#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Complete Chloroplast Genomes of Vachellia nilotica and Senegalia senegal: Comparative Genomics and Phylogenomic Placement in a New Generic System


Autoři: Sajjad Asaf aff001;  Arif Khan aff001;  Abdul Latif Khan aff001;  Ahmed Al-Harrasi aff001;  Ahmed Al-Rawahi aff001
Působiště autorů: Natural and Medical Sciences Research Center, University of Nizwa, Nizwa, Oman aff001;  Genomics Group, Faculty of Biosciences and Aquaculture, Nord University, Bodo, Norway aff002
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0225469

Souhrn

Vachellia and Senegalia are the most important genera in the subfamily Mimosoideae (Fabaceae). Recently, species from both genera were separated from the long-characterized Acacia due to their macro-morphological characteristics. However, this morpho-taxonomic differentiation struggles to discriminate some species, for example, Vachellia nilotica and Senegalia senegal. Therefore, sequencing the chloroplast (cp) genomes of these species and determining their phylogenetic placement via conserved genes may help to validate the taxonomy. Hence, we sequenced the cp genomes of V. nilotica and S. senegal, and the results showed that the sizes of the genomes are 165.3 and 162.7 kb, respectively. The cp genomes of both species comprised large single-copy regions (93,849~91,791 bp) and pairs of inverted repeats (IR; 26,093~26,008 bp). The total numbers of genes found in the V. nilotica and S. senegal cp genomes were 135 and 132, respectively. Approximately 123:130 repeats and 290:281 simple sequence repeats were found in the S. senegal and V. nilotica cp genomes, respectively. Genomic characterization was undertaken by comparing these genomes with those of 17 species belonging to related genera in Fabaceae. A phylogenetic analysis of the whole genome dataset and 56 shared genes was undertaken by generating cladograms with the same topologies and placing both species in a new generic system. These results support the likelihood of identifying segregate genera from Acacia with phylogenomic disposition of both V. nilotica and S. senegal in the subfamily Mimosoideae. The current study is the first to obtain complete genomic information on both species and may help to elucidate the genome architecture of these species and evaluate the genetic diversity among species.

Klíčová slova:

Comparative genomics – Genomic libraries – Chloroplast genome – Phylogenetic analysis – Phylogenetics – Ribosomal RNA – Transfer RNA – Senegal


Zdroje

1. Haque A. Investigation of the fungi associated with dieback of prickly acacia (Vachellia nilotica subsp. indica) in Northern Australia. PhD, The University of Queensland. 2015.

2. Kyalangalilwa B, Boatwright JS, Daru BH, Maurin O, van der Bank M. Phylogenetic position and revised classification of A cacia sl (F abaceae: M imosoideae) in A frica, including new combinations in V achellia and S enegalia. Botanical Journal of the Linnean Society. 2013;172(4):500–23.

3. Beshai AA. The economics of a primary commodity: Gum Arabic. Oxford bulletin of economics and statistics. 1984;46(4):371–81.

4. Khan IA, Abourashed EA. Leung's encyclopedia of common natural ingredients: used in food, drugs and cosmetics: John Wiley & Sons; 2011.

5. Al-Assaf S, Phillips GO, Aoki H, Sasaki Y. Characterization and properties of Acacia senegal (L.) Willd. var. senegal with enhanced properties (Acacia (sen) SUPER GUM™): Part 1—Controlled maturation of Acacia senegal var. senegal to increase viscoelasticity, produce a hydrogel form and convert a poor into a good emulsifier. Food Hydrocolloids. 2007;21(3):319–28.

6. Motlagh S, Ravines P, Karamallah K, Ma Q. The analysis of Acacia gums using electrophoresis. Food hydrocolloids. 2006;20(6):848–54.

7. Arce LR, Banks H. A preliminary survey of pollen and other morphological characters in neotropical Acacia subgenus Aculeiferum (Leguminosae: Mimosoideae). Botanical Journal of the Linnean Society. 2001;135(3):263–70.

