The Complete Chloroplast Genome of Critically Endangered Chimonobambusa hirtinoda (Poaceae: Chimonobambusa) and Phylogenetic Analysis

doi:10.21203/rs.3.rs-1019626/v1

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Research Article

The Complete Chloroplast Genome of Critically Endangered Chimonobambusa hirtinoda (Poaceae: Chimonobambusa) and Phylogenetic Analysis

https://doi.org/10.21203/rs.3.rs-1019626/v1

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Chimonobambusa hirtinoda is a threatened species and only naturally distributed in Doupeng Mountain, Duyun, Guizhou, China. Next-generation sequencing (NGS) is used obtained the complete chloroplast (cp) genome sequence of C. hirtinoda, and then the sequence was assembled and analyze for phylogenetic and evolutionary. We also analyzed comparing the cp genome among Chimonobambusa species with previously published. The complete cp genome of C. hirtinoda has the total length of 139, 561 bp, 38.90% GC content was detected. A total of 130 genes were founded in the cp genome, including 85 protein coding genes, 37 tRNA genes, 8 rRNA. Some genes are missing and the introns occur lost in the cp genome of C. hirtinoda. A total of 48 simple sequence repeat (SSR) were detected and by measuring the codon usage frequency of amino acids, the A/U preference of the third nucleotide in the cp genome of C. hirtinoda was obtained. Furthermore, phylogenetic analysis using complete cp sequences, matk gene exhibited genetic relationship within the Chimonobambusa genus.

Agricultural Engineering

Agronomy

Plant Physiology and Morphology

Plant Molecular Biology and Genetics

Chloroplast Genome

Critically Endangered Chimonobambusa hirtinoda

Phylogenetic Analysis

simple sequence repeat (SSR)

Chimonobambusa genus, most of the bamboo shoots in autumn, which not only delicious, but also contain various trace elements such as iron, sun, and zinc, and rich in nutrients^{1, 2}, it become a favorite food for people. Additionally, the material of the bamboo is rich in cellulose pulp fibers so that it is a high-quality raw material for papermaking, which can be produced for bamboo handicrafts, bamboo plywood and craft furniture, which has high economic, edible and cultural value^{3, 4, 5}.

Chimonobambusa hirtinoda, was listed in the red catalogue by IUCN in 2007 and rated as a national endangered plant. At present, it is only naturally distributed in Doupeng Mountain, Duyun, Guizhou, China^{6, 7}. However, in recent years, with the local government's development of tourism in Doupeng mountain and the impact of natural environment, the living environment of C. hirtinoda has been damaged and on the verge of extinction⁸. Thus, it is very necessary to protect the natural resources of C. hirtinoda from all aspects. Most of the woody bamboos are mainly based on reproduction of the rhizomes, with flowering period is not fixed such as some species only bloom once in a lifetime⁹. There is a great deal of controversy in the division of the Bambusoideae because of their classification and identification generally depend on the morphological characteristics of vegetative organs. Therefore, the research from morphological identification to molecular perspective is of great significance to the classification and evolutionary relationship of bamboo species.

The origin of chloroplast (cp) is generally believed to be obtained from cyanobacteria through endosymbiosis¹⁰. As the photosynthetic organelle of plant cells, chloroplast not only plays a key role in photosynthesis, but also has important implications in plant physiology and development^{11, 12}. The structure of chloroplast genome is very conservative, which is usually composed of a large single-copy (LSC) region, a small single-copy (SSC) region and two inverted repeat (IRs) region in opposite directions¹³. Therefore, chloroplast genomes have been widely used to as DNA barcodes to quickly identify species, provided useful phylogenetic studies and chloroplast haplotypes are used to analyze the genetic diversity of species¹⁴^{, 15, 16}.

