Imperial College London

Dr Tolga Bozkurt

Faculty of Natural SciencesDepartment of Life Sciences

Reader in Molecular Plant-Microbe
 
 
 
//

Contact

 

+44 (0)20 7594 5381o.bozkurt

 
 
//

Location

 

6167Sir Alexander Fleming BuildingSouth Kensington Campus

//

Summary

 

Publications

Publication Type
Year
to

77 results found

Guder F, Coatsworth P, Bozkurt O, Cotur Y, Collins AS-P, Olenik S, Zhou Z, Naik A, Asfour T, Gonzalez-Macia L, Chao D-Yet al., 2024, Time-resolved chemical monitoring of whole plant roots with printed electrochemical sensors and machine learning, Science Advances, Vol: 10, ISSN: 2375-2548

Traditional single-point measurements fail to capture dynamic chemical responses of plants, which are complex, nonequilibrium biological systems. We report TETRIS (time-resolved electrochemical technology for plant root environment in situ chemical sensing), a real-time chemical phenotyping system for continuously monitoring chemical signals in the often-neglected plant root environment. TETRIS consisted of low-cost, highly scalable screen-printed electrochemical sensors for monitoring concentrations of salt, pH, and H2O2 in the root environment of whole plants, where multiplexing allowed for parallel sensing operation. TETRIS was used to measure ion uptake in tomato, kale, and rice and detected differences between nutrient and heavy metal ion uptake. Modulation of ion uptake with ion channel blocker LaCl3 was monitored by TETRIS and machine learning used to predict ion uptake. TETRIS has the potential to overcome the urgent “bottleneck” in high-throughput screening in producing high-yielding plant varieties with improved resistance against stress.

Journal article

King F, Yuen ELH, Bozkurt TO, 2023, Border Control: Manipulation of the Host-Pathogen Interface by Perihaustorial Oomycete Effectors., Mol Plant Microbe Interact, ISSN: 0894-0282

Filamentous plant pathogens, including fungi and oomycetes, cause some of the most devastating plant diseases. These organisms serve as ideal models for understanding the intricate molecular interplay between plants and the invading pathogens. Filamentous pathogens secrete effector proteins via haustoria, specialised structures for infection and nutrient uptake, to suppress the plant immune response and to reprogram plant metabolism. Recent advances in cell biology have provided crucial insights into the biogenesis of the extrahaustorial membrane and the redirection of host endomembrane trafficking towards this interface. Functional studies have shown that an increasing number of oomycete effectors accumulate at the perihaustorial interface to subvert plant focal immune responses, with a particular convergence on targets involved in host endomembrane trafficking. In this review, we summarise the diverse mechanisms of perihaustorial effectors from oomycetes and pinpoint pressing questions regarding their role in manipulating host defense and metabolism at the haustorial interface.

Journal article

Moratto E, Rothery S, Bozkurt TO, Sena Get al., 2023, Enhanced germination and electrotactic behaviour of Phytophthora palmivora zoospores in weak electric fields, Physical Biology, Vol: 20, Pages: 1-10, ISSN: 1478-3967

Soil-dwelling microorganisms use a variety of chemical and physical signals to navigate their environment. Plant roots produce endogenous electric fields which result in characteristic current profiles. Such electrical signatures are hypothesised to be used by pathogens and symbionts to track and colonise plant roots.
The oomycete pathogen Phytophthora palmivora generates motile zoospores which swim towards the positive pole when exposed to an external electric field in vitro.
Here, we provide a quantitative characterization of their electrotactic behaviour in 3D. We found that a weak electric field (0.7 - 1.0 V/cm) is sufficient to induce an accumulation of zoospore at the positive pole, without affecting their encystment rate. We also show that the same external electric field increases the zoospore germination rate and orients the germ tube's growth. We conclude that several early stages of the P. palmivora infection cycle are affected by external electric fields.
Taken together, our results are compatible with the hypothesis that pathogens use plant endogenous electric fields for host targeting.

Journal article

Shepherd S, Yuen ELH, Carella P, Bozkurt TOet al., 2023, The wheels of destruction: Plant NLR immune receptors are mobile and structurally dynamic disease resistance proteins, CURRENT OPINION IN PLANT BIOLOGY, Vol: 74, ISSN: 1369-5266

Journal article

Contreras MP, Pai H, Selvaraj M, Toghani A, Lawson DM, Tumtas Y, Duggan C, Yuen ELH, Stevenson CEM, Harant A, Maqbool A, Wu C-H, Bozkurt TO, Kamoun S, Derevnina Let al., 2023, Resurrection of plant disease resistance proteins via helper NLR bioengineering, SCIENCE ADVANCES, Vol: 9, ISSN: 2375-2548

Journal article

Contreras MP, Pai H, Tumtas Y, Duggan C, Yuen ELH, Cruces AV, Kourelis J, Ahn H-K, Lee K-T, Wu C-H, Bozkurt TO, Derevnina L, Kamoun Set al., 2023, Sensor NLR immune proteins activate oligomerization of their NRC helpers in response to plant pathogens, The EMBO Journal, Vol: 42, ISSN: 0261-4189

