Multi-omics analysis reveals spatiotemporal regulation and function of heteromorphic leaves in Populus.

Despite the high economic and ecological importance of forests, our knowledge of the adaptive evolution of leaf traits remains very limited. Euphrates poplar (Populus euphratica), which has high tolerance to arid environment, has evolved four heteromorphic leaf forms, including narrow (linear and lanceolate) and broad (ovate and broad-ovate) leaves on different crowns. Here, we revealed the significant functional divergence of four P. euphratica heteromorphic leaves at physiological and cytological levels. Through global analysis of transcriptome and DNA methylation across tree and leaf developmental stages, we revealed that gene expression and DNA epigenetics differentially regulated key processes involving development and functional adaptation of heteromorphic leaves, such as hormone signaling pathways, cell division, and photosynthesis. Combined analysis of gene expression, methylation, ATAC-seq, and Hi-C-seq revealed longer interaction of 3D genome, hypomethylation, and open chromatin state upregulates IAA-related genes (such as PIN-FORMED1 and ANGUSTIFOLIA3) and promotes the occurrence of broad leaves while narrow leaves were associated with highly concentrated heterochromatin, hypermethylation, and upregulated abscisic acid pathway genes (such as Pyrabactin Resistance1-like10). Therefore, development of P. euphratica heteromorphic leaves along with functional divergence was regulated by differentially expressed genes, DNA methylation, chromatin accessibility, and 3D genome remodeling to adapt to the arid desert. This study advances our understanding of differential regulation on development and functional divergence of heteromorphic leaves in P. euphratica at the multi-omics level and provides a valuable resource for investigating the adaptive evolution of heteromorphic leaves in Populus.

Chromosome-scale assemblies of the male and female Populus euphratica genomes reveal the molecular basis of sex determination and sexual dimorphism.

Reference-quality genomes of both sexes are essential for studying sex determination and sex-chromosome evolution, as their gene contents and expression profiles differ. Here, we present independent chromosome-level genome assemblies for the female (XX) and male (XY) genomes of desert poplar (Populus euphratica), resolving a 22.7-Mb X and 24.8-Mb Y chromosome. We also identified a relatively complete 761-kb sex-linked region (SLR) in the peritelomeric region on chromosome 14 (Y). Within the SLR, recombination around the partial repeats for the feminizing factor ARR17 (ARABIDOPSIS RESPONSE REGULATOR 17) was potentially suppressed by flanking palindromic arms and the dense accumulation of retrotransposons. The inverted small segments S1 and S2 of ARR17 exhibited relaxed selective pressure and triggered sex determination by generating 24-nt small interfering RNAs that induce male-specific hyper-methylation at the promoter of the autosomal targeted ARR17. We also detected two male-specific fusion genes encoding proteins with NB-ARC domains at the breakpoint region of an inversion in the SLR that may be responsible for the observed sexual dimorphism in immune responses. Our results show that the SLR appears to follow proposed evolutionary dynamics for sex chromosomes and advance our understanding of sex determination and the evolution of sex chromosomes in Populus.

Complete chloroplast genome sequence of Populus euphratica from PacBio Sequel platform.

Populus euphratica Oliv., one of tall arbors growing in desert areas, has great stress resistance. The complete chloroplast genome was reported in this study using the PacBio Sequel Platform. The chloroplast genome with a total size of 157,881 bp consisted of two inverted repeats (IRs) (27,666 bp) separated by a large single-copy region (85,906 bp) and a small single-copy region (16,643 bp). Further annotation revealed the chloroplast genome contains 111 genes, including 77 protein-coding genes, 30 tRNA genes, and four rRNA genes. The information of the chloroplast genome will be useful for study on the evolution of P. euphratica in the future.

Complete chloroplast genome sequence of Populus pruinosa Schrenk from PacBio Sequel II Platform.

Populus pruinosa Schrenk plays an important role on ecological services in desert areas. The complete chloroplast genome was reported in this study using the PacBio Sequel II Platform. The chloroplast genome with a total size of 157,856 bp consists of two inverted repeats (IR, 27,673 bp) separated by a large single-copy region (LSC, 85,867 bp) and a small single-copy region (SSC, 16,645 bp). Further annotation revealed the chloroplast genome contains 111 genes, including 78 protein-coding genes, 29 tRNA genes, and 4 rRNA genes. A total of 151 simple sequence repeats (SSRs) were identified in the chloroplast genome. This information will be useful for study on the evolution and genetic diversity of P. pruinosa in the future.