Rapid Auxin-Induced Cell Expansion and Gene Expression: A Four-Decade-Old Question Revisited

Abstract

The classical effect of the plant hormone auxin is very rapid stimulation of cell expansion followed by sustained growth over a longer time period. However, auxins are also important in other responses, such as cell division and differentiation. Recently, the TRANSPORT INHIBITOR RESPONSE1/AUXIN-BINDING F-BOX PROTEIN (TIR1/AFB) family of auxin receptors regulating the expression of auxin-induced genes has garnered much attention regarding the precise role that TIR1/AFBs serve in auxin responses. Here, we show that major changes in gene expression mediated by these important receptors do not play the major role in triggering the very rapid phase of cell elongation. Fifty years after Charles and Francis Darwin predicted its existence, the plant hormone auxin was discovered in the 1930s to be a key molecule regulating rapid plant cell expansion (5–10 min). Soon thereafter, synthetic auxins such as 2,4-dichlorophenoxyacetic acid (2,4-D) were discovered, and these became economically important growth regulators for agriculture. It was learned that auxin also affects plant development such as organ formation. A remarkable feature about the mode of action of auxin is that it induces changes in global gene expression within 5 to 15 min of application (Abel et al., 1994); this remains one of the fastest regulations of gene transcription known. Changes in protein level are detectable around 15 to 30 min after auxin application (Oeller and Theologis, 1995). By the 1960s, the central question in the auxin field was whether the rapid auxin-induced change in instantaneous growth strictly requires the immediate synthesis of growth-limiting proteins through auxin-induced gene expression (Cleland, 1971) or rather is triggered by a direct stimulation of growth-limiting processes (Hager et al., 1971). It has been proposed that sustained growth involves both gene expression and stimulation of growth-limiting processes (Vanderhoef et al., 1976). This long-standing question remains unanswered.