8. Salih AA, El Fadl MA, Kaarakka V, Luukkanen O. Symbiotic nitrogen fixation in eight Acacia senegal provenances in dryland clays of the Blue Nile Sudan estimated by the 15 N natural abundance method. Plant and Soil. 2005;275(1–2):261–9.

9. Bargali K, Bargali S. Acacia nilotica: a multipurpose leguminous plant. Nature and Science. 2009;7(4):11–9.

10. Raj A, Chandrawanshi S. Acacia nilotica: a multipurpose tree and source of Indian gum Arabic. South Indian Journal of Biological Sciences. 2015;1(2):66–9.

11. Good A. Toward nitrogen-fixing plants. Science. 2018;359(6378):869–70. doi: 10.1126/science.aas8737 29472469

12. Donalisio M, Cagno V, Civra A, Gibellini D, Musumeci G, Rittà M, et al. The traditional use of Vachellia nilotica for sexually transmitted diseases is substantiated by the antiviral activity of its bark extract against sexually transmitted viruses. Journal of ethnopharmacology. 2018;213:403–8. doi: 10.1016/j.jep.2017.11.039 29203273

13. Rather LJ, Mohammad F. Acacia nilotica (L.): a review of its traditional uses, phytochemistry, and pharmacology. Sustainable Chemistry and Pharmacy. 2015;2:12–30.

14. Daru BH, Kyalangalilwa B, Maurin O, van der Bank M, Boatwright JS. Phylogenetic position and revised classification of Acacia s.l. (Fabaceae: Mimosoideae) in Africa, including new combinations in Vachellia and Senegalia. Botanical Journal of the Linnean Society. 2013;172(4):500–23. doi: 10.1111/boj.12047

15. Orchard AE, Maslin BR. The case for conserving Acacia with a new type. Taxon. 2005;54(2):509–12.

16. Gardner FP, Pearce RB, Mitchell RL. Physiology of crop plants: Scientific Publishers; 2017.

17. Taylor DB, Dhileepan K. Implications of the changing phylogenetic relationships of Acacia sl on the biological control of Vachellia nilotica ssp. indica in Australia. Annals of Applied Biology. 2019;174(2):238–47.

18. Jansen RK, Ruhlman TA. Plastid genomes of seed plants. Genomics of chloroplasts and mitochondria: Springer; 2012. p. 103–26.

19. Daniell H, Lin C-S, Yu M, Chang W-J. Chloroplast genomes: diversity, evolution, and applications in genetic engineering. Genome biology. 2016;17(1):134. doi: 10.1186/s13059-016-1004-2 27339192

20. Wicke S, Schneeweiss GM, Müller KF, Quandt D. The evolution of the plastid chromosome in land plants: gene content, gene order, gene function. Plant molecular biology. 2011;76(3–5):273–97. doi: 10.1007/s11103-011-9762-4 21424877

21. Delannoy E, Fujii S, Colas des Francs-Small C, Brundrett M, Small I. Rampant gene loss in the underground orchid Rhizanthella gardneri highlights evolutionary constraints on plastid genomes. Molecular Biology and Evolution. 2011;28(7):2077–86. doi: 10.1093/molbev/msr028 21289370

22. Wicke S, Müller KF, de Pamphilis CW, Quandt D, Wickett NJ, Zhang Y, et al. Mechanisms of functional and physical genome reduction in photosynthetic and nonphotosynthetic parasitic plants of the broomrape family. The Plant Cell. 2013;25(10):3711–25. doi: 10.1105/tpc.113.113373 24143802

23. Land M, Hauser L, Jun S-R, Nookaew I, Leuze MR, Ahn T-H, et al. Insights from 20 years of bacterial genome sequencing. Functional & integrative genomics. 2015;15(2):141–61.

24. Parks M, Cronn R, Liston A. Increasing phylogenetic resolution at low taxonomic levels using massively parallel sequencing of chloroplast genomes. BMC biology. 2009;7(1):84.

