Petra Boevink
Current research interests
The focus of my research is the cell biology of plant-pathogen interactions, in particular between the notorious oomycete pathogen Phytophthora infestans, the causal agent of the devastating potato late blight, and its hosts. This pathogen manipulates plant defence responses on multiple levels, suggesting complex exchanges of signals between host and pathogen. I work closely with Paul Birch (of Dundee University Plant Sciences, based at the James Hutton Institute) and Steve Whisson and other members of the strong Phytophthora team in Dundee and we are part of the Dundee Effector Consortium which encourages collaboration and exchange between teams working on different pathogen/pest-plant interactions.
P. infestans is a hemi-biotroph and the biotrophic phase of growth is essential for infection. It represents a point of vulnerability and is the stage at which the pathogen must exert the most control over the host defences. To do this the pathogen secretes a broad range of pathogenicity factors, referred to as effectors, many of which are protein. The P. infestans genome encodes hundreds of genes for small, secreted RXLR (+/-EER) effectors (their conserved motif similar to the one involved in protein translocation from the malaria parasite into host cells). The formation of haustoria, finger-like projections that breach the plant cell wall to make contact with the cell membrane, is crucial for the biotrophic phase of infection. We have shown that effectors are secreted at haustoria and that RXLR effectors are translocated into host cells.
We have characterised the activities of several RXLR effectors. These investigations reveal how the pathogen targets a broad range of host pathways that contribute to plant defence, often using multiple effectors to target different elements within the same pathway.
One fo the first effectors we examined, PiAVR3a, an essential RXLR effector, has 14 candidate host protein interactions. The complexities of the interaction between PiAVR3a and the E3 ligase CMPG1 alone took several years to unravel. The nuclear-targeted effector Pi04314, one of the most highly expressed effectors and one that gives a large boost to P. infestans infection when co-expressed in leaves, binds to isoforms of the protein phosphatase type 1 catalytic domain (PP1c) and forms a host-pathogen holoenzyme, exploiting the phosphatase activity to benefit infection. Similarly the nucleolar-associated effector Pi04089 exploits the activity of a KH type of RNA binding protein (StKRBP1), Pi02860 targets a predicted potato E3 ligase NPH3/RPT2-like 1 (StNRL1) and Pi17316 uses MAP3K StVIK1. Thus StPP1c's the StKRBP1, StNRL1 and StVIK1 are all susceptibility (S) factors. This reveals the potential of S factors as novel targets for development of plant resistance.
PiAVR3a is detected by R3a within the plant cell cytosol and the RXLR-EER motif is required for the recognition. We showed the RXLR-EER motif is required for translocation of PiAVR3a into the plant cytosol using a GUS fusion. Subsequently, using effectors that we showed to be nuclear localised when expressed in plant cells, we managed to observe effector translocation in live cells with fluorescent protein fusions. Inhibitor studies revealed that apolastic effectors and other pathogenicity proteins are conventionally secreted while the translocated RXLR efectors are secreted by a different pathway, i.e. they are non-conventionally secreted. Current work is investigating how RXLR effectors are targeted to the non-conventional route and how that results in them being translocated into host cells. We have shown that uptake of a range of RXLR effectors by plant cells involves clathrin-mediated endocytosis, the next question is, how are they then released from endosomes to reach their host targets in the cytosol or other locations?
The imaging and cell biology facilites and capabilites at The James Hutton Institute are managed by Alison Roberts, Kath Wright and Sean Chapman in addition to their own research activities. High quality imaging work is not possible without great training, ongoing support and facility management.
Bibliography
- McLellan, H.; Harvey, S.E.; Steinbrenner, J.; Armstrong, M.R.; He, Q.; Clewes, R.; Pritchard, L.; Wang, W.; Wang, S.; Nussbaumer, T.; Dohai, B.; Luo, Q.; Kumari, P.; Roberts, A.; Boevink, P.C.; Neumann, C.; Champouret, N.; Hein, I.; Falter-Braun, P.; Beynon, J.; Denby, K.; Birch, P.R.J. (2022) Exploiting breakdown in nonhost effector-target interactions to boost host disease resistance, Proceedings of the National Academy of Sciences USA, 119(35), Art. E2114064119
- Zhou, J.; Qi, Y.; Nie, J.; Guo, L.; Luo, M.; McLellan, H.; Boevink, P.; Birch, P.R.J.; Tian, Z. (2022) A Phytophthora effector promotes homodimerization of host transcription factor StKNOX3 to enhance susceptibility, Journal of Experimental Botany, 73(19), pp. 6902-6915
- Hermann, S.; Orlik, M.; Boevink, P.; Stein, E.; Scherf, A.; Kleeberg, I.; Schmitt, A.; Schikora, A. (2022) Biocontrol of Plant Diseases Using Glycyrrhiza glabra Leaf Extract, Plant Disease, 106(12), pp. 3133-3144
- Wang, H.; Wang, S.; Wang, W.; Welsh, L.; Gierlinski, M.; Whisson, S.; Hemsley, P.; Boevink, P.; Birch, P. (2022) Entering via the front door Cytoplasmic effectors are taken into host cells via endocytosis, 52nd Congress of the Southern African Society for Plant Pathologists (SASSP), 1-3 August 2022, Pretoria
- Wang, S.M.; Vetukuri, R.R.; Kushwaha, S.K.; Hedley, P.E.; Morris, J.; Studholme, D.J.; Welsh, L.R.J.; Boevink, P.C.; Birch, P.R.J.; Whisson, S.C. (2021) Haustorium formation and a distinct biotrophic transcriptome characterize infection of Nicotiana benthamiana by the tree pathogen Phytophthora kernoviae., Molecular Plant Pathology, 22, 954-968.
- Stam, R.; Motion, G.B.; Martinez-Heredia, V.; Boevink, P.C.; Huitema, E. (2021) A conserved oomycete CRN effector targets tomatoTCP14-2 to enhance virulence., Molecular Plant-Microbe Interactions, 34, 309-318.
