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In order to understand the evolution of the orchid plastome, we annotated and compared 124 complete plastomes of Orchidaceae representing all the major lineages in their structures, gene contents, gene rearrangements, and IR contractions/expansions. Forty-two of these plastomes were generated from the corresponding author's laboratory, and 24 plastomes-including nine genera ( , , , , , , , and )-are new in this study. All orchid plastomes, except and have a quadripartite structure consisting of a large single copy (LSC), two inverted repeats (IRs), and a small single copy (SSC) region. The IR region was completely lost in the plastomes. The SSC is lost in the plastome. The smallest plastome size was 19,047 bp, in and the largest plastome size was 178,131 bp, in . The small plastome sizes are primarily the result of gene losses associated with mycoheterotrophic habitats, while the large plastome sizes are due to the expansion of noncoding regions. The minimal number of common genes among orchid plastomes to maintain minimal plastome activity was 15, including the three subunits of (14, 16, and 36), seven subunits of (2, 3, 4, 7, 8, 11, and 14), three subunits of (5, 16, and 23), C-GCA, and P genes. Three stages of gene loss were observed among the orchid plastomes. The first was gene loss, which is widespread in Apostasioideae, Vanilloideae, Cypripedioideae, and Epidendroideae, but rare in the Orchidoideae. The second stage was the loss of photosynthetic genes ( , and ) and gene subunits, which are restricted to and some species of and . The third stage was gene loss related to prokaryotic gene expression ( , , and others), which was observed in , , and In addition, an intermediate stage between the second and third stage was observed in (Vanilloideae). The majority of intron losses are associated with the loss of their corresponding genes. In some orchid taxa, however, introns have been lost in 16 16, and P(2) without their corresponding gene being lost. A total of 104 gene rearrangements were counted when comparing 116 orchid plastomes. Among them, many were concentrated near the IRa/b-SSC junction area. The plastome phylogeny of 124 orchid species confirmed the relationship of {Apostasioideae [Vanilloideae (Cypripedioideae (Orchidoideae, Epidendroideae))]} at the subfamily level and the phylogenetic relationships of 17 tribes were also established. Molecular clock analysis based on the whole plastome sequences suggested that Orchidaceae diverged from its sister family 99.2 mya, and the estimated divergence times of five subfamilies are as follows: Apostasioideae (79.91 mya), Vanilloideae (69.84 mya), Cypripedioideae (64.97 mya), Orchidoideae (59.16 mya), and Epidendroideae (59.16 mya). We also released the first nuclear ribosomal (nr) DNA unit (18S-ITS1-5.8S-ITS2-28S-NTS-ETS) sequences for the 42 species of Orchidaceae. Finally, the phylogenetic tree based on the nrDNA unit sequences is compared to the tree based on the 42 identical plastome sequences, and the differences between the two datasets are discussed in this paper.

Lindera Thunb. (Lauraceae) consists of approximately 100 species, mainly distributed in the temperate and tropical regions of East Asia. In this study, we report 20 new, complete plastome sequences including 17 Lindera species and three related species, Actinodaphne lancifolia, Litsea japonica and Sassafras tzumu. The complete plastomes of Lindera range from 152,502 bp (L. neesiana) to 154,314 bp (L. erythrocarpa) in length. Eleven small inversion (SI) sites are documented among the plastomes. Six of the 11 SI sites are newly reported and they locate in rpoB-trnC, psbC-trnS, petA-psbJ, rpoA and ycf2 regions. The distribution patterns of SIs are useful for species identification. An average of 83 simple sequence repeats (SSRs) were detected in each plastome. The mono-SSRs accounted for 72.7% of total SSRs, followed by di- (12.4%), tetra- (9.4%), tri- (4.2%), and penta-SSRs (1.3%). Of these SSRs, 64.6% were distributed in an intergenic spacer (IGS) region. In addition, 79.8% of the SSRs are located in a large single copy (LSC) region. In contrast, almost no SSRs are distributed in inverted repeat (IR) regions. The SSR loci are useful to identifying species but the phylogenetic value is low because the majority of them show autapomorphic status or highly homoplastic characteristics. The nucleotide diversity (Pi) values also indicated the conserved nature of the IR region compared to LSC and small single copy (SSC) regions. Five spacer regions with high Pi values, trnH-psbA, petA-psbJ and ndhF-rpl32, rpl32-trnL and Ψycf1-ndhF, have a potential use for the molecular identification study of Lindera and related species. Lindera species form a paraphyletic group in the plastome tree because of the inclusion of related genera such as Actinodaphne, Laurus, Litsea and Neolitsea. A former member of tribe Laureae, Sassafras, forms a clade with the tribe Cinnamomeae. The SIs do not affect the phylogenetic relationship of Laureae. This result indicated that ancient plastome captures may have contribute to the mixed intergeneric relationship of Laureae. Alternatively, the result may indicate that the morphological characters defined the genera of Lauraceae originated for several times.