25. Jansen RK, Cai Z, Raubeson LA, Daniell H, Leebens-Mack J, Müller KF, et al. Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. Proceedings of the National Academy of Sciences. 2007;104(49):19369–74.

26. Kim K, Lee S-C, Lee J, Lee HO, Joh HJ, Kim N-H, et al. Comprehensive survey of genetic diversity in chloroplast genomes and 45S nrDNAs within Panax ginseng species. PloS one. 2015;10(6):e0117159. doi: 10.1371/journal.pone.0117159 26061692

27. Ross JH. A conspectus of African acacia species1979.

28. Miller JT, Bayer RJ. Molecular phylogenetics of Acacia subgenera Acacia and Aculeiferum (Fabaceae: Mimosoideae), based on the chloroplast matK coding sequence and flanking trnK intron spacer regions. Australian Systematic Botany. 2003;16(1):27–33.

29. Shi C, Hu N, Huang H, Gao J, Zhao Y-J, Gao L-Z. An improved chloroplast DNA extraction procedure for whole plastid genome sequencing. Plos one. 2012;7(2):e31468. doi: 10.1371/journal.pone.0031468 22384027

30. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nature methods. 2012;9(4):357. doi: 10.1038/nmeth.1923 22388286

31. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28(12):1647–9. doi: 10.1093/bioinformatics/bts199 22543367

32. Hahn C, Bachmann L, Chevreux B. Reconstructing mitochondrial genomes directly from genomic next-generation sequencing reads—a baiting and iterative mapping approach. Nucleic acids research. 2013;41(13):e129–e. doi: 10.1093/nar/gkt371 23661685

33. Wyman SK, Jansen RK, Boore JL. Automatic annotation of organellar genomes with DOGMA. Bioinformatics. 2004;20(17):3252–5. doi: 10.1093/bioinformatics/bth352 15180927

34. Schattner P, Brooks AN, Lowe TM. The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic acids research. 2005;33(suppl_2):W686–W9.

35. Lohse M, Drechsel O, Bock R. OrganellarGenomeDRAW (OGDRAW): a tool for the easy generation of high-quality custom graphical maps of plastid and mitochondrial genomes. Current genetics. 2007;52(5–6):267–74. doi: 10.1007/s00294-007-0161-y 17957369

36. Kumar S, Nei M, Dudley J, Tamura K. MEGA: A biologist-centric software for evolutionary analysis of DNA and protein sequences. Briefings in Bioinformatics. 2008;9(4):299–306. doi: 10.1093/bib/bbn017 18417537

37. Frazer KA, Pachter L, Poliakov A, Rubin EM, Dubchak I. VISTA: computational tools for comparative genomics. Nucleic acids research. 2004;32(suppl_2):W273–W9.

38. Kurtz S, Choudhuri JV, Ohlebusch E, Schleiermacher C, Stoye J, Giegerich R. REPuter: the manifold applications of repeat analysis on a genomic scale. Nucleic acids research. 2001;29(22):4633–42. doi: 10.1093/nar/29.22.4633 11713313

39. Kraemer L, Beszteri B, Gäbler-Schwarz S, Held C, Leese F, Mayer C, et al. S TAMP: Extensions to the S TADEN sequence analysis package for high throughput interactive microsatellite marker design. BMC bioinformatics. 2009;10(1):41.

