Professor Paul Birch FRSE
One of the most significant questions in plant pathology is: How do pathogens suppress or otherwise manipulate host defences to establish disease? To do this, they secrete proteins and other chemicals that can interact with the host cell. In some cases, virulence determinants called effector proteins are delivered (translocated) inside living host cells where they ‘re-programme’ defences and metabolism to the pathogen’s benefit.
My group mainly studies effector proteins from the potato late blight pathogen, Phytophthora infestans. P. infestans is an oomycete, a eukaryotic pathogen with a fungus-like lifestyle that develops haustoria - finger-like cell structures that form an intimate interaction with the host plasma membrane during the early stages of disease. We have shown that haustoria are a major site of delivery of a class of proteins called RXLR effectors. The RXLR motif within these secreted effectors is required for their translocation inside host cells. In the genome of P. infestans we predict that there are >425 RXLR effector genes, demonstrating a remarkable potential for manipulation of host processes. We are discovering that RXLR effectors interact directly with a range of regulatory proteins in the host cell to suppress or otherwise manipulate plant defences. In contrast, the RXLRs are also targets for host resistance proteins which activate immune responses that prevent further colonization by the pathogen.
Using comparative and functional genomics, the key questions we are addressing are:
- How are RXLR effectors delivered into host plant cells?
- When are RXLR proteins required by the pathogen and where are they localized during infection?
- What are the host targets of RXLR effectors and what roles do those targets play in plant defence or metabolism?
- How are RXLR effectors co-evolving with their targets in the host, and how are they evolving to evade detection by the plant immune system?
With other members of the Dundee Effector Consortium we are exploiting our understanding of effector biology and diversity within pathogen populations to seek corresponding resistance genes in both host and non-host plants. In particular, we are searching for plant genes that provide durable disease resistance to P. infestans, and to a range of other economically damaging pests and pathogens of Solanaceae crop species (potato, tomato and pepper).
- Franco-Orozco B, Berepiki A, Ruiz O, Gamble L, Griffe LL, Wang S, Birch PRJ, Kanyuka K, Avrova AO (2017) A new proteinaceous PAMP identified in Ascomycete fungi induces cell death in Solanaceae. New Phytologist in press
- Oroso B, He Q, Mesmar J, Yang C, Gilroy EM, McLellan H, Yang C, Craig A, Bailey M, Zhang C, Moore JD, Boevink PC, Tian Z, Birch PRJ*, Sadanandom A* (2017) BTB-BACK domain protein POB1 suppresses immune cell death by targeting ubiquitin E3 ligase PUB17 for degradation. PLoS Genetics, 13:e1005640.
- Eves van den Akker S, Birch PRJ (2016) Opening the effector protein toolbox in plant-cyst nematode interactions. Molecular Plant doi: 10.1016/j.molp.2016.09.008.
- Whisson SC, Boevink PC, Wang S, Birch PRJ (2016) The Cell biology of late blight disease. Curr Opinion in Microbiol. 34:127-135.
- Boevink P, McLellan H, Gilroy E, Naqvi S, He Q, Yang L, Wang X, Turnbull D, Armstrong M, Tian Z, Birch PRJ (2016) Oomycetes seek help from the plant: Phytophthora infestans effectors target host susceptibility factors. Molecular Plant 7:10311
- Yang L, Naqvi S, He Q, McLellan H, Boevink PC, Armstrong M, Wei Z, Tian Z, Zhan J, Gilroy EM, Birch PRJ (2016). Potato NPH3/RPT2-like protein StNRL1, targeted by a Phytophthora infestans RXLR effector, is a susceptibility factor. Plant Physiology, 171:645-57.
- Boevink P, Wang X, McLellan H, He Q, Naqvi S, Armstrong M, Wei Z, Hein I, Gilroy E, Tian Z, Birch PRJ (2016). A Phytophthora infestans RXLR effector targets plant PP1c isoforms that promote late blight disease Nature Communications 7:10311.
- Wang X, Boevink PC, McLellan M, Armstrong M, Bukharova T, Qin Z, Birch PRJ (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.
