Polyamines in chemiosmosis in vivo: A cunning mechanism for the regulation of ATP synthesis during growth and stress

Abstract

Polyamines (PAs) are low molecular weight amines that occur in every living organism. The three main PAs (putrescine, spermidine, and spermine) are involved in several important biochemical processes covered in recent reviews. As rule of thumb, increase of the cellular titer of PAs in plants is related to cell growth and cell tolerance to abiotic and biotic stress. In the present contribution, we describe recent findings from plant bioenergetics that bring to light a previously unrecognized dynamic behavior of the PA pool. Traditionally, PAs are described by many authors as organic polycations, when in fact they are bases that can be found in a charged or uncharged form. Although uncharged forms represent less than 0.1% of the total pool, we propose that their physiological role could be crucial in chemiosmosis. This process describes the formation of a PA gradient across membranes within seconds and is difficult to be tested in vivo in plants due to the relatively small molecular weight of PAs and the speed of the process. We tested the hypothesis that PAs act as permeable buffers in intact leaves by using recent advances in vivo probing. We found that an increase of PAs increases the electric component (Δψ) and decreases the ΔpH component of the proton motive force. These findings reveal an important modulation of the energy production process and photoprotection of the chloroplast by PAs. We explain in detail the theory behind PA pumping and ion trapping in acidic compartments (such as the lumen in chloroplasts) and how this regulatory process could improve either the photochemical efficiency of the photosynthetic apparatus and increase the synthesis of ATP or fine tune antenna regulation and make the plant more tolerant to stress.

Keywords: ATP synthesis; chloroplast; photosynthesis; polyamines; proton motive force; putrescine; stress.

FIGURE 1

(A) Chemiosmosis in all cells powers ATP synthesis by forming a proton motive force. Important for the establishment of pmf is a membrane the so-called coupling membrane. Proton producers are usually enzymes of the respiratory chain or photosynthetic subcomplexes. Proton consumers are usually proton-driven ATPases. (B) New chemiosmosis. PAs buffer acidic compartment and energize the membrane that houses ATPases. The triangle shows the central point of the PAs role in chemiosmosis. In other words PAs act as intermediates receiving protons from producers and deliver them to consumers.

FIGURE 2

PAs accumulate in the lumen and buffer the lumen pH during photophosphorylation. Photosynthetic reactions produce protons that are vectorially released in the lumen. Lumen acidification shifts equilibrium 1 to the right (production of charged Put in lumen). Depletion of free putrescine urges new free Put to diffuse from stroma into lumen (Le Chatelier principle equilibrium 2). Finally, free Put in stroma is replaced by charged Put in stroma which is ionized (equilibrium 3). The net result of this process (i.e., new poise of the 3 equilibria) is ion trapping. That is the accumulation of Put in lumen up to 100 times. The final concentration of Put depends mainly on ΔpH and counterion concentration (such as Cl^-).

FIGURE 3

The dual behavior of the Put pool during dark and light. (A) Equal distribution of protons leads to equal distribution of PAs (for example during the dark). (B) Establishment of a ΔpH between the two compartments leads to unequal distribution of PAs. Note in b that for ΔpH = 1 ten times more Put will accumulate in the acidic compartment.

FIGURE 4

A simplified scheme showing the effect of PAs on ATP production by thylakoids. Low doses of PAs stimulate photophosphorylation (α phase). Higher doses lead to reduction of ATP synthesis (γ phase). The x axis is qualitative because in all three PAs (Put, Spd, and Spm) the peak value corresponds to different concentration although the shape of the curve is similar.