What are Glaucophyta characteristics

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Glaucophyta The Glaucophyta include those algae that have Glauco phyta lack a wall and are surrounded by endo symbiotic cyanobac teria in the cyto plasm two membranes – the old food vesicle membrane instead of chloro plasts. Because of the nature of of the cyanome and the plasma membrane of their symbiotic associa tion, they are thought to the cyanelle. As evolu tion progressed, these two repre sent intermedi ates in the evolu tion of the membranes became the chloroplast envelope, the chloro plast. The endo symbiotic theory of chloro - cyanome cytoplasm took over the formation of plast evolu tion, first pro posed by Mereschkowsky the storage product and the polyhedral bodies in 1905, is the one most widely accepted. Accord - containing ribulose-1,5-bisphosphate carboxylase/ ing to this theory, a cyanobacterium was taken up oxygenase differentiated into the pyrenoid. by a phagocytic organ ism into a food vesicle. There are a number of similarities between Normally the cyanobacterium would be digested cyanobacteria and chloroplasts that support the by the flagellate, but by chance a muta tion endosymbiotic theory: (1) they are about the same occurred, with the flagellate being unable to size; (2) they evolve oxygen in photosynthesis; digest the cyanobacterium. This was probably a (3) they have 70S ribosomes; (4) they contain cir- beneficial muta tion because the cyanobacterium, cular prokaryotic DNA without basic proteins; by virtue of its lack of feedback inhibi tion, (5) nucleotide sequencing of rRNA or of DNA secreted consid erable amounts of metabolit es to encoding rRNAs have shown similarities; (6) they the host flagellate. The flagellate in turn gave the have chlorophyll a as the primary photosynthetic cyanobacterium a pro tected environ ment, and pigment. the composite organ ism was probably able to live The pigments of the Glaucophyta are similar in an ecolog ical niche where there were no photo - to those of the Cyanophyceae: both chlorophyll a syn thetic organ isms (i.e., a slightly acid body of and the phycobiliproteins are present; however, water where free-living cyanobacteria do not two of the cyanobacterial carotenoids, myxoxan- grow; see Chapter 2). Pascher (1914) coined terms thophyll and echinenone, are absent (Chapman, for this associa tion; he called the endo symbiotic 1966). cyanobacteria cyanelles; the host, a cyanome; and Although similar to cyanobacteria, the cyanel - the associa tion between the two, a syncyanosis. In les should be regarded as organelles rather than the original syn cyano sis the cyanelle had a wall endosymbiotic cyanobacteria (Helmchen et al., around it. Because the wall slowed the trans fer 1995; McFadden, 2001). Cyanobacteria have over of compounds from the cyanelle to the host and 3000 genes whereas cyanelles have about the vice versa, any muta tion that resulted in a loss same number of genes as plastids (about 200 of wall would have been beneficial and selected genes). It is clear the cyanelles (and plastid) for in evolution. Mos t of the cyanelles in the genomes have undergone substantial reduction86 EVOLUTION OF THE CHLOROPLAST during endosymbiosis. Many of the missing enzyme in photo syn thesis, consists of 16 sub- genes eventually relocated to the nucleus, while units, 8 large and 8 small. In higher plants the other genes were lost – made redundant in the large subunits are encoded by DNA of the plas- cyanelles’ new role as an endosymbiont. For exam- tids, whereas the small sub units are encoded ple, cyanobacteria have a respiratory electron- by nuclear DNA. In Cyanophora paradoxa, both chain whereas plastids do not, the respiratory sizes of subunits are encoded by cyanelle DNA. electron-chain is coded by the nucleus in eukary- This non-cyanobacterial ribulose-1,5-bisphosphate otic algae. carbo xylase/ oxygenase in cyanelles is now ratio- The organisms in the Glaucophyta are very nalized as lateral gene transfer or gene substitu- old; McFadden (2001) calls them the coelocanths tion from a mitochondrion or plastid (McFadden, of endosymbiosis. The Glaucophyta probably 2001). The mechanism of division of cyanelles in branched off the evolutionary tree before the Cyanophora paradoxa is intermediate between the divergence of red and green algae from one division of cyanobacteria and that of plastids. another (Keeling, 2004). Plastids have an inner and outer ring of electron- The fact that in such syn cyanoses one is deal- dense material in the area of the dividing ing with composite organ isms that exhibit organelle. In division of cyanelles of Cyanophora features alto gether new and no longer character - paradoxa, however, there is only an inner ring in istic of either partner alone, led Skuja in 1954 to the “stroma” inside the plasma membrane (“inner establish the phylum Glaucophyta. It must be envelope”) of the cyanelle. The outer ring, nor- appreciated that the organ isms in the phylum mally outside the outer chloroplast envelope, is repre sent a very old group, and that, when evolv- missing (Fig. 3.2) (Iino and Hashimoto, 2003). ing, they were very plastic and under going a great Glaucocystis is also a fresh water organ ism, deal of change in the attempt to reach the rela- found spar ingly in soft-water lakes (lakes low in tively stable level of a cell with a chloro plast. Such calcium). It has two groups of cyanelles, one on a dynamic group was formed consisting of a large each side of the nucleus (Fig. 3.1(b)). The deriva - number of organ isms not well suited to compete tion of Glaucocystis from a biflagellate ancestor is with their more highly developed progeny. Such a evident from the two reduced flagella found situa tion led to the demise of many of the original inside the cell wall. Both of these organ isms have members of the Glaucophyta, resulting in the starch formed in the cyto plasm, outside of the existence today of few extant members of the cyanelles, indicating that the host has accepted group. responsibil ity for the forma tion of the storage Cyanophora paradoxa is a freshwater flagellate product. with two cyanelles in the proto plasm, each There are other organ isms that have endo - cyanelle with a central dense body (Fig. 3.1(a)). symbiotic cyanobacteria that are not placed in the Nitrate reduc tion, photo syn thesis, and respira- Glaucophyta because they repre sent evolu tion ary tion in the cyanelles of Cyanophora paradoxa dead ends that did not lead to the evolu tion of are similar to the corresponding pro cesses