Abstract
The genus Actinidia, also called kiwifruit, is characterized with abundant balanced nutritional metabolites, including exceptionally high vitamin C content. However, the traditional classification could not fully reflect the actual Actinidia species’ relationships, which need further revision through more accurate approaches. Compared to the nuclear genome, the chloroplast genome has simple heredity characteristics, conserved genome structure and small size, suitable for deciphering complicated species’ phylogenetic relationships. Here, the genome-wide comprehensive comparative analyses were performed over 29 independent chloroplast genomes’ sequences derived from 25 Actinidia taxa. The average genome size is 156,673.38 bp, with an average 37.20% GC content. The long repeat sequences rather than SSRs (simple sequence repeats) in Actinidia were revealed to be the causal agent leading to the chloroplast genome size expansion. The clpP gene sequences with exon merge and intron deletion were annotated in all the 29 chloroplast genomes tested, which has been previously reported to be lost in Actinidia species. Comprehensive sequence analyses indicated the distinct variation at the clpP gene locus was Actinidiaceae-specific, emerging after the Actinidiaceae-other Ericales species divergence. Four highly divergent sequences (i.e., rps16 ~ trnQ-UUG, rps4 ~ trnT-UGU, petA ~ psbJ, and rps12 ~ psbB) evolved in the LSC (large single-copy) and SSC (small single-copy) regions embodying rps12 ~ psbB (including clpP gene and its up/downstream noncoding sequence) were identified as variation hot spots in Actinidia species. Based on either LSC region alone, combined sequences of LSC and SSC or the whole chloroplast genome sequences, three identical phylogenetic trees of the 25 Actinidia taxa with relatively improved resolution were reconstructed, consistently supporting the reticulate evolutionary lineage in Actinidia. Our findings could help to better understand the evolution characteristics of chloroplast genomes and phylogenetic relationships among Actinidia species.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The data presented in this study are available in the article and Supplementary Materials.
References
Ai F, Liu H (2019) The complete chloroplast genome sequence of Actinidia zhejiangensis. Mitochondrial DNA Part B 4(1):690–691. https://doi.org/10.1080/23802359.2019.1573117
Capella-Gutierrez S, Silla-Martinez JM et al (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25(15):1972–1973. https://doi.org/10.1093/bioinformatics/btp348
Chat J, Jauregui B et al (2004) Reticulate evolution in kiwifruit (Actinidia, Actinidiaceae) identified by comparing their maternal and paternal phylogenies. Am J Bot 91(5):736–747. https://doi.org/10.3732/ajb.91.5.736
Chen Y, Xu Y et al (2019) The complete chloroplast genome of Actinidia macrosperma. Mitochondrial DNA Part B 4(2):4188–4189. https://doi.org/10.1080/23802359.2019.1692733
Chen Y-T, Lai R-l et al (2020) The complete chloroplast genome sequence of actinidia valvata. Mitochondrial DNA Part B 5(3):2072–2073. https://doi.org/10.1080/23802359.2020.1764402
Cui Y, Chen X et al (2019) Comparison and phylogenetic analysis of chloroplast genomes of three medicinal and edible Amomum species. Int J Mol Sci 20(16):4040. https://doi.org/10.3390/ijms20164040
Daniell H, Lin CS et al (2016) Chloroplast genomes: diversity, evolution, and applications in genetic engineering. Genome Biol 17(1):134. https://doi.org/10.1186/s13059-016-1004-2
Delcher AL, Salzberg SL et al (2003) Using MUMmer to identify similar regions in large sequence sets. Curr Protoc Bioinform 1: 10.3.1–10.3.18. https://doi.org/10.1002/0471250953.bi1003s00
Ding F, Zhang L et al (2021) The complete chloroplast genome sequence of Actinidia arguta var. giraldii. Mitochondrial DNA B Resour 6(2):413–414. https://doi.org/10.1080/23802359.2020.1870884
Frazer KA, Pachter L et al (2004) VISTA: computational tools for comparative genomics. Nucleic Acids Res 32(Web Server issue):W273–W279. https://doi.org/10.1093/nar/gkh458
