of chloroplast and cytoplasm (Lembi & Lang,
1965). Ceils of the dinoflagellate AmphidinJum carteri (isolated by Guillard)
contain a single net-like chloroplast, which is located at the periphery of the
celt and sends arms inward to form a central pyrenoid (Gibbs, 1962a). Two
members of the Cryptophyta, Rhodomonas le~s Pascheret & Ruttner and
Cryptomo,nas sp. have each a single chloroplast consisting of two large lobes
joined by a bridge of pyrenoid material (Gibbs, 1962a). Although the pyrenoid
in these species is undoubtedly an integral part of the chloroplast, this is only
really apparent when suitable sections are viewed with the electron microscope.
It is possible therefore that the earlier reports of so-called cytoplasmic pyre-
noids (Kater, 1929; Smith, 1950) will prove to have been mistaken.
L i m i t i n g Membrane. In most of the algal species that have been studied
in detail there appears to be no membrane separating the pyrenoid from the rest
of the chloroplast. Very often, however, as in Chlamydomonas reinhardJ
Dang., there is a marked difference in density between the chloroplast matrix
and the pyrenoid, with an abrupt transition from the one to the other (Sager &
Palade, 1957). In this alga, as in many other members of the Chlorophyceae,
the pyrenoid is surrounded by a shell of starch grains, which help to delimit
the boundary of the pyrenoid (see Fig. 1). Careful examination has shown that
the starch grains are separated from the lamellar material of the chloroplast by
a thin, continuous layer of chloroplast matrix. Matrix material continuous with
FIG. 1. Section through the chloroplast of Chlamydoraonas reinhardi showing it to

contain numerous grana (g, g~ and g2) and to be bounded by a chloroplast envelope
(ce). The space among the grana is occupied by the stroma which contains osmiophilic
globules (o), starch granules (sg) and numerous ribosomes. The pyrenoid (p)
occupies the centre of the chloroplast and consists of a finely granular core surrounded
by a discontinuous shell of starch plates (sp) and penetrated by a network of tubules
(t). The profile marked cl is part of the irregularly deeply cut rim of the chloroplast
cup.
X 27,000
(m ---- mitochondrion; mb ~ cell membrane; ~w ~-- cell wall).
/From: OHAD, I., P. SIEKEVITZ, & G. E. PALADE, 1967. Jour. Cell Biol. 35: 521-552).
this layer also occupies the spaces between the starch grains, thus establishing
contact with the dense core of the pyrenoid.
The only examples of embedded pyrenoids that are bounded by a membrane
occur in certain diatoms (Drum & Pankratz, 1964; Holdsworth, 1968) where
the membrane has been described as a ridge that does not connect with any of
the chloroplast discs. It seems clear, however, that the membrane in these algae
is a definite structure and not merely an interface between the pyrenoid and the
chloroplast matrices. (See Fig. 2).
Projecting pyrenoids, because of their special position, are partially bounded
by a membrane that is a continuation of the compound surface membrane of the
plastid. Where the projecting pyrenoid has a distinct stalk, as in Chrysochromu-
lina minor Parke & Manton (Manton & Leedale, 1961), the contact between
the pyrenoid and the plastid is restricted to the stalk, and the pyrenoid body is
almost entirely surrounded by the plastid membrane.
Detailed investigation of the projecting pyrenoid of the brown alga Chorda
[~lunz (L.) Lamour (Bouck, 1965) has shown it to have three separate double
membranes or envelopes, the innermost being the continuation of the chloro-
plast envelope around the margin of the pyrenoid. Outside this chloroplast
envelope lies the chloroplast endoplasmic reticulum, which comprises the middle
of the three envelopes and is,continuous with the endoplasmic reticulum sur-
rounding the rest of the chloroplast. Finally, the outermost envelope of the pyre-
noid is composed of two membranes and may be greatly dilated. This outer
envelope terminates in the region of the neck and appears as a cap or sac ex-
tending over the pyrenoid.
A similar arrangement of membranes has been recorded for various other
algae with projecting pyrenoids (Evans, 1966; Manton, 1966a, 1966b), al-
though there may occasionally be some slight variation on this basic pattern.
Sometimes, as in Sphacelaria bipinnata Sauv., the entire cap may be lacking
(Evans, 1966), or, as in certain dinoflagellates, the cap may be without a bound-
ing membrane (Dodge, 1968). Another variation is shown by Olisthodiscus
sp., a small flagellate probably belonging to the Chrysophyceae, which has a
projecting pyrenoid enclosed within the chloroplast envelope. In this alga, how-
ever, the chloroplast endoplasmic reticulum, over part of the surface of the pyre-
noid, bulges out slightly over a row of membrane-limited tubules (Gibbs,
1962d).
M a t r i x . With the usual preparatory methods, the pyrenoid matrix presents a
dense uniformly granular appearance. Some detail of the matrix material has
been observed in Platymonas subcordiformis (Wille) Hazen., where it is de-
scribed as being composed of tightly-packed fibrils about 60 A in diameter,
FIc. 2. Section through the pyrenoid of Achnanthes bree:ipes showing the crystalline na-
ture of the matrix which is bounded by a "membrane" (pro). Within the pyrenoid ma-
trix can be seen a small area containing round, electron-opaque particles (rl) ten-
tatively identified as ribosomes. The "ribosome"-containing region is associated with a
double-disc membrane (ddm). x 120,000.
(cl ~ chloroplast lamellae; o = oil droplet; r ---- ribosome).
(From: HOLDSWORTH,R. H. 1968. Jour. Cell Biol. 37: 831-837).
GRIFFITHS: THE PYRENOID 33
which are apparently distinctly different from the scattered granules of the
chloroplast matrix (Gibbs, 1962b). A similar fibrillar or filamentous texture
of the pyrenoid matrix has been recorded for Haematococcus (Wygasch,

1964) and certain other green algae (Gibbs, 1962b) as well as in the brown
alga Pylaiella littoralis (L.) Kjellm. (Gibbs, 1962a).
The pyrenoid matrix of the diatom Achnanthes brevipes (Ag.) Kiitz. has
been shown to have a crystal-like structure composed of arrays of round sub-
units, which may be linearly arranged in rows or packed hexagonally (Holds-
worth, 1968) (see Fig. 2). The physical characteristics of the crystal, together
with the possible presence of pyrenoid-associated ribosomes, led Holdsworth to
suggest that the crystal was protein. Such a conclusion would be consistent with
the evidence, based on selective staining and fluorescence microscopy, that
pyrenoids are composed primarily of protein (Bose, 1941) and possibly a small
amount of RNA (Brown & Bold, 1964). A similar crystal lattice appearance,
resembling that of various forms of reserve protein, has also been described for
the pyrenoid matrix of the marine dinoflagellate Prorocentrum micans Ehren b.
(Kowalik, 1969).
In no other algal pyrenoid has such a clear-cut crystalline structure been
demonstrated, although Evans (1966) found that parts of the pyrenoids in
some species of brown algae sometimes had a crystalline appearance. A highly
ordered pyrenoid structure has also been observed in Carteria (Joyon & Fott,
1964), although in this alga it was not described as crystalline, but rather as
being composed of parallel "plastidious discs." Colchicine treatment of the di-
atom Navicula pelliculosa (Br~b.) Hilse may sometimes result in the appear-
ance of a para-crystalline structure in the pyrenoid (Coombs et al., 1968).
This is not a regular feature of colchicine-treated cells, however, and its
exact significance is not known.
Inclusions. In many algae the entire body of the pyrenoid is made up of the
fairly uniform granular matrix material. Included in this group are many green
algae such as Chlorella fusca Shihira & Krauss (Soeder, 1964), Scenedesmus
quadricauda, Br6b. (Gibbs, 1962b), Pediastrum biradiaturn Meyen. (Moner
& Chapman, 1960), and Chlorogonium elongatum Dang. (Hailer & Rouiller,
1961), several species of brown algae (Bouck, 1965; Evans, 1966; Bourne &
Cole, 1968), some cryptomonads (Gibbs, 1962a) and one member of the
Prasinophyceae, Micromonas squamata Manton & Parke (Manton & Parke,
1960). In contrast to these algae are those which have pyrenoids whose matrix
is traversed by inclusions of various kinds. There are many types of pyrenoid
inclusion, all of which, with one or two notable exceptions, bear a close struc-
tural relationship to the chloroplast thylakoids. Very often the connection be-
tween the pyrenoid inclusions and the chloroplast thylakoids is quite clear and
the latter pass into the pyrenoid without any noticeable modification of struc-
ture. Such a situation is found in a range of different algae (Leyon, 1954;
Ueda, 1961; Murakami et al., 1963; Kowalik, 1969).
The course taken by the pyrenoid thylakoids may be rather direct or more
meandering. In Spirogyra, for example, the thylakoids of the chloroplast appear
to continue their parallel path through the pyrenoid (Leyon, 1954), while in
certain species of Carteria, thylakoids extending between the starch grains from
adjacent pseudograna penetrate the pyrenoid matrix in a very contorted and
twisted manner (Lembi & Lang, 1965). A particularly interesting situation is

