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

Abstract

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.

Quantifying the role of genome size and repeat content in adaptive variation and the architecture of flowering time in Amaranthus tuberculatus

“…Recent work has shown that the A . tuberculatus chromosome that contains the male sex determining region harbors a fragment of the Flowering Time and Heading date 3a genes [ 79 ] in addition to the evidence we provide here of copy number and polygenic variation for flowering time being differentiated across sexes. Because the sex-determining region represents a large region of low recombination (the sex bias in genome size here suggesting up to 11 Mb of which may be absent in males), one possibility is that agricultural selection on a Y-haplotype that contained an early flowering variant of these genes could have by chance driven lower repeat content to higher frequency in such environments.…”

Seed protein biotyping in Amaranthus species: a tool for rapid identification of weedy amaranths of concern

“…These two species, are nevertheless closely related [ 7 , 64 ], as is the case for two other mismatches where our biotyping indicating A. watsonii had A. palmeri as phenotypic identification. In this latter case, previous research has shown that A. watsonii and A. palmeri are sister species according to morphological and molecular characterization [ 7 , 65 ]. This is also suggested by comparison of full chloroplast genomes done in our lab (unpublished), and by a recently published plastome comparison analysis [ 66 ].…”

Genome-Wide Comparative Analysis of Five Amaranthaceae Species Reveals a Large Amount of Repeat Content

“…The GC% of the genomes were very similar, ranging from 32.3 to 37.18% ( Table 8 ), which has also been observed in other related genomes such as C. quinoa [ 24 ], B. vulgaris [ 27 ], and S. aralocaspica [ 25 ]. Genome features, including genome size, repeat content, heterozygosity, polyploidy, and GC percentage, have been shown to affect the quality of de novo assemblies; hence, genome profiling offers important insight into achieving a high-quality genome assembly [ 31 ]. The assembly completeness analysis showed that amaranth genomes present 92.61–96% of all BUSCOs (analysis with eudicot database) ( Table 2 ), and, compared with the other sequenced genomes currently available ( S. aralocaspica ; 89.5%) [ 25 ], ( S. oleracea ; 97.2%) [ 32 ], ( C. quinoa ; 97.3%) [ 24 ], it represents the good quality assemblies of amaranth genomes.…”