Abstract
Key message
By comparing the chloroplast genomes of three willows, it is found that the genome structure is relatively conservative, and the large variations are more derived from the noncoding regions.
Abstract
Salix L., the largest genus in Salicaceae, has great value in ecology and economy. Here, we compared the chloroplast genomes of three important sand-fixing shrubs of the genus Salix: Salix gordejevii (size: 155,279 bp); S. cheilophila (size: 155,322 bp); and S. psammophila (size: 155,278 bp). The quadripartite circular structures of these genome sequences have the same structure and gene contents with 84 protein-coding genes, 38 tRNA genes, and eight rRNA genes. Long repeats including forward and palindromic repeats were found in three plastomes. The mononucleotide simple sequence repeats (SSRs) were dominant and accounted for more than 64% in all three plastomes, whereas hexanucleotide SSRs existed only in S. gordejevii. The noncoding and intergenic regions have greater variations than the coding regions, and eight highly variable regions were identified within the Salix chloroplast genomes, which could be utilized as potential markers for phylogenetic studies and phylogeography. In addition, we found 34 indels with more than 5 bases, which can be used to further identify S. gordejevii and S. psammophila with similar morphologies. Phylogenetic analysis based on whole cp genomes showed that S. gordejevii and S. magnifica are closely related, S. psammophila was a sister to S. suchowensis, and S. cheilophila clustered with them. The completed genomes in this study provide useful genetic resources for future research on species identification, phylogenetic relationships, and the adaptive evolution of Salix species.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and material
The datasets used or analyzed during the current study are available from the corresponding author upon reasonable request.
References
Abdollahzadeh A, Osaloo SK, Maassoumi AA (2011) Molecular phylogeny of the genus Salix (Salicaceae) with an emphasize to its species in Iran. Iran J Bot 17:244–253
Amiryousefi A, Hyvönen J, Poczai P (2018) IRscope: an online program to visualize the junction sites of chloroplast genomes. Bioinformatics 34:3030–3031. https://doi.org/10.1093/bioinformatics/bty220
Argus GW (1997) Infrageneric classification of Salix L. (Salicaceae) in the New World. Syst Bot Monogr 52:1–121. https://doi.org/10.2307/25096638
Argus GW (2010) Salix. In: Flora of North America Editorial Committee (ed) Flora of North America, vol 7. Magnoliophyta: Salicaceae to Brassicaceae. Oxford University Press, New York, pp 23–51
Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD et al (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19(5):455–477. https://doi.org/10.1089/cmb.2012.0021
Barkalov VY, Kozyrenko MM (2014) Phylogenetic analysis of the far eastern Salix (Salicaceae) based on sequence data from chloroplast DNA regions and ITS of nuclear ribosomal DNA. Bot Pac 3:3–19. https://doi.org/10.17581/bp.2014.03101
Boetzer M, Pirovano W (2012) Toward almost closed genomes with GapFiller. Genome Biol 13:R56. https://doi.org/10.1186/gb-2012-13-6-r56
Boetzer M, Henkel CV, Jansen HJ, Butler D, Pirovano W (2011) Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 27(4):578–579. https://doi.org/10.1093/bioinformatics/btq683
Chen JH, Sun H, Wen J, Yang YP (2010) Molecular phylogeny of Salix L. (Salicaceae) inferred from three chloroplast datasets and its systematic implications. Taxon 59(1):29–37. https://doi.org/10.3390/ijms19041042
Chen Y, Hu N, Wu H (2019) Analyzing and characterizing the chloroplast genome of Salix wilsonii. Biomed Res Int 2019:5190425. https://doi.org/10.1155/2019/5190425
