Two Aquaporins Mitigate Growth-Defence Trade-Offs by Facilitating CO2 and H2O2 Transport in Wheat

Abstract

The growth-defence trade-offs pose a major challenge to breeding high-yield and disease-resistant crops. Aquaporins are membrane channels that facilitate the transport of water and other small compounds, therefore regulating the growth-defence trade-offs. However, the molecular mechanism that governs the function of aquaporins in the trade-offs remains unclear. Here, we report that Triticum aestivum TaPIP1;6 and TaPIP2;10, aquaporins of the plasma membrane intrinsic protein (PIP) family, function as dual substrate channels that concurrently enhance plant growth and resistance to powdery mildew and English grain aphid. In wheat plants growing under normal conditions, TaPIP1;6 and TaPIP2;10 facilitate CO₂ transport from the atmosphere into wheat cells and promote photosynthesis, which leads to growth enhancement and grain yield increase. In wheat plants under attack by powdery mildew pathogen or English grain aphid, TaPIP1;6 and TaPIP2;10 function as concurrent H₂O₂ transport channels, mediating the influx of apoplastic H₂O₂ into the cytoplasm. In turn, the transported H₂O₂ activates innate immunity, including the MAPK cascade, callose deposition and defence gene expression, and thereby enhances wheat resistance to powdery mildew and the English grain aphid. In essence, co-overexpression of TaPIP1;6 and TaPIP2;10 exhibits synergistic effects on CO₂ and H₂O₂ transports, further amplifying both yield and resistance traits. Taken together, our results suggest that TaPIP1;6 and TaPIP2;10 function as dual-substrate transporting channels to promote growth by regulating CO₂ transport and to enhance resistance against pathogens and insects via H₂O₂-mediated immune responses. This finding provides crucial genetic targets for breeding crop varieties combining high yield with resistance traits.