HETEROKONTOPHYTA, PHAEOPHYCEAE	433

Fig. 21.9 Dieter G. Muller Born January 24, 1935, in Stuttgart, Germany. From 1956 to 1961, Dr. Muller studied at the Universitat Tubingen; from 1961 to 1963, he was a Postdoctoral Fellow at the University of Pennsylvania; from 1964 to 1973, he was Wissenschaftlicher Mitarbeiter at the Max-Planck-Institut fur Zuchtungsforschung at KolnVogelsang. In 1973, he received his Habilation at the University of Koln; and since 1973, he has been professor in the Fakultat für Biologie at the Universitat Konstanz. In 1964, Dr. Muller received strong support from Professor J. Straub, director of the Max-Planck-Institut, Koln, to work out in detail the life cycle of Ectocarpus siliculosus. After evidence for a sexual hormone was discovered, a cooperation scheme was established with the Institut für Biochemie at the University of Koln. These two events led to the characterization of the sexual hormones of the brown algae.

fucoserratene from Fucus serratus and F. vesiculosus

(Müller and Jaenicke, 1973) (Fig. 21.9).

Classification

The Phaeophyceae are an ancient lineage, originating between 150 (Medlin et al., 1997) and 200 million years ago (Lim et al., 1986). The Xanthophyceae and Phaeothamniophyceae are the closest known sister taxa to the Phaeophyceae. The first true brown alga was probably similar to the extant Choristocarpus tenellus (Fig. 21.10) with creeping filaments, apical growth, and an isomorphic life history (de Reviers and Rousseau, 1999; Draisma et al., 2001).

Fig. 21.10 Choristocarpus tenellus showing the uniseriate

filament and a propagule with an apical cell.

Within the Phaeophyceae, the Fucales are a sister group to the remainder of the algae in the class. The early divergence of the Fucales is consistent with the presence of a proboscis in the spermatozoids of Vaucheria and Fucus (de Reviers and Rousseau, 1999). Fossils similar to Cutleria occur in 25 million-year-old Miocene deposits while fossils similar to algae in the Laminariales and Fucales occur in 16–20 million year old Miocene deposits.

The orders considered here are presented in an evolutionary sequence with the Dictyotales and Sphacelariales being the most ancient and the Ectocarpales and the Laminariales the most recent (de Reviers and Rousseau, 1999; Draisma et al., 2001).

Order 1 Dictyotales: growth by an apical cell; meiosis occurring in the production of four to eight non-motile spores; oogamous sexual reproduction.

Order 2 Sphacelariales: growth by an apical cell; daughter cells divided longitudinally to give a polysiphonous structure; isogamous sexual reproduction.

Order 3 Cutleriales: trichothallic growth forming a fan-like thallus in at least one generation; anisogamous sexual reproduction.

434 CHLOROPLAST E.R.: EVOLUTION OF TWO MEMBRANES

Order 4 Desmarestiales: trichothallic growth forming axial cells; oogamous sexual reproduction.

Order 5 Ectocarpales: thallus consisting of filaments or filaments compacted together; reproduction isogamous or anisogamous.

Order 6 Laminariales: diploid thallus parenchymatous resulting from an intercalary meristem between the stipe and blade; reproduction oogamous.

Order 7 Fucales: growth primarily by a promeristem; gametophyte reduced to egg and sperm; oogamous sexual reproduction.

Dictyotales

This order has organisms that grow by means of an apical cell or by a marginal row of apical cells. There is an isomorphic alternation of erect, flattened, parenchymatous thalli. A distinctive character of this order is the modification of the unilocular sporangia to produce four to eight large aplanospores. Sexual reproduction is oogamous. The Dictyotales are common in warmer waters throughout the world.

Dictyota dichotoma has a single apical cell that forms the flattened annual thallus (Fig. 21.11). The mature thallus consists of three layers: a middle layer composed of large cells with few or no chloroplasts, surrounded on both sides by a layer of small cells densely packed with chloroplasts. Gametophytes form sex organs in projecting sori. Gametogenesis can be artificially induced by exposure of the gametophytes to blue light (Kumke, 1973). An oogonium develops from a surface cell that divides into a stalk cell and the oogonium proper. Each oogonium produces a single egg, which is liberated through the gelatinized apex of the wall. There are usually 25 to 50 oogonia in a sorus with sterile oogonia at the margin. The deep-brown color of the female sori contrasts with the white glistening spots that comprise the male sori. The male sori can be recognized early in their development by the disintegration of the chloroplasts in the cells. Like the oogonia, the antheridia develop from surface cells. These cells enlarge and divide horizontally into a stalk cell and a primary spermatogenous cell. This cell

divides and redivides in vertical and horizontal planes into between 650 and 1500 compartments (Williams, 1904). The content of each locule becomes a pear-shaped sperm with a single, laterally inserted, tinsel flagellum and an anterior eyespot (Phillips and Clayton, 1993). Although there is only one emergent flagellum, a second basal body is present (Manton, 1959), indicating a derivation from a biflagellate ancestor. The mature sperms are set free by dissolution of the walls of the antheridium. The male sorus is surrounded by elongated sterile cells that are regarded as undeveloped antheridia. The egg secretes the pheromone dictyotene (Fig. 21.8) (Pohnert and Boland, 2002) that attracts the sperm. The sperm fertilizes the egg to produce the zygote that germinates into the sporophyte; unfertilized eggs can germinate parthenogenetically but seldom develop normally and soon abort. The sporophytes produce haploid aplanospores (tetraspores) on the surface of the thallus. The tetrasporangia occur singly or in small groups. The naked tetraspores are released by gelatinization of the apex of the sporangium, and soon after liberation the large motionless spores secrete a cellulose wall and develop into the gametophytes.

