Plant tissue succulence engineering improves water-use efficiency, water-deficit stress attenuation and salinity tolerance in Arabidopsis

Tissue succulence (ratio of tissue water/leaf area or dry mass) or the ability to store water within living tissues is among the most successful adaptations to drought in the plant kingdom. This taxonomically widespread adaptation helps plants avoid the damaging effects of drought, and is often associated with the occupancy of epiphytic, epilithic, semi-arid and arid environments. Tissue succulence was engineered in Arabidopsis thaliana by overexpression of a codon-optimized helix-loop-helix transcription factor (VvCEB1(opt)) from wine grape involved in the cell expansion phase of berry development. VvCEB1(opt)-overexpressing lines displayed significant increases in cell size, succulence and decreased intercellular air space. VvCEB1(opt)-overexpressing lines showed increased instantaneous and integrated water-use efficiency (WUE) due to reduced stomatal conductance caused by reduced stomatal aperture and density resulting in increased attenuation of water-deficit stress. VvCEB1(opt)-overexpressing lines also showed increased salinity tolerance due to reduced salinity uptake and dilution of internal Na+ and Cl- as well as other ions. Alterations in transporter activities were further suggested by media and apoplastic acidification, hygromycin B tolerance and changes in relative transcript abundance patterns of various transporters with known functions in salinity tolerance. Engineered tissue succulence might provide an effective strategy for improving WUE, drought avoidance or attenuation, salinity tolerance, and for crassulacean acid metabolism biodesign.