- He, Q.; McLellan, H.; Boevink, P.C.; Birch, P.R.J. (2020) All roads lead to susceptibility: the many modes of action of fungal and oomycete intracellular effectors., Plant Communications, 1, Article No. 100050.
- McLellan, H.; Chen, K.; He, Q.; Wu, X.; Boevink, P.C.; Tian, Z.; Birch, P.R.J. (2020) The ubiquitin E3 ligase PUB17 positively regulates immunity by targeting a negative regulator, KH17, for degradation., Plant Communications, 1, Article No. 100020.
- Boevink, P.C.; Birch, P.R.J.; Turnbull, D.; Whisson, S.C. (2020) Devastating intimacy: the cell biology of plant-phytophthora interactions., New Phytologist, 228, 445-458.
- He, Q.; McLellan, H.; Hughes, R.K.; Boevink, P.C.; Armstrong, M.; Lu, Y.; Banfield, M.J.; Tian, Z.; Birch, P.R.J. (2019) Phytophthora infestans effector SFI3 targets potato UKB to suppress early immune transcriptional response., New Phytologist, 222, 438-454.
- Wang, S.; McLellan, H.; Bukharova, T.; He, Q.; Murphy, F.; Shi, J.; Sun, S.; van Weymers, P.; Ren, Y.; Thilliez, G.; Wang, H.; Chen, X.; Engelhardt, S.; Vleeshouwers, V.; Gilroy, E.M.; Whisson, S.W.; Hein, I.; Wang, X.; Tian, Z.; Birch, P.R.J.; Boevink, P.C. (2019) Phytophthora infestans RXLR effectors act in concert at diverse subcellular localisations to enhance host colonisation., Journal of Experimental Botany, 70, 343-356.
- Boevink, P.C.; Wang, S.; Pham, J.; Turnbull, D.; Welsh, L.; Whisson, S.C.; Birch, P.R.J. (2019) The oomycete RXLR motif determines non-conventional secretion for effector delivery., IS-MPMI Molecular Plant Microbe Interactions, XVIII Congress, Glasgow, 14-18 July 2019.
- Wang, S.M.; Welsh, L.; Thorpe, P.; Whisson, S.C.; Boevink, P.C.; Birch, P.R.J. (2018) The Phytophthora infestans haustorium is a site for secretion of diverse classes of infection-associated proteins., MBIO, 9, Article No. e01216-18.
- Zheng, X.Z.; Wagener, N.; McLellan, H.; Boevink, P.C.; Hua, C.L.; Birch, P.R.J.; Brunner, F. (2018) Phytophthora infestans RXLR effector SFI5 requires association with calmodulin for PTI/MTI suppressing activity., New Phytologist, 219, 1433-1446.
- Murphy, F.; He, Q.; Armstrong, M.; Giuliani, L.M.; Boevink, P.C.; Zhang, W.; Tian, Z.; Birch, P.J.; Gilroy, E.M. (2018) The potato MAP3K StVIK is required for Phytophthora infestans RXLR effector Pi17316 to promote disease., Plant Physiology, 177, 398-410.
- He, Q.; Naqvi, S.; McLellan, H.; Boevink, P.C.; Champouret, N.; Hein, I.; Birch, P.R.J. (2018) Plant pathogen effector utilizes host susceptibility factor NRL1 to degrade the immune regulator SWAP70., Proceedings of the National Academy of Sciences of the USA, 115, E7834-E7843.
- He ,Q.; Naqvi, S.; McLellan, H.; Boevink, P.C.; Champouret, N.; Hein, I.; Birch, P.R.J. (2018) A plant pathogen effector utilizes host Susceptibility factor NRL1 to degrade the immune regulator SWAP70, Oomycete Molecular Genetics Network Meeting, Shandong Agricultural University, Taian, China, 8-12 April 2018.
- Wang, S.; Boevink, P.C.; Whisson, S.C.; Birch, P.R.J. (2018) How are effectors secreted and delivered to the host?, Oomycete Molecular Genetics Network Meeting, Shandong Agricultural University, Taian, China, 8-12 April 2018.
- Boevink, P.C. (2017) Exchanging missives and missiles: the roles of extracellular vesicles in plant-pathogen interactions., Journal of Experimental Botany, 68, 5411-5414.
- Wang, S.; Boevink, P.C.; Welsh, L.; Zhang, R.F.; Whisson, S.C.; Birch, P.R.J. (2017) Delivery of cytoplasmic and apoplastic effectors from Phytophthora infestans haustoria by distinct secretion pathways., New Phytologist, 216, 205-215.
- Turnbull, D.; Yang, L.N.; Naqvi, S.; Breen, S.; Welsh, L.; Stephens, J.; Morris, J.; Boevink, P.C.; Hedley, P.E.; Zhan, J.; Birch, P.R.; Gilroy, E.M. (2017) RXLR effector AVR2 up-regulates a brassinosteroid responsive bHLH transcription factor to suppress immunity., Plant Physiology, 174, 356-369.
- Orosa, B.; He, Q.; Mesmar, J.; Gilroy, E.M.; McLellan, H.; Yang, C.W.; Craig, A.; Bailey, M.; Zhang, C.J.; Moore, J.D.; Boevink, P.C.; Tian, Z.D.; Birch, P.R.J.; Sadanandom, A. (2017) BTB-BACK domain protein POB1 suppresses immune cell death by targeting ubiquitin E3 ligase PUB17 for degradation., PLoS Genetics, 13, Article No. e1006540.
- Whisson, S.C.; Boevink, P.C.; Wang, S.M.; Birch, P.R.J. (2016) The cell biology of late blight disease., Current Opinion in Microbiology, 34, 127-135.
- Yang, L.; McLellan, H.; Naqvi, S.; Qin, He.; Boevink, P.C.; Armstrong, M.; Giuliani, L.M.; Zhang, W.; Tian, Z.; Zhan, J.; Gilroy, E.M.; Birch, P.J.R. (2016) Potato NPH3/RPT2-Like protein StNRL1, targeted by a Phytophthora infestans RXLR Effector, is a susceptibility factor., Plant Physiology, 171, 645-657.
