Monosiphonous growth and cell-death in an unusual Bostrychia (Rhodomelaceae, Rhodophyta): B. anomala sp. nov.

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  • ABSTRACT

    A morphologically distinct lineage within the Bostrychia moritziana-B. radicans species complex is described as a new species. Bostrychia anomala has thalli with branched monosiphonous filaments with apical cell divisions. The species has terminal tetrasporangial stichidia, each subtending cell bearing tetrasporangia with 2 cover cells. Discharged spores divide transversely, the lower cell first forming a narrow rhizoid and the upper cell forming a monosiphonous shoot. Females have subterminal procarps and males have terminal spermatangial stichidia. Carposporophytes are spherical. Isolates in culture show a pattern of cell death not associated with injury, reminiscent of programmed cell death. Bostrychia anomola shows cell death at intervals along the filaments resulting in division of adjacent cells on either side of the dead cell re-joining the filament; cell division of only one adjacent cell resulting in branching at that site; or filaments fragmenting at the cell death point with adjacent cells forming new apical cells, a means of thallus propagation. The cell death pattern could be a method of filament propagation in the mangrove environment where sexual reproduction is rare.


  • KEYWORD

    Bostrychia anomala sp. nov. , monosiphonous , ‘non-fusion-division’ , programmed-cell-death , Rhodomelaceae , sexual life history , vegetative propagation