40. Benson G. Tandem repeats finder: a program to analyze DNA sequences. Nucleic acids research. 1999;27(2):573. doi: 10.1093/nar/27.2.573 9862982

41. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular biology and evolution. 2013;30(4):772–80. doi: 10.1093/molbev/mst010 23329690

42. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of molecular evolution. 1980;16(2):111–20. doi: 10.1007/bf01731581 7463489

43. Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19(12):1572–4. doi: 10.1093/bioinformatics/btg180 12912839

44. Asaf S, Khan AL, Khan MA, Waqas M, Kang S-M, Yun B-W, et al. Chloroplast genomes of Arabidopsis halleri ssp. gemmifera and Arabidopsis lyrata ssp. petraea: Structures and comparative analysis. Scientific reports. 2017;7(1):7556. doi: 10.1038/s41598-017-07891-5 28790364

45. Wu Z, Tembrock LR, Ge S. Are differences in genomic data sets due to true biological variants or errors in genome assembly: an example from two chloroplast genomes. PLoS One. 2015;10(2):e0118019. doi: 10.1371/journal.pone.0118019 25658309

46. Wang Y-H, Qu X-J, Chen S-Y, Li D-Z, Yi T-S. Plastomes of Mimosoideae: structural and size variation, sequence divergence, and phylogenetic implication. Tree genetics & genomes. 2017;13(2):41.

47. Yang JB, Li DZ, Li HT. Highly effective sequencing whole chloroplast genomes of angiosperms by nine novel universal primer pairs. Molecular Ecology Resources. 2014;14(5):1024–31. doi: 10.1111/1755-0998.12251 24620934

48. Asaf S, Waqas M, Khan AL, Khan MA, Kang S-M, Imran QM, et al. The complete chloroplast genome of wild rice (Oryza minuta) and its comparison to related species. Frontiers in plant science. 2017;8:304. doi: 10.3389/fpls.2017.00304 28326093

49. Raubeson LA, Peery R, Chumley TW, Dziubek C, Fourcade HM, Boore JL, et al. Comparative chloroplast genomics: analyses including new sequences from the angiosperms Nuphar advena and Ranunculus macranthus. BMC Genomics. 2007;8(1):174. doi: 10.1186/1471-2164-8-174 17573971

50. Zhang S-D, Jin J-J, Chen S-Y, Chase MW, Soltis DE, Li H-T, et al. Diversification of Rosaceae since the Late Cretaceous based on plastid phylogenomics. New Phytologist. 2017;214(3):1355–67. doi: 10.1111/nph.14461 28186635

51. Ahmed I, Matthews PJ, Biggs PJ, Naeem M, McLenachan PA, Lockhart PJ. Identification of chloroplast genome loci suitable for high-resolution phylogeographic studies of Colocasia esculenta (L.) Schott (Araceae) and closely related taxa. Molecular Ecology Resources. 2013;13(5):929–37. doi: 10.1111/1755-0998.12128 23718317

52. Downie SR, Jansen RK. A comparative analysis of whole plastid genomes from the Apiales: expansion and contraction of the inverted repeat, mitochondrial to plastid transfer of DNA, and identification of highly divergent noncoding regions. Systematic Botany. 2015;40(1):336–51.

53. Dong W-L, Wang R-N, Zhang N-Y, Fan W-B, Fang M-F, Li Z-H. Molecular Evolution of Chloroplast Genomes of Orchid Species: Insights into Phylogenetic Relationship and Adaptive Evolution. International Journal of Molecular Sciences. 2018;19(3):716. doi: 10.3390/ijms19030716 29498674

54. Ye X, Hu D, Guo Y, Sun R. Complete Chloroplast Genome of Castanopsis sclerophylla (Lindl.) Schott: Genome Structures, Comparative and Phylogenetic Analysis. BioRxiv. 2019:540617.

55. Yang J, Vázquez L, Chen X, Li H, Zhang H, Liu Z, et al. Development of Chloroplast and Nuclear DNA Markers for Chinese Oaks (Quercus Subgenus Quercus) and Assessment of Their Utility as DNA Barcodes. Frontiers in Plant Science. 2017;8(816). doi: 10.3389/fpls.2017.00816 28579999

56. Firetti F, Zuntini AR, Gaiarsa JW, Oliveira RS, Lohmann LG, Van Sluys M-A. Complete chloroplast genome sequences contribute to plant species delimitation: A case study of the Anemopaegma species complex. American Journal of Botany. 2017;104(10):1493–509. doi: 10.3732/ajb.1700302 29885220

