The chromosome-scale genome and population genomics reveal the adaptative evolution of Populus pruinosa to desertification environment.

The Populus pruinosa is a relic plant that has managed to survive in extremely harsh desert environments. Owing to intensifying global warming and desertification, research into ecological adaptation and speciation of P. pruinosa has attracted considerable interest, but the lack of a chromosome-scale genome has limited adaptive evolution research. Here, a 521.09 Mb chromosome-level reference genome of P. pruinosa was reported. Genome evolution and comparative genomic analysis revealed that tandemly duplicated genes and expanded gene families in P. pruinosa contributed to adaptability to extreme desert environments (especially high salinity and drought). The long terminal repeat retrotransposons (LTR-RTs) inserted genes in the gene body region might drive the adaptive evolution of P. pruinosa and species differentiation in saline-alkali desert environments. We recovered genetic differentiation in the populations of the northern Tianshan Mountain and southern Tianshan Mountain through whole-genome resequencing of 156 P. pruinosa individuals from 25 populations in China. Further analyses revealed that precipitation drove the local adaptation of P. pruinosa populations via some genetic sites, such as MAG2-interacting protein 2 (MIP2) and SET domain protein 25 (SDG25). This study will provide broad implications for adaptative evolution and population studies by integrating internal genetic and external environmental factors in P. pruinosa.

Differences in the Functional Traits of Populus pruinosa Leaves in Different Developmental Stages.

Populus pruinosa Schrenk has the biological characteristics of heteromorphic leaves and is a pioneer species for wind prevention and sand fixation. The functions of heteromorphic leaves at different developmental stages and canopy heights of P. pruinosa are unclear. To clarify how developmental stages and canopy height affect the functional characteristics of leaves, this study evaluated the morphological anatomical structures and the physiological indicators of leaves at 2, 4, 6, 8, 10, and 12 m. The relationships of functional traits to the developmental stages and canopy heights of leaves were also analyzed. The results showed that blade length (BL), blade width (BW), leaf area (LA), leaf dry weight (LDW), leaf thickness (LT), palisade tissue thickness (PT), net photosynthetic rate (Pn), stomatal conductance (Gs), proline (Pro), and malondialdehyde (MDA) content increased with progressing developmental stages. BL, BW, LA, leaf dry weight, LT, PT, Pn, Gs, Pro, and the contents of MDA, indoleacetic acid, and zeatin riboside had significant positive correlations with canopy heights of leaves and their developmental stages. The morphological structures and physiological characteristics of P. pruinosa leaves showed more evident xeric structural characteristics and higher photosynthetic capacity with increasing canopy height and progressive developmental stages. Resource utilization efficiency and the defense ability against environmental stresses were improved through mutual regulation of each functional trait.

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.

Structural and Functional Responses of the Heteromorphic Leaves of Different Tree Heights on Populus euphratica Oliv. to Different Soil Moisture Conditions.

Populus euphratica Oliv., a pioneer species of desert riparian forest, is characterized heterophylly. To understand the adaptation strategies of the heteromorphic leaves of P. euphratica to soil drought, we assessed the structural and functional characteristics of the heteromorphic leaves at different heights in suitable soil moisture conditions (groundwater depth 1.5 m) and drought conditions (groundwater depth 5 m), which include morphology, anatomical structure, photosynthetic capacity, water use efficiency, osmotic adjustment capacity, and endogenous hormones. These results indicate that leaf area, leaf thickness, fence tissue, palisade-to-sea ratio, main vein xylem area, vessel area, net photosynthetic rate, transpiration rate, and proline, MDA, IAA, GA3, and ZR contents showed a positive correlation with the tree height under the two soil moisture conditions, but leaf shape index, leaf water potential (LWP), and ABA content showed a decreasing trend. In addition, the main vein vascular bundle area, main vein xylem area, and contents of malondialdehyde, ABA, GA3, and IAA were significantly greater under soil drought conditions than normal soil water content. Under soil drought stress, the heteromorphic leaves of P. euphratica showed more investment in anatomical structure and greater water use efficiency, proline, and hormone contents, and synergistic changes to maintain high photosynthetic efficiency. This is an adaptation strategy to water stress caused by soil drought and tree height changes.