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  • [Fig. 1.] Maximum-likelihood topology of rbcL sequences of members of the genus Bostrychia. Outgroups removed for clarity. The bootstrap values for maximum-parsimony trees (MP) (> 50%; right) and maximum-likelihood trees (ML) (≥ 50%; left) are given on each branch, and strongly supported branches (MP-bootstrap [BS] and ML-BS ≥ 95%) are indicated by asterisks. Bayesian inference values over 0.95 are shown by thicker branches. For further information on samples see West et al. (2006), Zuccarello and West (2006), and Zuccarello et al. (2012), except for newly derived sequences (underlined).
    Maximum-likelihood topology of rbcL sequences of members of the genus Bostrychia. Outgroups removed for clarity. The bootstrap values for maximum-parsimony trees (MP) (> 50%; right) and maximum-likelihood trees (ML) (≥ 50%; left) are given on each branch, and strongly supported branches (MP-bootstrap [BS] and ML-BS ≥ 95%) are indicated by asterisks. Bayesian inference values over 0.95 are shown by thicker branches. For further information on samples see West et al. (2006), Zuccarello and West (2006), and Zuccarello et al. (2012), except for newly derived sequences (underlined).
  • [Fig. 2.] Bostrychia anomala vegetative growth and cell death, 4613 (A-E, G & H) and 4588 (F). (A) Filaments with branch initials (bi) arising from intercalary cells and terminal tetrasporangial stichidium (t). (B) Lateral branch initial arising as a curved “lenticular” cell division from parent axis. (C) Lateral branch with actively dividing apical cell. (D) Paired rhizoids from intercalary cell. (E) Vegetative branches with many rhizoids. Cell deaths (cd) evident in one branch. (F) Many filaments with frequent cell death (cd). Collapsed green protoplast and dark brown collar around walls at both ends seen in many dead cells. (G) Sequence of 3 dead cells with collapsed protoplasts, tan colour around the walls and dark brown collars at ends of cells evident. (H) Cell death at base of lateral branch with possible rhizoid elongating toward the main filament on the left. Scale bars represent: A, E & F, 60 μm; B-D, G & H, 30 μm.
    Bostrychia anomala vegetative growth and cell death, 4613 (A-E, G & H) and 4588 (F). (A) Filaments with branch initials (bi) arising from intercalary cells and terminal tetrasporangial stichidium (t). (B) Lateral branch initial arising as a curved “lenticular” cell division from parent axis. (C) Lateral branch with actively dividing apical cell. (D) Paired rhizoids from intercalary cell. (E) Vegetative branches with many rhizoids. Cell deaths (cd) evident in one branch. (F) Many filaments with frequent cell death (cd). Collapsed green protoplast and dark brown collar around walls at both ends seen in many dead cells. (G) Sequence of 3 dead cells with collapsed protoplasts, tan colour around the walls and dark brown collars at ends of cells evident. (H) Cell death at base of lateral branch with possible rhizoid elongating toward the main filament on the left. Scale bars represent: A, E & F, 60 μm; B-D, G & H, 30 μm.
  • [Fig. 3.] Bostrychia anomala cell death, wound healing and branching, 4588 (A & B) and 4613 (C-G). (A) At each end of the dead cell (collapsed green protoplast and brown collars at either end visible), elongation and division of adjacent cells is seen. New cells with dense protoplast. (B) Cell death at lateral branch base with cell elongation of cell adjacent to dead cell, above, and a slight bulge of the cell adjacent on the main axis suggesting similar development. (C) Old cell wall visible with division of adjacent cells, connection with visible pit plug (arrow) and formation of lateral branch also visible. (D) Filament alignment slightly displaced, resulting in lower adjacent cell dividing to form new apical cell. (E) Cell death resulted in a broken filament, on left and right of central intact filament, and new apical cells at the ends of the broken filament. Old cell wall is visible (arrows). (F) After cell death cells adjacent to dead cell elongating. (G) Filament on left showing elongating cell above and below compressed dead cell; filament on right with disrupted connection at dead cell, a new shoot apex forming below, cell not visibly changed. Scale bars represent: A-G, 30 μm.
    Bostrychia anomala cell death, wound healing and branching, 4588 (A & B) and 4613 (C-G). (A) At each end of the dead cell (collapsed green protoplast and brown collars at either end visible), elongation and division of adjacent cells is seen. New cells with dense protoplast. (B) Cell death at lateral branch base with cell elongation of cell adjacent to dead cell, above, and a slight bulge of the cell adjacent on the main axis suggesting similar development. (C) Old cell wall visible with division of adjacent cells, connection with visible pit plug (arrow) and formation of lateral branch also visible. (D) Filament alignment slightly displaced, resulting in lower adjacent cell dividing to form new apical cell. (E) Cell death resulted in a broken filament, on left and right of central intact filament, and new apical cells at the ends of the broken filament. Old cell wall is visible (arrows). (F) After cell death cells adjacent to dead cell elongating. (G) Filament on left showing elongating cell above and below compressed dead cell; filament on right with disrupted connection at dead cell, a new shoot apex forming below, cell not visibly changed. Scale bars represent: A-G, 30 μm.
  • [Fig. 4.] Bostrychia anomala 4613 tetrasporophyte. (A) Terminal tetrasporangial stichidia. (B) Young tetrasporangial stichidium, apical cell (ac), first axial segment with pericentral cells (pc), middle segment with tier cells (tc). (C) Aniline-blue stained stichidium with developing tetrasporangia. (D) Aniline-blue stained stichidium with each segment forming 2-3 tetrasporangia and respective cover cells (arrows). (E) Live stichidium with 3 axial cell segments 2-3 tetrasporangia, each with 2 cover cells (arrows). (F) Sporeling with long rhizoidal filament (upwards) and shorter erect shoot (downwards). Scale bars represent: A-F, 30 μm.
    Bostrychia anomala 4613 tetrasporophyte. (A) Terminal tetrasporangial stichidia. (B) Young tetrasporangial stichidium, apical cell (ac), first axial segment with pericentral cells (pc), middle segment with tier cells (tc). (C) Aniline-blue stained stichidium with developing tetrasporangia. (D) Aniline-blue stained stichidium with each segment forming 2-3 tetrasporangia and respective cover cells (arrows). (E) Live stichidium with 3 axial cell segments 2-3 tetrasporangia, each with 2 cover cells (arrows). (F) Sporeling with long rhizoidal filament (upwards) and shorter erect shoot (downwards). Scale bars represent: A-F, 30 μm.
  • [Fig. 5.] Bostrychia anomala 4613 female and male. (A) Subterminal procarp with elongating trichogyne (t). (B) Mature procarp on intercalary cell. (C) Mature procarp with very long trichogyne and sterile tier cells at either side of procarpic branch (darker cells). (D) Spermatangial stichidium. (E) Mature cystocarp with mature carposporophyte visible within pericarp. (F) Mature cystocarp slightly squashed to discharge carpospores through the terminal ostiole. Old trichogyne (t) visible on the lower right side of cystocarp. Scale bars represent A-F, 30 μm.
    Bostrychia anomala 4613 female and male. (A) Subterminal procarp with elongating trichogyne (t). (B) Mature procarp on intercalary cell. (C) Mature procarp with very long trichogyne and sterile tier cells at either side of procarpic branch (darker cells). (D) Spermatangial stichidium. (E) Mature cystocarp with mature carposporophyte visible within pericarp. (F) Mature cystocarp slightly squashed to discharge carpospores through the terminal ostiole. Old trichogyne (t) visible on the lower right side of cystocarp. Scale bars represent A-F, 30 μm.
  • [Table1.] Isolates of Bostrychia moritziana-B. radicans in which monosiphonous filaments are occasionally seen
    Isolates of Bostrychia moritziana-B. radicans in which monosiphonous filaments are occasionally seen