- Fry W, Birch PRJ, Judelson HS, Grunwald N, Danies G, Everts KL, Gevens AJ, Gugino BK, Johnson DA, Johnson SB, McGrath MT, Myers KL, Ristaino JB, Roberts PD, Secor G, Smart CD (2015) Re-emerging Phytophthora infestans. Phytopathology 105:966-981.
- He Q, McLellan H, Boevink P, Sadanandom A, Xie C, Birch PRJ*, Tian Z* (2015) U-Box ubiquitin E3 ligase StPUB17 contributes to basal immunity to Phytophthora infestans in potato. J Exp Bot. 66:3189-3199.
- Kamoun S, et al (2015) The top 10 oomycete pathogens in molecular plant pathology. Mol Plant Pathol 16:413-434.
- Pritchard L, Birch PR (2014) The Zigzag model of plant-microbe interactions: is it time to move on? Mol Plant Pathol 15:865-870.
- King SRF, McLellan H, Boevink PC, Armstrong MA, Hall B, Sukarta O, Bukharova T, Kamoun S, Birch PRJ, Banfield M (2014). The Phytophthora infestans RXLR effector RD2 interacts with host MAP3Ke to suppress plant immunity related signalling. The Plant Cell 26:1345-1359.
- Zheng X, Fraiture M, Xiaoyu, L, McLellan H, Gilroy E, Boevink P, Ying C, Kandel K, Birch PRJ*, Brunner F* (2014) A subset of RXLR effectors from Phytophthora infestans suppress flg22-triggered early signalling in both Arabidopsis and tomato. PLoS Pathogens 10(4): e1004057.
- McLellan H, Armstrong M, Boevink P, Pritchard L, Gomez S, Morales J, Whisson SC, Beynon, JL, Birch PRJ (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(10): e1003670.
- Birch PRJ, Bryan G, Fenton B, Gilroy EM, Hein I, Jones J, Taylor M, Torrance L, Toth IK (2012) Crops that feed the world. Potato: are the trends of increased global production sustainable? Food Security 4:477-508.
- Wawra S, Agacan M, Boodey J, Davidson I, Gachon C, Zanda M, Grouffaud S, Whisson SC, Birch PRJ, Porter A, van West P (2012) The avirulence protein 3a (AVR3a) from Phytophthora infestans forms homodimers through its predicted translocation region and does not bind phospholipids. J Biol Chem 287:38101-38109.
- Engelhardt S, Boevink P, Armstrong M, Ramos MB, Hein I, Birch PRJ (2012) Re-localisation of late blight resistance protein R3a to endosomal compartments is associated with effector recognition and required for the immune response. The Plant Cell 24:5142-5458, doi/10.1105/tpc.112.104992.
- Cooke D, Cano L, Raffaele S, Bain R, Cooke L, Etherington G, Deahl K, Farrer R, Gilroy E, Goss E, Grunwald N, Hein I, MacLean D, Randall E, Oliva R, Pel M, Shaw D, Squires J, Taylor M, Vleeshouwers V, Birch PRJ, Lees A, Kamoun S (2012) Genome analyses of an aggressive and invasive lineage of the Irish Potato famine pathogen. PLoS Pathogens. 8(10):e1002940 doi: 10.1371/journal.ppat.1002940.
- Saunders D, Breen S, Schornack S, Win J, Hein I, Bozkurt T, Champouret N, Vleeshouwers V, Birch PRJ, Gilroy EM, Kamoun S (2012) Host protein BSL1 associates with Phytophthora infestans RXLR effector PiAVR2 and the immune receptor R2 to mediate disease resistance. The Plant Cell 24:3420-3434.
- Wawra, S, Bain J, Durward E, de Bruijn I, Minor K, Matena A, Whisson S, Bayer P, Porter A, Birch PRJ, Secombes C, van West P (2012) Host-targeting protein 1 (SpHTP1) from the oomycete Saprolegnia parasitica translocates specifically into fish cells in a tyrosine-O-sulphate-dependent manner. Proc. Natl. Acad. Sci. (USA) 109:2096