School of Biosciences
Emeritus Professor of Plant Cell Biology
- School of Biosciences
University of Birmingham
Noni Franklin-Tong’s research focuses on the cellular mechanisms involved in the model cell-cell recognition system of self-incompatibility (SI) in Papaver rhoeas (the Field Poppy). She is recognized at an international level for her work elucidating the cellular mechanisms responsible for regulating the rejection of “self” 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. SI was discovered by Darwin and plays a decisive role in determining plant reproductive success by preventing inbreeding. Regulation of pollination has high importance in relation to its impact on food security.
Noni initiated pioneering research of SI in Papaver rhoeas. Her development of an in vitro bioassay in the 1980s allowed investigation of the cell biology of SI for the first time. This model system enabled elucidation of the signals, targets and cellular mechanisms responsible for regulating the rejection of “self” incompatible pollen. Her research has uncovered an intricate intracellular signalling network triggered by a highly specific cell-cell interaction starting with tip growth inhibition and culminating in programmed cell death. Research continues in collaboration with various labs in the UK and internationally.
BSc (Hons) Biological Sciences (University of Birmingham) 1982
PhD Department of Genetics (University of Birmingham) 1986
Vernonica (Noni) Franklin-Tong was born in London, U.K. Noni was educated at a comprehensive school in Suffolk and then at the University of Birmingham. She received her BSc in Biological Sciences (1982) and PhD in Genetics (1986) from the University of Birmingham.
Most of her career has been based at Birmingham, though she has worked for brief periods of time in Umeå, Sweden, ICMB, University of Edinburgh and UMass, Amherst, USA. She obtained a BBSRC Advanced Research Fellowship in 1992, was appointed to a lectureship in 1997, and a Chair in Plant Cell Biology (2004-2014). Following breast cancer she is partially retired, working part-time research-only (2014-).
She was elected as a Fellow of the Royal Society (FRS) in 2021.
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. The ability to discriminate between self and non-self, is widespread in eukaryotes (e.g. in the immune response in animals and disease resistance and SI in plants). Flowering plants use complex pollen-pistil interactions to play a decisive role in determining reproductive success. A key mechanism to prevent inbreeding is self-incompatibility (SI), which is critical to prevent potentially deleterious inbreeding. SI is regulated by a polymorphic multi-allelic S-locus, comprising tissue-specific expressed pollen and pistil S-determinants which define mating types; this sophisticated allorecognition system prevents self-fertilization. Incompatible ("self") pollen is rejected and compatible ("non-self") pollen is allowed to fertilize the plant.
My research has primarily focused on investigating the signalling networks, targets and mechanisms regulating SI in Papaver. Major findings included identifying a signalling role for cytosolic free Ca2+ in the inhibition of incompatible Papaver pollen tube growth triggered by SI. Subsequent studies showed that the "self" interaction triggers a Ca2+-dependent signalling network resulting in programmed cell death (PCD), a cellular suicide that is universally used by eukaryotes to regulate development, stress and defence. This identified a new mechanism for SI, revealing a neat, targetted way to eliminate unwanted pollen grains. SI-induced caspase-like activities that are active only under acidic conditions were identified and cytosolic acidification was established as being critical for execution of SI-PCD in incompatible pollen. Identification of dramatic changes to F-actin organization in incompatible pollen tubes established a pivotal role for SI-induced actin remodelling that influences progression into PCD. Reactive oxygen species (ROS) are also involved in regulating SI-induced PCD. Another major finding was the identification of phosphorylation of a soluble inorganic pyrophosphatase (sPPase). Showing that this inhibits PPase activity identified a new regulatory mechanism for SI-mediated inhibition of pollen tube growth and established a new paradigm for the regulation of eukaryotic sPPases. A subsequent study established that phospho-regulation of key sites can inhibit the catalytic responsiveness of these proteins in concert with key intracellular events. As sPPases are essential for many biosynthetic pathways, phosphorylation may represent a potential master regulatory mechanism that could be used to attenuate metabolism.
Identification of the pistil and pollen S-determinants is a major goal of most SI researchers because they hold the key to how SI is specified. The diversity and distribution of SI systems suggest that SI evolved independently several times. Identification of the Papaver S-determinants: PrsS and PrpS, confirmed this. PrsS is a member of a large family of small cysteine-rich proteins; PrpS is a novel small transmembrane protein. Work is ongoing to learn more about their nature and how they interact and operate.
