The apoplastic pH is a key determinant in the hypocotyl growth response to auxin dosage and light

Auxin is a core phytohormone regulating plant elongation growth. While auxin typically promotes hypocotyl elongation, excessive amounts of auxin inhibit elongation. Moreover, auxin usually promotes light-grown, but inhibits dark-grown hypocotyl elongation. How dosage and light condition change the plant’s response to auxin, also known as auxin’s biphasic effect or dual effect, has long been mysterious. Auxin induces cell expansion primarily through apoplastic acidification and the subsequent ‘acid growth’ mechanism. Here we show that this pathway operates for both stimulatory and inhibitory auxin doses and under both dark and light conditions. Regardless of the dosage, more auxin induces more transcripts of SAURs (Small Auxin-Up RNAs), leading to a stronger activation of plasma membrane H+-ATPases (AHAs) and progressive acidification of the apoplast in hypocotyl epidermis. Apoplastic acidification promotes growth but only above a certain pH threshold, below which excessive acidification inhibits elongation. Auxin overdosage-triggered hypocotyl inhibition can be alleviated by suppressing the AHA activity or raising the apoplastic pH. Light-grown hypocotyls exhibit a higher apoplastic pH, which impedes cell elongation and counteracts auxin-induced over-acidification. Auxin and light antagonistically regulate the SAUR-PP2C.D-AHA pathway in the hypocotyl and influence plant elongation growth. Our findings suggest that the biphasic effect of auxin results from the biphasic response of hypocotyl cells to decreasing apoplastic pH. Auxin can promote or inhibit hypocotyl elongation. This biphasic effect has puzzled generations of plant biologists. Wang et al. shows that the decreasing apoplastic pH, stimulated by auxin, underlies the change in hypocotyl growth response.