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Cassytha) and Insights Into the Plastid Phylogenomics of Lauraceae

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Cassytha) and Insights Into the Plastid Phylogenomics of Lauraceae GBE Plastome Evolution in the Sole Hemiparasitic Genus Laurel Dodder (Cassytha) and Insights into the Plastid Phylogenomics of Lauraceae Chung-Shien Wu1,†, Ting-Jen Wang1,†,Chia-WenWu1, Ya-Nan Wang2, and Shu-Miaw Chaw1,* 1Biodiversity Research Center, Academia Sinica, Taipei 11529, Taiwan 2School of Forestry and Resource Conservation, Nation Taiwan University, Taipei 10617, Taiwan *Corresponding author: E-mail: [email protected]. †These authors contributed equally to this work. Accepted: September 6, 2017 Data deposition: This project has been deposited at DDBJ under the accession numbers LC210517, LC212965, LC213014, and LC228240. Abstract To date, little is known about the evolution of plastid genomes (plastomes) in Lauraceae. As one of the top five largest families in tropical forests, the Lauraceae contain many species that are important ecologically and economically. Lauraceous species also provide wonderful materials to study the evolutionary trajectory in response to parasitism because they contain both nonparasitic and parasitic species. This study compared the plastomes of nine Lauraceous species, including the sole hemiparasitic and herbaceous genus Cassytha (laurel dodder; here represented by Cassytha filiformis). We found differential contractions of the canonical inverted repeat (IR), resulting in two IR types present in Lauraceae. These two IR types reinforce Cryptocaryeae and Neocinnamomum— Perseeae–Laureae as two separate clades. Our data reveal several traits unique to Cas. filiformis, including loss of IRs, loss or pseudogenization of 11 ndh and rpl23 genes, richness of repeats, and accelerated rates of nucleotide substitutions in protein- coding genes. Although Cas. filiformis is low in chlorophyll content, our analysis based on dN/dS ratios suggests that both its plastid house-keeping and photosynthetic genes are under strong selective constraints. Hence, we propose that short generation time and herbaceous lifestyle rather than reduced photosynthetic ability drive the accelerated rates of nucleotide substitutions in Cas. filiformis. Key words: laurel, Lauraceae, hemiparasitic plant, plastid genome, substitution rate, genome rearrangement. Introduction studies have shown gene loss and plastome reduction in re- The primary function of plastids is photosynthesis, which pro- lation to the degree of parasitism in Cuscuta (Braukmann et al. duces essential carbon resources and allows for autotrophy. 2013) and Orobanchaceae (Wicke et al. 2016). Parasitic plants Plastid genomes (plastomes) of seed plants are highly con- have developed a differential organ, the haustorium, to pen- served in size, organization, and gene content (Jansen and etrate hosts for exploiting water and nutrients. In contrast, Ruhlman 2012). They typically have a quadripartite structure mycoheterotrophic plants do not penetrate another plant with a pair of canonical inverted repeats (IRA,IRB) separated by and obtain living resources with help from fungi. Despite their large single copy (LSC) and small single copy (SSC) regions. different ways of survival, these two groups share a similar However, when plants encounter lost or decreased photosyn- pattern related to loss of plastid genes (Barrett et al. 2014; thetic (PS) ability, their plastomes are subjected to relaxation Wicke et al. 2016), which indicates the convergence of plas- of selective constraints on the organization and gene content. tomic evolution. As a result, reductive and rearranged plastomes are often a There are 4,500 parasitic plants in 20 flowering plant hallmark of parasitic plants (Krause 2011; Wicke et al. 2011). families. It was proposed that flowering parasites have Parasitic plants provide excellent materials to study plas- evolved at least 11 times independently (Barkman et al. tomic evolution in response to altered lifestyles. Previous 2007). Despite low efficiency, most flowering parasites are ß The Author(s) 2017. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact [email protected] 2604 Genome Biol. Evol. 9(10):2604–2614. doi:10.1093/gbe/evx177 Advance Access publication September 6, 2017 Plastome Evolution in the Sole Hemiparasitic Genus Laurel Dodder GBE still able to perform photosynthesis (Heide-Jørgesen 2008). DNA Extraction and Plastome Sequencing and Assembly Thus, PS parasites are all hemiparasitic. However, only a tiny For each species, 2 g ground tissue was used for DNA extrac- fraction, circa 390 species, of flowering parasites are holopar- tion with the CTAB method (Stewart and Via 1993). The asitic. These holoparasites lack PS ability and require hosts to yielded DNA was sheared into 450 bp fragments for library complete their life cycle. Retention of PS ability in hemipara- construction. For Cas. filiformis, Cin. camphora,andCry. chi- sites was thought to have advantages in providing energy nensis, sequencing was conducted on an Illumina Hiseq 2500 before parasitizing hosts or to support development of flow- platform at Yourgene Bioscience (New Taipei City), and ers and fruit (Tesitel 2016). 