found in the desmid Closterium lunula Reins&., in which a number of groups
of parallel thylakoids may fold back on themselves giving an arrangement
that has been described as resembling the pieces cut from an onion arranged with
their sectioned surfaces turned outwards (Leyon, 1954).
Relatively few of the species that have been examined have lamellar struc-
tures in their pyrenoids, which are made up of exactly as many discs as their
counterparts in the rest of the chloroplast. The majority of these, as might be
expected, belong to the Rhodophyta, where the bands of the chloroplast consist
of only one disc (Brody & Vatter, 1959; Mitrakos, 1960; Gibbs, 1962a).
Among the other species that fall into this category are the dinoflagellate
Amphidinium carteri and two members of the Chrysophyta, Olisthodiscus sp.
and Nitzschda angularis Wm. Smith, in all of which the bands of the pyrenoid
and of the chloroplast contain three discs (Gibbs, 1962a).
In most of the pyrenoid-containing species, however, there is a reduction in
the number of its contained discs accompanying the entry of the chloroplast
band into the pyrenoid. In species of Pyramimonas and Spirogyra, for example,
where the bands of the chloroplast are made up of two to four appressed thyla-
koid discs, the bands which traverse the pyrenoid are reduced to single discs
(Gibbs, 1962b). Pyramimonas is particularly interesting, since there are
regions at the periphery of the pyrenoid where the bands still possess the four
discs most typical of chloroplast bands. Single discs have also been observed to
cross the pyrenoid in Cosrnarium lundelii Delponte (Chardard & Rouiller,
1961), Carte, ia sp. (Lembi & Lang, 1965), Closterium lunula (Leyon, 1954),
Chromulina psammobia Faur6-Fremiet (Rouiller & Faur6-Fremiet, 1958), and
Hydrurus foetidus (Vill.) Kirschn. (Hovasse & Joyon, 1960). In some algae,
e.g., Chaetomorpha linum (Miill.) K~tz., Rhizoclonium tortuosum (Kiitz.)
Stockm. (Gibbs, 1962b,) Cladophora fracta Ki.itz. (Strugger & Peveling, 1961),
the pyrenoid is divided into two hemispheres by a single membrane-limited
disc, which is continuous with one of the bands of three or more thylakoid
discs that traverse the chloroplast.
Other algae display varying degrees of reduction of the lamellar structures
that enter the pyrenoid. In Chlamydomonas moewussi Gerloff, for example,
the chloroplast bands, which usually consist of two to six thylakoid discs, are
invariably reduced to two discs when they cross the pyrenoid (Gibbs, 1962b).
Paired discs are also found in the pyrenoid of Chlorella pyrenoJdosa Pring-
sheim (Albertsson & Leyon, 1954; Murakami et al., 1963), Dunaliella salina
(Dunal.) Teod. (Trezzi, Galli, & Bellini, 1964), as well as in the pyrenoids
of certain euglenoids (Ueda, 1960; Gibbs, ]960, 1962a: Leedale, 1967),
diatoms (Drum & Pankratz, 1964; Holdsworth, 1968), and dino-flagellates
(Dodge, 1968).
The reduction in the number of discs as the bands enter the pyrenoid is
usually accompanied by an increase in the width of the disc (Leyon, 1954;
Gibbs, 1962a, 1962b). Sometimes, as in Euglena gracilis Klebs (Gibbs,
1962a), the discs of the chloroplast bands become wider shortly before they
enter the pyrenoid. Whether there is also a modification in the breadth of the
36 THE BOTANICALREVIEW
chloroplast thylakoids as they enter the pyrenoid is a little difficult to establish,

since all the evidence is necessarily obtained from sectioned material. How-
ever, the absence of tubular profiles from the pyrenoid of Carteria was in-
terpreted by Lembi & Lang (1965) as indicating that the pyrenoid discs in that
alga were probably as broad as the pseudograna themselves.
Occasionally there may be structural differences between the thylakoids of
the chloroplast and those of the pyrenoid. These may be rather minor differences
such as the undulating course followed by the central lamella of the double
discs of the pyrenoid of Chlamydomonas moewussii (Gibbs, 1962b) and in
certain other algae (Gibbs, 1962a). More often, however, the differences are
more marked, such as in Prasiola stipitata Suhr. (Manton & Friedmann, 1959),
in Chrysocbromulina chiton Parke & Manton (Parke, Manton, & Clarke,
1958) and in Nitzschia dissipata (Khtz.) Grun. (Elbers, Minnaert, & Thomas,
1957), where the single discs are reduced to tubules, or in Chrysochromulina
strobilis (Parke, Manton, & Clarke, 1959) where the two-disc bands of the
chloroplast are reduced to paired tubules in the pyrenoid. In the zoospores
of Haematococcus pluvialis Floto w era. Wille the canals which traverse the
pyrenoid may sometimes be bundled together in the shape of a centrally bound
wheat sheaf (Wygasch, 1964). Outside the pyrenoid each canal widens and
branches into short and partially flattened tubular projections, whose walls pass
continuously into the profile of the double thylakoids of the chromatophore.
Detailed investigation of the tubules of the pyrenoid of Chlamydomonas
reinhardi (Sager & Palade, 1957; Ohad et al., 1967) has shown them to be in
the form of a network embedded in the dense material of the pyrenoid core
(see Fig. 1). There is evidence that in this alga the tubules of the pyrenoid arise
by a coalescence of several chloroplast thylakoids. The preparations of Ohad
et al. (1967) show that each tubule is limited by a membrane (55-60 A thick),
resolvable in places into three layers, and contains in its lumen two to five
(usually three or four) dense, peripheral bodies (see Figs. 3 and 4). Longi-
tudinal sections show that these bodies are in the form of ridges protruding
from the limiting membrane and extending along the tubule, although in some
places they are completely detached from the limiting membrane (see Fig. 4).
The tubular lumen is clearly in continuity with the intradisc space of the chloro-
FIG. 3. Section through a portion of the pyrenoid of Chlamydomonas reinhardi showing

