HELGOLANDER MEERESUNTERSUCHUNGEN
Helgol~nder Meeresunters. 42, 339-383 (1988)
T h e e m e r g e n c e of a n e w c h l o r o p h y t a n s y s t e m , a n d
Dr. K o r n m a n n ' s c o n t r i b u t i o n thereto*
C. v a n d e n H o e k , W. T. S t a m & J. L. O l s e n
Department of Marine Biology, Biological Centre of the University of Groningen;
PO Box 14, 9750 A A Haren (Gn), The Netherlands
ABSTRACT: In traditional chlorophytan systems the organizational level was the primary character
for the distinction of main groups (classes a n d orders). For instance, in Fott (1971), the flagellate level
corresponds with the Volvocales, the coccoid level with the Chlorococcales, the filamentous level
with the Ulotrichales, the siphonocladous level with the Siphonocladales, a n d the siphonous level
with the Bryopsidales. The n e w system presented here is an elaboration a n d emendation of recently
proposed taxonomies a n d their underlying phylogenetic hypotheses, and it is mainly b a s e d on
ultrastructural features which have b e c o m e available over the last 15 years. The following criteria
are used for the distinction of classes a n d orders: (1) architecture of the flagellate cell (flagellate cells
are considered as the depositories of primitive characters); (2) type of mitosis-cytokinesis; (3) place of
meiosis in the life history and, consequently, the sexual hfe history type; (4) organizational level a n d
thallus architecture; (5) habitat type (marine versus feshwater and terrestrial); (6) chloroplast type.
The following classes are presented: Prasinophyceae, Chlamydophyceae, Ulvophyceae (orders
Codiolales, Ulvales, Cladophorales, Bryopsidales, Dasycladales), Pteurastrophyceae (?), Chlorophyceae s.s. (orders Cyhndrocapsales, Oedogoniales, Chaetophorales), Zygnematophyceae, Trentepohhophyceae, Charophyceae (orders Klebsormidiales, Coleochaetales, Charales). The n e w system no longer reflects the traditional hypothesis of a stepwise evolutionary progression of organizational levels in which the flagellate level represents the most primitive lineage, the coccoid a n d
sarcinoid levels h n e a g e s of intermediate derivation, and the filamentous, siphonocladous a n d
siphonous levels the most derived lineages. Instead, it is now hypothesized that these levels have
arisen over and over a g a i n in different chlorophytan h n e a g e s which are primarily characterized by
their type of flagellate cell. The flagellate g r e e n algal c/asses Prasinophyceae (with organic body
scales) and Chlamydophyceae probably represent bundles of highly conservative h n e a g e s that
diverged very long ago. Consequently, extant genera and species in these classes can be expected to
have emerged long ago. Fossil evidence points to a minimum age of 600 Ma of certain extant
Prasinophycean genera, a n d molecular evidence to a minimum age of 400-500 M a of a few
Chlamydomonas species. On the contrary, the most derived "green algal" lineage, the Angiosperms, can b e expected to consist of, on average, m u c h younger g e n e r a a n d species. Fossil
evidence points to a m i n i m u m age of g e n e r a of 5-60 Ma. Lineages of intermediate evolutionary
derivation (Ulvophyceae, Chlorophyceae, Charophyceae) can b e expected to encompass g e n e r a and
s p e d e s of intermediate age, Fossil and (limited) molecular evidence point to a m i n i m u m age of
230-70 Ma of extant g e n e r a in Bryopsidales, Dasycladales and Cladophorales (Ulvophyceae) a n d of
250-80 M a of extant g e n e r a in Charales (Charophyceae).
* Dedicated to Dr. h. c. P. Kornmann, on the occasion of his 80th birthday.
9 Biotogische Anstalt Helgoland, H a m b u r g
C. v a n d e n Hoek, W. T. Stare & J. L. Olsen
340
TRADITIONAL CHLOROPHYTAN SYSTEMS
In traditional chlorophytan systems (e.g. Fritsch, 1948; Fott, 1971; v a n d e n Hoek &
Jahns, 1978; Bold & Wynne, 1985; Bold et 'aL, 1987) the organizational level was the
primary character used for the distinction of the main groups (orders, classes) within the
division Chlorophyta.
Table 1. Subdivision of Chlorophyta according to Fott (1971)
(I) Class Chlorophyceae
Order J Suborder
Criterion:
organisational
level
Flagellate
Palmelloid
Coccoid
Volvocales
Tetrasporales
Chlorococcales
Filamentous
Ulotrichales
sarcinoid
- unbranched
filamentous
- unbranched
filamentous, cell
wall of H-pieces
- unbranched
filamentous, special
features of celldivision and
- Chlorosarcinineae
- Ulotrichineae
-
- Microsporineae
- Oedogoniineae
reproduction
- branched filamentous
Siphonocladous
Siphonous
- Chaetophoriineae
Siphonocladales
Bryopsidales
(II) Class Conjugatophyceae
Essentially with coccoid organisational level,
special features of reproduction (conjugation).
(III) Class Charophyceae
Special vegetative and reproductive architecture
As an example, Fott's chlorophytan system of 1971 is p r e s e n t e d in T a b l e 1. This
system reflects the phylogenetic hypothesis that flagellate unicellular chlorophytes are
primitive a n d have evolved, through coccoid a n d sarcinoid chlorophytes, into filamentous
a n d siphonous chlorophytes. This hypothesis is illustrated b y Figure i. It reflects ideas
developed already by Blackman (1900) a n d Pascher (1914). According to this hypothesis,
the Bryophytes a n d Tracheophytes are derived from b r a n c h e d filamentous chlorophytes.
A n e w chlorophytan system
12
6
9
10
7
I
VOLVOCALES
11
2
I I
TETRASPORA-
341
CHLOROCOCCALES
I
CHLO- MICRO- ULO- OEDO- CHAEROSAR- SPOT R I - GOTOSINI- RIC H I - NII
PHO~
BRYOPHYTES
+
II
SIPHONOCLADALES
BRYOPSIDALES
I
CONJUGATOPHYCEAE
C~.%ROPHYCEAE
TRACHEO-
U L O T R
H
L
I
\
I
I
C H L O R O P H Y C E A E
Fig. 1. Phylogeny and subdivision of Chlorophyta according to Fott (1971). 1 Flagellate organizational level (Chlarnydomonas). 2 Coccoid organizational level (Chlorococcum). 3 Sarcinoid (=
package-like) organizational level (Chlorosarcinopsis). 4 Filamentous organizational level (Microspora). 5 Thallose organizational level, derived from the filamentous level (Ulva). 6 Filamentous
organizational level (Uronema). 7 Filamentous organizational level (Oedogonium). 8 Branched
filamentous organizational level (Trentepohlia]. 9 Siphonocladous organizational level
(Cladophora). 10 Siphonous organizational level (Bryopsis). 11 Coccoid organizational level, special
features (Euastrum). 12 Chara-like architecture (Chara)
Fott points to the terrestrial chlorophytes Fritschiella and Trentepohli~ as possible
representatives of ancestral groups of the higher land plants.
W h e n in 1971 Fott presented his overview of the then, a n d perhaps e v e n now,
p r e d o m i n a n t hypothesis about chlorophytan phylogeny, Dr. K o r n m a n n was already
sowing the seeds of revolution against its basic assumption. Dr. K o r n m a n n had realized
that a group of morphologically very divergent g r e e n algae should be u n i t e d into one
order or even class (Kornmann, 1963, 1973), b e c a u s e they share a very characteristic type
of life history i n c l u d i n g a unicellular Codiolum-like stage containing the zygote nucleus.
In 1973 he proposed to range these chlorophytes in the class Codiolophyceae. This class
i n c l u d e d algae of the coccoid (Kornmann & Sahling, 1983), u n b r a n c h e d filamentous,
b r a n c h e d filamentous, siphonocladous a n d thallose organisational levels.
The concept of the Codiolophyceae would of course disrupt the basis of the traditional system a n d phylogeny, n a m e l y the a s s u m p t i o n that each organizational level
should represent one principal evolutionary l i n e a g e within the Chlorophyta.
342
C. v a n d e n Hoek, W. T. S t a m & J. L. Olsen
In the m e a n t i m e a n u m b e r of other r e s e a r c h e r s (e.g. P i c k e t t - H e a p s , Stewart &
Mattox, Moestrup, Melkonian, Floyd, O'Kelly, Lokhorst, Sluiman, P i e n a a r , Norris, Hori,
Triemer, Roberts) g r a d u a l l y a c c u m u l a t e d an e n o r m o u s a m o u n t of f a s c i n a t i n g m a i n l y
ultrastructural information which did not support the traditional h y p o t h e s i s that the
i n c r e a s i n g l y d e r i v e d organizational levels r e p r e s e n t the m a i n e v o l u t i o n a r y l i n e a g e s
within the Chlorophyta.
In the course of the p a s t 15 years various reconstructions of the c h l o r o p h y t a n system
a n d p h y l o g e n y h a v e b e e n p r o p o s e d on the basis of all these n e w d a t a ( M a t t o x & Stewart,
1984; M e l k o n i a n , 1982; O'Kelly & Floyd, 1984; Stewart & Mattox, 1978; S l u i m a n , 1985b;
Sluiman et al., 1980a). The system which w e will p r e s e n t h e r e is a further e l a b o r a t i o n a n d
e m e n d a t i o n of these proposals, whose e s s e n c e is, in their most r e c e n t form, a subdivision
of the C h l o r o p h y t a into four main evolutionary l i n e a g e s (classes): the P r a s i n o p h y c e a e ,
the C h l o r o p h y c e a e , the Ulvophyceae, a n d the C h a r o p h y c e a e .
A NEW C H L O R O P H Y T A N SYSTEM
First of all, w e p r o p o s e a n e w subdivision of the C h l o r o p h y t a in c l a s s e s a n d orders
(Table 2). Secondly, w e will shortly treat the m a i n criteria u s e d for this s u b d i v i s i o n (Table
2 a n d below). Thirdly, w e will discuss s e v e r a l implications of the n e w s y s t e m a n d its
u n d e r l y i n g p h y l o g e n e t i c hypotheses; implications which are often o v e r l o o k e d .
C r i t e r i a for t h e d i s t i n c t i o n o f c h l o r o p h y t a n c l a s s e s a n d o r d e r s
See T a b l e 2 for the m a i n criteria.
Architecture o f the flageflate cell
The evolutionary i m p o r t a n c e a s c r i b e d to the architecture of the f l a g e l l a t e cell is
b a s e d on the concept that this architecture t e n d s to b e conservative b e c a u s e flagellate
cells, with their typical e u k a r y o t a n flagella h a v i n g the "9+2" axoneme, o c c u r in w i d e l y
different e u k a r y o t a n organisms (e.g. most algal groups, certain fungi, ferns, animals).
The implication of this concept is that unicellular flagellate o r g a n i s m s t e n d to b e
evolutionarily more conservative than non-flagellate multicellular or m u l t i n u c l e a t e organisms.
Within the chlorophytes, at least five or even six different types of f l a g e l l a t e cells
h a v e n o w b e e n recognized.
(1) F r e e living flagellate cells whose b o d i e s a n d flagelia are c o v e r e d b y s e v e r a l layers
of more or less e l a b o r a t e organic scales w h i c h are p r o d u c e d in G o l g i - b o d i e s (Fig. 2).