ofchloro plasts. These organ isms have cyanelles that chloroplasts and dis similar to those of cyanobac- still have a cell wall and are cytolog ically similar teria (Floener and Bothe, 1982; Floener et al., to cyanobacteria, such as the cyanelles of the 1982). This fact is cited as evidence that the fungus Geosiphon (Schnepf, 1964). cyanelles of Cyanophora paradoxa are close to chloro plasts in evolu tion. However, the cyanelles of Cyanophora paradoxa are primitive in regard to where ribulose-1,5-bis phosphate carboxylase/ oxygenase is pro duced. Ribulose-1,5-bisphosphate carboxylase/oxygenase, the carbon dioxide-fixingGLAUCOPHYTA 87 Fig. 3.1 (a) Cyanophora paradoxa with two cyanelles (C), nucleus (N), and flagella (F). (b) Semidiagrammatic drawing of a cell of Glaucocystis nostochinearum showing two groups of cyanelles (C), reduced flagella (F), and a nucleus (N). ((a) after Mignot et al., 1969; (b) after Schnepf et al., 1966.)88 EVOLUTION OF THE CHLOROPLAST Fig. 3.2 Transmission electron micrographs of sections of dividing cells of Cyanophora paradoxa. (a) whole cell. (c) Cyanelle; (cb) central body. (b) A cross section of a division site with a septum (asterisk) dividing the inner envelope (double arrowhead) and the outer envelope (arrowhead). A cross section of an electron-dense cyanelle ring is seen at the leading edge of the inner envelope (arrow). (c) A moderately constricting cyanelle with a cyanelle ring (arrow) observed in a tangential section. (d) A deeply constricting division site. At the constricting neck, a pair of cross sections of a cyanelle ring is seen (arrow). (From Iino and Hashimoto, 2003.) Keeling, P. J. (2004). Diversity and evolutionary history REFERENCES of plastids and their hosts. Amer. J. Bot. 91:1481–93. Chapman, D. J. (1966). Pigments of the symbiotic McFadden, G. I. (2001). Primary and secondary endosym- algae (cyanomes) of Cyanophora paradoxa and biosis and the origin of plastids. J. Phycol. 37:951–9. Glaucocystis nostochinearum and two Rhodophyceae, Mereschkowsky, C. (1905). Ueber Natur und Ursprung Porphyridium aeruginosa and Asterocytis ramosa. Arch. den Chromatophoren in Pflanzenreich. Biol. Zentralbl. Mikrobiol. 55:17–25. 25:593–604. Floener, L., and Bothe, H. (1982). Metabolic activ ities Mignot, J. P., Joyon, L., and Pringsheim, E. G. (1969). in Cyanophora paradoxa and its cyanelles. Quelques particularités structurales de Cyanophora II. Photosynthesis and respira tion. Planta 156:78–83. paradoxa Korsch., proto zoaire flagellé. J. Protozool. Floener, L., Danneberg, G., and Bothe, H. (1982). 16:138–45. Metabolic activ ities in Cyanophora paradoxa and its Pascher, A. (1914). Uber Symbiosen von Spaltpilzen und cyanelles. I. The enzymes of assimilatory nitrate Flagellaten. Ber. Dtsch. Bot. Ges. 32:339–52. reduc tion. Planta 156:70–7. Schnepf, E. (1964). Zur Feinstruktur von Geosiphon pyri- Helmchen, T. A., Bhattacharya, D., and Melkonian, M. forme. Ein Versuch zur Deutung cytoplasmatischer (1995). Analysis of ribo somal RNA sequences from Membranen und Kompartimente. Arch. Mikrobiol. glaucocystophyte organelles provide new insights 49:112–31. into the evolutionary rela tion ships of plastids. J. Mol. Schnepf, E., Koch, W., and Deichgräber, G. (1966). Zur Evol. 41:203–10. Cytologie und taxonomischen Einordnung von Iino, M., and Hashimoto, H. (2003). Intermediate fea- Glaucocystis. Arch. Mikrobiol. 55:149–74. tures of cyanelle division of Cyanophora paradoxa Skuja, H. (1954). Glaucophyta. In Syllabus der (Glaucocystophyta) between cyanobacterial and Pflanzenfamilien, by A. Engler, ed. H. Melchoir, and E. plastid division. J. Phycol. 39:561–9. Werdermann, Vol. 1, pp. 56–7. Berlin: Borntraeger.Chapter 4 Rhodophyta dif fersaccordingtogeo graph icalregion.Thelarger RHODOPHYCEAE species of fleshy red algae occur in cool-temperate areas,whereasintrop icalseastheRhodophyceae (exceptformassivecalcare ousforms)aremostly The Rhodophyceae, or red algae, comprise the small, filamentous plants. The Rhodophyceae also only class in the division Rhodophyta. The Rhodo - have the ability to live at greater depths in the phyceae are probably one of the oldest groups of ocean than do members of the other algal classes. eukaryotic algae. The red algae are most likely They live at depths as great as 200 m, an ability directly descended from a cyanome in the relatedtothefunc tionoftheiraccessorypig ments Glaucophyta (see Chapter 3). It is likely that the inphoto syn thesis.About200speciesofRhodo - first red alga evolved into an ecological niche that phyceaearefoundinfresh water,wheretheydonot was unoccupied by cyanobacteria, the only extant reachasgreatasizeastheredsea weeds(Skuja, photosynthetic alga that evolved oxygen. This eco- 1938).Themajor ityoffresh waterredalgaeoccurin logical niche would have been in waters with a pH running waters of small to mid-sized streams less than 5, which, for some unknown reason, (Sheath and Hambrook, 1988). Few red algae occur cyanobacteria are not able to inhabit (Brock, 1 at currents of less than 30 cm s . This fast flow 1973). Indeed, modern phylogenetic studies uti- probably favors red algae because loosely attached lizing nucleic-acid sequencing have shown that competitors are washed out and because of a con- Cyanidium, an alga that lives in acidic waters, is stant replen ish mentofnutrientsandgases. probably the oldest extant red alga (Oliveira and Bhattacharya, 2000). The Rhodophyceae lack flagellated cells, have Cell structure chlorophyll a, phycobiliproteins, floridean starch as a storage product, and thylakoids occurring The major features of a red algal cell (Fig. 4.1) are singly in the chloroplast. a chloro plast with one thylakoid per band and no Amajor ityofthesea weeds are red algae, and chloro plast E.R., floridean starch grains in the there are more Rhodophyceae (about 4000 species) cyto plasm outside the chloro plast, no flagella, pit than all of the other major seaweed groups com- connec tions between cells in filamentous genera, bined. Although marine red algae occur at all and a eukaryotic type of nucleus (Scott et al., latitudes, there is a marked shift in their abun- 1980). dance from the equator to colder seas. There are few species in polarandsub polarregionswhere brownandgreenalgaepre dominate,butin Cell walls temperat eandtrop icalregionstheyfarout numberCelluloseformsthemicrofibrillarframe workin these groups. The average size of the plants also most rhodophycean cell walls, although in the90 EVOLUTION OF THE CHLOROPLAST Fig. 4.1 Semidiagrammatic drawing of a cell of Porphyridium