Functional modulation of an aquaporin to intensify photosynthesis and abrogate bacterial virulence in rice

Plant aquaporins are recently noted biological resource with a great potential to improve crop growth and defense traits. Here, we report functional modulation of Oryza sativa aquaporin OsPIP1;3 to enhance rice photosynthesis and grain production and to control bacterial blight and leaf streak, the most devastating world-wide bacterial diseases in the crop. We characterize OsPIP1;3 as a physiologically relevant CO2 -transporting facilitator, which supports 30% of rice photosynthesis on average. This role is nullified by OsPIP1;3 interaction with the bacterial protein Hpa1, an essential component of the type-III translocon that supports translocation of the bacterial type-III effectors PthXo1 and TALi into rice cells to induce leaf blight and streak, respectively. Hpa1 binding shifts OsPIP1;3 from CO2 transport to the effector translocation, aggravates bacterial virulence, but sacrifices rice photosynthesis. On the contrary, the external application of isolated Hpa1 to rice plants effectively prevents OsPIP1;3 from interaction with Hpa1 secreted by the bacteria that are infecting the plants. The inhibition of OsPIP1;3-Hpa1 interaction reverts OsPIP1;3 from the effector translocation to CO2 transport, abrogates bacterial virulence, and meanwhile induces defense responses in rice. These beneficial effects can combine to confer photosynthesis enhancement by 29-30%, bacterial disease reductions by 58-75%, and grain yield increase between 11% and 34%, in different rice varieties investigated in small-scale field trails implemented during the past years. Our results suggest that crop productivity and immunity can be coordinated by modulating physiological and pathological functions of a single aquaporin to break the growth-defense tradeoff barrier.