TAXA OF LIFE
PHYLUM CHAROPHYTA

EUKARYA>ARCHAEPLASTIDA>VIRIDIPLANTAE>STREPTOBIONTA>CHAROPHYTA

Charophyta (ka-RO-fa-ta) is derived from two Greek roots that mean joy (khara -χαρά); and plant (phyto -φυτό).  The reference is the the plant, Chara, after which the phylum was named, is the "joy of the water."

INTRODUCTION TO THE CHAROPHYTA

This phylum embraces all of the Streptophyte algae and almost certainly is paraphyletic.  The diversity in form and size is comparable to that of the Chlorophyta and exceeds that of any of the bryophyte and vascular plant phyla.  Characters that unite them include:

They range from motile unicells (Figure A) to colonial forms (Figures B&C), and filaments (Figure D).  The desmids (Figure E) and filamentous zygnemataleans like Spirogyra (Figure F) have lost flagellated stages, but are among the most successful freshwater groups.  Desmids are especially abundant in soft waters.  Plants like Chara and Coleochaete are quite complex, and, although haplontic in their life cycles, provide an intriguing model for the types of organisms that gave rise to the bryophytes and vascular plants.

Members of the class Mesostigmatophyceae resemble the Praesinophyta very much.  Mesostigma (Figure A) looks like a praesinophyte.  Aside from being motile unicells, they have a "wall" made of overlapping diamond-shaped scales.  Furthermore, they have laterally-inserted flagella that emerge from a crypt.  The cell has a single cup-shaped chloroplast with an eyespot in it.  On the other hand, Chaetosphaeridium (Figure B) is an attached alga often growing in groups bound by a common mucilage (filament-like).  Each cell has a prominent bristle.  They have a layer of cellulosic scales both on the cell and flagella.  Like Mesostigma, they have a cup-shaped chloroplast; however, they do not have an eyespot.

Chlorokybus (Figure C), the sole genus in the Chlorokybophyceae, is nonmotile and sarcinoid (packets of cells that develop within persistent gelatinized cell wall of the parent cell).  However, it shows its affinities with the charophytes when it produces motile cells.  The motile cells are biflagellate with the flagella inserted laterally from a groove (like a praesinophyte).  Zoospores are covered by scales, and flagella have hairs. 

Klebsormidium (Figure D) is an unbranched filament of the Klebshormidiophyceae.  It was once considered to be a relative of Ulothrix (in the Chlorophyta), but it is now known that the resemblance (unbranched filaments with parietal plate chloroplasts) is only superficial.  This alga often grows in dense mats in streams impacted by Acid Mine Drainage. The zoospores resemble motile cells of Chlorokybus.  

The Zygnemataceae has two very different groups: desmids, and the zygnematalians.  This class is characterized by the absence of motility in any stage (no zoospores or motile gametes).  The desmids look like paired cells, most of which have two semicells connected by an isthmus, which houses the nucleus.  Almost all of the desmids have a chloroplast, each with one or more large pyrenoids, in each semicell.  Cosmarium (Figure E) is one of the most common desmid genera.  These organisms are most common in still soft water, where they can be among the dominants.  A local soft water pond has a reliable bloom of a tiny Cosmarium species during the cool months.  I have documented them in bloom condition at over 20,000 cells per ml.  At cytokinesis, desmids separate at the center so that each daughter cell gets half of the parent wall.  The Cosmarium cell in Figure E had divided recently such that the left semicell was from the parent cell and the right semicell was in the act of expansion.  During sexual reproduction, reproductively compatible cells pair and form a conjugation tube.  Fusion of the nuclei and formation of the zygospore typically occurs in the conjugation tube.  The zygospore is the resting spore, which, upon germination, releases one or more haploid vegetative cells (i.e. zygotic meiosis).