There are many reports on the chloroplast genome of the Arundinariatae in the Bambusoideae ¹⁷, but less data available on Chimonobambusa genus. Thus, this study is the first time reported the chloroplast genome of C. hirtinoda, including gene content, codon usage and compared with allied species. Besides that, phylogenetic relationship was constructed based on previously published cp genomes of Bambusoideae to clarify the taxonomic position of C. hirtinoda. These finding will provide valuable genetic resources for further research on the phylogenetic location of C. hirtinoda and investigating evolutionary relationships of the order Bambusoideae.

Assembly and annotation of the chloroplast genomes of Chimonobambusa hirtinoda.

Assembly resulted in a whole cp genome sequence of C. hirtinoda with a length of 139, 561 bp (Fig. 1), and consisted of an 83, 166-bp large single-copy region, a 12, 811-bp small single-copy region, and two 21,792-bp IR regions, respectively, comprising the typical quadripartite structure of terrestrial plants. The cp genome of C. hirtinoda was annotated with 130 genes, including 85 protein coding genes, 37 tRNA genes, and 8 rRNA genes (Table 1). Most of the 15 genes in the C. hirtinoda cp genome contain introns; of these, 13 genes contain one intron (atpF, ndhA, ndhB, petB, petD, rpl2, rpl16, rps16, trnA-UGC, trnI-GAU, trnK-UUU, trnL-UAA, trnV-UAC) and only gene cyf3 includes two introns, while the intron of the gene clpP was found to be deleted(Supplementary TableS1). Unusually, it was determined that the rps12 gene contained two copies, and the three exons were spliced into a trans-splicing gene ¹⁸.

Table 1

Summary of the chloroplast genome of C. hirtinoda.

Genome features	C. hirtinoda
Genome size (bp)	139,561
LSC size (bp)	83,166
SSC size (bp)	12,811
IR size (bp)	21,792
GC content (%)	38.9%
No. of genes	130
No. of PCGs	85
No. of tRNA	37
No. of rRNA	8

Note that the accD, ycf1, and ycf2 genes are missing in the cp genome of C. hirtinoda, and that the introns in the genes clpP and rpoC1 have been lost. This phenomenon is consistent with previous systematic evolutionary studies on the genome structure of plants in Poaceae ¹⁹. Such a phenomenon of missing genes has also been reported in other plants ^20-23.

The total GC content found for the C. hirtinoda cp genome was 38.90%, The content for each the four bases A, T, G, and C was 30.63%, 30.46%, 19.57%, and 19.33%, respectively (Table 2). The LSC region (36.98%) and SSC region (33.21%) have much lower values than that in the IR region (44.23%), indicating that distribution of the content in the cp genome is not uniform. This is probably because there are four rRNAs in the IR region, which in turn makes the GC content higher in the IR region. These values were similar to cp genome results previously reported for some Poaceae plants ^{24, 25}.

Table 2

Base composition in the C. hirtinoda choloroplast genome.

Region	Length(bp)	A (%)	T (%)	G (%)	C (%)	GC (%)
LSC	83,166	31.24	31.78	18.76	18.22	36.98
SSC	12,811	36.02	30.78	16.17	17.04	33.21
IRA	21,792	27.96	27.81	21.19	23.04	44.23
IRB	21,792	27.96	27.81	21.19	23.04	44.23
Total genome	139,561	30.63	30.46	19.57	19.33	38.90
CDS	60,531	29.63	30.85	21.20	18.3	39.53

Repeat sequences and codon analysis.

SSR consists of approximately 10-bp-long base repeats and is widely used for exploring phylogenetic evolution and for genetic diversity analysis ^26-29.

In total, 48 SSRs were detected in C. hirtinoda, including 27 mononucleotide versions, which accounted for 56.25% of the total, mainly comprised of A or T. There were 4 dinucleotide repeats comprised of AT/TA and TC/CT repeats, and 3 tri, 13 tetra, and 1penta-repeats shown (Fig. 2A). From the perspective of SSR distribution, the vast majority of SSRs are found in the LSC area, with 38 (79%); in the IR region there are 6 (13%) and in the SSC region there are 4 (8%), respectively (Fig. 2B). Previous research reports suggest that the distribution of SSR numbers in each region and the differences among locations in terms of GC content are related to the expansion or contraction of the IR boundary³⁰.

