“The discovery of a potentially self-regulating feedback network for auxin distribution and response is the main message.”

The many effects of the plant hormone auxin on development have puzzled biologists for decades. How can a single molecule elicit a coordinated response in plant cells involving cell specification, cell division, and cell expansion? I suspect that our paper is frequently cited because it demonstrates and offers explanations for two aspects of this question: we reveal spatially separated roles of auxin and its transport machinery in the development of a single organ; and we show self-organizing properties of auxin distribution due to feedback from auxin responsive genes to the transport machinery that localizes auxin.

The discovery of a potentially self-regulating feedback network for auxin distribution and response is the main message. But we also describe a new technology in which auxins are locally produced in defined cell types after which their transport can be monitored.

In this paper, we show that the cooperation of five PIN genes encoding transmembrane proteins involved in polar auxin transport is needed in the root meristem of the model plant Arabidopsis for a special auxin distribution. Manipulation of this distribution by mutation of multiple PIN genes affects cell identity, cell division, and cell expansion in three spatially separated regions. We show that the coordinated transport of auxins by a group of redundantly acting PIN transmembrane proteins creates an auxin distribution in the Arabidopsis root tip that can trigger these different responses in different regions.

Further, we show that this transport is extremely dynamic in its regulation. First, PIN genes can replace one another in dramatic ways which reveals unusual redundancy between genes that are normally not coexpressed. Second, we recently discovered important targets of auxin accumulation in the root, the PLETHORA genes (Aida et al., Cell 119: 109-120, 2004). In the Blilou et al. paper we show that these first become expressed thanks to PIN activity and subsequently regulate PIN genes. This interaction loop can explain much of the apparently self-organizing responses to auxins.

Our earlier work had revealed an amazing connection in the Arabidopsis root between auxin distribution and transport on the one hand and cell division, cell polarity, and cell identity on the other hand (Sabatini et al., Cell 99: 463-472, 1999). At the same time the PIN proteins were identified as concrete players in polar auxin transport. Thanks to a fruitful collaboration with Drs. Jiri Friml and Klause Palme we were able to pursue concrete molecular mechanisms behind these striking connections (Friml et al, Cell 108: 661-673, 2002).

During the same years, we identified the redundant PLETHORA genes by enhancer trapping and showed that they are main players in specifying the auxin-dependent cell types as well as being expressed in an auxin-dependent way (Aida et al., Cell 119, 109-120, 2004). In the Blilou et al paper these two lines of investigation could be merged.