Patterning of leaf vein networks by convergent auxin transport pathways.
Patterning of leaf vein networks by convergent auxin transport pathways.
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DOI:
10.1371/journal.pgen.1003294
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发表时间:
2013
期刊:
影响因子:
4.5
通讯作者:
Scarpella E
中科院分区:
文献类型:
--
作者:
Sawchuk MG;Edgar A;Scarpella E
The formation of leaf vein patterns has fascinated biologists for centuries. Transport of the plant signal auxin has long been implicated in vein patterning, but molecular details have remained unclear. Varied evidence suggests a central role for the plasma-membrane (PM)-localized PIN-FORMED1 (PIN1) intercellular auxin transporter of Arabidopsis thaliana in auxin-transport-dependent vein patterning. However, in contrast to the severe vein-pattern defects induced by auxin transport inhibitors, pin1 mutant leaves have only mild vein-pattern defects. These defects have been interpreted as evidence of redundancy between PIN1 and the other four PM-localized PIN proteins in vein patterning, redundancy that underlies many developmental processes. By contrast, we show here that vein patterning in the Arabidopsis leaf is controlled by two distinct and convergent auxin-transport pathways: intercellular auxin transport mediated by PM-localized PIN1 and intracellular auxin transport mediated by the evolutionarily older, endoplasmic-reticulum-localized PIN6, PIN8, and PIN5. PIN6 and PIN8 are expressed, as PIN1 and PIN5, at sites of vein formation. pin6 synthetically enhances pin1 vein-pattern defects, and pin8 quantitatively enhances pin1pin6 vein-pattern defects. Function of PIN6 is necessary, redundantly with that of PIN8, and sufficient to control auxin response levels, PIN1 expression, and vein network formation; and the vein pattern defects induced by ectopic PIN6 expression are mimicked by ectopic PIN8 expression. Finally, vein patterning functions of PIN6 and PIN8 are antagonized by PIN5 function. Our data define a new level of control of vein patterning, one with repercussions on other patterning processes in the plant, and suggest a mechanism to select cell files specialized for vascular function that predates evolution of PM-localized PIN proteins. The beautiful and varied patterns of veins in plant leaves have intrigued both artists and scientists since antiquity. The seminal work of some of these scientists has shown that the plant hormone auxin and its transport in plant tissues control leaf vein patterning, but molecular details of auxin-transport-dependent vein patterning are still unknown. Here we find that vein patterning is controlled by the concerted action of two spatially separate auxin transport pathways. One pathway transports auxin from cell to cell, the other to and from different compartments within the cell. The cell-to-cell pathway of auxin transport seems to exist only in land plants with veins. The within-cell pathway of auxin transport seems to have appeared earlier in the evolution of plants and exists also in primitive land plants, which form vein-like structures. Our findings suggest an unsuspected level of control of vein patterning, one that regulates patterning of plant features beyond veins and that could even be relevant for the formation of vein-like structures of primitive land plants.
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