cruentum. (c) Chloroplast; (g) Golgi; (m) mitochondrion; (mu) mucilage; (n) nucleus; (p) pyrenoid; (phy) phycobilisomes; (s) starch; (v) vesicle. (Adapted from Gantt and Conti, 1965.) haploid phase of the Bangiales (Bangia and Porphyra) cell (Lichtlé and Giraud, 1969). Chloroplasts are a -1,3linkedxylan(poly saccharidecomposedof surrounded by the two membranes of chloroplast xyloseresidues)per formsthisfunc tion(Freiand envelope with no chloroplast endoplasmic reticu- Preston, 1964). Unicellular red algae have an amor- lum present (Figs. 4.1, 4.2, 4.3). Thylakoids occur phousmatrixofsulfatedpoly saccharideswith- singly inside the chloroplasts. The phycobilin pig- out cellulose surrounding the cells (Arad et al., ments are localized into phycobilisomes on the 1993).Theamorphouspoly saccharidesormucil - surface of the thylakoids, a situation similar to ages occur between the cellulose microfibrils in the that in the cyanobacteria. rest of the red algae. The two largest groups of Chlorophyll a is in the chloroplasts. There have amorphousmucil agesarethe agars (Fig. 1.11) and been erroneous reports of chlorophyll d occurring the carrageenans(Fig.4.15).Thesemucil agesmay in the chloroplast. It has been shown that the constitute up to 70% of thedryweight ofthecell chlorophyll d in these studies came from the wall. Cuticles, composed mostly of protein, can cyanobacterium Acaryochloris marina, an epiphyte occur outside the cell wall (Craigie et al., 1992). on red algae (Murakami et al., 2004). The phycobiliproteins include R-phycocyanin, Chloroplasts and storage products allophycocyanin, and three forms of phycoery- Chloroplasts are usually stellate with a central thrin, the phycoerythrins being present in the pyren oid in the morpho log ically simple Rhodo - greatest amount, giving the algae their pinkish phyceae (Fig. 4.1), whereas in the remainder of the color. B-phycoerythrin is present in the more prim- Rhodophyceae they are commonly discoid (Fig. itive red algae and has been found in Pophyridium 4.3). In the Rhodophyceae with apical growth, the (Fig. 4.1), Rhodosorus (Fig. 4.24 (a)), Rhodochorton (Fig. chloroplasts usually originate from small color- 4.31) and Smithora. R-phycoerythrin occurs in most less proplastids with few thylakoids in the apical higher red algae, and C-phycoerythrin occurs inRHODOPHYTA 91 Fig. 4.2 Transmission electron micrograph of a section of a cell of Rhodella violacea. (C) Chloroplast; (M) mitochondrion; (N) nucleus; (P) pyrenoid; (S) starch; (V) vacuole. (From Marquardt et al., 1999.) Fig. 4.3 Chloroplast in a carpospore of Polysiphonia. (From Tripodi, 1974.) Porphyridium (Fig. 4.1), Porphyra (Fig. 4.27), and Floridoside (O--D-galactopyranosyl-(1,2)-glyc- Polysiphonia (Figs. 4.44, 4.45). The phycobiliproteins erol) is the major product of photosynthesis in are in phycobilisomes on the surface of thylakoids the red algae, although mannitol, sorbitol, dige- (Fig. 4.1). The phycobilisomes are spherical if both neaside, and dulcitol also occur (Fig. 4.4) (Barrow phycoerythrin and phycocyanin are present. The et al., 1995; Karsten et al., 2003). The concentra- phycobilisomes are discoid if only phycocyanin is tion of floridoside increases in red algal cells as present (Gantt, 1969). thesalin ityofthemediumincreases(Reed,1985). Complementary chromatic adaptation occursThischangeinfloridosideconcentra tionis in the red algae. Orange and red light stimulate thought to compensate, at least in part, for the the production of long-wavelength absorbing phy- changes inexternalosmolar ity,therebypre - cocyanin, while green light stimulates the forma- venting water from leaving the algal cells as the tion of short-wavelength absorbing phycoerythrinsalin ityincreases.Thelevelsoffloridosidecanbe (Sagert and Schubert, 1995). The color will vary. as high as 10% of the tissue dry-weight in some92 EVOLUTION OF THE CHLOROPLAST phot osyn thesis.Floridosideappar entlyhasthe samefunc tionassucrose,thecommonproduct ofphoto synthesisingreenalgaeandhigher plants. Floridean starch (Fig. 1.28) is the long-term storage product, occurring as grains in the cyto - plasm outside of the chloro plast (Fig. 4.1). Floridean starch is similar to the amylopectin of higher plants, staining red-violet with iodine. In the more primitive Rhodophyceae the starch grains are clustered as a sheath around the pyren - oid of the chloro plast, whereas in the more advanced Rhodophyceae the starch grains are scattered in the cyto plasm (Hara, 1971; Lee, 1974). Pit connections Pitconnec tions occur between the cells in all of Fig. 4.4 Chemical structure of low molecular the orders except the Porphyridiales, and the hap- polysaccharides that occur in the red algae. loid phase of the Bangiales. It has been pointed outthattheterm“pitconnec tion”isinappropri - marinered-algalthalli.Thefirstobserv ableprod- ate because the structureisneithera“pit”nora uctofphoto syn thesisisphosphoglycericacid,as“connec tion”;however,becausethetermhasbeen is the case in higher plants. Floridoside appears used for so long, it is probably best to retain it. A after 30 seconds of illumination and after 2 pitconnec tionconsistsofapro teinaceousplug hours floridosideisthemajor productof core in between two thallus cells (Figs. 4.5, 4.6). Fig. 4.5 Semidiagrammatic drawing of the formation of a pit connection in a red alga. (a) The cross wall begins to furrow inward with the wall precursors found in vesicles derived from the cytoplasm; (b) the cross wall septum is complete, leaving an opening (aperture) in the center; (c) endoplasmic reticulum lies across the opening in the wall, and electron-dense material condenses in this area; (d) the pit connection is formed, consisting of a plug with the plasmalemma continuous from cell to cell. (Adapted from Ramus, 1969, 1971; Lee, 1971.)RHODOPHYTA 93 Fig. 4.6 A pit connection between cells of Palmaria mollis. The plasma membrane is continuous from cell to cell. The cap membrane is continuous with the plasma membrane. The inner and outer cap layers are on each side of the cap membrane. (From Pueschel, 1987.) Capmembranessepar atetheplugcorefromthe and Trick, 1991; Ramus, 1971). The pit connec tion adjacentcyto plasm.Thecapmembraneis may func tion as a site of structural strength on continu ouswiththeplasmamembrane,whichin the thallus (Kugrens and West, 1973). In some turn is continu ous from one cell to the next. On algae the plugs of the pit connec tions become dis - the inside of the cap membrane can be an inner lodged from between the cells of a developing layer, while on the outside of the cap membrane