Expression complementation between fundamental biological pathways in Populus hybrid contributes to heterosis in cadmium (Cd) accumulation and tolerance.

To reveal the pattern of heterosis in cadmium (Cd) bio-accumulation of poplar and whether the heterosis can promote the phytoremediation efficiency of Cd-polluted soil, the poplar hybrid variety QB-5 (I-101 × 84K) and its female parent I-101 (Populus alba) and male parent 84K (P. alba × P. glandulosa) were employed in a hydroponic experiment and a field trial. BPHs of leaf biomass, leaf area, free proline, CAT, SA and Cd bio-accumulation reached 100.30%, 97.23%, 57.96% 176.41%, 102.94% and 164.17%, respectively, under Cd exposure. A more in-depth analysis unveiled that most traits related to Cd bio-concentration, including root parameters, Cd translocation factor (TF), and Cd bioconcentration factor (BCF) in leaves, were dominant in 84K. In contrast, traits related to stress tolerance were dominant in I-101. Weighted gene co-expression network analysis (WGCNA) revealed that hub genes responsible for Cd translocation and bioconcentration were dominantly expressed in 84K, resulting in superior leaf Cd concentration in males compared to females. Conversely, most genes responsible for stress tolerance were highly expressed in I-101. The hybrid exhibited a high-parent complementation pattern for critical traits and relevant hub genes, contributing to better-parent heterosis for these traits. Overexpression of PagP5CS1, a gene showing above-high-parent expression in hybrid, increased Cd tolerance and Cd bio-accumulation in poplar, providing molecular evidence for the dominance hypothesis of heterosis. The efficiency of phytoremediation for Cd-contaminated soil can be largely promoted by exploring and utilizing heterosis in Cd tolerance and Cd bio-accumulation.