Evolutionary crossroads in developmental biology: Dictyostelium discoideum

Abstract

SummaryDictyostelium discoideum belongs to a group of multicellular life forms that can also exist for long periods as single cells. This ability to shift between uni-and multicellularity makes the group ideal for studying the genetic changes that occurred at the crossroads between uni-and multicellular life. In this Primer, I discuss the mechanisms that control multicellular development in Dictyostelium discoideum and reconstruct how some of these mechanisms evolved from a stress response in the unicellular ancestor.Key words: Evolution of multicellularity, Social amoeba, Encystation, Sporulation, Dictyostelium IntroductionThe social amoebas, or Dictyostelia, are a group of organisms that become multicellular by aggregation and then proceed to build fruiting bodies that consist of stalk cells and spores (see Glossary, Box 1). This developmental cycle is a response to starvation, and involves both highly coordinated cell movement and a tightly controlled programme of cell differentiation. Social amoebas belong to the supergroup of Amoebozoa (see Glossary, Box 1), a sister group to the clade of Opisthokonts (see Glossary, Box 1), which contains the animals and fungi. All supergroups contain unicellular protist-like organisms (see Glossary, Box 1) and, in several groups, multicellular life forms have evolved independently (Minge et al., 2009).The Amoebozoa supergroup consists mainly of unicellular amoeba-like organisms that have a simple life cycle. The feeding amoeba or trophozoite turns into a dormant cyst when faced with food shortage, drought or other life-threatening circumstances (Cavalier-Smith et al., 2004). Several clades of Amoebozoa have given rise to protostelid-like organisms (see Glossary, Box 1), which form a very simple fruiting body (see Glossary, Box 1) that consists of a single spore that sits on a simple stalk made by the same cell (Shadwick et al., 2009). However, only the Dictyostelia are able to form multicellular fruiting bodies that contain up to a million cells (Fig. 1).There are ~120 known species of Dictyostelia and a molecular phylogeny has been constructed to reveal the order in which they evolved (Schaap et al., 2006). The phylogeny subdivides species into four major groups (Fig. 2), with the model social amoeba Dictyostelium discoideum belonging to the most recently diverged group 4. Many species in groups 1-3 can still encyst as single cells when conditions are unfavourable for aggregation. However, group 4 species have lost the ability to encyst. Strikingly, all group 4 species tested secrete cyclic adenosine monophosphate (cAMP) to act as a chemoattractant for aggregation. This is most unusual, because almost all other organisms only use cAMP inside the cell to transduce the effect of other secreted stimuli, such as hormones, mating factors and neurotransmitters. None of the species in groups 1-3 uses cAMP for aggregation; some use glorin, a modified dipeptide of glutamate and ornithine, whereas others use folic acid, pterin or other as yet unidentified chemoattractants (Schaap e...

CyrA, a matricellular protein that modulates cell motility in Dictyostelium discoideum

“…After approximately 16 h of development, aggregated cells form multicellular structures called pseudoplasmodia or slugs that can migrate on the substratum in response to light and temperature. When conditions are suitable, the slugs culminate into fruiting bodies composed of dead stalk cells supporting a mass of viable spores (Schaap, 2011). If development is allowed to proceed in the dark, slugs will not immediately culminate.…”

Volvocine Algae: From Simple to Complex Multicellularity

“…Multicellular development and cell differentiation pathways (ensuring functional and reproductive unity and resulting in an increase in structural and functional complexity) have also evolved from pathways present in unicellular lineages-as in, for instance, the cellular slime mold Dictyostelium discoideum (Schaap 2011;Chap. 21) and the green alga Volvox carteri (Nedelcu 2009b).…”

Evolutionary diversity of social amoebae N-glycomes may support interspecific autonomy

“…Kin to other amoebae such as Acanthamoeba and Entamoeba , the group diverged from other major eukaryotic lineages during the crown radiation [1–3]. The social amoebae consist of over a hundred species that can cohabitate the same soil environment where they feed phagocytically on bacteria and yeasts.…”