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 ((Populus alba×(P. alba × P. glandulosa)) and its female parent I-101 (Populus alba) and male parent 84 K (P. alba × P. glandulosa) were employed in a hydroponic experiment and a field trial. Better-parent heterosis of leaf biomass, leaf area, free proline, catalase activity, salicylic acid 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 and Cd bioconcentration factor in leaves, were dominant in 84 K. In contrast, traits related to stress tolerance were dominant in I-101. Weighted gene co-expression network analysis revealed that hub genes responsible for Cd translocation and bioconcentration were dominantly expressed in 84 K, resulting in superior leaf Cd concentration in males compared with 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.