A critical review on natural compounds interacting with the plant plasma membrane H+ -ATPase and their potential as biologicals in agriculture.

The plant plasma membrane (PM) H+ -ATPase is an essential enzyme controlling plant growth and development. It is an important factor in response to abiotic and biotic stresses and is subject to tight regulation. We are in demand for new sustainable natural growth regulators and as a key enzyme for regulation of transport into the plant cell the PM H+ -ATPase is a potential target for these. In this review, we have evaluated the known non-protein natural compounds with regulatory effects on the PM H+ -ATPase, focusing on their mechanism of action and their potential as biologicals/growth regulators in plant production of future sustainable agriculture.

Tenuazonic acid from Stemphylium loti inhibits the plant plasma membrane H+ -ATPase by a mechanism involving the C-terminal regulatory domain.

Pathogenic fungi often target the plant plasma membrane (PM) H+ -ATPase during infection. To identify pathogenic compounds targeting plant H+ -ATPases, we screened extracts from 10 Stemphylium species for their effect on H+ -ATPase activity. We identified Stemphylium loti extracts as potential H+ -ATPase inhibitors, and through chemical separation and analysis, tenuazonic acid (TeA) as a potent H+ -ATPase inhibitor. By assaying ATP hydrolysis and H+ pumping, we confirmed TeA as a H+ -ATPase inhibitor both in vitro and in vivo. To visualize in planta inhibition of the H+ -ATPase, we treated pH-sensing Arabidopsis thaliana seedlings with TeA and quantified apoplastic alkalization. TeA affected both ATPase hydrolysis and H+ pumping, supporting a direct effect on the H+ -ATPase. We demonstrated apoplastic alkalization of A. thaliana seedlings after short-term TeA treatment, indicating that TeA effectively inhibits plant PM H+ -ATPase in planta. TeA-induced inhibition was highly dependent on the regulatory C-terminal domain of the plant H+ -ATPase. Stemphylium loti is a phytopathogenic fungus. Inhibiting the plant PM H+ -ATPase results in membrane potential depolarization and eventually necrosis. The corresponding fungal H+ -ATPase, PMA1, is less affected by TeA when comparing native preparations. Fungi are thus able to target an essential plant enzyme without causing self-toxicity.