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By Hengzhao Liu † , Hang Ye † , Naiyu Zhang , Jiayu Ma † , Jiangtao Wang , Guojia Hu , Mengdi Li and Peng Zhao *
Key Laboratory of Resource Biology and Biotechnology in Western China, Ministry of Education, College of Life Sciences, Northwest University, Xi’an 710069, China
An elucidation of how the selection pressures caused by habitat environments affect plant plastid genomes and lead to the adaptive evolution of plants, is a very intense area of research in evolutionary biology. The genus Paphiopedilum is a predominant group of orchids that includes over 66 species with high horticultural and ornamental value. However, owing to the destructive exploitation and habitat deterioration of wild germplasm resources of Paphiopedilum, it needs more molecular genetic resources and studies on this genus. The chloroplast is cytoplasmically inherited and often used in evolutionary studies. Thus, for this study, we newly sequenced, assembled and annotated five chloroplast genomes of the Paphiopedilum species. The size of these genomes ranged from 155, 886 bp (P. henryanum) to 160, 503 bp (P. ‘GZSLKY’ Youyou) and they contained 121–122 genes, which consisted of 76 protein coding genes, eight ribosomal RNAs, and 37–38 transfer RNAs. Combined with the other 14 Paphiopedilum species, the characteristics of the repeat sequences, divergent hotspot regions, and the condo usage bias were evaluated and identified, respectively. The gene transfer analysis showed that some fragments of the ndh and ycf gene families were shared by both the chloroplast and nucleus. Although the genomic structure and gene content was conserved, there was a significant boundary shift caused by the inverted repeat (IR) expansion and small single copy (SSC) contraction. The lower GC content and loss of ndh genes could be the result of adaptive evolutionary responses to its unique habitats. The genes under positive selection, including accD, matK, psbM, rpl20, rps12, ycf1, and ycf2 might be regarded as potential candidate genes for further study, which significantly contribute to the adaptive evolution of Paphiopedilum.
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During the evolutionary processes of certain plants, changing environments and habitats may impose selective genetic pressures, which leave a footprint of natural selection in the genes involved with environmental adaptation [1]. As essential organelles, chloroplast (cp) genomes derived from the endosymbiosis between non-photosynthetic hosts and independent living cyanobacteria play an indispensable role in several vital biochemical processes and the photosynthesis of green plants [2]. Over the last decade, advanced modeling has increasingly been employed for resolving the deep phylogeny, phytogeography, as well as the molecular evolution and adaptive diversification of plants with the features of haploid inheritance, self-replication, relatively small size and slow mutation rates compared with the nuclear genome [1, 2, 3].
In general, the cp genome has a conservative circle structure, gene order, and genetic content in most flowering plants. It is typically comprised of two inverted repeat copies (IRa and IRb), a large single copy region (LSC), and a small single copy region (SSC) [3, 4, 5]. However, although the cp genome being much more conservative than nuclear genomes or mitochondrial genomes, the gene rearrangements, inversion, gene loss, inverted repeats expansion still occur in some green plant lineages. Moreover, there were many mutation events have been found in cp genomes, which are including insertions, deletions, substitutions, and inversions [6]. These disparities might be precisely the evidence or embodiment of adaptive evolution, which are considered as the improvement of plant species to adapt the environmental conditions changing and during their evolutionary processes.
Nevertheless, the courses, tempos, and modes of evolutionary and genomic architectural changes in recent speciation background are still not clear, due to the microevolution of cp genomes and genomes genes in flowering plants remaining largely unknown [2]. Thus, in-depth comparisons of cp genomes in closely related plant species are urgently required to significantly improve the evolutionary inferences sensitivity with genomic structural knowledge towards a thorough elucidation of the mechanisms, rates, and directionality of cp genome evolution.
