Auxin activity: Past, present, and future

Abstract

Long before its chemical identity was known, the phytohormone auxin was postulated to regulate plant growth. In the late 1800s, Sachs hypothesized that plant growth regulators, present in small amounts, move differentially throughout the plant to regulate growth. Concurrently, Charles Darwin and Francis Darwin were discovering that light and gravity were perceived by the tips of shoots and roots and that the stimulus was transmitted to other tissues, which underwent a growth response. These ideas were improved upon by Boysen-Jensen and Paál and were later developed into the Cholodny-Went hypothesis that tropisms were caused by the asymmetric distribution of a growth-promoting substance. These observations led to many efforts to identify this elusive growth-promoting substance, which we now know as auxin. In this review of auxin field advances over the past century, we start with a seminal paper by Kenneth Thimann and Charles Schneider titled "The relative activities of different auxins" from the American Journal of Botany, in which they compare the growth altering properties of several auxinic compounds. From this point, we explore the modern molecular understanding of auxin-including its biosynthesis, transport, and perception. Finally, we end this review with a discussion of outstanding questions and future directions in the auxin field. Over the past 100 yr, much of our progress in understanding auxin biology has relied on the steady and collective advance of the field of auxin researchers; we expect that the next 100 yr of auxin research will likewise make many exciting advances.

Keywords: auxin; auxin history; metabolism; signaling; transport.

Fig. 1

Auxin response assays. (A) The Avena test. Compounds are tested for auxin activity in Avena sativa seedlings mounted on a test apparatus, and the tip of the coleoptile removed. After a few hours of growth, a larger portion of the coleoptile is removed, and the primary leaf pulled upward to detach it from the base. A block of agar containing the compound to be tested is placed on one side of the cut surface. After incubation, the curvature induced by the diffusion and transport of auxin from the agar block into the coleoptile of the Avena seedling is measured. Image modified from Went and Thimann (1937). (B) The Pisum test. Compounds are tested for auxin activity by removing the top of 7-d-old Pisum sativum seedlings below the terminal bud and the stem split lengthwise for 3 cm. The split stem section is excised a few millimeters below the split and split stems incubated in solutions containing compounds to be tested. After incubation, the curvature angles induced from the auxins causing cell expansion on one side of the coleoptile are measured. Image modified from Went and Thimann (1937). (C) The Arabidopsis root elongation test. Compounds are tested for auxin activity by plating sterilized seed of Arabidopsis thaliana on agar-solidified media containing compounds of interest. After 7–10 d of growth, seedling root lengths are measured.

Fig. 2

Structures of naturally occurring and synthetic auxins. Auxins found in plants include the active auxins indole-3-acetic acid (IAA), 4-Cl-IAA, and phenylacetic acid (PAA), as well as the inactive auxin precursors indole-3-butyric acid (IBA), and indole-3-propionic acid (IPrA). Synthetic auxins include the active 2,4-dichlorophenoxyacetic acid (2,4-D) and naphthalene acetic acid (NAA), and the inactive precursor 2,4-dichlorophenoxybutyric acid (2,4-DB). The occurrence of auxin a (auxenotriolic acid), auxin b (auxenolonic acid), benzofurane-3-acetic acid (BzFA), and phenyl-butyric acid (PBA) in plants or other organisms has been debated or is unknown.

Fig. 3

Auxin biosynthesis and storage forms in higher plants. (A) Possible pathways for plant auxin biosynthesis. Solid arrows indicate those steps for which enzymes are known. Dashed arrows indicate those steps for which no enzyme has been identified or the enzyme identity is in question. (B) Mean primary root lengths (±SE) of 8-d-old Arabidopsis seedlings grown in the presence of the indicated auxin or auxin precursor.

Fig. 4

Auxin transport mechanisms. AUX/LAX proteins localize to different faces of the cell depending on the particular cell type, where they act to influx auxin from the apoplast into the cytoplasm (depicted in green). The long PIN proteins localize to either the apical or basal face of the cell in the root to efflux auxin and establish auxin gradients. The short PIN proteins and PILS proteins localize to the ER, where they efflux auxin from the cytoplasm into the ER lumen, presumably to regulate auxin activity via compartmentalization, and possibly metabolism. The ABCB family of auxin transporters localize to the plasma membrane to efflux auxin outside the cell. Some members of the ABCB family have been shown to display both efflux and influx activity based on the cytoplasmic concentration of auxin. Two members of the ABCG family localize to the outer lateral domain in the epidermis, and transport IBA into the surrounding environment.

Fig. 5

The TIR1/AFB auxin signaling pathway. Under low auxin conditions, ARF activity is repressed by multimerization with Aux/IAA repressor proteins. In the presence of auxin, an Aux/IAA protein and a TIR1/AFB protein form an auxin coreceptor, the Aux/IAA protein is then polyubiqutiylated by the SCF^TIR1/AFB complex and targeted to the proteasome for degradation. This degradation of the Aux/IAA repressor relieves the repression of the ARF transcription factor to allow auxin-responsive gene transcription.

Fig. 6

The ABP1 auxin signaling pathway. Extracellular-localized ABP1 is tethered to the plasma membrane by CBP1. ABP1 interacts with TMK receptors in an auxin-dependent manner. ROP activity is regulated downstream of auxin perception by the ABP1-TMK complex. In the epidermal pavement cells of the Arabidopsis cotyledon, ROP2 and RIC4 positively regulate actin polymerization to form lobes and also affect PIN1 protein localization to alter auxin efflux. Alternatively, ROP6 and RIC1 positively regulate microtubule polymerization, leading to constrictions that ultimately form indentations. The outcome of this pathway leads to the puzzle-piece morphology of these cells.

Fig. 7

Arabidopsis root elongation responses to IAA and 2,4-D. Normalized mean primary root lengths (±SE) of 8-d-old Arabidopsis seedlings grown in the presence of the indicated concentration of (A) IAA or (B) 2,4-D.

Fig. 8

Auxin-related publications. Frequency of auxin-related publications from 1936 to 2013 (based on a PubMed search).