The genome evolution and low-phosphorus adaptation in white lupin

Abstract

White lupin (Lupinus albus) is a legume crop that develops cluster roots and has high phosphorus (P)-use efficiency (PUE) in low-P soils. Here, we assemble the genome of white lupin and find that it has evolved from a whole-genome triplication (WGT) event. We then decipher its diploid ancestral genome and reconstruct the three sub-genomes. Based on the results, we further reveal the sub-genome dominance and the genic expression of the different sub-genomes varying in relation to their transposable element (TE) density. The PUE genes in white lupin have been expanded through WGT as well as tandem and dispersed duplications. Furthermore, we characterize four main pathways for high PUE, which include carbon fixation, cluster root formation, soil-P remobilization, and cellular-P reuse. Among these, auxin modulation may be important for cluster root formation through involvement of potential genes LaABCG36s and LaABCG37s. These findings provide insights into the genome evolution and low-P adaptation of white lupin.

Fig. 1. Phylogenetic relationships of white lupin and its genome comparison to the other legume species.

a Phylogenetic tree of 16 legume species built on synonymous sites from syntenic homologous genes; A. thaliana was used as an outgroup species. The two red stars denote the whole-genome duplication event, while the three red stars denote the whole-genome triplication event. b Frequency distribution of K_s values between syntenic genes of compared genomes. c Dot plotting of syntenic genes between genomes of L. albus and L. angustifolius. d Dot plotting of syntenic genes between genomes of L. albus and P. vulgaris; the segments from the three sub-genomes in L. albus are plotted in red, green, and blue. The source data underlying Fig. 1b are provided as a Source Data file.

Fig. 2. Genome evolution trajectory of white lupin.

a Distribution of 26 genomic blocks (GBs) in the 11 chromosomes of P. vulgaris. b The re-arranged GBs in the eight chromosomes of M. truncatula. The numbers to the right of the GBs denote the order of fragmented GBs. c Distribution of 26 GBs in the deduced nine ancestral chromosomes of the diploid ancestor of white lupin. d Distribution of the triplicated 26 GBs in the 25 chromosomes of white lupin; the colors red, green, and blue indicate GBs from sub-genomes LF, MF1, and MF2, respectively. “′” denote inverted GBs.

Fig. 3. Sub-genome dominance phenomenon observed in the paleo-allopolyploidy genome of white lupin.

a The density of syntenic genes in three sub-genomes of L. albus compared to the deduced diploid ancestor of Lupinus (genes of diploid genome P. vulgaris were used as the reference). The x-axis denotes the physical position of each gene locus in the genome of the diploid ancestor. The y-axis denotes the percentage of retained homologous genes in white lupin sub-genomes around each diploid ancestor gene, where 500 genes flanking each side of a certain gene locus were analyzed, giving a total window size of 1001 genes. b The number of dominantly expressed paralogs between sub-genomes LF and MF1, with significantly more genes located at sub-genome LF (red) than their paralogs from sub-genome MF1 (green) under different rules to determine the status of dominant expression. c Similar to b, the number of dominantly expressed paralogs between sub-genomes LF and MF2, with significantly more genes located at sub-genome LF (red) than their paralogs from sub-genome MF2 (blue). d The number of dominantly expressed paralogs between sub-genomes MF1 and MF2; no significant differences were found. e The difference in average TE density in the vicinity regions of paralogous genes from the three sub-genomes of white lupin. f Sub-genomes LF and MF1 with the gene dominantly (d) expressed in LF (dLF). g Sub-genomes LF and MF2 with the gene dominantly expressed in LF. Source data are provided as a Source Data file.

Fig. 4. Expression profiles of the differentially expressed P-use efficiency genes of white lupin under P-sufficient or P-deficient conditions.

PUE, P-use efficiency; +P, P-sufficient condition; −P, P-deficient condition. Roots from the P-deficient condition were further dissected into normal roots (NRs) and four parts of cluster roots based on the developmental stages, including pre-emergent zone (PE, 2–3 cm behind the root tip of first-order laterals), young cluster roots (YCRs), mature cluster roots (MCRs), and old cluster roots (OCRs). Nine clusters were identified by Mfuzz clustering analysis. Functional categorization of the clusters containing genes with the higher expression in leaves, PE, YCRs, and MCRs under P deficiency is shown on the left. Several key homologs of the A. thaliana PUE genes are given on the right. SQD, sulfoquinovosyltransferase; GDPD, glycerophosphodiester phosphodiesterase; MGD, monogalactosyl diacylglycerol synthase; ABCG36, ATP-binding cassette G36; LBD, lateral organ boundaries domain; PLT, plethora; ACO, aconitase; MMDH, mitochondrial malate dehydrogenase; CSY, citrate synthase; FUM, fumarase; PHT, phosphate transporter; PAP, purple acid phosphatase.

Fig. 5. Roles of auxin modulation in cluster root formation of white lupin.

a Quantification of IAA contents (ng per g of fresh weight, ng g⁻¹ FW) in different types of white lupin roots. n = 3 plants. Effects of auxin polar transport inhibitors (b) and EDTA (c) on the formation of cluster roots in white lupin under P-sufficient (+P) or P-deficient (-P) conditions. n = 4 plants for (b) and n = 3 plants for (c). Error bars indicate s.e.m. P value was calculated using the unpaired two-sided Student’s t test. CHPAA, auxin influx inhibitor 3-chloro-4-hydroxyphenylacetic acid; NPA, auxin efflux inhibitor 1-naphtuylphthalamic acid; EDTA, metal chelator ethylenediaminetetraacetic acid. d Neighbor-joining phylogenetic tree of ABCG36 and ABCG37 genes from A. thaliana, P. vulgaris, and L. albus. e Expression profiles of LaABCG36a–d and LaABCG37a–c in roots under P-sufficient (+P) condition and normal roots (NRs) or different developmental stages of cluster roots under P deficiency (−P). PE, pre-emergent zone, 2–3 cm behind the root tip of first-order laterals; YCR, young cluster root; MCR, mature cluster root; OCR, old cluster root. The source data underlying Fig. 5a–c are provided as a Source Data file.