Research Article: The AUXIN BINDING PROTEIN 1 Is Required for Differential Auxin Responses Mediating Root Growth

Date Published: September 24, 2009

Publisher: Public Library of Science

Author(s): Alexandre Tromas, Nils Braun, Philippe Muller, Tatyana Khodus, Ivan A. Paponov, Klaus Palme, Karin Ljung, Ji-Young Lee, Philip Benfey, James A. H. Murray, Ben Scheres, Catherine Perrot-Rechenmann, Edward Newbigin.

Abstract: In plants, the phytohormone auxin is a crucial regulator sustaining growth and development. At the cellular level, auxin is interpreted differentially in a tissue- and dose-dependent manner. Mechanisms of auxin signalling are partially unknown and the contribution of the AUXIN BINDING PROTEIN 1 (ABP1) as an auxin receptor is still a matter of debate.

Partial Text: The plant hormone auxin plays crucial roles in plant development. While one F-box protein mediated signal transduction route has been discovered, mechanisms of auxin signalling are still partially unknown. Effects of differential accumulation of auxin have been closely analyzed in Arabidopsis roots, where auxin mediates stem cell specification, maintenance of the root meristem, patterning and growth. At the cellular level, auxin is interpreted differentially in a tissue- and dose-dependent manner. Auxin concentrations that promote cell expansion in shoot tissues inhibit cell elongation and promote cell division in roots suggesting that in addition to the importance of auxin distribution and local auxin concentration, differences of cell responsiveness also play critical roles. In the presence of auxin, Aux/IAA transcriptional repressor proteins are recruited by the F-box protein TIR1 within the SCFTIR1 complex, polyubiquitinylated and degraded via the 26S proteasome [1], [2]. TIR1 binds auxin and acts as an auxin receptor mediating rapid Aux/IAA protein degradation and subsequent Auxin Response Factor (ARF)-dependent activation of transcription [3], [4], [5]. Auxin responses, however, involve another putative auxin receptor, the AUXIN BINDING PROTEIN1 (ABP1) [6]. This protein was isolated based on its capacity to bind auxin and is involved in a set of early auxin responses such as rapid activation of ion fluxes at the plasma membrane [6]. Previous efforts to characterize ABP1’s role during plant development have been hampered by the embryo-lethality of the null abp1 mutant in Arabidopsis [7]. Developmental map of gene expression in Arabidopsis revealed that ABP1 (At4g02980) exhibit a fairly constant expression in almost all tissues throughout vegetative plant development suggesting that its role is not restricted to embryo development (supporting figure S1) [8], [9]. Using conditional ABP1 Arabidopsis lines, we recently showed that ABP1 is required for post-embryonic shoot development acting on various cellular responses in a context-dependent manner [10]. It remains, however, unknown whether auxin is required for ABP1-driven downstream responses and what is ABP1’s role in plant root growth.

Our data show that ABP1 is implicated to various degrees in the control of auxin responses mediating root growth, especially cell division, cell elongation, and gene expression. ABP1 is essential to maintain the mitotic activity of meristematic cells and stem cells (Figures 2,3). This critical control of cell division in roots confirms previous data obtained on BY2 cell suspension [27], embryo [7] and shoot tissues [10] and reveals the general nature of the control exerted by ABP1 on cell division. Interestingly, this effect is consistent with auxin’s permissive role in cell division. Based on analysis of root stem cells, ABP1 affects the D-type CYCLIN/RBR regulatory pathway (Figure 3). Although the molecular link between ABP1 and these cell cycle regulators may not be direct, it is clear that ABP1 is essential for the regulation of the G1/S transition. Within the CYCLIN D/RBR pathway there are multiple potential targets, amongst which CDK inhibitors (KRPs) and E2F transcriptional factors are additional relevant targets. For example, E2Fc has been reported to negatively affect cell division [28] and we cannot exclude that the increased accumulation of E2Fc mRNAs in ABP1 inactivated seedlings also contributes to the inhibition of cell division. Overproduction of E2Fc was shown to inhibit cell proliferation [28], [29]. The E2Fc protein is however submitted to rapid degradation in an ubiquitin dependent manner and changes at the RNA level might not reflect the amount of protein. Protein turnover of E2Fc, as well as activator E2Fb which has been shown to be stabilised in response to auxin in BY2 cells [30], will merit investigation in plants inactivated for ABP1.

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