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Complete Plastid Genome Sequencing of Eight Species from Hansenia, Haplosphaera and Sinodielsia (Apiaceae): Comparative Analyses and Phylogenetic Implications

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Complete Plastid Genome Sequencing of Eight Species from Hansenia, Haplosphaera and Sinodielsia (Apiaceae): Comparative Analyses and Phylogenetic Implications plants Article Complete Plastid Genome Sequencing of Eight Species from Hansenia, Haplosphaera and Sinodielsia (Apiaceae): Comparative Analyses and Phylogenetic Implications 1, 1, 2 1 1 Wei Gou y , Sheng-Bin Jia y, Megan Price , Xian-Lin Guo , Song-Dong Zhou and Xing-Jin He 1,* 1 Key Laboratory of Bio-Resources and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610065, China; [email protected] (W.G.); [email protected] (S.-B.J.); [email protected] (X.-L.G.); [email protected] (S.-D.Z.) 2 Sichuan Key Laboratory of Conservation Biology on Endangered Wildlife, College of Life Sciences, Sichuan University, Chengdu 610065, China; [email protected] * Correspondence: [email protected] Equal contributions to this work. y Received: 12 October 2020; Accepted: 6 November 2020; Published: 9 November 2020 Abstract: Hansenia Turcz., Haplosphaera Hand.-Mazz. and Sinodielsia H.Wolff are three Apiaceae genera endemic to the Hengduan Mountains and the Himalayas, which usually inhabit elevations greater than 2000 m. The phylogenetic relationships between and within the genera were uncertain, especially the placement of Hap. himalayensis and S. microloba. Therefore, we aimed to conduct comparative (simple sequence repeat (SSR) structure, codon usage bias, nucleotide diversity (Pi) and inverted repeat (IR) boundaries) and phylogenetic analyses of Hansenia, Haplosphaera and Sinodielsia (also compared with Chamaesium and Bupleurum) to reduce uncertainties in intergeneric and interspecific relationships. We newly assembled eight plastid genomes from Hansenia, Haplosphaera and Sinodielsia species, and analyzed them with two plastid genomes from GenBank of Hap. phaea, S. yunnanensis. Phylogenetic analyses used these ten genomes and another 22 plastid genome sequences of Apiaceae. We found that the newly assembled eight genomes ranged from 155,435 bp to 157,797 bp in length and all had a typical quadripartite structure. Fifty-five to 75 SSRs were found in Hansenia, Haplosphaera and Sinodielsia species, and the most abundant SSR was mononucleotide, which accounted for 58.47% of Hansenia, 60.21% of Haplosphaera and 48.01% of Sinodielsia. There was no evident divergence of codon usage frequency between the three genera, where codons ranged from 21,134 to 21,254. The Pi analysis showed that trnE(UUC)-trnT(GGU), trnH(GUG)-psbA and trnE(UUC)-trnT(GGU) spacer regions had the highest Pi values in the plastid genomes of Hansenia (0.01889), Haplosphaera (0.04333) and Sinodielsia (0.01222), respectively. The ndhG-ndhI spacer regions were found in all three genera to have higher diversity values (Pi values: 0.01028–0.2), and thus may provide potential DNA barcodes in phylogenetic analysis. IR boundary analysis showed that the length of rps19 and ycf1 genes entering IRs were usually stable in the same genus. Our phylogenetic tree demonstrated that Hap. himalayensis is sister to Han. weberbaueriana; meanwhile, Haplosphaera and Hansenia are nested together in the East Asia clade, and S. microloba is nested within individuals of S. yunnanensis in the Acronema clade. This study will enrich the complete plastid genome dataset of the Apiaceae genera and has provided a new insight into phylogeny reconstruction using complete plastid genomes of Hansenia, Haplosphaera and Sinodielsia. Keywords: Apiaceae; Hansenia; Haplosphaera; phylogeny; plastid genome; Sinodielsia Plants 2020, 9, 1523; doi:10.3390/plants9111523 www.mdpi.com/journal/plants Plants 2020, 9, 1523 2 of 17 1. IntroductionPlants 2020, 9, x FOR PEER REVIEW 2 of 19 Hansenia1. IntroductionTurcz., Haplosphaera Hand.-Mazz. and Sinodielsia H.Wolff are three endemic high-elevation (typicallyHansenia>2000 m)Turcz. genera, Haplosph of Apiaceae,aera Hand.-Mazz. mainly distributedand Sinodielsia in H.Wolff the Hengduan are three Mountains endemic high- and the Himalayaselevation (Figure (typically1)[ 1>200]. According0 m) genera toof theApiaceae latest, Apiaceaemainly distributed taxonomy, in theHansenia Hengduan, Haplosphaera Mountains and Sinodielsiaand thecomprise Himalayas five, (Figure two 1) and [1]. four According species, to the respectively latest Apiaceae [2–5 ].taxonomy, Previous Hansenia phylogenetic, Haplosphaera studies of Hanseniaand ,SinodielsiaHaplosphaera compriseand five,Sinodielsia two andbased four species, on two respectively plastid genome [2–5]. regionsPrevious( phylogeneticrpl16 and rps16 studiesintrons) and nuclearof Hansenia internal, Haplosp transcribedhaera and spacersSinodielsia (nrITSs) based foundon two thatplastidSinodielsia genomeis regions within ( therpl16Acronema