This t y p e is d e e m e d characteristic of the class Prasinophyceae. T h e form of the cell
a n d the construction of the flagellar a p p a r a t u s , i.e. the root system a n c h o r i n g the flagella
in the ceil, are h i g h l y variable (Fig. 18). However, the possession of p r o m i n e n t transv e r s e l y striated rhizoplasts is c o n s i d e r e d characteristic of this t y p e (Fig. 3). (A selection of
references: Ettl, 1983; Hori et al., 1985, 1986; Inouye et al., 1983, 1985; M e l k o n i a n , 1981a;
Moestrup, 1982; M o e s t r u p & Ettl, 1979; M o e s t r u p & Walne, 1979; Norris, 1980, 1982;
Norris & Pienaar, 1978; Parke et al., 1978; Pennick, 1984; Pienaar & A k e n , 1985).
(2) F l a g e l l a t e ceils of the cruciate t y p e with a 1 o'clock/7 o'clock c o n f i g u r a t i o n of the
flagellar a p p a r a t u s (Fig. 4).
A n e w chlorophytan system
343
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C. v a n d e n H o e k ,
344
W . T. S t a m & J. L. O l s e n
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A new chlorophytan system
The cruciate praslnopbycean
345
zoid type with four nearly parallel
~
basal bodies: Pyramimonas.
FL
N
GB
|
M
FL
CV
Fig. 2. Pyramimonas lunata, a zoid of the cruciate prasinophycean type (semidiagrammatic). a Light
microscopic image; b Electron-microscopic image; c Top view of cell. CHL-chloroplast; CV =
cylindrical vesicle containing outer body scales formed in the Golgi apparatus; FL = flagellum; FP =
flagellar pit; FS = flagellar scales; GB = Golgi body., IBS = inner layer body scales; M =
mitochrondrion; MB = microbody; MBS = middle layer body scales; MR = microtubular root of
flagellar apparatus; N = nucleus; OBS = outer layer body scales., P = pyrenoid; PMT = pit
microtubules; RH = rhizoplast; SPL = starch plate on pyrenoid; SR = scale reservoir; ST = stigma;
SY = synistosome; T = trichocyst; TH = thylakoid (Based on Inouye et al., 1983)
T h e cells, w h e n l a t e r a l l y v i e w e d , a r e a p p r o x i m a t e l y b i l a t e r a l l y s y m m e t r i c a l . T h e
f l a g e l l a r b a s a l b o d i e s a r e a n c h o r e d i n t h e cell b y four c r u c i a t e l y a r r a n g e d m i c r o t u b u l a r
roots w h e n t h e cell is v i e w e d o n its tip (Fig. 5). T w o o p p o s i t e r o o t s c o n s i s t e a c h of t w o
m i c r o t u b u l e s , a n d t h e t w o r e m a i n i n g o p p o s i t e r o o t s e a c h c o n s i s t of a v a r y i n g n u m b e r
( m o s t l y 3-8) m i c r o t u b u l e s . T h i s a r r a n g e m e n t of t h e m i c r o t u b u l a r r o o t s h a s b e e n t e r m e d
t h e X - 2 - X - 2 p a t t e r n ( M o e s t r u p , 1978). W h e n v i e w e d o n t h e tip of t h e cell, t h e t w o b a s a l
346
C. v a n d e n Hoek, W. T. Stam & J. L. Olsen
2R
IR
~r"
Fig. 3. Pyramirnonas, diagram of the flageUar apparatus. BAB = basal body of flagellum; LB = lateral
fibrous band; N = nucleus, NSC = nonstriated connective; 2-R = 2-stranded microtubular root;
4-R = 4-stranded microtubuIar root; Su = syrdstosome (Based on Pienaar & Aken, 1985)
bodies are not precisely in fine with one a n o t h e r b u t take 1 o'clock/7 o'clock positions
(Fig. 6).
Other ultrastructural features of the flageIlar apparatus are also c o n s i d e r e d characteristic of this type; for instance, the possession of a n u p p e r t r a n s v e r s e l y striated
connective h n k i n g the basal bodies (Fig. 5). The basal bodies are each (at l e a s t in some
species of Chlamydomonas a n d related genera) c o n n e c t e d by a rhizoplast to the n u c l e a r
envelope (not indicated in Fig. 5). These rhizoplasts are m u c h more dehcate t h a n those in
the Prasinophyceae, a n d have a p p a r e n t l y often b e e n overlooked (cf. Eyden, 1975; Hyams
& Chasey, 1974; Lembi, 1975; Katz & McLean, 1979; M e l k o n i a n & Preisig, 1984). This
flagellate cell type is considered characteristic of the Chlamydophyceae, a class of free
living g r e e n flagellates (Ettl, 1981; Ettl & Komhrek, 1982), a n d of the r e p r o d u c t i v e zoids in
the class Chiorophyceae s.s. In contrast to Ettl (198I, 1983), we also i n c l u d e "naked"
relatives of Chlamydomonas such as Dunafiella in the C h l a m y d o p h y c e a e . Dunafiella
appears to be covered b y a vestigial "wall" of glycoproteins which are also a n important
constituent of Chlamydomonas walls (Chardard, 1987). We agree with Ettl's i n c l u d i n g
"near-flagellate" coccoid g r e e n algae, such as Chlorococcum, in the C h l a m y d o p h y c e a e .
(A selection of references for C h l a m y d o p h y c e a e ; Brown et al., 1976; G o o d e n o u g h &
Weiss, 1978; G r e u e l & Floyd, 1985; H o o p s , 1984; Hoops & Floyd, 1983; Katz & McLean,
1979; Lembi, 1980; M e l k o n i a n & Preisig, 1984; Moestrup, 1978, 1982; O ' K e l l y & Floyd,
1984; and for Chlorophyceae: Buchheim & Hoffmann, 1986; Floyd & Hoops, 1980; Floyd
A new chlorophytan system
347
lOpm
ST.PS~SPk
IL
I
Fig. 4. The cruciate chlamydophycean and chlorophycean zoid type with a 1 o'clock/7 o'clock
configuration of the two basal bodies: Chlamydomonas. a Light microscope image; b Electron
microscopic image, schematic (BAB = basal body of flagellum; CHL = chloroplast; CV = contractile
vacuole; CW = cell wall; ER = endoplasmic reticulum; FL = flagellum; FLC = flagellar channel; GB
= Golgi body; M = mitochondrion; N = nucleus; PA = apical papiUa; PS = pyrenoid stroma; SPL =
starch plate on pyrenoid; SS = stroma starch; ST = stigma; TET = tubular extension of thylakoid in
pyrenoid; TH = thylakoid; UTSC = upper transversely striated connective b e t w e e n the basal
bodies). (a Based on Ettl, 1976; b on Ringo, 1967)
e t al., 1980; H o f f m a n n , 1984; M e l k o n i a n , 1977, 1978, 1983; M o e s t r u p , 1978, 1982;
O ' K e l l y & Floyd, 1984).
(3) F l a g e l l a t e cells of t h e c r u c i a t e t y p e w i t h a n 11 o ' c l o c k / 5 o ' c l o c k c o n f i g u r a t i o n of
t h e f l a g e l l a r a p p a r a t u s (Figs 6, 7).
This t y p e is r a t h e r similar to t h e p r e v i o u s t y p e , a p a r t f r o m t h e 11 o ' c l o c k / 5 o ' c l o c k
C. v a n d e n Hoek, W. T. Stam & J. L. Olsen
348
UTSC
2-R
BA/c_/2~_RR
BAB
LTSC/
4-~
Fig. 5. Plagellar apparatus of a cruciate chlamydophycean and chlorophycean zoid-type with a 1
o'clock/7 o'clock configuration of the basal bodies: Chlamydomonas. a Spatial top view of the two
basal bodies (BAB) and the four microtubular roots; b Spatial side view of the two basal bodies
(BAB), the four microtubular roots, the upper transversely striated connective (UTSC) and the two
lower transversely striated connectives (LTSC) between the basal bodies. (4-R -- 4-stranded microtubular root; 2-R = 2-stranded microtubular root). (a Based on Mattox & Stewart, 1984; b original)
positions of the basal bodies a n d the overlap of the two basal bodies w i t h attached
microtubular roots. Other ultrastructural features of the flagellar a p p a r a t u s are also
considered characteristic of this type, although they vary a m o n g the orders h a v i n g this
type. Examples are the possession of a n u p p e r non-striated connective l i n k i n g the basal
bodies (sometimes it is striated), a n d the possession of terminal caps on the l o w e r ends of
the basal bodies. (A selection of references: Bakker & Lokhorst, 1985; Floyd & O'Kelly,
1984; Floyd et al., 1985; Gori, 1979; H i r a y a m a & Hori, 1984; Hoops et al., 1982; Hold,
1977; Hori & Kobara, 1982; J 6 n s s o n & Chesnoy, 1984; Lokhorst, 1984; M e l k o n i a n , 1979,
1980, 1981b; Miyaji & Hori, 1984; O'Kelly & Floyd, 1983; O'Kelly et al., 1984; Roberts et
al., 1980, 1981, 1982; Sluiman, 1985b; S l u i m a n et al., 1980b, 1982; Stuessy et al., 1983).
This flagellate cell type is characteristic of the class Ulvophyceae.
(4) Flagellate cells strongly compressed, of the cruciate type, with a n 11 o'clock/5
o'clock configuration of the flagellar apparatus, a n d with columnar structures associated
with the basal bodies.
This type has additional special features. It characterizes the class T r e n t e p o h h o p h y ceae. (A selection of references: C h a p m a n , 1981, 1984; C h a p m a n & Henk, 1983, 1985;
Graham, 1984; G r a h a m & McBride, 1975; Roberts, 1984).
(5) Flagellate cells of the unilateral type (Fig. 8).
The flagella are not apically, b u t laterally implanted. The flagella are a n c h o r e d i n the
cell by one broad unilateral b a n d of m a n y microtubules. Near the basal bodies this
A n e w chlorophytan system
ii
o'clock-5
o'clock
12 o'clock-fi
o'clock
1
349
o'clock-7
o'clock
configuration of
Configuration of
Configuration of
basal bodies
basal bodies
basal bodies
(tranSitlnnal ) ,
b-1
a-1
c-I
Fig. 6. Cruciate microtubular root systems of flagellar apparatuses in green algae (diagram). Top
view of basal bodies with two- and four-membered microtubular roots, a-t, b-l, c-1 in biflagellate
zoids; a-2, b-2, c-2 in quadriflagellate zoids, a-t: Hypothetical ancestral configuration, the basal
bodies take a 12 o'clock and 6 o'clock position, b-l: The basal bodies take a mutually slightly
overlapping, 11 o'clock and a 5 o'clock position, c-1: The basal bodies take a 1 o'clock and a, non
overlapping, 7 o'clock position (Based on O'Kelly & Floyd, 1984; Mattox & Stewart, 1984)
microtubular b a n d is incorporated in a multilayered structure (MLS). Apart from the
microtubular layer, two laminate layers compose the MLS (Moestrup 1974, 1982).
The unilateral zoid type is d e e m e d characteristic of the class C h a r o p h y c e a e a n d of
the mosses a n d vascular plants. (A selection of references: G r a h a m & McBride, 1979;
G r a h a m & Wedemeyer, 1984; M a r c h a n t et al., 1973; Moestrup, 1970, 1974, 1982; PickettHeaps, 1975; Rogers et al., 1980; Sluiman, 1983, 1985b).