Nucleotide‐binding domain leucine‐rich repeat (NLR) immune receptors are important components of plant and metazoan innate immunity that can function as individual units or as pairs or networks. Upon activation, NLRs form multiprotein complexes termed resistosomes or inflammasomes. Although metazoan paired NLRs, such as NAIP/NLRC4, form hetero‐complexes upon activation, the molecular mechanisms underpinning activation of plant paired NLRs, especially whether they associate in resistosome hetero‐complexes, is unknown. In asterid plant species, the NLR required for cell death (NRC) immune receptor network is composed of multiple resistance protein sensors and downstream helpers that confer immunity against diverse plant pathogens. Here, we show that pathogen effector‐activation of the NLR proteins Rx (confers virus resistance), and Bs2 (confers bacterial resistance) leads to oligomerization of their helper NLR, NRC2. Activated Rx does not oligomerize or enter into a stable complex with the NRC2 oligomer and remains cytoplasmic. In contrast, activated NRC2 oligomers accumulate in membrane‐associated puncta. We propose an activation‐and‐release model for NLRs in the NRC immune receptor network. This points to a distinct activation model compared with mammalian paired NLRs.

Journal article

Ibrahim T, Khandare V, Mirkin FG, Tumtas Y, Bubeck D, Bozkurt TOet al., 2023, AlphaFold2-multimer guided high-accuracy prediction of typical and atypical ATG8-binding motifs, PLoS Biology, Vol: 21, Pages: 1-19, ISSN: 1544-9173

Macroautophagy/autophagy is an intracellular degradation process central to cellular homeostasis and defense against pathogens in eukaryotic cells. Regulation of autophagy relies on hierarchical binding of autophagy cargo receptors and adaptors to ATG8/LC3 protein family members. Interactions with ATG8/LC3 are typically facilitated by a conserved, short linear sequence, referred to as the ATG8/LC3 interacting motif/region (AIM/LIR), present in autophagy adaptors and receptors as well as pathogen virulence factors targeting host autophagy machinery. Since the canonical AIM/LIR sequence can be found in many proteins, identifying functional AIM/LIR motifs has proven challenging. Here, we show that protein modelling using Alphafold-Multimer (AF2-multimer) identifies both canonical and atypical AIM/LIR motifs with a high level of accuracy. AF2-multimer can be modified to detect additional functional AIM/LIR motifs by using protein sequences with mutations in primary AIM/LIR residues. By combining protein modelling data from AF2-multimer with phylogenetic analysis of protein sequences and protein-protein interaction assays, we demonstrate that AF2-multimer predicts the physiologically relevant AIM motif in the ATG8-interacting protein 2 (ATI-2) as well as the previously uncharacterized noncanonical AIM motif in ATG3 from potato (Solanum tuberosum). AF2-multimer also identified the AIM/LIR motifs in pathogen-encoded virulence factors that target ATG8 members in their plant and human hosts, revealing that cross-kingdom ATG8-LIR/AIM associations can also be predicted by AF2-multimer. We conclude that the AF2-guided discovery of autophagy adaptors/receptors will substantially accelerate our understanding of the molecular basis of autophagy in all biological kingdoms.

Journal article

Adachi H, Sakai T, Harant AO, Pai H, Honda K, Toghani A, Claeys J, Duggan C, Bozkurt T, Wu C-H, Kamoun Set al., 2023, An atypical NLR protein modulates the NRC immune receptor network in <i>Nicotiana benthamiana</i>, PLOS GENETICS, Vol: 19, ISSN: 1553-7404

Journal article

Coatsworth P, Gonzalez-Macia L, Collins ASP, Bozkurt T, Gueder Fet al., 2023, Continuous monitoring of chemical signals in plants under stress, NATURE REVIEWS CHEMISTRY, Vol: 7, Pages: 7-25

Journal article

Yuen ELH, Shepherd S, Bozkurt TO, 2023, Traffic Control: Subversion of Plant Membrane Trafficking by Pathogens, ANNUAL REVIEW OF PHYTOPATHOLOGY, Vol: 61, Pages: 325-350, ISSN: 0066-4286

Journal article

Zess EK, Dagdas YF, Peers E, Maqbool A, Banfield MJ, Bozkurt TO, Kamoun Set al., 2022, Regressive evolution of an effector following a host jump in the Irish potato famine pathogen lineage, PLOS PATHOGENS, Vol: 18, ISSN: 1553-7366

Journal article

Leong JX, Raffeiner M, Spinti D, Langin G, Franz-Wachtel M, Guzman AR, Kim J-G, Pandey P, Minina AE, Macek B, Hafren A, Bozkurt TO, Mudgett MB, Boernke F, Hofius D, Uestuen Set al., 2022, A bacterial effector counteracts host autophagy by promoting degradation of an autophagy component, EMBO JOURNAL, Vol: 41, ISSN: 0261-4189

