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Local, Efflux-Dependent Auxin Gradients As a Common Module for Plant Organ Formation

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Local, Efflux-Dependent Auxin Gradients As a Common Module for Plant Organ Formation CORE Metadata, citation and similar papers at core.ac.uk Provided by Elsevier - Publisher Connector Cell, Vol. 115, 591–602, November 26, 2003, Copyright 2003 by Cell Press Local, Efflux-Dependent Auxin Gradients as a Common Module for Plant Organ Formation Eva Benkova´ ,1,2,3,* Marta Michniewicz,1 growing shoots or roots bearing a secondary meristem Michael Sauer,1 Thomas Teichmann,2 at the tip. Aerial organs such as leaves and secondary Daniela Seifertova´ ,1 Gerd Ju¨ rgens,1 and Jirˇ´ı Friml1,* shoots, including flowers, originate from primordia on 1Zentrum fu¨ r Molekularbiologie der Pflanzen the flanks of the shoot meristem. Flower primordia give Universita¨ tTu¨ bingen rise to lateral organs, such as sepals, petals, stamens, 72076 Tu¨ bingen and carpels. Carpels fuse to form the gynoecium, which Germany produces organs—ovules—along the placenta of the 2 Max-Delbru¨ ck-Laboratorium ovary. Ovules, in turn, initiate integuments as lateral der Max-Planck-Gesellschaft primordia (Esau, 1977). The situation is less complex in 50829 Ko¨ ln the root where lateral root primordia are initiated from Germany localized cell groups within the pericycle (Dubrovsky et 3 Institute for Biophysics al., 2000). ASCR The morphological diversity of plant organs depends 61265 Brno on the developmental origin of their primordia: shoot Czech Republic meristems generate leaves, floral meristems floral or- gans, pistils ovules, ovules integuments, and roots make lateral roots. The difference between leaves and floral Summary organs, for example, can be attributed to the expression of floral homeotic genes in the latter but not the former Plants, compared to animals, exhibit an amazing organs (Honma and Goto, 2001). A common feature of adaptability and plasticity in their development. This all shoot-derived, as opposed to root-derived, organ is largely dependent on the ability of plants to form primordia is the expression of the AINTEGUMENTA tran- new organs, such as lateral roots, leaves, and flowers scription factor (Elliott et al., 1996). Another example is during postembryonic development. Organ primordia the involvement of the WUSCHEL homeobox protein in develop from founder cell populations into organs by both flower and ovule development (Gross-Hardt et al., coordinated cell division and differentiation. Here, we 2002). By contrast, underground organs such as lateral show that organ formation in Arabidopsis involves dy- roots are developmentally distinct from aerial organs in namic gradients of the signaling molecule auxin with terms of primordium initiation, subsequent development maxima at the primordia tips. These gradients are me- as well as regulatory gene expression (Malamy and Ben- diated by cellular efflux requiring asymmetrically local- fey, 1997). These observations suggested at least two ized PIN proteins, which represent a functionally re- different regulatory mechanisms for postembryonic or- dundant network for auxin distribution in both aerial gan formation in plants. and underground organs. PIN1 polar localization un- Studies focused on the initiation and positioning of dergoes a dynamic rearrangement, which correlates organs, such as leaves (Reinhardt et al., 2000), flowers with establishment of auxin gradients and primordium (Okada et al., 1991; Oka et al., 1999), and lateral roots development. Our results suggest that PIN-depen- (Laskowski et al., 1995), have implicated the plant-sig- dent, local auxin gradients represent a common mod- naling molecule auxin. Auxin is unique among plant hor- ule for formation of all plant organs, regardless of their mones in being actively and directionally transported mature morphology or developmental origin. from the place of synthesis in young apical parts. Current models propose that members of the PIN protein family Introduction of auxin efflux regulators represent an important part of a network for auxin distribution throughout the plant Plasticity and adaptability of development represent the (reviewed in Friml, 2003). PIN proteins have been shown most important life strategy of plants. Unlike animals, to mediate various developmental processes such as which can escape unfavorable conditions by behavioral vascular tissue and flower development (PIN1; Ga¨ lweiler responses, plants compensate for their sessile lifestyle et al., 1998), tropisms (PIN2, PIN3; Mu¨ ller et al., 1998, by changing their development in response to external Friml et al., 2002b), as well as patterning of the root cues. Whereas animals establish the entire body organi- (PIN4; Friml et al., 2002a). Cellular polarities of PIN pro- zation during embryogenesis, the adult life form