Cho K-S, Yun B-K, Yoon Y-H, Hong S-Y, Mekapogu M, Kim K-H, Yang T-J (2015) Complete chloroplast genome sequence of tartary buckwheat (Fagopyrum tataricum) and comparative analysis with common buckwheat (F. esculentum). PLoS One 10:e0125332. https://doi.org/10.1371/journal.pone.0125332
Danecek P, Auton A, Abecasis G, Albers CA, Banks E, Depristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST et al (2011) The variant call format and VCFtools. Bioinformatics 27(15):2156–2158. https://doi.org/10.1093/bioinformatics/btr330
Dong W, Xu C, Li C, Dong W, Chao Xu, Li C, Sun J, Zuo Y, Shi S, Cheng T, Guo J, Zhou S (2015) ycf1, the most promising plastid DNA barcode of land plants. Sci Rep 5:8348. https://doi.org/10.1038/srep08348
Drescher A, Ruf S, Calsa T, Carrer H, Bock R (2000) The two largest chloroplast genome-encoded open reading frames of higher plants are essential genes. Plant J 22(2):97–104. https://doi.org/10.1046/j.1365-313x.2000.00722.x
Du SH, Wang ZS, Li YX (2015) Consistency between molecular phylogeny and morphological classification of the Salix matsudana Koidz. complex (Salicaceae). Genet Mol Res 14:8663–8671. https://doi.org/10.4238/2015.July.31.15
Dugas DV, Hernandez D, Koenen EJ, Schwarz E, Straub S, Hughes CE, Jansen RK, Nageswara-Rao M, Staats M, Trujillo JT, Hajrah NH, Alharbi NS, Al-Malki AL, Sabir JS, Bailey CD (2015) Mimosoid legume plastome evolution: IR expansion, tandem repeat expansions, and accelerated rate of evolution in clpP. Sci Rep 5:16958. https://doi.org/10.1038/srep16958
Fang ZF, Zhao SD, Skvortsov AK (1999) Salicaceae. In: Wu Z, Raven PH (eds) Flora of China, vol 4. Missouri Botanical Garden Press, St. Louis, pp 139–274
Grevich JJ, Daniell H (2005) Chloroplast genetic engineering: recent advances and future perspectives. Crit Rev Plant Sci 24(2):83–107. https://doi.org/10.1080/07352680590935387
Hao L, Zhang G, Lu D, Hu J, Jia H (2019) Analysis of the genetic diversity and population structure of Salix psammophila based on phenotypic traits and simple sequence repeat markers. Peer J 7:e6419. https://doi.org/10.7717/peerj.6419
He L, Zhang Y, Lee SY (2021) Complete plastomes of six species of Wikstroemia (Thymelaeaceae) reveal paraphyly with the monotypic genus Stellera. Sci Rep 11(1):13608. https://doi.org/10.1038/s41598-021-93057-3
Huang G, Zhao XY, Su YG, Zhao HL, Zhang TH (2008) Vertical distribution, biomass, production and turnover of fine roots along a topographical gradient in a sandy shrubland. Plant Soil 308:201–212. https://doi.org/10.1007/s11104-008-9620-6
Huang Y, Wang J, Yang Y, Fan C, Chen J (2017) Phylogenomic analysis and dynamic evolution of chloroplast genomes in Salicaceae. Front Plant Sci 8:1050. https://doi.org/10.3389/fpls.2017.01050
Huang W, Zhao X, Zhao X, Li Y, Feng J, Su N, Pan C, Luo Y (2018) Environmental determinants of genetic diversity in Salix gordejevii (Salicaceae) in three Sandy Lands, northern China. Acta Oecol 92:67–74. https://doi.org/10.1016/j.actao.2018.08.007
Hurst LD (2002) The Ka/Ks ratio: diagnosing the form of sequence evolution. TRENDS Genet 18:486–487. https://doi.org/10.1016/S0168-9525(02)02722-1
Jansen RK, Saski C, Lee S, Hansen AK, Daniell H (2011) Complete plastid genome sequences of three rosids (Castanea, Prunus, Theobroma): Evidence for at least two independent transfers of rpl22 to the nucleus. Mol Biol Evol 28(1):835–847. https://doi.org/10.1093/molbev/msq261
Jia H, Yang H, Sun P, Li J, Zhang J, Guo Y, Han X, Zhang G, Lu M, Hu J (2016) De novo transcriptome assembly, development of EST-SSR markers and population genetic analyses for the desert biomass willow, Salix psammophila. Sci Rep 6(1):39591. https://doi.org/10.1038/srep39591
