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Degradation of Key Photosynthetic Genes in the Critically Endangered Semi-Aquatic Flowering

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Degradation of Key Photosynthetic Genes in the Critically Endangered Semi-Aquatic Flowering bioRxiv preprint doi: https://doi.org/10.1101/2019.12.22.886283; this version posted December 23, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 1 Degradation of key photosynthetic genes in the critically endangered semi-aquatic flowering 2 plant Saniculiphyllum guangxiense (Saxifragaceae) 3 4 5 6 Ryan A. Folk1,*,†, Neeka Sewnath2,†, Chun-Lei Xiang3, Brandon T. Sinn4, Robert P. Guralnick2 7 8 1. Department of Biological Sciences, Mississippi State University, Mississippi State, 9 Mississippi, U.S.A. 10 2. Florida Museum of Natural History, University of Florida, Gainesville, Florida, U.S.A. 11 3. CAS Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming 12 Botanical Garden, Kunming, Yunnan, P.R. China 13 4. Department of Biology & Earth Science, Otterbein University, Westerville, Ohio, U.S.A. 14 * Author for correspondence: [email protected] 15 † Co-first authors bioRxiv preprint doi: https://doi.org/10.1101/2019.12.22.886283; this version posted December 23, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 2 16 Abstract 17 Background—Plastid gene loss and pseudogenization has been widely documented in 18 parasitic and mycoheterotrophic plants, which have relaxed selective constraints on 19 photosynthetic function. More enigmatic are sporadic reports of degradation and loss of 20 important photosynthesis genes in lineages thought to be fully photosynthetic. Here we report the 21 complete plastid genome of Saniculiphyllum guangxiense, a critically endangered and 22 phylogenetically isolated plant lineage, along with genomic evidence of reduced chloroplast 23 function. We also report 22 additional plastid genomes representing the diversity of its 24 containing clade Saxifragales, characterizing gene content and placing variation in a broader 25 phylogenetic context. 26 Results—We find that the plastid genome of Saniculiphyllum has experienced 27 pseudogenization of five genes of the NDH complex (ndhA, ndhB, ndhD, ndhF, and ndhK), 28 previously reported in flowering plants with an aquatic habit, as well as the more surprising 29 pseudogenization of two genes more central to photosynthesis (ccsA and cemA), contrasting with 30 strong phylogenetic conservatism of plastid gene content in all other sampled Saxifragales. 31 These genes participate in photooxidative protection, cytochrome synthesis, and carbon uptake. 32 Nuclear paralogs exist for all seven plastid pseudogenes, yet these are also unlikely to be 33 functional. 34 Conclusions—Saniculiphyllum appears to represent the greatest degree of plastid gene 35 loss observed to date in any fully photosynthetic lineage, yet plastid genome length, structure, 36 and substitution rate are within the variation previously reported for photosynthetic plants. These 37 results highlight the increasingly appreciated dynamism of plastid genomes, otherwise highly bioRxiv preprint doi: https://doi.org/10.1101/2019.12.22.886283; this version posted December 23, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 3 38 conserved across a billion years of green plant evolution, in plants with highly specialized life 39 history traits. 40 Key words—plastid genome, plastome, pseudogene, organelle, Saxifragaceae, 41 Saniculiphyllum bioRxiv preprint doi: https://doi.org/10.1101/2019.12.22.886283; this version posted December 23, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 4 42 Background 43 Plastid genome structure and content is highly conserved among most of the ~500,000 44 species of land plants and their closest green algal relatives. Nevertheless, widespread loss or 45 pseudogenization of photosynthetic genes is a familiar feature of the plastids of diverse non- 46 photosynthetic plant lineages, reflecting the reduced need for photosynthetic genes in lineages 47 with heterotrophic strategies. Accumulating evidence, however, has increasingly documented the 48 loss of “accessory” photosynthetic genes, only conditionally essential under stress, in fully 49 photosynthetic plants. Although not universal, many of these losses are associated with highly 50 specialized life history traits such as aquatic habit [1–3], carnivory [4, 5], and a 51 mycoheterotrophic life-stage [6]; the functional significance of these losses remains enigmatic 52 [7]. 