ScienceWeek

CELL BIOLOGY: ON ETHYLENE SIGNALING IN PLANTS

The following points are made by J.M. Alonso and A.N. Stepanova (Science 2004 306:1513):

1) Several signaling molecules with hormone-like functions have been identified in plants, the simplest of all being ethylene. Despite its structural simplicity, this gaseous hormone plays a critical role in the regulation of developmental programs throughout the plant life cycle and serves as a major response mediator to various environmental signals [1-3]. Seed germination, cell elongation, fertilization, fruit ripening, seed dispersal, defense against pathogens, and response to external stress factors are among the essential processes regulated by ethylene [2,4]. A combination of genetic, biochemical, and molecular approaches is uncovering this remarkable signaling pathway in plants [5]. Although the initial hunt for the major elements of the ethylene pathway was performed in the model plant Arabidopsis thaliana, identification and functional analysis of the corresponding genes in other plant species uncovered a high degree of conservation of this signaling cascade in the plant kingdom.

2) The first prerequisite for any signaling molecule to be functional is the existence of a detection system to precisely monitor its levels. The specific recognition of ethylene by a receptor protein presents uncommon challenges because of the extreme structural simplicity of this hormone and the consequent small number of possible interaction points between the signal molecule and its receptor. In plants, this challenge is met by a family of endoplasmic reticulum (ER)-localized ethylene receptors that share sequence similarity with the bacterial two-component histidine kinases. The particular physicochemical properties of the ethylene gas allow it to freely diffuse through the membranes and the cytoplasm, eliminating the need for an active transporter system to deliver the ligand to its receptors in the ER.

3) The required high binding affinity and specificity of the ethylene receptors is achieved with the help of a copper cofactor associated with the hydrophobic ligand-binding pocket of the receptor molecule. Mutations in the hydrophobic domain of any of the five Arabidopsis receptors -- ETR1, ETR2, EIN4, ERS1, and ERS2 -- result in dominant ethylene insensitivity of the corresponding mutant plants. Some of these mutations abolish ethylene binding, which suggests that in the absence of the hormone, the receptors actively repress the ethylene response. Conclusive evidence for the negative regulatory role of the receptors was obtained from the analysis of loss-of-function mutants. Lack of phenotypes in the single loss-of-function receptor mutants indicated a high degree of functional redundancy among the receptors, whereas the constitutive activation of the ethylene response in double, triple, and quadruple loss-of-function mutants confirmed the role of the receptors as repressors of this signaling pathway.

4) In summary: Plants use a structurally very simple gas molecule, the hydrocarbon ethylene, to modulate various developmental programs and coordinate responses to a multitude of external stress factors. How this simple molecule generates such a diverse array of effects has been the subject of intense research for the past two decades. A fascinating signaling pathway, with classical as well as novel plant-specific signaling elements, is emerging from these studies. Four main modules constitute this signaling pathway: a phosphotransfer relay, an EIN2-based unit, a ubiquitin-mediated protein degradation component, and a transcriptional cascade. The canonical and Arabidopsis ethylene signaling pathways elucidated by research provide a complete panoramic view of these signaling events in plants.

References (abridged):

1. F. Abeles, P. Morgan, M. Saltveit, Ethylene in Plant Biology (Academic Press, San Diego, CA, 1992)

2. P. R. Johnson, J. R. Ecker, Annu. Rev. Genet. 32, 227 (1998)

3. A. Mattoo, J. Suttle, The Plant Hormone Ethylene (CRC Press, Boca Raton, FL, 1991)

4. K. L. Wang, H. Li, J. R. Ecker, Plant Cell 14 (suppl.), S131 (2002)

5. H. Guo, J. R. Ecker, Curr. Opin. Plant Biol. 7, 40 (2004)

Science http://www.sciencemag.org

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Related Material:

PLANT BIOLOGY: AUXIN AND THE APICAL-BASAL AXIS

The following points are made by Jiri Friml et al (Nature 2003 426:147):

1) The development of higher eukaryotes includes the generation of a species-specific body plan. As a first step, a multicellular organization is established from a single-celled zygote during embryogenesis, with cells adopting specific fates according to their relative positions. In Drosophila, maternal organizers initiate a cascade of spatially restricted transcription factors that partitions the anterior posterior axis of the embryo(1). In Caenorhabditis elegans, sperm entry triggers anterior posterior axis specification, initiating a series of asymmetric cell divisions that establish founder cells with different fate potential(2).