Journal article

Adachi H, Sakai T, Harant A, Duggan C, Bozkurt TO, Wu C-H, Kamoun Set al., 2021, An atypical NLR protein modulates the NRC immune receptor network

<jats:title>ABSTRACT</jats:title><jats:p>The NRC immune receptor network has evolved in asterid plants from a pair of linked genes into a genetically dispersed and phylogenetically structured network of sensor and helper NLR (nucleotide-binding domain and leucine-rich repeat-containing) proteins. In some species, such as the model plant <jats:italic>Nicotiana benthamiana</jats:italic> and other Solanaceae, the NRC network forms up to half of the NLRome, and NRCs are scattered throughout the genome in gene clusters of varying complexities. Here, we describe NRCX, an atypical, but essential member of the NRC family that lacks canonical features of these NLR helper proteins, such as a functional N-terminal MADA motif and the capacity to trigger autoimmunity. In contrast to other NRCs, systemic gene silencing of <jats:italic>NRCX</jats:italic> markedly impairs plant growth resulting in a dwarf phenotype. Remarkably, dwarfism of <jats:italic>NRCX</jats:italic> silenced plants is partially dependent on NRCX paralogs NRC2 and NRC3, but not NRC4. Despite its negative impact on plant growth when silenced systemically, transient RNA interference of <jats:italic>NRCX</jats:italic> in mature <jats:italic>N. benthamiana</jats:italic> leaves doesn’t result in visible cell death phenotypes. However, alteration of <jats:italic>NRCX</jats:italic> expression modulates the hypersensitive response mediated by NRC2 and NRC3 in a manner consistent with a negative role for NRCX in the NRC network. We conclude that NRCX is an atypical member of the NRC network that has evolved to contribute to the homeostasis of this genetically unlinked NLR network.</jats:p>

Journal article

Zess EK, Dagdas YF, Peers E, Maqbool A, Banfield MJ, Bozkurt TO, Kamoun Set al., 2021, Regressive evolution of an effector following a host jump in the Irish Potato Famine Pathogen Lineage

<jats:title>Abstract</jats:title><jats:p>In order to infect a new host species, the pathogen must evolve to enhance infection and transmission in the novel environment. Although we often think of evolution as a process of accumulation, it is also a process of loss. Here, we document an example of regressive evolution in the Irish potato famine pathogen (<jats:italic>Phytophthora infestans</jats:italic>) lineage, providing evidence that a key sequence motif in the effector PexRD54 has degenerated following a host jump. We began by looking at PexRD54 and PexRD54-like sequences from across<jats:italic>Phytophthora</jats:italic>species. We found that PexRD54 emerged in the common ancestor of<jats:italic>Phytophthora</jats:italic>clade 1b and 1c species, and further sequence analysis showed that a key functional motif, the C-terminal ATG8-interacting motif (AIM), was also acquired at this point in the lineage. A closer analysis showed that the<jats:italic>P. mirabilis</jats:italic>PexRD54 (PmPexRD54) AIM appeared unusual, the otherwise-conserved central residue mutated from a glutamate to a lysine. We aimed to determine whether this PmPexRD54 AIM polymorphism represented an adaptation to the<jats:italic>Mirabilis jalapa</jats:italic>host environment. We began by characterizing the<jats:italic>M. jalapa</jats:italic>ATG8 family, finding that they have a unique evolutionary history compared to previously characterized ATG8s. Then, using co-immunoprecipitation and isothermal titration calorimetry assays, we showed that both full-length PmPexRD54 and the PmPexRD54 AIM peptide bind very weakly to the<jats:italic>M. jalapa</jats:italic>ATG8s. Through a combination of binding assays and structural modelling, we showed that the identity of the residue at the position of the PmPexRD54 AIM polymorphism can underpin high-affinity binding to plant ATG8s. Finally, we conclude that th

Journal article

Bozkurt O, Savage Z, Duggan C, 2021, Chloroplasts alter their morphology and accumulate at the pathogen interface during infection by Phytophthora infestans, The Plant Journal, Vol: 107, Pages: 1771-1787, ISSN: 0960-7412

Upon immune activation, chloroplasts switch off photosynthesis, produce anti-microbial compounds, and associate with the nucleus through tubular extensions called stromules. Although it is well-established that chloroplasts alter their position in response to light, little is known about the dynamics of chloroplasts movement in response to pathogen attack. Here, we report that chloroplasts accumulate at the pathogen interface during infection by the Irish potato famine pathogen Phytophthora infestans, associating with the specialized membrane that engulfs the pathogen haustorium. Chemical inhibition of actin polymerization reduces the accumulation of chloroplasts at the pathogen haustoria, suggesting this process is partially dependent on the actin cytoskeleton. However, chloroplast accumulation at haustoria does not necessarily rely on movement of the nucleus to this interface and is not affected by light conditions. Stromules are typically induced during infection, embracing haustoria and facilitating chloroplast interactions, to form dynamic organelle clusters. We found that infection-triggered stromule formation relies on BRASSINOSTEROID INSENSITIVE 1-ASSOCIATED KINASE 1 (BAK1) mediated surface immune signaling, whereas chloroplast repositioning towards haustoria does not. Consistent with the defense-related induction of stromules, effector mediated suppression of BAK1 mediated immune signaling reduced stromule formation during infection. On the other hand, immune recognition of the same effector stimulated stromules, presumably via a different pathway. These findings implicate chloroplasts in a polarized response upon pathogen attack and point to more complex functions of these organelles in plant-pathogen interactions.