gonimoblast, leaving the proto plasm continu ous can be an outer cap layer (Pueschel, 1987). The between the cells and allowing the passage of structureofthepitconnec tioncanvary.Themore metabolites to the developing repro ductive cells primitive red algae, such as Rhodochaete and (Turner and Evans, 1978). Compsopogon,lackcap membranes and cap layers, with only a plug core present. It has been postu- Calcification latedthatthisrepre sentstheancestralcondi tion (Pueschel, 1989). All members of the Corallinales and some of the There are two types of pit connec tions. Primary pit connec tions are formed between two Nemaliales (Liagora (Fig. 4.17 (a), (b)), Galaxaura cells during cell divi sion. Secondary pit connec - (Fig. 4.34)) deposit CaCO extracelluarly in the cell 3 tions result when two cells fuse. Both types of pit walls. Anhydrous calcium carbonate occurs in two crystalline forms, calcite (rhomboidal) and arago- connec tions have the same structure (Kugrens and West, 1973). Primary pit connec tions are nite (orthorhombic) (Fig. 4.7). The two forms differ formed as follows (Fig. 4.5) (Ramus, 1969): soon markedly in specific gravity, hardness, and solu- after nuclear divi sion, the cross wall grows bility. The Corallinales deposit CaCO primarily as 3 calcite, whereas the calcified members of the inward from the lateral wall. When the cross wall is complete, there remains a hole (aperture) Nemaliales deposit CaCO primarily as aragonite. 3 in the center through which the proto plasm of In Liagora (Fig. 4.17(a), (b)) (Nemaliales), the arago- the two cells is continu ous. A number of parallel nite occurs as needle-like crystals in the wall, whereas in the Corallinales, the calcite occurs vesicles traverse the hole, with electron-dense material condensing around the vesicles. Even - as massive deposits (Borowitzka et al., 1974). tually the vesicles dis appear, and the electron- Calcified walls of living cells probably have a dense material fills the hole. A membrane is mucilaginous component that slows the loss of 2 Ca into the medium (Pearse, 1972). If a calcified formed around this material, pro ducing a plug in the hole. The pit connec tion has been reported to thallus is killed, the dispersal of the calcified wall contain pro teins and polysacc harides (Pueschel is greatly accelerated.94 EVOLUTION OF THE CHLOROPLAST Fig. 4.7 The crystal structure of aragonite and calcite. Rhodoliths are unattached biogenic (pro- calcification ma y be linked to photo syn thesis duced from living organisms) nodules composed (Pearse, 1972). The most quoted theory on calcifi- at least partly of calcified red algae. A rhodolith cation is that calcium salts are pre cipitated from begins as a central nucleus composed of a pebble sea water by the alkalin ity brought about by the or fragment of coral. Non-articulated coralline extrac tion of carbon dioxide during photo syn - algae attach to the nucleus and grow. The shape thesis, calcium carbonate being less soluble in of the rhodolith is determined by its environ- alkaline waters than acid. The obvious and often ment, often being generally spherical because of men tioned drawback to this theory is that frequent overturning due to water motion. because all algae carry out photo syn thesis, it is Rhodoliths can reach 30 cm in diameter and be difficult to under stand why they do not all calcify. 500–800 years old. Sections of rhodoliths that Also the continued calcification of corallines in reveal the banding of the coralline red algae can the dark is another argu ment against this theory. be used to determine the environment at the time Seawater is more or less saturated with respect of wall deposition (Halfar et al., 2000). to calcium carbonate, and the addi tion of either Skeletons of coralline algae are formed with calcium or carbonate will cause the carbonate to 2 little biological control, by impregnation of cell pre cipitate. The concentra tion of CO is related 3 walls with magnesium and calcium at a ratio sim- through a complex series of equilibria (Digby, ilar to the Mg/Ca in the water. Therefore, the Mg/Ca 1977a,b): ratio in the cell walls reflects the Mg/Ca ratio in the    2    CO  H O H CO H  HCO 2H  CO    2 2 2 3 3 3 water. Analysis of the Mg/Ca ratio in cell walls of fossil coralline red algae since the beginning of the then Paleozoic Era have shown that there have been 2 2  CO  Ca CaCO (ppt.)  3 3 times of “aragonite seas” with relatively high Mg The addi tion of acid will drive the reac tions to in seawater, resulting in coralline algae with cells walls contain high-Mg calcite and aragonite, and theleft and cause carbonate to dis solve, whereas times of “calcite seas” with relatively low-Mg sea- the addi tion of base will drive the reac tions to the right and form more carbonate. At the pH of sea - water, resulting in coralline algae with low-Mg cal- water (8.4), almost all of the CO in the water is in cite (Fig. 4.8) (Stanley et al., 2002). The differences 2  in the Mg/Ca ratios in seawater are due to changes the form of bicarbonate ion, HCO . The addi tion 3 in the mid-ocean spreading rates. of one equivalent of hydroxyl ions to seaw ater sat- urated with respect to calcium carbonate will pre - The coralline algae thrive in rock pools and on cipitate one equivalent of calcium carbonate: rocky shores exposed to very strong wave action and swift tidal currents. The red algae that have 2    Ca  HCO  OH CaCO (ppt.) H O  3 3 2 the highest rates of calcification also have the highest rates of photo syn thesis and are usually The fact that seaw ater is nearly saturated with cal- found in waters less than 20 m deep (Goreau, cium carbonate was demonstrated with sea water 1963). Calcification of the thallus occurs about from the coast of Maine by Digby (1977a). By rais- two to three times more rapidly in the light than ing the pH of this seaw ater to 9.6, he caused precipita tion of carbonates. Calcium carbonate in the dark, although significant calcification does occur in the dark (Okazaki et al., 1970). The pre cipitated first, being less soluble, followed by above observa tions have led to the theory that carbonate richer in magnesium.RHODOPHYTA 95 Fig. 4.8 Effects of the Mg/Ca ratio of seawater on the mineralogy of carbonate deposition in coralline red algae. High Mg/Ca ratio in seawater results in the deposition of aragonite and calcite high in Mg, resulting in “aragonite seas.” Low Mg/Ca ratio in seawater results in the deposition of calcite low in Mg and “calcite seas.” (Modified from Stanley et al., 2002.) Digby (1977b) pro posed a theory of calcifica- It has been the or ized that calcification of red tion of red algae based on raising the pH of the algal thalli evolved as a pro tec tion against grazing sea water immedi ately outside the cells, causing by organi sms such as limpets, although it has also pre cipita tion of carbonates as out lined above. The been pointed out that grazing is beneficial to the first process is the normal photo syn thetic split- coralline algae in that the grazers remove epi - ting of water: phytes from the red algal thallus (Pueschel and Miller, 1996). 