- Boevink, P.C.; McLellan, H.; Gilroy, E.M.; Naqvi, S.; He, Q.; Yang, L.N.; Wang, X.D.; Turnbull, D.; Armstrong, M.R.; Tian, Z.D.; Birch, P.R.J. (2016) Oomycetes seek help from the plant: Phytophthora infestans effectors target host susceptibility factors., Molecular Plant, 9, 636-638.
- Boevink, P.C.; Wang, X.D.; McLellan, H.; He, Q.; Naqvi, S.; Armstrong, M.R.; Zhang, W.; Hein, I.; Gilroy, E.M.; Tian, Z.D.; Birch, P.R.J. (2016) A Phytophthora infestans RXLR effector targets plant PP1c isoforms that promote late blight disease., Nature Communications, 7, Article No. 10311.
- Wang, X.D.; Boevink, P.; McLellan, H.; Armstrong, M.; Bukharova, T.; Qin, Z.W.; Birch, P.R.J. (2015) A host KH RNA-binding protein is a susceptibility factor targeted by an RXLR effector to promote late blight disease., Molecular Plant, 8, 1385-1395.
- He, Q.; McLellan, H.; Boevink, P.C.; Sadanandom, A.; Xie, C.H.; Birch, P.R.J.; Tian, Z.D. (2015) U-box E3 ubiquitin ligase PUB17 acts in the nucleus to promote specific immune pathways triggered by Phytophthora infestans., Journal of Experimental Botany, 66, 3189-3199.
- King, S.R.F.; McLellan, H.; Boevink, P.C.; Armstrong, M.R.; Bukharova, T.; Sukarta, O.; Win, J.; Kamoun, S.; Birch, P.R.J.; Banfielda, M.J. (2014) Phytophthora infestans RXLR Effector PexRD2 interacts with Host MAPKKK epsilon to suppress plant immune signaling., The Plant Cell, 26, 1345-1359.
- Zheng, X.; McLellan, H.; Fraiture, M.; Liu, X.; Boevink, P.C.; Gilroy, E.M.; Chen, Y.; Kandel, K.; Sessa, G.; Birch, P.R.J.; Brunner, F. (2014) Functionally redundant RXLR effectors from Phytophthora infestans act at different steps to suppress early flg22-triggered immunity., PLoS Pathogens 10, Article No. e1004057.
- Chapman, S.; Stevens, L.J.; Boevink, P.C.; Engelhardt, S.; Alexander, C.J.; Harrower, B.; Champouret, N.; McGeachy, K.; Van Weymers, P.S.M.; Chen, X.; Birch, P.R.J.; Hein, I. (2014) Detection of the virulent form of AVR3a from phytophthora infestans following artificial evolution of potato resistance gene R3a., PLoS ONE, 9, Article No. e110158.
- Boevink, P.; Wang, X.; McLellan, H.; Armstrong, M.; Bukharova, T.; Birch, P.R.J. (2014) Targeting of PP1c isoforms by an RXLR effector., Oomycete Molecular Genetics Network Meeting, Norwich, July 2014.
- Stevens, L.; Chapman, S.; Boevink, P.; Engelhardt, S.; Chen, X.; Birch, P.; Hein, I. (2014) Shuffling resistance genes to protect solanaceous plants., British Society for Plant Pathology Presidential Meeting, University of St Andrews, 1-2 September 2014.
- Boevink, P.; McLellan, H.; Bukharova, T.; Engelhardt, S.; Birch P.R.J. (2014) In vivo protein-protein interaction studies with BiFC: conditions, cautions, and caveats., In: Birch, P.R.J., Jones, J.T. & Bos, J.I.B. (eds.). Plant-Pathogen Interactions: Methods and Protocols. Methods in Molecular Biology, Humana Press, New York, 2nd ed. Volume 1127, Chapter 6, 81-90.
- McLellan, H.; Boevink, P.C.; Armstrong, M.R.; Pritchard, L.; Gomez, S.; Morales, J.; Whisson, S.C.; Beynon, J.L.; Birch, P.R.J. (2013) An RxLR effector from Phytophthora infestans prevents re-localisation of two plant NAC transcription factors from the endoplasmic reticulum to the nucleus., PLoS Pathogens, 9, Article No. e1003670.
- Stam, R.; Jupe, J.; Howden, A.J.M.; Morris, J.A.; Boevink, P.C.; Hedley, P.E.; Huitema, E. (2013) Identification and characterisation CRN effectors in Phytophthora capsici shows modularity and functional diversity., PLoS ONE, 8, Article No. e59517.
- Engelhardt, S.; Boevink, P.C.; Armstrong, M.R.; Ramos, M.; Hein, I.; Birch, P.R.J. (2012) Relocalization of late blight resistance protein R3a to endosomal compartments is associated with effector recognition and required for the immune response., The Plant Cell, 24, 5142-5158.
- Whisson, S.C.; Avrova, A.O.; Boevink, P.C.; Armstrong, M.R.; Seman, Z.A.; Hein, I.; Birch, P.R.J. (2011) Exploiting knowledge of pathogen effectors to enhance late blight resistance in potato., Potato Research, 54, 325-340.
- Gilroy, E.M.; Breen, S.; Whisson, S.C.; Squires, J.; Hein, I.; Kaczmarek, M.; Turnbull, D.; Boevink, P.; Lokossou, A.; Cano, L.M.; Morales, J.; Avrova, A.O.; Pritchard, L.; Randall, E.; Lees, A.K.; Govers, F.; van West, P.; Kamoun, S.; Vleeshouwers, V.G.A.A.; Cooke, D.E.L.; Birch, P.R.J. (2011) Presence/absence, differential expression and sequence polmorphisms between PiAVR2 and PiAVR2-like in Phytophthora infestans determine virulence on R2 plants., New Phytologist, 191, 763-776.
- Gilroy, E.M.; Taylor, R.M.; Hein, I.; Boevink, P.; Sadanandom, A.; Birch, P.R.J. (2011) CMPG1-dependent cell death follows perception of diverse pathogen elicitors at the host plasma membrane and is suppressed by Phytophthora infestans RXLR effector AVR3a., New Phytologist, 190, 653-666.