In D. dichotoma, the gametes are released at regular intervals. This was first noticed by Williams (1905) in Great Britain, where the gametes are released fortnightly. Müller (1962) showed that moonlight is the synchronizing factor for the release. When he grew the alga in natural light, gametes were released every 14 to 15 days. If the alga was grown under artificial conditions with a 14 hours light : 10 hours dark cycle, then few gametes were released, and there was no synchronony. If the artificially lighted cultures had the lights left on all night, then 10 days later a burst of gametes was released. The lights being left on all night simulated moonlight.

Species of Dictyota produce terpenoids, such as pachydictyol and (6R)-6-hydroxydichotoma-3, 14-diene-1,17,dial (Fig. 21.12), that inhibit grazing of Dictyota by herbivorous fish, amphipods, and sea urchins (Schmitt et al., 1998; Pereira et al., 2000).

The only calcified genus in the Phaeophyceae, Padina, is in the Dictyotales.

HETEROKONTOPHYTA, PHAEOPHYCEAE	435

Fig. 21.11 The life cycle of Dictyota dichotoma. (Adapted

from Thuret and Bornet, 1878; Williams, 1898; Taylor, 1960.)

436 CHLOROPLAST E.R.: EVOLUTION OF TWO MEMBRANES

Fig. 21.12 The chemical structure

of two secondary metabolites

secreted by Dictyota spp. that act as

antifoulants.

Sphacelariales

This order is characterized by an apical meristematic cell that divides transversely to produce the daughter cells. The algae produce distinctive vegetative propagules. Another less precise characteristic is blackening of the cell walls when treated with bleaching liquid (Draisma et al., 2002).

Sphacelaria (Fig. 21.13) grows attached to rocks or other algae and has one or more freely branched shoots arising from a discoid holdfast. The apical cell undergoes transverse divisions, with subsequent longitudinal septation of the daughter cells to produce a polysiphonous structure. Although the maturing axes and branches undergo septation into smaller and smaller cells, they do not enlarge; thus the diameter of the filament is essentially the same from the base to the apex. Older axes, though, may become corticated by downward-growing filaments. The erect axes are usually abundantly branched, usually in a regular, distichous manner.

Asexual reproduction is by means of propagula (Fig. 21.13), which are specialized branchlets of distinctive form that are produced throughout the vegetative parts of the plants. They are formed much more frequently than sporangia or gametangia. Each propagule has an apical cell and usually two to three protuberances. After falling from the parent plant and contacting a suitable substrate, the propagule develops into a new plant. Propagula are formed only at temperatures above 12 °C and under daylight conditions longer than 12 hours (Colijn and van den Hoek, 1971).

In S. bipinnata, the sporophyte forms both unilocular and plurilocular sporangia terminally on branches (Fig. 21.13). The plurilocular sporangia produce zoospores that re-form the parent

sporophyte. Meiosis occurs in the production of zoospores in the unilocular sporangia (Clint, 1927). Over 200 zoospores are released through an apical pore in the unilocular sporangium (Papenfuss, 1934). The zoospores germinate to presumably form gametophytes that are similar to the sporophytes. The gametophytes produce plurilocular gametangia of one type, which release isogamous gametes. Ectocarpene (Fig. 21.8) is used as a pheromone in gamete attraction (Pohnert and Boland, 2002). The fusion of gametes takes place while they are motile and produces a quadriflagellate zygote that may continue moving for several hours. The life cycle of another species, S. furcigera, involves anisogamy and unisexual gametophytes, which are somewhat smaller than the sporophytes (van den Hoek and Flinterman, 1968). The life cycle is controlled by temperature and photoperiod.

Cutleriales

This order contains only two genera, Cutleria and Zanardinia. The genera show an alternation of generations that is heteromorphic in Cutleria and isomorphic in Zanardinia. The thallus is flattened, blade-like, or disc-like, with entirely or partially trichothallic growth. The sporophytes produce only unilocular sporangia, whereas the gametophytes are heterothallic and markedly anisogamous.

Cutleria is a warm-water plant of the Northern Hemisphere that may be closely related to Saccorhiza in the Laminariales (Rousseau et al., 1997). The gametophyte is an erect, flattened blade with numerous dichotomies (Fig. 21.14). Growth is trichothallic at the base of many erect uniseriate hairs at the upper margin of the blade. The cells that are cut off below the hairs contribute to the thallus. The innermost of these cells gradually enlarge to form the medulla, whereas

HETEROKONTOPHYTA, PHAEOPHYCEAE	437

Fig. 21.13 The life cycle of Sphacelaria (S. cirrhosa and

S. bipinnata). (Adapted from Savaugeau, 1900–14; Papenfuss,

1934; Taylor, 1957.)

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Fig. 21.14 The life cycle of Cutleria multifida. (Adapted

from Kuckuck, 1899; Savaugeau, 1899.)