Gastrodia pubilabiata is a nonphotosynthetic and mycoheterotrophic orchid belonging to subfamily Epidendroideae. Compared to other typical angiosperm species, the plastome of G. pubilabiata is dramatically reduced in size to only 30,698 base pairs (bp). This reduction has led to the loss of most photosynthesis-related genes and some housekeeping genes in the plastome, which now only contains 19 protein coding genes, three tRNAs, and three rRNAs. In contrast, the typical orchid species contains 79 protein coding genes, 30 tRNAs, and four rRNAs. This study decoded the entire mitogenome of G. pubilabiata, which consisted of 44 contigs with a total length of 867,349 bp. Its mitogenome contained 38 protein coding genes, nine tRNAs, and three rRNAs. The gene content of G. pubilabiata mitogenome is similar to the typical plant mitogenomes even though the mitogenome size is twice as large as the typical ones. To determine possible gene transfer events between the plastome and the mitogenome individual BLASTN searches were conducted, using all available orchid plastome sequences and flowering plant mitogenome sequences. Plastid rRNA fragments were found at a high frequency in the mitogenome. Seven plastid protein coding gene fragments (ndhC, ndhJ, ndhK, psaA, psbF, rpoB, and rps4) were also identified in the mitogenome of G. pubilabiata. Phylogenetic trees using these seven plastid protein coding gene fragments suggested that horizontal gene transfer (HGT) from plastome to mitogenome occurred before losses of photosynthesis related genes, leading to the lineage of G. pubilabiata. Compared to species phylogeny of the lineage of orchid, it was estimated that HGT might have occurred approximately 30 million years ago.

The Vanilloideae (vanilloids) is one of five subfamilies of Orchidaceae and is composed of fourteen genera and approximately 245 species. In this study, the six new chloroplast genomes (plastomes) of vanilloids (two Lecanorchis, two Pogonia, and two Vanilla species) were decoded, and then the evolutionary patterns of plastomes were compared to all available vanilloid plastomes. Pogonia japonica has the longest plastome, with 158,200 bp in genome size. In contrast, Lecanorchis japonica has the shortest plastome with 70,498 bp in genome size. The vanilloid plastomes have regular quadripartite structures, but the small single copy (SSC) region was drastically reduced. Two different tribes of Vanilloideae (Pogonieae and Vanilleae) showed different levels of SSC reductions. In addition, various gene losses were observed among the vanilloid plastomes. The photosynthetic vanilloids (Pogonia and Vanilla) showed signs of stage 1 degradation and had lost most of their ndh genes. The other three species (one Cyrotsia and two Lecanorchis), however, had stage 3 or stage 4 degradation and had lost almost all the genes in their plastomes, except for some housekeeping genes. The Vanilloideae were located between the Apostasioideae and Cypripedioideae in the maximum likelihood tree. A total of ten rearrangements were found among ten Vanilloideae plastomes when compared to the basal Apostasioideae plastomes. The four sub-regions of the single copy (SC) region shifted into an inverted repeat (IR) region, and the other four sub-regions of the IR region shifted into the SC regions. Both the synonymous (dS) and nonsynonymous (dN) substitution rates of IR in-cooperated SC sub-regions were decelerated, while the substitution rates of SC in-cooperated IR sub-regions were accelerated. A total of 20 protein-coding genes remained in mycoheterotrophic vanilloids. Almost all these protein genes show accelerated base substitution rates compared to the photosynthetic vanilloids. Two of the twenty genes in the mycoheterotrophic species faced strong “relaxed selection” pressure (p-value < 0.05).