2) In plants, the mature embryo displays a main axis of polarity, with the shoot meristem flanked by the cotyledons (embryonic leaves) at the top end and separated by hypocotyl (embryonic stem) and root from the root meristem at the opposite pole. The origin of this apical basal pattern, which is remarkably uniform across flowering plant species, has been traced back to early embryogenesis in Arabidopsis(3). The zygotic division generates a smaller apical and a larger basal cell. The apical cell divides vertically and eventually gives rise to all apical embryo structures. The basal cell continues to divide horizontally and produces the suspensor, which connects the embryo with the maternal tissue(3). The uppermost suspensor cell is subsequently recruited by the embryo and specified to become the hypophysis --the founder of the root meristem. At the triangular stage, the apical pole of the embryo is organized with the initiation of two symmetrically positioned cotyledons.

3) Several indirect lines of evidence implicated the plant hormone auxin (indole-3-acetic acid, IAA) in embryo development. Embryo patterning mutants, such as monopteros (mp), bodenlos (bdl) or gnom (gn) (4,5), lack basal structures and display variably fused cotyledons. Molecular analysis of these mutants has revealed that MP and BDL encode the transcriptional activator auxin response factor 5 (ARF5) and the corresponding transcriptional repressor IAA12, respectively, both of which are involved in auxin response, and that GN encodes a regulator of vesicle trafficking that mediates the subcellular targeting of auxin-transport components. For later development, chemical manipulation of auxin distribution has suggested a link between patterning and auxin transport. Moreover, in wheat and carrot later-stage embryos, auxin has been detected using a microscale technique.

4) In summary: Axis formation occurs in plants, as in animals, during early embryogenesis. However, the underlying mechanism is not known. The authors demonstrate that the first manifestation of the apical basal axis in plants, the asymmetric division of the zygote, produces a basal cell that transports and an apical cell that responds to the signalling molecule auxin. This apical basal auxin activity gradient triggers the specification of apical embryo structures and is actively maintained by a novel component of auxin efflux, PIN7, which is located apically in the basal cell. Later, the developmentally regulated reversal of PIN7 and onset of PIN1 polar localization reorganize the auxin gradient for specification of the basal root pole. An analysis of pin quadruple mutants identifies PIN-dependent transport as an essential part of the mechanism for embryo axis formation. The authors suggest their results indicate how the establishment of cell polarity, polar auxin efflux, and local auxin response result in apical basal axis formation of the embryo, and thus determine the axiality of the adult plant.

References (abridged):

1. St Johnston, D. & Nüsslein-Volhard, C. The origin of pattern and polarity in the Drosophila embryo. Cell 68, 201-219 (1992)

2. Lyczak, R., Gomes, J. & Bowerman, B. Heads or tails: cell polarity and axis formation in the early Caenorhabditis elegans embryo. Dev. Cell 3, 157-166 (2002)

3. Jürgens, G. Apical-basal pattern formation in Arabidopsis embryogenesis. EMBO J. 20, 3609-3616 (2001)

4. Mayer, U., Torres Ruiz, R. A., Berleth, T., Misera, S. & Jürgens, G. Mutations affecting body organization in the Arabidopsis embryo. Nature 353, 402-407 (1991)

5. Hamann, T., Mayer, U. & Jürgens, G. The auxin-insensitive bodenlos mutation affects primary root formation and apical-basal patterning in the Arabidopsis embryo. Development 126, 1387-1395 (1999)

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