Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity

Abstract

Plant development is characterized by a profound ability to regenerate and form tissues with new axes of polarity. An unsolved question concerns how the position within a tissue and cues from neighboring cells are integrated to specify the polarity of individual cells. The canalization hypothesis proposes a feedback effect of the phytohormone auxin on the directionality of intercellular auxin flow as a means to polarize tissues. Here we identify a cellular and molecular mechanism for canalization. Local auxin application, wounding, or auxin accumulation during de novo organ formation lead to rearrangements in the subcellular polar localization of PIN auxin transport components. This auxin effect on PIN polarity is cell-specific, does not depend on PIN transcription, and involves the Aux/IAA-ARF (indole-3-acetic acid-auxin response factor) signaling pathway. Our data suggest that auxin acts as polarizing cue, which links individual cell polarity with tissue and organ polarity through control of PIN polar targeting. This feedback regulation provides a conceptual framework for polarization during multiple regenerative and patterning processes in plants.[Keywords: Auxin signaling; auxin transport; cell and tissue polarity; lateral root development; phyllotaxis; vasculature development] Supplemental material is available at http://www.genesdev.org.

Manipulation of Auxin Transport in Plant Roots during Rhizobium Symbiosis and Nematode Parasitism

“…A recent report identified >400 proteins of the secretome of a root-knot nematode, including several putative transcriptional regulators, although their targets remain elusive (Bellafiore et al, 2008). Alternatively, auxin itself can alter its own transport by relocating PIN proteins (Sauer et al, 2006), so any alterations of auxin concentration could also affect changes in auxin transporters.…”

PIN Polar Targeting

“…Indeed, predicted rearrangements of PIN polarity have been observed during leaf vasculature formation (Scarpella et al, 2006) and during vasculature regeneration after wounding (Sauer et al, 2006). The underlying mechanism is unknown, but feedback regulations of PIN polarity by auxin itself are the indispensable parts of models describing different auxin-dependent patterning processes, such as the phylotactic pattern of organ initiation (Barbier de Reuille et al, 2006;Jö nsson et al, 2006;Smith et al, 2006).…”

“…The PINFORMED (PIN) proteins have been identified and characterized as key regulators of a multitude of auxin-mediated developmental processes, including tropic growth (Chen et al, 1998;Luschnig et al, 1998;Mü ller et al, 1998;Utsuno et al, 1998;Friml et al, 2002b), axis formation in embryogenesis , postembryonic organogenesis (Benková et al, 2003;Reinhardt et al, 2003), root meristem maintenance (Friml et al, 2002a;Blilou et al, 2005), and vascular tissue differentiation and regeneration (Sauer et al, 2006;Scarpella et al, 2006). PIN proteins are PM proteins that act as auxin efflux carriers (Petrášek et al, 2006) and have mainly a polar localization that correlates with and is required for the direction of auxin flow .…”

COP1 mediates the coordination of root and shoot growth by light through modulation of PIN1- and PIN2-dependent auxin transport in Arabidopsis

“…5G,H). Because auxin can modulate PIN intracellular localization and stability (Paciorek et al, 2005;Sauer et al, 2006;Abas et al, 2006;Sieberer et al, 2000;Vieten et al, 2005), we wondered whether reduced shoot-to-root PAT in darkness could cause these changes. To 3407 RESEARCH ARTICLE COP1 regulates root growth test this, we inhibited shoot-to-root PAT in light-grown DR5:GUS, DR5rev:GFP , PIN1:PIN1-GFP and PIN2:PIN2-GFP seedlings using local NPA application to the hypocotyl (Fig.…”