The genus Zoysia Willd. (Chloridoideae) is widely distributed from the temperate regions of Northeast Asia—including China, Japan, and Korea—to the tropical regions of Southeast Asia. Among these, four species—Zoysia japonica Steud., Zoysia sinica Hance, Zoysia tenuifolia Thiele, and Zoysia macrostachya Franch. & Sav.—are naturally distributed in the Korean Peninsula. In this study, we report the complete plastome sequences of these Korean Zoysia species (NCBI acc. nos. MF953592, MF967579~MF967581). The length of Zoysia plastomes ranges from 135,854 to 135,904 bp, and the plastomes have a typical quadripartite structure, which consists of a pair of inverted repeat regions (20,962~20,966 bp) separated by a large (81,348~81,392 bp) and a small (12,582~12,586 bp) single-copy region. In terms of gene order and structure, Zoysia plastomes are similar to the typical plastomes of Poaceae. The plastomes encode 110 genes, of which 76 are protein-coding genes, 30 are tRNA genes, and four are rRNA genes. Fourteen genes contain single introns and one gene has two introns. Three evolutionary hotspot spacer regions—atpB~rbcL, rps16~rps3, and rpl32~trnL-UAG—were recognized among six analyzed Zoysia species. The high divergences in the atpB~rbcL spacer and rpl16~rpl3 region are primarily due to the differences in base substitutions and indels. In contrast, the high divergence between rpl32~trnL-UAG spacers is due to a small inversion with a pair of 22 bp stem and an 11 bp loop. Simple sequence repeats (SSRs) were identified in 59 different locations in Z. japonica, 63 in Z. sinica, 62 in Z. macrostachya, and 63 in Z. tenuifolia plastomes. Phylogenetic analysis showed that the Zoysia (Zoysiinae) forms a monophyletic group, which is sister to Sporobolus (Sporobolinae), with 100% bootstrap support. Within the Zoysia clade, the relationship of (Z. sinica, Z japonica), (Z. tenuifolia, Z. matrella), (Z. macrostachya, Z. macrantha) was suggested.

In this study, we report the first complete plastome sequence of Vitex rotundifolia (Lamiaceae) (MT937186). In addition, the plastome sequences of Phryma leptostachya subsp. asiatica (Phrymaceae) (153,324 bp; MT948145) and Mazus pumilus (Mazaceae) (152,847 bp; MT937187) are also included. The gene orders and structures of the three plastomes are collinear with those of the typical plastome of angiosperm. The plastome size of V. rotundifolia is 154,370 bp in length and consists of a large single-copy region of 85,079 bp and a small single-copy region of 17,917 bp, which are separated by a pair of 25,687 bp-long inverted repeat regions. In addition, the plastome sizes of P. leptostachya subsp. asiatica and M. pumilus are 153,324 bp and 152,847 bp, respectively. The three plastomes contain 113 genes, including 79 protein-coding, 30 tRNA, and four rRNA genes. Sixteen genes contain one intron and two genes have two introns. A total of 41 simple sequence repeat loci was identified in the V. rotundifolia plastome. Phylogenetic analysis shows that Viticoideae is a sister group of the last of Lamiaceae except Nepetoideae. The Mazaceae are a sister group of Lamiaceae, while Phrymaceae form a sister group to the Paulowniaceae-Orobanchaceae clade.