57. Weng M-L, Blazier JC, Govindu M, Jansen RK. Reconstruction of the ancestral plastid genome in Geraniaceae reveals a correlation between genome rearrangements, repeats, and nucleotide substitution rates. Molecular biology and evolution. 2013;31(3):645–59. doi: 10.1093/molbev/mst257 24336877

58. Xue J, Wang S, Zhou S-L. Polymorphic chloroplast microsatellite loci in Nelumbo (Nelumbonaceae). American Journal of Botany. 2012;99(6):e240–e4. doi: 10.3732/ajb.1100547 22615305

59. Khan AL, Al-Harrasi A, Asaf S, Park CE, Park G-S, Khan AR, et al. The first chloroplast genome sequence of Boswellia sacra, a resin-producing plant in Oman. PloS one. 2017;12(1):e0169794. doi: 10.1371/journal.pone.0169794 28085925

60. Dugas DV, Hernandez D, Koenen EJ, Schwarz E, Straub S, Hughes CE, et al. Mimosoid legume plastome evolution: IR expansion, tandem repeat expansions, and accelerated rate of evolution in clpP. Scientific reports. 2015;5:16958. doi: 10.1038/srep16958 26592928

61. Greiner S, Wang X, Rauwolf U, Silber MV, Mayer K, Meurer J, et al. The complete nucleotide sequences of the five genetically distinct plastid genomes of Oenothera, subsection Oenothera: I. Sequence evaluation and plastome evolution. Nucleic acids research. 2008;36(7):2366–78. doi: 10.1093/nar/gkn081 18299283

62. Jeon J-H, Kim S-C. Comparative Analysis of the Complete Chloroplast Genome Sequences of Three Closely Related East-Asian Wild Roses (Rosa sect. Synstylae; Rosaceae). Genes. 2019;10(1):23.

63. Bouchenak-Khelladi Y, Maurin O, Hurter J, Van der Bank M. The evolutionary history and biogeography of Mimosoideae (Leguminosae): an emphasis on African acacias. Molecular Phylogenetics and Evolution. 2010;57(2):495–508. doi: 10.1016/j.ympev.2010.07.019 20696261

64. Luckow M, Miller JT, Murphy DJ, Livshultz T. A phylogenetic analysis of the Mimosoideae (Leguminosae) based on chloroplast DNA sequence data. Advances in legume systematics, part. 2003;10:197–220.

65. Miller JT, Seigler D. Evolutionary and taxonomic relationships of Acacia sl (Leguminosae: Mimosoideae). Australian Systematic Botany. 2012;25(3):217–24.

66. Givnish TJ, Spalink D, Ames M, Lyon SP, Hunter SJ, Zuluaga A, et al. Orchid phylogenomics and multiple drivers of their extraordinary diversification. Proceedings of the Royal Society B: Biological Sciences. 2015;282(1814):20151553.

67. Wysocki WP, Clark LG, Attigala L, Ruiz-Sanchez E, Duvall MR. Evolution of the bamboos (Bambusoideae; Poaceae): a full plastome phylogenomic analysis. BMC evolutionary biology. 2015;15(1):50.

68. Henry RJ. Plant diversity and evolution: genotypic and phenotypic variation in higher plants: Cabi Publishing; 2005.


Článek vyšel v časopise

PLOS One


2019 Číslo 11
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

plice
INSIGHTS from European Respiratory Congress
nový kurz

Současné pohledy na riziko v parodontologii
Autoři: MUDr. Ladislav Korábek, CSc., MBA

Svět praktické medicíny 3/2024 (znalostní test z časopisu)

Kardiologické projevy hypereozinofilií
Autoři: prof. MUDr. Petr Němec, Ph.D.

Střevní příprava před kolonoskopií
Autoři: MUDr. Klára Kmochová, Ph.D.

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#