Journal article

Duggan C, Moratto E, Savage Z, Hamilton E, Adachi H, Wu C-H, Leary AY, Tumtas Y, Rothery SM, Maqbool A, Nohut S, Martin TR, Kamoun S, Bozkurt Oet al., 2021, Dynamic localization of a helper NLR at the plant-pathogen interface underpins pathogen recognition, Proceedings of the National Academy of Sciences of USA, Vol: 118, Pages: 1-12, ISSN: 0027-8424

Plants employ sensor-helper pairs of NLR immune receptors to recognize pathogen effectors and activate immune responses (1). Yet the subcellular localization of NLRs pre- and post-activation during pathogen infection remains poorly understood. Here we show that NRC4, from the ‘NRC’ solanaceous helper NLR family (1), undergoes dynamic changes in subcellular localization by shuttling to and from the plant-pathogen haustorium interface established during infection by the Irish potato famine pathogen Phytophthora infestans. Specifically, prior to activation, NRC4 accumulates at the extra-haustorial membrane (EHM), presumably to mediate response to perihaustorial effectors, that are recognized by NRC4- dependent sensor NLRs. However not all NLRs accumulate at the EHM, as the closely related helper NRC2, and the distantly related ZAR1, did not accumulate at the EHM. NRC4 required an intact N-terminal coiled coil domain to accumulate at the EHM, whereas the functionally conserved MADA motif implicated in cell death activation and membrane insertion was dispensable for this process. Strikingly, a constitutively autoactive NRC4 mutant did not accumulate at the EHM and showed punctate distribution that mainly associated with the plasma membrane, suggesting that post-activation, NRC4 may undergo a conformation switch to form clusters that do not preferentially associate with the EHM. When NRC4 is activated by a sensor NLR during infection however, NRC4 forms puncta mainly at the EHM and to a lesser extent at the plasma membrane. We conclude that following activation at the EHM, NRC4 may spread to other cellular membranes from its primary site of activation to trigger immune responses.

Journal article

Bozkurt O, 2021, An oomycete effector subverts host vesicle trafficking to channel starvation-induced autophagy to the pathogen interface, eLife, Vol: 10, Pages: 1-35, ISSN: 2050-084X

Eukaryotic cells deploy autophagy to eliminate invading microbes. In turn, pathogens have evolved effector proteins to counteract antimicrobial autophagy. How adapted pathogens co opt autophagy for their own benefit is poorly understood. The Irish famine pathogen Phytophthora infestans secretes the effector protein PexRD54 that selectively activates an unknown plant autophagy pathway that antagonizes antimicrobial autophagy at the pathogen interface. Here we show that PexRD54 induces autophagosome formation by bridging vesicles decorated by the small GTPase Rab8a with autophagic compartments labelled by the core autophagy protein ATG8CL. Rab8a is required for pathogen-triggered and starvation induced but not antimicrobial autophagy, revealing specific trafficking pathways underpin selective autophagy. By subverting Rab8a mediated vesicle trafficking, PexRD54 utilizes lipid droplets to facilitate biogenesis of autophagosomes diverted to pathogen feeding sites. Altogether, we show that PexRD54 mimics starvation-induced autophagy to subvert endomembrane trafficking at the host-pathogen interface, revealing how effectors bridge distinct host compartments to expedite colonization.

Journal article

Petre B, Contreras MP, Bozkurt TO, Schattat MH, Sklenar J, Schornack S, Abd-El-Haliem A, Castells-Graells R, Lozano-Duran R, Dagdas YF, Menke FLH, Jones AME, Vossen JH, Robatzek S, Kamoun S, Win Jet al., 2021, Host-interactor screens of Phytophthora infestans RXLR proteins reveal vesicle trafficking as a major effector-targeted process, The Plant Cell, Vol: 33, Pages: 1447-1471, ISSN: 1040-4651

