Evolutionary development of the plant and spore wall

Abstract

Background and aims: Many key innovations were required to enable plants to colonize terrestrial habitats successfully. One of these was the acquisition of a durable spore/pollen wall capable of withstanding the harsh desiccating and UV-B-rich environment encountered on land. The spores of 'lower' spore-bearing plants and the pollen of 'higher' seed plants are homologous. In recent years, researchers have begun to investigate the molecular genetics of pollen wall development in angiosperms (including the model organism Arabidopsis thaliana). However, research into the molecular genetics of spore wall development in more basal plants has thus far been extremely limited. This review summarizes the literature on spore/pollen wall development, including the molecular genetics associated with pollen wall development in angiosperms, in a preliminary attempt to identify possible candidate genes involved in spore wall development in more basal plants.

Presence in moss of genes involved in pollen wall development: Bioinformatic studies have suggested that genes implicated in pollen wall development in angiosperms are also present in moss and lycopsids, and may therefore be involved in spore wall development in basal plants. This suggests that the molecular genetics of spore/pollen development are highly conserved, despite the large morphological and functional differences between spores and pollen.

Future work: The use of high-throughput sequencing strategies and/or microarray experiments at an appropriate stage of 'lower' land plant sporogenesis will allow the identification of candidate genes likely to be involved in the development of the spore wall by way of comparison with those genes known to be involved in pollen wall development. Additionally, by conducting gene knock-out and gene swap experiments between 'lower' land plant species, such as the moss model species Physcomitrella patens, and the angiosperm model species arabidopsis it will be possible to test the role of these candidate genes.

Fig. 1

Phylogenetic tree for land plant evolution derived from analysis by Qui et al. (2006). The bryophytes are a paraphyletic group comprising three separate lineages. Together with the vascular plants (which include the angiosperms), bryophytes form the embryophytes, which have a sister group relationship to the green algae.

Fig. 2

Proposed model of spore wall development in physcomitrella. The exine foundation layer is laid down first by way of sporopollenin accumulation on WLCL. The rest of the exine layer is deposited outside the foundation layer centrifugally. Note the appearance of callose in the inner exine, which is confined to the expanded aperture region at the proximal pole.

Fig. 3

Proposed model of spore wall development in selaginella microspores. The thin inner exine layer forms first and comprises lamellae formed centripetally on WLCL. The outer exine starts to form once the inner layer is complete. Note the presence of callose at early developmental stages around the spore mother cell.

Fig. 4

Diagram of arabidopsis pollen wall structure. The inner intine and the various components of the outer exine are indicated. Note the pollen coat (tryphine and pollenkitt) filling the cavities of the exine sculpture. Taken from Suzuki et al. (2008).

Fig. 5

Proposed functions of genes implicated in arabidopsis pollen wall exine development. Expected time and location of gene expression are indicated. Not all arabidopsis genes described in this review are included due to a lack of information regarding the time and locality of their expression. Modified from Suzuki et al. (2008).