A sixth type of flagellate reproductive cell has an 11 o'clock/5 o'clock configuration
of the flagellar apparatus (as in the Ulvophyceae). The strongly compressed cells have
the usual X-2-X-2 pattern of microtubular roots. The tips of the X-roots overlie a faintly
layered structure with some r e s e m b l a n c e to the MLS of the unilateral zoids. Possibly this
flagellate cell type characterizes another chlorophytan class, the Pleurastrophyceae.
(Selected references: Mattox & Stewart, 1984; M e l k o n i a n & Bems, 1983; Sluiman, 1985b;
Deason & Floyd, 1987).
Type of mitosis-cytokinesis
The processes of mitosis a n d cytokinesis are thought to provide evolutionary old
characters, as all eukaryotes n e e d these processes for a precise distribution of identical
C. v a n d e n H o e k , W . T. S t a m & J. L. O l s e n
350
2-R
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Fig. 7. T h e cruciate u l v o p h y c e a n zoid t y p e w i t h a n I 1 o'clock/5 o ' c l o c k c o n f i g u r a t i o n o f t h e two b a s a l
b o d i e s : t h e g a m e t e of Acrosiphonia. a T o p v i e w of flagellar a p p a r a t u s , b a s a l b o d i e s p i c t u r e d as
c y h n d e r s (diagram); b Idem, t h e lower p a r t s of t h e flagellar a p p a r a t u s are s h o w n t h r o u g h t h e
t r a n s p a r e n t b a s a l bodies; c Electron m i c r o s c o p i c a l side v i e w of t h e w h o l e g a m e t e ( d i a g r a m ) ; d side
v i e w of b a s a l b o d y s h o w i n g o n e of t h e two t r a n v e r s e l y striated fibres c o n n e c t i n g o n e of t h e two
t h r e e - s t r a n d e d m i c r o t u b u l a r roots with o n e of t h e two p r o x i m a l (lower) s h e a t h s (diagram); e
L o n g i t u d i n a l s e c t i o n t h r o u g h t h e apical papilla in t h e p l a n e p e r p e n d i c u l a r to t h a t of F i g u r e 7C. A P A
= apical papilla; A X = a x o n e m e ; BAB = b a s a l body; C H L = chloroplast; ER = e n d o p l a s m i c
r e t i c u l u m ; FL = f l a g e l l u m ; M = m i t o c h o n d r i o n ; M S = m a t i n g s t r u c t u r e ; N = n u c l e u s ; P = p y r e n o i d ;
PS = p r o x i m a l (= lower) s h e a t h ; 2-R = t w o - s t r a n d e d m i c r o t u b u l a r root; 3-R = t h r e e - s t r a n d e d
m i c r o b u t u l a r root; SF = tiny s e c o n d (striated) fibre c o n n e c t i n g b a s a l bodies; S M P S = s t r i a t e d
m a t e r i a l c o n n e c t i n g t h e two p r o x i m a l (lower) s h e a t h s ; ST = s t i g m a ; T C = t e r m i n a l c a p (partly
c l o s i n g t h e b a s a l e n d of t h e b a s a l body); T H = thylakoid; T M T = tail m i c r o t u b u l e ; T S F = o n e of two
t r a n s v e r s e l y s t r i a t e d fibres c o n n e c t i n g o n e of t h e two t h r e e - s t r a n d e d m i c r o t u b u l a r r o o t s w i t h o n e of
t h e p r o x i m a l s h e a t h s ; U N C = u p p e r n o n - s t r i a t e d c o n n e c t i v e b e t w e e n t h e b a s a l b o d i e s ; VES =
v e s i c l e s p r o b a b l y w i t h sticky m a t e r i a l for a t t a c h m e n t of zoid (Based o n Miyaji & Hori, 1984)
A new chlorophytan system
351
MBA
PM
SC
b~,L
Fig. 8. The unilateral charophycean zoid type with a broad lateral band of rnicrotubules and a MLS
(rnultilayered structure): the Chaetosphaeridium zoospore, a Longitudinal section; b transverse
section of the microtubular band of the flagellar apparatus. CHL = chloroplast; ER = endoplasrnic
reticulum; GB = Golgi body; M = mitochondrion; MB -- rnicrobody; MBA = rnicrotubular b a n d of
flagellar apparatus; N = nucleus; MLS --- rnultilayered structure; P --- pyrenoid; SC --- layer of organic
diamond scales; SPL = starch plate on pyrenoid; SS = stroma starch; TSF = transversely striated
fibre connecting basal bodies; V = vacuole (Based on Moestrup, 1974; van den Hoek, 1981)
g e n o m e s a n d sets of o r g a n e l l e s o v e r two d a u g h t e r cells d u r i n g n u c l e a r a n d c e l l u l a r
division.
At l e a s t e i g h t d i f f e r e n t t y p e s of m i t o s i s - c y t o k i n e s i s c a n b e d i s c e r n e d in t h e
C h l o r o p h y t a . O n l y the m o s t p r o m i n e n t f e a t u r e s will b e briefly m e n t i o n e d .
I. O p e n mitosis w i t h a p e r s i s t e n t t e l o p h a s e spindle; c y t o k i n e s i s b y a c l e a v a g e f u r r o w
of t h e p l a s m a m e m b r a n e . T h e t w o s p i n d l e p o l e s e a c h consist of a set of b a s a l b o d i e s w i t h
a r h i z o p l a s t (Fig. 9, top).
This t y p e is e x h i b i t e d b y t h e p r a s i n o p h y c e a n Pyramimonas. Nephroselmis, a
p r a s i n o p h y c e a n w i t h two u n i l a t e r a l l y i m p l a n t e d flagella, h a s a similar t y p e of mitosisc y t o k i n e s i s w h i c h is, h o w e v e r , c l o s e d (i.e. t h e n u c l e a r e n v e l o p e is l a r g e l y r e t a i n e d d u r i n g
mitosis) (Fig. 18, t y p e Ia) (Mattox & S t e w a r t , 1977; P e a r s o n & Norris, 1975; W o o d s &
T r i e m e r , 1981).
II. C l o s e d mitosis w i t h a n o n - p e r s i s t e n t t e l o p h a s e s p i n d l e (i.e. t h e s p i n d l e c o l l a p s e s
e a r l y at t e l o p h a s e so t h a t t h e d a u g h t e r n u c l e i a p p r o a c h o n e a n o t h e r closely); c y t o k i n e s i s
C. v a n d e n Hoek, W. T. Stam & J. L. Olsen
352
|
|
9
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Fig. 9. Mitosis-cytokinesis type I. Open mitosis with a persistent telophase spindle; cytokinesis by a
cleavage furrow (Pyramimonas). Mitosis-cytokinesis type II. Glosed mitosis with a non-persistent
telephase spindle; cytokinesis by a cleavage furrow in a phycoplast (Chlamydomonas). a Early
prophase; b Metaphase; c Late telophase; d Early interphase. Arrows indicate 90 ~ rotation of
dividing cell within parent cell wall. BAB = basal body; BABP = pair of basal bodies; C =
chromosone; CF = cleavage furrow; CHL = chloroplast; CW = cell wall; ER = endoplasmic
reticulum; GB = Golgi body; K = kinetochore; N = nucleus; NE = nuclear envelope; PHMT =
phycoplast microtubule; RH = rhizoplast (I based on Woods & Triemer, 1981; II based on Triemer &
Brown, 1974)
by a c l e a v a g e furrow of the plasma m e m b r a n e in a phycoplast (i.e. a plate of rnicrotubules
in the division plane). T h e two spindle poles each consist of a set of basal b o d i e s (Fig. 9,
bottom).
This type is e x h i b i t e d by C h l a m y d o p h y c e a e (Lembi, 1980; T r i e m e r & Brown, 1974;
Pickett-Heaps, 1975).
III. Closed mitosis with a non-persistent t e l o p h ase spindle; cytokinesis b y a cell plate
of smooth e n d o p l a s m i c reticulum (ER) vesicles, in a p h y c o p l a s t (Fig. 10, top).
A cell plate is a p l a t e of vesicles in the division p l a n e w h i c h c o a l e s c e to form the
transverse s e p t u m dividing the two d a u g h t e r cells. After completion of t h e transverse
s e p t u m the Golgi-bodies secrete a n e w cell wall a r o u n d e a c h d a u g h t e r protoplast (Fig.
10, top).
This is the type of mitosis-cytokinesis w h i c h is p r o b a b l y ex h i b i t ed by m a n y coccoid,
but also by sarcinoid a n d filamentous g r e e n al g ae (Sluiman, 1984, 1985a, b).
A new chlorophytan system
|
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CHL--
353
9
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-
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g.."
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I !1
Fig. 10. Mitosis-cytokinesis type III. Closed mitosis with a non-persistent spindle; cytokinesis by a
cell plate of smooth ER-vesicles in a phycoplast (Cylindrocapsa). Mitosis-cytokinesis type IV. Closed
mitosis with a non-persistent telophase spindle; cytokinesis by a cell plate of Golgi-derived vesicles
in a phycoplast (Uronema). a Early prophase; b Metaphase; c Late telophase; d Early interphase.
C = chromosome; CHL = chloroplast; CEP = pair of centrioles; CPGVES = cell plate of Golgiderived vesicles; CPSER = cell plate of smooth ER-vesicles; CW --- cell wall; CW1 = old cell wall;
CW2 --- young cell wall; ERR = rough endoplasmic reticulum; GB = Golgi body; GVES = Golgiderived vesicles; K - kinetochore; MB = microbody; MTLEF = microtubules along leading edge of
cleavage furrow of plasma m e m b r a n e ; NE = nuclear envelope; PD = plasmodesma; PER =
perinuclear endoplasmic reticulum; PHMT -- phycoplast microtubules; PHRM = phragmoplast
microtubule; PMT -- perinuclear microtubules; V = vacuole (III b a s e d on Sluiman, 1984, 1985a; IV
on Floyd et al., 1972b)
IV. C l o s e d m i t o s i s w i t h a n o n - p e r s i s t e n t t e l o p h a s e s p i n d l e ; c y t o k i n e s i s b y a cell p l a t e
of G o l g i - d e r i v e d v e s i c l e s i n a p h y c o p l a s t (Fig. 10, b o t t o m ) .
T h e G o l g i - d e r i v e d cell p l a t e v e s i c l e s c o n t a i n cell w a l l m a t e r i a l . C o a l e s c e n c e of t h e
v e s i c l e s r e s u l t s i n t h e f o r m a t i o n of t h e t r a n s v e r s e cell w a l l w h i c h r e m a i n s t r a v e r s e d b y
p l a s m o d e s m a t a b e t w e e n t h e d a u g h t e r ceils.
C e r t a i n f i l a m e n t o u s r e p r e s e n t a t i v e s of t h e class C h l o r o p h y c e a e h a v e t h i s t y p e of
m i t o s i s - c y t o k i n e s i s (Floyd e t al., 1972a; M a t t o x e t al., 1974; M c B r i d e , 1967, 1970; P i c k e t t H e a p s , 1975).
V. C l o s e d m i t o s i s w i t h a p e r s i s t e n t t e l o p h a s e s p i n d l e ; c y t o k i n e s i s b y a c I e a v a g e
f u r r o w of t h e p l a s m a m e m b r a n e to w h i c h G o l g i - d e r i v e d v e s i c l e s a r e a d d e d (Fig. 11, top).