The zygnematalians are unbranched filaments with distinctive chloroplast types (stars, plates, and spiraled ribbons).  These are decidedly slimy and common in many different types of freshwater environments (usually calm water).  Many of the taxa increase in abundance when acid sensitive waters experience acid rain.  Spirogyra (Figure F) is a very common genus that has one or more parietal ribbon-like chloroplasts that wind in a spiral down the cell.  They reproduce vegetatively by fragmentation and sexually by conjugation.  In conjugation all members of this order align compatible filaments and develop conjugation tubes.  Zygospores might develop in the conjugation tube, but more likely they develop in cells of the filament of one of the mating types.  The type of conjugation tube, placement of the zygospore, and the appearance of the zygospore are all important in keying these to species.

Chara (Figure G), the joy of the water, is a member of a class (Charophyceae) that contains macroscopic, multicellular taxa. They have internodes composed of single, large axial cells with whorls of branches at the nodes.  In Chara, the nodal branches lie appressed to the large axial cell making a fluted, corticated stem, which may be heavily calcified.  Growth takes place from an apical cell.  They undergo oogamous sexual reproduction by flagellated antherozoids (motile cells that resemble those of the bryophytes and hepatophytes) in spherical antheridia and eggs in complex oogonia that bear a striking resemblance to archegonia.  Zygotes develop into small protonemata that, in turn, produce the upright, gamete-bearing gametophyte. There is no asexual reproduction.  Some species of Chara can dominate the benthic macrophyte community in local areas.  One in particular, C. foetida, lives up to its name and imparts quite a stench to the water.  Charphytes have been members of the freshwater macrophyte community for some time.  I collected numerous fossil charophyte oogonia from the Baum limestone, a freshwater lake deposit, of central Oklahoma.

Coleochaetae (Figure H; in the Coleochaetophyceae) is an attached flat plate of cells that grows as an appressed, branched network. They form upright oogonia sheathed by sterile cells and spermatozoids formed in antheridia.  They do exhibit asexual reproduction by means of zoospore production.  Although the charophyceae look more similar to the bryophytes, Graham (1985) presents convincing evidence for a Coleochaete-like ancestor to the land plants.

SYSTEMATICS OF THE CHAROPHYTA

Older taxonomic systems of the algae (e.g. Smith 1950) place all of the green algae into a single group.  A body of ultrastructural evidence began to accrue (summarized by Pickett-Heaps 1975; and Mattox and Stewart 1984) that supported the occurrence of a group of green algae that had characters in common with the land plants (i.e. phragmoplast, cell plate, acentric and open mitosis).  Also, their motile cells usually had a multilayered structure (MLS) and laterally-inserted flagella.  Indeed, Graham (1985) presents convincing evidence for a Coleochaete-like ancestor to the land plants.  However, this group spans the range of characters that connect it to the Praesinophyta and the Non-Vascular EmbryophytesEven otherwise classical taxonomic systems like Bold and Wynne (1985) separated the Charales and Coleochaetales from the other green algae as a consequence of the ultrastructural and early molecular work.  One of the early surprises was that the Ulotrichales, an order of morphologically well-defined taxa, was paraphyletic and the unbranched filaments of Ulothrix (a chlorophyte) and Klebshormidium (a charophyte) only superficially resemble each other (Floyd et al. 1972b; Marchant et al. 1973).

Although Pickett-Heaps (1975) suspected that the zygnematalian algae had affinities with the the charophytes, the definitive characters from the motile cells were absent (the zygnematalians do not have motile cells at any stage; Baldauf and Palmer, 1990; and Surek et al., 1994).  Margulis and Schwartz (1988 and 1998) separate the desmids and zygnematales (Gamophyta, Pr-14 and Pr-26, respectively) from the other green algae (Chlorophyta, Pr-15 and Pr-25, respectively) because the "gamophytes" have no motility and reproduce by conjugation. Hoshaw et al. (1990) consider the conjugatophytes to be members of the green algae even though their editors separate the conjugatophytes from the green algae. Mattox and Stewart (1984) indicate that there are so many similarities between the "gamophytes" and the charalian greens that a more parsimonious view would be that the "gamophytes" lost their flagellar apparatus. I agree that the gamophytes should be considered green algae but separate them into their own class of charophytes.