- McLellan, H.; Harvey, S.E.; Steinbrenner, J.; Armstrong, M.R.; He, Q.; Clewes, R.; Pritchard, L.; Wang, W.; Wang, S.; Nussbaumer, T.; Dohai, B.; Luo, Q.; Kumari, P.; Roberts, A.; Boevink, P.C.; Neumann, C.; Champouret, N.; Hein, I.; Falter-Braun, P.; Beynon, J.; Denby, K.; Birch, P.R.J. (2022) Exploiting breakdown in nonhost effector-target interactions to boost host disease resistance, Proceedings of the National Academy of Sciences USA, 119(35), Art. E2114064119
- Zhou, J.; Qi, Y.; Nie, J.; Guo, L.; Luo, M.; McLellan, H.; Boevink, P.; Birch, P.R.J.; Tian, Z. (2022) A Phytophthora effector promotes homodimerization of host transcription factor StKNOX3 to enhance susceptibility, Journal of Experimental Botany, 73(19), pp. 6902-6915
- Hermann, S.; Orlik, M.; Boevink, P.; Stein, E.; Scherf, A.; Kleeberg, I.; Schmitt, A.; Schikora, A. (2022) Biocontrol of Plant Diseases Using Glycyrrhiza glabra Leaf Extract, Plant Disease, 106(12), pp. 3133-3144
- Wang, S.M.; Vetukuri, R.R.; Kushwaha, S.K.; Hedley, P.E.; Morris, J.; Studholme, D.J.; Welsh, L.R.J.; Boevink, P.C.; Birch, P.R.J.; Whisson, S.C. (2021) Haustorium formation and a distinct biotrophic transcriptome characterize infection of Nicotiana benthamiana by the tree pathogen Phytophthora kernoviae., Molecular Plant Pathology, 22, 954-968.
- Stam, R.; Motion, G.B.; Martinez-Heredia, V.; Boevink, P.C.; Huitema, E. (2021) A conserved oomycete CRN effector targets tomatoTCP14-2 to enhance virulence., Molecular Plant-Microbe Interactions, 34, 309-318.
- He, Q.; McLellan, H.; Boevink, P.C.; Birch, P.R.J. (2020) All roads lead to susceptibility: the many modes of action of fungal and oomycete intracellular effectors., Plant Communications, 1, Article No. 100050.
- McLellan, H.; Chen, K.; He, Q.; Wu, X.; Boevink, P.C.; Tian, Z.; Birch, P.R.J. (2020) The ubiquitin E3 ligase PUB17 positively regulates immunity by targeting a negative regulator, KH17, for degradation., Plant Communications, 1, Article No. 100020.
- Boevink, P.C.; Birch, P.R.J.; Turnbull, D.; Whisson, S.C. (2020) Devastating intimacy: the cell biology of plant-phytophthora interactions., New Phytologist, 228, 445-458.
- He, Q.; McLellan, H.; Hughes, R.K.; Boevink, P.C.; Armstrong, M.; Lu, Y.; Banfield, M.J.; Tian, Z.; Birch, P.R.J. (2019) Phytophthora infestans effector SFI3 targets potato UKB to suppress early immune transcriptional response., New Phytologist, 222, 438-454.
- Wang, S.; McLellan, H.; Bukharova, T.; He, Q.; Murphy, F.; Shi, J.; Sun, S.; van Weymers, P.; Ren, Y.; Thilliez, G.; Wang, H.; Chen, X.; Engelhardt, S.; Vleeshouwers, V.; Gilroy, E.M.; Whisson, S.W.; Hein, I.; Wang, X.; Tian, Z.; Birch, P.R.J.; Boevink, P.C. (2019) Phytophthora infestans RXLR effectors act in concert at diverse subcellular localisations to enhance host colonisation., Journal of Experimental Botany, 70, 343-356.
- Wang, S.M.; Welsh, L.; Thorpe, P.; Whisson, S.C.; Boevink, P.C.; Birch, P.R.J. (2018) The Phytophthora infestans haustorium is a site for secretion of diverse classes of infection-associated proteins., MBIO, 9, Article No. e01216-18.
- Zheng, X.Z.; Wagener, N.; McLellan, H.; Boevink, P.C.; Hua, C.L.; Birch, P.R.J.; Brunner, F. (2018) Phytophthora infestans RXLR effector SFI5 requires association with calmodulin for PTI/MTI suppressing activity., New Phytologist, 219, 1433-1446.
- Murphy, F.; He, Q.; Armstrong, M.; Giuliani, L.M.; Boevink, P.C.; Zhang, W.; Tian, Z.; Birch, P.J.; Gilroy, E.M. (2018) The potato MAP3K StVIK is required for Phytophthora infestans RXLR effector Pi17316 to promote disease., Plant Physiology, 177, 398-410.
- He, Q.; Naqvi, S.; McLellan, H.; Boevink, P.C.; Champouret, N.; Hein, I.; Birch, P.R.J. (2018) Plant pathogen effector utilizes host susceptibility factor NRL1 to degrade the immune regulator SWAP70., Proceedings of the National Academy of Sciences of the USA, 115, E7834-E7843.
- Boevink, P.C. (2017) Exchanging missives and missiles: the roles of extracellular vesicles in plant-pathogen interactions., Journal of Experimental Botany, 68, 5411-5414.
- Wang, S.; Boevink, P.C.; Welsh, L.; Zhang, R.F.; Whisson, S.C.; Birch, P.R.J. (2017) Delivery of cytoplasmic and apoplastic effectors from Phytophthora infestans haustoria by distinct secretion pathways., New Phytologist, 216, 205-215.
- Turnbull, D.; Yang, L.N.; Naqvi, S.; Breen, S.; Welsh, L.; Stephens, J.; Morris, J.; Boevink, P.C.; Hedley, P.E.; Zhan, J.; Birch, P.R.; Gilroy, E.M. (2017) RXLR effector AVR2 up-regulates a brassinosteroid responsive bHLH transcription factor to suppress immunity., Plant Physiology, 174, 356-369.