T h e n e w cross w a l l is n o t t r a v e r s e d b y p l a s m o d e s m a t a . N e i t h e r a p r o n o u n c e d p h y c o p l a s t
( T y p e s III, IV) n o r a p r o n o u n c e d p h r a g m o p l a s t ( T y p e VIII) a r e i n v o l v e d i n c y t o k i n e s i s .
T h i s t y p e of m i t o s i s - c y t o k i n e s i s is e n c o u n t e r e d i n f i l a m e n t o u s t h a l l o s e a n d s o m e
C. v a n d e n Hoek, W. T. Stam & J. L. Olsen
354
|
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Pig. 11. Mitosis-cytokinesis type V. Closed mitosis with a persistent telophase spindle; cytokinesis by
a cleavage furrow to which Golgi-derived vesicles are added (U/othr/x). Mitosis-cytokinesis type VI.
Closed mitosis with a prominent persistent telophase spindle, causing a typical dumb-beU shape;
cytokinesis does not immediately follow mitosis (Valonia). Fbr abbreviations, see text to Figure 10
(V based on Sluiman et al., 1983; VI on Hori & Enomoto, 1978b)
siphonocladous U l v o p h y c e a e (Hudson & W a a l a n d , 1974; Lokhorst, 1984, 1985; Lokhorst
& Star, 1983; Levhe & Br&ten, 1968, 1970; M c A r t h u r & Moss, 1978; S l u i m a n et al., 1983).
VI. Closed mitosis with a p r o m i n e n t p e r s i s t e n t t e l o p h a s e spindle g i v i n g the t e l o p h a s e
nucleus a typical d u m b b e l l - s h a p e ; cytokinesis does not i m m e d i a t e l y follow mitosis {Pig,
11, bottom).
This t y p e is characteristic of most siphonocladous, a n d of s i p h o n o u s U l v o p h y c e a e
(Burr & West, 1970; Hori, 1981; Hori & Enomoto, 1978a, 1978b; L i d d l e et al., 1976;
M c D o n a l d & Pickett-Heaps, 1976; Scott & Bullock, 1976).
VII. O p e n mitosis with a p r o m i n e n t persistent telophase spindle; c y t o k i n e s i s b y a
c l e a v a g e furrow of the p l a s m a m e m b r a n e . The cross wall is not t r a v e r s e d b y p l a s m o d e s m a t a (Fig. 12, top).
This t y p e of mitosis-cytokinesis is characteristic of the simplest r e p r e s e n t a t i v e s of the
class C h a r o p h y c e a e (ChappeI1 & Floyd, 1981; Floyd et al,, 1972b; L o k h o r s t & Star, 1985;
Lokhorst, 1987; Pickett-Heaps, 1972, 1974, 1975, 1976).
VIII. Open mitosis with a p r o m i n e n t persistent t e l o p h a s e spindle; c y t o k i n e s i s b y a
cell plate of G o l g i - d e r i v e d vesicles in a p h r a g m o p l a s t . A p h r a g m o p l a s t is t h e c o m p l e x of
old spindle microtubules plus n e w p e r i p h e r a l l y a d d e d microtubules t h a t a r e p a r a l l e l to
the spindle (Pig. 12, bottom).
A n e w chlorophytan system
|
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.
355
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Fig. 12. Mitosis-cytokinesis type VII. Open mitosis with a prominent persistent telophase spindle;
cytokinesis by a cleavage furrow (Klebsormidium). Mitosis-cytokinesis type VIII. Open mitosis with
a prominent persistent telophase spindle; cytokinesis by a cell plate of Golgi-derived vesicles in a
phragmoplast. For abbreviations, see text to Figure 10 (VII based,on Lokhorst & Star, 1985; VIII on
Marchant & Pickett-Heaps, 1973)
The G o l g i - d e r i v e d vesicles contain cell wall material a n d are a r r a n g e d in a cell plate,
"guided" by the p h r a g m o p l a s t . Their c o a l e s c e n c e results in the formation of the cross
wall which r e m a i n s t r a v e r s e d b y p l a s m o d e s m a t a .
This type of mitosis-cytokinesis is characteristic of the more sophisticated r e p r e s e n tatives of the class C h a r o p h y c e a e , of the mosses a n d vascular plants, a n d of the
T r e n t e p o h l i o p h y c e a e ( C h a p m a n & Good, 1978; C h a p m a n & H e n k , 1986; M a r c h a n t &
Pickett-Heaps, 1973; Pickett-Heaps, 1975).
Place of meiosis in the life history and, consequently, the sexual life history type
Meiosis is t h o u g h t to have arisen in the early history of the p r i m a e v a l eukaryotes. In
its ultrastructural details (e.g. the s y n a p t o n e m a l complexes), meiosis is similar in very
d i v e r g e n t eukaryotes. Therefore, the p l a c e of meiosis a n d the r e l a t e d sexual life history
are thought to potentially provide conservative characters. A c c o r d i n g to this reasoning,
sexual r e p r o d u c t i o n has arisen only once in e u k a r y o t a n evolution, b u t it has b e e n
secondarily lost in the n u m e r o u s e u k a r y o t e s l a c k i n g sexual reproduction.
Our k n o w l e d g e on life histories is still deficient for m a n y g r e e n algal groups,
expecially with r e g a r d to the ploidy levels of the different hfe history s t a g e s a n d the
position of meiosis. On the basis of the e v i d e n c e a v a i l a b l e it w o u l d s e e m that the majority
of g r e e n algal groups h a v e an haplontic hfe history with only the zygote nucleus b e i n g
C. v a n d e n Hoek, W. T. Stam & J. L. Olsen
356
diploid. Only in the fresh-water classes Chlamydophyceae, C h l o r o p h y c e a e a n d
C h a r o p h y c e a e are the zygote nuclei e n c a s e d in hypnozygotes. These are p r o b a b l y a n
adaptation to life in freshwater, a n d serve for. survival after desiccation of w a t e r bodies or
during transport from one freshwater body to the other. The geologically e p h e m e r a l
n a t u r e of freshwater bodies in comparison to the world ocean should b e recalled.
f
c
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c'
Fig. 13, Chlorocystis cohnfi (Ulvophyceae, Codiolales), life history, a,a i Gametophyte; b,b 1 the cell
contents have divided into quadriflagellate asexual spores; c,c 1 the cell contents have divided into
biflagellate anisogametes; d,d i asexual quadriflagellate zoopores; e germling; f male gametes; fi
female gametes; g copulation; h planozygote; i young zygote; j full-grown, stalked, Codiolum-like
zygote; k,k i quadriflagellate zoospores, presumably meiospores; 1gelatinous matrix of tube forming
diatom (m), CHL = chloroplast, P = pyrenoid. (Based on Kornmann & Sahhng, 1983)
The (presumablY) haplontic life history of the order Codiolales (class Ulvophyceae)
with a Codiolum-hke zygote stage is highly characteristic of this order (Figs 13, 14). Dr.
K o r n m a n n has reiterated the phylogenetic importance of this character. His proposal
(Kornmann 1963, 1973) to regard the g r e e n algae with this type of hfe history as a taxon of
high hierarchical level (order, class) was only rarely followed b e c a u s e the o r g a n i z a t i o n a l
levels contained in this taxon are very divergent a n d r a n g e from coccoid unicellular to
b r a n c h e d siphonocladous a n d e v e n thallose. Recent ultrastructural studies on the reproductive flagellate cells (Floyd & O'Kelly, 1984; J6nsson & Chesnoy, 1984; Miyaji & Hori,
1984; S l u i m a n et al., 1980b, 1982) a n d the processes of mitosis a n d cytokinesis (Hudson &
A n e w chlorophytan system
357
Fig. 14. Ulothrix zonata (Ulvophyceae, Codiolales), life history, a,a 1 Gametophyte; b,b 1 the cell
contents have divided into quadriflagellate asexual zoospores; c,c 1 the cell contents have divided
into biflagellate isogametes; d,d ~ asexual quadriflagellate zoospores; e,e 1 germlings; f,fl,g copulation of isogametes; h planozygote; i,j young zygote; k,1 older, Codiolum-like zygote; m,m 1 quadriflagellate zoospores, presumably raeiospores (Based on Lokhorst & Vroman, 1972)
W a a l a n d , 1974; Lokhorst, 1984, 1985; Lokhorst & Star, 1983; Sluiman et al., 1983) h a v e
confirmed the validity of Dr. Kornmann's proposal. T h e orders D a s y c l a d a l e s a n d Bryopsidales h a v e long b e e n considered as b e i n g f u n d a m e n t a l l y diplontic a n d as h a v i n g g a m e t i c
meiosis. At present, the early karyological e v i d e n c e is q u e s t i o n e d (Tanner, 1981; v a n d e n
Hoek, 1981). Recent studies (Koop, 1975, 1979; Spring et al., 1978; Kloppstech, 1982;
S h i h i r a - I s h i k a w a & Kuroiwa, 1984; Liddle et al., 1976) h a v e p r o d u c e d e v i d e n c e t h a t only
the g i a n t zygote nucleus in the D a s y c l a d a l e a n life history is diploid (Fig. 15). This diploid
nucleus is c o n t a i n e d in a young, at first spherical, stage. Later on, the a d u l t plant
d e v e l o p s from this y o u n g stage, a n d it receives n u m e r o u s haploid nuclei after v e g e t a t i v e
meiosis of the giant zygote nucleus,
The life histories in the r e l a t e d order Bryopsidales s e e m to be rather similar for they
include y o u n g zygote stages with giant zygote nuclei, for instance in U d o t e a (Meinesz,
C. v a n d e n Hoek, W. T. Stare & J. L. Olsen
358
k'~ .,,~/
k
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. (~.
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l
c
d
e
f
Fig. 15. Acetabularia acetabulum (Ulvophyceae, DasycladaCles), life history, a Young zygote with
diploid zygote nucleus; b older zygote with growing diploid zygote nucleus; c young erect plant with
diploid zygote nucleus in rhizoidal portion of plant; d,e development of whorls of sterile hairs on
plant with diploid giant nucleus; f after meiosis of the giant nucleus the haploid daughter nuclei
have formed, by successive mitoses, numerous tiny haploid nuclei which are transported to other
parts of the plant by protoplasmic streaming; an umbrella-hke whorl of gametangia has been formed
on the tip of the stalk; g the umbrella-like whorl of gametangia, each gametangium filled with
numerous gametangial cysts; h,h 1 two cysts, each with one haploid nucleus; j,jl the cysts have
produced biflagellate isogametes of opposite sex; 1,m isogamy. GC = gametangial cyst; GN2n =
giant nucleus, diploid; MHN(n) = migrating haploid (n) nuclei; R] = reduction division; WH = whorl
of hairs; WHS = whorl of hairscars; U = umbrella-like whorl of gametangia
1969, 1972b, 1980) (Fig. 16), Halimeda (Meinesz, 1972a, 1980), Caulerpa (Price, 1972;
Enomoto & Ohba, 1987), Bryopsis (Rietema, 1969, 1970, 1971, 1975; N e u m a n n , 1969a).
Karyological e v i d e n c e is, however, lacking or u n c o n v i n c i n g .
In t h e life history of Derbesia (Fig. 17) a spherical g a m e t o p h y t e stage a l t e r n a t e s with
a b r a n c h e d sporophyte stage. This life history was discovered 50 y e a r s ago b y Dr.
