Downloaded from http://cshperspectives.cshlp.org/ on September 28, 2021 - Published by Cold Spring Harbor Laboratory Press Odyssey of Auxin Steffen Abel1 and Athanasios Theologis2 1Department of Molecular Signal Processing, Leibniz-Institute of Plant Biochemistry, D-06120 Halle (Saale), Germany 2Plant Gene Expression Center, Albany, California 94710 Correspondence: [email protected] The history of plant biology is inexorably intertwined with the conception and discovery of auxin, followed by the many decades of research to comprehend its action during growth and development. Growth responses to auxin are complex and require the coordination of auxin production, transport, and perception. In this overview of past auxin research, we limit our discourse to the mechanism of auxin action. We attempt to trace the almost epic voyage from the birth of the hormonal concept in plants to the recent crystallographic studies that resolved the TIR1-auxin receptor complex, the first structural model of a plant hormone receptor. The century-long endeavor is a beautiful illustration of the power of scientific reasoning and human intuition, but it also brings to light the fact that decisive progress is made when new technologies emerge and disciplines unite. he simple hormone related to tryptophan, its spatio-temporal patterns of biosynthesis, Tindole-3-acetic acid (IAA or auxin), has reversible conjugation, and degradation, is still probably been the most intensely studied mole- unfolding. For example, significant progress cule in plants as it impacts virtually every facet has been made charting the biosynthetic path- during their life cycle. In fact, a total failure in ways by a combination of genetic and biochem- IAA production has not been reported for any ical approaches, which revealed the operation of plant alive. Thus, it is not surprising that auxin at least five different routes to IAA. Our current biology is one of the oldest fields of experi- understanding of the redundant metabolic pro- mental plant research and that the underlying cesses that determine auxin supply has re- mechanisms of its action have captivated many cently been reviewed (Woodward and Bartel generations of scientists. 2005; Delker et al. 2008; Chandler 2009). The The regulation of growth and develop- delivery of auxin from its biosynthetic sources ment by IAA is largely executed via the coordi- to its sites of perception follows two major, nation of a triumvirate of complex processes: unrelated modes of transportation: rapid long- auxin metabolism, auxin translocation, and distance movement via the phloem sap, and auxin response. The intricate maze of meta- slower cell-to-cell distribution over shorter bolic reactions related to IAA, encompassing distances. The latter process is unique among Editors: Mark Estelle, Dolf Weijers, Karin Ljung, and Ottoline Leyser Additional Perspectives on Auxin Signaling available at www.cshperspectives.org Copyright # 2010 Cold Spring Harbor Laboratory Press; all rights reserved; doi: 10.1101/cshperspect.a004572 Cite this article as Cold Spring Harb Perspect Biol 2010;2:a004572 1 Downloaded from http://cshperspectives.cshlp.org/ on September 28, 2021 - Published by Cold Spring Harbor Laboratory Press S. Abel and A. Theologis plant hormones and signaling molecules because structural model of a plant hormone receptor, of its tissue-dependent directionality, which is es- the Rosetta stone in auxin biology. tablished by the asymmetric subcellular localiza- tion of auxin influx and efflux carrier proteins. BIRTH OF “AUXANO” The chemiosmotic hypothesis of polar auxin transport proposed a mechanistic framework The concept of hormone action is deeply rooted and made astonishingly visionary predictions in the history of botany and can be traced back (Rubery and Sheldrake 1974; Raven 1975). The for more than 250 years. The phenomenon of interference of local, cell-specific auxin biosyn- correlations, that is the influence exerted by thesis and directional intercellular auxin trans- one plant organ on another, or in today’s words, port causes a differential distribution of auxin functional relationships between distant parts in a given tissue, which, in its extreme, can give of a plant, was first formulated in 1758 by Henri rise to distinct and steep auxin maxima or mini- Lois Duhamel du Monceau. His studies on ma, or establish more graded differences in auxin growth and strength of wood led him to con- concentration between its cells. Such auxin gra- clude that two streams of sap moving in oppo- dients are often influenced by diverse internal site directions are responsible for establishing and external cues and have been implicated in such correlations. A typical experiment would the regulation of numerous auxin-mediated pro- show