- Orosa, B.; He, Q.; Mesmar, J.; Gilroy, E.M.; McLellan, H.; Yang, C.W.; Craig, A.; Bailey, M.; Zhang, C.J.; Moore, J.D.; Boevink, P.C.; Tian, Z.D.; Birch, P.R.J.; Sadanandom, A. (2017) BTB-BACK domain protein POB1 suppresses immune cell death by targeting ubiquitin E3 ligase PUB17 for degradation., PLoS Genetics, 13, Article No. e1006540.
- Whisson, S.C.; Boevink, P.C.; Wang, S.M.; Birch, P.R.J. (2016) The cell biology of late blight disease., Current Opinion in Microbiology, 34, 127-135.
- Yang, L.; McLellan, H.; Naqvi, S.; Qin, He.; Boevink, P.C.; Armstrong, M.; Giuliani, L.M.; Zhang, W.; Tian, Z.; Zhan, J.; Gilroy, E.M.; Birch, P.J.R. (2016) Potato NPH3/RPT2-Like protein StNRL1, targeted by a Phytophthora infestans RXLR Effector, is a susceptibility factor., Plant Physiology, 171, 645-657.
- Boevink, P.C.; McLellan, H.; Gilroy, E.M.; Naqvi, S.; He, Q.; Yang, L.N.; Wang, X.D.; Turnbull, D.; Armstrong, M.R.; Tian, Z.D.; Birch, P.R.J. (2016) Oomycetes seek help from the plant: Phytophthora infestans effectors target host susceptibility factors., Molecular Plant, 9, 636-638.
- Boevink, P.C.; Wang, X.D.; McLellan, H.; He, Q.; Naqvi, S.; Armstrong, M.R.; Zhang, W.; Hein, I.; Gilroy, E.M.; Tian, Z.D.; Birch, P.R.J. (2016) A Phytophthora infestans RXLR effector targets plant PP1c isoforms that promote late blight disease., Nature Communications, 7, Article No. 10311.
- Wang, X.D.; Boevink, P.; McLellan, H.; Armstrong, M.; Bukharova, T.; Qin, Z.W.; Birch, P.R.J. (2015) A host KH RNA-binding protein is a susceptibility factor targeted by an RXLR effector to promote late blight disease., Molecular Plant, 8, 1385-1395.
- He, Q.; McLellan, H.; Boevink, P.C.; Sadanandom, A.; Xie, C.H.; Birch, P.R.J.; Tian, Z.D. (2015) U-box E3 ubiquitin ligase PUB17 acts in the nucleus to promote specific immune pathways triggered by Phytophthora infestans., Journal of Experimental Botany, 66, 3189-3199.
- King, S.R.F.; McLellan, H.; Boevink, P.C.; Armstrong, M.R.; Bukharova, T.; Sukarta, O.; Win, J.; Kamoun, S.; Birch, P.R.J.; Banfielda, M.J. (2014) Phytophthora infestans RXLR Effector PexRD2 interacts with Host MAPKKK epsilon to suppress plant immune signaling., The Plant Cell, 26, 1345-1359.
- Zheng, X.; McLellan, H.; Fraiture, M.; Liu, X.; Boevink, P.C.; Gilroy, E.M.; Chen, Y.; Kandel, K.; Sessa, G.; Birch, P.R.J.; Brunner, F. (2014) Functionally redundant RXLR effectors from Phytophthora infestans act at different steps to suppress early flg22-triggered immunity., PLoS Pathogens 10, Article No. e1004057.
- Chapman, S.; Stevens, L.J.; Boevink, P.C.; Engelhardt, S.; Alexander, C.J.; Harrower, B.; Champouret, N.; McGeachy, K.; Van Weymers, P.S.M.; Chen, X.; Birch, P.R.J.; Hein, I. (2014) Detection of the virulent form of AVR3a from phytophthora infestans following artificial evolution of potato resistance gene R3a., PLoS ONE, 9, Article No. e110158.
- McLellan, H.; Boevink, P.C.; Armstrong, M.R.; Pritchard, L.; Gomez, S.; Morales, J.; Whisson, S.C.; Beynon, J.L.; Birch, P.R.J. (2013) An RxLR effector from Phytophthora infestans prevents re-localisation of two plant NAC transcription factors from the endoplasmic reticulum to the nucleus., PLoS Pathogens, 9, Article No. e1003670.
- Stam, R.; Jupe, J.; Howden, A.J.M.; Morris, J.A.; Boevink, P.C.; Hedley, P.E.; Huitema, E. (2013) Identification and characterisation CRN effectors in Phytophthora capsici shows modularity and functional diversity., PLoS ONE, 8, Article No. e59517.
- Engelhardt, S.; Boevink, P.C.; Armstrong, M.R.; Ramos, M.; Hein, I.; Birch, P.R.J. (2012) Relocalization of late blight resistance protein R3a to endosomal compartments is associated with effector recognition and required for the immune response., The Plant Cell, 24, 5142-5158.
- Whisson, S.C.; Avrova, A.O.; Boevink, P.C.; Armstrong, M.R.; Seman, Z.A.; Hein, I.; Birch, P.R.J. (2011) Exploiting knowledge of pathogen effectors to enhance late blight resistance in potato., Potato Research, 54, 325-340.
- Gilroy, E.M.; Breen, S.; Whisson, S.C.; Squires, J.; Hein, I.; Kaczmarek, M.; Turnbull, D.; Boevink, P.; Lokossou, A.; Cano, L.M.; Morales, J.; Avrova, A.O.; Pritchard, L.; Randall, E.; Lees, A.K.; Govers, F.; van West, P.; Kamoun, S.; Vleeshouwers, V.G.A.A.; Cooke, D.E.L.; Birch, P.R.J. (2011) Presence/absence, differential expression and sequence polmorphisms between PiAVR2 and PiAVR2-like in Phytophthora infestans determine virulence on R2 plants., New Phytologist, 191, 763-776.
