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Application of Chloroplast Phylogenomics to Resolve Species Relationships Within the Plant Genus Amaranthus

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Abstract

Amaranthus species are an emerging and promising nutritious traditional vegetable food source. Morphological plasticity and poorly resolved dendrograms have led to the need for well resolved species phylogenies. We hypothesized that whole chloroplast phylogenomics would result in more reliable differentiation between closely related amaranth species. The aims of the study were therefore: to construct a fully assembled, annotated chloroplast genome sequence of Amaranthus tricolor; to characterize Amaranthus accessions phylogenetically by comparing barcoding genes (matK, rbcL, ITS) with whole chloroplast sequencing; and to use whole chloroplast phylogenomics to resolve deeper phylogenetic relationships. We generated a complete A. tricolor chloroplast sequence of 150,027 bp. The three barcoding genes revealed poor inter- and intra-species resolution with low bootstrap support. Whole chloroplast phylogenomics of 59 Amaranthus accessions increased the number of parsimoniously informative sites from 92 to 481 compared to the barcoding genes, allowing improved separation of amaranth species. Our results support previous findings that two geographically independent domestication events of Amaranthus hybridus likely gave rise to several species within the Hybridus complex, namely Amaranthus dubius, Amaranthus quitensis, Amaranthus caudatus, Amaranthus cruentus and Amaranthus hypochondriacus. Poor resolution of species within the Hybridus complex supports the recent and ongoing domestication within the complex, and highlights the limitation of chloroplast data for resolving recent evolution. The weedy Amaranthus retroflexus and Amaranthus powellii was found to share a common ancestor with the Hybridus complex. Leafy amaranth, Amaranthus tricolor, Amaranthus blitum, Amaranthus viridis and Amaranthus graecizans formed a stable sister lineage to the aforementioned species across the phylogenetic trees. This study demonstrates the power of next-generation sequencing data and reference-based assemblies to resolve phylogenies, and also facilitated the identification of unknown Amaranthus accessions from a local genebank. The informative phylogeny of the Amaranthus genus will aid in selecting accessions for breeding advanced genotypes to satisfy global food demand.

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References

  • Achigan-Dako EG, Sogbohossou OE, Maundu P (2014) Current knowledge on Amaranthus spp.: research avenues for improved nutritional value and yield in leafy amaranths in sub-Saharan Africa. Euphytica 197:303–317

    Article  CAS  Google Scholar 

  • Akond M, Islam S, Wang X (2013) Genotypic variation in biomass traits and cell wall components among 35 diverse accessions of Amaranthaceae family. J Appl Phytotechnol Environ Sanit 2:37–45

    CAS  Google Scholar 

  • Alamgir M, Kibria M, Islam M (2011) Effects of farm yard manure on cadmium and lead accumulation in Amaranth (Amaranthus oleracea L.). J Soil Sci Environ Manag 2:237–240

    Google Scholar 

  • Alemayehu RF, Bendevis MA, Jacobsen SE (2015) The potential for utilizing the seed crop amaranth (Amaranthus spp.) in East Africa as an alternative crop to support food security and climate change mitigation. J Agron Crop Sci 201:321–329

    Article  CAS  Google Scholar 

  • Barrett CF, Davis JI, Leebens-Mack J, Conran JG, Stevenson DW (2013) Plastid genomes and deep relationships among the commelinid monocot angiosperms. Cladistics 29:65–87

    Article  Google Scholar 

  • Bell KL, de Vere N, Keller A, Richardson RT, Gous A, Burgess KS, Brosi BJ (2016) Pollen DNA barcoding: current applications and future prospects 1. Genome 59:629–640

    Article  PubMed  Google Scholar 

  • Bezeng B, Davies TJ, Daru BH, Kabongo RM, Maurin O, Yessoufou K, van der Bank H, Van der Bank M (2017) Ten years of barcoding at the African Centre for DNA barcoding. Genome 60:629–638

    Article  CAS  PubMed  Google Scholar 

  • Braukmann TW, Kuzmina ML, Sills J, Zakharov EV, Hebert PD (2017) Testing the efficacy of DNA barcodes for identifying the vascular plants of Canada. PLoS ONE 12:e0169515

    Article  PubMed  PubMed Central  Google Scholar 

  • Brenner DM, Baltensperger DD, Kulakow PA, Lehmann JW, Myers RL, Slabbert MM, Sleugh BB (2000) Genetic resources and breeding of Amaranthus. In: Janick J (ed) Plant breeding reviews, vol 19. Wiley, New York, pp 227–285

