The evolutionary history of ferns inferred from 25 low‐copy nuclear genes

Rothfels, Carl J.; Li, Fay‐Wei; Sigel, Erin M.; Huiet, Layne; Larsson, Anders; Bürge, Dylan O.; Ruhsam, Markus; Deyholos, Michael K.; Soltis, Douglas E.; Stewart, C. Neal; Shaw, Shane W.; Pokorny, Lisa; Chen, Tao; dePamphilis, Claude W.; DeGironimo, Lisa; Chen, Li; Wei, Xiaofeng; Sun, Xiao; Korall, Petra; Stevenson, Dennis Wm.; Graham, Sean W.; Wong, Gane Ka‐Shu; Pryer, Kathleen M.

doi:10.3732/ajb.1500089

Cited by 174 publications

(241 citation statements)

References 176 publications

(296 reference statements)

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“…Recent insights on monilophyte backbone phylogeny placing horsetails (Equisetales) as sister to all remaining monilophytes (Knie et al 2015; Rothfels et al 2015) are used to root the tree in figure 2. The phylogenetic tree is fully congruent with a modern understanding of monilophyte phylogeny.…”

Section: Resultsmentioning

confidence: 99%

Convergent Evolution of Fern-Specific Mitochondrial Group II Intron atp1i361g2 and Its Ancient Source Paralogue rps3i249g2 and Independent Losses of Intron and RNA Editing among Pteridaceae

2016

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Mitochondrial intron patterns are highly divergent between the major land plant clades. An intron in the atp1 gene, atp1i361g2, is an example for a group II intron specific to monilophytes (ferns). Here, we report that atp1i361g2 is lost independently at least 4 times in the fern family Pteridaceae. Such plant organelle intron losses have previously been found to be accompanied by loss of RNA editing sites in the flanking exon regions as a consequence of genomic recombination of mature cDNA. Instead, we now observe that RNA editing events in both directions of pyrimidine exchange (C-to-U and U-to-C) are retained in atp1 exons after loss of the intron in Pteris argyraea/biaurita and in Actiniopteris and Onychium. We find that atp1i361g2 has significant similarity with intron rps3i249g2 present in lycophytes and gymnosperms, which we now also find highly conserved in ferns. We conclude that atp1i361g2 may have originated from the more ancestral rps3i249g2 paralogue by a reverse splicing copy event early in the evolution of monilophytes. Secondary structure elements of the two introns, most characteristically their domains III, show strikingly convergent evolution in the monilophytes. Moreover, the intron paralogue rps3i249g2 reveals relaxed evolution in taxa where the atp1i361g2 paralogue is lost. Our findings may reflect convergent evolution of the two related mitochondrial introns exerted by co-evolution with an intron-binding protein simultaneously acting on the two paralogues.

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Section: Resultsmentioning

confidence: 99%

Convergent Evolution of Fern-Specific Mitochondrial Group II Intron atp1i361g2 and Its Ancient Source Paralogue rps3i249g2 and Independent Losses of Intron and RNA Editing among Pteridaceae

2016

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“…2 a and b ). For the baseml runs, we used a GTR + G substitution model, with a fixed topology and divergence times derived from the 25-nuclear-locus study of Rothfels et al (2015). The 2-rate models were tested against the 1-rate model using likelihood-ratio tests.…”

Section: Methodsmentioning

confidence: 99%

“…The phylogeny on the left shows the relationships among the sampled fern chloroplast genomes; a part of their genome organization is shown on the right. The tree topology and divergence times are derived from Rothfels et al (2015). Gene lengths are not to scale, gene arrow tips indicate the direction of transcription, and a few genes are omitted for clarity.…”

Section: Introductionmentioning

confidence: 99%

Genes Translocated into the Plastid Inverted Repeat Show Decelerated Substitution Rates and Elevated GC Content