- Gilroy, E.M.; Taylor, R.M.; Hein, I.; Boevink, P.; Sadanandom, A.; Birch, P.R.J. (2011) CMPG1-dependent cell death follows perception of diverse pathogen elicitors at the host plasma membrane and is suppressed by Phytophthora infestans RXLR effector AVR3a., New Phytologist, 190, 653-666.
- Bos, J.I.B.; Armstrong, M.R.; Gilroy, E.M.; Boevink, P.; Hein, I.; Taylor, R.M.; Tian, Z.D.; Engelhardt, S.; Vetukuri, R.R.; Harrower, B.E.; Dixelius, C.; Bryan, G.J.; Sadanandom, A.; Whisson, S.C.; Kamoun, S.; Birch, P.R.J. (2010) Phytophthora infestans effector AVR3a is essential for virulence and manipulates plant immunity by stabilizing host E3 ligase CMPG1., Proceedings of the National Academy of Sciences of the United States of America (PNAS), 107, 9909-9914.
- Bollmann, S.R.; Bos, J.I.B.; Bulone, V.; Cai, G.H.; Cakir, C.; Carrington, J.C.; Chawner, M.; Conti, L; Costanzo, S.; Ewan, R.; Fahlgren, N.; Fischbach, M.A.; Fugelstad, J.; Gilroy, E.M.; Gnerre, S.; Green, P.J.; Grenville-Briggs, L.J.; Griffith, J.; Grunwald, N.J.; Horn, K.; Horner, N.R.; Hu, C.H.; Huitema, E.; Jeong, D.H.; Jones, A.M.E.; Jones, J.D.G.; Jones, R.W.; Karlsson, E.K.; Kunjeti, S.G.; Lamour, K.; Liu, Z.Y.; Ma, L.J.; MacLean, D.; Chibucos, M.C.; McDonald, H.; McWalters, J.; Meijer, H.J.G.; Morgan, W.; Morris, P.F.; Munro, C.A.; O'Neill, K.; Ospina-Giraldo, M.; Pinzon, A.; Pritchard, L.; Ramsahoye, B.; Ren, Q.H.; Restrepo, S.; Roy, S.; Sadanandom, A.; Savidor, A.; Schornack, S.; Schwartz, D.C.; Schumann, U.D.; Schwessinger, B.; Seyer, L.; Sharpe, T.; Silvar, C.; Song, J.; Studholme, D.J.; Sykes, S.; Thines, M.; van de Vondervoort, P.J.I.; Phuntumart, V.; Wawra, S.; Weide, R.; Win, J.; Young, C.; Zhou, S.G.; Fry, W.; Meyers, B.C.; van West, P.; Ristaino, J.; Govers, F.; Birch, P.R.J.; Whisson, S.C.; Judelson, H.S.; Nusbaum, C. (2009) Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans., Nature, 461, 393-398.
- Birch, P.R.J.; Armstrong, M.R.; Bos, J.; Boevink, P.; Gilroy, E.M.; Taylor, R.M.; Wawra, S.; Pritchard, L.; Conti, L.; Ewan, R.; Whisson, S.C.; van West, P.; Sadanandom, A.; Kamoun, S. (2009) Towards understanding the virulence functions of RXLR effectors of the oomycete plant pathogen Phytophthora infestans., Journal of Experimental Botany, 60, 1133-1140.
- Birch, P.R.J.; Whisson, S.C.; Boevink, P.; Armstrong, M.R.; Gilroy, E.M.; Pritchard, L.; Grouffaud, S.; Sandanandom, A.; Taylor, R.; Kamoun, S.; Bos, J.I. (2008) Translocated oomycete effectors that target the plant immune system., Comparative Biochemistry and Physiology Part A: Molecular and Integrative Physiology, 150, S176-S177.
- Birch, P.R.J.; Boevink, P.; Gilroy, E.M.; Hein, I.; Pritchard, L.; Whisson, S.C. (2008) Oomycete RXLR effectors: delivery, functional redundancy and durable disease resistance., Current Opinion in Plant Biology, 11, 373-379.
- Avrova, A.O.; Boevink, P.; Young, V.; Grenville-Briggs, L.J.; van West, P.; Birch, P.R.J.; Whisson, S.C. (2008) A novel Phytophthora infestans haustorium-specific membrane protein is required for infection of potato., Cellular Microbiology, 10, 2271-2284.
- Latijnhouwers, M.; Gillespie, T.; Boevink, P.; Hawes, C.L.; Carvalho, C. (2007) Localization and domain characterization of Arabidopsis Golgin Candidates., Journal of Experimental Botany, 58, 4373-4386.
- Boevink, P.; McLellan, H.; Bukharova, T.; Engelhardt, S.; Birch P.R.J. (2014) In vivo protein-protein interaction studies with BiFC: conditions, cautions, and caveats., In: Birch, P.R.J., Jones, J.T. & Bos, J.I.B. (eds.). Plant-Pathogen Interactions: Methods and Protocols. Methods in Molecular Biology, Humana Press, New York, 2nd ed. Volume 1127, Chapter 6, 81-90.
- Boevink, P.; Birch, P.R.J.; Whisson, S.C. (2011) Imaging fluorescently tagged Phytophthora effector proteins inside infected plant tissue., In: McDowell, J.M. (ed.). Methods in Molecular Biology Plant Immunity: Methods and Protocols. Humana Press, Totowa, New Jersey, USA, Chapter 712, pp195-209.
- Oparka, K.J.; Boevink, P. (2004) Techniques for imaging intercellular transport., In: Plasmodesmata (ed. K.J. Oparka). Blackwell Publishing, Oxford, pp241-262
- Hawes, C.; Boevink, P.; Moore, I. (2000) GFP in plants., In: Fluorescence Microscopy of Proteins: A Practical Approach (ed. V. Allen). Irl Press, pp163-177
- Neuhaus, J.; Boevink, P. (2000) The green fluorescent protein (GFP) as a reporter in plant cells., In: Plant Cell Biology: A Practical Approach (eds. C.L. Hawes and B. Satiat-jeunemaitre). Oxford University Press, Oxford, pp127-142.