Pathogens modulate plant cell structure and function by secreting effectors into host tissues. Effectors typically function by associating with host molecules and modulating their activities. This study aimed to identify the host processes targeted by the RXLR class of host-translocated effectors of the potato blight pathogen Phytophthora infestans. To this end, we performed an in planta protein-protein interaction screen by transiently expressing P. infestans RXLR effectors in Nicotiana benthamiana leaves followed by co-immunoprecipitation and liquid chromatography tandem mass spectrometry. This screen generated an effector-host protein interactome matrix of 59 P. infestans RXLR effectors x 586 N. benthamiana proteins. Classification of the host interactors into putative functional categories revealed over 35 biological processes possibly targeted by P. infestans. We further characterized the PexRD12/31 family of RXLR-WY effectors, which associate and co-localize with components of the vesicle trafficking machinery. One member of this family, PexRD31, increased the number of FYVE positive vesicles in N. benthamiana cells. FYVE positive vesicles also accumulated in leaf cells near P. infestans hyphae, indicating that the pathogen may enhance endosomal trafficking during infection. This interactome data set will serve as a useful resource for functional studies of P. infestans effectors and of effector-targeted host processes.

Journal article

Leong JX, Raffeiner M, Spinti D, Langin G, Franz-Wachtel M, Guzman AR, Kim J-G, Pandey P, Minina AE, Macek B, Hafrén A, Bozkurt TO, Mudgett MB, Börnke F, Hofius D, Üstün Set al., 2021, A bacterial effector counteracts host autophagy by promoting degradation of an autophagy component

<jats:title>Abstract</jats:title><jats:p>Beyond its role in cellular homeostasis, autophagy plays anti- and pro-microbial roles in host-microbe interactions, both in animals and plants. One prominent role of anti-microbial autophagy is to degrade intracellular pathogens or microbial molecules, in a process termed xenophagy. Consequently, microbes evolved mechanisms to hijack or modulate autophagy to escape elimination. Although well-described in animals, the extent to which xenophagy contributes to plant-bacteria interactions remains unknown. Here, we provide evidence that <jats:italic>Xanthomonas campestris</jats:italic> pv. <jats:italic>vesicatoria (Xcv)</jats:italic> suppresses host autophagy by utilizing type-III effector XopL. XopL interacts with and degrades the autophagy component SH3P2 via its E3 ligase activity to promote infection. Intriguingly, XopL is targeted for degradation by defense-related selective autophagy mediated by NBR1/Joka2, revealing a complex antagonistic interplay between XopL and the host autophagy machinery. Our results implicate plant antimicrobial autophagy in depletion of a bacterial virulence factor and unravels an unprecedented pathogen strategy to counteract defense-related autophagy.</jats:p>

Journal article

Duggan C, Moratto E, Savage Z, Hamilton E, Adachi H, Wu C-H, Leary AY, Tumtas Y, Rothery SM, Maqbool A, Nohut S, Kamoun S, Bozkurt TOet al., 2021, Dynamic accumulation of a helper NLR at the plant-pathogen interface underpins pathogen recognition

<jats:title>Abstract</jats:title><jats:p>Plants employ sensor-helper pairs of NLR immune receptors to recognize pathogen effectors and activate immune responses. Yet the subcellular localization of NLRs pre- and post-activation during pathogen infection remains poorly known. Here we show that NRC4, from the ‘NRC’ solanaceous helper NLR family, undergoes dynamic changes in subcellular localization by shuttling to and from the plant-pathogen haustorium interface established during infection by the Irish potato famine pathogen <jats:italic>Phytophthora infestans.</jats:italic> Specifically, prior to activation, NRC4 accumulates at the extra-haustorial membrane (EHM), presumably to mediate response to perihaustorial effectors, that are recognized by NRC4-dependent sensor NLRs. However not all NLRs accumulate at the EHM, as the closely related helper NRC2, and the distantly related ZAR1, did not accumulate at the EHM. NRC4 required an intact N-terminal coiled coil domain to accumulate at the EHM, whereas the functionally conserved MADA motif implicated in cell death activation and membrane insertion was dispensable for this process. Strikingly, a constitutively autoactive NRC4 mutant did not accumulate at the EHM and showed punctate distribution that mainly associated with the plasma membrane, suggesting that post-activation, NRC4 probably undergoes a conformation switch to form clusters that do not preferentially associate with the EHM. When NRC4 is activated by a sensor NLR during infection however, NRC4 formed puncta mainly at the EHM and to a lesser extent at the plasma membrane. We conclude that following activation at the EHM, NRC4 may spread to other cellular membranes from its primary site of activation to trigger immune responses.</jats:p><jats:sec><jats:title>Significance statement</jats:title><jats:p>Plant NLR immune receptors function as intracellular sensors of pathogen virulence factors

