The origin of red algae: implications for plastid evolution

Abstract

The origin of the red algae has remained an enigma. Historically the Rhodophyta were classified first as plants and later as the most ancient eukaryotic organisms. Recent molecular studies have indicated similarities between red and green plastids, which suggest that there was a single endosymbiotic origin for these organelles in a common ancestor of the rhodophytes and green plants. Previous efforts to confirm or reject this effort by analyses of nuclear DNA have been inconclusive; thus, additional molecular markers are needed to establish the relationship between the host cell lineages, independent of the evolutionary history of their plastids. To furnish such a data set we have sequenced the largest subunit of RNA polymerase II from two red algae, a green alga and a relatively derived amoeboid protist. Phylogenetic analyses provide strong statistical support for an early evolutionary emergence of the Rhodophyta that preceded the origin of the line that led to plants, animals, and fungi. These data, which are congruent with results from extensive analyses of nuclear rDNA, argue for a reexamination of current models of plastid evolution.

Figure 1

Degenerate oligonucleotide primers based on conserved amino acid motifs in RPB1 from plant, animal, and fungal sequences.

Figure 2

Phylogenetic analyses based on RPB1 sequences. (A) Congruent bootstrapped parsimony (paup 3.1.1; ref. 24) and neighbor-joining (protdist, phylip3.53; ref. 25) trees. Trees are unrooted, but the largest subunit of polymerase III RPC1 from S. cerevisiae was used as the outgroup (21). Distances were estimated using the Dayhoff PAM matrix for amino acid substitutions. Percent appearances in 1,000 parsimony/100 distance bootstrap replicates are given above each node. Only one value is given when bootstrap values agree. (B) Tree with the maximum likelihood (codeml, paml 1.1; ref. 26) using the Jones, Taylor, Thornton matrix for amino acid substitutions. Branch lengths are approximately proportional to the estimated number of substitutions leading to the subsequent node. Six categories were used to estimate the γ distribution for rate variation, and likelihood estimates made with α = 1 and α = 0.5 produced the same tree topology. Because paml disregards any position in an alignment in which a gap occurs in any one of the aligned sequences, truncated sequences (Giardia, RPC1, Spirogyra) were deleted from the analysis to prevent loss of large portions of the data set.

Figure 3

Hypothetical evolutionary reduction of secondary plastids to give the appearance of primary plastids. Organisms representative of the condition are given below each diagram. Conditions 1 (65) through 4 are widely accepted (3, 4, 8, 9, 54, 55, 63, 64) to explain membrane variability in the plastids of photosynthetic eukaryotes. N1, primary host cell nucleus; N2, secondary host cell nucleus; Nm, nucleomorph (vestigial endosymbiont nucleus); P, plastid.