Conservation and Innovation in Plant Signaling Pathways

Horticultural Sciences Department duced proteins in plants. Dominant mutations in the IAA University of Florida domain that confer insensitivity to auxin also strongly Gainesville, Florida 32611 inhibit turnover of IAA proteins (Worley et al., 2000). †The Howard Hughes Medical Institute Protein–protein interactions mediated by the IAA doThe Salk Institute for Biological Studies mains are proposed to modify activity of the ARF (auxin La Jolla, California 92037 response factor) transcription factors bound to auxin response elements (AXRE) of auxin induced genes (Ulmasov et al., 1999). Phytochrome, the photoreceptor for red and far-red Introduction light responses, exists in two photo-interconvertible As nature’s second grand experiment in complex develforms (Figure 1 and below). Phytochrome is a red-lightopment, vascular plants have strategic importance to activated serine/threonine kinase (Yeh and Lagarias, our understanding of the mechanisms and evolution of 1998; Fankhauser et al., 1999). Five isoforms of phytosignal transduction pathways. At least a billion years chrome (A, B, C, D, and E) that have different physiologihave passed since plants, animals, and fungi diverged at cal functions have been identified in Arabidopsis. Upon the base of the eukaryotic crown (Doolittle et al., 1996). stimulation with red light, phytochrome moves from the While it is unclear whether multicellularity evolved indecytosol to the nucleus. The different isoforms of phytopendently in plant and animal lineages, these phyla have chrome are translocated to the nucleus with different at the very least undergone major independent changes kinetics. One identified substrate of the PHYA kinase, in structure and organization. The emergence of comPKS1, is localized in the cytosol, where it acts as a plete genome sequences from strategic eukaryotic negative regulator of phytochrome signaling (Fankmodels and recent advances in the molecular analysis hauser et al., 1999). Nuclear-localized PHYB interacts of plant signaling pathways allow comparative analysis specifically with PIF3 (PHYTOCHROME INTERACTING of the signal transduction pathways in plants and aniFACTOR), a helix-loop-helix transcription factor that mals. The results offer new insight into the nature and binds a light response element upstream of one class complexity of signaling pathways that were present in of light regulated genes (Martinez-Garcia, 2000). Thus, a common ancestor. Moreover, we can begin to discern phytochrome signaling involves both nuclear and cytothe sources of novelty and innovation that differentiate solic interactions. the plant and animal lineages particularly with respect Key components of the ethylene signal transducto development. In this review, we pay particular attention pathway (reviewed by Johnson and Ecker, 1998) tion to origins of novelty in the evolution of signaling include ETR1 (ETHYLENE TRIPLE RESPONSE-1), the pathways in plants. ethylene receptor; CTR1 (CONSTITUTIVE ETHYLENE REThe three important signal transduction pathways deSPONSE-1), a raf-like protein kinase; EIN2 (ETHYLENE picted in Figure 1 illustrate an intermingling of conserved INSENSITIVE-2), a membrane protein related to mamand novel mechanisms that is typical of plant signal malian NRAMP proteins; and EIN3 (ETHYLENE INSENSItransduction pathways. Auxin (indole acetic acid) signalTIVE-3), a novel transcription factor. In the absence of ing, a central pathway of plant development, is mediated ethylene, ETR1 and related receptors actively inhibit the by a highly conserved ubiquitin ligase complex (del Pozo ethylene response (Hua and Meyerowitz, 1998). The inet al., 1998; Gray et al., 1999). The pathway is defined hibitory action of ETR1 requires the CTR1 kinase. Hence, by the AXR (AUXIN RESISTANT) and TIR (AUXIN ethylene binding to ETR1 is proposed to cause inactivaTRANSPORT INHIBITOR RESISTANT) mutants of A. tion of CTR. Inactivation of CTR1 potentiates signaling thaliana. AXR1 and a partner protein, ECR1, comprise mediated by the C-terminal cytoplasmic domain of EIN2 a RUB (related to ubiquitin)-activating enzyme analo(Alonso et al., 1999). EIN2 signaling leads to activation gous to E1 of the ubiquitin pathway (del Pozo et al., of the EIN3 transcription factor in the nucleus. EIN3 is 1998). These proteins together with a RUB-conjugating a direct activator of the ETHYLENE RESPONSE FACTOR enzyme, RCE1, RUB-modify AtCUL, a cullin homolog (ERF) genes. ERF transcription factors in turn bind to (del Pozo and Estelle, 1999). AtCUL is a component of ethylene response elements of downstream ethylene an SCF (SKP-cullin-F-box) ubiquitin ligase complex that induced genes. includes TIR1, the F-box protein, and ASK1, a homolog In order to understand the forces that have shaped of yeast SKP1 (Gray et al., 1999). Mutations in TIR1 and the evolution of these and other signaling pathways, it ASK1 inhibit the auxin response, suggesting that the is useful to place them in the broader context of plant SCFTIR1 complex regulates turnover of a repressor. biology. Plant evolution clearly has taken a very different Possible downstream targets of the SCFTIR1 complex course under a very different set of constraints than include IAA domain proteins such as those defined by animal evolution. Among the more obvious features are photoautotrophic growth, absence of mobility, and the presence of a semirigid cell wall. The capture and assim‡ To whom correspondence should be addressed (e-mail: drm@