In this study, we determined the complete plastome sequence of Gonocaryum lobbianum (Miers) Kurz (Cardiopteridaceae) (NCBI acc. no. MK390345). This is the first reported complete plastome sequence from the family Cardiopteridaceae of the order Aquifoliales. The complete plastome of G. lobbianum is 158,905 bp in length and consists of a large single copy of 87,705 bp and a small single copy of 19,346 bp, separated by two inverted repeats of 25,927 bp. The plastome contains 112 genes, of which 78 are protein-coding genes, 30 are tRNA genes, and four are rRNA genes. The rpoA gene was pseudogenized because of deletion and following frame-shift mutations. We also confirmed the pseudonization of rpoA gene using PCR and conventional Sanger sequencing methods. Sixteen genes contain one intron and two genes have two introns. The average A-T content of the plastome is 62.7%. A total of 73 simple sequence repeat loci were identified within the genome. Phylogenetic analysis revealed that G. lobbianum is a sister group of Aquifoliaceae-Helwingiaceae with 100% bootstrap value. The Aquifoliales clade is a sister group to the Apiales-Asterales-Dipsacales clade with 100% bootstrap support.

In this study, we determined the complete plastome sequence of Bunchosia argentea (Jacq.) DC. (Malpighiaceae) (NCBI acc. no. MK390344). The gene order and the structure of the B. argentea plastome are collinear with those of the typical plastomes of land plants. The complete plastome size is 158,741 bp in length and consists of a large single-copy region of 88,345 bp and a small single-copy region of 16,816 bp, which are separated by a pair of 26,790 bp-long inverted repeat regions. The overall A-T content of the plastome sequence is 63.5%. The plastome contains 110 genes, of which 76 are protein-coding genes, 30 are tRNA genes, and four are rRNA genes. The rpl32 was lost and two genes (infA and rps7) were pseudogenized. Sixteen genes contain one intron and two genes have two introns. A total of 87 simple sequence repeat loci were identified within the genome. Phylogenetic analysis revealed that B. argentea and two Byrsonima species formed a clade with 100% bootstrap support.

In this study, we determined the complete plastome sequence of Pouteria campechiana (Kunth) Baehni (Sapotaceae) (NCBI acc. no. KX426215). This is the first time a plastome from the Sapotaceae has been sequenced. The gene order and structure of the P. campechiana plastome are collinear with those of the typical plastome of land plants. The complete plastome size is 157,922 bp in length and consists of a large single-copy region of 87,122 bp and a small single-copy region of 18,559 bp, which are separated by a pair of 26,120 bp-long inverted repeat regions. The overall A–T content of the plastome sequence is 63.2%. The plastome contains 113 genes, of which 79 are protein-coding genes, 30 are tRNA genes, and 4 are rRNA genes. Sixteen genes contain one intron and two genes have two introns. A total of 91 simple sequence repeat loci were identified within the genome. Phylogenetic analysis revealed that P. campechiana is a sister group of the Primulaceae-Ebenaceae clade with 100% bootstrap support.

In this study, we determined the complete plastome sequence of Psidium guajava L. (Myrtaceae) (NCBI acc. no. KX364403). The gene order and structure of the P. guajava plastome are similar to those of a typical angiosperm. The complete plastome is 158,841 bp in length, and consists of a large single copy of 87,675 bp and a small single copy of 18,464 bp, separated by two inverted repeats of 26,351 bp. The overall AT content of the sequence is 63.0%. The plastome contains 112 genes, of which 78 are protein-coding genes, 30 are tRNA genes, and four are rRNA genes. Sixteen genes contain one intron and two genes have two introns. A total of 100 simple sequence loci were identified from the genome. Phylogenetic analysis revealed that P. guajava is a sister group of Eugenia uniflora with 100% bootstrap support.