Kuraku S, Zmasek CM, Nishimura O, Katoh K (2013) aLeaves facilitates on-demand exploration of metazoan gene family trees on MAFFT sequence alignment server with enhanced interactivity. Nucleic Acids Res 41:W22–W28. https://doi.org/10.1093/nar/gkt389
Kurtz S, Choudhuri JV, Ohlebusch E, Schleiermacher C, Stoye J, Giegerich R (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
Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9(4):357–359. https://doi.org/10.1038/nmeth.1923
Lauron-Moreau A, Pitre FE, Argus GW, Labrecque M, Brouillet L (2015) Phylogenetic Relationships of American Willows (Salix L., Salicaceae). PLoS ONE 10: e0121965 https://doi.org/10.1371/journal.pone.0121965
Li DM, Li J, Wang DR, Xu YC, Zhu GF (2021) Molecular evolution of chloroplast genomes in subfamily Zingiberoideae (Zingiberaceae). BMC Plant Biol 21(1):558. https://doi.org/10.1186/s12870-021-03315-9
Liu GZ, Liu GH, Lan Q, Li HY, Cao R, Wang J, Liu LH (2016) Comparative study on morphological characteristics and ecological adaptability of vessel elements of Salix gordejevii and S. microstachya var. bordensis. Acta Bot Boreali Occidentalia Sin 36(2):0316–0322. https://doi.org/10.7606/j.issn.1000-4025.2016.02.0316. (in Chinese)
Lohse M, Drechsel O, Bock R (2007) Organellar Genome DRAW (OGDRAW): a tool for the easy generation of high-quality custom graphical maps of plastid and mitochondrial genomes. Curr Genet 52:267–274. https://doi.org/10.1007/s00294-007-0161-y
Lowe TM, Chan PP (2016) tRNAscan-SE on-line: integrating search and context for analysis of transfer RNA genes. Nucleic Acids Res 44:W54–W57. https://doi.org/10.1093/nar/gkw413
Lu DY, Hao L, Huang HG, Zhang GS (2019) The complete chloroplast genome of Salix psammophila, a desert shrub in northwest China. Mitochondrial DNA B 4(2):3432–3433. https://doi.org/10.1080/23802359.2019.1675485
Makalowski W, Boguski MS (1998) Evolutionary parameters of the transcribed mammalian genome: an analysis of 2,820 orthologous rodent and human sequences. Proc Natl Acad Sci USA 95(16):9407–9412. https://doi.org/10.1073/pnas.95.16.9407
Martin W, Rujan T, Richly E, Hansen A, Cornelsen S, Lins T, Leister D, Stoebe B, Hasegawa M, Penny D (2002) Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc Natl Acad Sci USA 99(19):12246–12251. https://doi.org/10.1073/pnas.182432999
Millen RS, Olmstead RG, Adams KL, Palmer JD, Lao NT, Heggie L, Kavanagh TA et al (2001) Many parallel losses of infA from chloroplast DNA during angiosperm evolution with multiple independent transfers to the nucleus. Plant Cell 13(3):645–658. https://doi.org/10.2307/3871412
Mo Z, Lou W, Chen Y, Jia X, Zhai M, Guo Z, Xuan J (2020) The chloroplast genome of Carya illinoinensis: genome structure, adaptive evolution, and phylogenetic analysis. Forests 11(2):207. https://doi.org/10.3390/f11020207
Nauman M, Kale RK, Singh RP (2018) Polyphenols of Salix aegyptiaca modulate the activities of drug metabolizing and antioxidant enzymes, and level of lipid peroxidation. BMC Complement Altern Med 18(1):81. https://doi.org/10.1186/s12906-018-2143-7
Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3(5):418–426. https://doi.org/10.1093/oxfordjournals.molbev.a040410
Newsholme C (1992) Willows: the genus Salix. Timber Press, Portland
Nielsen R (2005) Molecular signatures of natural selection. Annu Rev Genet 39:197–218. https://doi.org/10.1146/annurev.genet.39.073003.112420
Ohyama K, Fukuzawa H, Kohchi T, Shirai H, Sano T, Sano S, Umesono K, Shiki Y et al (1986) Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha chloroplast DNA. Nature 322:572–574. https://doi.org/10.1038/322572a0
Park J, Yongsung K, Hong X (2019) The complete chloroplast genome sequence of male individual of Korean endemic willow, Salix koriyanagi Kimura ex Goerz(Salicaceae). Mitochondrial DNA B 4(1):1619–1621. https://doi.org/10.1080/23802359.2019.1602012
