The anthocerote chloroplast: a review

Abstract

SUMMARY This review covers previous data, together with new information from our laboratories, on the subject of the anthocerote chloroplast. Unlike all other archegoniates, most species of anthocerote have pyrenoids in their chloroplasts. The pyrenoid is the site of accumulation of the first enzyme in the C3 photosynthetic cycle, ribulose bispbosphate carboxylase/oxygenase. Unlike most algae, the hornwort pyrenoid is composed of distinct subunits, numbering up to several hundred. Pyrenoid morphology is quite variable among the genera in shape, fine structure, and distribution of inclusions. Another unique feature of the anthocerote chloroplast is the presence of thylakoids that connect adjacent granal stacks at right angles to the long axis of the granum (so‐called channel thylakoids), resulting in a 'spongy’arrangement of the thylakoid system. The granal stacks of anthocerotes are like the‘pseudograna’of green algae because they lack the highly‐curved end membranes typical of all other embryophytes. The channel thylakoids are enriched in photosystem (PS) I and the grana are enriched in PS II. The chloroplast envelope is a double membrane structure with regions of appression, much like that of other green plants. The apieal cell of the gametophyte contains chloroplasts similar to the mature chloroplasts of the thallus, although certain gametophytic tissues may contain underdeveloped plastids. Chloroplasts in cells around Nostoc colonies and in cells invaded by mycorrhizal fungi have thylakoids mainly in pairs, and small or absent pyrenoids. A number of similarly reduced plastids are noted in the placental cells at the sporophyte/gametophyte junction and in developing spores. The greatest reduction is observed in spermatid cell plastids, which at maturity consist of only a small starch grain surrounded by the envelope. Chromoplast‐like organelles are found in the cells of the antheridial jacket in some genera; these contain numerous osmiophilic globules that are probably pigment aggregations. Colourless bead‐like plastids occur in the rhizoids; these seem to develop by fragmentation of the single chloroplast in the rhizoid initials, concomitant with the loss of chlorophyll. Chloroplast division is a tightly controlled process and, in uniplastidic species, always occurs just before nuclear division, with the participation of a unique system of chloroplast‐associated microtubules. The number of chloroplasts per cell is quite variable in some genera, although most species have but a single chloroplast in each cell of the gametophyte. Chloroplast shape is also variable from ellipsoidal, dumbbell‐shaped, to irregular. These data indicate that the anthocerote chloroplast is unique among the embryophytes and are in line with the notion of an isolated position in the plant kingdom. Certain features of chloroplast morphology appear to be typical of certain genera and might prove useful in taxonomic decisions at the generic level.

Phylotranscriptomic analysis of the origin and early diversification of land plants

“…The placement of hornworts and a moss+liverwort clade as successively sister to vascular plants is consistent with analyses based on morphological and developmental characters (78,79), including dextral sperm in hornworts rather than sinistral sperm, as in all other land plants, and the retention of the pyrenoid, a plastid structure that is the site of RUBISCO localization, shared by hornworts and streptophytic algae (reviewed in ref. 80). The possibility that some of these trait mappings are the product of evolutionary convergence should also be considered, and seems likely in the case of the pyrenoid (81).…”

The role of carbonic anhydrase in photosynthesis and the activity of the carbon‐concentrating‐mechanism in bryophytes of the class Anthocerotae

“…Additionally, the pyrenoid, a starch-coated structure containing Rubisco (Vaughn et al, 1992) present in the chloroplast of many microalgae and some Anthocerotae, might play a functional role, being directly analogous with the cyanobacterial carboxysome, or providing a means of separating oxygenic PSII from Rubisco. Alternatively, the pyrenoid might provide tight packaging of Rubisco fuelled by CO # from the intrathylakoid CA which would enhance the CO # :O # ratio at Rubisco.…”

“…Further physiological investigation of members of the Anthocerotae which lack a pyrenoid and in some cases are multiplastidic (Vaughn et al, 1992), is likely to contribute to the elucidation of the precise role of the pyrenoid in the functioning of the CCM. As yet these species have proved difficult to grow in controlled conditions and in this investigation all members of the Anthocerotae studied possessed a pyrenoid.…”

Hornwort pyrenoids, carbon-concentrating structures, evolved and were lost at least five times during the last 100 million years

“…The ultrastructure of hornwort pyrenoids ranges from compact pyrenoids, as found in species of Notothylas, to highly dissected pyrenoids in some Nothoceros and Phymatoceros (12). Additionally, hornwort plastids have a stacked arrangement of thylakoid membranes (grana) that results in the spatial separation of photosystems and increases the efficiency of light capture in terrestrial environments (13). Hornwort grana consist of stacks of short thylakoids and lack end membranes.…”