the continuity of a pyrenoid tubule (t2) with a chloroplast granum (g~) and suggesting
that the ridges or infoldings of this tubule are in continuity with the fused membranes
of the discs of the granum. Other grana appear at gl and ga, and other pyrenoid
tubules at tl (cross section) and t~ (oblique section).
x 120,000.
(cr ----chloroplast ribosome; o ----osmiophilic globule; pp= pyrenoid particles; sp =
starch plates).
Fie. 4. A pyrenoid tubule of Chlamydomonas reinhardi at higher magnification showing
layered structure of the membrane (arrows) and the presence of at least one internal
secondary tubule (st) presumably formed by a "detached" ridge.
x 200,000.
(Both figures from: OHAD,I., P. SIEKEVITZ• G. E. PALADE,1967. Jour. Cell Biol, 35:
521-552).
G R I F F I T H S : T H E PYRENO1D 37
plast thylakoids, while the internal folds or ridges are continuous with the fused
partitions of the grana (see Fig. 5). These pictures confirm the earlier suggestion
of Lembi & Lang (1965) that the limiting layer of the tubules is probably de-
rived from the single outer membrane of a group of chloroplast thylakoids and
that the thickenings probably represent the thick double membranes of ap-
pressed thylakoids.
How the process of narrowing from a sheet-like thylakoid to a tubule occurs
is not yet understood, but it must clearly entail an active morphological change
and not just a simple rearrangement of membranes. A similar narrowing of the
chloroplast thylakoids to form tubules within the pyrenoid has been observed in
the projecting pyrenoid of Chrysochromulina minor (Manton & Leedaie,
1961).
One question that arises is whether the structural differences between the discs
of the pyrenoid and those of the chloroplast also reflect differences in their
respective content of chlorophyll. Too much weight should not be given to
earlier attempts to demonstrate the presence of chlorophyll in the pyrenoids of
whole cells, since the high density of the pyrenoids would make them appear
as dark bodies within the chloroplast. Work with Closterium acerosum
(Schrank) Ehrenb. (Leyon, 1954) has attempted to isolate the pyrenoid from
Fxc. 5. Section through a portion of the periphery of the pyrenoid (p) of Chlamy-
domonas reinhardi showing a clear continuity between a granum (g4) and a pyrenoid
tubule (t,). It can be seen that most of the intradisc spaces are continuous with the
tubular lumen, and that three of the fused partitions of the granum can be followed
into three ridges (or fused infoldings) of the tubule wall. The fourth partition stops
at the arrow.
x 53,000.
(ce ~ chloroplast envelopes; gl, g2, g3 = chloroplast grana; sp ~ starch plates).
(From: OHAD, I., P. SIEKEVXTZ, & G. E. PALADF.. 1967. Jour. Cell Biol. 35: 553-584).
the rest of the cell by micro-dissection. Microscopic examination of such iso-

lated pyrenoids led Leyon to suggest that in this alga the pyrenoid probably
contains chlorophyll. However, Butterfass (1957) observed that the pyrenoids of
Spirogyra, which are traversed by a number of single discs, do not fluoresce.
Similarly, Brody & Vatter (1959) noted that when Porphyridium cruentum
(Ag.) Naegeli was examined with red or with green light, the pyrenoids ap-
peared as light centers in the dark chloroplast. It is possible, of course, as has
been pointed out by Gibbs (1962a), that the apparent lack of fluorescence or
absorption in these two cases may simply be due to the fact that there are sig-
nificantly fewer membranous discs in the pyrenoid than in the chloroplast
proper. In Euglena gracilis, however, even after allowing for the reduction in
the number of discs, the chlorophyll content of the pyrenoid discs is very much
reduced if not completely absent (Gibbs, 1962a). Clearly the greater the degree
of structural modification of the pyrenoid discs, the less likely they are to have
a high chlorophyll content. This possibility is supported by the observation
(Gibbs, 1962e) that in the developing chloroplasts of Ochromonas danica
Pringsheim, the only observable change that occurs as the amount of chloro-
phyll per chloroplast increases from 50 to 100 per cent of the maximum, is
a narrowing of the chloroplast discs and an exact aligning of their membranes.
The projecting pyrenoid of Platymonas subcardiformis (Fig. 7) is a little
unusual with regard to the nature of its tubules. The membrane-limited struc-
tures contained within the pyrenoid of this alga are apparently in no way re-
lated to the thylakoid discs or tubules present in other algae (Gibbs, 1962b).
They are cross sections of fingers of cytoplasm that project into the pyrenoid
from its interior face. Most commonly a single median channel of cytoplasm
enters the pyrenoid and then branches into a number of fingers. The membrane
bordering the channels is continuous with the chloroplast envelope. The ribo-
somes and other membranous elements of the cytoplasm extend into the main
channel, but the ends of the side channels are filled with another substance that
resembles starch in its very low electron density. Similar invasions of extra-
plastidial cytoplasm into the pyrenoid matrix have been noted in Oedogon-
ium cardiacum Wittrock (Hoffman, 1968a), in certain members of the Crypto-
phyta (Gibbs, 1962a), and in Prasinocladus (Manton & Leedale, 1961),
although in the latter the invaginating channel is filled with a protrusion of the
nucleus.
In the diatom Streptotheca thamesis Shrubsole (Esser, 1967) the single thy-
lakoid-like membrane that passes longitudinally through the pyrenoid is not in
connection with any of the plastid thylakoids. It is in the form of a very flat disc
that ends in the peripheral zone of the pyrenoid. Pretreatment of the material
with DNAase resulted in the disappearance of the membrane, suggesting that
it consists of a high percentage of DNA. The significance of this observation
is not obvious, and a proper evaluation must clearly await further investiga-
tion.
ASSOCIATED RESERVE SUBSTANCES
A common characteristic of the pyrenoids of most green algae grown in the
light is the conspicuous shell of starch grains which separates the pyrenoid
matrix from that of the chloroplast (see Figs. 1 and 3). The only other plant in
which the starch grains surrounding the pyrenoid lie within the chloroplast is
the bryophyte Anthoceros. It would appear, however, that the Chlorophyta and
Anthoceros are the exceptions in this respect since in none of the other pyrenoid-
containing forms is there such a close connection between the pyrenoid and the
reserve substances. Indeed, in some instances, as in certain members of the
Bacillariophyceae and of the Rhodophyta, the assimilatory products occur quite
independently of the pyrenoids. The starch grains in the red algae Polysiphonia
denudata K~itz., Nemalio Nemalion multifidum (Web. & Mohr.) J. Ag. (Gibbs
1962c), Porphyra tenera Kjellm. (Ueda 1961), and Porphyridium cruentum
(Gantt and Conti 1965), for example, are scattered throughout the cytoplasm
and show no particular association with the pyrenoid (see Fig. 6) whilst in the
diatoms Biddulphia pulchella Gray and Nitzschia (Ueda, 1961) and in the dino-
flagellate Prorocentrum micans (Kowalik, 1969) the reserve products are simi-
larly quite independent of the pyrenoid.
Many other species fall into an intermediate group in which the assimila-
tory product, although fairly closely associated with the pyrenoid, is never-
theless situated outside the chloroplast. In many species having projecting pyre-
noids, the outside surface of the pyrenoid is bounded by a cap of electron trans-
parent material which may be solid or liquid (Gibbs, 1962a, Manton, 1957).
In the euglenoid flagellates the reserve material is solid paramylum, and
sections of the cup-shaped paramylum caps have shown them to be membrane-
limited cavities, closely neighbouring the pyrenoid, but clearly outside the plastid
envelope (Leedale, 1967). In fact, the paramylum caps may often be separated
from the plastid envelope in places by a narrow region of cytoplasmic matrix.
A similar capping of transparent material occurs in association with the
pyrenoid of Chrysochromulina chiton (Manton, 1966b), although its chemical
nature in this organism has not been definitely established.
The starch grains which surround the pyrenoid in the cryptomonads and
dinoflagellates also lie outside the chloroplast envelope (Gibbs, 1962a, 1962c).
Rhodomonas lens, a member of the Cryptophyceae, has large starch grains
surrounding the pyrenoid but lying outside the chloroplast envelope (Gibbs,
1962c), The starch grains in this alga, like those of Cryptomonas sD. (Gibbs,
1962a), are, however, separated from the cytoplasm by a double membrane
formed by an outfolding of the outer membrane of the nuclear envelope. In
two marine dinoflagellates investigated by Dodge (1968) the mature pyrenoid
is surrounded by a halo of electron-transparent material tentatively identified
as polysaccharide, but probably not starch. The pyrenoid halo of these dino-
Ftc. 6. Section through a dividing cell of Porphyridiura cruentura showing the chloro-
plast with a centrally located pyrenoid (P) as the dominant structure. Starch grains
(S), lacking a bounding membrane, are randomly distributed throughout the cytoplasm,
Chloroplast lametlae extend into and through the pyrenoid.
x 25,000.
(M ---- mitochrondrion; N ~ nucleus; O.B. = osmiophilic body; the arrows shows the
position of the cleavage furrow which develops during cytokineses).
(From: GAN~r, E. & S. F. CoN~, 1965. Jour. Cell Biology 26: 365-381).
flagellates, however, is unlike that of any other known stalked pyrenoid in not
being membrane-limited. Instead, the halo abuts directly onto the cell cyto-
plasm.
The cap of transparent reserve material associated with the pyrenoid of