Journal article

Klionsky DJ, Abdel-Aziz AK, Abdelfatah S, Abdellatif M, Abdoli A, Abel S, Abeliovich H, Abildgaard MH, Abudu YP, Acevedo-Arozena A, Adamopoulos IE, Adeli K, Adolph TE, Adornetto A, Aflaki E, Agam G, Agarwal A, Aggarwal BB, Agnello M, Agostinis P, Agrewala JN, Agrotis A, Aguilar P, Ahmad ST, Ahmed ZM, Ahumada-Castro U, Aits S, Aizawa S, Akkoc Y, Akoumianaki T, Akpinar HA, Al-Abd AM, Al-Akra L, Al-Gharaibeh A, Alaoui-Jamali MA, Alberti S, Alcocer-Gomez E, Alessandri C, Ali M, Al-Bari MAA, Aliwaini S, Alizadeh J, Almacellas E, Almasan A, Alonso A, Alonso GD, Altan-Bonnet N, Altieri DC, Alves S, da Costa CA, Alzaharna MM, Amadio M, Amantini C, Amaral C, Ambrosio S, Amer AO, Ammanathan V, An Z, Andersen SU, Andrabi SA, Andrade-Silva M, Andres AM, Angelini S, Ann D, Anozie UC, Ansari MY, Antas P, Antebi A, Anton Z, Anwar T, Apetoh L, Apostolova N, Araki T, Araki Y, Arasaki K, Araujo WL, Araya J, Arden C, Arevalo M-A, Arguelles S, Arias E, Arikkath J, Arimoto H, Ariosa AR, Armstrong-James D, Arnaune-Pelloquin L, Aroca A, Arroyo DS, Arsov I, Artero R, Asaro DML, Aschner M, Ashrafizadeh M, Ashur-Fabian O, Atanasov AG, Au AK, Auberger P, Auner HW, Aurelian L, Autelli R, Avagliano L, Avalos Y, Aveic S, Aveleira CA, AvinWittenberg T, Aydin Y, Ayton S, Ayyadevara S, Azzopardi M, Baba M, Backer JM, Backues SK, Bae D-H, Bae O-N, Bae SH, Baehrecke EH, Baek A, Baek S-H, Baek SH, Bagetta G, Bagniewska-Zadworna A, Bai H, Bai J, Bai X, Bai Y, Bairagi N, Baksi S, Balbi T, Baldari CT, Balduini W, Ballabio A, Ballester M, Balazadeh S, Balzan R, Bandopadhyay R, Banerjee S, Banerjee S, Bao Y, Baptista MS, Baracca A, Barbati C, Bargiela A, Barila D, Barlow PG, Barmada SJ, Barreiro E, Barreto GE, Bartek J, Bartel B, Bartolome A, Barve GR, Basagoudanavar SH, Bassham DC, Jr RCB, Basu A, Batoko H, Batten I, Baulieu EE, Baumgarner BL, Bayry J, Beale R, Beau I, Beaumatin F, Bechara LRG, Beck GR, Beers MF, Begun J, Behrends C, Behrens GMN, Bei R, Bejarano E, Bel S, Behl C, Belaid A, Belgareh-Touzeet al., 2021, Guidelines for the use and interpretation of assays for monitoring autophagy (4th edition), Autophagy, Vol: 17, Pages: 1-382, ISSN: 1554-8627

In 2008, we published the first set of guidelines for standardizing research in autophagy. Since then, this topic has received increasing attention, and many scientists have entered the field. Our knowledge base and relevant new technologies have also been expanding. Thus, it is important to formulate on a regular basis updated guidelines for monitoring autophagy in different organisms. Despite numerous reviews, there continues to be confusion regarding acceptable methods to evaluate autophagy, especially in multicellular eukaryotes. Here, we present a set of guidelines for investigators to select and interpret methods to examine autophagy and related processes, and for reviewers to provide realistic and reasonable critiques of reports that are focused on these processes. These guidelines are not meant to be a dogmatic set of rules, because the appropriateness of any assay largely depends on the question being asked and the system being used. Moreover, no individual assay is perfect for every situation, calling for the use of multiple techniques to properly monitor autophagy in each experimental setting. Finally, several core components of the autophagy machinery have been implicated in distinct autophagic processes (canonical and noncanonical autophagy), implying that genetic approaches to block autophagy should rely on targeting two or more autophagy-related genes that ideally participate in distinct steps of the pathway. Along similar lines, because multiple proteins involved in autophagy also regulate other cellular pathways including apoptosis, not all of them can be used as a specific marker for bona fide autophagic responses. Here, we critically discuss current methods of assessing autophagy and the information they can, or cannot, provide. Our ultimate goal is to encourage intellectual and technical innovation in the field.