Raisi Dehkordi Z, Rafieian-Kopaei M, Hosseini-Baharanchi FS (2019) A double-blind controlled crossover study to investigate the efficacy of salix extract on primary dysmenorrhea. Complement Ther Med 44:102–109. https://doi.org/10.1016/j.ctim.2019.04.002
Raman G, Park KT, Kim JH, Park SJ (2020) Characteristics of the completed chloroplast genome sequence of Xanthium spinosum: comparative analyses, identification of mutational hotspots and phylogenetic implications. BMC Genom 21:855. https://doi.org/10.21203/rs.3.rs-60093/v1
Ravi V, Khurana JP, Tyagi AK, Khurana P (2008) An update on chloroplast genomes. Pl Syst Evol 271:101–122. https://doi.org/10.1007/s00606-007-0608-0
Sharp PM, Li WH (1987) The rate of synonymous substitution in enterobacterial genes is inversely related to codon usage bias. Mol Biol Evol 4(3):222–230. https://doi.org/10.1093/oxfordjournals.molbev.a040443
Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayshida N, Matsubayasha T, Zaita N, Chunwongse J et al (1986) The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. Plant Mol Biol Rep 4:111–148. https://doi.org/10.1002/j.1460-2075.1986.tb04464.x
Souza U, Vitorino LC, Bessa LA, Silva SG (2020) The complete plastid genome of Artocarpus camansi: a high degree of conservation of the plastome structure in the family Moraceae. Forests 11(11):1179. https://doi.org/10.3390/f11111179
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9):1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Sun C, Li J, Dai X, Chen Y (2016) Analyzing and characterization of the chloroplast genome of Salix suchowensis. PeerJ Preprints 4:e2388v1. https://doi.org/10.7287/PEERJ.PREPRINTS.2388
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729. https://doi.org/10.1093/molbev/mst197
Teraminami T, Nakashima A, Ominami M, Yamamoto M, Zhang GS, Yoshikawa K (2013) Effects of sand burial depth on the root system of Salix cheilophila seedlings in Mu Us Sandy Land, Inner Mongolia, China. Landsc Ecol Eng 9(2):249–257. https://doi.org/10.1007/s11355-012-0205-4
The Chimpanzee Sequencing and Analysis Consortium (2005) Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437(7055):69–87. https://doi.org/10.1038/nature04072
Ueda M, Fujimoto M, Arimura S, Murata J, Tsutsumi N, Kadowaki K (2007) Loss of the rpl32 gene from the chloroplast genome and subsequent acquisition of a preexisting transit peptide within the nuclear gene in Populus. Gene 402(1–2):51–56. https://doi.org/10.1016/j.gene.2007.07.019
Wang ZS, Du SH, Dayanandan S, Wang DS, Zeng YF, Zhang JG (2014) Phylogeny reconstruction and hybrid analysis of Populus (Salicaceae) based on nucleotide sequences of multiple single-copy nuclear genes and plastid fragments. PLoS One 9:e103645. https://doi.org/10.1371/journal.pone.0103645
Wu Z (2015) The new completed genome of purple willow (Salix purpurea) and conserved chloroplast genome structure of Salicaceae. J Nat Sci 1:e49
Wu J, Nyman T, Wang DC, Argus GW, Yang YP, Chen JH (2015) Phylogeny of Salix subgenus Salix s.l. (Salicaceae): delimitation, biogeography, and reticulate evolution. BMC Evol Biol 15:31. https://doi.org/10.1186/s12862-015-0311-7
Wyman SK, Jansen RK, Boore JL (2004) Automatic annotation of organellar genomes with DOGMA. Bioinformatics 20(17):3252–3255. https://doi.org/10.1093/bioinformatics/bth352
Yang Y, Zhu J, Feng L, Zhou T, Bai G, Yang J, Zhao G (2018) Plastid genome comparative and phylogenetic analyses of the key genera in Fagaceae: highlighting the effect of codon composition bias in phylogenetic inference. Front Plant Sci 9:82. https://doi.org/10.3389/fpls.2018.00082
Yang H, Wang L, Chen H, Jiang M, Wu W, Liu S, Wang J, Liu C (2021) Phylogenetic analysis and development of molecular markers for five medicinal Alpinia species based on complete plastome sequences. BMC Plant Biol 21(1):431. https://doi.org/10.1186/s12870-021-03204-1