1   H O→ ⁄ 2O  2H  2e 2 2 The oxygen then diffuses out of the cell. As men - Secretory cells tioned above, in the sea most of the carbon diox- ide is in the form of bicarbonate ions; these ions diffuse into the cells and receive the elec trons Secretory cells (vesicular cells) occur in some freed initially by photo syn thesis. The bicarbonate Rhodophyceae (Fig. 4.9(a), (b)). These cells are col- ions are then converted into carbonate ions and orless at maturity and commonly have a large cen- hydro gen according to the following reac tion: tral vacuole. The secretory cells in Bonnemaisonia are prominent and associated with high concen-    2 2HCO  2e 2H  2CO  3 3 trations of iodine (Fig. 4.9(a)). The concentration of The carbonate ions diffuse out of the cell where iodine can be high enough to produce a blue color they partially dis sociate, forming bicarbonate and in herbarium paper with starch as a filler (the hydroxyl ions and thereby raising the pH: chemical test for starch). Secretory cells are vesti- gial, lacking the large vacuole with its refractile 2    2CO  H O 2HCO  2OH  3 2 3 contents, when these algae are grown in a When satura tion with regard to calcium and car- medium without bromine (Wolk, 1968). Bromine bonate is reached by a rise in pH outside the cells, can also occur as granular deposits in mucilage, calcium carbonate pre cipitates on the walls: such as in the thallus medulla of Thysanocladia densa (Pallaghy et al., 1983) or in the cuticle of 2 2 2Ca  2CO  2CaCO (ppt.) 3 3 Polysiphonia nigrescens (Peders’en et al., 1981). Continued pre cipita tion of CaCO results in the Other types of secretory cells not associated 3 calcified wall of the Rhodophyceae. Although the with the accumulation of halogens occur. The above theory explains the mechanism of calcifica- cells are often called secretory cells, even though tion, it does not explain why calcification is they are appar ently not involved in secre tion. specific to certain red algae. In Antithamnion (Figs. 4.9(b), 4.10(a)), these cells96 EVOLUTION OF THE CHLOROPLAST Fig. 4.9 (a) Vesicular cell of the Trailiella stage of Bonnemaisonia. (b) Vesicular cells of Antithamnion plumula. (c) Iridescent bodies in the vacuole of a cell of Chondria caerulescens. ((a) after Kylin, 1956; (b) after Kylin, 1930; (c) adapted from Feldmann, 1970a.) have a large central vacuole containing sulfated dif ferent causes by different investigators. acidic polysacc haride (Young and West, 1979). In Feldmann (1970a,b) found iridescent bodies in Opuntiella californica, there are “gland cells” with a Chondria (Fig. 4.9(c)) and Gastroclonium, whereas large vacuole containing a homo gene ous pro - Gerwick and Lang (1977) attrib uted the irides- teinaceous material (Young, 1979) (Fig. 4.10(b)). cence in Iridaea to a multi layer cuticle. These “secretory cells” and “gland cells” may have compounds that act as deterrents to grazing, or Epiphytes and parasites they may accumulate special reserves for meta- bolic use. Rhodophycean organ isms range from auto trophic, inde pendent plants to complete hetero trophic Iridescence parasites. The spectrum includes non-obligate epiph ytes (in the Acrochaetium–Rhodochorton com- The thalli of some Rhodophyceae show a marked plex), obligate epi phytes (Polysiphonia lanosa on blue or green iridescence when observed in Ascophyllum (Fig. 4.11)), semi parasites that have reflected light. Iridescence is solely a phys icalsome photo syn thetic pig ments (Choreocolax (Fig. inter fer ence and is not related to any light- 4.13), Gonimophyllum), and parasites with no color - producing phenomena such as phosphorescencea tion (Harveyella, Holmsella). or bio luminescence (Gerwick and Lang, 1977). It The associa tion between the obligate epi phyte results from the inter fer ence of light waves red alga P. lanosa and its brown alga host reflected from the surfaces of very thin multi ple Ascophyllum has been well studied. After the spore lamina tions separat ed by equally thin or thinner of P. lanosa germinates on the host, the red alga layers of material with a contrasting refractive sends down a rhizoid that digests its way into the index; the layers are uniform and pro duced by host tissue by means of enzymatic digestion of t he periodic secre tion and deposi tion. Iridescence host tissues. The enzymes are dis charged from vesi- in the Rhodophyceae has been attrib uted to cles at the tip of the rhizoid. Once the rhizoid hasRHODOPHYTA 97 (b) (a) Fig. 4.10 (a) Semidiagrammatic drawing of the fine Choreocolax polysiphoniae is an example of a structure of a vesicular cell of Antithamnion. The cell has a rhodophycean parasite (Fig. 4.12). The alga is a large central vacuole surrounded by protoplasm containing complete parasite and is inter esting in that it is rough endoplasmic reticulum (RER), mitochondria, parasitic on Polysiphonia fastigata, which is itself chloroplasts (C), and a nucleus (N). (b) Semidiagrammatic epi phytic on Ascophyllum (Fig. 4.11). Because drawing of the fine structure of a gland cell of Opuntiella Choreocolax is in the Gigartinales, and Polysi phonia californica. The cell has a large central vacuole containing is in the Ceramiales, this is a case of alloparasit - chloroplasts (C), a nucleus (N), and mitochondria. ((a) after Young and West, 1979; (b) after Young, 1979.) ism. Choreocolax consists of a more or less hemi - spher ical white external portion made up of sub dichotomously branched filaments enclosed established itself, intrusive cells form the basal and surrounded by gelatinous matter, and a mass parietal cells of the thallus (Fig. 4.11) (Rawlence, of haustorial cells growing inside the host (Sturch, 1972). Although P. lanosa is an obligate epi phyte, there is no trans fer of metabolites from the host to the epi phyte, the epi phyte manufacturing all of its own requirem ents through photo syn thesis (Harlin and Craigie, 1975; Turner and Evans, 1978). Parasitic red algae can be either adelphopara- sites (adelpho brother) or alloparasites (allo other). Adelphoparasites are closely related to, or belong to the same family as their hosts and constitute 90% of parasitic red algae (Goff et al., 1996). Alloparasites are not closely related to their hosts. The parasitic habit appar ently has been adapted more easily when the host is closely related to the parasite (adelphoparasites) than when it is not (alloparasites), partially because it Fig. 4.11 (a) The rhizoid of Polysiphonia lanosa penetrating is easier for the parasite to establish secondary pit tissue of Ascophyllum nodosum. (b) Polysiphonia epiphytic on connec tions with the host (and there fore trans fer Ascophyllum. ((a) after Rawlence, 1972.) nutrients) if the host and parasite are related.98 EVOLUTION OF THE CHLOROPLAST Fig. 4.12 Drawing of a section of Choreocolax polysiphoniae on Polysiphonia. The parasitic Choreocolax has carposporophytes in various stages of development. (After Sturch, 1926.) 