- Whisson, S.C.; Boevink, P.; Pritchard, L.; Avrova, A.O.; Morales, J.; Birch, P.R.J. (2006) Effector protein translocation in the Phytophthora infestans - potato infection., Annual Report of the Scottish Crop Research Institute for 2006, pp24-25.
- Latijnhouwers, M.; Boevink, P.; Hawes, C.L.; Oparka, K.J. (2004) In search of plant Golgi matrix proteins., Annual Report of the Scottish Crop Research Institute for 2003/2004, 131-132.
- Boevink, P.; Calcutt, J.; Roberts, A.G.; Oparka, K.J. (2004) Real time studies of cell-to-cell communication., Annual Report of the Scottish Crop Research Institute for 2003/2004, 129-130.
- Gillespie, T.; Toth, R.; Haupt, S.; Boevink, P.; Roberts, A.G.; Chapman, S.N.; Oparka, K.J. (2001) A DNA-shuffled movement protein enhances virus transport by evasion of a host-mediated degradation pathway., Annual Report of the Scottish Crop Research Institute for 2000/2001, pp107-111.
- Roberts, A.G.; Santa, Cruz, S.; Boevink, P.; Roberts, I.M.; Sauer, N.; Oparka, K.J. (1999) The sink-source transition in leaves - new insights., Annual Report of the Scottish Crop Research Institute for 1998/99, 76-79.
- Santa, Cruz, S.; Boevink, P.; Duncan, G.; Roberts, A.G.; Prior, D.A.M.; Oparka, K.J. (1998) Probing the virus long-distance tranport pathway., Annual Report of the Scottish Crop Research Institute for 1997/98, 114-117.
- Boevink, P.; Hawes, C.L.; Prior, DA.M.; Santa, Cruz, S.; Oparka, K.J. (1998) New insights into the plant secretory pathway using virus-delivered green fluorescent protein., Annual Report of the Scottish Crop Research Institute for 1997/98, 67-70.
- Wang, H.; Wang, S.; Wang, W.; Welsh, L.; Gierlinski, M.; Whisson, S.; Hemsley, P.; Boevink, P.; Birch, P. (2022) Entering via the front door Cytoplasmic effectors are taken into host cells via endocytosis, 52nd Congress of the Southern African Society for Plant Pathologists (SASSP), 1-3 August 2022, Pretoria
- Boevink, P.C.; Wang, S.; Pham, J.; Turnbull, D.; Welsh, L.; Whisson, S.C.; Birch, P.R.J. (2019) The oomycete RXLR motif determines non-conventional secretion for effector delivery., IS-MPMI Molecular Plant Microbe Interactions, XVIII Congress, Glasgow, 14-18 July 2019.
- He ,Q.; Naqvi, S.; McLellan, H.; Boevink, P.C.; Champouret, N.; Hein, I.; Birch, P.R.J. (2018) A plant pathogen effector utilizes host Susceptibility factor NRL1 to degrade the immune regulator SWAP70, Oomycete Molecular Genetics Network Meeting, Shandong Agricultural University, Taian, China, 8-12 April 2018.
- Wang, S.; Boevink, P.C.; Whisson, S.C.; Birch, P.R.J. (2018) How are effectors secreted and delivered to the host?, Oomycete Molecular Genetics Network Meeting, Shandong Agricultural University, Taian, China, 8-12 April 2018.
- Boevink, P.; Wang, X.; McLellan, H.; Armstrong, M.; Bukharova, T.; Birch, P.R.J. (2014) Targeting of PP1c isoforms by an RXLR effector., Oomycete Molecular Genetics Network Meeting, Norwich, July 2014.
- Stevens, L.; Chapman, S.; Boevink, P.; Engelhardt, S.; Chen, X.; Birch, P.; Hein, I. (2014) Shuffling resistance genes to protect solanaceous plants., British Society for Plant Pathology Presidential Meeting, University of St Andrews, 1-2 September 2014.
- Breen, S.; Gilroy, E.M.; Armstrong, M.R.; Morales, J.G.; Hein, I.; Douglas, E.; Boevink, P.; McLellan, H.; Randall, E.; Tian, Z.D.; Avrova, A.O.; Pritchard, L.; Lokossou, A.A.; Govers, F.; van der Vossen, E.A.G.; Vleeshouwers, V.G.A.A.; Brunner, F.; Whisson, S.C.; Birch, P.R.J. (2010) Avr2, an RXLR effector from Phytophthora infestans., Oomycete Molecular Genetics Network Congress, Toulouse, France, 6-8 June 2010.
- Armstrong, M.R.; Boevink, P.; Bukharova, T.; McLellan, H.; Ramos, M.; Gilroy, E.M.; Pritchard, L.; Whisson, S.C.; Beynon, J.; Birch, P.R.J. (2010) Identifying candidate host 'targets' of Phytophthora infestans translocated RXLR proteins., Oomycete Molecular Genetics Network Congress, Toulouse, France, 6-8 June 2010.
- Engelhardt, S.; Armstrong, M.R.; Boevink, P.; Ramos, M.; Gilroy, E.M.; Birch, P.R.J. (2010) R3a-mediated recognition of AVR3a: Cell biological and biochemical characterisation., Oomycete Molecular Genetics Network Congress, Toulouse, France, 6-8 June 2010.
- Gilroy, E.M.; Breen, S.; Hein, I.; Tian, Z.D.; Armstrong, M.R.; Douglas, E.; Lokossou, A.A.; Boevink, P.; McLellan, H.; Randall, E.; Morales, J.G.; Avrova, A.O.; Pritchard, L.; van der Vossen, E.A.G.; Whisson, S.C.; Birch, P.R.J. (2009) Amino acid polymorphisms upstream of the RXLR motif in Phytophthora infestans effector Avr2 condition R gene recognition., The Fungal Cell, British Mycological Society Meeting, Westpark Conference Centre, Dundee, 1-4 September 2009.
