Development of multicellular spores in the hornwort genus Dendroceros (Dendrocerotaceae, Anthocerotophyta) and the occurrence of endospory in Bryophytes

摘要

Dendroceros is a clearly-defined tropical genus readily differentiated from other hornworts in that it grows on tree bark and leaves, and produces green multicellular spores. To further understand hornwort morphological diversity, we conducted a comprehensive ultrastructural investigation of post-meiotic development of multicellular spores in two species of Dendroceros. Following meiosis, unicellular spores remain in tetrads, expand to 60–75 μm in diameter, and fill the intracapsular space. At this stage, the spore wall consists of a highly convoluted homogeneous electron-opaque outer exine and narrow fibrillar inner exine. The single chloroplast is randomly organized with patches of pyrenoid precursors and poorly-differentiated thylakoids. With successive divisions, the solitary chloroplast differentiates into the large, star-shaped organelle with a distinct pyrenoid typical of mature gametophyte cells. Concomitant with these changes and an increase in cell number is a decrease in cell size, and an increase in cell content, especially protein storage bodies in vacuoles. There is no precise pattern of cell division and multicellular spores vary in shape and cell number, assuming the size and shape of the space in which they develop. Basipetal differentiation of multicellular spores is completed where the sporophyte emerges from the long involucre. Our study points to a novel hypothesis on the evolution of precocious endospory in epiphytic and epiphyllous hornworts. Because cell organization and organelle substructure undergo dramatic transformations during cell cycles, we speculate that endosporic and precocious divisions are a means to protect the nascent spore while it develops the biochemical and structural machinary to withstand drying. Therefore, we view the condition in Dendroceros, the only desiccation tolerant hornwort, as a feature directly related to this capability. As in Dendroceros, epiphytism and precocious endospory exist together in the leafy liverworts of the Porellales and several moss clades, also suggesting that desiccation tolerance may play a role in this co-occurrence.