1926). When the haustorial cells have reached a the host to the parasite where it is accumulated as certain distance from t he original point of infec - floridoside, mannitol, and starch (Fig. 4.4) (Evans tion, they frequently give rise to a second external et al., 1973). cushion. Secondary pit connec tions are estab- lished between the haustorial inter nal filaments Defense mechanisms of the red algae of the parasite and the larger cells of the host. Apically dividing filaments of the parasite Benthic marine red seaweeds are particularly sus- Choreocolax cells produce small conjunctor cells (Fig. 4.13) by the asymmetrical divi sion of a cell. A ceptible to being overgrown by epiphytes because conjunctor cell contains a highly condensed, small nucleus. The conjunctor cell fuses with an adjacent host Polysiphonia cell. The nucleus and cyto plasm of the conjunctor cell are incorporated into the host cell. The pit connec tion that origi- nally connected the conjunctor cell and the sister Choreocolax cell now connects the host Polysiphonia cell and the parasite. This is often called a “sec- ondary pit connec tion,” even though it is actually an ordinary pit connec tion. Up to several hundred Choreocolax cells can fuse with a single host cell. The infected host Polysiphonia cell enlarges and the vacuole decreases in size with a concomi- tant increase in cyto plasmic contents (Goff and Coleman, 1984). The chloro plasts become scattered through out the cyto plasm, instead of lying in the peripheral cyto plasm as they do in the Fig. 4.13 A drawing illustrating the progressive formation of non-in fected cells. Although the parasite cells are conjunctor cells by a filament of the parasitic red alga colorless, t hey do contain very reduced plastids Choreocolax living on a host Polysiphonia cell, leaving the pit connection of the conjunctor cell as a secondary pit (Kugrens and West, 1973). In the associa tion connection. (C) Conjunctor cell; (HN) Polysiphonia host between the colorless parasite Holmsella pachy- nucleus; (PN) Choreocolax parasite nucleus introduced into the derma and the host Gracilaria verrucosa, both of host cell after fusion with the conjunctor cell of the parasite; which are Rhodophyceae, the main product of (S) secondary pit connection. (After Goff and Coleman, 1984.) photo syn thesis, floridoside, is trans ferred fromRHODOPHYTA 99 they are sessile and are restricted to the photic zone resulted in the selection of epiphytic bacteria where conditions for fouling organisms are opti- that are relatively insensitive to these chemicals. mal. Epiphytes can significantly harm seaweeds by Corynebacterium-Arthrobacter 1 bacteria were rela- reducing the light, resulting in decreased photo- tively resistant to hydrogen peroxide whereas synthesis and growth, by increasing drag and hence Vibrio 1 and Flavobacterium 7 bacteria were sensi- their susceptibility to breakage or being torn from tive (Bouarab et al., 1999; Potin, et al., 1999). the substrate, and by decreasing the reproductive Volatile halocarbons, consisting of bromi- output of the host. nated, chlorinated or iodinated hydrocarbons, are Some red seaweeds secrete compounds that also produced on exposure of Gracilaria cells to the kill or retard the growth of epiphytes growing on oligosaccharide. These volatile hydrocarbons are them. Delisea secretes halogenated furones (Fig. electrophilic, attacking a variety of organic com- 4.14) that affect the growth of epiphytes and keep pounds and acting as natural biocides (pesti- the thallus clean (de Nys et al., 1995). cides). “White tip” disease of Gracilaria is due to Gracilaria conferta (Fig. 4.42) has a defense the release of these biocides in response to bacte- mechanism that limits bacterial infection of rial infection. The bleaching of the tips of the alga the red alga. Invasive bacteria secrete agarases is killing some of the algal cells while containing that break down the cell-wall agar of Gracilaria the pathogens at the site of attack (Largo et al., into shorter neoagarosehexaose oligosaccharides. 1995). Gracilaria cells respond to nanomolar concentra- tions of the oligosaccharides by increasing respi- Commercial utilization of red algal ration and producing active oxygen species such mucilages as hydrogen peroxide (H O ) and hydroxyl radicals 2 2  (OH ) (Potin et al., 1999). The hydrogen per oxide is The two most important polysacc harides derived degraded to water and molecular oxygen: from the Rhodophyceae are agar and carrageenan. 1 H O → H O ⁄ 2O 2 2 2 2 Agar is defined pharmaceutically as a phycocol- Molecular oxygen is toxic and results in the elim- loid of red algal origin that is insoluble in cold water but readily soluble in hot water; a 1.5% ination of 90% of the epiphytes within 15 minutes under experimental conditions (Weinberger and solution is clear and f orms a solid and elastic Friedlander, 2000). Gracilaria conferta has also gel on cooling to 32 to 39 °C, not dis solving again been shown to release activated oxygen each at a temperature below 85 °C. Agar is composed of two poly saccharides, agarose (Fig. 1.11) and morning after exposure to light. This short time release of activated oxygen, in addition to the agaropectin (Lahaye, 2001). defense related release of hydrogen peroxide, Agar is obtained commercially from species of Gelidium (Figs. 4.40, 4.41) and Pterocladia as well as from various other algae, such as Acanthopeltis, Ahnfeltia, and Gracilaria (Fig. 4.42) (Melo, 1998; Mollet et al., 1998). These algae are often loosely referred to as agarophytes. Commercial produc- tion of agar was a world monopoly of the Japanese for many years, and