Chrysochromulina chiton has been investigated in detail by Manton (1966b).
By a careful examination of the membranes on the pyrenoid surface and, in
particular, of the nature of the membranes separating the pyrenoid from its
transparent cap, Manton was able to suggest a possible sequence of events in the
development of the cap. The first step, according to Manton, might be an ac-
cumulation of some translucent metabolite between the two components of the
chloroplast double membrane where they overlay the pyrenoid. The effect of this
accumulation would be to separate the two membranes, forming a blister. The
blister would then force its way out through a gap in the cisterna of endoplas-
mic reticulum which, in this alga, is always found immediately outside the
chloroplast double membrane. Further lateral development of the blister would
produce the typical cap of translucent material covering the endoplasmic
reticulum which lies around the outside of the pyrenoid. This sequence of events,
suggested by Manton is, of course, mere speculation which could be confirmed
only by extensive experimental evidence.
In Nemalion multifidum (Gibbs, 1962a) the pyrenoid is surrounded by
a rim of small, dense, lipid-like globules. Another red alga Kylinia sp. also has
lipid globules in the chloroplast although, in this species, they do not show the
same tendency to rim the pyrenoid. The same is also true of the diatom Nitz-
schia angularis where the globules, although most abundant in the area around
the pyrenoid, do not lie directly against it (Gibbs, 1962a).
The genus EutreptJa and the subgenus Radiatae of Euglena have what have
been termed "paramylum centres" (Leedale, 1967). Each "paramylum centre",
of which there may be one, two or three in a ceil, apparently functions as a
pyrenoid. It is often surrounded by a sheath of separate paramylum granules,
recalling the starch sheath in members of the Chlorophyta. The paramylum
granules are bounded by a unit membrane, and in suitably oriented sections,
elements identical in appearance with the tubular endoplasmic reticulum arise
from the membrane around the granule and join with elements of the vesicular
endoplasmic reticulum. This arrangement has been interpreted by Leedale
(1967) as suggesting that paramylum granules are formed either within the
endoplasmic reticular cavity or else in vesicles which become connected with it.
GROWTH AND DIVISION OF PYRENOIDS

Pyrenoid-containing algae can be divided into two groups with regard to
the behavior of the pyrenoid during cell division. On the one hand are those
species in which division of the pyrenoid precedes division of the chloroplast;
on the other hand are those species in which the pyrenoid disappears before cell
division and is re-formed de novo in the daughter cells.
Examples of the former situation can be found in a range of algae which
includes species having projecting pyrenoids as well as those having immersed
pyrenoids. Studies of the changes in subceIlular structure throughout the cellular
life cycle of synchronous cultures of Chlorella ellipsoidea Gerneck (Murakami
et al., 1963) have shown that in this organism, the pyrenoid is present at all
stages of development, including that in which autospores are still retained
within the mother-cell wall. It would seem that in Chlorella ellipsoidea,

as in various other green algae (Bourquin, 1917; Hartman, 1921), euglenoid
flagellates (Leedale, 1967) and red algae (Gantt & Conti, 1965), the pyrenoid
divides when the chloroplast divides, thus ensuring continuity of the pyrenoid
material.
The bulging pyrenoid of Chrysochromulina chiton often assumes a bilobed
condition (Manton, 1966b), and this fact, together with the observation that
the bilobed condition is found immediately preceding mitosis, is clear evidence
that it represents a dividing pyrenoid. In this case, as in many others involving
division of a projecting pyrenoid (Manton & Leedale, 1961), the plane of
division of the chloroplast must pass through the pyrenoid. Thus, in those mem-
bers of the euglenoid flagellates where the pyrenoid is of the stalked variety,
division of the pyrenoid begins at the distal end and is followed by constriction
and fission of the chloroplast body (Leedale, 1967). The projecting pyrenoids
of certain brown algae appear not to divide with the chromatophore (Evans,
1966). Instead, a new pyrenoid is budded off from the point of attachment of
the old one, the plane of fission then passing between the two.
There is no clear evidence as to the behavior of the pyrenoid inclusions
during division except for the observation of Manton & Leedale (1961) with
Chrysochromulina minor, in which they apparently become more contorted
during the early stages of division.
The most detailed investigation of a pyrenoid which disappears during cell
division has been carried out by Bisalputra & Weier (1964). They examined
the behavior of the pyrenoid of Scenedesmus quadricaz~da by both light and
electron microscopy and were able to trace the development of the pyrenoid
from the time of its first appearance in the daughter cell until its final state of
maximum growth. Their observations confirmed the previous findings of Smith
(1914) that the pyrenoid of Scenedesmus which is extremely large before the
onset of cell division, disappears during cell cleavage and a new pyrenoid is
formed in each of the daughter cells. The pyrenoid of Scenedesmus can be first
distinguished as an accumulation of rather dense material between two broad
bands of stacked chloroplast lamellae. The dense area represents the matrix of
the newly formed pyrenoid and is flanked on either side by two small, round
starch grains. Further development of the pyrenoid is marked by the gradual
elaboration of the surrounding starch sheath and by the encircling of the pyre-
noid and its starch sheath by the continuous growth of the thylakoid discs.
A particularly interesting situation is encountered in those algae having large
multipyrenoidal chromatophores where the relation between the growth of the
chromatophore and of its contained pyrenoids can be readily examined. Szejn-
man (1933) was able to follow the development of pyrenoids in the chromato-
phore of Spirogyra by means of a hanging drop culture. Growth of the ribbon-
shaped chromatophore was found to be most intense during the night which
followed a cellular division. New pyrenoids were formed during the morning
hours, such that a doubling of the length of the chromatophore produced a
doubling in the number of pyrenoids. It is not clear from Szejnman's work how
the pyrenoids arise, although in Oedogoniurn it appears that incipient pyrenoids,
lacking the membrane-limited channels characteristic of mature pyrenoids,