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The genus Paphiopedilum Pfitz. belongs to the Orchidaceae family, which includes over 66 species, of which 18 are natively distributed as ornamental plants that span Southwest to South China due to their large and exquisite flowers [7, 8, 9, 10, 11]. Paphiopedilum are often referred to as slipper orchids as they possess a bag-like lip that is akin to ladies’ slippers [9, 10, 11]. They have significant ornamental, horticultural, and medicinal value and grow primarily within the cracks in cliffs, or rocky well-drained sites in evergreen broadleaved forests, at altitudes of ~1000 m as a type of terrestrial, lithophytic/epiphytic herb [12, 13, 14]. Their unique ecosystems make them ideal for the study of environmental adaptation and evolution [9, 10, 11].
Unfortunately, owing to the destructive exploitation and habitat deterioration of wild Paphiopedilum germplasm resources, it has been listed in the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) and is prohibited from ruthless collection and international exploitation [8, 15, 16]. Thus far, many species of Paphiopedilum have been designated as first-class protected plants in China, as well as being listed on the IUCN Red List of Endangered (EN) even Critically Endangered (CR) Species [15, 16, 17].
In past years, research into Paphiopedilum has focused primarily on ecological characteristics and cultivation [18, 19, 20], genetic diversity and differentiation based on DNA molecular markers (e.g., ITS and plastid gene fragments) [21, 22], and historical biogeography [14, 23]. Recently, there were some reports also focused on comparative analysis, phylogeny, and evolution based on the whole chloroplast genomes [9, 10, 11, 12]. With the rapid development of the Next-Generation Sequencing (NGS) technologies, many cp genomes of the Orchidaceae family along with the Paphiopedilum species were available in the public database [9, 10, 11, 12, 23, 24, 25, 26, 27]. These assembled cp genomes offered useful genetic data for Paphiopedilum phylogenetic and evolution studies [9, 10, 11, 12, 28, 29]. However, the phylogenetic relationships and evolution of Paphiopedilum are quite complex [12, 21, 22, 30]. Investigations into the evolution and adaption of this plant have rarely been reported. The lack of genome-wide investigations limits the capacity to identify genomic characteristics that are under natural selection. Consequently, additional molecular and genetic resources are urgently required to provide a genetic basis for comparative cp genomes, phylogeny, evolutionary biology, and effective protection strategies for Paphiopedilum.
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Moreover, the chromosomal karyotypes of different Paphiopedilum species are heterogeneous such that variable numbers of alleles present obstacles to genetic research based on nuclear genes [31, 32, 33]. Hence, in this case, the efficient and convenient cp genome which, with many advantages, has become an ideal tool for the genetic and evolutionary analysis of Paphiopedilum. Additionally, according to previous studies, the cp genomes of Paphiopedilum might provide unique opportunities to reveal the boundary shift impacts on cp genome structures and gene evolution due to their exceptional peculiarities [12, 34]. Owing to the large number of species of the Orchidaceae family in the world, cp genomes have been widely used in their phylogenetics, evolutionary biology, and population genetics [9, 10, 11, 12, 13, 14, 24, 25, 26, 27].
Thus, in this study, we performed comparative analyses to afford comprehensive insights into the evolution and adaptation of the cp genomes of several Paphiopedilum species. Firstly, in addition to a previous study, we sequenced and assembled five cp genomes of Paphiopedilum species. Secondly, we conducted comparative cp genome analyses for these five genomes in addition to the other fourteen chloroplast genomic sequences of Paphiopedilum, which were originally distributed in China [8] and obtained from GenBank (Table S1).
