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While enhancers are often regulated at the level of accessibility by pioneer factors, promoters tend to be constitutively accessible and poised for activation by paused Pol II — thus are often not considered as sites of developmental regulation. Here we show that the accessibility of promoters and the acquisition of paused Pol II can be subject to developmental regulation by pioneer factors. We show that Lola-I, a Drosophila zinc finger transcription factor, is ubiquitously expressed at the end of embryogenesis and causes its target promoters to become accessible and acquire paused Pol II throughout the embryo. This promoter transition is required but not sufficient for tissue-specific target gene expression. Lola-I mediates this function by binding to the edges of the promoter nucleosomes, which leads to their depletion, similar to the action of pioneer factors at enhancers. These results uncover a level of regulation for promoters that is normally found at enhancers, providing further evidence that promoters and enhancers display unexpectedly similar characteristics.

We sequenced mitochondrial genomes from five diverse diatoms (Toxarium undulatum, Psammoneis japonica, Eunotia naegelii, Cylindrotheca closterium, and Nitzschia sp.), chosen to fill important phylogenetic gaps and help us characterize broadscale patterns of mitochondrial genome evolution in diatoms. Although gene content was strongly conserved, intron content varied widely across species. The vast majority of introns were of group II type and were located in the cox1 or rnl genes. Although recurrent intron loss appears to be the principal underlying cause of the sporadic distributions of mitochondrial introns across diatoms, phylogenetic analyses showed that intron distributions superficially consistent with a recurrent-loss model were sometimes more complicated, implicating horizontal transfer as a likely mechanism of intron acquisition as well. It was not clear, however, whether diatoms were the donors or recipients of horizontally transferred introns, highlighting a general challenge in resolving the evolutionary histories of many diatom mitochondrial introns. Although some of these histories may become clearer as more genomes are sampled, high rates of intron loss suggest that the origins of many diatom mitochondrial introns are likely to remain unclear.

PREMISE OF THE STUDY Loss of photosynthesis is a common and often repeated trajectory in nearly all major groups of photosynthetic eukaryotes. One small subset of "apochloritic" diatoms in the genus Nitzschia have lost their ability to photosynthesize and require extracellular carbon for growth. Similar to other secondarily nonphotosynthetic taxa, apochloritic diatoms maintain colorless plastids with highly reduced plastid genomes. Although the narrow taxonomic breadth of apochloritic Nitzschia suggests a single loss of photosynthesis in their common ancestor, previous phylogenetic analyses suggested that photosynthesis was lost multiple times. METHODS We analyzed genes from the nuclear, plastid, and mitochondrial genomes for a broad set of taxa to test whether photosynthesis was lost one or multiple times in Bacillariales. We also sequenced and characterized the plastid genome of a nonphotosynthetic Nitzschia species. KEY RESULTS Phylogenetic analyses showed that genes from all three genetic compartments either supported or failed to reject monophyly of apochloritic Nitzschia species, consistent with a single loss of photosynthesis in this group. The plastid genomes of two apochloritic Nitzschia are highly similar in all respects, indicating streamlining of the plastid genome before the split of these two species. CONCLUSIONS A better understanding of the phylogeny and ecology of apochloritic Nitzschia, together with emerging genomic resources, will help identify the factors that have driven and maintained the loss of photosynthesis in this group of diatoms. Finally, some habitats host diverse communities of co-occurring nonphotosynthetic diatoms, reflecting resource abundance or resource partitioning in ecologically favorable habitats.

Loss of photosynthesis is a common and often repeated trajectory in nearly all major groups of photosynthetic eukaryotes. One small subset of ‘apochloritic’ diatoms in the genus Nitzschia have lost their ability to photosynthesize and require extracellular carbon for growth. Similar to other secondarily nonphotosynthetic taxa, apochloritic diatoms maintain colorless plastids with highly reduced plastid genomes. Although the narrow taxonomic breadth of apochloritic diatoms suggests a single loss of photosynthesis in the common ancestor of these species, previous phylogenetic analyses suggested that photosynthesis was lost multiple times. We sequenced additional phylogenetic markers from the nuclear and mitochondrial genomes for a larger set of taxa and found that the best trees for datasets representing all three genetic compartments provided low to moderate support for monophyly of apochloritic Nitzschia, consistent with a single loss of photosynthesis in diatoms. We sequenced the plastid genome of one apochloritic species and found that it was highly similar in all respects to the plastid genome of another apochloritic Nitzschia species, indicating that streamlining of the plastid genome had completed prior to the split of these two species. Finally, it is increasingly clear that some locales host relatively large numbers apochloritic Nitzschia species that span the phylogenetic diversity of the group, indicating that these species co-exist because of resource abundance or resource partitioning in ecologically favorable habitats. A better understanding of the phylogeny and ecology of this group, together with emerging genomic resources, will help identify the factors that have driven and maintained the loss of photosynthesis in this group, a rare event in diatoms.