arise de novo in the chloroplast stroma (Hoffman, 1968b).
Finally, mention must be made of the rather unusual situation in Chloro-
gonium elongatum, in which multiplication of the pyrenoid may take any one
of three different forms (Ueda, 1963). The pyrenoid may divide either simul-
taneously with cell division or independently of cell division, or a new pyrenoid
may be formed in the chloroplast.
FUNCTION OF PYRENOIDS
Formation of the Stareh Sheath. Although the close assodation of the
starch sheath with the body of the pyrenoid points to the implication of the
pyrenoid in its formation, there is very little evidence as to the mechanism in-
volved. The earlier suggestions (Schimper, 1883, 1885; Schmitz, 1884; Tim-
berlake, 1901; Bold, 1930; Lutman, 1910) that the substance of the pyrenoid
becomes itself changed into starch, have not been confirmed by more recent
observations with the electron microsope. A view of starch sheath formation
which is perhaps more easily reconciled with the ultrastructural evidence is
that which visualizes a process of secretion of the precursors of starch syn-
thesis from the pyrenoid. Such a view would be more in agreement with the
morphological evidence which, on the whole, points to the pyrenoid's being a
more or less permanent body which retains its identity during starch formation.
There seems to be very little information, however, as to how the starch sheath
becomes built up, apart from the observation (e.g., Ohad et al., 1967) that the
starch plates may sometimes, especially at their periphery, show a periodic
structure consisting of parallel or concentric layers, spaced at approximately
50 A.
The picture of the pyrenoid as a mass of proteinaceous material is not
inconsistent with current views on the mechanism of photosynthesis in algae.
It is now quite clear that when algal cells are under nutrient conditions
suitable for growth, amino acids form a significant proportion of the early
products of photosynthesis (Holm-Hansen et al., 1959; Syrett, 1962). Ac-
cordingly, the pyrenoid of green algae could be regarded as a temporary
storage region of the early products of photosynthesis which, under conditions
of overproduction, could be readily converted into more permanent storage
material in the form of the starch sheath.
The apparent presence of chlorophyll in the pyrenoidal starch of Meso-
taenium caldariorum Lagerheim as indicated by optical methods (Wartenberg,
1965) has been interpreted as evidence of the synthesis of chlorophyll in the
pyrenoid of this alga. According to Wartenberg, the pyrenoidal starch represents
a vehicle for the transportation of chlorophyll (chlorophyll a in particular)
from its site of synthesis in the pyrenoid to the chloroplast. This is an interesting
suggestion, but one which clearly needs verification at the biochemical level.
Formation of Stromal Starch. In many of the starch-producing algae
there are two forms of storage starch, the pyrenoidal starch and the so-called
stromal starch, which is more or less randomly distributed throughout the
chloroplast stroma. There is fairly clear evidence that in many algae the stromal
starch has its origin in the pyrenoid. This view is based partly on the observed
tendency for starch grains to form successive concentric rings around the
pyrenoid and partly on the fact that the pyrenoidal starch ring is often fissured
in various ways indicating a continual separation of small starch masses from
it. Such a situation is clearly seen in Chlorococcum infusionum (Schrank)
Meneghini, in which the similarity in the shape of the stromal starch grains
and those grains still attached to the pyrenoidal ring has been interpreted as in-
dicating that the former are derived from the starch sheath by a centrifugal
migration (Bold, 1930). A similar condition has been described for many other
green algae (Boubier, 1899; Timberlake, 1901; Smith, 1914, 1916).
Further evidence on this point comes from the observation that young cells
very often have their starch grains almost entirely confined to the area of the
pyrenoid (Lang, 1963) and that when starch-containing cells are placed in the
dark, the starch disappears last from the pyrenoid area (Fritsch, 1935; Granick,
1955). In Chlamydomonas reinhardi the first starch formed is stored in the
plates which surround the pyrenoid, but under conditions of starch accumula-
tion, small granules appear scattered throughout the rest of the chloroplast as
well (Sager & Palade, 1957). The latter, it has been shown, have the same
fine structure as the starch sheath and also react in the same way to the various
preparatory prodecures used.
The detailed investigations of Bisalputra & Weier (1964) in which
they followed the development of the pyrenoid of Scenedesmus quadricauda,
point unequivocally to the pyrenoidal origin of the stromal starch in that alga.
They confirmed the tendency for the stromal starch grains of growing cells to
form concentric rings around the pyrenoid and further demonstrated a tran-
sition, within the vicinity of the pyrenoid, in the shape of the starch grains from
concavo-convex platelets (typical of the starch sheath) to lenticular (typical of
the stromal starch). Moreover, the starch grains around the pyrenoid were
shown to be interconnected with each other and with the platelets around the
pyrenoid matrix by narrow bridges.
The evidence presented by Bisalputra and Weier shows that new starch
platelets can be formed in Scenedesmus without any association with the
chloroplast thylakoids. Thus, the intrusive growth of the thylakoids into the
periphery of the pyrenoid matrix, which progressively leads to the separation
of the starch grains into individual pockets, was observed to occur only after
the starch platelets have been deposited in the periphery of the pyrenoid matrix.
This build-up of reserve starch continues throughout the life cycle of the
alga until the onset of cell division when most of it disappears, presumably
to meet the extra demand for energy associated with the division process. How-
ever, it is clear from the observations of Bisalputra & Weier that the parental
starch is not entirely expended at this time and that a certain amount of starch
is passed on to the daughter cells. The distribution of the parental starch
within the daughter cells will depend upon the plane of cleavage of the mother
cells. It could come to be situated well away from the new pyrenoid and there-
fore resemble what might otherwise be referred to as stromal starch. In fact,
Bisalputra & Weier were able to conclude that most of the starch grains of
Sce,nedesmus could be traced, perhaps through a few generations, to the pyre-