K o r n m a n n (Kornmann, 1938). Meiosis was later i n d u b i t a b l y d e m o n s t r a t e d in the pearshaped sporangia of Derbesia ( N e u m a n n , 1969b; Rietema, 1972, 1975). E c k h a r d t et al.
(1986; see also Eckhardt & Schnetter, 1984; Schnetter et al., 1985) d i s c o v e r e d that
gametic fusion results i n the growth of a n haploid, dikaryotic sporophyte. O n l y i n the tips
of the p e a r - s h a p e d meiosporangia do the nuclei fuse to form the large zygote nuclei.
These zygote nuclei are apparently the only diploid nuclei in this life history.
A new chlorophytan system
359
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i
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Fig. 16. Udotea petiolata (Ulvophyceae, Bryopsidales), life history, a,a ~ Gametophyte; b,b i exit
papillae of gametes along margins of holocarpic thallus; c biflagellate male gamete; c I biflagellate
female gamete; d anisogamy; e young zygote; f-h development of young zygote into full-grown
spherical zygote (protosphere) with giant nucleus (GN); i after nuclear division the protosphere buds
off an erect and a rampant siphon; k,k I development of dichotomously branching plants from the
protosphere; I,li initiationof fan-like fronds from special swollen primordia on stolons grown from
protosphere (Based on Meinesz, 1980)
Haplodiplontic life histories seem to have evolved at least four times in the
Chlorophyta; namely in the orders Ulvales and Cladophorales of the class Ulvophyceae
(see Tanner, 1981; van den Hoek, 1981), presumably in the class Trentepohliophyceae
(Chapman, 1984} and in the mosses and vascular plants {the charophycean lineage}.
360
C. v a n d e n Hoek, W. T. Stain & J. L. Olsen
.......
\
Fig, 17. Derbesia marina (Ulvophyceae, Bryopsidales), life history, a Male gametophyte; b female
gametophyte ("Halicystis stage" ); c male gametes; d female gametes; e anisogamy; f heterokaryotic
(dikaryotic), haploid product of cytogamy; g sporophyte ("Derbesia stage"); h heterokaryotic
sporophyte, detail with young sporangium, karyogamy between male {open) and female {filled)
nuclei in apical portion of young sporangium; j heterokaryotic, haploid sporophyte, detail with
young sporangium, diploid zygote nuclei in apical portion of sporangium just before meiosis; k
heterokaryotic sporophyte, detail with full-grown sporangium after meiosis, note that half of the
young meiospores contain male {open) nuclei, the other half female (filled) nuclei, note also the basal
plug separating the sporangium from the vegetative thallus; 1,n stephanokontan meiospores with
male (open) nuclei; m,o stephanokontan meiospores with female (filled) nuclei (Based on Kornmann,
1938; Eckhardt et al., 1986)
Organizational level and thallus architecture
Each of the three classes Ulvophyceae, Chlorophyceae a n d C h a r o p h y c e a e contains
one order with widely divergent organizational levels, n a m e l y the Codiolales, Cylindrocapsales, a n d Klebsormidiales, respectively (Table 2).
A new chlorophytan system
361
Most orders have only one organizational level, and this often exhibits features that
are unique to the order (or sometimes class). Examples are the Dasycladales, Oedogoniales, Zygnematophyceae, Charales. These are traditionally uncontroversial groups.
Habitat type
Habitat type is here considered characteristic at the class level. Some hneages have
evolved in the sea, others in freshwater, and still others on the land (probably from
freshwater ancestors). There are a few exceptions in several groups. For instance, within
the Ulvophyceae several species of U/othr/x (Codiolales) and Cladophora (Cladophorales) are restricted to freshwater. The reverse (occurrence of species of freshwater classes
in the sea) is quite rare, although penetration into brackish water does occur (e.g. by
Charales, Zygnematophyceae).
IMPLICATIONS OF THE NEW SYSTEM AND ITS UNDERLYING HYPOTHESES
Figure 18 summarizes the new system and the underlying hypotheses. Note that the
phyiogenetic tree no longer reflects the idea of a step-wise evolutionary progression of
organizational levels in which the flagellate level represents the most primitive lineage,
the coccoid and sarcinoid levels lineages of intermediate derivation, and the filamentous,
siphonocladous and siphonous levels the most derived lineages (Fig. 1).
Only the traditional hypothesis that the flagellate organizational level is primitive,
has b e e n retained in the new phylogenetic scenario. In this scenario, the various
organizational levels have been realized over and over ~gain within the main lineages
(classes). For instance, unbranched U/othr/x-like filaments occur in the Ulvophyceae
(Ulothrix, order Codiolales), the Chlorophyceae (Uronema, order Chaetophorales) and
the Charophyceae (Klebsormidium, order Klebsormidiales). The phylogenetic
heterogeneity of Ulothrix-like filaments has recently been confirmed by Schl6sser's
(1987) discovery that Uronerna-autolysins are also effective in other filamentous genera
of the order Chaetophorales, class Chlorophyceae (Stigeocloniurn, Draparnaldia,
Chaetophora), but not in Ulothrix (Ulvophyceae) and Klebsormidium (Charophyceae).
Autolysins bring about the dissolution of filaments into cells, or the opening of exit pores
through enzymatic degradation of cell wall polysaccharides.
Coccoid representatives are known in the Chlamydophyceae (e.g. Chlorococcum),
Ulvophyceae (Chlorocystis, order Codiolales), the Chlorophyceae (e.g. Golentdnia, order
Cylindrocapsales) and the Charophyceae (e.g. Raphidonema, order Klebsormidiales).
Sarcinoid genera occur in the Chlorophyceae (e.g. Chlorosarcinopsis, order Cyhndrocapsales), in the putative class Pleurastrophyceae (Friedmannia, cf. Melkonian & Berns,
1983) and in the Charophyeae (Chlorokybus, order Klebsormidiales).
Each of the three classes Ulvophyceae, Chlorophyceae and Charophyceae contains
one order with considerable diversity in the organizational levels, namely the orders
Codiolales, Cylindrocapsales, and Klebsormidiales, respectively. Each of these three
orders can possibly be interpreted as being relatively primitive within its own class, as it
contains some representatives which have retained a primitive, ancestral coccoid or
sarcinoid organization. Even these within-class coccoid and sarcinoid forms are probably
C. v a n d e n H o e k , W. T. S t a m & J. L. O l s e n
362
CODIO-:ULVA-:CLADO-:BRYOP[ALES :LES :PHORA-:SIDA!
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Fig. 18. Phylogeny a n d subdivision of Chlorophyta in the present treatise. 1 Nephrosolmis (the scaly
covering is indicated); 2 P~amimonas (note the scaly covering); 3 Tetraselmis (note the theca
around the cell); 4 ChIorococcum; 5 Eudofina; 6 Chlamydomonas (note the cell wall); 7 Chlorocystis;
8 Ulothfix; 9 Urospora; I0 Acrosiphonia; 11 Monostroma; 12 Acrochaete; 13 UIwa;14 Cladophora; 15
Udotea; 16 Acetabularia; 17 Sphaeroplea; 18 RadJofflum; 19 Chlorosarcinopsis; 20 Scenedesmus; 21
Golenkim'a; 22 Stigeoclonium; 23 Schizomeris; 24 Oedogonium; 25 Uronema; 26 Spirogyra; 27
Cosmarium; 28 Trentepohlia; 29, 30 Igebsormidium; 31 Chlorokybus; 32 Raphidonema; 33 Coleochaete; 34 Chara. Life history types: ? unknown, H! haplontic, karyological evidence available; H?
presumably haplontic, no karyological evidence; HD! haplodidplontic, karyological e v i d e n c e available; HD? presumably haplodiplontic, no karyological evidence available. T y p e of mitosiscytokinesis {see also Pigs 9-12). I. O p e n mitosis with a persistent telophase spindle, cytokinesis by a
cleavage furrow. Ia. Closed mitosis with a persistent telophase spindle, cytokinesis b y a cleavage
furrow. II. Closed mitosis with a non-persistent telophase spindle, cytokinesis by a c l e a v a g e furrow
in a phycoplast III. Closed mitosis with a non-persistent telophase spindle, cytokinesis b y a cell plate
363
A new chlorophytan system
:K LEBSOR-ICOLEO-:CHABA-:
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of smooth ER vesicles in a phycoplast. IV. Closed mitosis with a non-persistent telophase spindle,
cytakinesis by a cell plate of Golgi-derived vesicles in a phycoplast V. Closed mitosis with a
persistent telophase spindle; cytokinesis b y a cleavage furrow to which Golgi-derived vesicles are
added. VI. Closed mitosis with a p r o m i n e n t persistent telophase spindle giving the telophse nucleus
a typical dumbbell shape, cytokinesis does not immediately follow mitosis. VII. Open mitosis with a
prominent persistent telophase spindle, cytokinesis by a cleavage furrow. VIII. Open mitosis with a
prominent persistent telophase spindle, cytokinesis by a cell plate of Golgi-derived vesicles in a
phragmoplast. The pictures of the cruciate zoids in the Ulvophyceae and Trentepohliophyceae
contain a top view of the 11 o'clock/5 o'clock configuration of the basal bodies; the pictures of the
zoids in the Chlorophyceae and Chlamydophyceae contain a top view of the 1 o'clock/7 o'clock
configuration of the basal bodies. Note the scaly coverings of zoids in the Prasinophyceae, Ulvophyceae (Codiolales), and Charophyceae. Note also the hypothetical uniflagellate scaly prasinophycean ancestor (bottom left). The present day species Mantoniella squamata is the model of this
ancestor (Manton & Parke, 1960; Ettl, 1983)
364
C. van d e n Hoek, W. T. Stam & J. L. Olsen
p a r a p h y l e t i c as t h e y v a r y in cell structure, more particularly in chloroplast structure
(Groover & Bold, 1969; Kom~rek & Fott, 1983).
The coccoid "genus" Chlorefla a n d e v e n p h e n o t y p i c "species" a p p e a r e d to b e
genetically highly h e t e r o g e n e o u s (Kessler, 1984; Huss et al., 1986, 1987a, 1987b) a n d this
supports the a b o v e i d e a that coccoid forms, e v e n within one order, m a y b e p a r a p h y l e t i c ,
or e v e n c o n v e r g e n t if coccoid forms w e r e the result of reduction from m u l t i c e l l u l a r forms.
T h e order Ulvales (class Ulvophyceae) contains b r a n c h e d filamentous a n d thallose
architectures.
The r e m a i n i n g orders within the a b o v e three classes h a v e e a c h virtually one
o r g a n i z a t i o n a l level. Most of t h e s e r e m a i n i n g orders h a v e m a n y u n i q u e f e a t u r e s which
define t h e m as internally consistent (e.g. Cladophorales, Dasycladales, O e d o g o n i a l e s ,
Charales). This latter r e m a r k is also valid for the classes Z y g n e m a t o p h y c e a e and
Trentepohliophyceae.