of plants tein localization correlate with directions of auxin flux is largely dependent on postembryonic development. (reviewed in Friml, 2003). The flexibility of the transport Self-maintaining stem cell systems—the meristems, system may result, at the cellular level, from the continu- which are established at both ends of the apical-basal ous cycling of PIN proteins between the plasma mem- embryonic axis—are able to perpetuate existing organs brane and endosomes (Geldner et al., 2001, 2003a), and initiate new organ primordia (Steeves and Sussex, allowing for rapid changes in PIN polar localization and 1989). Some primordia develop into determinate organs hence redirection of auxin fluxes in development. So with finite cell numbers, whereas others develop into far, this has been demonstrated for PIN3 relocation in response to gravity stimulation (Friml et al., 2002b). It *Correspondence: [email protected] (J.F.), eva. remains to be determined whether PIN relocation for [email protected] (E.B.) auxin redistribution could also provide a general mecha- Cell 592 Figure 1. Distribution of Auxin and Its Re- sponse in Lateral Root Primordia (A) Spatial pattern of DR5::GUS expression during primordium development: the DR5 ac- tivity gradient with the maximum at the pri- mordium tip is gradually established. OL and IL, outer and inner layers; central cells out- lined. (B) DR5::GUS in columella initial region of the mature lateral root. (C) 2,4-D treatment: loss of DR5 gradient and induction of DR5 activity in the entire pri- mordium. (D) NPA treatment: impaired DR5 gradient after inhibition of auxin efflux. (E) Immunolocalization of IAA during primor- dium development: the IAA gradient with the maximum at the tip is gradually established. Inset shows increased signal, however no change of the gradient after the IAA treatment. (F) IAA accumulation in columella initial re- gion of the mature lateral root. Inset shows negative control, no signal without IAA fix- ation. Division planes marked by arrowheads and developmental stages indicated in the upper right corner: I, II, III, IV, V, and e – emergence. GUS signal in blue (A–D), IAA signal in brown (E and F). nism for other developmental processes including or- activity was highest in columella initials and surrounding gan formation. cells (Figure 1B), identical to the reported pattern in Here, we analyze the role of auxin in the formation of primary roots (Sabatini et al., 1999). diverse organs during Arabidopsis development. In each The activity of the DR5 reporter does not necessarily case, developmentally regulated changes in PIN polar reflect auxin levels in all cases because of its own sensi- localization redirect auxin fluxes to create local auxin tivity threshold and saturation of the auxin-signaling gradients required for the establishment of primordia pathway. Therefore, we examined whether DR5 can be and their development into mature organs. Our data used in lateral root primordia as a reporter of endoge- suggest that efflux-mediated auxin gradients represent nous auxin levels. The exogenously applied naturally a common module that operates in the formation of all occurring auxin IAA or its synthetic analog NAA (up to plant organs, regardless of their developmental origin 10 ␮M, 12 hr) increased the intensity of the DR5 signal and fate. in the primordia without changing its spatial pattern (data not shown) similar like it has been shown in the Results primary root (Friml et al., 2002a). In contrast, the same treatment with another auxin analog 2,4-D, which can Auxin and Auxin Response Gradients be only poorly transported by auxin efflux (Delbarre et in Lateral Root Primordia al., 1996) or metabolized, induced DR5 activity in all The synthetic auxin responsive promoters such as DR5 lateral root primordium cells (Figure 1C). In addition, (Ulmasov et al., 1997) have become useful tools for mon- inhibition of efflux by the phytotropin NPA interfered itoring auxin response in planta. It has been shown that with the auxin response gradient (Figure 1D). These data activity of these reporters correlates with auxin content demonstrate an active auxin efflux in lateral root primor- in roots (Casimiro et al., 2001). We examined auxin re- dia, which can handle exogenously applied auxin and sponse during lateral root formation using DR5::GUS in this manner maintain the endogenous auxin distribu- (Figure 1A) and DR5rev::PEH A, which gave identical tion. It also suggests that the spatially restricted signals results. DR5 activity was absent from the entire differen- in untreated roots reflect differences in auxin levels. To tiated root and was detected only within the pericycle obtain additional confirmation, the distribution of auxin in the presumptive founder cells of primordia (stage 0). itself was visualized using an anti-IAA antibody, which After the formation of short
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