The REPuter program revealed that the cp genome of C. hirtinoda was identified with 61 repeats consisting of 15 palindromic repeats, 19 forward and no reverse and complement repeats (Fig.3). We notice that repeat analyses of three Chimonobambusa genus species showed a total of 61- 65 repeats, and there is only one reverse in C. hejiangensis. Most of the repeat lengths between 30 to 100 bp and almost all the repeat sequences were located in either IR or LSC region³¹ (Supplementary TableS2).

There were 20,180 codons identified in the coding region of C. hirtinoda (Fig. 4, Supplementary TableS3). Among these, the codon AUU of Ile was most widely used, and the codon TER of UAG was least often used, not counting the termination codons (817 and 19). Of those amino acids encoded by codons, Leu had the highest presence with 2,170 and TER was lowest at 85. A relative synonymous codon usage (RSCU) value greater than 1.0 means a codon is used more frequently³². The RSCU values for 31 codons exceeded 1 in the C. hirtinoda cp genome, and of these the third most frequent codon was A/U with 29 (93.55%), and the codons ending in C and G had values of 1 (3.23%) and 1, respectively (3.23%).

Comparative analysis of genome structure.

The nucleotide variability (Pi) values for of the three cp genomes found in the Chimonobambusa genus species ranged from 0 to 0.021 with an average value of 0.000544, as found from analysis with the software package DnaSP 5.10. In Figure 5 that there are clearly five high peaks in the two single-copy regions, and the highest peak is in the trnT-trnE-trnY region of the LSC region. The Pi value for LSC and SSC is significantly higher than that of the IR region. In the IR region, no highly different sequences are found, and this is a highly conserved region. The sequences of these highly variable regions have also been reported in other plants during examinations for species identification, phylogenetic analysis, and population genetics research ^33-35.

The structural information for the complete cp genomes among three Chimonobambusa genus species examined showed that those sequences in most regions were mostly conserved (Fig. 6). It can be seen from Figure 6 that the LSC and SSC regions show a large degree of variation, far higher than for the IR region, and the noncoding region demonstrates higher variability than is found in the coding region. In noncoding regions, 7-9k, 28-30k, 36k and other gene loci differ greatly. In the protein coding region, genes rpoC2, rps19, ndhJ and other regions show high differences. However, the agreement between the tRNA and rRNA regions is almost 100%. A similar phenomenon has also been reported by others³⁶.

IR contraction and expansion in the chloroplast genome.

There are four regions and four boundaries in the cp genome of plants. During the process of species evolution, the stability of the two IR region sequences is ensured by the IR region of the chloroplast genome expanding and contracting to some degree, and this adjustment becomes the main reason for changes in chloroplast genome length^{37, 38}.

It can be seen from Figure 6 that the three Chimonobambusa genus chloroplast genomes were found to highly similar in organization, gene content and gene order. The size of IR ranges fom 21, 797 bp (C. tumidissinoda) to 21,835 bp (C. hejiangensis). The ndhH gene spans the IRa/SSC boundary and has a duplication of 181–224 bp in the IRa region. The gene rps15 is located in the IR region (Fig. 7).

No inversion or translocation is found in the six genome sequences by mauve alignment, and the sequence is the same blocks, indicating that the cp genomes of the six species have not gene rearrangements (Fig. 8)

Phylogenetic analysis.

We performed phylogenetic analysis with both the complete chloroplast genomes and matK gene and observed complete chloroplast genome performed better to identify related species, consistent with previous study³⁹. The maximum likehood (ML) analysis indicated 7 nodes with fully branch support (100% bootstrap values), however the three Chimonobambusa genus with moderately supported relationship as a result of less samples use, which supported C. hirtinoda to be closely related with C. tumidissinoda with 62 % bootstrap value more than C. hejiangensis. The result of phylogenetic tree based on matK gene showed that Chimonobambusa species clustered in one branch was consistent with the phylogenetic tree constructed by the complete cp genome tree (Fig. 10).