2 Gb of 126 bp paired-end reads was obtained for each Lauraceae (laurel family) is the largest family of Laurales, species. For Neo. delavayi, 2 Gb of 150 bp paired-end reads grouped in magnoliids of the “basal angiosperms” clade were sequenced by using the Illumina NextSeq 500 platform (Jansen et al. 2007). The laurel family includes 3,000 spe- at Genomics (New Taipei City). cies (Christenhusz and Byng 2016). They are woody trees We used CLC Genomics Workbench 4.9 (CLC Bio, Arhus, or shrubs, except for the herbaceous vine genus Cassytha, Denmark) for quality trimming and de novo assembling. The the laurel dodder, which contains a dozen hemiparasitic thresholds for trimming were error probability < 0.01, ambig- species. Although many Lauraceous species are the major uous nucleotides ¼ 1, and removal of <15 bp reads, and components of tropical and subtropical forests, the avail- parameters for assembling were word size ¼ 31, bubble size ability of their plastomes is limited to nine species that rep- 50, minimum contig length ¼ 1 kb, and mapping reads to resent only six of the 45 genera (http://www.ncbi.nlm.nih. contigs. Contigs with 50Â sequencing depths were used gov/genbank/, last accessed on February 2017). Previously, in BLAST searches against the plastome sequences of molecular phylogenetics of Lauraceae was mostly based on Machilus balansae (NC028074), and those with <10À10 E-val- a single or a few loci (Rohwer 2000; Chanderbali et al. ues were considered plastomic contigs. Gaps between the 2001; Rohwer and Rudolph 2005; Wang et al. 2010). plastomic contigs were closed with sequences of PCR ampli- The plastid phylogenomic approach, which constructs trees cons obtained by using specific primers (supplementary table from most of the genes encoded in plastomes, was rarely S1, Supplementary Material online). The complete plastome used for estimating intergeneric relationships of Lauraceae. sequences were imported into CLC Genomics Workbench to In addition, unlike the other parasitic family of magnoliids, estimate average sequencing depths with the parameters of Hydnoraceae, in which all species are parasitic, the sole mismatch cost ¼ 2, insertion cost ¼ 3, deletion cost ¼ 3, length herbaceous and parasitic genus, Cassytha, allows for fraction ¼ 0.5, and similarity fraction ¼ 0.8. Plastome maps within-family comparisons of plastomes between parasitic were visualized by using Circos 0.67 (Krzywinski et al. 2009). and nonparasitic species and between herbaceous and woody plants. To this end, we have sequenced the plastomes of Plastome Annotation Cassytha filiformis and its three nonparasitic relatives. Gene prediction was performed in DOGMA (Wyman et al. With these and other available plastomes, we aimed to 1) 2004) and tRNA genes were predicted by using tRNAscan-SE use plastid phylogenomics to infer the phylogeny of 1.21 (Schattner et al. 2005). The boundaries of predicted Lauraceous genera, 2) uncover the dynamics of plastomic genes/exons were confirmed by aligning them with their organizations and nucleotide substitution rates in the laurel orthologous genes/exons of other magnoliid species. family, and 3) compare the plastomes between parasitic Repeats were identified with BlastN (NCBI) by searching and nonparasitic species within Lauraceae to understand each plastome against itself. We discarded the repeats with the evolution of traits relevant to altered lifestyles in the sequence identity < 90%. parasitic Cas. filiformis. Materials and Methods Sequence Alignment and Phylogenetic Tree Construction Sequences of the 67 shared protein-coding genes were Collection of Plant Materials extracted from the plastomes of the 20 examined basal angio- Fresh stems of Cas. filiformis (voucher Chaw 1498) were col- sperms (supplementary table S1, Supplementary Material on- lected from an individual growing at the seashore in Tainan line). For each genes, MUSCLE (Edgar 2004) implemented in City. For Cinnamomum camphora (voucher Chaw 1510), MEGA 6.06 (Tamura et al. 2013) was used for sequence align- Cryptocarya chinensis (voucher Chaw 1500), and ment with the option of aligning codons. All gene alignments
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