Draft genome of the peanut A-genome progenitor (Arachis duranensis) provides insights into geocarpy, oil biosynthesis, and allergens

Abstract

Peanut or groundnut (Arachis hypogaea L.), a legume of South American origin, has high seed oil content (45-56%) and is a staple crop in semiarid tropical and subtropical regions, partially because of drought tolerance conferred by its geocarpic reproductive strategy. We present a draft genome of the peanut A-genome progenitor, Arachis duranensis, and 50,324 protein-coding gene models. Patterns of gene duplication suggest the peanut lineage has been affected by at least three polyploidizations since the origin of eudicots. Resequencing of synthetic Arachis tetraploids reveals extensive gene conversion in only three seed-to-seed generations since their formation by human hands, indicating that this process begins virtually immediately following polyploid formation. Expansion of some specific gene families suggests roles in the unusual subterranean fructification of Arachis For example, the S1Fa-like transcription factor family has 126 Arachis members, in contrast to no more than five members in other examined plant species, and is more highly expressed in roots and etiolated seedlings than green leaves. The A. duranensis genome provides a major source of candidate genes for fructification, oil biosynthesis, and allergens, expanding knowledge of understudied areas of plant biology and human health impacts of plants, informing peanut genetic improvement and aiding deeper sequencing of Arachis diversity.

Keywords: Arachis duranensis; gene duplication; gene models; genome sequence; polyploidizations.

Fig. 1.

A. duranensis genome overview. From the outer edge inward, circles represent the 50 largest DNA sequence scaffolds (green), the genes on each scaffold (purple), SNP density at 100-kb intervals (blue), repeat density at 100 kb (green), transposable element density at 100 kb (yellow), and the fold-change values of transcripts (red). Links in the core connect duplicated sets of genes (E-value threshold of <1e-10 and 85% similarity).

Fig. 2.

Comparative genomic and evolutionary analysis. (A) Scatter plot of percentage of A. duranensis transcription factors in relation to soybean, Medicago, Lotus, chickpea, and pigeonpea. (B) Syntenic relationship between A. duranensis scaffolds and soybean chromosomes. (C) Phylogenetic tree for 16 plant species based on single copy orthologous genes. (D) Distribution of synonymous nucleotide substitutions (Ks) for A. duranensis, soybean, Medicago, and grape. (E) Allelic changes between the A and B subgenomes of synthetic tetraploid peanut lines, ISATGR 184 (Upper) and ISATGR 1212 (Lower).

Fig. 3.

Genes, TFs, and pathways related to the biological process “Aerial flower, subterranean fruit.” (A) Peanut fruit development (2, 3, 4, 5, 6, 7, 9, 12, and 17 indicate days after fertilization, DAF). Upon fertilization the gynophore reverts from upward growth after sensing gravity followed by signal transduction and organ response. Seed development is triggered only if the elongated peg penetrates soil. (B) Comparison of ω (K_a/Ks) of gravitropic orthologs in Arabidopsis thaliana-A. duranensis and A. thaliana-G. max for genes involved in photomorphogenesis (blue) or gravitropism (red). Circled genes show evidence of positive selection in both A. duranensis and G. max. (C) Gravitropism phases (gravity sensing, signal transduction and organ response) where three functionally identified genes (ARL2, AUX1, and RGD3) were found positively selected. (D) Numbers of TF family members identified in A. duranensis compared with other plant species (blue indicating low and red indicating high numbers). TFs in brackets have been found in large numbers in A. duranensis.

Fig. 4.

Genes involved in oil biosynthesis and encoding allergens. (A) Expression patterns of genes involved in fatty acid synthesis and TAG assembly in peanut seed. Expression levels were estimated by fragments per kilobase of transcript per million mapped fragments (FPKM) for each gene obtained by sequencing RNA samples from peanut seeds at six developmental stages. (B) Phylogenetic tree of allergens and their homologs identified in A. hypogaea and A. duranensis and other allergenic crops (wheat and soybean). A total of 69 allergens or homologous genes from 14 families group into 6 major clusters differentiated with colors. Different families having the same colors are more similar to each other than to other families. “Dots” indicate genes identified in the A. duranensis genome and “triangles” indicate genes previously identified in A. hypogaea. This figure also shows the distribution of 12 newly identified putative allergen genes from the A. duranensis assembly falling into different clusters and families.