The jojoba genome reveals wide divergence of the sex chromosomes in a dioecious plant

Abstract

Most flowering plants are hermaphrodites, but around 6% of species are dioecious, having separate male and female plants. Sex chromosomes and some sex-specific genes have been reported in plants, but the genome sequences have not been compared. We now report the genome sequence of male and female jojoba (Simmondsia chinensis) plants, revealing a very large difference in the sex chromosomes. The male genome assembly was 832 Mb and the female 822 Mb. This was explained by the large size differences in the Y chromosome (37.6 Mb) compared with the X chromosome (26.9 Mb). Relative to the X chromosome, the Y chromosome had two large insertions each of more than 5 Mb containing more than 400 genes. Many of the genes in the chromosome-specific regions were novel. These male-specific regions included many flowering-related and stress response genes. Smaller insertions found only in the X chromosome totalled 877 kb. The wide divergence of the sex chromosomes suggests a long period of adaptation to diverging sex-specific roles. Male and female plants may have evolved to accommodate factors such as differing reproductive resource allocation requirements under the stress of the desert environment in which the plants are found. The sex-determining regions accumulate genes beneficial to each sex. This has required the evolution of many more novel sex-specific genes than has been reported for other organisms. This suggest that dioecious plants provide a novel source of genes for manipulation of reproductive performance and environmental adaptation in crops.

Keywords: Simmondsia chinensis; dioecious plants; jojoba; sex chromosomes; sexual dimorphism.

Figure 1

Comparison of (a) HiFi male assembly and (b) HiFi female assembly against male genome chromosome‐level assembly (Omni‐C scaffolding). The x‐axis shows the 26 pseudomolecules representing the chromosomes in the male genome and the y‐axis shows the contigs of the HiFi assembly of the (a) male and (b) female genome.

Figure 2

Illustration of sex chromosomes in jojoba. The numbers indicate the name and position of contigs. (a) 2D plot of alignment between the female‐specific region within contig 265F and the Y chromosome assembly. The purple circle shows the two insertions in contig 265F. (b) The X chromosome includes 877 Kb in two insertions which are not found in the Y chromosome or other parts of the male genome (female‐specific). The Y chromosome contains two male‐specific insertions, which are not found in the X chromosome or elsewhere in the female genome. The total length of the male‐specific insertions is approximately 10.7 Mb (5.5 Y₁ + 5.2 Mb Y₂). (c) 2D dot plot of alignment between the female genome assembly (contigs) and the Y chromosome assembly. The blue circle shows the two insertions into the Y chromosome (ChrY9).

Figure 3

Characterisation of male‐specific regions in the Y chromosomes. Illumina paired‐end read mapping coverage along the male‐specific Y chromosome (Figure 2) as the reference. Region 1 (distal end); region 2 (male‐specific Y₁); region 3 (region between Y₁ and Y₂); region 4 (male‐specific Y₂); and region 5 (distal end). (a) SA1‐Male (Saudi), Dadi Dadi, and T100: jojoba male genotypes. (b) SA1‐Female (Saudi), Wadi Wadi, and Q103: Jojoba female genotypes. Region‐wise average coverage values are normalised with respect to the total nucleotides of paired‐end reads of the SA1‐Female (Saudi) genotype mapped to the jojoba male‐specific Y chromosome. (c) Repetitive element mapping track of a region of the jojoba male‐specific Y₁ chromosome region. The sex‐specific regions are gene‐rich. The space between the coding sequences (intergenic spaces and introns) is almost completely filled with repetitive sequences.