Abstract
Evolutionary mechanisms underlying innovation of cell types have remained largely unclear. In multicellular eukaryotes, the evolutionary molecular origin of sperm differentiation is unknown in most lineages. Here, we report that in algal ancestors of land plants, changes in the DNA-binding domain of the ancestor of the MYB transcription factor DUO1 enabled the recognition of a new cis-regulatory element. This event led to the differentiation of motile sperm. After neo-functionalization, DUO1 acquired sperm lineage-specific expression in the common ancestor of land plants. Subsequently the downstream network of DUO1 was rewired leading to sperm with distinct morphologies. Conjugating green algae, a sister group of land plants, accumulated mutations in the DNA-binding domain of DUO1 and lost sperm differentiation. Our findings suggest that the emergence of DUO1 was the defining event in the evolution of sperm differentiation and the varied modes of sexual reproduction in the land plant lineage.
Highlights
Evolutionary mechanisms underlying innovation of cell types have remained largely unclear
The network controlled by DUO POLLEN 1 (DUO1) in Arabidopsis comprises the two closely related transcription factor (TF), DUO1ACTIVATED ZINC FINGER1 (DAZ1) and DAZ2 which, together with DUO1, regulate the expression of the sperm-specific histone variant H3.10 and the fusogenic factors GENERATIVE CELL-SPECIFIC 1 /HAPLESS 2 (GCS1/HAP2) and GAMETE EXPRESSED 2 (GEX2)[12]
DUO1 differs from all other R2R3 MYB TFs by a supernumerary lysine residue between the R2 and R3 repeats of its MYB domain[11]
Summary
Evolutionary mechanisms underlying innovation of cell types have remained largely unclear. Sperm differentiation is fully restored when the MpDUO1 DNA-binding domain is fused to the AtDUO1 C-terminal activation domain and the resultant chimera is expressed under control of the AtDUO1 promoter (Chimera 1; Fig. 3b). Together these results show that DUO1 orthologs have controlled sperm-cell differentiation and morphogenesis since the evolution of land plants.
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