Journal article

Sahin S, Gozde Kanmaz Kutman H, Bozkurt O, Yavanoglu Atay F, Emre Canpolat F, Uras N, Suna Oguz S, Underwood MAet al., 2020, Effect of withholding feeds on transfusion-related acute gut injury in preterm infants: a pilot randomized controlled trial, JOURNAL OF MATERNAL-FETAL & NEONATAL MEDICINE, Vol: 33, Pages: 4139-4144, ISSN: 1476-7058

Journal article

Oikawa K, Fujisaki K, Shimizu M, Takeda T, Saitoh H, Hirabuchi A, Hiraka Y, Białas A, Langner T, Kellner R, Bozkurt TO, Cesari S, Kroj T, Maidment JHR, Banfield MJ, Kamoun S, Terauchi Ret al., 2020, The blast pathogen effector AVR-Pik binds and stabilizes rice heavy metal-associated (HMA) proteins to co-opt their function in immunity

<jats:title>Abstract</jats:title><jats:p>Plant intracellular nucleotide-binding domain and leucine-rich repeat-containing (NLR) immune receptors have a complex architecture. They can include noncanonical integrated domains that are thought to have evolved from host targets of pathogen effectors to serve as pathogen baits. However, the functions of host proteins with similarity to NLR integrated domains and the extent to which they are targeted by pathogen effectors remain largely unknown. Here, we show that the blast fungus effector AVR-Pik binds a subset of related rice proteins containing a heavy metal-associated (HMA) domain, one of the domains that has repeatedly integrated into plant NLR immune receptors. We find that AVR-Pik binding stabilizes the rice HMA proteins OsHIPP19 and OsHIPP20. Knockout of <jats:italic>OsHIPP20</jats:italic> causes enhanced disease resistance towards the blast pathogen, indicating that <jats:italic>OsHIPP20</jats:italic> is a susceptibility gene (<jats:italic>S</jats:italic>-gene). We propose that AVR-Pik has evolved to bind HMA domain proteins and co-opt their function to suppress immunity. Yet this binding carries a trade-off, it triggers immunity in plants carrying NLR receptors with integrated HMA domains.</jats:p>

Journal article

Petre B, Contreras MP, Bozkurt TO, Schattat MH, Sklenar J, Schornack S, Abd-El-Haliem A, Castells-Graells R, Lozano-Duran R, Dagdas YF, Menke FLH, Jones AME, Vossen JH, Robatzek S, Kamoun S, Win Jet al., 2020, Host-interactor screens of <i>Phytophthora infestans</i> RXLR proteins reveal vesicle trafficking as a major effector-targeted process

<jats:title>ABSTRACT</jats:title><jats:p>Pathogens modulate plant cell structure and function by secreting effectors into host tissues. Effectors typically function by associating with host molecules and modulating their activities. This study aimed to identify the host processes targeted by the RXLR class of host-translocated effectors of the potato blight pathogen <jats:italic>Phytophthora infestans.</jats:italic> To this end, we performed an <jats:italic>in planta</jats:italic> protein-protein interaction screen by transiently expressing <jats:italic>P. infestans</jats:italic> RXLR effectors in <jats:italic>Nicotiana benthamiana</jats:italic> leaves followed by co-immunoprecipitation (co-IP) and liquid chromatography tandem mass spectrometry (LC-MS/MS). This screen generated an effector-host protein interactome matrix of 59 <jats:italic>P. infestans</jats:italic> RXLR effectors x 586 <jats:italic>N. benthamiana</jats:italic> proteins. Classification of the host interactors into putative functional categories revealed over 35 biological processes possibly targeted by <jats:italic>P. infestans.</jats:italic> We further characterized the PexRD12/31 family of RXLR-WY effectors, which associate and co-localize with components of the vesicle trafficking machinery. One member of this family, PexRD31, increased the number of FYVE positive vesicles in <jats:italic>N. benthamiana</jats:italic> cells. FYVE positive vesicles also accumulated in leaf cells near <jats:italic>P. infestans</jats:italic> hyphae, indicating that the pathogen may enhance endosomal trafficking during infection. We anticipate that the interactome dataset we generated will serve as a useful community resource for functional studies of <jats:italic>P. infestans</jats:italic> effectors and of effector-targeted host processes.</jats:p>

Working paper

Gao C, Xu H, Huang J, Sun B, Zhang F, Savage Z, Duggan C, Yan T, Wu C-H, Wang Y, Vleeshouwers VGAA, Kamoun S, Bozkurt TO, Dong Set al., 2020, Pathogen manipulation of chloroplast function triggers a light-dependent immune recognition, Proceedings of the National Academy of Sciences of the United States of America, Vol: 117, Pages: 9613-9620, ISSN: 0027-8424

In plants and animals, nucleotide-binding leucine-rich repeat (NLR) proteins are intracellular immune sensors that recognize and eliminate a wide range of invading pathogens. NLR-mediated immunity is known to be modulated by environmental factors. However, how pathogen recognition by NLRs is influenced by environmental factors such as light remains unclear. Here, we show that the agronomically important NLR Rpi-vnt1.1 requires light to confer disease resistance against races of the Irish potato famine pathogen Phytophthora infestans that secrete the effector protein AVRvnt1. The activation of Rpi-vnt1.1 requires a nuclear-encoded chloroplast protein, glycerate 3-kinase (GLYK), implicated in energy production. The pathogen effector AVRvnt1 binds the full-length chloroplast-targeted GLYK isoform leading to activation of Rpi-vnt1.1. In the dark, Rpi-vnt1.1–mediated resistance is compromised because plants produce a shorter GLYK—lacking the intact chloroplast transit peptide—that is not bound by AVRvnt1. The transition between full-length and shorter plant GLYK transcripts is controlled by a light-dependent alternative promoter selection mechanism. In plants that lack Rpi-vnt1.1, the presence of AVRvnt1 reduces GLYK accumulation in chloroplasts counteracting GLYK contribution to basal immunity. Our findings revealed that pathogen manipulation of chloroplast functions has resulted in a light-dependent immune response.

