Abstract
The flexible development of plants is characterized by a high capacity for post-embryonic organ formation and tissue regeneration, processes, which require tightly regulated intercellular communication and coordinated tissue (re-)polarization. The phytohormone auxin, the main driver for these processes, is able to establish polarized auxin transport channels, which are characterized by the expression and polar, subcellular localization of the PIN1 auxin transport proteins. These channels are demarcating the position of future vascular strands necessary for organ formation and tissue regeneration. Major progress has been made in the last years to understand how PINs can change their polarity in different contexts and thus guide auxin flow through the plant. However, it still remains elusive how auxin mediates the establishment of auxin conducting channels and the formation of vascular tissue and which cellular processes are involved. By the means of sophisticated regeneration experiments combined with local auxin applications in Arabidopsis thaliana inflorescence stems we show that (i) PIN subcellular dynamics, (ii) PIN internalization by clathrin-mediated trafficking and (iii) an intact actin cytoskeleton required for post-endocytic trafficking are indispensable for auxin channel formation, de novo vascular formation and vascular regeneration after wounding. These observations provide novel insights into cellular mechanism of coordinated tissue polarization during auxin canalization.
Highlights
The development of plants is a very flexible and dynamic process, which is characterized, among others, by post embryonic organ formation of new leaves, flowers and roots and a high capability of regeneration after wounding [1]
Given that PIN proteins undergo clathrin-mediated constitutive endocytic recycling, and this was proposed to be important for various PIN relocations [15], we first tested the involvement of clathrin-mediated endocytosis (CME) in vasculature regeneration
Secondary cell wall patterning was recognizable (Fig. 1B, inset). Both of the analyzed clathrin heavy chain-defective mutants chc2-1 and chc2-2 either did not show any signs of vasculature regeneration near the wound (Fig. 1C) or the regenerated vasculature was highly defective as seen in case of chc2-2 (Supplementary Fig. S1A)
Summary
The development of plants is a very flexible and dynamic process, which is characterized, among others, by post embryonic organ formation of new leaves, flowers and roots and a high capability of regeneration after wounding [1]. The canalization hypothesis describes the unique property of auxin being transported actively from cell to cell in a directional manner by regulating the polarity of its own flow [3,4,5]. This feed-back regulation has been proposed to be a key prerequisite for a spontaneous formation of these auxin transport channels [6]. During vascular formation in leaves [9], shoot apical meristem organogenesis [10,11], shoot branching [12] or regeneration of wounded vasculature [13], it has been shown that localized and polarized PIN1 expression and directional auxin transport routes demarcate the position of future vascular strands. When the polar auxin flow is disrupted by wounding they can adapt dynamically and re-establish auxin flow by the formation of new channels and leading to the formation of new vasculature strands [5,12]
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