that interruption of the downward mov- cesses relevant to the adaptation of plant form ing sap by clamps or ring wounds caused swell- and function. Research on polar auxin distribu- ings that often formed callus tissue and gave tion enjoyed a renaissance during the past decade rise to root formation above the site of injury. and the remarkable progress made has been For about a century, the idea of physiological documented in various excellent reviews (see correlations lost its appeal to the study of plant Benjamins and Scheres 2008; Petra´sˇek and Friml anatomy, however, only until the discovery of 2009; Vanneste and Friml 2009). the sieve elements together with their asso- The positional information encrypted in ciated role in sap conductance. The concept the landscape of differential auxin distribution regained momentum in the 1880s when Julius in a field of cells is believed to determine indi- von Sachs unified known facts on correlation vidual cell responses to the hormone (Vanneste phenomena with advances in morphology. He and Friml 2009), which brings into focus the proposed a first coherent framework of root- mechanism of auxin perception and ensuing forming, flower-inducing, and other special action. In this article, we revisit the long-sought substances, which move in different directions and sometimes hard-fought quest to under- through the plant to control its growth and stand these fundamental processes. After more development (see Went and Thimann 1937). than seven decades of incremental progress, Directional growth responses such as pho- occasionally disrupted by stagnation or distrac- totropism and geotropism were soon regarded tion, today it is well established that auxin pri- as a special kind of correlation phenomenon marily acts by reprogramming gene expression and their study directly led to the discovery of to influence plant growth (Chapman and Estelle auxin. Charles Darwin, who became interested 2009). However, it was only recently that the in- in plant tropisms, showed that light and gravity itial mechanism of auxin perception was uncov- are perceived by the tips of shoots and roots, and ered, which revealed a surprisingly short path to that the effect of an asymmetric stimulus is the execution of transcriptional response (Tan transmitted to the lower region beneath the tip, et al. 2007), envisioned more than two decades which then responds with differential growth, ago (Theologis 1986). In this brief overview, causing curvature. For the phototropic re- we highlight the almost epic voyage from the sponse, he performed simple but insightful emergence of the hormone concept in plants, experiments on coleoptiles of etiolated canary followed by the discovery of IAA and the strug- grass seedlings by shielding either the tip or gle to understand its mode of action, to the first the elongatingbasefromunilateralillumination. 2 Cite this article as Cold Spring Harb Perspect Biol 2010;2:a004572 Downloaded from http://cshperspectives.cshlp.org/ on September 28, 2021 - Published by Cold Spring Harbor Laboratory Press Odyssey of Auxin He also noted that when the tip was removed, no and advanced Paa´l’s line of reasoning to make curvature occurred in the lower part of the the definitive discovery of the hormone, named coleoptile. The essence of these observations is auxin soon after its structural identification in encapsulated in his famous and widely cited 1934/35 (a term derived from the Greek verb phrase “we must, therefore, conclude that when auxano, which means “to grow or to expand”). seedlings are freely exposed to a lateral light, He placed excised Avena coleoptile tips on agar some influence is transmitted from the upper to blocks that received the growth-promoting sub- the lower part, causing the latter to bend”, pub- stance by diffusion and could then serve as an lished in his book The Power of Movement in artificial but potent stimulus source for induc- Plants (1880). Thus, Darwin is credited for con- ing curvature of decapitated coleoptiles. Went ceiving the idea of a transmittable correlation developed the Avena coleoptile curvature test factor regulating growth at a distant site. How- to a quantitative bioassay, which he applied to ever, the nature of this factor remained elusive determine some of the physicochemical proper- for more than 30 years. Building on Darwin’s ties of the hormone. Whereas Frits Went suc- observations, Peter Boysen-Jensen showed that ceeded in capturing the substance by a simple the phototropic stimulus is transmitted from diffusion technique, its isolation and the deter- an excised tip across a gelatin barrier into the mination of its chemical identity followed a me- lower part of an Avena coleoptile where it still andering path. Because of insufficient analytical elicits