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).
Cai Q, He B, Wang S, Fletcher S, Niu D, Mitter N, Birch PRJ, Jin H. 2021. Message in a Bubble: Shuttling Small RNAs and Proteins Between Cells and Interacting Organisms Using Extracellular Vesicles. Annual Review of Plant Biology. 72:497-524. https://doi.org/10.1146/annurev-arplant-081720-010616
McLellan H, Armstrong MR, Birch PRJ. 2021. Yeast Two-Hybrid Screening for Identification of Protein-Protein Interactions in Solanum tuberosum. Dobnik D, Gruden K, Ramšak Ž, Coll A, editors. In Solanum tuberosum: Methods and Protocols. 1 ed. New York: Humana Press. pp. 95-110. (Methods in Molecular Biology). https://doi.org/10.1007/978-1-0716-1609-3_4
Wang S, Vetukuri RR, Kushwaha SK, Hedley PE, Morris J, Studholme DJ, Welsh LRJ, Boevink PC, Birch PRJ, Whisson SC. 2021. Haustorium formation and a distinct biotrophic transcriptome characterize infection of Nicotiana benthamiana by the tree pathogen Phytophthora kernoviae. Molecular Plant Pathology. 22(8):954-968. https://doi.org/10.1111/mpp.13072
Wang H, Trusch F, Turnbull D, Aguilera-Galvez C, Breen S, Naqvi S, Jones JDG, Hein I, Tian Z, Vleeshouwers V, Gilroy E, Birch PRJ. 2021. Evolutionarily distinct Resistance proteins detect a pathogen effector through its association with different host targets. New Phytologist. 232(3):1368-1381. https://doi.org/10.1111/nph.17660
Boevink PC, Birch PRJ, Turnbull D, Whisson SC. 2020. Devastating intimacy: the cell biology of plant-Phytophthora interactions. New Phytologist. https://doi.org/10.1111/nph.16650
He Q, McLellan H, Boevink PC, Birch PRJ. (2020). All roads lead to susceptibility: the many modes-of-action of fungal and oomycete intracellular effectors. Plant Communications. Article 100050. https://doi.org/10.1016/j.xplc.2020.100050
Lin X, Wang S, de Rond L, Bertolin N, Wouters RHM, Wouters D, Domazakis E, Bitew MK, Win J, Dong S, Visser RGF, Birch P, Kamoun S, Vleeshouwers VGAA. (2020). Divergent Evolution of PcF/SCR74 Effectors in Oomycetes Is Associated with Distinct Recognition Patterns in Solanaceous Plants. MBio. 11(3):Article e00947-20. https://doi.org/10.1128/mBio.00947-20
McLellan H, Chen K, He Q, Wu X, Boevink PC, Tian Z, Birch PRJ (2020) The ubiquitin E3 ligase PUB17 positively regulates immunity by targeting a negative regulator, KH17, for degradation. Plant Communications DOI:https://doi.org/10.1016/j.xplc.2020.100020
He Q, McLellan H, Hughes R, Boevink P, Armstrong M, Lu Y, Banfield M, Tian Z, Birch PRJ (2019) Phytophthora infestans RXLR effector SFI3 targets potato UBK to suppress early PAMP-triggered immune responses. New Phytologist 222:438-454; doi: 10.1111/nph.15635.
Ren Y, Armstrong M, Qi Y, McLellan H, Zhong C, Wang H, Zhou J, Birch PRJ, Tian Z (2019) Phytophthora infestans effectors target parallel steps in an immune signal transduction pathway. Plant Physiol 180:2227-2239.
Thilliez G, Tze-Yin Lim J, Baker K, Armstrong M, Huitema E, Birch PRJ, Hein I (2019). Pathogenicity factor enrichment and sequencing enables massively parallel diagnostic analysis of avirulence genes and revised genome annotation of Phytophthora infestans RXLR effectors. New Phytologist doi: 10.1111/nph.15441
Turnbull D, Wang H, Breen S, Malek M, Naqvi S, Yang L, Welsh L, Hemsley P, Tian Z, Brunner F, Gilroy EM, Birch PRJ (2019) Phytophthora infestans Avr2 targets BSL phosphatases as susceptibility factors to suppress host immunity and enhance late blight disease. Plant Physiol 180(1):571-581.
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, Whisson S, Hein I, Wang X, Tian Z, Birch PRJ, Boevink P (2019) Phytophthora infestans RXLR Effectors act in concert at diverse subcellular localisations to enhance host colonisation. J Exp Bot. 70(1):343-356. doi: 10.1093/jxb/ery360.
He Q, Naqvi S, McLellan H, Boevink P, Champouret N, Hein I, Birch PRJ (2018) A Phytophthora infestans RXLR effector associates with host Susceptibility factor NRL1 to degrade the positive immune regulator SWAP70. Proc Natl Acad Sci (USA) 115:E7834-E7843 doi: 10.1073/pnas.1808585115.
Lilley C, Maqbool A, Wu D, Yusup H, Jones LM, Birch PRJ, Banfield M, Urwin PE, Eves-van-den-Akker S (2018). Effector gene birth in plant parasitic nematodes: Neofunctionalization of a housekeeping glutathione synthetase gene. PLoS Genetics 14(4):e1007310. doi: 10.1371/journal.pgen.1007310.
Murphy F, He Q, Armstrong A., Giuliani L, Tian Z, Birch PRJ, Gilroy EM (2018) Potato MAP3K StVIK is an S factor required for Phytophthora infestans RXLR Effector 17316 to promote disease. Plant Physiol. 177:398-410.
Thordal-Christensen H, Birch PRJ, Spanu P, Panstruga R (2018) Why did filamentous plant pathogens evolve the potential to secrete hundreds of effectors to enable disease? Mol Plant Pathol 19:781-785.
Wang S, Welsh L, Thorpe P, Whisson S, Boevink P, Birch PRJ (2018) The Phytophthora infestans haustorium is a site for secretion of diverse classes of infection-associated proteins. mBio pii:e01216-18.
Zheng X, Wagener N, McLellan H, Boevink P, Hua C, Birch PRJ, Brunner F (2018). Phytophthora infestans RXLR effector SFI5 requires association with calmodulin for PTI/MTI suppressing activity. New Phytologist 219:1433-1446.
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 214:1657-1672.
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.
Turnbull D, Yang L, Naqvi S, Breen S, Welsh L, Stevens J, Morris J, Boevink P, Hedley P, Zhan J, Birch PRJ, Gilroy EM (2017) Phytophthora infestans AVR2 up-regulates the brassinosteroid responsive bHLH StCHL1 to antagonise immunity. Plant Physiology 174:356-369.#
Wang S, Boevink P, Welsh L, Zhang R, Whisson S, Birch PRJ (2017). Delivery of Cytoplasmic and Apoplastic Effectors from Phytophthora infestans Haustoria by Distinct Secretion Pathways. New Phytologist 216:205-215.
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 9:636-638
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.
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.
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.