even in 1939 Japan was still the major pro ducer. Wartime demands in areas deprived of Japanese agar led to the develop ment of agar industries in many of the Fig. 4.14 Left: The chemical structure of furan, the basic Allied countries, some of which have continued building block of the furanones. Right: One of the and prospered while others have declined or halogenated furanones released by the red alga Delisea disappeared. The agarophytes are collected by pulchra. Halogenated furanones inhibit the growth of diving, dragging, or raking them offshore at low epiphytes on this red alga. tide. In the trad itional pro cessing pro cedure the100 EVOLUTION OF THE CHLOROPLAST Fig. 4.15 The chemical structures of the different types of Carrageenan (Fig. 4.15) is a phycocolloid similar carrageenans that occur in the red algae. to agar but with a higher ash content and requir- ing higher concentra tions to form gels. It is com- plants are then cleaned and bleached in the sun, posed of varying amounts of the principal with several washings in fresh water used to facil- components, -carrageenan and -carrageenans, itate bleaching. The material is boiled for several both negatively charged high-molecular-weight hours, and the extract is acidified. This extract is poly mers (Chiovitti et al., 1995; Therkelsen, 1993). then frozen and thawed. On thawing, water flows -Carrageenan is distrib uted throughout the wall from the agar, carrying impur ities with it. The while -carrageenan is local ized to the cuticle agar that remains is dried and marketed as flakes (Vreeland et al., 1992). -carrageenan pre cipitates or cakes. The more modern method extracts the selectively from a cold, dilute solution in the agar under pressure in auto claves. The agar is presence of potassium ions. It forms a gel when decolorized and deodorized with activated char- heated and cooled with potassium ions and is coal, filtered under pressure, and evaporated therefore the gelling component. -Carrageenan is under reduced pressure. Further purification by the non-gelling component and is not precipitated freezing is then undertak en. or gelled by potassium. -Carrageenan contains The greates t use of agar is in associa tion with galactose-2,6-disulfate, whereas -carrageenan con- food prepara tion and technology, and in the phar- tains 3,6-anhydro-D-galactose. It has been shown in maceutical industry. It is used for gelling and Chondrus crispus and Gigartina stellata that the pro - thick ening purposes, particularly in the canningpor tion of - and - carrageenan in the cell wall of fish and meat, reducing the unde sirable ef fects varies according to the ploidy of the plant. In the of the can and pro viding some pro tec tion againsttetra sporophyte the amount of -carrageenan shaking of the product in transit. It is also used in present is high as com pared with the amount of the manufacture of pro cessed cheese, mayon- -carrageenan, whereas just the opposite is true in naise, puddings, creams, and jellies. Pharma ceuti - the gametophyte (Chen et al., 1973). Such results cally agar is used as a laxative, but more may prove valuable in determining the ploidy of frequently it serves as an inert carrier for drug Rhodophyceae that have unknown life cycles. products where slow release of the drug is Carrageenan is usually obtained from wild required, as a stabilizer for emul sions, and as a popula tions of Irish moss, the name for a mix - constitu ent of cosmetic skin prepara tions, oint- ture of Chondrus crispus and the various species of ments, and lotions. The use of agar as a stiffening Gigartina, particularly G. stellata. In the Philippines, agent for growth media in bacteriology and Eucheuma, and in Vietnam and India, Kappophycus mycology, which was its main use almost a cen- (Fig. 4.16) are extensively cultivated as a source tury ago, is still responsible for a very consid er - of carrageenan (Reddy et al., 2003). Commercial able part of the demand. extrac tion is similar to that for agar althoughRHODOPHYTA 101 Fig. 4.16 Cultivation of the carrageenan-containing the carrageenan binding to a loop on the HIV mol- Kappophycus alvarezii in an offshore area (left) and a shrimp ecule. A carrageenan-based vaginal microbicide pond (right) in Vietnam. (From Ohno et al., 1996.) called Carraguard® has been shown to block HIV and other sexually transmitted diseases in vitro. carrageenan cannot be purified by freezing. The Carraguard has entered clinical trials involving 600 dried alga is washed with fresh water to reduce the non-pregnant, HIV-negative women in South Africa salt content and then boiled with 2 to 4 parts of and Botswana (Spieler, 2002; Smit, 2004). alga to 100 parts of water. The soluble carrageenan is separ ated from the insoluble residue in a cen- Reproductive structures trifuge. Following filtration and some evapora tion under vacuum, the carrageenan is dried on a rotary drier. The Rhodophyceae have no flagellated cells or Carrageenans are used extensively for many of cells with any vestigial structure of flagellation, such as basal bodies. In sexual reproduction, sper- the same purposes as agar; however, because of their lower gel strength, carrageenans are used matia are produced which are carried passively by less for stiffening purposes than is agar, although water currents to the female organ, the carpogo- for stabiliza tion of emul sions in paints, cosmet- nium (Figs. 4.17(a), 4.18). The fertilized carpogo- nium produces gonimoblast filaments that form ics, and other pharmaceutical prepara tions car- rageenans are pre ferred to agar. Also, for the carposporangia and diploid carpospores (Fig. stiffening of milk and dairy products, such as ice 4.17(b)). The carpospores produce the diploid cream, carrageenans have supplanted agar com- tetrasporophyte which subsequently gives rise to haploid tetraspores. Advanced red algae form pletely in recent years, and it is in this area that demands for these products are the greates t. One chiefly tetrahedral tetrasporangia (Fig. 4.17(d)) particular use is for instant puddings, sauces, and with large spores, whereas less advanced groups creams, made possible by the gelling action, generally form cruciate or zonate tetrasporangia (Fig. 4.17(d), (e)) with smaller spores (Ngan and which does not require refrigera tion. Carrageenans inhibit human immunodefi- Price, 1979). Tetraspores are generally larger than ciencyvirus(HIV)replica tionandreversetrans - carpospores. The tetraspores complete the life criptionase in vitro (in the test tube) (Bourgougnon cycle by germinating to