Hong Z, Wu Z et al (2020) Comparative analyses of five complete chloroplast genomes from the genus Pterocarpus (Fabacaeae). Int J Mol Sci 21(11):3758. https://doi.org/10.3390/ijms21113758
Huang H, Li Z et al (2002) Phylogenetic relationships in Actinidia as revealed by RAPD analysis. J Am Soc Hortic Sci 127(5):759–766
Huang S, Ding J et al (2013) Draft genome of the kiwifruit Actinidia chinensis. Nat Commun 4:2640. https://doi.org/10.1038/ncomms3640
Huang J, Yu Y et al (2020) Comparative chloroplast genomics of Fritillaria (Liliaceae), inferences for phylogenetic relationships between Fritillaria and Lilium and plastome evolution. Plants (basel) 9(2):133. https://doi.org/10.3390/plants9020133
Kalyaanamoorthy S, Minh BQ et al (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14(6):587–589. https://doi.org/10.1038/nmeth.4285
Katoh K, Rozewicki J et al (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20(4):1160–1166. https://doi.org/10.1093/bib/bbx108
Kim S-C, Lee J-W et al (2018) The complete chloroplast genome sequence of Actinidia Rufa (Actinidiaceae). Mitochondrial DNA Part B 3(2):564–565. https://doi.org/10.1080/23802359.2018.1450676
Kurtz S, Choudhuri JV et al (2001) REPuter: the manifold applications of repeat analysis on a genomic scale. Nucleic Acids Res 29(22):4633–4642. https://doi.org/10.1093/nar/29.22.4633
Lan Y, Cheng L et al (2017) The complete chloroplast genome sequence of Actinidia kolomikta from north China. Conserv Genet Resour 10(3):475–477. https://doi.org/10.1007/s12686-017-0852-8
Li J, Huang H et al (2002) Molecular phylogeny and infrageneric classification of Actinidia (Actinidiaceae). Syst Bot 27(2):408–415
Li W, Lu Y et al (2018) The complete chloroplast genome sequence of Actinidia arguta: gene structure and genomic resources. Conserv Genet Resour 10(3):423–425. https://doi.org/10.1007/s12686-017-0840-z
Li X, Zuo Y et al (2019) Complete chloroplast genomes and comparative analysis of sequences evolution among seven Aristolochia (Aristolochiaceae) medicinal species. Int J Mol Sci 20(5):1045. https://doi.org/10.3390/ijms20051045
Lin M, Qi X et al (2018) The complete chloroplast genome sequence of Actinidia arguta using the PacBio RS II platform. PLoS One 13(5):e0197393. https://doi.org/10.1371/journal.pone.0197393
Lin H, Jiang L et al (2019) Assembly and phylogenetic analysis of the complete chloroplast genome sequence of Actinidia setosa. Mitochondrial DNA Part B 4(2):3679–3680. https://doi.org/10.1080/23802359.2019.1678423
Lin H, Xu Y et al (2020) The complete chloroplast genome of Actinidia valvata (Actinidiaceae). Mitochondrial DNA Part B 5(2):1607–1608. https://doi.org/10.1080/23802359.2020.1745105
Liu YF, Li DW et al (2017) Rapid radiations of both kiwifruit hybrid lineages and their parents shed light on a two-layer mode of species diversification. New Phytol 215(2):877–890. https://doi.org/10.1111/nph.14607
Liu Y, Xie X et al (2020) Phylogenetic relationship and characterization of the complete chloroplast genome of Actinidia callosa var. strigillosa. Mitochondrial DNA Part B 5(3):3420–3421. https://doi.org/10.1080/23802359.2020.1823258
Martin W, Deusch O et al (2005) Chloroplast genome phylogenetics: why we need independent approaches to plant molecular evolution. Trends Plant Sci 10(5):203–209. https://doi.org/10.1016/j.tplants.2005.03.007
Nguyen LT, Schmidt HA et al (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32(1):268–274. https://doi.org/10.1093/molbev/msu300
Nie L, Cui Y et al (2019) Gene losses and variations in chloroplast genome of parasitic plant Macrosolen and phylogenetic relationships within Santalales. Int J Mol Sci 20(22):5812. https://doi.org/10.3390/ijms20225812
Park I, Song JH et al (2019) Cuscuta species identification based on the morphology of reproductive organs and complete chloroplast genome sequences. Int J Mol Sci 20(11):2726. https://doi.org/10.3390/ijms20112726