Phylogeography Reveals Geographic and Environmental Factors Driving Genetic Differentiation of Populus sect. Turanga in Northwest China.

Populus sect. Turanga (hereafter referred to as "Populus"), including Populus euphratica and Populus pruinosa, are the predominant tree species in desert riparian forests in northwestern China. These trees play key roles in maintaining ecosystem balance, curbing desertification, and protecting biodiversity. However, the distribution area of Populus forests has been severely diminished and degraded in recent years due to increased habitat destruction and human activity. Understanding the genetic diversity among Populus individuals and populations is essential for designing conservation strategies, but comprehensive studies of their genetic diversity in northwest China are lacking. Here, we assessed the population structures and genetic diversity of 1,620 samples from 85 natural populations of Populus (59 P. euphratica and 26 P. pruinosa populations) covering all of northwestern China using 120 single nucleotide polymorphism (SNP) markers. Analysis of population structure revealed significant differentiation between these two sister species and indicated that strong geographical distribution patterns, a geographical barrier, and environmental heterogeneity shaped the extant genetic patterns of Populus. Both P. euphratica and P. pruinosa populations in southern Xinjiang had higher genetic diversity than populations in other clades, perhaps contributing to local geographic structure and strong gene flow. Analysis of molecular variance (AMOVA) identified 15% variance among and 85% variance within subpopulations. Mantel tests suggested that the genetic variation among P. euphratica and P. pruinosa populations could be explained by both geographical and environmental distance. The genetic diversity of P. euphratica showed a significant negative correlation with latitude and longitude and a positive correlation with various environmental factors, such as precipitation of warmest quarter and driest month, temperature seasonality, and annual mean temperature. These findings provide insights into how the genetic differentiation of endangered Populus species was driven by geographical and environmental factors, which should be helpful for designing strategies to protect these genetic resources in the future.

Complete chloroplast genome sequence of Peganum harmala (Zygophyllaceae).

Peganum harmala L. is a perennial herbaceous plant belonging to the family of Zygophyllaceae, and is grows in semi-arid climates, such as Xinjiang, Gansu, Ningxia, Qinghai, and Inner Mongolia in China, and also Middle East and North Africa. This species is of high medicinal value. The complete chloroplast genome was reported in this study. The chloroplast genome with a total size of 159,957 bp consists of two inverted repeats (IR, 26,550 bp) separated by a large single-copy region (LSC, 88,098 bp) and a small single-copy region (SSC, 18,759 bp). Further annotation revealed the chloroplast genome contains 113 genes, including 79 protein-coding genes, 30 tRNA genes, and four rRNA genes. A total of 90 simple sequence repeats (SSRs) were identified in the chloroplast genome. This information will be useful for study on the evolution and genetic diversity of Peganum harmala in the future.

Complete chloroplast genome sequence of Thermopsis turkestanica Gand. (Leguminosae).

Thermopsis turkestanica Gand. is a perennial herbaceous plant belonging to the genus Thermopsis, Leguminosae, and is mainly distributed in dry areas. Most of the species in this genus have high medicinal value. The complete chloroplast genome was reported in this study. The chloroplast genome with a total size of 149,551 bp consists of two inverted repeats (IRs, 24,159 bp) separated by a large single-copy region (LSC, 83,692 bp) and a small single-copy region (SSC, 17,541 bp). Further annotation revealed the chloroplast genome contains 110 genes, including 77 protein coding genes, 29 tRNA genes, and four rRNA genes. This information will be useful for study on the evolution and genetic diversity of Thermopsis turkestanica in the future.

Complete chloroplast genome sequence of Sphaerophysa salsula (Leguminosae).

Sphaerophysa salsula (Pall.) DC. is a perennial herbaceous plant belonging to the genus Sphaerophysa, Galegeae, Leguminosae, and is mainly distributed in dry areas in Central Asia and Northwest China. The complete chloroplast genome with a total size of 123,300 bp was reported in this study. Further annotation revealed the chloroplast genome contains 109 genes, including 76 protein coding genes, 29 tRNA genes, and four rRNA genes. A total of 107 simple sequence repeats (SSRs) from mononucleotide to hexa-nucleotide repeat motif were identified in the chloroplast genome. This information will be useful for study on the evolution and genetic diversity of Sphaerophysa salsula 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.