Auxin as a positional signal in pattern formation in plants.

Abstract

By using a novel, extremely sensitive and specific gas chromatography-mass spectrometry technique we demonstrate in Pinus sylvestris (L.) trees the existence of a steep radial concentration gradient of the endogenous auxin, indole-3-acetic acid, over the lateral meristem responsible for the bulk of plant secondary growth, the vascular cambium. This is the first evidence that plant morphogens, such as indole-3-acetic acid, occur in concentration gradients over developing tissues. This finding gives evidence for a regulatory system in plants based on positional signaling, similar to animal systems.Formation of patterns is one of the most intriguing phenomena in biology. Pattern development requires that gene activity must be strictly controlled in time and space. Every cell must receive information about its position and express the appropriate genes. The existence of morphogenetic fields has been suggested as a possible source of such information in both animal and plant systems (1-4). This field is thought to consist of one or more diffusable and physiologically active substances (morphogens) which originate from organizing centers. The concentration gradients created would then influence on tissue and organ differentiation. Current examples of morphogens of this sort in animals are retinoic acid in vertebrate limb development and activin in early amphibian development (5, 6). In plants, positional signaling has been discussed mainly on the basis of the orderly induction of leaf and root primordia and the organization of vascular tissues (7), but neither the mechanisms nor the morphogens behind these patterns have been elucidated. Auxins and cytokinins are plant hormones that have been characterized as important signals in plant development, being involved in the induction and maintenance of meristems as well as in plant polarity (8). Not surprisingly, these substances have been proposed to function as positional signals in pattern specification (9, 10). To date, this proposition has not found much support due to the lack of data proving that such endogenous plant hormone gradients are found in plants (11,12).The formation of secondary vascular tissues is a well described phenomenon of patterned growth in plants. This pattern has both radial and longitudinal components (13). Phloem and xylem differentiate radially on each side of the lateral meristem (the vascular cambium). The cambial derivatives which form xylem first pass through a zone of cell expansion and then a zone of secondary wall formation and, finally, a zone of programmed cell death. Phloem derivatives expand and differentiate forming a living tissue (Fig. 1) MATERIALS AND METHODSBlocks (2 x 5 cm) consisting of extraxilary tissues and a few annual rings were chiseled out at breast height during active (late June) and dormant (mid-January) periods from Pinus sylvestris (L.) trees (-120 years old, 19 m tall, 34 cm in diameter at breast height, location 64°14'N, 19°46'E) and immediately frozen in liquid N2. After trimming the blocks, specific ...

Mathematical model of morphogen electrophoresis through gap junctions

“…The magnitude of the serotonin gradient predicted from our model matches well with the reported auxin gradients, which are thought to be approximately 10-fold (Edlund et al, 1995;Uggla et al, 1996). We also compared the gradient with another likely morphogen (although one which is not GJC-related): retinoic acid.…”

Brassinosteroid signaling and auxin transport are required to establish the periodic pattern of Arabidopsis shoot vascular bundles

“…Auxin is essential for vascular tissue formation and differentiation (13,14). In leaves, it has been shown that auxin accumulates in the procambial cells (15,16), leading to the gradual canalization of auxin into the leaf vascular strands through polarization of auxin efflux carriers (4,5,17). In the shoot, it has been shown that the auxin efflux carrier PIN1 is expressed in the procambium and xylem cells, at the basal side and in a fraction of the lateral cell membranes (18).…”

Tracing a key player in the regulation of plant architecture: the columnar growth habit of apple trees (Malus × domestica)

“…IAA also regulates secondary growth, which is more pronounced in trees because their longevity combined with the indeterminate growth of plants leads to a higher average plant size and biomass compared with annual plants, necessitating the reinforcement of the plant body. In this context, the formation of a radial auxin gradient with a peak in the cambium and the adjacent first few layers of xylem cells and its synergistic action with GA in wood formation have been intensively researched (Uggla et al 1996(Uggla et al , 1998Eriksson et al 2000;Israelsson et al 2005;Björklund et al 2007;Nilsson et al 2008;Mauriat and Moritz 2009;Han et al 2011;Chen et al 2013). Furthermore, GAs affect elongation growth Elias et al 2012) as well as flowering of perennial plants (Zawaski et al 2011;Randoux et al 2012).…”