- Gilroy, E.M.; Armstrong, M.R.; Bos, J.; Taylor, R.; Morales, J.; Hein, I.; Douglas, E.; Boevink, P.; Avrova, A.O.; Breen, S.; van West, P.; Pritchard, L.; Whisson, S.C.; Sadanandom, A.; Kamoun, S.; Birch, P.R.J. (2009) Functional analysis of Phytophthora infestans RXLR effectors Avr2 and Avr3a., Fungal Genetics Conference, Asilomar Conference Grounds, Pacific Grove, California, USA, 17-22 March 2009.
- Birch, P.R.J.; Armstrong, M.R.; Gilroy, E.M.; Bos, J.; Taylor, R.M.; Morales, J.G.; Hein, I.; Douglas, E.; Boevink, P.; Breen, S.; Pritchard, L.; Whisson, S.C.; Sadanandom, A.; Kamoun, S. (2009) Localisation and function of Phytophthora infestans RXLR effectors and their host targets., XIV MPMI Conference, Montreal, Canada, 19-23 July 2009.
- Boevink, P.; Ramos, M.; Armstrong, M.R.; Allen, R.; Gilroy, E.M.; Donovan, S.; Rehmany, A.; Beynon, J.; Birch, P.R.J. (2009) Evolutionarily distinct RXLR effectors from distantly related oomycetes target the plant exocyst., 14th International Congress on Molecular Plant-Microbe Interactions, Quebec, Canada, 19-23 July 2009.
- Grouffaud, S.; Boevink, P.; Avrova, A.O.; van West, P.; Birch, P.R.J.; Whisson, S.C. (2008) Translocation of effector proteins from the oomycete Phytophthora infestans into plant cells., 9th European Conference on Fungal Genetics, Edinburgh, 5-8 April 2008.
- McLellan, H.; Gilroy, E.M.; Hein, I.; Boevink, P.; Birch, P.R.J.; Loake, G. (2007) The roles of cathespin B-like proteases in plant disease resistance., XIII International Congress on Molecular Plant-Microbe Interactions, Sorrento, Italy, 22-26 July 2007.
- Avrova, A.O.; Boevink, P.; Grenville-Briggs, L.J.; van West, P.; Birch, P.R.J.; Whisson, S.C. (2007) Identification of novel pathogenicity factors in the late blight pathogen, Phytophthora infestans., XIII International Congress on Molecular Plant-Microbe Interactions, Sorrento, Italy, 22-26 July 2007.
- Whisson, S.C.; Boevink, P.; Moleleki, L.N.; Avrova, A.O.; Morales, J.G.; Gilroy, E.M.; Armstrong, M.R.; Toth, I.K.; Pritchard, L.; Birch, P.R.J. (2007) A translocation signal for delivery of oomycete effector proteins into host plant cells., XIII International Congress on Molecular Plant-Microbe Interactions, Sorrento, Italy, 22-26 July 2007.
- Gilroy, E.M.; Venter, E.; McLellan, H.; Hein, I.; Hrubikova, K.; Holeva, M.C.; Boevink, P.; Loake, G.J.; Lacomme, C.; Birch, P.R.J. (2006) Inducible disease resistance involves an apoplastic cysteine protease Cathepsin B., Proceedings of IOBC/wprs Joint Working Group Meeting: Breeding for Inducible Resistance against Pests and Diseases, Heraklion, Crete, 27-29 April 2006.
- Carvalho, C.; Latijnhouwers, M.; Osterrieder, A.; Boevink, P.; Oparka, K.J.; (2005) Screening for plant Golgi-associated proteins., Mini-Symposium on Improving the Plant Secretory System for Nutrition and Health, Grasmere, 23-26 May 2005.
- Latijnhouwers, M.; Hawes, C.L.; Oparka, K.J.; Carvalho, C.; Boevink, P. (2005) Plant golgi matrix proteins., Mini-Symposium on Improving the Plant Secretory System for Nutrition and Health, Grasmere, 23-26 May 2005.
- Haupt, S.; Wright, K.M.; Cowan, G.H.; Boevink, P.; Gillespie, T.; Ziegler, A.; Roberts, A.G.; Chapman, S.N.; Oparka, K.J.; Torrance, L. (2005) Plant virus proteins traffic in the endomembrane system., Mini-Symposium on Improving the Plant Secretory System for Nutrition and Health, Grasmere, 23-26 May 2005.
- Boevink, P.; Wright, K.M.; Chapman, S.N.; Oparka, K.J. (2005) Tools for protein tracking., Plant Sciences Seminar and Workshop; Applications for Fluorescence Microscopy, Rothamsted Research, Harpenden, 11-15 April 2005.
- Boevink, P.; Chapman, S.N.; Bell, K.; Jackson, K.; Wright, K.M.; Latijnhouwers, M.; Gillespie, T.; Oparka, K.J.; Roberts, A.G. (2005) Investigating protein location, motion and function in living plant cells., Biotechnology, Havana, Cuba, 27 November - 2 December 2005.
- Boevink, P.; Wright, K.M.; Roberts, A.G.; Wood, N.; MacKenzie, K.; Oparka, K.J. (2005) Towards a new model for TMV movement., Plasmodesmata 2004, Monterey, California, USA, 17-21 August 2004.
- Roberts, A.G.; Boevink, P.; Calcutt, J.; Chapman, S.N.; Wright, K.M.; Oparka, K.J. (2004) New fluorescent proteins light up plant intercellular communication., SEB Plant Frontiers - The Visible Cell Biosensors and Bioreceptors Session, Exeter 3-6 July 2004.
- Wright, K.M.; Wood, N.T.; Roberts, A.G.; Boevink, P.; Gillespie, T.; MacKenzie, K.; Oparka, K.J. (2004) Plasmodesmal targeting of TMV movement protein utilises the ER/actin network., Plasmodesmata 2004, Monterey, California, USA, August 17-21 2004.
- Boevink, P.; Oparka, K.J. (2004) Real-time studies of plasmodesmatal gating in developing leaf cells., Plasmodesmata 2004, Monterey, California, USA, 17-21 August 2004.