Exploiting breakdown in nonhost effector–target interactions to boost host disease resistance

Abstract

Plants are resistant to most microbial species due to nonhost resistance (NHR), providing broad-spectrum and durable immunity. However, the molecular components contributing to NHR are poorly characterised. We address the question of whether failure of pathogen effectors to manipulate nonhost plants plays a critical role in NHR. RxLR (Arg-any amino acid-Leu-Arg) effectors from two oomycete pathogens, Phytophthora infestans and Hyaloperonospora arabidopsidis , enhanced pathogen infection when expressed in host plants ( Nicotiana benthamiana and Arabidopsis, respectively) but the same effectors performed poorly in distantly related nonhost pathosystems. Putative target proteins in the host plant potato were identified for 64 P . infestans RxLR effectors using yeast 2-hybrid (Y2H) screens. Candidate orthologues of these target proteins in the distantly related non-host plant Arabidopsis were identified and screened using matrix Y2H for interaction with RxLR effectors from both P . infestans and H . arabidopsidis . Few P . infestans effector-target protein interactions were conserved from potato to candidate Arabidopsis target orthologues (cAtOrths). However, there was an enrichment of H . arabidopsidis RxLR effectors interacting with cAtOrths. We expressed the cAtOrth AtPUB33, which unlike its potato orthologue did not interact with P . infestans effector PiSFI3, in potato and Nicotiana benthamiana. Expression of AtPUB33 significantly reduced P . infestans colonization in both host plants. Our results provide evidence that failure of pathogen effectors to interact with and/or correctly manipulate target proteins in distantly related non-host plants contributes to NHR. Moreover, exploiting this breakdown in effector-nonhost target interaction, transferring effector target orthologues from non-host to host plants is a strategy to reduce disease.

Novel stripe rust effector boosts the transcription of a host susceptibility factor through affecting histone modification to promote infection in wheat

“…Viewed from the pathogen perspective, the failure of Pst urediniospores infection of barberry is mainly due to the inability of secreted effectors to modulate or suppress host defense factors. For example, the majority of the Phytophthora infestans effectors are not able to recognize the Arabidopsis proteins homologous to the corresponding targets of effectors in the potato host (McLellan et al ., 2022). TaSIG is a wheat susceptibility factor, which is presents only in monocot plants.…”

Cyclophilin effector Al106 of mirid bug Apolygus lucorum inhibits plant immunity and promotes insect feeding by targeting PUB33

“…7). Our result is consistent with a recent study that demonstrated that AtPUB33 is a positive regulator of plant immunity, and expression of this gene reduces P. infestans colonization of host plants (McLellan et al ., 2022). However, further investigation is required to determine the substrate of NbPUB33 ubiquitination and to determine the role of NbPUB33 in promoting plant immune response.…”

Tuning the Wavelength: Manipulation of Light Signaling to Control Plant Defense

“…The RXLR effector Pi06099 from P. infestans is nucleo-cytoplasmically localized and promotes pathogen colonization [ 101 ]. Pi06099 interacts with the RL receptor phyB from both Arabidopsis and potato in Y2H and by CoIP ( Figure 2 ) [ 99 ]. Nothing further is known about how this interaction affects RL signaling, although phyB mutant plants are more susceptible to a variety of pathogens and display reduced SA and JA signaling [ 113 ].…”

“…More recently, it was demonstrated that the perception of BL by StPhot1 suppresses plant defenses and also enhances StNRL1’s ability to target SWAP70 for degradation [ 75 ]. Moreover, Pi02860 also interacts with 14-3-3 phosphobinding proteins in potato and Arabidopsis ( Figure 2 ) [ 99 ]. The 14-3-3 proteins may have many pleiotropic functions but also interact with NRL proteins to modulate their activity following BL perception [ 98 ].…”