hold.
The pyrenoidal origin of stromal starch is not always as obvious as this. In
Zygnema, for example, it appears that the plastid gives rise to minute starch
grains in its periphery, either between the larger grains or entirely beyond them
(Bourquin, 1917). The radial arrangement of the starch gains about the pyren-
old was interpreted by Bourquin as an indication, not of their information from
the pyrenoid, but rather of their method of growth from the periphery of the
plastid. It should be mentioned that this interpretation does not agree with the
earlier findings of Chmilewskij (1896) with similar material. There is fairly
clear evidence, however, that in some starch-producing algae, the pyrenoid
is not an obligate centre of starch formation. Thus Lang (1963) has reported
that in some colonial green algae which normally contain pyrenoids, certain
cells which lack a pyrenoid may nevertheless form stromal starch.
F o r m a t i o n of O t h e r S t o r a g e Materials. The presence of pyrenoids in
certain algae that do not produce starch points to their being concerned, in
these algae, with the synthesis of non-starch storage material. The clearest evi-
dence on this point comes from the work of Manton (1966b) on the projecting
pyrenoids of the genus ChrysochromuI~na. Manton, in her investigation of the
stages of development of the cap of translucent material around the projecting
pyrenoid of C. chiton, obtained clear evidence that the capping material,
though doubtless ultimately dependent on photosynthesis, is itself a product
of translocation which is not light dependent. This conclusion was based on the
observation that the capping material becomes conspicuous in the early hours
of darkness though in full daylight it may remain unformed. It would appear
that in this species, the pyrenoid is a probable pathway by which metabolic
products diffuse into the cytoplasm from the chloroplast. According to this
view, one could picture an enzymic specialization in the surface membranes of
the pyrenoid, permitting local accumulation of products in a form suitable
for temporary storage.
Bouck (1965) in his investigation of the projecting pyrenoids of the brown
algae, Giffordia and Chorda, made a special study of the envelope of chloro-
plast endoplasmic reticulum (E.R.) which forms a loosely fitting sac surround-
ing the chloroplast. By comparing certain features of this envelope in the
vicinity of the pyrenoid on the one hand, and around the rest of the chloroplast
on the other, Bouck was able to make some interesting suggestions as to its
probable role in these two situations. He concluded that, in the vicinity of the
pyrenoid, there could perhaps be a transport of materials across the chloro-
plast E.K, that is to say, from the pyrenoid into the pyrenoid sac which lies
just external to the chloroplast E.R. This contrasts with what happens over
the remainder of the chloroplast E.R. where translocation of materials is
probably along the chloroplast E.R. The validity of Bouck's suggestion
cannot, without further investigation, be properly assessed. If it is correct,
then it would seem that, in these brown algae, the pyrenoid is concerned with
the manufacture and storage (in the collecting sac) of materials destined
for the internal use of the cell, whereas other materials synthesized within the
chloroplast are passed through the surrounding E.R. system, sequestered by the
Golgi apparatus, and ultimately extruded from the cell.
Paramylum, the characteristic storage product of the euglenoid flagellates, is
often formed in sheaths around the pyrenoids, pointing to the implication of the
pyrenoid in its synthesis. However, paramylum also occurs independently of the
pyrenoid, distributed throughout the cytoplasmic matrix of the cell (Leedale,
1967). It is not clear what precise relationship either or both of these forms
of paramylum have with the pyrenoid and the same is also true of various
other non-starch producing algae which have been described (e.g., Drum &
Pankratz, 1964).
Role of the Pyrenoid Inclusions. It is tempting to assign some conduc-
tional significance to the various types of inclusions which penetrate the pyre-
noid. One possibility is that they may represent a drainage system, conducting
the products of photosynthesis from the photosynthetic thylakoids to a region
specialized for the synthesis of storage material. Such a hypothesis would seem
to be particularly appropriate in those algae where the pyrenoid inclusions, be
they thylakoids or tubules, are directly continuous with the chloroplast thyla-
koids. It is interesting to note, in this connection, that the double-disc membranes
that extend into the pyrenoid of the diatom Achnanthes brevipes have asso-
ciated with them small areas of the pyrenoid matrix containing particles which
have been tentatively identified as ribosomes (Holdsworth, 1968) (see Fig. 2).
The presence of these pyrenoid-associated ribosomes is particularly significant in
view of the suggested protein make-up of the pyrenoid and, although there is
no real evidence that the pyrenoidal ribosomes represent the site of synthesis
of the pyrenoid protein, such an idea is clearly very attractive.
In those algae having pyrenoid inclusions in the form of cytoplasmic
channels lined with the invaginated chloroplast envelope, it is possible that
such channels are involved in translocation away from the pyrenoid. In Platy-
monas and Prasinocladus, both members of the Prasinophyceae (Gibbs, 1962c;
Manton, 1966) and in Oedogonium cardiacum (Hoffman, 1968a), the pyre-
noid is penetrated by a system of branched canaliculae entering from the cyto-
plasm. These cytoplasmic channels might represent the means whereby specific
products generated within the chloroplast and required for specific cell functions,
are translocated from the chloroplast to the cell. According to this view,
the pyrenoids are regarded as sites not only of storage, but also of liberation
of metabolites to the cell.
Relation between the Pyrenoid and the Nucleus. In some algae there
appears to be a very close structural relationship between the pyrenoid and the
nucleus. In Chrysochromuli, na minor, for example, the chloroplast endopIas-
mic reticulum, through its connection with the nuclear envelope, provides a
ready means of contact between the nucleus on the one hand and the plastid or
pyrenoid on the other (Manton & Leedale, 1961).
An outfolding of the nuclear membrane which encloses the chloroplast
has been found in a number of algae (Gibbs, 1962d) and where this happens,
the nucleus is usually situated adjacent to the pyrenoid region of the chloro-
plast. Such an arrangement would clearly allow materials to pass directly be-
tween the pyrenoid and the nucleus without entering the cytoplasm. It may be
significant that the starch grains in the Cryptophyceae are deposited in the space
between the chloroplast envelope and the outer envelope, that is, between the
pyrenoid and the nucleus.
In Chrysochromulina kappa Parke & Manton and C. minor the nucleus is
commonly applied so closely to the projecting pyrenoid as to be virtually
wrapped round it (Manton & Leedale, 1961), whilst in Prasio~ocladus the
pyrenoid is penetrated by canals filled with protrusions of the nucleus. It is not
known whether the special contact established in these examples, between the
nucleus and the pyrenoid, is metabolically significant or not. If an interchange
of materials between the pyrenoid and the nucleus is indeed a significant factor
then the projecting pyrenoid itself might become interpretable in an adaptive
sense as in some way facilitating this. However, Manton (1966a) warns
against such a facile explanation and suggests that a purely mechanical inter-
pretation of the position of the nucleus seems at least as likely.
PYRENOIDS UNDER ABNORMAL CONDITIONS

Relatively little work which could be described as experimental in nature
has been done on pyrenoids. What little there is, has been concerned in the main
with the appearance of the pyrenoid following various treatments. Some treat-
ments result in a complete disappearance of the pyrenoid and are chiefly
important in that they often provide suitable material for investigation of the
reconstitution of the pyrenoid during the recovery period.
Lefort (1962) followed the reappearance of the pyrenoid during light-
recovery of an X-ray-induced mutant of Chlorella vulgaris Beijerink. Dark
grown cells of the mutant form have chloroplasts in which the thylakoids are
reduced to vesicles, but after a period of one hour in the light, the vesicles
begin to fuse to form double lamellae which later produce the thylakoids typical
of normal autotrophic cells. It is only after 8 hours recovery, however, that the
first indication of a pyrenoid is observed and a period of 48 hours illumination
is required before the pyrenoid is fully constituted. New pyrenoids were also
observed to arise in cells of Closterium moniliferum Ehrenb. within 36 hours
after the existing pyrenoids had been displaced by centrifugation (Weber,
1965). The centrifuged pyrenoids, according to Weber, seemed to retain their
integrity and to become distributed among the daughter cells during subse-
quent divisions. In neither of these instances, however, were any details of the
mechanism of pyrenoid formation observed.
Treatment of Chlamydomonas with colchicine induces marked changes in
chloroplast ultrastructure. One of the effects is an increase in the number of
pyrenoids (Bell, 1955; Buffaloe, 1959; Walne, 1967), which is usually first
apparent after 18-24 hours exposure to colchicine and continues for the dura-
tion of the treatment. Enlarged cells with 8-10 pyrenoids occur among cultures
subjected to the drug for 48 hours or more. Apart from the increase in number,
there do not appear to be any modifications in the ultrastmcture (Walne,
1967). It is not stated, however, whether the pyrenoids arise from division of
pre-existing pyrenoids or whether they arise de novo in the chloroplast stroma.
GRIFFITHS: THE PYRENOED 49
When cultures of Scenedesmus quadricauda are treated for 3 days with

