Application of Chloroplast Phylogenomics to Resolve Species Relationships Within the Plant Genus Amaranthus
- 189 Downloads
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.
KeywordsPhylogenomics Chloroplast Amaranthus Barcode
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.
Compliance with Ethical Standards
Conflict of interest
The authors declare that they have no conflict of interest.
- 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 2:37–45Google 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 2:237–240Google 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 227–285Google 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 25:1369–1379CrossRefPubMedGoogle 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 5:989–997Google Scholar
- Mandal N, Das P (2002) Intra-and interspecific genetic diversity in grain Amaranthus using random amplified polymorphic DNA markers. Plant Tissue Cult 12:49–56Google 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 5:135–145Google Scholar
- Mnkeni A, Masika P, Maphaha M (2007) Nutritional quality of vegetable and seed from different accessions of Amaranthus in South Africa. Water SA 33:377–380Google Scholar
- Mosyakin SL, Robertson KR (1996) New infrageneric taxa and combinations in Amaranthus (Amaranthaceae). A Bot Fennici 33:275–281Google 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 101:1987–2004Google Scholar
- Srivastava R (2017) An updated review on phyto-pharmacological and pharmacognostical profile of Amaranthus tricolor: A herb of nutraceutical potentials. Pharma Innov J 6:127–129Google Scholar
- Timofte I, Timofte N, Brega V (2009) Development of bioenergy in Moldova. Problemele Energeticii Regionale 2:1–12Google 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 33:317–326Google Scholar
- Waselkov K (2013) Population Genetics and Phylogenetic Context of Weed Evolution in the Genus Amaranthus: Amaranthaceae. PhD Thesis, University of WashingtonGoogle 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 21:372–387CrossRefPubMedGoogle Scholar