Basic to the n e w system is the hypothesis that e a c h m a i n evolutionary l i n e a g e (as a
class) is d e f i n e d b y its own t y p e of flagellate cell. Thus the U l v o p h y c e a e h a v e cruciate
r e p r o d u c t i v e zoids with 11 o'clock/5 o'clock positions of the b a s a l bodies; t h e C h l o r o p h y c e a e h a v e cruciate r e p r o d u c t i v e zoids with 1 o'clock/7 o'clock positions of the b a s a l
bodies; a n d the C h a r o p h y c e a e h a v e u n i l a t e r a l r e p r o d u c t i v e zoids with a MLS. Note that
the b r y o p h y t e s a n d t r a c h e o p h y t e s in this scenario b e l o n g to the C h a r o p h y c e a e as they
h a v e unilateral zoids a n d a c h a r o p h y c e a n mitosis-cytokinesis: To a c c o m m o d a t e the
e n o r m o u s diversity in the l a n d plants one n e e d s at least classes (e.g. Coniferopsida) or
e v e n divisions (e.g. Coniferophyta) for their m a i n groups. W e h a v e here r e f r a i n e d from an
a t t e m p t to devise a unified taxonomic h i e r a r c h y for the g r e e n a l g a e a n d t h e m o s s e s a n d
vascular plants. This w o u l d b e p e r h a p s d e s i r a b l e from a theoretical, b u t not from a
practical point of view.
Zoids are thought to b e the depositories of evolutionarily old characters, b e c a u s e
flagellate cells with their e u k a r y o t a n "9+2" flagella occur in w i d e l y different organisms.
The implication of this i d e a is that free living flagellates of one major g r o u p such as the
C h l o r o p h y t a are m o r e primitive (i.e. h a v e p r e s e r v e d more ancestral characters) t h a n their
non-flagellate r e p r e s e n t a t i v e s a n d that all non-flagellate r e p r e s e n t a t i v e s h a v e u l t i m a t e l y
evolved f r o m flagellate ancestors. F l a g e l l a t e forms h a v e often b e e n r a n g e d in one m a i n
group (e.g. the Volvocales in the Chlorophyta) which w a s c o n s i d e r e d a n c e s t r a l to all
other groups.
With r e g a r d to the flagellate chlorophytes, however, the i d e a g r a d u a l l y g a i n e d support
that there is, a p a r t from the Volvocales, at least one other m a i n l i n e a g e of c h t o r o p h y t a n
flagellates. This l i n e a g e is n o w g e n e r a l l y d e s i g n a t e d as the class P r a s i n o p h y c e a e which
is, as w e h a v e seen, c h a r a c t e r i z e d b y its h i g h l y e l a b o r a t e organic b o d y a n d flagellar
scales (cf. Norris, 1980), On the basis of various a r g u m e n t s the P r a s i n o p h y c e a e are
g e n e r a l l y r e g a r d e d as the most primitive group of the C h l o r o p h y t a (see Norris, 1980).
O n e a r g u m e n t is that the architectural diversity of this group d e s i g n a t e s it as a l a b o r a t o r y
for the evolution of the different g r e e n flagellate cell forms. This diversity of f l a g e l l a t e cell
architecture in the P r a s i n o p h y c e a e is s c h e m a t i c a l l y illustrated in F i g u r e 18. N o t e that the
h y p o t h e t i c a l ancestral p r a s i n o p h y c e a n (for which the p r e s e n t - d a y Mantoniella serves as
an e x a m p l e ) is scaly a n d uniflagellate. The i d e a is that biflagellate, q u a d r i f l a g e l l a t e a n d
even octoflagellate P r a s i n o p h y c e a e evolved e v e n t u a l l y from a uniflagellate a n c e s t o r b y a
shift in the timing of cytokinesis relative to the semi-conservative b a s a l b o d y (and h e n c e
A new chlorophytan system
365
flageUar) replication (cf. Norris, 1980; Melkonian et al., 1987; Melkonian, pers. comm.). A
recent argument for the primitiveness of the Prasinophyceae is that the main character of
this class, the possession of body scales, is shared with the reproductive zoids in widely
divergent chlorophytes (Fig. 18). The possession of this ancestral trait is thought to have
been conserved in several very remote multiceUular chlorophytes and to point to an
ancient divergence of these groups. In a comparable way, the possession of the 9+2
flagellum by unrelated eukaryotes as mammals, chytrids and chlorophytes is thought to
point to an exceedingly ancient evolutionary divergence in the primaeval eukaryotes.
This comparison also indicates the problematic nature of the characterization of the
Prasinophyceae by an admittedly primitive, ancestral trait which can be identified as
such because of its occurrence in other widely different classes. Actually, even though an
ancestral trait such as the possession of organic body and flagellar scales is conserved in
only a portion of the lineages contained in the Chlorophyta, it can only be used to
characterize the Chlorophyta as a whole. In a similar way, the possession of "9+2"
flagella can only characterize (almost) the whole realm of the eukaryotes, although some
lineages have secondarily lost these flagella (in the chlorophytes, a.o., the Zygnematophyceae and most vascular plants, see Fig. 18).
The above reflections apparently undermine the concept of the class Prasinophyceae
as proposed at the beginning of this paper. For further, different reasons, the phylogenetic scenario of the chlorophytes in Figure 18 is incompatible with the concept of the
Prasinophyceae.
The cruciate reproductive zoids of the Ulvophyceae plus Chlorophyceae are thought
to have evolved from a free hving scaly prasinophycean ancestor (Hoops et al., 1982;
Stewart & Mattox, 1978). Tetraselmis has been suggested as the nearest hving relative of
this ancestor (Moestrup, 1982; Sluiman et al., 1980a; Ste~vart & Mattox, 1975).
The present scenario specifies this idea as follows. In the ancient epoch of divergence
and radiation in the early flagellate chlorophytes, one Chlamydomonas-hke chlorophyte
possibly emerged which still had a scaly covering and 12 o'clock/6 o'clock positions of the
basal bodies. This was the common ancestor of the Chlamydophyceae, and of the
multicellular and siphonous green algae with cruciate reproductive zoids. In this latter
assemblage, an early divergence took place between the multiceilular greens whose
cruciate reproductive zoids evolved 11 o'clock/5 o'clock positions of the basal bodies (the
Ulvophyceae); and the multicellular greens with reproductive cells having 1 o'clock/7
o'clock positions of the basal bodies. This latter configuration does not differ much from
the hypothetical 12 o'clock/6 o'clock ancestral configuration.
The unilateral reproductive zoid of the Charophyceae, in its turn, might be thought to
have evolved from a free-living unilateral prasinophycean ancestor. Nephroselmis has
b e e n suggested as the nearest living relative of this ancestor (Moestrup & Ettl, 1979).
Nephroselmis does superficially resemble the unilateral charophycean zoid, with which it
shares a broad lateral microtubular root, the possession of a MLS-hke structure, and a
scaly covering (Fig. 8). The implication of the above two hypotheses is that Tetraselmis
would be more closely related to the Chlamydophyceae, Chlorophyceae and the
Ulvophyceae than to the remaining Prasinophyceae, and that Nephroselmis would be
more closely related to the Charophyceae than to the remaining Prasinophyceae.
A scenario in which the cruciate reproductive zoid is derived from a Tetraselmis-like
ancestor, and the unilateral reproductive zoid from a Nephroselmis-hke ancestor, also
366
C. van den Hoek, W. T. Stam & J. L. Olsen
implies that these two free living chlorophytan flagellates have survived almost unchanged
since the early radiation of non-flagellate chlorophytes. This accords with the basic
hypothesis that flagellate cells are phermtypically conservative. A consequence of this basic
hypothesis is therefore that the Prasinophyceae are a conglomerate of very old lineages
(classes) which have retained the ancestral trait of the organic body and flagellar scales. The
high diversity in flagellate cell architecture (e.g. in Ettl, 1983, Table I, p. 97), in flagellar root
systems (Melkonian, 1984; Moestrup, 1982, 1987; Norris, 1980), and types of mitosiscytokinesis (Baflow & Cattohco, 1981; Mattox & Stewart, 1977; Norris, 1980; Pearson &
Norris, 1975; Stewart et al., I974; Woods & Triemer, 198I) which are encountered in the
Prasinophyceae underline the heterogeneity of the "class" (see Fig. 18).
It would perhaps now be theoretically preferable to place each Prasinophycean
genus in its own class, but this would result in an unwieldy system which would in
practice hamper the discussions. We would also hesitate to place Tetraselmis and
Nephroselmis in other classes than the Prasinophyceae, as the homologies justifying such
decisions are of a highly tentative nature. For instance, the MLS-like structure in
Nephroselmis differs in details from that in the Charophyceae (Moestrup & Ettl, 1979)
and there are wide differences between Tetraselmis and Chlamydomonas.
Only limited ultrastructural information is available about the genera ranged here
under the Chlamydophyceae (Ettl & Moestrup, 1980). This information suggests that the
class is characterized by a cruciate 1 o'clock/7 o'clock configuration of the flagellar
apparatus and by a closed mitosis with a non-persistent telophase spindle and by a
glycoprotein lattice in the cell wall (Table 2; Fig. 9, bottom); cytokinesis is by a cleavage
furrow in a phycoplast.
The class harbours architecturally very diverse (especially with regard to chloroplast
structure) cruciate flagellates whose ultrastructure is largely unknown (see Ettl, 1983,
Table Ill on p. 194). This high diversity suggests that the Chlamydophyceae also consist
of a bundle of old lineages (classes), as flagellates are hypothesized to be phenotypically
conservative and therefore to change slowly.
In most recently proposed phylogenies (Deason, 1984; Hoops et al., 1982; Mattox &
Stewart, 1984; Melkonian, 1982; O'Kelly & Floyd, 1984; Sluiman, 1985b; Sluiman et al.,
1980a) the Chlamydophyceae (proposed by Ettl, 1981, and here adopted in a slightly
different sense) are included in the Chlorophyceae because of the similarity in flagellate
cell architecture. This is, however, not consistent with the basic hypothesis that flagellates are primitive with regard to multicellular and siphonous algae. In these phylogenies, the ulvophycean type of cruciate zoid (with an 11 o'clock/5 o'clock configuration of the basal bodies; Figs 6, 7) is generally considered more primitive than the
chlorophycean type of cruciate zoid (with a 1 o'clock/7 o'clock configuration, Figs 5, 6).
One important reason is that many ulvophycean zoids are covered by organic body scales
which resemble the underlayer body scales of the Prasinophyceae (Hoops et al., 1982;
Mattox & Stewart, 1984; O'Kelly & Floyd, 1983; Sluiman, 1985b). The chlorophycean type
of zoid is thought to have evolved from the ulvophycean zoid type by a gradual clockwise
shift of the basal bodies (cf. Fig. 6) and by the loss of organic body scales. One illogical
consequence of this reasoning is that a group of free-living flagellates-Chlamydomonas
and its allies - is considered as derived from a group of multicellular and siphonous green
algae. This clearly contradicts the basic hypothesis that free-living flagellate green algae
are primitive with regard to the non-flagellate greens.
A new chlorophytan system
367
The flagellate ,,classes" Prasinophyceae and Chlamydophyceae are probably bundles of ancient, conservative lineages each of which could be theoretically considered as a
separate class. A comparable reasoning could, be apphed to the putatively primitive
orders Codiolales (class Ulvophyceae), Cylindrocapsales (class Chlorophyceae), and
Klebsormidiales (class Charophyceae). These orders contain, by definition, relatively
conservative genera and could hence be considered as bundles of evolutionarily old
lineages (e.g. orders).
We have argued above that the primitive, ancestral, phenotypically conservative
chlorophytan hneages within Prasinophyceae and Chlamydophyceae in our phylogenetic hypothesis are very ancient lineages.
