In long-standing plant-pathogen interactions, competition for carbon sources is a key determinant of infection success 1. Accordingly, the acquisition of sugars fixed by host-plant photosynthesis is a crucial process that ensures the growth and proliferation of plant pathogenic microbes. They have evolved diverse mechanisms to gain access to sugars, but the underlying molecular mechanisms remain incompletely understood 2. Bacterial pathogens colonise the apoplast, where they acquire nutrients by manipulating host transporters alongside metabolic reprogramming. Apoplastic sucrose availability is mainly controlled by SWEETs (Sugars Will Eventually be Exported Transporters), STPs (Sugar Transport Proteins), SUTs (Sucrose Transporters), and CWINs (Cell Wall Invertases) 1. SWEETs, in particular, facilitate the efflux of sucrose or hexoses from host cells. Multiple pathogens target SWEET transporters to facilitate sugar efflux from plant cells to feed the pathogens 3. Some Xanthomonas spp. get host sucrose by injecting transcription activation-like (TAL) effectors to upregulate the transcriptions of SWEETs. Additionally, biotrophic fungi and oomycetes absorb sugars from the host cytoplasm through specialised haustoria. During necrotrophic growth, fungal and oomycete pathogens mainly absorb nutrients released from dead tissue or apoplasts. Notably, sugar transporter-mediated sugar partitioning between host and pathogen depends on their cellular locations and can differentially affect infection strategies: on one hand, transporters that promote pathogen access to sugars favour pathogen colonisation; on the other hand, those that reduce sugar availability for pathogens contribute to resistance. While traditional models assume that pathogens rely on preexisting host sugars, the recent study by Wang et al. reveals a genus-wide ‘private pantry’ within the host cells, driven by effector-mediated biosynthesis of a pathogen-specific nutrient 4. This strategy is initiated by the translocation of the conserved type III effector (T3E) AvrBs2 from Xanthomonas spp. into host cells. AvrBs2 is now unmasked as a sugar phosphodiester synthase with a pivotal role in virulence 4, 5. AvrBs2 does not merely suppress immunity or induce sugar efflux like other T3Es; instead, it catalyses the host uridine 5′-diphosphate (UDP)-α-D-galactose into a novel cyclic sugar phosphodiester, xanthosan (bis-(1,6)-cyclic dimeric α-D-galactose-phosphate) 6. Unlike sucrose or glucose, which are universally accessible currencies in the apoplast, xanthosan cannot be metabolised by the host and is exported to the apoplast, where it serves as a pathogen-specific carbon source for Xanthomonas. Although some pathogens can utilise specific forms of carbon to reduce direct competition with the host or potentially other microbes, the direct synthesis of pathogen-specific nutrients from host metabolites represents a distinct and relatively rarely described strategy 3, 7. The ingenuity of this strategy further demonstrated that the conserved permease (XanT) and phosphodiesterase (XanP) genes clustered with avrBs2. Once xanthosan accumulates in the apoplast, XanT selectively imports it into the bacterial cell. Then, XanP hydrolyses xanthosan into metabolically utilisable galactose-1-phosphate. The AvrBs2-XanT-XanP module forms a closed ‘generation-uptake-utilization’ metabolic circuit. By converting a common host sugar substrate into an exclusive nutrient, Xanthomonas establishes a privileged nutritional niche. This conservative mechanism across diverse Xanthomonas lineages redefines our understanding of bacterial virulence, shifting the narrative from simple nutrient competition to active niche construction. This suggests that the evolutionary interaction between plants and pathogens is not only about immune suppression but also involves complex metabolic engineering where pathogens synthetically dictate the nutritional landscape of the infection site. Plants deploy multiple layers to counter pathogen threats, not only by activating innate immunity to eliminate pathogens but also by blocking pathogen access to sugars for their colonisation 4. Breeding for ‘pathogen-starvation’ has focused on restricting pathogen access to host sugars through the manipulation of plant sugar transporters as key targets, either by interfering with the binding of TAL effectors to block the induction of SWEET genes or by regulating host STP expression to limit sugar supply 8. For example, genome editing of three SWEET gene promoters to disrupt TAL effector binding confers broad-spectrum resistance against Xanthomonas 