Novel genetic code and record-setting AT-richness in the highly reduced plastid genome of the holoparasitic plant Balanophora

Abstract

Plastid genomes (plastomes) vary enormously in size and gene content among the many lineages of nonphotosynthetic plants, but key lineages remain unexplored. We therefore investigated plastome sequence and expression in the holoparasitic and morphologically bizarre Balanophoraceae. The two Balanophora plastomes examined are remarkable, exhibiting features rarely if ever seen before in plastomes or in any other genomes. At 15.5 kb in size and with only 19 genes, they are among the most reduced plastomes known. They have no tRNA genes for protein synthesis, a trait found in only three other plastid lineages, and thus Balanophora plastids must import all tRNAs needed for translation. Balanophora plastomes are exceptionally compact, with numerous overlapping genes, highly reduced spacers, loss of all cis-spliced introns, and shrunken protein genes. With A+T contents of 87.8% and 88.4%, the Balanophora genomes are the most AT-rich genomes known save for a single mitochondrial genome that is merely bloated with AT-rich spacer DNA. Most plastid protein genes in Balanophora consist of ≥90% AT, with several between 95% and 98% AT, resulting in the most biased codon usage in any genome described to date. A potential consequence of its radical compositional evolution is the novel genetic code used by Balanophora plastids, in which TAG has been reassigned from stop to tryptophan. Despite its many exceptional properties, the Balanophora plastome must be functional because all examined genes are transcribed, its only intron is correctly trans-spliced, and its protein genes, although highly divergent, are evolving under various degrees of selective constraint.

Principles of plastid reductive evolution illuminated by nonphotosynthetic chrysophytes

“…This supports previous suggestions that this functional gene set represents the minimum required for the retention of red-algal-derived plastid genomes (1). Different trends may apply in other plastid lineages: for example, the plastid genomes of the parasitic plants Epifagus and Balanophora do not encode Fe-S cluster synthesis proteins, which are nucleus encoded in plants (2,28,29), but do encode the fatty acid synthesis subunit accD, which is nucleus encoded in ochrophytes (5) (and is absent from "Spumella" sp. NIES-1846, per the lack of plastid fatty acid synthesis in this species; SI Appendix, Figs.…”

A systematic comparison of chloroplast genome assembly tools

“…the loss of the whole ndh gene family in Droseraceae [15]). Even more extreme evolutionary cases, where chloroplasts show a very low GC content and a modified genetic code are described [16].…”

Developmental Biology: Go with the Flow to Keep the Body Straight

“…Cantaut-Belarif et al [1] shed light on this puzzle. They demonstrated a link between motile cilia and an extracellular thread called the Reissner fiber, which runs through the brain ventricles and down the central canal.…”

“…The Reissner fiber is predominantly composed of the glycoprotein SCO-spondin and, though it was first discovered in 1860, its function has remained enigmatic. By generating zebrafish mutants lacking scospondin, Cantaut-Belarif et al [1] demonstrated that the Reissner fiber is needed to keep the body straight: mutant embryos exhibited classic curly tail down, mimicking cilia motility mutants. Consequently, the authors assessed motile cilia and CSF flow, but they found that both were normal in the absence of the Reissner fiber.…”

“…Thus, adrenaline is likely transported by CSF flow from the brain ventricles down the central canal to CSF-cNs, where it drives Urp neuropeptide expression. Intriguingly, the Reissner fiber is known to bind and transport adrenaline molecules [9], and so its formation downstream of CSF flow [1] might play a critical part in the delivery of adrenergic signals to CSF-cNs. It will now be interesting to test this model by asking whether urp1/2 expression is affected in scospondin mutants that lack the Reissner fiber but maintain CSF flow, and whether adrenaline treatment can rescue the curly tail down of these mutants.…”