    Google Scholar 

  • Burgess KS, Fazekas AJ, Kesanakurti PR, Graham SW, Husband BC, Newmaster SG, Percy DM, Hajibabaei M, Barrett SC (2011) Discriminating plant species in a local temperate flora using the rbcL + matK DNA barcode. Methods Ecol Evol 2:333–340

    Article  Google Scholar 

  • Chan K, Sun M (1997) Genetic diversity and relationships detected by isozyme and RAPD analysis of crop and wild species of Amaranthus. TAG 95:865–873

    Article  CAS  Google Scholar 

  • Chaney L, Mangelson R, Ramaraj T, Jellen EN, Maughan PJ (2016) The complete chloroplast genome sequences for four Amaranthus species (Amaranthaceae). Appl Plant Sci 4:1600063

    Article  Google Scholar 

  • Chung H-J, Jung JD, Park H-W, Kim J-H, Cha HW, Min SR, Jeong W-J, Liu JR (2006) The complete chloroplast genome sequences of Solanum tuberosum and comparative analysis with Solanaceae species identified the presence of a 241-bp deletion in cultivated potato chloroplast DNA sequence. Plant Cell Rep 25:1369–1379

    Article  CAS  PubMed  Google Scholar 

  • Costea M, Brenner DM, Tardif FJ, Tan YF, Sun M (2006) Delimitation of Amaranthus cruentus L. and Amaranthus caudatus L. using micromorphology and AFLP analysis: an application in germplasm identification. Genet Resour Crop Ev 53:1625–1633

    Article  Google Scholar 

  • Cuénoud P, Savolainen V, Chatrou LW, Powell M, Grayer RJ, Chase MW (2002) Molecular phylogenetics of Caryophyllales based on nuclear 18S rDNA and plastid rbcL, atpB, and matK DNA sequences. Am J Bot 89:132–144

    Article  PubMed  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772–772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Das S (2011) Systematics and taxonomic delimitation of vegetable, grain and weed amaranths: a morphological and biochemical approach. Genet Resour Crop Evol 59:289–303

    Article  Google Scholar 

  • Davis CC, Xi Z, Mathews S (2014) Plastid phylogenomics and green plant phylogeny: almost full circle but not quite there. BMC Biol 12:11–15

    Article  PubMed  PubMed Central  Google Scholar 

  • Dong W, Xu C, Cheng T, Lin K, Zhou S (2013) Sequencing angiosperm plastid genomes made easy: a complete set of universal primers and a case study on the phylogeny of Saxifragales. GenBiol Evol 5:989–997

    Google Scholar 

  • Dong W, Liu H, Xu C, Zuo Y, Chen Z, Zhou S (2014) A chloroplast genomic strategy for designing taxon specific DNA mini-barcodes: a case study on ginsengs. BMC Genet 15:138

    Article  PubMed  PubMed Central  Google Scholar 

  • Dong W, Xu C, 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ebert AW (2014) Potential of underutilized traditional vegetables and legume crops to contribute to food and nutritional security, income and more sustainable production systems. Sust 6:319–335

    Article  Google Scholar 

  • Gerrano AS, van Rensburg WSJ, Adebola PO (2015) Genetic diversity of Amaranthus species in South Africa. S. Afr J Plant Soil 32:39–46

    Article  Google Scholar 

  • Gudu S, Gupta V (1988) Male-sterility in the grain amaranth (Amaranthus hypochondriacus ex-Nepal) variety Jumla. Euphytica 37:23–26

    Article  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Hackett SJ, Kimball RT, Reddy S, Bowie RC, Braun EL, Braun MJ, Chojnowski JL, Cox WA, Han K-L, Harshman J (2008) A phylogenomic study of birds reveals their evolutionary history. Science 320:1763–1768

    Article  CAS  PubMed  Google Scholar 

  • Hollingsworth PM, Graham SW, Little DP (2011) Choosing and using a plant DNA barcode. PLoS ONE 6:e19254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hollingsworth PM, Li D-Z, van der Bank M, Twyford AD (2016) Telling plant species apart with DNA: from barcodes to genomes. Phil Trans R Soc B 371:20150338

    Article  PubMed  PubMed Central  Google Scholar 

  • Huang H, Shi C, Liu Y, Mao S-Y, Gao L-Z (2014) Thirteen Camellia chloroplast genome sequences determined by high-throughput sequencing: genome structure and phylogenetic relationships. BMC Evol Biol 14:151–168