Qu XJ, Moore MJ et al (2019) PGA: a software package for rapid, accurate, and flexible batch annotation of plastomes. Plant Methods 15:50. https://doi.org/10.1186/s13007-019-0435-7
Rozas J, Ferrer-Mata A et al (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 34(12):3299–3302. https://doi.org/10.1093/molbev/msx248
Shi L, Chen H et al (2019) CPGAVAS2, an integrated plastome sequence annotator and analyzer. Nucleic Acids Res 47(W1):W65–W73. https://doi.org/10.1093/nar/gkz345
Tang P, Shen R et al (2019a) The complete chloroplast genome sequence of Actinidia eriantha. Mitochondrial DNA Part B 4(2):2114–2115. https://doi.org/10.1080/23802359.2019.1623111
Tang P, Xu Q et al (2019b) Phylogenetic relationship in Actinidia (Actinidiaceae) based on four noncoding chloroplast DNA sequences. Plant Syst Evol 305(9):787–796. https://doi.org/10.1007/s00606-019-01607-0
Testolin R, Huang H et al (2016) The kiwifruit genome. Springer International Publishing, Berlin
Tillich M, Lehwark P et al (2017) GeSeq—versatile and accurate annotation of organelle genomes. Nucleic Acids Res 45(W1):W6–W11. https://doi.org/10.1093/nar/gkx391
Tyagi S, Jung JA et al (2020) Comparative analysis of the complete chloroplast genome of mainland Aster spathulifolius and other Aster species. Plants (basel) 9(5):568. https://doi.org/10.3390/plants9050568
Wang WC, Chen SY et al (2016) Chloroplast genome evolution in Actinidiaceae: clpP loss, heterogenous divergence and phylogenomic practice. PLoS One 11(9):e0162324. https://doi.org/10.1371/journal.pone.0162324
Wu H, Li M et al (2019) The complete chloroplast genome sequence of Actinidia callosa var. henryi. Mitochondrial DNA Part B 4(1):652–653. https://doi.org/10.1080/23802359.2018.1561223
Xiaoqiong Q, Xiaodong X et al (2021) Characterization of the complete chloroplast genome of Actinidia hemsleyana. Mitochondrial DNA B Resour 6(11):3259–3260. https://doi.org/10.1080/23802359.2021.1993100
Xu Y-S, Zhang C-G et al (2020) The complete chloroplast genome of Actinidia rubus (Actinidiaceae). Mitochondrial DNA Part B 5(1):366–367. https://doi.org/10.1080/23802359.2019.1703571
Yang A, Liu S et al (2020) The complete chloroplast genome sequence of Actinidia styracifolia C. F. Liang. Mitochondrial DNA Part B 5(1):90–91. https://doi.org/10.1080/23802359.2019.1698337
Yao X, Tang P et al (2015) The first complete chloroplast genome sequences in Actinidiaceae: genome structure and comparative analysis. PLoS One 10(6):e0129347. https://doi.org/10.1371/journal.pone.0129347
Zhang J, Liu H (2019) The complete choloroplast genome sequence of Actinidia lanceolate. Mitochondrial DNA Part B 4(1):1187–1188. https://doi.org/10.1080/23802359.2019.1591200
Zhang F, Yan Z et al (2019) The complete chloroplast genome of Actinidia fulvicoma. Mitochondrial DNA Part B 4(2):4089–4090. https://doi.org/10.1080/23802359.2019.1691949
Funding
This work was supported by grants from the National Natural Science Foundation of China (Grant nos. 31972474, 31671259 and 31440028).
Author information
Authors and Affiliations
Contributions
LW, BL and YY: methodology, data analysis, visualization, validation, and writing—original draft preparation and writing. QZ and SC: data analysis and visualization. YL and SH: conceptualization, supervision, project administration, funding acquisition, writing—original draft preparation and writing—review and editing. All authors have read and agreed to the published version of the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
All the authors declare no conflicts of interest.
Additional information
Communicated by Bing Yang.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Wang, L., Liu, B., Yang, Y. et al. The comparative studies of complete chloroplast genomes in Actinidia (Actinidiaceae): novel insights into heterogenous variation, clpP gene annotation and phylogenetic relationships. Mol Genet Genomics 297, 535–551 (2022). https://doi.org/10.1007/s00438-022-01868-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-022-01868-4