The physiology of the auxin-induced 10,000-fold increase in light sensitivity of a phytochrome-mediated growth response (Shinkle and Briggs, 1984 Proc Natl Acad Sci USA 81: 3742-3746) has been characterized in subapical coleoptile sections from dark-grown oat (Avena sativa L. cv Lodi) seedlings. Six micromolar indole-3-acetic acid (IAA) must be present for 1 hour before to 2 hour after irradiation in order to confer maximal sensitivity to light. The direct effect of IAA on growth can be separated from its effect on light sensitivity. Several classes of synthetic auxins will substitute for IAA in inducing an increase in sensitivity to light, as will both the phytotoxin fusicoccin and treatment of sections with pH 4.5 buffer. The increase in sensitivity to light induced by 6 micromolar IAA is completely inhibited by buffering the sections at pH 5.9 with 30 millimolar 2-(N-morpholino)ethanesulfonic acid. These findings suggest that the capacity to respond to very low fluences of light is regulated by extracellular pH.Between 10 and 15 millimolar K(+) will inhibit the induction of the increased sensitivity to light, independent of the mechanism of induction. The effect of K(+) appears to be specific to the process by which the sections respond to very low levels of light.