    Article  PubMed  PubMed Central  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  CAS  PubMed  Google Scholar 

  • Kavita P, Gandhi P (2017) Rediscovering the therapeutic potential of Amaranthus species: a review. Egypt J Basic Appl Sci 4:196–205

    Article  Google Scholar 

  • Kim JS, Kim JH (2013) Comparative genome analysis and phylogenetic relationship of order Liliales insight from the complete plastid genome sequences of two Lilies (Lilium longiflorum and Alstroemeria aurea). PLoS One 8:e68180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kress WJ, Erickson DL (2007) A two-locus global DNA barcode for land plants: the coding rbcL gene complements the non-coding trnH-psbA spacer region. PLoS ONE 2:e508

    Article  PubMed  PubMed Central  Google Scholar 

  • Kuzoff RK, Gasser CS (2000) Recent progress in reconstructing angiosperm phylogeny. Trends Plant Sci 5:330–336

    Article  CAS  PubMed  Google Scholar 

  • Lahaye R, Van der Bank M, Bogarin D, Warner J, Pupulin F, Gigot G, Maurin O, Duthoit S, Barraclough TG, Savolainen V (2008) DNA barcoding the floras of biodiversity hotspots. PNAS 105:2923–2928

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Cao H, Cai Y-F, Wang J-H, Qu S-P, Huang X-Q (2014) The complete chloroplast genome sequence of sugar beet (Beta vulgaris ssp. vulgaris). Mitochondrial DNA 25:209–211

    Article  CAS  PubMed  Google Scholar 

  • Lightfoot DJ, Jarvis DE, Ramaraj T, Lee R, Jellen EN, Maughan PJ (2017) Single-molecule sequencing and Hi-C-based proximity guided assembly of amaranth (Amaranthus hypochondriacus) chromosomes provide insights into genome evolution. BMC Biol 15:74

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Huo N, Dong L, Wang Y, Zhang S, Young HA, Feng X, Gu YQ (2013) Complete chloroplast genome sequences of Mongolia medicine Artemisia frigida and phylogenetic relationships with other plants. PLoS ONE 8:e57533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lubbe E, Rodda N (2016) Effects of greywater irrigation on germination, growth and photosynthetic characteristics in selected African leafy vegetables. Water SA 42:203–212

    Article  CAS  Google Scholar 

  • Ma P-F, Zhang Y-X, Zeng C-X, Guo Z-H, Li D-Z (2014) Chloroplast phylogenomic analyses resolve deep-level relationships of an intractable bamboo tribe Arundinarieae (Poaceae). Syst Biol 63:933–950

    Article  PubMed  Google Scholar 

  • Mallory MA, Hall RV, McNabb AR, Pratt DB, Jellen EN, Maughan PJ (2008) Development and characterization of microsatellite markers for the grain amaranths. Crop Sci 48:1098–1106

    Article  CAS  Google Scholar 

  • Mandal N, Das P (2002) Intra-and interspecific genetic diversity in grain Amaranthus using random amplified polymorphic DNA markers. Plant Tissue Cult 12:49–56

    Google Scholar 

  • Maughan PJ, Yourstone SM, Jellen EN, Udall JA (2009) SNP discovery via genomic reduction, barcoding, and 454-pyrosequencing in amaranth. The Plant Gen J 2:260–270

    Article  CAS  Google Scholar 

  • Mlakar SG, Turinek M, Jakop M, Bavec M, Bavec F (2010) Grain amaranth as an alternative and perspective crop in temperate climate. J Geogr 5:135–145

    Google Scholar 

  • Mnkeni A, Masika P, Maphaha M (2007) Nutritional quality of vegetable and seed from different accessions of Amaranthus in South Africa. Water SA 33:377–380

    CAS  Google Scholar 

  • Mosyakin SL, Robertson KR (1996) New infrageneric taxa and combinations in Amaranthus (Amaranthaceae). A Bot Fennici 33:275–281

    Google Scholar 

  • Nikiforova SV, Cavalieri D, Velasco R, Goremykin V (2013) Phylogenetic analysis of 47 chloroplast genomes clarifies the contribution of wild species to the domesticated apple maternal line. Mol Biol Evol 30:1751–1760

    Article  CAS  PubMed  Google Scholar 

  • Nock CJ, Waters DL, Edwards MA, Bowen SG, Rice N, Cordeiro GM, Henry RJ (2011) Chloroplast genome sequences from total DNA for plant identification. Plant Biotechnol J 9:328–333