In contrast, the most derived phenotypically highly differentiated chlorophytan
hneages, for instance those in flowering plants, should be, according to our hypotheses,
very young and the product of rapid phenotypic change. Lineages of intermediate
derivation, for instance the classes of the Ulvophyceae, Chlorophyceae and Charophyceae should have an intermediate age. Within the most ancient and conservative
lineages, extant genera and species can also be expected to be phenotypically conservative and hence to be "old". Within the youngest phenotypically most derived lineages, on
the other hand, the genera and species can be also expected to be phenotypically derived
and hence to be "young".
Our phylogenetic scenario therefore predicts that the extant phenotypically defined
genera and species in ancestral conservative lineages have, on average, diverged
relatively long ago because phenotypic change is here a slow process; and that phenotypically defined genera and species in derived lineages have diverged, on average,
much more recently because phenotypic change is here a rapid process.
This prediction can be tested by two approaches; firsf by inspecting the fossil record;
second by estimating relative divergence times on the basis of comparisons between
macromolecules bearing genetic information.
Fossil e v i d e n c e
Figure 19 summarizes the available fossil evidence about the geologic occurrence of
chlorophytan taxa. Uninterrupted lines indicate more or less solid evidence, interrupted
lines more or less speculative identifications. Actually, only for the geologic occurrence of
the Prasinophyceae, the Bryopsidales, the Dasycladales and the Charales is abundant
and rehable evidence available. The occurrence of vascular plants is well documented
from ca 400 million years ago onwards, and of flowering plants from about 115 million
years onwards (not indicated in Fig. 19).
The fossil evidence suggests indeed that the Prasinophyceae are very ancient (at
least 600 Ma, perhaps 1400 Ma). The oldest rehable records of the Ulvophyceae and
Charophyceae are about 400-500 Ma, and these are fossils of the most derived orders
within the two classes (the Dasycladales in the Ulvophyceae, the Charales in the
Charophyceae). The oldest vascular plants are ca. 400 Ma. These data suggest that the
radiation of the chlorophytan classes took place far earlier than 500 Ma ago.
If we consider the geologic occurrence of still extant genera, the differences become
more striking. The prasinophycean genera Pterosperma and Pachysphaera would be at
C. v a n d e n Hoek, W. T. Stam & J. L. Olsen
368
u ~mmm
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Fig. 19. Geologic occurrence of chlorophytan classes and orders, and of a number of extant genera
(Based on Bassoulet et al., 1978; Colbath, 1983; Elliott, 1981; Hillis-Colinvaux, 1980; Parke et al.,
1978; Souli~-M~rsche, 1979; Tappan, 1980)
least 600 M a old if the fossil g e n e r a Pterospermella and Tasmanites do i n d e e d b e l o n g to
the two recent g e n e r a (Boalch & Parke, 1970; Parke et al., 1978).
Some extant u l v o p h y c e a n g e n e r a would have m i n i m u m - a g e s of a b o u t 230-80 Ma;
and some extant charophycean genera (in the Charales) of about 250-80 M a (Fig, 19),
S o m e extant conifer genera are at least 150-50 M a old; and extant flowering plant genera
about 60-5 M a (Meyen, 1987; MflUer, 1981; Thomas & Spicer, 1986).
The m u c h smaller phenotypic change within the primitive chlorophytes than in the
derived chlorophytan groups is also suggested by the low green algal diversity
(7000-8000 species) as compared to the high diversity in the vascular plants (ca 250,000
species, Of which ca 200,000 are flowering plants).
A new chiorophytan system
369
Macromolecular evidence
After two related evolutionary hneages have diverged, their initially similar genomes
will automatically and inexorably diverge with time even when these hneages remain
morphologically highly similar (Ayala, 1986; Nei, 1987; Thorpe, 1982). By comparing the
genetic codes as stored in nuclear DNA, chloroplast DNA, ribosomal RNA, proteins, it is
possible to quantify the measure of genetic divergence between hneages of more or less
related organisms and thus to indicate which lineages are genetically more closely
related (i.e. diverged more recently) and which are more distantly related (i.e. diverged
relatively long ago). These methods do of course not permit the reconstruction of extinct
ancestors.
By comparing with these methods genomes of representative species of principal
hypothetical lineages one can attain estimates of relative divergence times among
hneages and thus test the validity of the hypothetical phylogeny. This approach has been
applied by Hori and his associates (Hori et al., 1985; Hori & Osawa, 1987). They have
studied the phylogenetic relationships among a wide spectrum of extant organisms using
5S ribosomal RNA sequences. This is one of the molecules suited to the study of
evolutionary relationships among widely separate organisms because of its universal
occurrence and the low substitution rates of its nucleotides. As a part of these studies, the
evolutionary relationships among the green plants (Chlorophyta, mosses, hverworts, and
vascular plants) were determined. The results are summarized in Figure 20. Only a few
green algae from divergent groups were included in this study.
One is actually amazed that various hypotheses underlying the phylogenetic tree of
Figure 18 are supported by Hori's 5S rRNA-phylogenetic tree. The following hypotheses
are confirmed:
(1) The mosses, liverworts and vascular plants evolved from green algal ancestors.
(2) The nearest green algal ancestor of the mosses, liverworts and vascular plants is
in the lineage of the Charales. This supports the concept of the class Charophyceae.
(3) Chlamydomonas represents an ancient lineage in the green plants. This supports
the idea that the free hving green flagellates represent the most ancient lineages in the
green algae.
(4) The remaining hneages of the green algae in this study emerged, in the course of
evolution, after Chlamydomonas and before the Charales. Ulva and Cladophora on the
one hand and the three coccoid green algae Scenedesmus A, Scenedesmus B and
Chlorella on the other hand are distantly related; this supports the concepts of the classes
Ulvophyceae and Chlorophyceae. Zygnematophyceae seem to be close to the
Chlorophyceae.
(5) Chlamydomonas and the three coccoid green algae clearly do not belong to the
same hneage (as proposed by Deason, 1984; Hoops et al., 1982; Mattox & Stewart, I984;
Melkonian, 1982; O'Kelly & Floyd, 1984; Sluiman, 1985b; Sluiman et al., 1980a).
Rather, the concepts of the separate classes Chlamydophyceae and Chlorophyceae,
as proposed by Ettl (1981) and here adopted with shght modification, are confirmed by
Hori's results.
One hypothesis pictured in Figure 18 is not confirmed by Hori's phylogenetic tree,
namely the derivation of the Charophyceae from a separate (i.e. unilateral) green
flagellate ancestor. Rather, the charophycean lineage seems to emerge at an early stage
C. v a n d e n Hoek, W. T. Stam & J. L. Olsen
3'70
&
I!
iii
gl ~1 ,-I .,-t
m~
4a.,~
t~,-i
ml:~m
tqr
!1 .,-t
Y
J
0.1 84
J
J
j/
/
a2-
1/2Knuc
Fig. 20. Phylogenetic tree Of 5S rRNA's from green plants (modified after Hori et al., 1985, and Hori &
Osawa, 1987). Knuc is the evolutionary distance between two sequences; 189
between the point
of divergence and each of the two sequences. Knuc estimates the number of base substitutions per
nucleotide site that have occurred since the separation of the two sequences. S c e n e d e s m u s 1 = S.
o b l i q u u s ; S.2 = S. q u a d r i c a u d a ; A n t h o c e r o s p. = A . p u n c t a t u s ; M a r c h a n t i a p. = M . p o l y m o r p h a ,
Lophocolea
Lycopodium
q u o t a = 5/1.
[.u'num u. =
esculentum;
h. = L. h e t e r o p h y l l a ; P l a g i o m n i u m
= P. t n ' c h o m a n e s ; P s i l o t u m n. = P. n u d u m ;
c. = L. d a v a t u m ; E q u i s e t u m a. = E. a r v e n s e ; D r y o p t e r i s a. = D. a c u m i n a t a ; M e t a s e g l y p t o s t r o b o i d e s ; G i n k g o = G. b f l o b a ; C y c a s r. = C. r e v o l u t a ; L e m n a m . = L. m i n o r ;
L. u s i t a s i s s i m u m ; T r i t i c u m = T. a e s t i v u m ; S e c a l e = S. c e r e a l e ; L y c o p e r s i c u m = L.
H e l i a n t h u s = H. a n n u u s ; S p i n a c i a = S. o l e r a c e a ; L u p i n u s = L. t u t e u s ; P h a s e o l u s = P.
v u l g a r i s ; V i c i a = V. f a b a
from a c o m m o n l i n e a g e of multicellular g r e e n algae. This suggests that t h e evolutionary
step from free living g r e e n flagellates to multicellular g r e e n al g ae took p l a c e only once.
A n o t h e r suggestion is that the unilateral r e p r o d u c t i v e zoids in the C h a r o p h y c e a e origin a t e d from cruciate reproductive zoids. T h e number, h o w e v e r , of species a n d the n u m b e r
of orders an d classes r e p r e s e n t e d is still e x t r e m e l y ]imited in this s t u d y so that t h e
conclusions can only b e prehminary. H o w e v e r , so far the studies of Hori a n d his
collaborators are quite u n i q u e in phycology.
By c o m p a r i n g g e n o m e s of p h e n o t y p i c a l l y close relatives one could, in principle, test
the hypothesis that extant g e n e r a a n d species in p r e s u m p t i v e ancient h n e a g e s are on
A new chlorophytan system
371
average old (i,e, diverged long ago),-as compared to genera and species in derived and
young hneages. The literature contains scattered reports which might be relevant in this
context. These reports are studies on chloroplast genome structure in green plants
including green algae; DNA-DNA hybridization studies on the Cladophorales; and
immunological studies in the latter group.
Chloroplast g e n o m e s in g r e e n plants
The organization of the chloroplast genomes of over 200 flowering plants, one
gymnosperm, three ferns and two mosses, has been investigated. In contrast, the
chloroplast genomes of only about ten green algae have been studied, among them four
species of Chlamydomonas (Palmer, 1985).
With rare exceptions, the chloroplast genomes of land plants are extraordinarily
conserved in size, gene content and gene order. The large majority of angiosperms and
other land plants have chloroplast DNAs that vary between 120 Kb and 160 Kb in size.
Most of this variation can be accounted for by changes in the size of the large rRNA
encoding inverted repeat and this is caused by rare deletions and duplications. Inversions
and other mutations that change the relative order of genes are extremely rare in the
chloroplast DNAs of land plants.
Overall, the angiosperms and other land plants have the same conserved gene
arrangement in the chloroplast genome. For instance, the arrangement of the liverwort
Marchant~'a polymorpha is similar to that of most angiosperms, and this would imply that
the land plant arrangement of the chloroplast genes exists at least since the evolutionary
divergence of vascular plants and bryophytes ca 400 Ma ago (Palmer, 1985; Palmer et al.,
1987).
In contrast to this high similarity of chloroplast genomes in the land plants, the
chloroplast DNAs of two distantly related Chlamydomonas species (C. eugametos and
C. reinhard~) are extremely divergent expecially with regard to gene order (Palmer,
1985; Lemieux et al., 1985). Lemieux and his co-workers suggest that C. eugametos and
C. reinhardtii represent green algal lineages that diverged much earlier than the land
plant lineages. This suggests a minimum age of 400-500 Ma for the genus Chlamydomonas. Clearly this interpretation is in support of the basic hypothesis that the free
living green algal flagellates represent phenotypically conserved, very slowly changing
lineages.