This study mainly explored the chloroplast genome of C. hirtinoda and compared it with those of related species within Chimonobambusa. These data provide useful genetic information that advances the genetic research on Chimonobambusa. Through successfully assembling, annotating, and analyzing the whole chloroplast genome sequence of C. hirtinoda, a phenomenon of genes loss was discovered. This loss is probably associated with the rapid evolution of the Poaceae species and the extensive rearrangements of chloroplast structures that took place during that process. The acquisition of these data, particularly in terms of SSR, will enhance the study of the phylogenetic relationships of Chimonobambusa plants, cp genome variation among them, and the function of genes.

Comparative analysis of the Chimonobambusa species studied revealed that coding regions are more conservative than noncoding regions in the cp chloroplast genome. Such a change in genetic structure can reflect a relationship with the changes in species, but the mechanism that generates such variations and the subsequent results need further study.

The Poaceae family is generally divided into two large evolutionary branches (BEP and PACCMAD), among which the Bambusoideae, Pooideae, and Oryzoideae belong to the BEP branch. Panicoideae, Arundinoideae, Chloridoideae, Aristidoideae, Arundinoideae, and Micrairoideae belong to the PACCMAD branch. Here, the complete chloroplast genomes based phylogenetic tree (Fig. 10A) shows high values of bootstrap support (only three values less than 80 %), and these species can be polymerized into two clades and an outgroup with strong support. The genus Bambusa constitutes an isolated evolutionary branch, becoming a monophyletic group, a conclusion that is consistent with previous reports ⁴⁰. Also, the two phylogenetic trees revealed that C. hirtinoda, C. hejiangensis and C. tumidissinoda formed a group that was closely related to the group. On the evolutionary subclade of the second branch, the genus Ampelocalamus and C. longiusculus have a very close relationship.

Plant materials.

Four to six fresh leaf of native habitats are collected in Doupeng Mountain, Guizhou Province, China (N 26°22′32.55′′, E 107°22′9′′, altitude 1074.93 m). Those fresh leaf were dried with silica gel and stored at the Natural Museum of Guizhou University (accession number: GACP) for further DNA extraction (Fig. 9). The identification of the species by Professor Guangqian Gou, the director of Bamboo Research Institute in college of life sciences, Guizhou University.

The collection and experiments of plant materials has complied with relevant guidelines and regulations of Doupeng mountain virgin forest nature reserve.

DNA extraction, Chloroplast genome sequencing.

Total genomic DNAs were extracted from sample using the TIANGEN DNA extraction kit (TIANGEN BIOTECH CO., Beijing, China) and the DNA concentration was detected using spectrophotometry, and total DNA quality was detected via 1% agarose gel electrophoresis. All of the DNA obtained from C. hirtinoda was sent to BGI (Wuhan, China. https://www.genomics.cn), and the total DNA was sequenced using an Illumina sequencer with an HiSeq2500 system, with library type selected to be the De Novo Sequencing ≤800 bp conventional library.

Genome aassembly and annotation.

De novo assembly of the C. hirtinoda cp genome was performed in a GetOrganelle pipeline⁴¹ (https://github.com/Kinggerm/GetOrganelle). Using the complete chloroplast genome of C. hejiangensis (#MT884004) as a reference sequence, PGA (https://github.com/quxiaojian/PGA) annotated the chloroplast genes of C. hirtinoda, followed by manual correction using the software Generous 10.0.5⁴², with uploading to NCBI after the sequence was confirmed to be correct. The GenBank accession number of C. hirtinoda was OK046142.

Using the online software package Organellar Genome DRAW (OGDraw)⁴³ (http://ogdraw.mpimp-golm.mpg.de/index.shtml), a physical map of the chloroplast group was created.