Journal article

Bozkurt TO, Kamoun S, 2020, The plant–pathogen haustorial interface at a glance, Journal of Cell Science, Vol: 133, Pages: 1-6, ISSN: 0021-9533

Many filamentous pathogens invade plant cells through specialized hyphae called haustoria. These infection structures are enveloped by a newly synthesized plant-derived membrane called the extrahaustorial membrane (EHM). This specialized membrane is the ultimate interface between the plant and pathogen, and is key to the success or failure of infection. Strikingly, the EHM is reminiscent of host-derived membrane interfaces that engulf intracellular metazoan parasites. These perimicrobial interfaces are critical sites where pathogens facilitate nutrient uptake and deploy virulence factors to disarm cellular defenses mounted by their hosts. Although the mechanisms underlying the biogenesis and functions of these host–microbe interfaces are poorly understood, recent studies have provided new insights into the cellular and molecular mechanisms involved. In this Cell Science at a Glance and the accompanying poster, we summarize these recent advances with a specific focus on the haustorial interfaces associated with filamentous plant pathogens. We highlight the progress in the field that fundamentally underpin this research topic. Furthermore, we relate our knowledge of plant–filamentous pathogen interfaces to those generated by other plant-associated organisms. Finally, we compare the similarities between host–pathogen interfaces in plants and animals, and emphasize the key questions in this research area.

Journal article

Adachi H, Contreras MP, Harant A, Wu C-H, Derevnina L, Sakai T, Duggan C, Moratto E, Bozkurt TO, Maqbool A, Win J, Kamoun Set al., 2020, An N-terminal motif in NLR immune receptors is functionally conserved across distantly related plant species, eLife, Vol: 8, Pages: 1-31, ISSN: 2050-084X

The molecular codes underpinning the functions of plant NLR immune receptors are poorly understood. We used in vitro Mu transposition to generate a random truncation library and identify the minimal functional region of NLRs. We applied this method to NRC4—a helper NLR that functions with multiple sensor NLRs within a Solanaceae receptor network. This revealed that the NRC4 N-terminal 29 amino acids are sufficient to induce hypersensitive cell death. This region is defined by the consensus MADAxVSFxVxKLxxLLxxEx (MADA motif) that is conserved at the N-termini of NRC family proteins and ~20% of coiled-coil (CC)-type plant NLRs. The MADA motif matches the N-terminal α1 helix of Arabidopsis NLR protein ZAR1, which undergoes a conformational switch during resistosome activation. Immunoassays revealed that the MADA motif is functionally conserved across NLRs from distantly related plant species. NRC-dependent sensor NLRs lack MADA sequences indicating that this motif has degenerated in sensor NLRs over evolutionary time.

Journal article

Leary AY, Savage Z, Tumtas Y, Bozkurt Tet al., 2019, Contrasting and emerging roles of autophagy in plant immunity, CURRENT OPINION IN PLANT BIOLOGY, Vol: 52, Pages: 46-53, ISSN: 1369-5266

Journal article

Gao C, Huang J, Sun B, Zhang F, Wu CH, Wang Y, Vleeshouwers VGAA, Bozkurt TO, Kamoun S, Dong Set al., 2019, Pathogen effector triggered plant immunity is modulated by light rhythm, 18th Congress of International-Society-for-Molecular-Plant-Microbe-Interactions (IS-MPMI), Publisher: AMER PHYTOPATHOLOGICAL SOC, Pages: 63-63, ISSN: 0894-0282

Conference paper

Win J, Contreras MP, Petre B, Bozkurt TO, Schattat MH, Sklenar J, Abd-el-Haliem A, Dagdas YF, Lozano-Duran R, Jones AME, Vossen JH, Robatzek S, Kamoun Set al., 2019, Host-interactor screens of RXLR effectors reveal plant processes manipulated by Phytophthora, 18th Congress of International-Society-for-Molecular-Plant-Microbe-Interactions (IS-MPMI), Publisher: AMER PHYTOPATHOLOGICAL SOC, Pages: 173-173, ISSN: 0894-0282

Conference paper

This data is extracted from the Web of Science and reproduced under a licence from Thomson Reuters. You may not copy or re-distribute this data in whole or in part without the written consent of the Science business of Thomson Reuters.

Request URL: http://wlsprd.imperial.ac.uk:80/respub/WEB-INF/jsp/search-html.jsp Request URI: /respub/WEB-INF/jsp/search-html.jsp Query String: respub-action=search.html&id=00806293&limit=30&person=true