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Chloroplast genomic diversity in Bulbophyllum section Macrocaulia (Orchidaceae, Epidendroideae, Malaxideae): Insights into species divergence and adaptive evolution

ABSTRACT: Bulbophyllum is the largest genus in Orchidaceae with a pantropical distribution. Due to highly significant diversifications, it is considered to be one of the most taxonomically and phylogenetically complex taxa. The diversification pattern and evolutionary adaptation of chloroplast genomes are poorly understood in this species-rich genus, and suitable molecular markers are necessary for species determination and phylogenetic analysis. A natural Asian section Macrocaulia was selected to estimate the interspecific divergence of chloroplast genomes in this study. Here, we sequenced the complete chloroplast genome of four Bulbophyllum species, including three species from section Macrocaulia. The four chloroplast genomes had a typical quadripartite structure with a genome size ranged from 156,182 to 158,524 bp. The chloroplast genomes included 113 unique genes encoding 79 proteins, 30 tRNAs and 4 rRNAs. Comparison of the four chloroplast genomes showed that the three species from section Macrocaulia had similar structure and gene contents, and shared a number of indels, which mainly contribute to its monophyly. In addition, interspecific divergence level was also great. Several exclusive indels and polymorphism SSR loci might be used for taxonomical identification and determining interspecific polymorphisms. A total of 20 intergenic regions and three coding genes of the most variable hotspot regions were proposed as candidate effective molecular markers for future phylogenetic relationships at different taxonomical levels and species divergence in Bulbophyllum. All of chloroplast genes in four Bulbophyllum species were under purifying selection, while 13 sites within six genes exhibited site-specific selection. A whole chloroplast genome phylogenetic analysis based on Maximum Likelihood, Bayesian and Parsimony methods all supported the monophyly of section Macrocaulia and the genus of Bulbophyllum. Our findings provide valuable molecular markers to use in accurately identifying species, clarifying taxonomy, and resolving the phylogeny and evolution of the genus Bulbophyllum. The molecular markers developed in this study will also contribute to further research of conservation of Bulbophyllum species. Highlights • The first study on comparative chloroplast genomes analysis in four Chinese Bulbophyllum species.• The chloroplast genomes of Bulbophyllum section Macrocaulia showed both conservative and divergence.• A number of exclusive SSRs were identified for taxonomical identification and interspecific polymorphisms determination.• A number of hotspot regions were identified for phylogenetic and evolutionary studies.

SUBMITTER: Tang H

PROVIDER: S-EPMC8591142 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Bulbophyllum is one of the largest genera and presents some of the most intricate taxonomic problems in the family Orchidaceae, including species of ornamental and medical importance. The lack of knowledge regarding the characterization of Bulbophyllum chloroplast (cp) genomes has imposed current limitations on our study. Here, we report the complete cp genomes of seven Bulbophyllum species, including B. ambrosia, B. crassipes, B. farreri, B. hamatum, B. shanicum, B. triste, and B. violaceolabellum, and compared with related taxa to provide a better understanding of their genomic information on taxonomy and phylogeny. A total of 28 Bulbophyllum cp genomes exhibit typical quadripartite structures with lengths ranging from 145,092 bp to 165,812 bp and a GC content of 36.60% to 38.04%. Each genome contained 125-132 genes, encompassing 74-86 protein-coding genes, 38 tRNA genes, and eight rRNA genes. The genome arrangements, gene contents, and length were similar, with differences observed in ndh gene composition. It is worth noting that there were exogenous fragment insertions in the IR regions of B. crassipes. A total of 18-49 long repeats and 38-80 simple sequence repeats (SSRs) were detected and the single nucleotide (A/T) was dominant in Bulbophyllum cp genomes, with an obvious A/T preference. An analysis of relative synonymous codon usage (RSCU) revealed that leucine (Leu) was the most frequently used codon, while cysteine (Cys) was the least used. Six highly variable regions (rpl32-trnLUAG > trnTUGU-trnLUAA > trnFGAA-ndhJ > rps15-ycf1 > rbcL-accD > psbI-trnSGCU) and five coding sequences (ycf1 > rps12 > matK > psbK > rps15) were identified as potential DNA markers based on nucleotide diversity. Additionally, 31,641 molecular diagnostic characters (MDCs) were identified in complete cp genomes. A phylogenetic analysis based on the complete cp genome sequences and 68 protein-coding genes strongly supported that 28 Bulbophyllum species can be divided into four branches, sects. Brachyantha, Cirrhopetalum, and Leopardinae, defined by morphology, were non-monophyly. Our results enriched the genetic resources of Bulbophyllum, providing valuable information to illustrate the complicated taxonomy, phylogeny, and evolution process of the genus.

Project description:BackgroundChloroplast (cp) genomes are useful and informative molecular markers used for species determination and phylogenetic analysis. Bulbophyllum is one of the most taxonomically complex taxa in Orchidaceae. However, the genome characteristics of Bulbophyllum are poorly understood.MethodsBased on comparative morphological and genomic analysis, a new species Bulbophyllum pilopetalum from eastern Himalaya belonging to section Cirrhopetalum is described and illustrated. This study used chloroplast genomic sequences and ribosomal DNA (nrDNA) analysis to distinguish the new Bulbophyllum species and determine its phylogenetic position. An additional phylogenetic analysis was conducted using 74 coding sequences from 15 complete chloroplast genomes from the genus Bulbophyllum, as well as nrDNA sequences and two chloroplast DNA sequences from 33 Bulbophyllun species.ResultsThe new species is morphologically similar to B. pingnanense, B. albociliatum, and B. brevipedunculatum in vegetative and floral morphology, but it can be distinguished by its ovate-triangle dorsal sepal without a marginal ciliate. The chloroplast genome of the new Bulbophyllum species is 151,148 bp in length, and includes a pair of inverted repeats (IRs) of 25,833 bp, a large single-copy region (LSC) of 86,138 bp, and a small single-copy region (SSC) of 13,300 bp. The chloroplast genome includes 108 unique genes encoding 75 proteins, 30 tRNAs, and four rRNAs. Compared with the cp genomes of its two most closely-related species, B. pingnanense and B. albociliatum, this chloroplast genome exhibited great interspecific divergence and contained several Indels that were specific to the new species. The plastid tree showed that B. pilopetalum is most closely-related to B. pingnanense. The phylogenetic tree based on combined nrDNA and chloroplast DNA sequences indicated that section Cirrhopetalum was monophyletic and B. pilopetalum was a member of this section.DiscussionThe taxonomic status of the new species is strongly supported by cp genome data. Our study highlights the importance of using the complete cp genome to identify species, elucidate the taxonomy, and reconstruct the phylogeny of plant groups with complicated taxonomic problems.

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Chloroplast genomic diversity in Bulbophyllum section Macrocaulia (Orchidaceae, Epidendroideae, Malaxideae): Insights into species divergence and adaptive evolution

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