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Enlarged and Highly Repetitive Plastome of Lagarostrobos and Plastid 2 Phylogenomics of Podocarpaceae

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Enlarged and Highly Repetitive Plastome of Lagarostrobos and Plastid 2 Phylogenomics of Podocarpaceae bioRxiv preprint doi: https://doi.org/10.1101/392357; this version posted August 16, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 Enlarged and highly repetitive plastome of Lagarostrobos and plastid 2 phylogenomics of Podocarpaceae 3 4 Edi Sudiantoa,b,c, Chung-Shien Wuc, Lars Leonhardd, William F. Martine,*, and Shu- 5 Miaw Chawa,c,* 6 7 aBiodiversity Program, Taiwan International Graduate Program, Academia Sinica and 8 National Taiwan Normal University, Taipei 11529, Taiwan 9 bDepartment of Life Science, National Taiwan Normal University, Taipei 11677, 10 Taiwan 11 cBiodiversity Research Center, Academia Sinica, Taipei 11529, Taiwan 12 dBotanical Garden, Heinrich-Heine-University, 40225 Düsseldorf, Germany 13 eInstitute of Molecular Evolution, Heinrich-Heine-University, 40225 Düsseldorf, 14 Germany 15 16 *Author for correspondence: 17 18 Dr. Shu-Miaw Chaw, Biodiversity Research Center, Academia Sinica, Taipei 11529, 19 Taiwan. Tel +886 2787 1021, Fax +886 2789 8711, E-mail: [email protected] 20 Prof. Dr. William Martin, Institute of Molecular Evolution, Heinrich-Heine-Universitaet 21 Düsseldorf, Universitätsstr. 1, 40225 Duesseldorf, Germany. Tel +49-211-811-3011, 22 Fax +49-211-811-3554, E-mail : [email protected] 23 24 Data deposition: The complete plastid genomes of eight Podocarpaceous genera have 25 been deposited at DDBJ under the accession numbers AP018899-AP018906. 26 27 Running header: Enlarged and highly repetitive plastome of Lagarostrobos 28 29 Declarations of interest: none 1 bioRxiv preprint doi: https://doi.org/10.1101/392357; this version posted August 16, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 30 Abstract 31 Podocarpaceae is the largest family in cupressophytes (conifers II), but their plastid 32 genomes (plastomes) are poorly studied, with plastome data currently existing for 33 only four of the 19 Podocarpaceous genera. In this study, we assembled the 34 plastomes from representatives of eight additional genera, including Afrocarpus, 35 Dacrydium, Lagarostrobos, Lepidothamnus, Microstrobos, Phyllocladus, Prumnopitys, 36 and Saxegothaea. We found that Lagarostrobos, a monotypic genus native to 37 Tasmania, has the largest plastome among any cupressophytes studied to date 38 (151,496 bp). Plastome enlargement in Lagarostrobos coincides with increased 39 intergenic spacers, repeats, and duplicated genes. Among Podocarpaceae, 40 Lagarostrobos has the most rearranged plastome, but its substitution rates are 41 modest. Plastid phylogenomic analyses clarify the positions of previously conflicting 42 Podocarpaceous genera. Tree topologies firmly support the division of 43 Podocarpaceae into two sister clades: (1) the Prumnopityoid clade and (2) the clade 44 containing Podocarpoid, Dacrydioid, Microstrobos, and Saxegothaea. The 45 Phyllocladus is nested within the Podocarpaceae, thus familial status of the 46 monotypic Phyllocladaceae is not supported. 47 48 Keywords: podocarp; cupressophytes; Huon pine; plastid genome; plastome 49 evolution; repetitive DNA 50 51 1. Introduction 52 Plastid genomes (plastomes) of seed plants have an average size of 145 kb and 53 contain highly conserved structure, including two large inverted repeats (IRs) and 54 two single copy (SC) regions (Jansen and Ruhlman, 2012). In seed plants, the smallest 55 plastome was found in a parasitic plant, Pilostyles (11 kb; Bellot and Renner, 2015), 56 while the largest one resides in Pelargonium transvaalense (242 kb; Tonti-Filippini et 57 al., 2017) with the IR longer than 70 kb. Plastid gene order is highly syntenic among 58 seed plants (Jansen and Ruhlman, 2012), except for some lineages, such as Jasminae 2 bioRxiv preprint doi: https://doi.org/10.1101/392357; this version posted August 16, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 59 (Lee et al., 2007), Trifolium subterraneum (Cai et al., 2008), Trachelium caeruleum 60 (Haberle et al., 2008), Geraniaceae (Guisinger et al., 2011), and cupressophytes (Wu 61 and Chaw 2014, 2016; Chaw et al. 2018). In Geraniaceae, the degree of plastomic 62 inversions is positively associated with the repeat abundance and their sizes (Weng 63 et al., 2014). Moreover, nucleotide substitution rates and inversion frequencies are 64 positively correlated in the plastomes of Geraniaceae (dN only; Weng et al., 2014) 65 and cupressophytes (both dN and dS; Wu and Chaw, 2016). 