Yap JY, Rohner T, Greenfield A, Van DMM, Mcpherson H, Glenn W, Kornfeld G, Marendy E, Annie YHP, Wilton A, Wilkins MR, Rossetto M, Delaney SK (2015) Complete chloroplast genome of the wollemi pine (Wollemia nobilis): structure and evolution. PLoS One 10:e0128126. https://doi.org/10.1371/journal.pone.0128126
Yue XF, Cui JY, Zhang TH, Wang SK, Lian J, Wang XY, Yun JY (2013) Characteristics of rainfall interception and redistribution for Salix gordejevii in Horqin sandy land, Northeast China. Acta Pratacult Sin 22(6):46–52. https://doi.org/10.11686/cyxb20130606. (in Chinese)
Zhang J (2000) Rates of conservative and radical nonsynonymous nucleotide substitutions in mammalian nuclear genes. J Mol Evol 50(1):56–68. https://doi.org/10.1007/s002399910007
Zhang Z, Li J, Zhao XQ, Wang J, Wong KSG, Yu J (2006) KaKs_calculator: calculating Ka and Ks through model selection and model averaging. Genom Proteom Bioinf 4(4):259–263. https://doi.org/10.1016/S1672-0229(07)60007-2
Zhang L, Xi Z, Wang M, Guo X, Ma T (2018) Plastome phylogeny and lineage diversification of Salicaceae with focus on poplars and willows. Ecol Evol 8(16):7817–7823. https://doi.org/10.1002/ece3.4261
Zhang J, Jiang Z, Su H, Zhao H, Cai J (2019) The complete chloroplast genome sequence of the endangered species Syringa pinnatifolia (Oleaceae). Nord J Bot 37(5):2201–2212. https://doi.org/10.1111/njb.02201
Zhao Y, Wang L, Knighton J, Jaivime E, Wassen M (2021) Contrasting adaptive strategies by Caragana korshinskii and Salix psammophila in a semiarid revegetated ecosystem. Agr Forest Meteorol 300:108323. https://doi.org/10.1016/j.agrformet.2021.108323
Zhou M, Long W, Li X (2008) Analysis of synonymous codon usage in chloroplast genome of Populus alba. J for res 19(4):293–297. https://doi.org/10.1007/s11676-008-0052-1
Zhu Y, Wang G, Li R (2016) Seasonal dynamics of water use strategy of two Salix shrubs in alpine sandy land, Tibetan Plateau. PLoS One 11:e0156586. https://doi.org/10.1371/journal.pone.0156586
Funding
This study was funded by the Inner Mongolia Autonomous Region Natural Science Fund Project of China (grant number: 2018MS03013) and by the National Natural Science Foundation of China (grant number: 31160167).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Consent for publication
Written informed consent for publication was obtained from all participants.
Additional information
Communicated by K. Braeutigam.
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.
468_2023_2388_MOESM1_ESM.pdf
Supplementary file1 Figure S1: Amino acid frequencies of the protein-coding sequences of the three Salix plastomes. (PDF 45 KB)
468_2023_2388_MOESM2_ESM.pdf
Supplementary file2 Figure S2: Nucleotide diversity (pi) values of coding regions in the whole plastomes of six Salix species. (PDF 149 KB)
468_2023_2388_MOESM3_ESM.pdf
Supplementary file3 Figure S3: Nucleotide diversity (pi) values of non-coding regions in the whole plastomes of six Salix species. (PDF 231 KB)
468_2023_2388_MOESM8_ESM.pdf
Supplementary file8 Figure S8: Phylogenetic trees of 29 Salicaceae species based on the protein-coding genes (single-copy) dataset. (PDF 146 KB)
468_2023_2388_MOESM11_ESM.xlsx
Supplementary file11Table S3. The RSCU value in S. gordejevii, S. cheilophila and S. psammophila plastomes. (XLSX 14 KB)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Lu, D., Huang, H., Zhang, L. et al. Complete chloroplast genomes of three sand-fixing Salix shrubs from Northwest China: comparative and phylogenetic analysis and interspecific identification. Trees 37, 849–861 (2023). https://doi.org/10.1007/s00468-023-02388-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00468-023-02388-3