9. While ‘pathogen-starvation’ revealed that host sugar transporters as targets can be engineered to defend against pathogen invasion, altering major sugar transporters can inadvertently disrupt plant carbon allocation, leading to yield reduction or developmental defects 3. Furthermore, pathogens often overcome these blockades by evolving TAL effectors to target alternative host genes, perpetuating an endless evolutionary arms race 10. Wang et al. 4 propose a novel ‘pathogen-starvation’ strategy that shifts from modifying host physiology to actively sabotaging the pathogen's private pantry. By expressing the bacterial enzyme XanP in rice, the pathogen-specific sugar xanthosan is hydrolysed before its export to the apoplast, thereby depriving Xanthomonas of a critical nutrient source and attenuating its virulence. Additionally, as xanthosan is a xenometabolite and not a physiological sugar like sucrose, its targeted degradation imposes little collateral damage on crop yield or quality. Pathogens can easily mutate effectors to evade recognition by host R proteins, while they cannot easily modify the enzymatic core of AvrBs2 without abolishing the very capability required to construct their nutritional niche. Because the avrBs2 gene cluster and its key catalytic residues are highly conserved across Xanthomonas species and AvrBs2 enzymatic activity is biochemically stable in vitro, this strategy is promising to combine high specificity for pathogen-derived metabolites with broad applicability and prospective durability (Figure 1). Two routes to sugar acquisition in pathogenic bacteria and corresponding ‘pathogen-starvation’ strategies. (1) Injection of TAL effectors into plant cells activates the expression of SWEET transporters, resulting in sucrose efflux into the apoplast and providing a nutrient source for bacterial growth. Resistance is achieved by genome editing of the promoter effector-binding elements region of SWEET genes to block TAL effector binding, thereby cutting off the sugar supply. (2) The T3E AvrBs2 converts host UDP-galactose into xanthosan, a pathogen-specific nutrient. A novel resistance strategy involves engineered expression of the bacterial phosphodiesterase XanP in the plant cells, which hydrolyses xanthosan before it reaches the apoplast. The nutrient battle between plants and pathogens is both intense and dynamic. The pathogen-driven synthesis of specific metabolites contributes to the construction of an exclusive nutritional niche. By establishing a ‘private pantry’ with the avrBs2 gene cluster, Xanthomonas avoids direct carbon competition with the host and potentially other microbes, which is crucial for bacterial colonisation 4. However, similar pathogen-specific nutrient circuits operating beyond Xanthomonas species remain unclear. In this context, the enzymatic activities of effectors merit further investigation. Similarly, a quest for identification of pathogen-like XanP in plants should be a focus of subsequent research. Furthermore, given the high conservation of the avrBs2 gene cluster, comparative metabolomics offers a feasible approach to identify pathogen-specific metabolites. Thus, future work to uncover analogous nutrient circuits in other plant-pathogen systems is also required. In addition, limiting pathogen nutrient acquisition is likely to be a new direction for agricultural resistance. Wang et al. 4 provides a promising solution to these long-standing production diseases caused by Xanthomonas, such as citrus bacterial canker and rice bacterial leaf streak, which still suffer from a severe lack of effective resistant germplasm. Whether by degrading pathogen-specific nutrients within plant cells or by editing SWEET promoters to restrict pathogen access to host sugars, ‘pathogen-starvation’ represents an efficient plant protection strategy. Moreover, how the ‘pathogen-starvation’ strategy intersects with immune signalling pathways needs further investigation. This will provide deeper insights into durable resistance breeding and could help safeguard global food security. Yixuan Mi: visualization, writing – original draft, writing – review and editing. Yuheng Yang: conceptualization, writing – review and editing, funding acquisition. This work was supported by the National Key Research and Development Program of China (2022YFD1901402), and the Fundamental Research Funds for the Central Universities (SWU-KF25017). The authors declare no conflicts of interest. Data sharing not applicable to this article as no datasets were generated or analysed during the current study.
Mi et al. (Thu,) studied this question.