Plant Poly(A) Polymerases

Among the conserved proteins of the polyadenylation complex, seen in all eukaryotes (including the highly-reduced polyadenylation complex in Giardia) is the enzyme that adds the poly(A) tail – polynucleotide adenylyltransferase or, more colloquially, poly(A) polymerase.  One would think that the evolutionary history of such a core component of the gene expression machinery would be rather unremarkable – it should be present at the outset and pretty much conserved throughout evolutionary history.

Of course, reality is much more interesting.  A former student of mine did her thesis on Arabidopsis poly(A) polymerases, characterizing the four (4!) genes and the protein isoforms.  A former postdoc in the lab had done some work in rice poly(A) polymerase genes, and found an equally interesting multiplicity of genes as well as some fascinating expression characteristics.  This work has been recently published in PLoS ONE; as is my custom, this post is intended to point out the paper and invite (here or at the journal’s site for the paper) comment, discussion, and criticism.

A brief recap and one or two of the more provocative findings:

Higher plants possess poly(A) polymerase gene families that number between 4 and 5 (or more; although not in the paper, plants whose genomes have undergone recent duplications may have twice these numbers).  Interestingly, all of the plant genes arose from a single ancestral gene, based on the highly-conserved positions of introns.  These positions are different from those seen in animal poly(A) polymerase genes (and, curiously enough, from those seen in the single Chlamydomonas poly(A) polymerase gene).

The results obtained with Arabidopsis mutants indicates that all of the expressed plant isoforms are essential for viability.  This and the expression studies performed with rice and Arabidopsis are most consistent with idea that the different isoforms have undergone a degree of functional specialization.

One of the plant isoforms is a cytoplasmic enzyme.  The gene encoding the Arabidopsis cytoplasmic poly(A) polymerase is strongly pollen-specific.  These characteristics are reminiscent of a mammalian poly(A) polymerase isoform.  However, the data in this paper indicate that the mammalian and plant cytoplasmic poly(A) polymerases have independent evolutionary histories; in other words, the occurrence of cytoplasmic poly(A) polymerases in plants and animals is a case of convergent evolution.

Here is Figure 6 from the paper – my attempt to illustrate the history of these genes in the plant lineage.

The hypothetical poly(A) polymerase gene in the common ancestor of the lineages shown here and other eukaryotes is depicted with a light blue rectangular box; that the Chlamydomonas gene may be similar to this is indicated as the Chlamydomonas lineage retaining this gene. Distinctly plant poly(A) polymerases are represented with circles, with the relationships with the four Arabidopsis poly(A) polymerases indicated according to the colors shown at the upper left. The properties of the various poly(A) polymerase gene families are shown beneath the timeline, and the times of occurrences of putatiuve duplications above the timeline. The question marks in the P. patens genes indicates some uncertainty as to the relation ships of these genes to the hypothetical common ancestor of the genes in the rest of the plant lineage; this uncertainty owes to the absence of introns in these genes, and raises similar questions about the ancestral gene. Pseudogenes are represented as gray circles.

The citation:

Meeks LR, Addepalli B, Hunt AG. 2009. Characterization of Genes Encoding Poly(A) Polymerases in Plants: Evidence for Duplication and Functional Specialization.  PLoS ONE 4(11): e8082. doi:10.1371/journal.pone.0008082.