Studies of Chlorokybus (Lokhorst et al. 1988) and Mesostigma (Sym and Pienaar 1993) suggested that they, too, had affinities with the charophytes.  Curiously, they also had sets of characters in common with the praesinophytes (laterally-inserted flagella in a groove, some with cellular scales).  In fact, some of the praesinophytes had a MLS, which suggests that the structure is primitive.  Marin and Melkonian (1999) in their examination of these taxa, showed convincingly that Mesostigma and Chaetosphaeridium grouped together in a clade that they interpreted as a class (Mesostigmatophyceae) distinct from the class Chlorokybophyceae.

mesostigma_bgw-MBL.jpg (14600 bytes)

A. Mesostigma shares many features in common with the prasenophytes, among those are the laterally-inserted flagella as illustrated here.

chaetosphaeridium-UMD.jpg (137807 bytes)

B. Chaetosphaeridium is an attached alga often growing in groups bound by a common mucilage.  Note the prominent bristle.

chlorokybus-umd.jpg (88466 bytes)

C. Chlorokybus is a coccoid organism whose motile cells identify it as a streptophyte alga.

Klebsormidium-umd.jpg (16536 bytes)

D. Klebsormidium once considered to be a relative of Ulothrix is now known that the resemblance is only superficial.  This alga often grows in dense mats in streams impacted by Acid Mine Drainage. 

cosmarium (400x).jpg (585081 bytes)

E. Cosmarium is one of the most common desmids, most of which have a characteristic incised appearance with the nucleus occupying the isthmus.  This cell recently divided and the right semicell is expanding until it will mirror the left side.

Spirogyra.jpg (6757 bytes)

F. Spirogyra is an unbranched filamentous organism that is related to the desmids.  It has characteristic spiraled parietal chloroplasts.

chara_zeylanica-ULB.gif (58633 bytes)

G. Chara produces plants that are as big as and as structurally complex as some of the vascular plants.  Illustrated is an oogonium (the oblong structure) and an antheridium (the spherical structure).

coleochaete-ASU.jpg (26541 bytes)

H. Coleochaetae is an attached flat plate of cells.  The dark spheres are zygotes contained within the oogonia.

Images taken from:
A: http://microscope.mbl.edu/baypaul/microscope/images/t_imgAZ/mesostigma_bgw.jpg
B-D: http://www.life.umd.edu/labs/delwiche/Strp/
E-F: The Systematic Biology Biodiversity Collection
G:
http://bib18.ulb.ac.be/Botanique_I/image/210168992005_chara_zeylanica.gif
H:
http://lifesciences.asu.edu/plb598/coleochaete.JPG

SYNOPTIC DESCRIPTION OF THE CHAROPHYTA

The following description comes from Pickett-Heaps (1975), Hoshaw et al. (1990), van den Hoek et al. (1995) and Graham and Wilcox (2000)

I. SYNONYMS: Stoneworts, brittleworts.

II. NUMBER: >300 species.

III. PHYLUM CHARACTERISTICS:

A. Structure and Physiology

Cell Form: unicells, sarcinoid colonies, filaments, pseudoparenchymatous, some with corticated filaments.

Flagella: A pair of subapical flagella, covered with scales and laterally inserted, some without flagella in any stage.

Basal Bodies: Basal bodies perpendicular, usually associated with a multilayered structure.

Cell Covering: A wall of cellulose; some with cellulosic scales.

Chloroplasts: Grass green with chlorophylls a and b, B-carotene and various xanthophylls. 

Food Reserves: True starch that is deposited within the chloroplast in association with a pyrenoid.

Mitochondria: Plate-like cristae.

