Research Theme within School of Biosciences: Plant Genetics and Cell Biology
Targets and mechanisms involved in the self-incompatibility response in Papaver rhoeas pollen
Sexual reproduction in higher plants involves pollination, involving specific interactions between pollen and pistil. A key mechanism to prevent inbreeding is self-incompatibility (SI), which is a controlled by a single, multi-allelic S-locus. Incompatible ("self") pollen is rejected and compatible ("non-self") pollen is allowed to fertilize the plant.
My lab is investigating the signalling cascades, targets and mechanisms regulating pollen tube tip growth inhibition induced by SI in Papaver. The "self" interaction triggers a Ca2+-dependent signalling network, resulting in incompatible pollen tube tip growth being inhibited and programmed cell death being induced. Our long-term goal is to establish how the different components integrate and interact in what has turned out to be a complex signalling network. Currently research falls into several areas:
1. Investigations into programmed cell death in the SI response.
Programmed cell death (PCD) is an important mechanism responsible for the controlled death of targeted cells in animal and plant cells. We recently demonstrated that PCD is triggered in incompatible pollen. We have identified several caspase-like activities (a VEIDase and a LEVDase) that are activated by an incompatible SI response. We are currently investigating the early events involved in PCD in pollen further, and are investigating if reactive oxygen species (ROS) and nitric oxide (NO) are involved in the SI response in incompatible pollen.
2. Alterations in the actin cytoskeleton
In many cells alterations to the cytoskeleton are the first visible response to extracellular stimuli. We have shown that both the actin and microtubule cytoskeleton are important target for SI signals, and recently obtained evidence for crosstalk between actin and microtubules. In animal cells sustained actin depolymerization can stimulate apoptosis via caspases. We recently showed that actin depolymerization can trigger PCD in pollen. We are currently investigating signalling to the actin cytoskeleton further.
3. Cytosolic soluble inorganic pyrophosphatases are targets for SI signals
Soluble inorganic pyrophosphatases (sPPases) are enzymes that catalyse hydrolysis of inorganic pyrophosphate (PPi), to two inorganic phosphates (2Pi). Their activity is essential for making a wide variety of biosynthetic processes thermodynamically favourable. We established that a pollen sPPase is phosphorylated during the SI response. This represents the first report of a eukaryotic sPPase being phosphorylated and of regulation of its activity by phosphorylation. Our identification of sPPases as a target for the SI response implicates an additional mechanism utilized for SI-mediated inhibition of pollen tube growth. We are currently investigating the significance of the phosphorylation in a joint project with Dr Scott White.
4. Investigating a possible functional role for the pollen gene, PrpS, as the pollen of S-receptor.
This project is a collaborative project with Professor Chris Franklin. We recently identified the pollen S-locus determinant, named PrpS. We are currently investigating binding of the proposed pollen S-receptor with the pistil component, which will test our longstanding hypothesis that the pistil S protein interacts with the pollen S-locus determinant through a receptor-ligand interaction.
Initiating investigations into the nature of the pollen S determinant, PrpS as a receptor/ion channel, and its interaction with the PrsS ligand. This BBSRC-funded project is focusing on aspects of the receptor-ligand interaction and very early signaling events upstream of all the events so far characterised. (in collaboration with Christoph Baumann (York), Dale Sanders (JIC), Josh Rappoport and Steve Publicover (University of Birmimgham) (York), Dale Sanders (JIC), and (University of Birmimgham)
Pursuing possible commercial aspects of using SI, by investigating whether poppy SI can be transferred to other species. This follows on from filing a patent in November 2008, based on preliminary data that suggested that transferring the pollen S-determinant, PrpS1, to Arabidopsis allowed it to recognise poppy recombinant PrsS proteins resulting in the inhibition of PrpS1-GFP pollen germination. This is a very exciting opportunity, and LES College KT Development funding (£20,000) allowed us to pursue obtaining further data to consolidate the patent. Links have been made with PBL, who are currently marketing this application, which could be of immense value to plant breeders in the production of F1 hybrids.
Barend H. J. de Graaf, Sabina Vatovec, Javier Andrés Juárez-Díaz, Lijun Chai, Kreepa Kooblall, Katie A. Wilkins, Huawen Zou, F. Christopher H. Franklin and Vernonica E. Franklin-Tong. The Papaver self-incompatibility pollen S-determinant, PrpS, functions in Arabidopsis thaliana. Current Biology 22 (2), 154-159. doi:10.1016/j.cub.2011.12.006
Katie A. Wilkins, James Bancroft, Maurice Bosch, Jennifer Ings, Nicholas Smirnoff and Vernonica E. Franklin-Tong (2011). ROS and NO mediate actin reorganization and programmed cell death in the Self-Incompatibility response of Papaver. Plant Physiology 156, 404-416. DOI: 10.1104/pp.110.167510.
