Cross-talk in plant hormone signalling: what Arabidopsis mutants are telling us

Abstract

Genetic screens have been extremely useful in identifying genes involved in hormone signal transduction. However, although these screens were originally designed to identify specific components involved in early hormone signalling, mutations in these genes often confer changes in sensitivity to more than one hormone at the whole-plant level. Moreover, a variety of hormone response genes has been identified through screens that were originally designed to uncover regulators of sugar metabolism. Together, these facts indicate that the linear representation of the hormone signalling pathways controlling a specific aspect of plant growth and development is not sufficient, and that hormones interact with each other and with a variety of developmental and metabolic signals. Following the advent of arabidopsis molecular genetics we are beginning to understand some of the mechanisms by which a hormone is transduced into a cellular response. In this Botanical Briefing we review a subset of genes in arabidopsis that influence hormonal cross-talk, with emphasis on the gibberellin, abscisic acid and ethylene pathways. In some cases it appears that modulation of hormone sensitivity can cause changes in the synthesis of an unrelated hormone, while in other cases a hormone response gene defines a node of interaction between two response pathways. It also appears that a variety of hormones may converge to regulate the turnover of important regulators involved in growth and development. Examples are cited of the recent use of suppressor and enhancer analysis to identify new nodes of interaction between these pathways.

Fig. 1. Three hormone signalling pathways as defined by genetic and molecular analysis. A, In the absence of ethylene the family of ethylene receptors (ETR1, ETR2, ERS1, ERS2, EIN4) activates CTR1, which in turn represses the positive membrane protein regulator EIN2. Addition of ethylene inactivates the ethylene receptors resulting in inactivation of CTR1 thereby releasing EIN2 to activate EIN3. The EIN3 transcription factor binds to regulatory sequences in the promoter of ethylene‐regulated genes inducing transcription. B, A receptor for ABA has not been defined. However, genetically downstream of ABA reception, dephosphorylation (ABI1/2), protein farnesylation (ERA1) and RNA processing (ABH1) are all required to attenuate the ABA signal. At the bottom of the pathway three transcription factors (ABI3, ABI4, ABI5) are responsible for at least seed sensitivity to ABA. C, The receptor for GA has not been defined. However, in the absence of GA a family of transcription factors (GAI, RGA, RGL1 and RGL2) inhibits various GA‐mediated responses. Through unknown mechanisms, GA antagonizes these proteins resulting in expression of GA‐regulated genes. SLY1 and SPY are also thought to regulate these transcriptional repressors. Green molecules indicate transcription factors, blue molecules indicate signalling intermediates, and yellow molecules represent receptors. Arrows represent positive regulation and bars represent negative regulation.

Fig. 2. Hormone signalling can be regulated by the turnover of signalling components. The SCF‐complex is composed of four subunits (CUL1, ASK1, RBX1 and an F‐box protein). The cullin (CUL1) requires RUB modification mediated by AXR1‐ECR1 for normal activity of the complex. By interacting with specific substrates the F‐box proteins confer specificity to the degradation machinery. Loss‐of‐function mutations in the genes encoding the F‐box proteins TIR1, COI1 and SLY1 confer impaired sensitivity only to a single hormone, in this case auxin, JA and GA, respectively. In contrast, mutations in the ARX1 gene, which encodes the activating enzyme of the RUB complex, affect a variety of hormone responses such as auxin, JA and ABA. In the example shown, the AUX/IAA proteins associate with the TIR1 F‐box protein allowing them to be ubiquitinated by the SCF complex. This targets the AUX/IAA proteins for degradation. The removal of these proteins allows dimerization of ARF transcription factors allowing transcription of auxin response genes. JA signalling follows a similar mechanism, except that the F‐box protein is COI1.

Fig. 3. Hormone signalling as described by genetic interaction. Using the sensitized genetic backgrounds of era1 (increased sensitivity to ABA) and abi1 (decreased sensitivity to ABA) as a starting point, second site suppressor and enhancer mutations were identified. Lines connect second site mutations to the original mutation that was being suppressed or enhanced. Screens used seed germination as the assay for ABA sensitivity. Blue molecules represent known ABA‐response genes, green molecules represent known GA‐response genes and yellow molecules represent known ethylene response genes.