Golgi: Present.

Nucleus: Haploid in vegetative forms.

Centrioles: Absent.

Inclusions and Ejectile Organelles: Not present.

B. Mitosis, Meiosis and Life History

Mitosis: Variable, open to closed; phragmoplast (in most); cytokinesis by cell plate formation.

Meiosis: Present.

Sexual Reproduction and Life History: Isogamy to oogamy. Some of the charophytes grow from a protonema.

C. Ecology: Mainly found in fresh water.

HIERARCHICAL CLASSIFICATION OF THE CHAROPHYTA

This system is a modification of van den Hoek et al. (1995) and Graham and Wilcox (2000).  This system has 6 classes and more than 300 species.

CLASS MESOSTIGMATOPHYCEAE

A group of motile or filamentous taxa.  Motile cells with layers of scales.  Chloroplast with or without eyespots.  The class has 2 orders.

ORDER MESOSTIGMATALES

Unicellular and motile; flagella inserted laterally in a crypt.  Chloroplast cup-shaped with an eyespot in it.  Cells covered by naviculoid scales.

Mesostigma.

ORDER CHAETOSPHAERIDALES

Filamentous; motile cells with 1 layer of scales on surface and flagella.  Chloroplast without eyespot.

Chaetosphaeridium.

CLASS CHLOROKYBOPHYCEAE

A clade of a single genus.  The organism is nonmotile and sarcinoid (packets of cells that develop within persistent cell wall of the parent cell).  The motile cells are biflagellate with the flagella inserted laterally from a groove (like a praesinophyte).  Zoospores are covered by scales flagella with hairs.  

ORDER CHLOROKYBALES

Chlorokybus.

CLASS KLEBSHORMIDIOPHYCEAE

Unbranched filaments with parietal plate chloroplasts, superficially resembling members of the Ulotrichales.  The zoospores resemble motile cells of Chlorokybus.  

ORDER KLEBSHORMIDIALES

Klebshormidium.

CLASS ZYGNEMATOPHYCEAE = CONJUGATOPSIDA (GAMOPHYTA OF MARGULIS AND SCHWARTZ 1998)

Filamentous or unicellular; reproduction involving conjugation between 2 cells; no flagellated stages; haploid, with zygotic meiosis; all fresh water. This class has 2 orders.

ORDER COSMARIALES (DESMIDIALES)

Variously shaped unicells; usually 2 chloroplasts with nucleus sited between them; often with a narrow isthmus; mobility by mucilage secretion. "Desmids."

Cosmarium, Micrasterias, Staurastrum, Hyalotheca, Desmidium, Closterium, Mesotaenium, Spirotaenia, Cylindrocystis, Netrium.

ORDER ZYGNEMATALES

Unbranched, filamentous; varied forms of chloroplasts; cell wall usually slimy; conjugation results in resistant zygospore.

Zygnema, Spirogyra, Mougeotia.

CLASS CHAROPHYCEAE

Macroscopic; composed of very large cells forming rhizoids and stems with whorls of branches at nodes; growth takes place from an apical cell; cell walls may be heavily calcified; sexual reproduction by flagellated antherozoids and oogonia in complex oogonium; no zoospores.  Zygotes develop into small protonemata that, in turn, produce the upright, gamete-bearing gametophyte. 

ORDER CHARALES.

Chara, Nitella, Nitellopsis, Tolypella.

CLASS COLEOCHAETOPHYCEAE

Prostrate, pseudoparenchymatous thallus with sheathed reproduction; oogonia protected by sterile cells; asexual reproduction by zoospores.

ORDER COLEOCHAETALES.

Coleochaete.

LITERATURE CITED

Baldauf, S. L. and J. D. Palmer. 1990. Evolutionary transfer of the chloroplast tufA gene to the nucleus. Nature. 344: 262-265. 