    Article  CAS  PubMed  Google Scholar 

  • Panero JL, Funk V (2008) The value of sampling anomalous taxa in phylogenetic studies: major clades of the Asteraceae revealed. Mol Phylogenet Evol 47:757–782

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Patil SM, Rane NR, Adsul AA, Gholave AR, Yadav SR, Jadhav JP, Govindwar SP (2016) Study of molecular genetic diversity and evolutionary history of medicinally important endangered genus Chlorophytum using DNA barcodes. Biochem Syst Ecol 65:245–252

    Article  CAS  Google Scholar 

  • Poliseno L, Salmena L, Zhang J, Carver B, Haveman WJ, Pandolfi PP (2010) A coding-independent function of gene and pseudogene mRNAs regulates tumour biology. Nature 465:1033–1038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Puigbò P, Garcia-Vallvé S, McInerney JO (2007) TOPD/FMTS: a new software to compare phylogenetic trees. Bioinformatics 23:1556–1558

    Article  PubMed  Google Scholar 

  • Raju M, Varakumar S, Lakshminarayana R, Krishnakantha T, Baskaran V (2007) Carotenoid composition and vitamin A activity of medicinally important green leafy vegetables. Food Chem 101:1598–1605

    Article  CAS  Google Scholar 

  • Rastogi A, Shukla S (2013) Amaranth: a new millennium crop of nutraceutical values. Crit Rev Food Sci Nutr 53:109–125

    Article  CAS  PubMed  Google Scholar 

  • Sangeetha RK, Baskaran V (2010) Carotenoid composition and retinol equivalent in plants of nutritional and medicinal importance: efficacy of β-carotene from Chenopodium album in retinol-deficient rats. Food Chem 119:1584–1590

    Article  CAS  Google Scholar 

  • Sato S, Nakamura Y, Kaneko T, Asamizu E, Tabata S (1999) Complete structure of the chloroplast genome of Arabidopsis thaliana. DNA Res 6:283–290

    Article  CAS  PubMed  Google Scholar 

  • Sauer JD (1967) The grain amaranths and their relatives: a revised taxonomic and geographic survey. Ann Mo Bot Gard 54:103–137

    Article  Google Scholar 

  • Schmitz-Linneweber C, Maier RM, Alcaraz J-P, Cottet A, Herrmann RG, Mache R (2001) The plastid chromosome of spinach (Spinacia oleracea): complete nucleotide sequence and gene organization. Plant Mol Biol 45:307–315

    Article  CAS  PubMed  Google Scholar 

  • Shaw J, Shafer HL, Leonard OR, Kovach MJ, Schorr M, Morris AB (2014) Chloroplast DNA sequence utility for the lowest phylogenetic and phylogeographic inferences in angiosperms: the tortoise and the hare IV. AmJBot 101:1987–2004

    Google Scholar 

  • Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayashida N, Matsubayashi T, Zaita N, Chunwongse J, Obokata J, Yamaguchi-Shinozaki K (1986) The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. The EMBO J 5:2043–2049

    CAS  PubMed  Google Scholar 

  • Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539–545

    Article  PubMed  PubMed Central  Google Scholar 

  • Soltis PS, Soltis DE, Chase MW (1999) Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature 402:402–404

    Article  CAS  PubMed  Google Scholar 

  • Srivastava R (2017) An updated review on phyto-pharmacological and pharmacognostical profile of Amaranthus tricolor: A herb of nutraceutical potentials. Pharma Innov J 6:127–129

    Google Scholar 

  • Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 22:2688–2690

    Article  Google Scholar 

  • Stetter MG, Schmid KJ (2017) Analysis of phylogenetic relationships and genome size evolution of the Amaranthus genus using GBS indicates the ancestors of an ancient crop. Mol Phylogenet Evol 109:80–92

    Article  PubMed  Google Scholar 

  • Stetter MG, Müller T, Schmid KJ (2017) Genomic and phenotypic evidence for an incomplete domestication of South American grain amaranth (Amaranthus caudatus). Mol Ecol 26:871–886

    Article  CAS  PubMed  Google Scholar 

  • Straub SC, Parks M, Weitemier K, Fishbein M, Cronn RC, Liston A (2012) Navigating the tip of the genomic iceberg: next-generation sequencing for plant systematics. Am J Bot 99:349–364