Because SI has huge applied potential to produce F1 hybrids, transferring a SI system between species has been the elusive ambition of plant breeders. For this reason, most researchers work on SI in crop species. Despite this, the poppy S-determinants were used to make the first functional trans-genera transfer of a SI system. As hallmark features of Papaver SI were exhibited in Arabidopsis, it suggests that common, endogenous signalling components are recruited to elicit this response, raising questions about the evolution and functional diversification of these signalling networks. Subsequently, co-expression of PrsS and PrpS-GFP in A. thaliana was shown to result in SI in vivo. This landmark study showed that these two Papaver S-determinants can act as a functional synthetic S-locus in a highly divergent self-compatible species. This breakthrough has huge implications for translational work, as it was thought that functional transfer of S-determinants to distant species was impossible. Longer-term it is hoped that the Papaver S-determinants can be used to aid F1 hybrid plant breeding.
I continue to explore the targets and mechanisms involved in regulating the self-incompatibility (SI) and the cellular responses in Papaver rhoeas (the field poppy) in collaboration with Dr Maurice Bosch (IBERS) , Prof Moritz Nowack(VIB, Gent), Dr Zongcheng Lin (VIB, Gent) and Prof. Nick Smirnoff (Exeter). The long-term goal is to understand the mechanisms involved and to establish how the different components integrate and interact in what has turned out to be a complex signalling network.
Current research includes:
Elucidating the role of ROS in mediating SI-induced PCD
SI triggers increases in reactive oxygen species (ROS) and nitric oxide (NO) during SI-PCD. In collaboration with Dr Maurice Bosch (IBERS) and Prof Nick Smirnoff (University of Exeter) analysis of incompatible pollen using a mass spectrometry approach recently identified that SI-induced ROS are responsible for predominantly irreversible oxidative modifications of pollen proteins, which have hardly been reported to date in plants. In animal cells irreversible oxidation triggers apoptosis and cell death. Current research aims to establish how oxidation functionally alters key pollen proteins, how this affects metabolism and results in PCD as well as identifying the source(s) of ROS.
The functionality of Papaver S-determinants in heterologous systems
In collaboration with Dr Maurice Bosch (IBERS) and Prof Moritz Nowack (VIB, Gent) and Dr Zongcheng Lin (VIB, Gent) further mechanistic components involved in regulating the inhibition of incompatible pollen as well as the nature of the PrsS -PrpS “receptor-ligand” interaction are being investigated. This team recently showed that the poppy PrpS functions when ectopically expressed in vegetative tissues of Arabidopsis thaliana. Excitingly, this demonstrates that these genes can function outside of their usual reproductive situation.
In collaboration with Dr Maurice Bosch (IBERS) and Prof Lijun Chai (Huazhong Agricultural University, Wuhan), we are exploring transferring the poppy S-determinants to Citrus, an economically important crop.
Noni was Secretary General for the International Association of Sexual Plant Reproduction Research (IASPRR) 2010-13. She has served on BBSRC Research Council Committee (2007-10) and the Society for Experimental Biology (SEB) Plant Biology Committee (1998-2011) and Council (2002-6). She has acted as an evaluator for the Newton Prize (UK National Commission for UNESCO) 2017-. She is currently on the Editorial Board of Plant Reproduction (2006-). She is a member of the External Review Panel for the UKRI-BBSRC Norwich Research Park Biosciences Doctoral Training Partnership (2021-).
Noni has a long-term commitment to enthusing children about science education and has been involved in providing the general public with a broader understanding of science through a number of activities. She was one of the original BBSRC Regional Coordinators of the Schools Liaison Scheme.
As a BAME female professor, she strives to be a role model for equality and diversity.