Bold, H. C. and M. J. Wynne. 1985. Introduction to the Algae. 2nd Edition. Prentice-Hall, Inc. Englewood Cliffs. NJ. 

Floyd, G. L., K. D. Stewart, and K. R. Mattox. 1972b. Cellular organization, mitosis, and cytokinesis in the ulotrichalean alga, Klebshormidium. Journal of Phycology. 8: 170-184.

Graham, L. E. 1985. The origin of the life cycle of land plants. American Scientist 73: 178-186. 

Graham, L. E. 1990. Charophyceae (Orders Chlorokybales, Klebsormidiales, Coleochaetales). In: Margulis, L., J.O. Corliss, M. Melkonian, and D.J. Chapman, eds. 1990. Handbook of the Protoctista; the structure, cultivation, habits and life histories of the eukaryotic microorganisms and their descendants exclusive of animals, plants and fungi. Jones and Bartlett Publishers. Boston. pp. 636-640. 

Graham, L. E., and L. W. Wilcox. 2000. Algae. Prentice Hall, Upper Saddle River, NJ.

Hoshaw, R. W., R. M. McCourt, and J. C. Wang. 1990. Conjugaphyta. In: Margulis, L., J.O. Corliss, M. Melkonian, and D.J. Chapman, eds. 1990. Handbook of the Protoctista; the structure, cultivation, habits and life histories of the eukaryotic microorganisms and their descendants exclusive of animals, plants and fungi. Jones and Bartlett Publishers. Boston. pp. 119-133.

Lokhorst, G. M., H. J. Sluiman, and W. Star. 1988. The ultrastructure of mitosis and cytokinesis in the sarcinoid Chlorokybus atmophyticus (Chlorophyta, Charophyceae) revealed by rapid freeze fixation and freeze substitution. Journal of Phycology. 24: 237-248. 

Marchant, H.J., J.D. Pickett-Heapes, and K. Jacobs. 1973. An ultrastructural study of zoosporogenesis and the mature zoospore of Klebshormidium flaccidum. Cytobios. 8:95-107.

Margulis, L. and K. Schwartz. 1988. Five kingdoms, an illustrated guide to the phyla of life on earth. 2nd Edition. W.H. Freeman and Co.  New York. 

Margulis, L. and K. Schwartz. 1998. Five kingdoms, an illustrated guide to the phyla of life on earth. 3rd Edition. W. H. Freeman and Company.  New York. 

Marin, B. and M. Melkonian. 1999. Mesostigmatophyceae, a new class of streptophyte green algae revealed by SSU rRNA sequence comparisons. Protist. 150: 399-417. 

Mattox, K. R. and K. D. Stewart. 1984. Classification of the green algae: a concept based on comparative cytology. In:  Irvine  , D. E. G. and D. M. John, eds. Systematics of the Green Algae. Academic Press. London. pp. 29-72.

Pickett-Heaps, J. D. 1975. Green Algae: Structure, Reproduction and Evolution in Selected Genera. Sinauer Associates, Inc. Sunderland , Massachusetts .

Pickett-Heaps, J. D. and H. J. Marchant. 1972. The phylogeny of the green algae: a new proposal. Cytobios. 6:255-264.

Smith, G. M. 1950. The fresh-water algae of the United States . McGraw-Hill Book Co. New York

Surek, B., U. Beemelmanns, M. Melkonian, and D. Bhattacharya. 1994. Ribosomal RNA sequence comparisons demonstrate an evolutionary relationship between Zygnematales and Charophytes. Pl. Syst. Evol., 191: 171-81.

Sym, S. D. and R. N. Pienaar. 1993. The Class Praesinophyceae. In: F. E. Round and D. J. Chapman, eds. Progress in Phycological Research. 9: 281-376.

Van den Hoek, C., D. G. Mann, and H. M. Jahns. 1995. Algae, An Introduction to Phycology. Cambridge University Press.  Cambridge.

By Jack R. Holt.  Last revised: 03/21/2010