Haplotype-resolved genome of Prunus zhengheensis provides insight into its evolution and low temperature adaptation in apricot

Abstract

Prunus zhengheensis, an extremely rare population of apricots, originated in warm South-East China and is an excellent material for genetic breeding. However, most apricots and two related species (P. sibirica, P. mandshurica) are found in the cold northern regions in China and the mechanism of their distribution is still unclear. In addition, the classification status of P. zhengheensis is controversial. Thus, we generated a high-quality haplotype-resolved genome for P. zhengheensis, exploring key genetic variations in its adaptation and the causes of phylogenetic incongruence. We found extensive phylogenetic discordances between the nuclear and organelle phylogenies of P. zhengheensis, which could be explained by incomplete lineage sorting. A 242.22-Mb pan-genome of the Armeniaca section was developed with 13 chromosomal genomes. Importantly, we identified a 566-bp insertion in the promoter of the HSFA1d gene in apricot and showed that the activity of the HSFA1d promoter increased under low temperatures. In addition, HSFA1d overexpression in Arabidopsis thaliana indicated that HSFA1d positively regulated plant growth under chilling. Therefore, we hypothesized that the insertion in the promoter of HSFA1d in apricot improved its low-temperature adaptation, allowing it to thrive in relatively cold locations. The findings help explain the weather adaptability of Armeniaca plants.

Figure 1

Genomic characterization of P. zhengheensis and collinearity analysis of related species. A Genome survey of P. zhengheensis. B Genome-wide Hi-C map showing the interaction frequency distribution of Hi-C links among the chromosomes of P. zhengheensis. C From a to d: GC content, repeats, gene count, and chromosomes; in the circle are gene links. (D) Collinearity analysis of two haplotype genomes of P. zhengheensis (Pzhap1 and Pzhap2), apricotCZH and P. mume.

Figure 2

Geographical distribution, morphological comparison and phylogenetic analysis of P. zhengheensis with P. mume and apricot. A Geographical distribution map of P. zhengheensis, wild apricot, cultivated apricot, P. mandshurica, P. sibirica, wild P. mume and cultivated P. mume. B Morphological characteristics of P. zhengheensis, P. mume and apricot. C Phylogenetic analysis of P. zhengheensis based on 151 single-copy genes. P. armeniaca ‘Jintaiyang’, P. armeniaca ‘Longwangmao’, P. armeniaca ‘Yinxiangbai’, P. armeniaca ‘Chuanzhihong’, P. armeniaca ‘Stella’ and P. armeniaca accession ‘Marouch #14’ are represented by apricotSun, apricotLWM, apricotYXB, apricotCZH, apricotStella and apricotMarouch, respectively. D Phylogenetic analysis of P. zhengheensis based on chloroplast genomes.

Figure 3

Estimated insertion time of full-length LTR retrotransposons in five Armeniaca species. The X axis represents insertion time and the Y axis represents density. Prunus sibirica is represented by PruSib, P. mandshurica by PrunMan and P. mume var. tortuosa by Pmtor.

Figure 4

Pan-genome analysis of the Armeniaca section. A Total chromosome length of 13 Armeniaca genomes. Prunus sibirica is represented by PruSib, P. mandshurica by PrunMan, P. mume var. tortuosa by Pmtor, P. mume by Pm, P. hongpingensis by Ph and P. zhengheensis, published recently, by Pz. B Influence of the number of Armeniaca genomes on the number of pan and core gene families. C Characteristics of each individual genome and the pan-genome. The histogram depicts the number of gene families in various genomes. The percentage of gene families in each category is displayed in the pie chart. Core gene families are found in all genomes. Softcore families are gene families that make up >90% of the genome. Private gene families are present in a single genome. The remaining gene families are assigned to dispensable gene families. D CDS lengths and gene lengths in core, dispensable and private gene families. E Petal map of specific gene families in 13 Armeniaca genomes. F Graph-based pan-genome of 13 Armeniaca genomes. From the inside out: GC content, repeats, gene count, chromosomes.

Figure 5

Structural variation in 13 Armeniaca genomes. A Counts and sequence lengths of seven SV types in 13 Armeniaca genomes. B Deletion SVs of 13 genomes in a Venn diagram. C The promoter of the HSFA1d gene had a 566­ bp insertion that was absent in P. zhengheensis and P. mume. DRE and LTRE are cis-acting elements associated with low temperature and present in SV fragments.

Figure 6

HSFA1d gene function research. A Relative RNA expression level of the HSFA1d gene in apricot and P. zhengheensis after 4 and 25°C treatment for 12 h. BHSFA1d promoted hypocotyl growth under chilling in overexpressing A. thaliana. C Transient expression assay of luminescence intensity showing the transcription activity of promoters of PzHSFA1d and PaHSFA1d (^**** Pvalue < 0.0001).