Subsequently, we reconstructed a phylogeny of Paphiopedilum using the cp genomes of forty-one Paphiopedilum individuals combined with four species of a closely related genus and two Lilium species as outgroups (Table S1). Finally, we performed selective pressures to survey whether the protein coding genes were under negative (purifying) selection or positive selection. This study not only provides beneficial knowledge and resources for the conservation and utilization of one of the most world-wide cultivated plant germplasms, but also offers clues into adaptive evolution for the future investigation of epiphytic
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The genus Paphiopedilum Pfitz. belongs to the Orchidaceae family, which includes over 66 species, of which 18 are natively distributed as ornamental plants that span Southwest to South China due to their large and exquisite flowers [7, 8, 9, 10, 11]. Paphiopedilum are often referred to as slipper orchids as they possess a bag-like lip that is akin to ladies’ slippers [9, 10, 11]. They have significant ornamental, horticultural, and medicinal value and grow primarily within the cracks in cliffs, or rocky well-drained sites in evergreen broadleaved forests, at altitudes of ~1000 m as a type of terrestrial, lithophytic/epiphytic herb [12, 13, 14]. Their unique ecosystems make them ideal for the study of environmental adaptation and evolution [9, 10, 11].
Unfortunately, owing to the destructive exploitation and habitat deterioration of wild Paphiopedilum germplasm resources, it has been listed in the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) and is prohibited from ruthless collection and international exploitation [8, 15, 16]. Thus far, many species of Paphiopedilum have been designated as first-class protected plants in China, as well as being listed on the IUCN Red List of Endangered (EN) even Critically Endangered (CR) Species [15, 16, 17].
In past years, research into Paphiopedilum has focused primarily on ecological characteristics and cultivation [18, 19, 20], genetic diversity and differentiation based on DNA molecular markers (e.g., ITS and plastid gene fragments) [21, 22], and historical biogeography [14, 23]. Recently, there were some reports also focused on comparative analysis, phylogeny, and evolution based on the whole chloroplast genomes [9, 10, 11, 12]. With the rapid development of the Next-Generation Sequencing (NGS) technologies, many cp genomes of the Orchidaceae family along with the Paphiopedilum species were available in the public database [9, 10, 11, 12, 23, 24, 25, 26, 27]. These assembled cp genomes offered useful genetic data for Paphiopedilum phylogenetic and evolution studies [9, 10, 11, 12, 28, 29]. However, the phylogenetic relationships and evolution of Paphiopedilum are quite complex [12, 21, 22, 30]. Investigations into the evolution and adaption of this plant have rarely been reported. The lack of genome-wide investigations limits the capacity to identify genomic characteristics that are under natural selection. Consequently, additional molecular and genetic resources are urgently required to provide a genetic basis for comparative cp genomes, phylogeny, evolutionary biology, and effective protection strategies for Paphiopedilum.
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Moreover, the chromosomal karyotypes of different Paphiopedilum species are heterogeneous such that variable numbers of alleles present obstacles to genetic research based on nuclear genes [31, 32, 33]. Hence, in this case, the efficient and convenient cp genome which, with many advantages, has become an ideal tool for the genetic and evolutionary analysis of Paphiopedilum. Additionally, according to previous studies, the cp genomes of Paphiopedilum might provide unique opportunities to reveal the boundary shift impacts on cp genome structures and gene evolution due to their exceptional peculiarities [12, 34]. Owing to the large number of species of the Orchidaceae family in the world, cp genomes have been widely used in their phylogenetics, evolutionary biology, and population genetics [9, 10, 11, 12, 13, 14, 24, 25, 26, 27].
Thus, in this study, we performed comparative analyses to afford comprehensive insights into the evolution and adaptation of the cp genomes of several Paphiopedilum species. Firstly, in addition to a previous study, we sequenced and assembled five cp genomes of Paphiopedilum species. Secondly, we conducted comparative cp genome analyses for these five genomes in addition to the other fourteen chloroplast genomic sequences of Paphiopedilum, which were originally distributed in China [8] and obtained from GenBank (Table S1).
Subsequently, we reconstructed a phylogeny of Paphiopedilum using the cp genomes of forty-one Paphiopedilum individuals combined with four species of a closely related genus and two Lilium species as outgroups (Table S1). Finally, we performed selective pressures to survey whether the protein coding genes were under negative (purifying) selection or positive selection. This study not only provides beneficial knowledge and resources for the conservation and utilization of one of the most world-wide cultivated plant germplasms, but also offers clues into adaptive evolution for the future investigation of epiphytic
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