Evolutionary Comparisons of the Chloroplast Genome in Lauraceae and Insights into Loss Events in the Magnoliids

GBE Evolutionary Comparisons of the Chloroplast Genome in Lauraceae and Insights into Loss Events in the Magnoliids Yu Song1,2,†, Wen-Bin Yu1,2,†, Yunhong Tan1,2,†, Bing Liu3, Xin Yao1, Jianjun Jin4, Michael Padmanaba1, Jun-Bo Yang4,*, and Richard T. Corlett1,2,* 1 Center for Integrative Conservation, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla, China 2 Southeast Asia Biodiversity Research Institute, Chinese Academy of Sciences, Yezin, Nay Pyi Taw, Myanmar 3 State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing, China 4 Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, China *Corresponding authors: E-mails: ; . † These authors contributed equally to this work. Accepted: September 1, 2017 Data deposition: This project has been deposited at GenBank of NCBI under the accession number MF939337 to MF939351. Abstract Available plastomes of the Lauraceae show similar structure and varied size, but there has been no systematic comparison across the family. In order to understand the variation in plastome size and structure in the Lauraceae and related families of magnoliids, we here compare 47 plastomes, 15 newly sequenced, from 27 representative genera. We reveal that the two shortest plastomes are in the parasitic Lauraceae genus Cassytha, with lengths of 114,623 (C. filiformis) and 114,963 bp (C. capillaris), and that they have lost NADH dehydrogenase (ndh) genes in the large single-copy region and one entire copy of the inverted repeat (IR) region. The plastomes of the core Lauraceae group, with lengths from 150,749 bp (Nectandra angustifolia) to 152,739 bp (Actinodaphne trichocarpa), have lost trnI-CAU, rpl23, rpl2, a fragment of ycf2, and their intergenic regions in IRb region, whereas the plastomes of the basal Lauraceae group, with lengths from 157,577 bp (Eusideroxylon zwageri) to 158,530 bp (Beilschmiedia tungfangensis), have lost rpl2 in IRa region. The plastomes of Calycanthus (Calycanthaceae, Laurales) have lost rpl2 in IRb region, but the plastome of Caryodaphnopsis henryi (Lauraceae) remain intact, as do those of the nonLaurales magnoliid genera Piper, Liriodendron, and Magnolia. On the basis of our phylogenetic analysis and structural comparisons, different loss events occurred in different lineages of the Laurales, and fragment loss events in the IR regions have largely driven the contraction of the plastome in the Lauraceae. These results provide new insights into the evolution of the Lauraceae as well as the magnoliids as a whole. Key words: Lauraceae, chloroplast, genome, phylogenetic relationship, loss event. Introduction In land plants, most chloroplast genomes are single, circular, double-stranded DNA sequences 100–220 kb in size, with a quadripartite structure including one large single-copy (LSC) region, one small single-copy (SSC) region, and a pair of inverted repeat (IR) regions (Bock 2007). Together these regions include >30 structural RNA genes and around 80 protein-coding genes, with the latter including genes related to photosynthesis, transcription or translation, and other functions (Gao et al. 2010). Generally, the ribosomal RNA genes are in the IR region, almost all of the photosynthesis related genes in the LSC region, and a number of the NADPH dehydrogenase genes in the SSC region. The plastomes of land plants originated once, from a free-living algal ancestor (Turmel et al. 2006), but the gene contents and order vary considerably among species, and significant structural rearrangements and gene losses have been reported in several unrelated lineages, including ferns (Roper et al. 2007; Karol et al. 2010), gnetophytes (McCoy et al. 2008; Wu et al. 2009), and multiple angiosperm families (Goremykin et al. 2003a; Cai et al. 2006), as well as nonphotosynthetic plants (Wicke et al. 2016). ß The Author 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 2354 Genome Biol. Evol. 9(9):2354–2364. doi:10.1093/gbe/evx180 Advance Access publication September 4, 2017 GBE Evolutionary Comparison of the Plastome in the Magnoliids Comparative analyses of the plastomes of algae and embryophytes show that four genes, tufA, ftsH, odpB, and rpl5, have been lost or transferred to the nucleus and three genes, matK, ycf1, and ycf2, have been gained in charophyte algae and embryophytes (Turmel et al. 2006). For example, the tufA gene, encoding chloroplast protein synthesis elongation factor Tu, is encoded in the plastomes of most algae, but is a pseudogene in Isoetes, fragmented in Anthoceros, cycads, and Gingko, and completely lost in the angiosperms (Karol et al. 2010). Within the angiosperms, three genes, ycf1, ycf2, and accD, have been lost in the Poaceae (Guisinger et al. 2010), whereas rpl22, infA, and accD were lost in the legumes, Lemnoideae, and Acoraceae, respectively (Wang and Messing 2011; Goremykin et al. 2005; Doyle et al. 1995). In plants with a heterotrophic lifestyle, pseudogenization and entire loss events of ndh-genes were detected (Wickett et al. 2008; Barrett et al. 2014; Wicke et al. 2016). However, the ndh-gene loss events have also occurred in autotrophic orchids, gnetophytes, and Pinaceae (Braukmann et al. 2009; Kim et al. 2015; Wakasugi et al. 1994). In addition to gene losses, large inversions, and other structural rearrangements have been also reported. In ferns and seed plants, a 30-kb fragment flanked by the complete matK and rpoC2 has been identified as an inversion, with gene organization different from that in liverworts, mosses, hornworts, lycophytes, and Chaetosphaeridium (Wickett et al. 2011). In rice, maize, Calamus, and orchids, two identical trnH-rps19 gene clusters were detected as a duplication event before the diversification of extant monocot lineages (Chang et al. 2006; Wang et al. 2008; Luo et al. 2016). In Tetracentron and Trochodendron, a 4-kb extra region containing the five genes rpl22, rps3, rpl16, rpl14, and rps8 was found as evidence for unstable boundaries of the IR region across early-diverging eudicots (Sun et al. 2013, 2016). Interestingly, most of the rearrangements were detected in the boundary regions of IR, suggesting that the IR regions represent hotspots for structural rearrangements within the plastome (Wicke et al. 2011; Zhu et al. 2016). The IR regions in the plastome of angiosperms have been used as evolutionary markers for elucidating relationships among some taxa, because they are frequently subject to contraction, expansion, or even complete loss (L (...truncated)