Genomic Analysis Reveals the Fast-Growing Trait and Improvement Potential for Stress Resistance in the Elite Poplar Variety Populus × euramericana 'Bofeng 3'

Abstract

Enhancing stress tolerance represents a critical objective in the genetic improvement of poplar trees. Populus × euramericana 'Bofeng 3' is a nationally certified elite poplar variety that was approved as a premium pulpwood variety for the southern area of Northeastern China. This variety grows quickly, has good yield, and resists frost; however, its weaker drought and salt tolerance limits its broader use in diverse environments. The aim of this study is to understand the genetic basis of the fast growth and stress-adaptation traits of this variety and to provide support for future molecular breeding efforts. We present a chromosome-scale genome assembly of Populus × euramericana 'Bofeng 3', totaling 445.53 Mb, of which with 90.39% is anchored to 19 chromosomes, containing 33,309 protein-coding genes and 45.36% repetitive elements. Comparative genomics showed that 'Bofeng 3' has expanded gene families related to photosynthesis and metabolism, and contracted families involved in stress responses, distinguishing it from other Populus species. Under drought (9137 leaf, 9403 root differentially expressed genes (DEGs)) and salt stress (2840 leaf, 3807 root DEGs), trend analysis revealed specific expression patterns. Several unique and expanded genes, including those for photosynthetic proteins, peroxidases, gamma-aminobutyric acid metabolism, and disease resistance, showed stress-responsive trends. Weighted gene co-expression network analysis identified five modules (three positive, two negative) that significantly correlated with photosynthetic traits, highlighting key candidates such as bZIP transcription factors and auxin/indole acetic acid genes. This study determined the genetic basis underlying the rapid growth traits of Populus × euramericana 'Bofeng 3', while providing genomic resources to establish a robust foundation for future gene editing and molecular breeding studies, including critical candidate genetic resources for developing superior drought- and salt-tolerant poplar varieties via targeted genome editing technologies.

Keywords: Populus × euramericana ‘Bofeng 3’; comparative genomics; drought tolerances; genome; salt resistance; transcriptome.

Figure 1

Overview of the Populus × euramericana ‘Bofeng 3’ genome. (a) Morphology of P. × euramericana ‘Bofeng 3’. (b) Hi-C heatmap of P. × euramericana ‘Bofeng 3’ chromosome interactions.

Figure 2

Characterization and synteny of the P. × euramericana ‘Bofeng 3’ genome. (a) The density of Ogre, a family of Gypsy LTR-RTs, (b) the density of all Gypsy LTR-RTs, (c) the density of all Copia LTR-RTs, (d) gene density, and (e) histogram of the GC content. The colored lines connect homologous regions.

Figure 3

(a) The Venn diagram represents the shared and unique gene families. The poplars shown in the picture include P. × euramericana ‘Bofeng 3’, P. nigra, P. deltoides, P. euphratica, P. simonii, and P. pruinosa, and the outgroup specie N. tangutorum. (b) Phylogenetic relationship. Expansion/ contraction of gene families and estimation of divergence time. Blue numbers indicate the divergence time on the nodes, with the confidence range in parentheses. (c) The distribution of 4DTV. (d) The distribution of Ks.

Figure 4

Syntenic plots between P. × euramericana ‘Bofeng 3’ and other examined species. Syntenic blocks are marked using gray lines.

Figure 5

(a–d) Changes in photosynthetic parameters of potted seedlings under drought/salt stress. L_CK, L_320g, and L_re_320g are the leaves of the control group, those dried for 2 weeks, and those rehydrated for 24 h, respectively; L_50M and L_100M are the leaves of plants treated with 50 mmol·L⁻¹ and 100 mmol·L⁻¹ salt for 2 weeks, respectively. (e) Module–trait association analysis. The heatmap displays Pearson correlation coefficients between module eigengenes and external traits, with statistical significance denoted as follows: * p < 0.05 (significant), ** p < 0.01 (highly significant), and for 0.05 ≤ p < 0.1 (marginally significant).