PIN-dependent auxin transport: action, regulation, and evolution

Abstract

Auxin participates in a multitude of developmental processes, as well as responses to environmental cues. Compared with other plant hormones, auxin exhibits a unique property, as it undergoes directional, cell-to-cell transport facilitated by plasma membrane-localized transport proteins. Among them, a prominent role has been ascribed to the PIN family of auxin efflux facilitators. PIN proteins direct polar auxin transport on account of their asymmetric subcellular localizations. In this review, we provide an overview of the multiple developmental roles of PIN proteins, including the atypical endoplasmic reticulum-localized members of the family, and look at the family from an evolutionary perspective. Next, we cover the cell biological and molecular aspects of PIN function, in particular the establishment of their polar subcellular localization. Hormonal and environmental inputs into the regulation of PIN action are summarized as well.

Figure 1.

Examples of Auxin-Mediated Developmental Processes. Auxin response maxima (visualized by transcriptional auxin response reporters; green in [A] and [C]; blue in [E]) are established by the action of polarly localized PIN proteins (green in [B] and [F]; red in [D]) during the development of shoot apical meristem-derived primordia ([A] and [B]), embryo ([C] and [D]), and lateral root ([E] and [F]). s, upper suspensor cell; hy, hypophysis I, IV, VI, and VII; e, developmental stages of lateral roots. Reproduced with modifications from Benková et al. (2003) ([A], [B], [E], and [F]) and Friml et al. (2003) ([C] and [D]). (A) In the shoot apical meristem, auxin accumulates at the position of incipient primordia and in primordium tips (indicated by arrowheads in [A] and [B]). (B) In epidermis, PIN1 is polarized toward these auxin maxima, while in the inner tissues, basally localized PIN1 presumably drives auxin away from the primordium (inset). (C) During embryogenesis, auxin response is first observed in apical parts of the embryo (left; eight-cell stage) and later in the basal parts (right; globular stage). (D) PIN7 localizes apically in the basal cell of a two-cell embryo (left; magnified in inset) and PIN1 basally in provascular initials at 16/32-cell stage (right; indicated by arrowhead). (E) Auxin concentrates at the apical end of a developing lateral root (arrowheads indicate cell division planes). (F) PIN1 gradually establishes polarized localizations (indicated by arrowheads) in the inner tissues of the developing lateral root.

Figure 2.

Subcellular Trafficking and Polarity Maintenance of PIN Proteins. Polar localization of PIN proteins is established by GNOM-mediated recycling and clathrin-mediated endocytosis (CME) and maintained by clustering in the plasma membrane as well as cell wall-plasma membrane connections. Apical-basal polarity is determined by reversible phosphorylation by PID/WAG kinases and PP2A phosphatase. Auxin transport activity of PIN is mediated by D6PK. PINs undergo trafficking through multivesicular body (MVB) for degradation in the lytic vacuole. Endogenous (hormones and signal peptides) and environmental (light, gravity, and salinity) signals influence various aspects of PIN trafficking. GA, Golgi apparatus; TGN/EE, trans-Golgi network/early endosome.

Figure 3.

A Model of Auxin Transport Canalization by Extracellular Auxin Perception by ABP1. This figure shows an update of the model presented by Wabnik et al. (2010). PIN proteins gradually polarize to form a canal of auxin flow connecting auxin source to the sink. Two neighboring cells share an apoplastic pool of ABP1 molecules. ABP1 exists in auxin-free and auxin-bound states, whereby it promotes endocytosis or is inactive, respectively. Due to an auxin concentration gradient across the apoplastic space, cell A (closer to the auxin source) experiences higher apoplastic auxin levels and fewer auxin-free ABP1 and thus has low PIN endocytosis rates, resulting in stabilization of PIN at the plasma membrane. The extracellular space near cell B has lower auxin concentration and more free ABP1 molecules that promote PIN removal from the plasma membrane.