Lin, Z, Xie, F, Triviño, M, Karimi, M, Bosch, M, Franklin-Tong, VE & Nowack, MK 2020, 'Ectopic Expression of a Self-Incompatibility Module Triggers Growth Arrest and Cell Death in Vegetative Cells', Plant Physiology, vol. 183, no. 4, pp. 1765-1779. https://doi.org/10.1104/pp.20.00292
Liang, M, Cao, Z, Zhu, A, Liu, Y, Tao, M, Yang, H, Xu, Q, Wang, S, Liu, J, Li, Y, Chen, C, Xie, Z, Deng, C, Ye, J, Guo, W, Xia, R, Larkin, RM, Deng, X, Bosch, M, Franklin-Tong, VE & Chai, L 2020, 'Evolution of self-compatibility by a mutant Sm-RNase in citrus', Nature Plants, vol. 6, no. 2, pp. 131-142. https://doi.org/10.1038/s41477-020-0597-3
Wang, L, Triviño, M, Lin, Z, Carli, J, Eaves, DJ, Van Damme, D, Nowack, MK, Franklin-Tong, VE & Bosch, M 2020, 'New opportunities and insights into Papaver self-incompatibility by imaging engineered Arabidopsis pollen', Journal of Experimental Botany, vol. 71, no. 8, pp. 2451-2463. https://doi.org/10.1093/jxb/eraa092
Haque, T, Eaves, DJ, Lin, Z, Zampronio, CG, Cooper, HJ, Bosch, M, Smirnoff, N & Franklin-tong, VE 2020, 'Self-Incompatibility Triggers Irreversible Oxidative Modification of Proteins in Incompatible Pollen', Plant Physiology, vol. 183, no. 3, pp. 1391-1404. https://doi.org/10.1104/pp.20.00066
Zhao, W, Qu, X, Zhuang, Y, Wang, L, Bosch, M, Franklin-tong, VE, Xue, Y & Huang, S 2020, 'Villin controls the formation and enlargement of punctate actin foci in pollen tubes', Journal of Cell Science, vol. 133, no. 6, jcs237404. https://doi.org/10.1242/jcs.237404
Eaves, DJ, Haque, T, Tudor, RL, Barron, Y, Zampronio, CG, Cotton, NPJ, de Graaf, BHJ, White, SA, Cooper, H, Franklin, FCH, Harper, JF & Franklin-Tong, VE 2017, 'Identification of Phosphorylation Sites Altering Pollen Soluble Inorganic Pyrophosphatase Activity', Plant Physiology, vol. 173, no. 3, pp. 1606-1616. https://doi.org/10.1104/pp.16.01450
Chai, L, Tudor, RL, Poulter, NS, Wilkins, KA, Eaves, DJ, Franklin, FCH & Franklin-tong, VE 2017, 'MAP Kinase PrMPK9-1 Contributes to the Self-Incompatibility Response', Plant Physiology, vol. 174, no. 2, pp. 1226-1237. https://doi.org/10.1104/pp.17.00213
Wilkins, KA, Bosch, M, Haque, T, Teng, N, Poulter, NS & Franklin-tong, VE 2015, 'Self-incompatibility-induced programmed cell death in field poppy pollen involves dramatic acidification of the incompatible pollen tube cytosol', Plant Physiology, vol. 167, no. 3, pp. 766-779. https://doi.org/10.1104/pp.114.252742
Lin, Z, Eaves, DJ, Sanchez-Moran, E, Franklin, FCH & Franklin-Tong, VE 2015, 'The Papaver rhoeas S determinants confer self-incompatibility to Arabidopsis thaliana in planta', Science, vol. 350, no. 6261, pp. 684-687. https://doi.org/10.1126/science.aad2983
Eaves, DJ, Flores-Ortiz, C, Haque, T, Lin, Z, Teng, N & Franklin-Tong, VE 2014, 'Self-incompatibility in Papaver: advances in integrating the signalling network', Biochemical Society Transactions, vol. 42, no. 2, pp. 370-376. https://doi.org/10.1042/BST20130248
Dresselhaus, T & Franklin-Tong, V 2013, 'Male-female crosstalk during pollen germination, tube growth and guidance, and double fertilization', Molecular Plant, vol. 6, no. 4, pp. 1018-36. https://doi.org/10.1093/mp/sst061
de Graaf, BH, Vatovec, S, Juárez-Díaz, JA, Chai, L, Kooblall, K, Wilkins, K, Zou, H, Forbes, T, Franklin, F & Franklin Tong, V 2012, 'The Papaver Self-Incompatibility Pollen S-Determinant, PrpS, Functions in Arabidopsis thaliana', Current Biology, vol. 22, no. 2, pp. 154-159. https://doi.org/10.1016/j.cub.2011.12.006
van Doorn, WG, Beers, EP, Dangl, JL, Franklin-Tong, VE, Gallois, P, Hara-Nishimura, I, Jones, AM, Kawai-Yamada, M, Lam, E, Mundy, J, Mur, LAJ, Petersen, M, Smertenko, A, Taliansky, M, Van Breusegem, F, Wolpert, T, Woltering, E, Zhivotovsky, B & Bozhkov, PV 2011, 'Morphological classification of plant cell deaths', Cell Death & Differentiation , vol. 18, no. 8, pp. 1241-1246. https://doi.org/10.1038/cdd.2011.36
Li, S, Franklin Tong, V, Dissmeyer, N & Schnittger, A 2011, Modulating and Monitoring MAPK Activity During Programmed Cell Death in Pollen. in Methods in Molecular Biology: Plant Kinases. vol. 779.
Smertenko, A & Franklin Tong, V 2011, 'Organisation and regulation of the cytoskeleton in plant programmed cell death', Cell Death & Differentiation , vol. 18, no. 8, pp. 1263-1270. https://doi.org/10.1038/cdd.2011.39
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