A vacuolar H-pyrophosphatase differential activation and energy coupling integrate the responses of weeds and crops to drought stress

Background

Cyperus rotundus L. is a C4 weed of large vegetative and reproductive vigor endowed with competitive advantages over most crop species mainly under adverse environmental conditions. Vacuole functions are critical for the mechanisms of drought resistance, and here the modulation of the primary system of vacuolar ion transport is investigated during a transient water stress imposed to this weed and to C4 crop species (Zea mays L.).

Methods

The vacuolar H⁺ pumps, the H⁺-ATPase and H⁺-PP_iase, expression, activities and the energy coupling were spectrophotometrically investigated as key elements in the differential drought-resistance mechanisms developed by weeds and crops.

Results

In C. rotundus tonoplasts, ATP hydrolysis was more sensitive to drought than its coupled H⁺ transport, which was in turn at least 3-folds faster than that mediated by the H⁺-PP_iase. Its PP_i hydrolysis was only slightly affected by severe water deficit, contrasting with the disruption induced in the PP_i-dependent H⁺-gradient. This effect was antagonized by plant rehydration as the H⁺-PP_iase activity was highly stimulated, reassuming a coupled PP_i-driven H⁺ pumping. Maize tonoplasts exhibited 2–4 times lower hydrolytic activities than that of C. rotundus, but were able to overactivate specifically PP_i-dependent H⁺ pumping in response to stress relief, resulting in an enhanced H⁺-pumps coupling efficiency.

Conclusion

These results together with immunoanalysis revealed profiles consistent with pre- and post-translational changes occurring on the tonoplast H⁺-pumps, which differ between weeds and crops upon water deficit.

General significance

The evidences highlight an unusual modulation of the H⁺-PP_iase energy coupling as a key biochemical change related to environmental stresses adaptive capacity of plants.