sufficient Amitrol (3-amino-l,2,4,-triazole) to inhibit cell division almost com-
pletely (Castelfranco & BisaIputra, 1965) the cells develop enormously large
starch grains which crowd the other organelles. It seems clear from the observa-
tions, however, that this starch accumulation is not primarily due to an increased
activity of the pyrenoid, but rather to a deposition of starch directly in the chlo-
roplast stroma. This is particularly interesting in view of the suggestion (Bisal-
putra & Weier, 1964) mentioned earlier, that all the starch of normal cells of
this alga is probably derived from the pyrenoid. One possible explanation is that
inhibition of some segment of the cell's metabolism (e.g., purine metabolism)
causes a diversion of the synthetic machinery towards excessive starch formation
and that this abnormal situation allows starch to be synthesized and to accumu-
late in a region where, because of the demands of a variety of synthetic proces-
ses it would not normally be able to accumulate.
A similar diversion of the cell's synthetic processes towards starch synthesis
has been noted in the non-dividing 'giant' cells of the Emerson strain of Chlo-
rella vulgaris which are formed under heterotrophic conditions (Griffiths,
1965). Autotrophically-grown cells of this strain have their starch content very
largely confined to the starch sheath surrounding the pyrenoid. In the hetero-
trophically-grown "giant" cells, although the starch sheath is bulkier than is the
case in normal cells, the most massive starch deposits occur in the chloroplast
stroma where they tend to disrupt the sparsely developed chloroplast lamellae
(Griffiths & Griffiths, 1969). It is clear that here, as in the Amitrol-treated cells
of Scenedesmus mentioned above, the abnormal situation created by the treat-
ment allows for the functioning of starch-synthesizing centres which are not
normally active.
According to this view, the pyrenoid of these algae could be regarded as a
specialized region of the cell where the starch-synthesizing machinery is
favoured over the various other processes which normally drain the products
of photosynthesis. The idea of the pyrenoid as an area of protection is supported
by the observation that under conditions of starch mobilization (e.g., condi-
tions of starvation), pyrenoidal starch is the last to disappear.
Some algae, when cultured in the dark, lose their pyrenoids completely
(Andreyeva & Sedova, 1965). This disappearance of the pyrenoids apparently
occurs even in those algae growing well under heterotrophic nutritional
conditions. It would appear, therefore, that the pyrenoid in these algae is
not an important component of the metabolic machinery when the carbon
and energy supply comes from a non-photosynthetic source.
TAXONOMIC CONSIDERATIONS
The fact that, with the exception of Anthoceros, pyrenoid-containing species
are found only among the algae has led to some speculation as to the signifi-
cance of this. Leyon (1954) in noting that pyrenoids are found only in plants
whose chloroplasts do not contain grana, argued that there may be some con-
nection as to function or phylogenesis between the grana of archegoniates and
phanerogams on the one hand and the pyrenoids of algae on the other.
It seems far more logical, however, to regard these two systems, the grana
and the pyrenoids, as being phylogenetically distinct, with their respective
evolutionary changes not functionally related in any way. Support for this idea
comes from the observation that the chloroplast of Chlamydomonas may con-
tain partly differentiated grana, a well developed pyrenoid, as well as extra-
pyrenoidal deposits of starch (Sager & Palade, 1957). This was taken to indicate
that the grana represent an advanced organization of chloroplast discs, whereas
the pyrenoid is a primitive organ of starch synthesis whose function is gradu-
ally taken over by certain interdisc regions of the chloroplast.
A similar view has been put forward by Klein & Cronquist (1967) who
interpreted the absence of pyrenoids from the most advanced members of cer-
tain algal groups as reflecting a greater specialization of the chloroplast in
the~e species. They argued that the increasing organization and specialization of
the chloroplast for photosynthesis alone has required the replacement of the
pyrenoid by an alternative, less bulky mechanism for performing its functions.
Further support for this idea comes from the observed similarity between the
crystalline structure of the pyrenoid of some species and certain crystals found in
the chloroplasts of higher plants (Holdsworth, 1968; Kowalik, 1969). It may
be significant that the only alga reported to have crystalline bodies within its
chloroplast is a cryophilic form, tentatively identified as a species of Chlamy-
domonas, which does not have a pyrenoid (Stein & Bisalputra, 1969).
It could be said, therefore, that pyrenoids may also be present in arche-
goniates and phanerogams but are too finely distributed to be discerned. The
pyrenoid of Anthoceros would seem to have particular significance in this con-
nection. It is reported to consist of small units (25 to many hundreds) which
may form an aggregate central mass within the chloroplast, or may be distri-
buted throughout the whole chloroplast as small separate producers of starch.
Kaja (1954), in fact, describes the evolutionary steps in pyrenoid disintegration
in a comparison of different species of Anthoceros, which show a range of
types, from a homogenous pyrenoid to complete dispersal throughout the chloro-
plast. It could be argued, therefore, that the pyrenoid of Anthoceros holds an
intermediary position between the typical pyrenoid of algae and the situation
as it exists in higher plants.
Klein & Cronquist (1967), in their review of the thallophytes, drew parti-
cular attention to the absence of a pyrenoid from the photosynthetic bacteria
and the blue-green algae. In these forms, where the photosynthetic apparatus is
not contained within a membrane-bounded chloroplast, the dark reactions, it
was argued, would probably take place away from the site of the light reactions.
The organization of the photosynthetic apparatus into a compact chloroplast
in all the other major algal groups might therefore be expected to limit the
dispersal of the products of the light reaction thus forcing the dark reactions to
take place within the chloroplast. The pyrenoid, according to Klein & Cronquist,
could thus be interpreted as the first evolutionary answer to the necessity of
removing photosynthate from the site of continuing photosynthesis. Those algae
not possessing a pyrenoid, it could be argued, have evidently evolved an alter-
native mechanism to accomplish this, as has clearly occurred in all the other
major plant groups with the exception of the Anthocerotae.
The usefulness of the pyrenoid as a criterion in the classification of algae
appears to be rather limited. One of the major inconveniences is the extreme
difficulty with which the pyrenoid can be effectively investigated with the
light microscope. This applies particularly to certain algal groups such as the
Chrysophyceae where the pyrenoid is a colorless region in a small and often
rather pale plastid which does not stain with any of the usual reagents giving
diagnostic color reactions with other cell components. The electron micro-
scope, therefore, becomes an indispensable instrument for establishing the basic
facts.
Pyrenoid-containing species are distributed throughout the major algal
groups, and it is difficult to correlate the presence or absence of a pyrenoid
with any of the other major criteria for classification. Within the brown algae,
for example, pyrenoids have been shown to be present in certain members of
the Ectocarpales, Chordariales, Scytosiphonales and Dictyosiphonales, but absent
from species belonging to the Tilopteridales, Sphacelariales, Cutleriales, Dictyo-
tales, Sporochnales, Desmarestiales, Laminariales and Fucales (Simon, 1954).
There is, moreover, some variation within these groups. Thus, although pyre-
noids are generally present in the Dictyosiphonales they are apparently absent
from the family Dictyosiphonaceae (Simon, 1954); and the presence of pyre-
noids in Sphacelaria bJpinnata (Evans, 1966) is contrary to the general absence
of pyrenoids from the Sphacelariales. Even more confusing is the conflicting
evidence regarding the presence of pyrenoids in American representatives of
Chorda filum (Bouck, 1965) as compared with the complete absence of pyre-
noids from related European species (Evans, 1966). Occasionally, as in a
number of brown algae (Evans, 1966; Bourne & Cole, 1968), pyrenoids
may be present in cells of the sporelings but absent from cells of the mature
thallus.
In the red algae, there is perhaps some correlation between the presence of
pyrenoids and the assumed degree of evolutionary specialization in that pyre-
niods are commonly found only in species belonging to the two most "primi-
tive" orders, the Bangiales and the Nemalionales (Gibbs, 1962a). In the
Chrysophyta, pyrenoi.ds are relatively widespread in the Chrysophyceae and
Bacillariophyceae, but are present in only a few members of the Xanthophyceae
(Gibbs, 1962a).
Projecting pyrenoids have been described in species belonging to several
algal groups, namely, the Phaeophyceae, the Dinophyceae, the Haptophyceae, and
the Euglenophyceae. It is tempting to try to assign some phylogenetic signi-
ficance to this fact. However, on the basis of the complexity of the chromato-
phore lamellations, the nature of the pigments, and the capacity of the thyla-
koids to adhere together in stacks, such a conclusion is very difficult to justify.
A further difficulty is the extreme variability in the structure of the pyrenoids
within any one group. Thus, within the group recognized as the euglenoid
flagellates (Leedale, 1967) there are certain genera (e.g. Phacus, Lepocinclis,
Klebsiella) which have numerous discoid chloroplasts without pyrenoids and

