2025/05/19 by Francisco Percio, Miguel A. Botella · 1 voice
Agricultural and Biological Sciences · #Mycorrhizal Fungi and Plant Interactions #Plant Parasitism and Resistance #Plant-Microbe Interactions and Immunity
paper · pdf · doi:10.1111/pce.15628
openalex publication_date 2025/05/19 · openalex created_date 2025/10/10 · openalex updated_date 2026/07/22
Plants' antagonistic relationship with pathogens is a multistep conflict in which both sides try to overcome each other (Vo et al. 2023). It begins with the detection of microbe-associated molecular patterns or damage-associated molecular patterns by plant cell-surface pattern recognition receptors. This sensing induces pattern-triggered immunity (PTI), a broad-range response against a plethora of different pathogens. To get over this primary defense, pathogens use effector proteins that promote infection through several mechanisms such as protease activity or inhibition of host protein enzymatic activity. Plants strike back by detecting these effectors using nucleotide-binding domain, leucine-rich repeat receptors (NLRs), which lead to effector-triggered immunity (ETI). To thrive, pathogens have developed diverse strategies to overcome ETI and PTI and promote infection. One of these strategies is to subvert the plant endomembrane system to avoid immunity responses (Noack and Mukherjee 2020). Vesicular trafficking in plants occurs through the endomembrane system, from the endoplasmic reticulum (ER), Golgi apparatus, trans-Golgi network (TGN), prevacuolar compartment/multivesicular bodies (PVC/MVB) up to the vacuole. At the PVC/MVB, vesicular sorting receptors (VSRs) execute protein trafficking to the vacuole. Targeting host cell trafficking pathway VSRs proteins appears to be a common strategy used by pathogens to increase their infection capacity (Zhang et al. 2025). In Arabidopsis, the VSR4 protein is hijacked by the Turnip mosaic virus 6K2 protein, which uses the endomembrane system to promote viral replication vesicles and intracellular transfer (Wu et al. 2022). The aphid effector Mp1 from Myzus persicae interacts with the host vacuolar protein sorting-associated protein 52 (VPS52), altering its localization and function. As a result of this interaction, plant defences are suppressed, promoting susceptibility (Rodriguez et al. 2017). The smut fungus Sporisorium scitamineum causes a major disease in sugarcane (Bhuiyan et al. 2021). The infection mechanisms were investigated by Ling et al. (2022) through a weighted gene co-expression network analysis of both smut fungus and sugarcane. They identified the fungal effector SsPele1 and the sugarcane receptor gene ScPEPR1 as highly coexpressed. SsPele1 mimics and negatively competes with the plant elicitor peptide recognized by ScPEPR1, reducing the plant immune response. In a recent work by Ling et al. (2025), published in Plant, Cell & Environment, the authors investigate the relationship between another set of coexpressed genes during infection, the sugarcane ScVSR1 and the fungal SsPE15 effector. Interestingly, the interaction of these proteins is part of an immune evasion strategy by which the smut fungus S. scitamineum effector SsPE15 uses the plant ScVSR1 to relocalize into the vacuole to avoid triggering ETI responses. The authors showed that ScVSR1 contains conserved domains associated with the vacuole sorting process, presenting a typical localization of this type of proteins based on confocal analysis and plays a negative regulatory role in plant defence. This is supported by the findings that overexpression of ScVSR1 in Arabidopsis thaliana caused a decrease in resistance to powdery mildew. Surprisingly, SsPE15 is a secreted effector that localizes at PVCs, showing the same localization pattern as ScVSR1 when expressed in Nicotiana benthamiana leaves. They further showed that ScVSR1 and SsPE15 interact In Vitro by pulldown experiment and In Vivo using bimolecular fluorescence complementation and co-immunoprecipitation experiments. They further mapped the interactive region of SsPE15 to the C-terminus of the protein that contains an increased composition in hydrophobic and basic residues, which suggested to comprise a C-terminus vacuole sorting signal (ctVSS). Therefore, the authors hypothesized that the C-terminus of SsPE15 interacts with ScVSR1 leading to SsPE15 import into the vacuole. The role of SsPE15 in virulence was further investigated using two different approaches. First, they generated a SsPE15 gene knockout strain and found a higher infection in sugarcane than the wild-type strain. Second, overexpression of SsPE15 in A. thaliana and N. benthamiana led to increased resistance to the fungal and oomycete pathogens Golovinomyces cichoracearum and Phytophthora nicotianae, respectively. Therefore, they concluded that SsPE15 is an immune elicitor that triggers immune responses in host cells leading to reduced fungal infection. Consequently, the authors propose a model in which the interaction of SsPE15 effector with the vesicle sorting receptor ScVSR leads to its internalization into vesicles to avoid detection by the host immune system and increase infection efficiency (Figure 1A). To further test this hypothesis, the authors used the model pathosystem involving A. thaliana, Pseudomonas syringae, and the bacterial effector AvrRpt2 (Schröpfer et al. 2021). As expected, P. syringe carrying wild-type AvrRpt2 caused HR in all the Arabidopsis infiltrated plants leading to induced resistance (Figure 1B). However, fusing the C-terminus of SsPE15 (ctVSS signal peptide, responsible for its interaction with ScVSR1) to AvrRpt2 altered its localization from the cytosol to the PVC, drastically reducing HR responses and decreasing resistance (Figure 1C). Finally, a construct in which AvrRpt2 was fused to the SSPE15 N-terminus behaved as AvrRpt2 wild-type, showing a cytosolic localization, high HR response and increased resistance (Figure 1D). Taken together, this data support that SsPE15 is an immune elicitor that triggers host response and that its C-terminus region leads to its internalization into vesicles to decrease immune recognition and increase disease. Nevertheless, important questions remain open. The identification of this effector across different fungal species suggests a conserved mechanism. However, whether unrelated effectors could use a similar method, that is, evading host immunity by localizing into membrane structures is unknown. Additionally, aside from evading host defense responses, the evolutive advantage of this conservation and the biological significance of the internalization of the effector into vesicles remains unclear. It could provide a fitness advantage for the fungus, which could have a biological function in the vacuole or play a different role in other hosts in which it is not recognized and sequestered into the vacuole, but acting as an effector in the cytosol. Further research is needed to address these possibilities. In summary, Ling et al. (2025) provide novel insights into pathogen strategies to overcome plant immune detection. Their demonstration on how the effector SsPE15 of S. scitamineum uses sugarcane VSR-mediated protein trafficking to avoid immune detection increases our understanding of the mechanisms by which pathogens target host machinery to promote infection. Moreover, they show that this mechanism can be applicable to unrelated pathogens (i.e. bacteria) effectors. Further studies on this topic to identify effector targets and study their mechanistic functions will open biotechnological opportunities to assess pathogen strategies that can be used to enhance crop resilience to pathogens. M.A.B was funded by the Ministerio de Ciencia e Innovación (grant no. PID2023-147983OB-I00). F.P. was funded by the Universidad de Málaga. Funding for open access charge: Universidad de Málaga/CBUA. The authors declare no conflicts of interest. The authors have nothing to report.