Evolutionary reconstruction of pattern formation in 98 Dictyostelium species reveals that cell-type specialization by lateral inhibition is a derived trait

Abstract

BackgroundMulticellularity provides organisms with opportunities for cell-type specialization, but requires novel mechanisms to position correct proportions of different cell types throughout the organism. Dictyostelid social amoebas display an early form of multicellularity, where amoebas aggregate to form fruiting bodies, which contain only spores or up to four additional cell-types. These cell types will form the stalk and support structures for the stalk and spore head. Phylogenetic inference subdivides Dictyostelia into four major groups, with the model organism D. discoideum residing in group 4. In D. discoideum differentiation of its five cell types is dominated by lateral inhibition-type mechanisms that trigger scattered cell differentiation, with tissue patterns being formed by cell sorting.ResultsTo reconstruct the evolution of pattern formation in Dictyostelia, we used cell-type specific antibodies and promoter-reporter fusion constructs to investigate pattern formation in 98 species that represent all groupings. Our results indicate that in all early diverging Dictyostelia and most members of groups 1–3, cells differentiate into maximally two cell types, prestalk and prespore cells, with pattern formation being dominated by position-dependent transdifferentiation of prespore cells into prestalk cells. In clade 2A, prestalk and stalk cell differentiation are lost and the prespore cells construct an acellular stalk. Group 4 species set aside correct proportions of prestalk and prespore cells early in development, and differentiate into up to three more supporting cell types.ConclusionsOur experiments show that positional transdifferentiation is the ancestral mode of pattern formation in Dictyostelia. The early specification of a prestalk population equal to the number of stalk cells is a derived trait that emerged in group 4 and a few late diverging species in the other groups. Group 4 spore masses are larger than those of other groups and the differentiation of supporting cell types by lateral inhibition may have facilitated this increase in size. The signal DIF-1, which is secreted by prespore cells, triggers differentiation of supporting cell types. The synthesis and degradation of DIF-1 were shown to be restricted to group 4. This suggests that the emergence of DIF-1 signalling caused increased cell-type specialization in this group.Electronic supplementary materialThe online version of this article (doi:10.1186/2041-9139-5-34) contains supplementary material, which is available to authorized users.

A core phylogeny of Dictyostelia inferred from genomes representative of the eight major and minor taxonomic divisions of the group

“…Group 4 taxa display major phenotypic innovations, such as two more cell types, cell-type proportioning, extensive slug migration and enhanced fruiting body robustness, which are not yet evident in the “violaceum” complex [18, 20]. To identify the molecular changes that caused these innovations, the genomes of taxa in the “violaceum” complex can now be considered as the baseline from which these changes occurred.…”

“…Although one might argue whether four isolates of the same species make up a “major division”, as suggested previously [12], we feel that the polycephalid isolates with their distinctive phenotype are likely to represent a group of cryptic species. Unlike all other non-group 4 species, polycephalids form very long actively migrating slugs, which unlike group 4 slugs do not show a pattern of prestalk and prespore cells [20]. Also unlike group 4 slugs, polycephalid slugs subdivide into many small fruiting structures with stalks that adhere tightly `along approximately their lower two-thirds.…”

“…Mapping of phenotypic characters onto the phylogeny revealed that groups 1, 2 and 3 share many common features, such as small clustered or branched fruiting bodies with stalks being formed by dedifferentiation of prespore cells, use of glorin as attractant for aggregation and retention of encystation, the survival strategy of unicellular amoebas [18, 20]. Group 4 taxa generally form large, solitary and unbranched fruiting bodies, and set aside a proportion of specialized cells to form the stalk.…”

Evolution of developmental signalling in Dictyostelid social amoebas

“…This is distinct from groups 1–3, which use other chemoattractants for aggregation, form small clustered fruiting bodies without supporting discs, and form the stalk by redifferentiation of prespore cells. Many group 1–3 species, such as Polysphondylium pallidum , additionally retain the ancestral survival strategy of encystment as individuals [6, 33•]. The enzymes AcrA, AcgA, RegA and PKA are conserved throughout Dictyostelia, and except for AcgA, also in unicellular Amoebozoa [34•, 35].…”

Two potential evolutionary origins of the fruiting bodies of the dictyostelid slime moulds

“…Prestalk cells remaining after the construction of the stalk may also contribute to the upper cup (Early et al , ). Cup cells and basal disc cells are only found in Dictyostelium discoideum and closely related species; the same seems to be true of differentiation inducing factor 1 (DIF‐1) polyketide signalling, which generates these cells (Schilde et al , ).…”