others (e.g. Cotacium), some species of Trachetomonas, one species of Euglena,
(Iyengar, 1962) having large, well developed pyrenoids projecting from the in-
ner surface of plate-like chloroplasts. Aslo included in this group are species
with the pyrenoid embedded within the chloroplast and either sheathed with
caps of the polysaccharide paramylum (e.g., subgenus Catilliferae of Euglena,
some species of Trachelomonas) or "naked" with no associated paramylum
(e.g., Euglena subgenus SerDentes and some species of Trachelomonas). Two
rather different types of pyrenoid can be encountered among the array of species
described under the comprehensive genus Chrysochromulina (Manton & Leedale,
1961). Thus, pro~ecting pyrenoids occur in C. chiton, C. minor and C. kappa;
immersed pyrenoids in C. strobilus, C. erecta, C. ephippum, C. olifer and C.
brevifilum. Members of the Bacillariophyceae may have pyrenoids embedded in
the chloroplast but bounded by a membrane (e.g. Surirella ovalis Br~b., Nitzschia
(two species), Cymbella a[finis Kiitz., Achnanthes minutissima Kiitz and
Cydotella meneghiniania Kiitz.) or without a membrane and separated from
the chloroplast matrix only by a boundary (e.g., Gomphonema parvulum
Kfitz., Streptotheca thamesis) (Drum & Pankratz, 1964; Esser, 1967).
A similar variability occurs in the detailed internal structure of the pyre-
noids, and very often a whole range of different types of pyrenoid inclusions
may occur within a group of closely-related species. Sometimes, the number of
layers in the pyrenoid inclusions may vary from a few to a great many, even
within one species (Ueda, 1961). In two species of Chrysochomulina having
projecting pyrenoids one, C. minor., has a few two-disc bands crossing the
pyrenoid (Manton & Leedale, 1961), while the other, C. chiton, has short single
discs or tubules (Parke, Manton, & Clarke, 1958).
It seems fairly clear that the detailed structure of the pyrenoid bears no
relation with the systematic position of the alga. For example, in the diatom
Lithodesmium undulatum Ehrenb. (Manton, 1966a) the lamellations recall
those of some of the brown algae, but the pyrenoid core closely resembles those
of the simpler green algae. An even closer parallel with the latter can be found
in many members of the Chrysophyta e.g. Chrysochromulina strobilus, Prym-
nesium parvum Carter (Manton, 1966a). It is therefore extremely unlikely
that the pyrenoid will provide distinctive taxonomic characters at anything above
the generic level. At this level, however, pyrenoid characteristics may prove use-
ful as seems to have happened in Chlamydomonas, where two new species
Fro. 7. Longitudinal section through a cell of Platymonas subcordi[ormis. In this section

a channel of cytoplasm extends all the way across the pyrenoid (p) and separates one
lobe of the chloroplast from the rest. Fingers of cytoplasm (el) extend into the pyrenoid
from the main channel. A substance (sl) which resembles starch in its low electron
density is present at the ends of the fingers.
X 31,000.
(ee = chloroplast envelope; m = mitochondrion; r = ribosomes; s = starch grains).
(From: GIBBS, S. P. 1962. Jour. Ultrastruct. Research 7: 262-272).
GRIFFITHS: T H E PYRENOID 53
described by Ettl (1960) were both apparently characterised by a deviating

structure of the pyrenoids.
C O N C L U D I N G REMARKS
During the last decade or so there has been a tremendous increase in our
knowledge of the structural relationships between the pyrenoid and the chloro-
plast in a wide variety of algae. Relatively little, however, appears to be known
about the physiological significance of the various structural arrangements.
It would seem that the common character represented by all the various types of
pyrenoid is not the reserve material which may or may not be associated with
the pyrenoid and even when present may take various forms, but rather some
involvement with the machinery controlling the distribution of the products of
photosynthesis to the cell.
Pyrenoid-containing species would seem to occupy a rather special posi-
tion in the evolution of the process of photosynthesis. The pyrenoid could per-
haps be regarded as the first evolutionary answer to the problems of transloca-
tion of photosynthate which arise from the establishment of a membrane-
enclosed chloroplast. The variety of different pyrenoid structures could, there-
fore, be interpreted as a reflection of the ways in which different algal types
have dealt with this aspect of their metabolic functions. This is seen most
clearly in those algae where there appears to be a close structural relationship
between the pyrenoid and certain other cellular organelles, in particular the en-
doplasmic reticulum or the nucleus. Where such structural connections with
other organelles are not so obvious, the pyrenoid seems to be more concerned
with the storage of materials within the cell. The various structural features such
as the pyrenoid inclusions of some algae, which probably facilitate movement
of the products of photosynthesis to the pyrenoid, are clearly involved in the
diversion of a certain portion of the photosynthetic products towards storage,
rather than towards various metabolic requirements inside or outside the cell.
Obviously, a great deal more evidence is required before the exact role of the
pyrenoid in the metabolism of different algae can be adequately explained.
What is particularly required is an experimental follow-up of the cytological
evidence now available, including a biochemical verification of the processes
involved. Unfortunately, the pyrenoid, because of its peculiar nature and posi-
tion, does not lend itself very readily to the usual procedures of bulk isolation
which have been so successfully used with various other cellular organelles.
However, there is no doubt that the time is ripe for a more physiological
approach to the study of pyrenoids.
ACKNOWLEDGMENTS
The author wishes to thank the following for so kindly providing photo-
graphs from their published papers: I. Ohad, P. Siekevitz, and G. E. Palade
(Figs. 1, 3, 4, and 5); R. H. Holdsworth (Fig. 2); E. Gantt and S. F. Conti
(Fig. 6); and Sarah P. Gibbs (Fig. 7).
Permission to republish these photographs was very kindly granted by the
Rockefeller University Press, New York (Figs. 1-6) and the Academic Press,
New York (Fig. 7).
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The Botanical Review 1970 v36

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THE PYRENOID

Bundoora, Victoria, Australia

Embedded pyrenoids are usually spherical or sub-spherical bodies set deeply

FIG. 1. Section through the chloroplast of Chlamydoraonas reinhardi showing it to

of the pyrenoid matrix has been recorded for Haematococcus (Wygasch,

twisted manner (Lembi & Lang, 1965). A particularly interesting situation is

chloroplast thylakoids as they enter the pyrenoid is a little difficult to establish,

FIG. 3. Section through a portion of the pyrenoid of Chlamydomonas reinhardi showing

the rest of the cell by micro-dissection. Microscopic examination of such iso-

The cap of transparent reserve material associated with the pyrenoid of

GROWTH AND DIVISION OF PYRENOIDS

within the mother-cell wall. It would seem that in Chlorella ellipsoidea,

lacking the membrane-limited channels characteristic of mature pyrenoids,

Sce,nedesmus could be traced, perhaps through a few generations, to the pyre-

PYRENOIDS UNDER ABNORMAL CONDITIONS

When cultures of Scenedesmus quadricauda are treated for 3 days with

Klebsiella) which have numerous discoid chloroplasts without pyrenoids and

Fro. 7. Longitudinal section through a cell of Platymonas subcordi[ormis. In this section

described by Ettl (1960) were both apparently characterised by a deviating

ANDREYEVA, U. M. & T. V. SEDOVA. 1965. Ob izmenchivosti sistematicheskikh priznakov

9 1962b. The Ultrastructure of the pyrenoids of green algae. Jour. Ultra-

LEX'ON, H. 1954. The structure of chloroplasts. III. A study of pyrenoids. Exptl.

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