Comparative analysis of dioecious Amaranthus plastomes and phylogenomic implications within Amaranthaceae s.s.

BACKGROUND: The genus Amaranthus L. consists of 70-80 species distributed across temperate and tropical regions of the world. Nine species are dioecious and native to North America; two of which are agronomically important weeds of row crops. The genus has been described as taxonomically challenging and relationships among species including the dioecious ones are poorly understood. In this study, we investigated the phylogenetic relationships among the dioecious amaranths and sought to gain insights into plastid tree incongruence. A total of 19 Amaranthus species' complete plastomes were analyzed. Among these, seven dioecious Amaranthus plastomes were newly sequenced and assembled, an additional two were assembled from previously published short reads sequences and 10 other plastomes were obtained from a public repository (GenBank). RESULTS: Comparative analysis of the dioecious Amaranthus species' plastomes revealed sizes ranged from 150,011 to 150,735 bp and consisted of 112 unique genes (78 protein-coding genes, 30 transfer RNAs and 4 ribosomal RNAs). Maximum likelihood trees, Bayesian inference trees and splits graphs support the monophyly of subgenera Acnida (7 dioecious species) and Amaranthus; however, the relationship of A. australis and A. cannabinus to the other dioecious species in Acnida could not be established, as it appears a chloroplast capture occurred from the lineage leading to the Acnida + Amaranthus clades. Our results also revealed intraplastome conflict at some tree branches that were in some cases alleviated with the use of whole chloroplast genome alignment, indicating non-coding regions contribute valuable phylogenetic signals toward shallow relationship resolution. Furthermore, we report a very low evolutionary distance between A. palmeri and A. watsonii, indicating that these two species are more genetically related than previously reported. CONCLUSIONS: Our study provides valuable plastome resources as well as a framework for further evolutionary analyses of the entire Amaranthus genus as more species are sequenced.

Genomic profiling of dioecious Amaranthus species provides novel insights into species relatedness and sex genes.

BACKGROUND: Amaranthus L. is a diverse genus consisting of domesticated, weedy, and non-invasive species distributed around the world. Nine species are dioecious, of which Amaranthus palmeri S. Watson and Amaranthus tuberculatus (Moq.) J.D. Sauer are troublesome weeds of agronomic crops in the USA and elsewhere. Shallow relationships among the dioecious Amaranthus species and the conservation of candidate genes within previously identified A. palmeri and A. tuberculatus male-specific regions of the Y (MSYs) in other dioecious species are poorly understood. In this study, seven genomes of dioecious amaranths were obtained by paired-end short-read sequencing and combined with short reads of seventeen species in the family Amaranthaceae from NCBI database. The species were phylogenomically analyzed to understand their relatedness. Genome characteristics for the dioecious species were evaluated and coverage analysis was used to investigate the conservation of sequences within the MSY regions. RESULTS: We provide genome size, heterozygosity, and ploidy level inference for seven newly sequenced dioecious Amaranthus species and two additional dioecious species from the NCBI database. We report a pattern of transposable element proliferation in the species, in which seven species had more Ty3 elements than copia elements while A. palmeri and A. watsonii had more copia elements than Ty3 elements, similar to the TE pattern in some monoecious amaranths. Using a Mash-based phylogenomic analysis, we accurately recovered taxonomic relationships among the dioecious Amaranthus species that were previously identified based on comparative morphology. Coverage analysis revealed eleven candidate gene models within the A. palmeri MSY region with male-enriched coverages, as well as regions on scaffold 19 with female-enriched coverage, based on A. watsonii read alignments. A previously reported FLOWERING LOCUS T (FT) within A. tuberculatus MSY contig was also found to exhibit male-enriched coverages for three species closely related to A. tuberculatus but not for A. watsonii reads. Additional characterization of the A. palmeri MSY region revealed that 78% of the region is made of repetitive elements, typical of a sex determination region with reduced recombination. CONCLUSIONS: The results of this study further increase our understanding of the relationships among the dioecious species of the Amaranthus genus as well as revealed genes with potential roles in sex function in the species.