and rps16clade, whileintrons) the closely and nuclear related internalHansenia transcribedand Haplosphaera spacers (nrITSs)are found located that in Sinod theielsia East is Asiawithin clade, the Acronema albeit from clade, while the closely related Hansenia and Haplosphaera are located in the East Asia clade, limited sampling [6–11]. One study of 106 nrITS sequences representing 100 species from 52 genera albeit fr of Chinese Apiaceae found that the Acronema clade and the East Asia clade were well-supported (posterior probability both valued 100% by Bayesian inference) [8]. Additionally, Hap. himalayensis and S. microloba were unknown at the time of these previous studies and remain as two little-known species. FigureFigure 1. Plants1. Plants of ofHansenia Hansenia, HaplosphaeraHaplosphaera andand SinodielsiaSinodielsia. (A) .(Han.A forbesii) Han., (B forbesii) Han. forrestii,(B) Han., (C) Han. forrestii , (C) Han.oviformis oviformis, (D) ,(Han.D) Han.weberbaueriana weberbaueriana, (E) Hap.,( Ehimalayensis) Hap. himalayensis, (F) Hap. ,(phaeaF) Hap., (G) phaeaS. microloba,(G) S. and microloba (H) S. and (H) S.yunnanensis yunnanensis. WithWith the developmentthe development of of second-generation second-generation sequencingsequencing technology, technology, more more plastid plastid genomes genomes have have been used in phylogeny and comparative studies, and fairly good results have been obtained [12]. been used in phylogeny and comparative studies, and fairly good results have been obtained [12]. Generally the circular genome consists of two inverted repeats (IRs) divided by two regions, the large Generally the circular genome consists of two inverted repeats (IRs) divided by two regions, the large (LSC) and small single-copy (SSC) regions [13,14], and most angiosperm complete plastid genomes (LSC)are and between small single-copy115 and 165 kb (SSC) in length regions [15]. [13 The,14 gene], and content most and angiosperm order of pl completeastid genomes plastid are genomes usually are betweenhighly 115 conserved, and 165 and kb inthe length substitution [15]. rate The in gene plastid content DNA is and much order lower of than plastid in plant genomes nuclear are DNA usually highly[16]. conserved, The similarity and of the gene substitution length and the rate low in substi plastidtution DNA rate of is plant much plastids lower make than them in plant valuable nuclear DNAsources [16]. The of genetic similarity markers of genefor phylogenetic length and studies the low [17]. substitution rate of plant plastids make them valuable sourcesIn our previous of genetic studies, markers we sequenced for phylogenetic two plastid studies genomes [17 of]. Hap. phaea [18] and S. yunnanensis In(HB: our Zhongdian previous studies,population) we sequenced[19] and provided two plastid preliminary genomes phylogenetic of Hap. phaea positions[18] and forS. the yunnanensis two (HB: Zhongdianspecies. Following population) on from [19 this,] and we provided aimed to preliminary conduct comparative phylogenetic (simple positions sequence for repeat the two (SSR), species. Following on from this, we aimed to conduct comparative (simple sequence repeat (SSR), codon Plants 2020, 9, 1523 3 of 17 usage bias, nucleotide diversity (Pi) and IR) and phylogenetic analyses of Hansenia, Haplosphaera Plants 2020, 9, x FOR PEER REVIEW 3 of 19 and Sinodielsia to reduce uncertainties in intergeneric and interspecific relationships. Analyses were conductedcodon usingusage abias, 32 completenucleotide plastiddiversity genome (Pi) and dataset, IR) and which phylogenetic was compiled analyses from of Hansenia eight newly, assembledHaplosphaera plastid and genomes Sinodielsia from to reduceHan. uncertainties forbesii, Han. in forrestiiintergeneric, Han. and oviformis interspecific, Han. relationships. weberbaueriana , Hap.Analyses himalayensis were, S.conducted microloba using, S. yunnanensisa 32 complete(EY: plastid Eryuan genome County dataset, pop.) which and wasS. compiled yunnanensis from (KM: Kunmingeight pop.),newly as assembled well as previously plastid genomes sequenced from genomes. Han. forbesii Our, studyHan. providesforrestii, Han. newly oviformis complete, Han. plastid genomesweberbaueriana of Hansenia, Hap., Haplosphaera himalayensis,and S. microlobaSinodielsia, S.species, yunnanensis and (EY: since Eryuan these threeCounty genera pop.) are and endemic S. to Pan-Himalayanyunnanensis (KM: regions, Kunming the pop.), information as well as provided previously herein sequenced is indispensable genomes. Our for study Apiaceae provides plastid newly complete plastid genomes of Hansenia, Haplosphaera and Sinodielsia species, and since these evolutionary and phylogenetic studies. three genera are endemic to Pan-Himalayan regions, the information provided herein is 2. Resultsindispensable and Discussion for Apiaceae plastid evolutionary and phylogenetic studies. 2.1. Phylogenetic2. Results and
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