form the gametophyte. Although this is the general life cycle of most et al., 1996). Replication of the HIV virus depends on inter ac tionofaglycoproteinontheHIVvirusenve- Rhodophyceae, there are a number of modifica- lope with a receptor on the target cells in the tions of it. human body. The sulfated carrageenans prevent The postfertiliza tion events vary from one order to another. The more advanced orders attach mentoftheHIVvirustothetargetcells.This  occurs by the stronger negative R-O-SO groups on have auxiliary cells with which the fertilized 3102 EVOLUTION OF THE CHLOROPLAST Fig. 4.17 (a) A filament of Liagora viscida with a carpogonial branch. (b) Gonimoblast filaments of L. viscida with carpospores. (c) Aspermatangial branch of Acrochaetium corymbiferum with spermatangia and spermatangial mother cells. (d) Tetrahedral and cruciate tetrasporangia of Nemas - toma laingii. (e) Zonate tetraspor - angia of Hypnea musciformis. (f) Polysporangium of Pleonosporium vancouverianum. (g) Monosporangia of Kylinia rhipidandra. ((a), (b), (c), (e) after Kylin, 1930; (f) after Kylin, 1924; (g) after Kylin, 1928.) carpogonium fuses to form a multi nucleate moblast filaments, the pit connec tions between fusion cell. Papenfuss (1966) recognizes two types the older gonimoblast cells usually dis solve of auxiliary cells, nutritive and generativ e. (Kugrens and West, 1972a, 1973, 1974). Nutritive auxiliary cells provide nutrients for the developing carposporophyte, whereas generative Carpogonium auxiliary cells give rise to gonimoblast filaments The female organ, or carpogonium, consists of a (Figs. 4.18, 4.33, 4.44). The diploid tissue formed dilated basal portion and a usually narrow gelati- from the fertilized carpogonium forms the nous elongate tip, the trichogyne,which receives gonimoblast filaments. The gonimoblast fila- the malecells (Figs. 4.6(a), 4.10). Usually there are ments produce terminal carposporangia, whichtwonucleiinacarpogonium,oneinthetri cho - in turn form the carpospores. The carposporangiagyne,whichdegener atessoonafterthecarpogo- enlarge consid er ably during their matura tion nium matures, and one in the basal part of the because of the develop ment of the chloro plastscarpogonium,whichfunc tionsasthefemale and the vesicles containing wall pre cursors. The gamate nucleus. In most Rhodophyceae the car- pit connec tion between the carposporangium and pogonium terminates a short, often branched, the gonimoblast breaks before release of the car- three- to four-celled lateral called the carpogonial pospore. Also during the develop ment of the goni- branch. The cell from which the carpogonialRHODOPHYTA 103 Fig. 4.18 Simplified life cycle of a typical red alga. branch arises is the supporting cell. The carpogo- and make up half the volume of the sper- nium and carpogonial branch are commonly color- matangium. Subsequently the vacuoles fuse to less, although in some Nemaliales this is not true. form one large vacuole. The spermatium is released by the gelatiniza tion of the spermatan- gial wall near the apex and the concurrent release Spermatium The spermatia of the Rhodophyceae are spher ical of the fibrous material in the basal vacuole. The or oblong cells pro duced in spermatangia, a fibrous material pre sum ably swells and pushes single spermatium being formed in a sper- the spermatium out of the spermatangium (Fig. matangium and then released, leaving the empty 4.19). The fibrous material is sticky, and some of it sporangium (Fig. 4.19). The spermatangia (Fig. adheres to the spermatium, thereby facilitating 4.22) are formed on spermatangial mother cells attach ment to the tri chogyne (Fig. 4.22(c)). During (Fig. 4.17(c)). The young spermatangia frequently the develop ment of the spermatium the pit have a pro nounced polar orienta tion, with the connec tion with the spermatium mother cell is nucleus in the apical portion and one or more vac- severed. The mature spermatium is unin ucleate, uoles in the basal portion (Scott and Dixon, and wall-less, but surrounded by mucilage, and 1973a). As the spermatangium ages, vacuoles may (Simon-Bichard-Bréaud, 1971; Peyrière, 1971) form in the basal area. These vacuoles contain or may not (Kugrens and West, 1972a; Kugrens, fibrous material (probably mucopolysaccharides) 1974) contain func tional chloro plasts.104 EVOLUTION OF THE CHLOROPLAST Fig. 4.19 A semidiagrammatic drawing of the formation of the spermatium in the Rhodophyceae. (a) Young spermatium. (b) Formation of vacuoles containing fibrous material. (c) Fusion of vacuoles, breaking of the pit connection, and gelatinization of the wall of the spermatangium. (d) Extrusion of mucilage and release of the spermatium. (Adapted from Scott and Dixon, 1973a; Kugrens, 1974.) Fertilization occurred, the trichogyne becomes separated at its The spermatium usually is carried passively by base from the rest of the carpogonium by the pro- water currents to the tri chogyne of the carpogo- gressive thickening of the cell wall. nium, although some spermatia can glide in a There is a relatively low statistical probability manner similar to the gliding in Porphyridium. that the non-motile spermatia will be carried to Actin filaments in the spermatium and carpogo- receptive trichogynes of carpogonia. Some species nium are involved in the subsequent steps have appendages on the spermatia that extend (Fig. 4.20) (Kim and Kim, 1999; Pickett-Heaps et al., the reach of the spermatia five- to tenfold result- 2001). The wall of the spermatium and that of the ing in a better chance of attaching to a recep- carpogonium dissolve, the male nucleus divides, tive carpogonium. The appendages are initially and the male nuclei move into the carpogonium. contained within vesicles within the spermangia Fusion of one male nucleus and the carpogonial and unfold when the spermatia are released (Fig. nucleus occurs in the basal portion of the car- 4.22). The appendages increase the surface area pogonium. Fertilization stimulates the produc- of the spermatium more than 30-fold, increasing tion of polyamine spermine (Fig. 4.21) which steers the likelihood of interaction with a trichogyne of the carpogonial branch toward the production of a carpogonium. Moieties of the sugar mannose carpospores (Sacramento et al., 2004). The trichog- cover the surface of the appendages. The surface yne will usually continue to grow until contact is of the trichogyne is covered with the lectin made with a spermatium. After fertilization has concanavalin A which binds the mannose

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