Abstract
Polar auxin transport (PAT) is a major determinant of plant morphology and internal anatomy with important roles in vascular patterning, tropic growth responses, apical dominance and phyllotactic arrangement. Woody plants present a highly complex system of vascular development in which isolated bundles of xylem and phloem gradually unite to form concentric rings of conductive tissue. We generated several transgenic lines of hybrid poplar (Populus tremula x alba) with the auxin-responsive DR5 promoter driving GUS expression in order to visualize an auxin response during the establishment of secondary growth. Distinct GUS expression in the cambial zone and developing xylem-side derivatives supports the current view of this tissue as a major stream of basipetal PAT. However, we also found novel sites of GUS expression in the primary xylem parenchyma lining the outer perimeter of the pith. Strands of primary xylem parenchyma depart the stem as a leaf trace, and showed GUS expression as long as the leaves to which they were connected remained attached (i.e., until just prior to leaf abscission). Tissue composed of primary xylem parenchyma strands contained measurable levels of free indole-3-acetic acid (IAA) and showed basipetal transport of radiolabeled auxin (3H-IAA) that was both significantly faster than diffusion and highly sensitive to the PAT inhibitor NPA. Radiolabeled auxin was also able to move between the primary xylem parenchyma in the interior of the stem and the basipetal stream in the cambial zone, an exchange that was likely mediated by ray parenchyma cells. Our results suggest that (a) channeling of leaf-derived IAA first delineates isolated strands of pre-procambial tissue but then later shifts to include basipetal transport through the rapidly expanding xylem elements, and (b) the transition from primary to secondary vascular development is gradual, with an auxin response preceding the appearance of a unified and radially-organized vascular cambium.
Highlights
The plant hormone auxin serves as a major regulator of plant morphology and anatomy with critical roles in developmental processes including embryogenesis, phyllotactic and vascular patterning, apical dominance and tropic responses
PtaDR5 response to exogenous and endogenous auxin All 14 PtaDR5 lines were auxin-responsive as indicated by exogenous indole-3-acetic acid (IAA) application (PtaDR5-2 shown in Figure 2) the strength of the response varied
In the absence of exogenous IAA GUS expression was consistently found in axillary meristems, the cambial zone, poles of primary xylem parenchyma (PXP) around the outer margin of the pith, and both primary and lateral root tips (Figure 2a2c)
Summary
The plant hormone auxin serves as a major regulator of plant morphology and anatomy with critical roles in developmental processes including embryogenesis, phyllotactic and vascular patterning, apical dominance and tropic responses. Originally conceived through classical development studies, the canalization hypothesis [4,5] has been repeatedly supported and refined by molecular work demonstrating that auxin transport and accumulation is mediated by at least three classes of specific membrane proteins (PIN, AUX1/LAX and MDR/ABCB families; for reviews see [6,7,8]). The PIN proteins in particular appear to satisfy several critical requirements of the canalization hypothesis: they are often asymmetrically localized in the plasma membrane where they are able to be rapidly repositioned (e.g., [9]) and their localization is auxin-responsive, providing the positive feedback mechanism required to effect ’canalized’ flow [10]
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