Structural of the C. hirtinoda cp genome.

A simple repeat sequence (SSR) is also called a microsatellite. It can be detected using the identification tool MISA⁴⁴ and REPuter⁴⁵, respectively. The number for the repeat parameter was set to at least 10, 5, 4, 3, 3 and 3 repeat units, from mononucleotide to hexanucleotide. The codon bias for the chloroplast genome was analyzed using the software package CodonW1.4.2 (http://downloads.fyxm.net/CodonW-76666.html).

Sequence divergence.

Determining the nucleotide diversity of the whole cp genome can make the identification of related species more accurate and help to solve similar problems arising in the phylogenetic research ^{46, 47}. In order to compare the differences, three species of Chimonobambusa were selected, using C. hejiangensis as the control. The software package MAFFT ⁴⁸ was used to compare the whole cp genomes of the three species, with results of the comparison manually truncated at both ends. Then the software package DnaSP5.10 was used to calculate the Pi values between species sequences ⁴⁹, The sliding window was set to 600 and the step size was 200. The online program mVISTA⁵⁰ was used to compere three species, using C. hejiangensis annotation as the reference. The software MAUVE⁵¹ provided rearrangements of those gene sequences.

Phylogenetic analyses.

For 14 sequences of complete chloroplast genome sequences and matK gene of Bambusoideae species and Hypolytrum nemorum (Cyperaceae: Hypolytrum) was selected as an outgroup for construction the phylogenetic tree to identify the taxonomic position of the C. hirtinoda. All sequences were aligned using the tool MAFFT and the maximum likelihood (ML) phylogenetic tree constructed using the software package MEGA-X ⁵² and the bootstrap replicates parameter was set to 1,000.

Specimen collection statement.

The collection of fresh leaves obtained the permission of the nature reserve.

Acknowledgements

This study was supported by The Breeding of Improved Bamboo Varieties for Shoot (Te-Lin-Yan 2020-17).

Author contributions

Yanjiang Liu conceived and designed the experiments, performed the experiments, analyzed the data, provided reagents/materials/analysis tools, prepared figures and/or tables, wrote and reviewed drafts of the manuscript, and approved the final draft.

Xiao Zhu analyzed the data, contributed reagents/materials/analysis tools, authored and reviewed drafts of the manuscript, and approved the final draft.

Mingli Wu and Xue Xu prepared figures and/or tables, authored and reviewed drafts of the manuscript, and approved the final draft.

Zhaoxia Dai and Guangqian Gou conceived and designed the experiments, authored or reviewed drafts of the manuscript, and approved the final draft.

Competing interests

The authors declare that there are no conflicts of interest.

Additional information

Correspondence and requests for materials should be addressed to Zhaoxia Dai and Yanjiang Liu.

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No competing interests reported.

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Editorial decision: Major revision
14 Mar, 2022
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Reviewers agreed at journal
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Reviewers invited by journal
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Editor assigned by journal
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Editor invited by journal
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First submitted to journal
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The Complete Chloroplast Genome of Critically Endangered Chimonobambusa hirtinoda (Poaceae: Chimonobambusa) and Phylogenetic Analysis

Status:

Version 1

Abstract

Figures

Background

Results And Discussion

Assembly and annotation of the chloroplast genomes of Chimonobambusa hirtinoda.

Repeat sequences and codon analysis.

Comparative analysis of genome structure.

IR contraction and expansion in the chloroplast genome.

Phylogenetic analysis.

Conclusions

Materials & Methods

Plant materials.

DNA extraction, Chloroplast genome sequencing.

Genome aassembly and annotation.

Structural of the C. hirtinoda cp genome.

Sequence divergence.

Phylogenetic analyses.

Specimen collection statement.

Declarations

Acknowledgements

Author contributions

Competing interests

Additional information

References

Additional Declarations

Supplementary Files

Status:

Version 1