The possible role of redox-associated protons in growth of plant cells

Abstract

The protons excreted by plant cells may arise by two different mechanisms: (1) by the action of the plasma membrane H(+)-ATPase and (2) by plasma membrane redox reactions. The exact proportion from each source is not known, but the plasma membrane H(+)-ATPase is, by far, the major contributor to proton efflux. There is still some questions of whether the redox-associated protons produced by NADH oxidation on the inner side of the plasma membrane traverse the membrane in a 1:1 relationship with electrons generated in the redox reactions. Membrane depolarization observed in the presence of ferricyanide reduction by plasma membranes of whole cells or tissues or the lag period between ferricyanide reduction and medium acidification argue that only scalar protons may be involved. The other major argument against tight coupling between protons and electrons involves the concept of strong charge compensation. When ferricyanide is reduced to ferrocyanide on the outside of cells or tissues, an extra negative charge arises, which is compensated for by the release of H+ or K+, so that the total ratio of increased H+ plus K+ equals the electrons transferred by transmembrane electron transport. These are strong arguments against a tight coupling between electrons and protons excreted by the plasma membrane. On the other hand, there is no question that inhibitor studies provide evidence for two mechanisms of proton generation by plasma membranes. When the H(+)-ATPase activity is totally inhibited, the addition of ferricyanide induces a burst of extra proton excretion, or vice versa, when plasma membrane redox reactions are inhibited, the H(+)-ATPase can function normally. Since plasma membrane redox reactions and associated H+ excretion are related to growth it is possible that in plants the ATPase-generated protons have a different function from redox-associated protons. The H(+)-ATPase-generated protons have been considered for many years to be necessary for cell wall expansion, allowing elongation to take place. A special function of the redox-generated protons may be in initiating proliferative cell growth, based on the presence of a hormone-stimulated NADH oxidase in membranes of soybean hypocotyls and stimulation of root growth by low concentrations of oxidants. Here we propose that this NADH oxidase and the redox protons released by its action control growth. The mechanism for this may be the evolution of protons into a special membrane domain, from which a signal to initiate cell proliferation may originate, independent of the action of the H(+)-ATPase-generated protons.(ABSTRACT TRUNCATED AT 400 WORDS)