Sweet revenge: AtSWEET12 in plant defense against bacterial pathogens by apoplastic sucrose limitation

Abstract

Depriving bacterial pathogens of sugars is a potential plant defense strategy. The relevance of SUGARS WILL EVENTUALLY BE EXPORTED TRANSPORTERS (SWEETs) in plant susceptibility to pathogens has been established, but their role in plant defense remains unknown. We identified Arabidopsis thaliana SWEETs (AtSWEETs) involved in defense against nonhost and host Pseudomonas syringae pathogens through reverse genetic screening of atsweet1-17 mutants. Double/triple mutant, complementation, and overexpression line analysis, and apoplastic sucrose estimation studies revealed that AtSWEET12 suppresses pathogen multiplication by limiting sucrose availability in the apoplast. Localization studies suggested that plant defense occurred via increased plasma membrane targeting of AtSWEET12 with concomitant AtSWEET11 protein reduction. Moreover, the heterooligomerization of AtSWEET11 and AtSWEET12 was involved in regulating sucrose transport. Our results highlight a PAMP-mediated defense strategy against foliar bacterial pathogens whereby plants control AtSWEET11-mediated sucrose efflux in the apoplast through AtSWEET12. We uncover a fascinating new mechanism of pathogen starvation as a broad-spectrum disease resistance mechanism in parallel with existing immune pathways.

Increased susceptibility to Chrysanthemum Yellows phytoplasma infection in Atcals7ko plants is accompanied by enhanced expression of carbohydrate transporters

“…It has been reported that OsSWEET12 (Li et al 2013 ) and AtSWEET11 (Wipf et al 2021 ) interact with AtRBOHD, a membrane NADP oxidase producing reactive oxygen species involved in defence-related processes. In line with the present interpretation, SWEETs were proposed to modulate the sucrose availability for pathogens (Fatima and Senthil-Kumar 2021 ).…”

SWEET11 and SWEET12 transporters function in tandem to modulate sugar flux in Arabidopsis: An account of the underlying unique structure–function relationship

“…The study traced the AtSWEET11-mediated sucrose flux to be modulated through AtSWEET12 via plasma membrane targeting and an oligomerization-dependent regulatory mechanism in Arabidopsis. This also indicates the exclusive role of AtSWEET12 in suppressing bacterial multiplication and the role of AtSWEET11 in supplying sugars to bacterial pathogens in the apoplast (Fatima and Senthil-Kumar, 2021).…”

“…It is highly plausible that these transporters are independently regulated through PTM at the CTD, which might be a reason for distinct and exclusive roles of these two transporters in various plant physiological processes. Although, the phenotypic analysis for the double mutant of AtSWEET11 and AtSWEET12 points towards the functional redundancy (Chen et al, 2012; Gebauer et al, 2016; Walerowski et al, 2018), the histochemical and expression-based studies of the single mutants of these two transporters demonstrate their distinct roles in various developmental processes (Chen et al, 2015; Le Hir et al, 2015), as well as in response to environmental stimuli (Fatima and Senthil-Kumar, 2021). The differential expression of AtSWEET11 and AtSWEET12 orthologs also support their specific roles in different plant species ( Supplementary Figure 8 ).…”

“…The biochemical transport assays suggest an oligomerization-based function of SWEETs (Xuan et al, 2013; Han et al, 2017). AtSWEET11 and AtSWEET12 could homo- or heterodimerize with each other (Xuan et al, 2013; Fatima and Senthil-Kumar, 2021) and the hetero-oligomerization of AtSWEET11 and AtSWEET12 impacts the sucrose transport activity (Fatima and Senthil-Kumar, 2021).…”

AtSWEET11 and AtSWEET12 transporters function in tandem to modulate sugar flux in plants

“…The study traced the AtSWEET11‐mediated sucrose flux to be modulated through AtSWEET12 via plasma membrane targeting and an oligomerization‐dependent regulatory mechanism in Arabidopsis. This also indicates the exclusive role of AtSWEET12 in suppressing bacterial multiplication and the role of AtSWEET11 in supplying sugars to bacterial pathogens in the apoplast (Fatima & Senthil‐Kumar, 2021). In the present study, a large number of cis‐acting elements related to defense and biotic stress, such as MYB and MYC elements were abundantly distributed in the promoter sequences of AtSWEET11 and AtSWEET12 orthologs from different plant species, followed by STRE, ARE, LTR, W box, WUN, and MBS elements (Figure 4).…”