66 Generally, plastid protein-coding genes are single copy, except those in IRs (Xiong 67 et al., 2009). Seed plant IRs vary in size from 20 to 30 kb (Palmer, 1990), and their 68 expansion or contraction influences the number of duplicate genes as well as 69 plastome size. Typically, 15–17 duplicate genes are located in the IR of seed plants 70 (Zhu et al., 2016). However, extreme IR contraction or expansion has led to only one 71 or even >50 genes located in the IR of Pinaceae (Wakasugi et al. 1994; Lin et al., 72 2010; Sudianto et al., 2016) or Pelargonium x hortorum (Chumley et al., 2006), 73 respectively. Outside the IR, plastid gene duplication has been reported in Pinus 74 thunbergii (Wakasugi et al., 1994), Trachelium caeruleum (Haberle et al., 2008), 75 Euglena archaeoplastidiata (Bennett et al., 2017), Monsonia emarginata (Ruhlman et 76 al., 2017), and Geranium phaeum and G. reflexum (Park et al., 2017). Nevertheless, 77 mechanisms underlining gene duplication in SC regions remain poorly known. 78 Having lost their IR (Wu et al., 2011), cupressophytes (conifers II) offer excellent 79 resources to study the evolution of plastome size and gene duplication that are 80 irrelevant to IR expansion or contraction. It has been revealed that in 81 cupressophytes, synonymous substitution rates are negatively correlated with 82 plastome size (Wu and Chaw, 2016), in agreement with the mutational burden 83 hypothesis (Lynch, 2006). In addition, the cupressophyte plastomes are highly 84 rearranged with the lowest GC-content among gymnosperms (Chaw et al., 2018). 85 Only a few duplicate genes were reported in the cupressophyte plastomes, including 86 trnQ-UUG (Yi et al., 2013; Guo et al., 2014), trnN-GUU (Vieira et al., 2014, 2016; Wu 87 and Chaw, 2016), trnI-CAU and partial rpoC2 (Hsu et al., 2016), trnD-GUC (Vieira et 88 al., 2016), and rrn5 (Wu and Chaw, 2016). Most of these duplicate genes are involved 3 bioRxiv preprint doi: https://doi.org/10.1101/392357; this version posted August 16, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 89 in generating family-specific short IRs that are capable of mediating homologous 90 recombination (Wu and Chaw, 2016). 91 Podocarpaceae is the largest cupressophyte family, including three major clades 92 (Dacrydioid, Podocarpoid, and Prumnopityoid), 18–19 genera, and 173–187 species 93 (Biffin et al. 2011; Cernusak et al., 2011; Christenhusz and Byng, 2016). 94 Podocarpaceous species are mainly distributed in the Southern Hemisphere, with 95 the species diversity hotspot in Malesian (Enright and Jaffré, 2011). Previous 96 phylogenetic studies were inconclusive or controversial as to the positions of some 97 Podocarpaceous genera, such as Lagarostrobos, Lepidothamnus, Phyllocladus, and 98 Saxegothaea (Figure 1). For example, Conran et al. (2000) and Knopft et al. (2012) 99 placed Saxegothaea as the first diverging genus of Podocarpaceae, but six other 100 studies did not recover the same result. Moreover, Phyllocladus was once treated as 101 a monogeneric family (the so-called Phyllocladaceae), separate from Podocarpaceae 102 on the basis of morphological characteristics, chromosome numbers, and 103 phytochemistry (Keng, 1977, 1978; Molloy, 1996; Page, 1990). Nonetheless, various 104 molecular phylogenetic studies congruently held the genus belonging to 105 Podocarpaceae (Conran et al., 2000; Kelch, 2002; Biffin et al., 2011). The 106 classification of Prumnopityoid clade also varies across studies, e.g. Sinclair et al. 107 (2002) and Biffin et al. (2011, 2012) only included Lagarostrobos, Manoao, 108 Parasitaxus, Halocarpus, and Prumnopitys in the clade. Some authors, however, also 109 added Lepidothamnus (Knopft et al., 2012) or Phyllocladus (Conran et al., 2000; 110 Knopft et al. 2012) into the clade (see Figure 1). 111 Plastome diversity and evolution in the Podocarpaceae have yet to be 112 systematically studied. To date, only the plastomes of the four genera – Dacrycarpus, 113 Nageia, Podocarpus, and Retrophyllum, which are of the Dacrydioid and Podocarpoid 114 clades, have been reported. However, samplings of the two clades are 115 incomprehensive, and those of the Prumnopityoid clade have never been elucidated 116 before. These may lead us to underestimate the plastome complexity in the 117 Podocarpaceae. To this end, we have sequenced the complete plastomes from 118 another eight Podocarpaceous genera with four representatives from the 119 Prumnopityoid clade. The aim of this study was to (1) better sample Podocarpaceous 4 bioRxiv preprint doi: https://doi.org/10.1101/392357; this version posted August 16, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights
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