Evolutionary signatures of the erosion of sexual reproduction genes in domesticated cassava (Manihot esculenta)

Abstract

Centuries of clonal propagation in cassava (Manihot esculenta) have reduced sexual recombination, leading to the accumulation of deleterious mutations. This has resulted in both inbreeding depression affecting yield and a significant decrease in reproductive performance, creating hurdles for contemporary breeding programs. Cassava is a member of the Euphorbiaceae family, including notable species such as rubber tree (Hevea brasiliensis) and poinsettia (Euphorbia pulcherrima). Expanding upon preliminary draft genomes, we annotated 7 long-read genome assemblies and aligned a total of 52 genomes, to analyze selection across the genome and the phylogeny. Through this comparative genomic approach, we identified 48 genes under relaxed selection in cassava. Notably, we discovered an overrepresentation of floral expressed genes, especially focused at 6 pollen-related genes. Our results indicate that domestication and a transition to clonal propagation have reduced selection pressures on sexually reproductive functions in cassava leading to an accumulation of mutations in pollen-related genes. This relaxed selection and the genome-wide deleterious mutations responsible for inbreeding depression are potential targets for improving cassava breeding, where the generation of new varieties relies on recombining favorable alleles through sexual reproduction.

Keywords: Plant Genetics and Genomics; cassava; clonal reproduction; deleterious mutations; evolution; sexual reproduction.

Fig. 1.

Assembly quality statistics. Assembly size and N50 are shown for long and short-read assemblies we produced, as well as the public assemblies used in this study (a). BUSCO scores are plotted with species’ text color matching sources (b).

Fig. 2.

Ortholog occurrence across all assemblies and phylogenetic relationships. An ortholog frequency histogram with the number of species that are represented in each ortholog group across all assemblies (a). Phylogenetic tree created from 4-fold degenerate sites from 1,000 randomly selected genes. The Euphorbiaceae subfamilies are designated by color (b). Cassava (M. esculenta) is part of the Crotonoideae subfamily and designated with “*”.

Fig. 3.

Selection signatures dN/dS gene conservation. a) Histogram of dN/dS values from all genes across cassava, with values >2 plotted at dN/dS = 2 (top). b) The difference in dN/dS score between the 52 species used in this study and cassava for each gene in cassava, with the y-axis showing the log ratio test P-value between these 2 models and dotted line showing multiple test correction significance threshold. c) The difference in dN/dS score between the 52 species used in this study and cassava summarized for each orthogroup in cassava, with the y-axis showing the log ratio test P-value between these 2 models and dotted line showing multiple test correction significance threshold. Arrows indicate difference in selection in cassava (i.e. ΔdN/dS < 0 implies a relaxation of purifying selection in cassava, or a transition to more positive selection, and ΔdN/dS > 0 implies a stronger purifying selection in cassava).

Fig. 4.

Identification of deleterious mutations in genes using within species residual variation intolerance scores. Regression for number of nonsynonymous SNPs (a) and putative deleterious SNPs (b) against the total number of SNPs in each gene in cassava. The residuals from each regression give RVIS and DRVIS scores, with the top and bottom 5% (n = 1287) shown.

Fig. 5.

Distributions of ΔdN/dS, RVIS, and DRVIS between pollen and nonpollen-related genes. Histograms are shown between pollen (blue) and nonpollen (orange) related genes for ΔdN/dS, RVIS, and DRVIS. Nonpollen-related genes are subsampled to an equal number of genes for visual comparison.