Smertenko, A. & Franklin-Tong, VE(2011). Organization & Regulation of the cytoskeleton in plant programmed cell death. Cell Death & Differentiation 18, 1263-1270. doi:10.1038/cdd.2011.39
Wouter G. van Doorn, Eric P. Beers, Jeffery L. Dangl, Vernonica E. Franklin-Tong, Hiroo Fukuda, Patrick Gallois, Jean Greenberg, Ikuko Hara-Nishimura, Alan M. Jones, Maki Kawai-Yamada, Eric Lam11, John Mundy12, Luis Mur, Morten Petersen, Andrei Smertenko, Michael Taliansky, Frank van Breusegem16, Thomas Wolpert, Ernst Woltering, Boris Zhivotovsky, Peter V. Bozhkov(2011). Morphological classification of plant cell deaths. Cell Death & Differentiation 18, 8, 1241-1246.doi:10.1038/cdd.2011.36
Noni Franklin-Tong (2011). Self-fertilization: article in: Brenner’s Encyclopedia of Genetics.
V.E. Franklin-Tong (ed.) Self-Incompatibility in Flowering Plants – Evolution, Diversity, and Mechanisms. Publ. Springer-Verlag Berlin Heidelberg 2008. This is the first monograph on this topic for 30 years.
Natalie S. Poulter, Maurice Bosch, &Vernonica E. Franklin-Tong (2011) Proteins implicated in mediating Self-Incompatibility-induced alterations to the actin cytoskeleton of Papaver pollen. Annals of Botany: doi:10.1093/aob/mcr022.
Juyou Wu, Su Wang, Yuchun Gu, Shaoling Zhang, Stephen J Publicover and V. E. Franklin-Tong (2011) Self-incompatibility in Papaver rhoeas activates non-specific cation conductance(s) permeable to Ca2+ and K+. Plant Physiology 155: 963-973.
Maurice Bosch, Natalie S. Poulter, Ruth M. Perry, Katie Wilkins and V. E. Franklin-Tong (2010). Characterization of a legumain/vacuolar processing enzyme and YVADase activity in Papaver pollen. Plant Molecular Biology 74 (4), 381-393. DOI: 10.1007/s11103-010-9681-9.
Natalie S. Poulter, Christopher J. Staiger, Joshua Z. Rappoport, and Vernonica E. Franklin-Tong (2010). Actin-Binding Proteins Implicated in the Formation of the Punctate Actin Foci Stimulated by the Self-Incompatibility Response in Papaver. Plant Physiol. 152: 1274-1283.
Wheeler, M.J., de Graaf, B.H.J., Hadjiosif, N.E., Perry, R.M., Poulter, N.S., Osman, K., Vatovec, S., Harper, A., Franklin, F.C.H & Franklin-Tong, V.E. (2009). Identification of the pollen self-incompatibility determinant in Papaver rhoeas. Nature 459, 992-995.
Poulter, N. S., Vatovec, S. and Franklin-Tong VE. (2008). Microtubules Are a Target for Self-Incompatibility Signaling in Papaver Pollen. Plant Physiol. 146, 1358-1367.
Bosch M. & Franklin-Tong VE. (2007). Temporal and spatial activation of caspase-like enzymes induced by self-incompatibility in Papaver pollen. Proc. Natl. Acad. Sci. USA. 104 (46) 18327-18332.
S. Li, J. Samaj & V. E. Franklin-Tong. (2007). A MAP kinase signals to Programmed Cell Death induced by Self-Incompatibility in Papaver pollen. Plant Physiol 145, 236-245.
B.H.J. de Graaf, J.J. Rudd, M. J. Wheeler, R.M. Perry, E. M. Bell, K. Osman, F. C.H. Franklin & V. E. Franklin-Tong (2006). Self-incompatibility in Papaver targets soluble inorganic pyrophosphatases in pollen. Nature 444, 490-493. Selected for "Editor’s Choice" in Nature.
Thomas, S. Huang , S. Li, C.J. Staiger and V.E. Franklin-Tong. (2006). Actin depolymerization is sufficient to induce programmed cell death in self-incompatible pollen. S.G. Journal of Cell Biology 174, 221-229. This article was selected for a highlight JCB "In This Issue" section and by Cell in a "Leading Edge"; Aug 11th 2006 issue of Cell).
Huang, S., Blanchoin, L., Chaudhry, F., Franklin-Tong, V.E. and Staiger, C.J. (2004) A gelsolin-like protein from Papaver rhoeas pollen (PrABP80) stimulates calcium-regulated severing and depolymerization of actin filaments. Journal of Biological Chemistry 279, 23364-23375.
Thomas, S.G. & Franklin-Tong, VE. (2004) Programmed Cell Death is triggered by self-incompatibility in Papaver pollen. Nature 429, 305-309.