Plants coordinate the polarity of hundreds of cells during vein formation, but how they do so is unclear. The prevailing hypothesis proposes that GNOM, a regulator of membrane trafficking, positions PIN-FORMED auxin transporters to the correct side of the plasma membrane; the resulting cell-to-cell, polar transport of auxin would coordinate tissue cell polarity and induce vein formation. Contrary to predictions of the hypothesis, we find that vein formation occurs in the absence of PIN-FORMED or any other intercellular auxin-transporter; that the residual auxin-transport-independent vein-patterning activity relies on auxin signaling; and that a GNOM-dependent signal acts upstream of both auxin transport and signaling to coordinate tissue cell polarity and induce vein formation. Our results reveal synergism between auxin transport and signaling, and their unsuspected control by GNOM in the coordination of tissue cell polarity during vein patterning, one of the most informative expressions of tissue cell polarization in plants.

BackgroundTissue networks such as the vascular networks of plant and animal organs transport signals and nutrients in most multicellular organisms. The transport function of tissue networks depends on topological features such as the number of networks’ components and the components’ connectedness; yet what controls tissue network topology is largely unknown, partly because of the difficulties in quantifying the effects of genes on tissue network topology. We address this problem for the vein networks of plant leaves by introducing biologically motivated descriptors of vein network topology; we combine these descriptors with cellular imaging and molecular genetic analysis; and we apply this combination of approaches to leaves of Arabidopsis thaliana that lack function of, overexpress or misexpress combinations of four PIN-FORMED (PIN) genes—PIN1, PIN5, PIN6, and PIN8—which encode transporters of the plant signal auxin and are known to control vein network geometry.ResultsWe find that PIN1 inhibits vein formation and connection, and that PIN6 acts redundantly to PIN1 in these processes; however, the functions of PIN6 in vein formation are nonhomologous to those of PIN1, while the functions of PIN6 in vein connection are homologous to those of PIN1. We further find that PIN8 provides functions redundant and homologous to those of PIN6 in PIN1-dependent inhibition of vein formation, but that PIN8 has no functions in PIN1/PIN6-dependent inhibition of vein connection. Finally, we find that PIN5 promotes vein formation; that all the vein-formation-promoting functions of PIN5 are redundantly inhibited by PIN6 and PIN8; and that these functions of PIN5, PIN6, and PIN8 are independent of PIN1.ConclusionsOur results suggest that PIN-mediated auxin transport controls the formation of veins and their connection into networks.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-015-0208-3) contains supplementary material, which is available to authorized users.

No abstract

No abstract