Signatures of selection in recently domesticated macadamia

Abstract

Macadamia is a high value nut crop that is recently domesticated, ideal for testing the effect of artificial selection. Here, we sequence the genome of Hawaiian cultivar 'Kau' and assemble into 794 Mb in 14 pseudo-chromosomes with 37,728 genes. Genome analysis reveals a whole-genome duplication event, occurred 46.8 million years ago. Gene expansions occurred in gene families involves in fatty acid biosynthesis. Gene duplication of MADS-Box transcription factors in proanthocyanidin biosynthesis are relevant for seed coat development. Genome re-sequencing of 112 accessions reveals the origin of Hawaiian cultivars from Mount Bauple in southeast Queensland in Australia. Selective sweeps are detected in macadamia cultivars, including genes involved in fatty acid biosynthesis, seed coat development, and heat stress response. Such strong effects of artificial selection in few generations reveals the genomic basis for 'one-step operation' for clonal crop domestication. The knowledge gained could accelerate domestication of new crops from wild species.

Fig. 1. Distribution of genomic features along the macadamia genome.

a karyotype in Mbp. b Gene density, red means high density, and green indicate low density. c Gene expression, red indicates high expression level, and blue means low. d LTRs distribution in chromosomes. e DNA transposable elements distribution in chromosomes, red means high density and blue means low density.

Fig. 2. Evolutionary comparison and gene conservation of the macadamia (M. integrifolia) genome.

a Inter-genomic comparison between M. integrifolia and N. nucifera. b Inferred phylogenetic tree across seven plant species including macadamia, calibrated using the divergence time of A. thaliana and C. papaya (68–72 million years ago) and monocot and eudicot (120–140 million years ago) as calibrators. c Synonymous substitution rate (Ks) distributions of syntenic blocks for M. integrifolia and paralogs and orthologs with N. nucifera as shown by colored lines. d Shared gene families among At = A. thaliana, Os = O. sativa, Sly = S. lycopersicum, Vv = V. vinifera, Nu = N. nucifera, and Mi = M. integrifolia. The six species contain 8955 common gene families, and M. integrifolia has 42 specific gene families.

Fig. 3. Shell development in M. integrifolia.

a Phenotype of shell and kernel at different stages of fruit development. b Venn plot of up expression genes in stage Stage 1, Stage 2, Stage 3, Stage 4, and Stage 5 of shells. c Mfuzz clustering of differentially expressed transcripts in shell, kernel, and other tissues. d Schematic of shell development and hardening. A proposed model of STK, TT16, and Prx17 in regulation of shell development and hardening. e Phylogenetic tree of STK, AG, FUL, and SHP genes in multiple species, including M. integrifolia, N. nucifera, A. thaliana, V. vinifera, and C. papaya. STK, AG, FUL, and SHP clades are indicated in different colors. f Phylogenetic tree of Prx17 in M. integrifolia, N. nucifera, A. thaliana, V. vinifera, S. lycopersicum, Z. mays L., O. sativa, and S. bicolor.

Fig. 4. Kernel development in M. integrifolia.

a Expression of fatty acid biosynthesis-related genes in kernels and other tissues of macadamia. b Schematic of lipid biosynthesis pathway. KAS, ketoacyl synthases; SAD stearoyl-ACP desaturase, DGAT diacylglycerol acyltransferase. c Phylogeny of the KASI genes family in M. integrifolia. LPA lysophosphatidic acid, DAG diacylglycerol, TAG triacylglycerol, FFA free fatty acid. d Expression of fatty acid biosynthesis genes in tissues of M. integrifolia. Source data underlying a, d are provided as a Source Data file.

Fig. 5. Geographic distribution and drift paths of wild to varieties.

a Genetic-flow paths visualized on the map, the map was based on OpenStreetMap (Base map © OpenStreetMap, see https://www.openstreetmap.org/copyright) b Gene-drift in wild groups and varieties. c F_ST and π values of each groups. d LD decay for three wild groups (C1–C3) and varieties of M. integrifolia. e PCA clustering of three wild groups (C1–C3) and varieties of M. integrifolia. f Effective population size (N_e) history estimated using ANGSD using g (generation time) = 8 years and m (neutral mutation rate per generation) = 4.175*10⁻⁹ and plot by software Stairway plots with 200 bootstrap iterations. Source data underlying d, f are provided as a Source Data file.

Fig. 6. Signatures of selected signals in chromosomes 1, 2, 3, and 5 of M. integrifolia genome.

The upmost dotplot is nucleotide diversity (π) values, red indicate varieties and green line indicate wild group; the second lay is fixation index (F_ST) between the wild and cultivated macadamia accessions; the third lay is Tajima’s D values, red indicate varieties and green line indicate a wild group. The bottom is the genome-wide distribution of selective-sweep signals identified based on the cross-population composite likelihood ratio test (XP-CLR). TT12, TRANSPARENT TESTA; SDR short-chain dehydrogenase reductase, ANS anthocyanidin synthase.