Plastid gene loss and pseudogenization has been widely documented in parasitic and mycoheterotrophic plants, which have relaxed selective constraints on photosynthetic function. More enigmatic are sporadic reports of degradation and loss of important photosynthesis genes in lineages thought to be fully photosynthetic. Here we report the complete plastid genome of Saniculiphyllum guangxiense, a critically endangered and phylogenetically isolated plant lineage, along with genomic evidence of reduced chloroplast function. We also report 22 additional plastid genomes representing the diversity of its containing clade Saxifragales, characterizing gene content and placing variation in a broader phylogenetic context.

We find that the plastid genome of Saniculiphyllum has experienced pseudogenization of five genes of the NDH complex (ndhA, ndhB, ndhD, ndhF, and ndhK), previously reported in flowering plants with an aquatic habit, as well as the more surprising pseudogenization of two genes more central to photosynthesis (ccsA and cemA), contrasting with strong phylogenetic conservatism of plastid gene content in all other sampled Saxifragales. These genes participate in photooxidative protection, cytochrome synthesis, and carbon uptake. Nuclear paralogs exist for all seven plastid pseudogenes, yet these are also unlikely to be functional. Saniculiphyllum appears to represent the greatest degree of plastid gene loss observed to date in any fully photosynthetic lineage, yet plastid genome length, structure, and substitution rate are within the variation previously reported for photosynthetic plants. These results highlight the increasingly appreciated dynamism of plastid genomes, otherwise highly conserved across a billion years of green plant evolution, in plants with highly specialized life history traits.

Alignments

Individual alignments of chloroplast orthologs and the nuclear Saniculiphyllum paralogs are in the following files: 

ndhK.fasta
ndhD.fasta
ndhF.fasta
cemA.fasta
ndhB.fasta
ccsA.fasta
ndhA.fasta
 

The chloroplast tree alignment is chloroplast_alignment.phy, with the partition file at chloroplast_alignment_partition_FINAL.txt, and the resultant topology at RAxML_bipartitions.saniculiphyllum.tre. A version preserving the gene annotations is at allchloroplast_RAFedited.geneious.

Gene trees

The plastid gene tree topologies with nuclear paralogs are at:

RAxML_bipartitions.ndhA.reduced.tre
RAxML_bipartitions.ndhK.reduced.tre
RAxML_bipartitions.cemA.reduced.tre
RAxML_bipartitions.ccsA.reduced.tre
RAxML_bipartitions.ndhF.reduced.tre
RAxML_bipartitions.ccsA.tre
RAxML_bipartitions.ndhD.tre