Kuo

Pryer

et al. 2016

Genome Biol Evol

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Plant chloroplast genomes (plastomes) are characterized by an inverted repeat (IR) region and two larger single copy (SC) regions. Patterns of molecular evolution in the IR and SC regions differ, most notably by a reduced rate of nucleotide substitution in the IR compared to the SC region. In addition, the organization and structure of plastomes is fluid, and rearrangements through time have repeatedly shuffled genes into and out of the IR, providing recurrent natural experiments on how chloroplast genome structure can impact rates and patterns of molecular evolution. Here we examine four loci (psbA, ycf2, rps7, and rps12 exon 2–3) that were translocated from the SC into the IR during fern evolution. We use a model-based method, within a phylogenetic context, to test for substitution rate shifts. All four loci show a significant, 2- to 3-fold deceleration in their substitution rate following translocation into the IR, a phenomenon not observed in any other, nontranslocated plastid genes. Also, we show that after translocation, the GC content of the third codon position and of the noncoding regions is significantly increased, implying that gene conversion within the IR is GC-biased. Taken together, our results suggest that the IR region not only reduces substitution rates, but also impacts nucleotide composition. This finding highlights a potential vulnerability of correlating substitution rate heterogeneity with organismal life history traits without knowledge of the underlying genome structure.

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“…Previous studies based primarily on plastid data uncovered considerable rate heterogeneity within this family, especially with respect to the morphologically simplified, epiphytic vittarioid lineage [23, 25]. However, it was unclear whether such patterns extended to the nuclear genomes in these ferns [58]. Using pairwise rate comparisons for 2091 nuclear loci, we ask whether the significant variation in molecular evolutionary rates previously reported for plastid loci is mirrored in fern nuclear genomes.…”

Section: Discussionmentioning

confidence: 95%

Transcriptome sequencing reveals genome-wide variation in molecular evolutionary rate among ferns

2016

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BackgroundTranscriptomics in non-model plant systems has recently reached a point where the examination of nuclear genome-wide patterns in understudied groups is an achievable reality. This progress is especially notable in evolutionary studies of ferns, for which molecular resources to date have been derived primarily from the plastid genome. Here, we utilize transcriptome data in the first genome-wide comparative study of molecular evolutionary rate in ferns. We focus on the ecologically diverse family Pteridaceae, which comprises about 10 % of fern diversity and includes the enigmatic vittarioid ferns—an epiphytic, tropical lineage known for dramatically reduced morphologies and radically elongated phylogenetic branch lengths. Using expressed sequence data for 2091 loci, we perform pairwise comparisons of molecular evolutionary rate among 12 species spanning the three largest clades in the family and ask whether previously documented heterogeneity in plastid substitution rates is reflected in their nuclear genomes. We then inquire whether variation in evolutionary rate is being shaped by genes belonging to specific functional categories and test for differential patterns of selection.ResultsWe find significant, genome-wide differences in evolutionary rate for vittarioid ferns relative to all other lineages within the Pteridaceae, but we recover few significant correlations between faster/slower vittarioid loci and known functional gene categories. We demonstrate that the faster rates characteristic of the vittarioid ferns are likely not driven by positive selection, nor are they unique to any particular type of nucleotide substitution.ConclusionsOur results reinforce recently reviewed mechanisms hypothesized to shape molecular evolutionary rates in vittarioid ferns and provide novel insight into substitution rate variation both within and among fern nuclear genomes.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3034-2) contains supplementary material, which is available to authorized users.

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The evolutionary history of ferns inferred from 25 low‐copy nuclear genes

Abstract: Our study demonstrates the utility of a curated phylogenomics approach to inferring fern phylogeny, and highlights the need to consider underlying data characteristics, along with data quantity, in phylogenetic studies.

Cited by 174 publications

References 176 publications

Convergent Evolution of Fern-Specific Mitochondrial Group II Intron atp1i361g2 and Its Ancient Source Paralogue rps3i249g2 and Independent Losses of Intron and RNA Editing among Pteridaceae

Convergent Evolution of Fern-Specific Mitochondrial Group II Intron atp1i361g2 and Its Ancient Source Paralogue rps3i249g2 and Independent Losses of Intron and RNA Editing among Pteridaceae

Genes Translocated into the Plastid Inverted Repeat Show Decelerated Substitution Rates and Elevated GC Content

Transcriptome sequencing reveals genome-wide variation in molecular evolutionary rate among ferns

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