    Article  CAS  PubMed  Google Scholar 

  • Stull GW, Moore MJ, Mandala VS, Douglas NA, Kates HR, Qi X, Brockington SF, Soltis PS, Soltis DE, Gitzendanner MA (2013) A targeted enrichment strategy for massively parallel sequencing of angiosperm plastid genomes. Appl Plant Sci 1:1200497

    Article  Google Scholar 

  • Sugiura M (1992) The chloroplast genome. In: Schilperoort RA, Dure L (eds) 10 Years plant molecular biology. Springer, Dordrecht, pp 149–168

    Chapter  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Timofte I, Timofte N, Brega V (2009) Development of bioenergy in Moldova. Problemele Energeticii Regionale 2:1–12

    Google Scholar 

  • Van Rensburg WJ, Van Averbeke W, Slabbert R, Faber M, Van Jaarsveld P, Van Heerden I, Wenhold F, Oelofse A (2007) African leafy vegetables in South Africa. Water SA 33:317–326

    Google Scholar 

  • Venskutonis PR, Kraujalis P (2013) Nutritional components of amaranth seeds and vegetables: a review on composition, properties, and uses. Comp Rev Food Sci Food Saf 12:381–412

    Article  CAS  Google Scholar 

  • Waselkov K (2013) Population Genetics and Phylogenetic Context of Weed Evolution in the Genus Amaranthus: Amaranthaceae. PhD Thesis, University of Washington

  • Wassom JJ, Tranel PJ (2005) Amplified Fragment Length Polymorphism-Based genetic relationships among weedy Amaranthus species. J Hered 96:410–416

    Article  CAS  PubMed  Google Scholar 

  • Williams AV, Miller JT, Small I, Nevill PG, Boykin LM (2016) Integration of complete chloroplast genome sequences with small amplicon datasets improves phylogenetic resolution in Acacia. Mol Phylogenet Evol 96:1–8

    Article  CAS  PubMed  Google Scholar 

  • Xu F, Sun M (2001) Comparative analysis of phylogenetic relationships of grain amaranths and their wild relatives (Amaranthus; Amaranthaceae) using internal transcribed spacer, amplified fragment length polymorphism, and double-primer fluorescent intersimple sequence repeat markers. Mol Phylogenet Evol 21:372–387

    Article  CAS  PubMed  Google Scholar 

  • Yang J-B, Yang S-X, Li H-T, Yang J, Li D-Z (2013) Comparative chloroplast genomes of Camellia species. PLoS One 8:e73053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang YJ, Ma PF, Li DZ (2011) High-throughput sequencing of six bamboo chloroplast genomes: phylogenetic implications for temperate woody bamboos (Poaceae: Bambusoideae). PLoS ONE 6:e20596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang T, Fang Y, Wang X, Deng X, Zhang X, Hu S, Yu J (2012) The complete chloroplast and mitochondrial genome sequences of Boea hygrometrica: insights into the evolution of plant organellar genomes. PLoS ONE 7:e30531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors wish to thank the Department of Science and Technology of South Africa, the National Research Foundation and the Professional Development Program of the Agricultural Research Council (ARC) in South Africa for providing funding for the PhD study from where this work originated. The authors also thank Dr Charles Hefer at the ARC for bioinformatics support. The authors thank Mr Willem Jansen van Rensburg and his staff at the ARC Vegetable and Ornamental Plant Institute for providing the Amaranthus germplasm set (SAG) as well as plant maintenance. The authors thank the Core Facility team at the ARC Biotechnology Platform for DNA sequencing.

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Authors and Affiliations

  1. Biotechnology Platform, Agricultural Research Council, Onderstepoort, Pretoria, 0110, South Africa

    Erika Viljoen & David J. G. Rees

  2. Department of Plant and Soil Sciences, Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Hatfield, 0083, South Africa

    Erika Viljoen & Dave K. Berger

  3. International Crops Research Institute for the Semi-Arid Tropics, Nairobi, Kenya

    Damaris A. Odeny

  4. Department of Genetics, Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Hatfield, 0083, South Africa

    Martin P. A. Coetzee

  5. Department of Life and Consumer Sciences, College of Agricultural and Environmental Sciences, University of South Africa, Florida, 1710, South Africa

    David J. G. Rees

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  1. Erika Viljoen
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Viljoen, E., Odeny, D.A., Coetzee, M.P.A. et al. Application of Chloroplast Phylogenomics to Resolve Species Relationships Within the Plant Genus Amaranthus. J Mol Evol 86, 216–239 (2018). https://doi.org/10.1007/s00239-018-9837-9

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