Heterosis of overcoming the trade-off between growth and drought tolerance in hybrid poplar leaves: the role of synergistically transgressive expression of critical genes

Plant drought tolerance frequently results in growth limitations, which has been known as the trade-off between drought tolerance and growth. Heterosis, the phenotypic superiority of hybrids over their parents in many traits, has yet to be applied to overcoming the trade-off between drought tolerance and growth. Here, we demonstrated that the transgressive expression of expansin proteins (PagEXPs) participated in the vigorous cell expansion and leaf enlargement in hybrid, and this process is correlated with the modulation of auxin transporter (PagPIN8), which is also transgressively upregulated in hybrid leaf. Meanwhile, the transgressive expression of PagP5CS1 in hybrid resulted in higher free proline level in hybrid leaf than both parents and contributed to heterosis in drought tolerance. A new transcription factor PagWRKY45 that regulates the transgressive expression of PagP5CS1 in hybrid leaf was identified and characterized by yeast-one-hybrid screen, which directly regulated the expression of PagP5CS1 by binding the W-box motif in promoter of PagP5CS1. These hub genes work in concert to contributes heterosis of drought tolerance in hybrid leaf. The gene-stacking effect resulting from the co-expression of key genes in growth and tolerance pathways enabling the hybrid poplar to overcomes the trade-off between drought tolerance and growth. An integrative model that synergistically overcomes the classic trade-off between growth and drought tolerance in hybrid poplar was proposed. This model provides a guideline for improving capacity of overcoming the trade-off between drought tolerance and growth via cross breeding and molecular breeding.