Apoplastic pH determines the hypocotyl response to auxin dosage and light

Abstract

Abstract The phytohormone auxin and light both regulate plant elongation growth. Light suppresses hypocotyl elongation, whereas auxin promotes it. However, auxin can reverse its effect and inhibit elongation when applied to etiolated seedlings or in high dosages. How dosages or light conditions change the effect of auxin on hypocotyl growth has long been mysterious. We found that, regardless of the dosage, more auxin induces more transcription of SAURs (Small Auxin-Up RNAs), leading to a stronger activation of plasma membrane proton pump H+-ATPases (AHAs), and consequently, progressive acidification of the apoplast in hypocotyls. Apoplastic acidification promotes growth, but when the pH drops below a threshold, further acidification inhibits elongation. The short hypocotyl phenotype caused by auxin overdosage can be alleviated by inactivating the AHA activity. Light irradiation downregulates SAUR levels and decreases AHA activity in the hypocotyl. Light-grown hypocotyls exhibit a higher apoplastic pH, which impedes cell elongation and counteracts auxin induced over-acidification. Our findings indicate that the biphasic effect of auxin results from the biphasic response of cell elongation to decreasing apoplastic pH. Auxin and light antagonistically regulate the SAUR-PP2C.D-AHA pathway, eventually achieving the apoplastic pH appropriate for the hypocotyl growth of the given environment.