53 Saniculiphyllum guangxiense C.Y. Wu & T.C. Ku is a semi-aquatic flowering plant now 54 restricted to a miniscule area in Yunnan province, China. It grows partially submersed in the 55 flow of small shaded waterfalls, and is critically endangered, with only four small extant 56 populations in an area ~10 km2 known to science, as well as several other populations known to 57 have been extirpated within the last 30 years [8]. Consistent with the isolated morphological and 58 ecological traits of this lineage within the family Saxifragaceae, its phylogenetic affinities remain 59 uncertain. The most recent attempts to place this species [8–10] exhibit strong disagreement. [8], 60 using six loci generated by Sanger sequencing, could not confidently place this lineage beyond 61 its membership in the Heucheroid clade, while [9], using the same genetic loci, were able to 62 place this lineage with 0.93-1.0 posterior probability (depending on the analysis) as sister to the 63 Boykinia group, a difference Deng et al. attribute to alignment differences in a single rapidly 64 evolving genetic locus (ITS). Relationships in these studies based on Sanger sequencing data bioRxiv preprint doi: https://doi.org/10.1101/2019.12.22.886283; this version posted December 23, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 5 65 differ substantially in several areas from those recovered on the basis of more than 300 nuclear 66 genes [10], where Saniculiphyllum was placed with moderate bootstrap support (80%) as sister to 67 a clade containing the Astilbe and Boykinia groups. 68 In the course of organellar genome surveys across Saxifragales, we found anomalous 69 photosynthetic gene sequences in Saniculiphyllum. Here, we report new plastid genome 70 sequences of phylogenetically pivotal taxa, analyze plastid gene evolution across the 71 Saxifragales and place the Saniculiphyllum plastid genome in a phylogenetic context to assess 72 evolutionary relationships and rates of plastid evolution. 73 74 Results 75 Assembly results—For all samples, NOVOPlasty successfully assembled a complete 76 circular genome. We individually confirmed all sequence features noted below by mapping the 77 reads back to the assembly, and found no evidence of misassembly. 78 Basic genome features—Saniculiphyllum has a chloroplast genome 151,704 bp long (Fig. 79 1). The large-scale structure of the genome is canonical for land plants, with an inverted repeat 80 (26,109 bp) separating the large-single-copy region (LSC; 84,479 bp) and small-single-copy 81 region (SSC, 15,007 bp). Excluding putative pseudogenes, gene content was as expected, 82 comprising 73 distinct protein-coding genes, 30 tRNA genes, and 4 rRNA genes. 83 Evidence for pseudogenization—We found genomic evidence for pseudogenization in 5 84 genes of the NDH complex (ndhA, ndhB, ndhD, ndhF, and ndhK), and two other photosynthetic 85 genes (cemA, ccsA), summarized in Table 1. These were either driven by frame-shift mutations 86 (ccsA, ndhA, ndhD, and ndhF) or by premature stop codons without a frameshift (due to a point 87 mutation in ndhB and a short inversion in ndhK). Three genes (cemA, ndhD, and ndhF) lack bioRxiv preprint doi: https://doi.org/10.1101/2019.12.22.886283; this version posted December 23, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 6 88 much of the conserved gene sequence due to large deletions >100 bp. Among these, cemA has no 89 premature stop codons, but it has an unconventional predicted protein size (5 extra amino acids) 90 in a gene that otherwise shows no size variation in Saxifragales; while lacking 18% of the 3’ end 91 of this gene, Saniculiphyllum has 137 additional bp before a novel stop codon, the sequence of 92 which is homologous with adjacent intergenic spacers in its relatives, making it unlikely that this 93 sequence is functional. Additionally, frameshift has resulted in the loss of the conserved stop 94 codon site of ndhA. The three genes with large deletions (cemA, ndhD, and ndhF) also have 95 hydrophobicity outside the range of variation of other Saxifragales (cemA 50% hydrophobic 96 amino acids vs. the 95% confidence interval for other Saxifragales [50.4%, 52.2%]; ndhD 47.8% 97 vs. [62.2%, 63.6%]; ndhF 54.9% vs. [55.6%, 58.2%]). bioRxiv preprint doi: https://doi.org/10.1101/2019.12.22.886283; this version posted December 23, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license.
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