Interestingly, phenotypically similar pairs of related, (partly) interfertile, species of
Chlamydomonas (C. reinhardtii and C. smithfi; C. eugametos and C. moewush) share
essentially the same arrangement of common sequences. There are, however, small
differences in an order comparable to those among the land plants. Moore & Coleman
(1987) recently reported that geographically isolated populations in one and the same
syngen (= interbreeding set of populations) of the colonial green flagellate Pandorina
morum, differed in their chloroplast DNAs with an order comparable to that between
genera and families in the flowering plants.
Non-interbreeding populations of the morphological species Pandorina morum,
however, showed extensive differences in their chloroplast genomes. These results also
support the idea that green algal flagellates are phenotypically highly conservative
372
C. van den Hoek, W. T. Stam & J. L. Olsen
hneages. They suggest for the morphological species Pandorina morum a minimum age
of 400-500 Ma. See Figure 19 which indicates the fossil occurrence of "Eovolvox" nearly
400 Ma ago.
Single-copy DNA-DNA hybridization
Certain highly disjunct distributions of s e a w e e d species may suggest their minimum
ages. For instance, many tropical seaweed species occur in the Caribbean and the IndoW. Pacific, and this distribution pattern may be explained as being a Tethyan rehct
distribution (Elliott, 1981; HiUis-Cohnvaux, 1980, 1986; van den Hoek, 1984b; Joosten &
van den Hoek, 1986). Of an originally continuous Tethyan area the western (Caribbean)
and eastern (Indo-W. Pacific) portions became definitively separated bY the Miocene (20
Ma) uphft of the Middle East, but earlier temporary closures had also occurred. This
suggests a minimum age of 20 Ma for morphological species with this distribution
pattern.
A considerable number of genera and species within the orders Cladophorales,
Bryopsidales and Dasycladales of the class Ulvophyceae exhibit this tropical disjunct
distribution. Fossil representatives of the extant Dasycladalean genera Dasycladus,
Cymopoh'a, Neomeris and Acetabularia (see Fig. 19) had indeed a continuous distribution around the Tethys Ocean throughout the Cretaceous and the early Caenozoic
(Elliott, 1981).
In our laboratory we try to estimate divergence times between infraspecific disjunct
populations of morphological species using single-copy DNA-DNA hybridization. The
difference in thermal stabihty between homoduplexes and heteroduplexes as determined
from thermal elution profiles provides a measure of genotypic relationship. The temperatures are taken at which 50 % of the hybrids are eluted. A difference (STM(e)) of 1 ~
is estimated to equal on average 5.5 Ma (Stare et al., 1988). Using this approach two
disjunct Dictyosphaeria cavernosa isolates (Cladophorales) from Hawaii a n d the Virgin
Islands were estimated to have diverged 55 Ma ago and D. cavernosa and D. versluysii
isolates ca 70 Ma ago (Olsen et al., 1987). This indicates a high degree of morphological
conservatism in Dictyosphaeria, with an u n c h a n g e d D. cavernosa morphology from
70-50 Ma ago to present. In our laboratory, Bot obtained comparable results with highly
disjunct isolates of morphological Cladophora species or species complexes (Bot et al., in
prep.). Comparably low DNA homologies exist between strains of one a n d the same
phenotypic Chlorella species, while different Chlorella species have a v e r y low, or an
undetectable level of DNA homology (Huss et al., 1986, 1987a, 1987b).
The above Dictyosphaeria isolates were also included in a broad study of phylogenetic relationships within the Cladophorales on the basis of immunological distance data
(Olsen-Stojkovich e t al., 1986; Olsen-Stojkovich, 1986). The relative divergence times of
the three Dictyosphaeria isolates were the same as in the DNA-DNA hybridization study.
In the immunological study the relative divergence times (as immunological distances) were estimated between 43 isolates belonging to 26 species in 16 g e n e r a (Fig. 21).
The results indicate a high degree of morphological conservatism within the Cladophorales as a whole, and also in its separate hneages representing the extant genera. Different
Cladophora species emerged in distant portions of the phylogenetic tree and this
confirms van den Hoek's idea that the genus Cladophora is paraphyletic (van den Hoek,
1984a). The different genera in the Cladophorales can be interpreted as various speciah-
A n e w chlorophytan system
373
zations of the s i m p l e Cladophora
architecture (probably of the C. pellucida-type; s e e v a n
den Hoek, 1984b). The b r a n c h e s of the phylogenetic tree that c h a n g e d relatively little in
morphology retained, in shghtly different forms, the simple ancestral Cladophora
architecture. In a comparable way, sarcinoid a n d coccoid green algae form p r o b a b l y
primitive paraphyletic b u n d l e s in the Cylindrocapsales (Chlorophydeae) a n d the Klebsormidiales (Charophyceae).
-100
immunological
distance
Fig. 21. Phylogenetic tree of genera in the Cladophorales, based on immunological distances per
genus, as average of one or more species. OG = outgroup = Acetabularia; AP = Apjohnia
laetevqrens; C V = Cladophora vagabunda; C H = Chaetomorpha 4 spp.; V A = Valonia 3 spp.; V P =
VaZoniopsis pachynema~ W : Vent~icaria ventricosa; DI = Dictyosphaeria 4 spp.; SI --- Siphonocladus tropicus; B F = Boergesenia [orbesii~ E V = Ernodesmis verticillata; C P = Cladophora
prolifera; A N = Anadyomene stellata; M I = Microdictyon setchellianum; C A = Chamaedor~s
peniculum; CL = Cladophoropsis membranacea; S T = Struvea anastomosans; B O = Boodlea
composita. Note that two species of Cladophora (dots) e m e r g e at two different points of the tree,
indicating the paraphyletic nature of this "genus" (Based on Olsen-Stojkovich, 1986)
374
C. v a n d e n Hoek, W. T. Stam & J. L. Olsen
Table 3. Summary of estimated minimum age of extant genera and species in some chlorophytan
classes. Between brackets: number of genera/species for which estimates are available. (f) = fossil
evidence; (m) = macromolecular evidence
Classes
Orders
Prasinophyceae
Chlamydophyceae
Ulvophyceae
BryopsidaIes
Dasydadales
Cladophorales
Charophyceae
Charales
Angiosperms
Minimum age extant
genera in Ma
600
(2) (f)i
400-500 (2) (m)2
Minimum age extant
species in Ma
400-500 (1) (m)3
230-75 (2) (f)4
220-80 (4) (f)s
70 (1) (m)5
250-80 (7) (f)8
5-60
(numerous) (f)s
55-70
(I) (m)7
20-40 (14) (m) l~
5-I0
(numerous) (f)ll
<
1: Colbath, 1983; Parke et al., 1978; Tappan, 1980.
2, 3: Lemieux et al., 1985; Moore & Coleman, 1987; Palmer, 1985; Palmer et al., 1987.
4: Elliott, 1981; Hillis-Colinvaux, 1980; Tappan, 1980.
5: Bassoulet et al., 1978; Elliott, 1981.
6, 7: Olsen et al. 1987.
8: Souli4-M~irsche, 1979.
9, 11: Mfiller, 1981.
10: Belford & Thompson, 1981.
CONCLUSIONS
We do have some fossil evidence a n d some macromolecular e v i d e n c e in support of
the following hypotheses r e g a r d i n g the p h y l o g e n y of the chlorophytes.
(1) The free living g r e e n flagellates represent the oldest, most c o n s e r v a t i v e lineages
in the Chlorophyta, a n d they are ancestral to the other, non-flagellate Chlorophyta. This
hypothesis has b e e n formulated on the basis of mainly morphological, ultrastructural a n d
life history evidence, a n d it is confirmed by a (limited) 5S rRNA p h y l o g e n y .
(2) The first implication of the hypothesis in p a r a g r a p h 1 is that e x t a n t g e n e r a a n d
species in the flagellate chlorophytes can be expected to be, on a v e r a g e , a n c i e n t a n d
phenotypically conservative relative to g e n e r a a n d species in d e r i v e d nonflagellate
lineages. Fossil e v i d e n c e indicates that the extant p r a s i n o p h y c e a n g e n e r a Pterosperma
a n d Pachysphaera are probably at least 600 Ma old. Comparison of chloroplast g e n o m e s
suggest that the g e n u s Chlamydomonas a n d the morphological species Pandorina
morum are p e r h a p s older t h a n 400-500 Ma.
(3) The s e c o n d implication of the hypothesis in p a r a g r a p h 1 is that e x t a n t g e n e r a a n d
species in the most derived Chlorophytes {the Angiosperms) can b e e x p e c t e d to be, on
average, y o u n g a n d morphologically c h a n g e a b l e in comparison to the flagellate lineages.
Fossil e v i d e n c e indicates that m a n y extant g e n e r a of flowering plants a r e at least 5-60
Ma old. D N A - D N A hybridization experiments with Atriplex species s u g g e s t species
divergences b e t w e e n 20-40 M a ago (Belford & Thompson, 1981). N u m e r o u s flowering
A new cblorophytan system
375
p l a n t f a m i l i e s (e.g. B r a s s i c a c e a e , P r i m u l a c e a e , L a m i a c e a e , F a b a c e a e ) a p p e a r e d as l a t e as
M i o c e n e (10-5 Ma) (M/filer, 1981). T h e i r g e n e r a a n d species a r e of c o u r s e e v e n y o u n g e r .
(4) T h e t h i r d i m p l i c a t i o n of t h e h y p o t h e s i s in p a r a g r a p h 1 is that e x t a n t g e n e r a a n d
s p e c i e s in t h e c h l o r o p h y t e s of i n t e r m e d i a t e d e r i v a t i o n (e.g. U l v o p h y c e a e , C h a r o p h y c e a e )
c a n b e e x p e c t e d to h a v e an i n t e r m e d i a t e a g e a n d m o r p h o l o g i c a l c o n s e r v a t i s m . Fossil
e v i d e n c e i n d i c a t e s that six e x t a n t g e n e r a in t h e B r y o p s i d a l e s a n d D a s y c l a d a l e s are at
l e a s t 2 3 0 - 8 0 M a old, a n d that s e v e n g e n e r a in t h e C h a r a l e s a r e at least 2 5 0 - 8 0 M a old.
T h e g e n u s Dictyosphaeria (Cladophorales) is e s t i m a t e d to b e ca 70 M a old on t h e basis of
D N A - D N A h y b r i d i z a t i o n w h e r e a s the m o r p h o l o g i c a l s p e c i e s D. cavernosa is t h o u g h t to
b e 5 5 - 7 0 M a old (See T a b l e 3 for a s u m m a r y of i t e m s 1-4).
(5) T h e m a i n p h y l o g e n e t i c l i n e a g e s in t h e C h l o r o p h y t a are n o t r e p r e s e n t e d b y t h e
p r o g r e s s i v e l y m o r e d e r i v e d o r g a n i z a t i o n a l l e v e l s (flagellate level, c o c c o i d level, s a r c i n o i d
level, f i l a m e n t o u s level, s i p h o n o c l a d o u s level, s i p h o n o u s level). This t r a d i t i o n a l
h y p o t h e s i s of c h l o r o p h y t a n e v o l u t i o n s h o u l d n o w b e a b a n d o n e d . Dr. K o r n m a n n ' s i d e a
that d i v e r g e n t o r g a n i z a t i o n a l l e v e l s h a v e b e e n r e a l i z e d w i t h i n o n e c h l o r o p h y t a n g r o u p is
correct.
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