Organellar DNA Polymerases in Complex Plastid-Bearing Algae

Abstract

DNA replication in plastids and mitochondria is generally regulated by nucleus-encoded proteins. In plants and red algae, a nucleus-encoded enzyme called POP (plant and protist organellar DNA polymerase) is involved in DNA replication in both organelles by virtue of its dual localization. POPs are family A DNA polymerases, which include bacterial DNA polymerase I (PolI). POP homologs have been found in a wide range of eukaryotes, including plants, algae, and non-photosynthetic protists. However, the phylogeny and subcellular localizations of POPs remain unclear in many algae, especially in secondary and tertiary plastid-bearing groups. In this study, we report that chlorarachniophytes possess two evolutionarily distinct POPs, and fluorescent protein-tagging experiments demonstrate that they are targeted to the secondary plastids and mitochondria, respectively. The timing of DNA replication is different between the two organelles in the chlorarachniophyte Bigelowiella natans, and this seems to be correlated to the transcription of respective POP genes. Dinoflagellates also carry two distinct POP genes, possibly for their plastids and mitochondria, whereas haptophytes and ochrophytes have only one. Therefore, unlike plants, some algal groups are likely to have evolved multiple DNA polymerases for various organelles. This study provides a new insight into the evolution of organellar DNA replication in complex plastid-bearing organisms.

Inventory and Evolution of Mitochondrion-localized Family A DNA Polymerases in Euglenozoa

“…Pioneering studies demonstrated that the previously described mitochondrion-localized DNA polymerases, namely Polγ, POP, trypanosomatid PolIA-D belong to family A [10,23]. Thus, we surveyed family A DNA polymerases in both public and in-house transcriptome data of four kinetoplastids, four diplonemids, and six euglenids (14 species in total).…”

“…Trypanosomatid PolIB, C and D were shown to be closely related to each other but remote from PolIA in previous phylogenetic studies [10,23]. In this section, we describe the distribution and evolution of PolIB, C, D and "PolIBCD-related" DNA polymerases in Euglenozoa.…”

“…In the genus Trypanosoma, phylogenetically diverse DNA polymerases were experimentally shown to be localized in mitochondria; (i) PolIA, PolIB, PolIC, and PolID [3] belong to family A, the members of which bear the sequence similarity to bacterial DNA polymerase I (PolI) [4], two of DNA polymerase beta in family X [5], and a DNA polymerase kappa in family Y [6]. Besides PolIA-D in trypanosomatids, several DNA polymerases of family A are known to be localized in mitochondria, such as DNA polymerase gamma (Polγ) in animals and yeasts [7] and plant and protist organellar DNA polymerase (POP), which is also targeted to the plastids of plants and algae [8][9][10].…”

The draft nuclear genome sequence and predicted mitochondrial proteome of Andalucia godoyi, a protist with the most gene-rich and bacteria-like mitochondrial genome

“…DNA and RNA metabolism (C) DNA replication and repair Unlike animals and fungi, which utilize a T3/T7 bacteriophage-like DNA polymerase (DNAP) γ for mtDNA replication [33,78], eukaryotes other than opisthokonts use a bacterial Pol A-like (Pol I) DNAP. This enzyme was given the name "plant organellar DNA polymerase" (POP) by Moriyama et al [79,80] but has since been identified also in protists [33,81]. It constitutes a distinct phylogenetic group without close relatives and hence of unclear origin [33,[79][80][81].…”

“…This enzyme was given the name "plant organellar DNA polymerase" (POP) by Moriyama et al [79,80] but has since been identified also in protists [33,81]. It constitutes a distinct phylogenetic group without close relatives and hence of unclear origin [33,[79][80][81]. In bacteria, Pol I plays an essential role in replication through its 5′-to-3′ exonuclease activity, which together with the 5′-to-3′ polymerase activity catalyzes the removal of RNA primers from replication intermediates.…”