Sugar conundrum in plant-pathogen interactions: roles of invertase and sugar transporters depend on pathosystems

Abstract

It has been increasingly recognized that CWIN (cell wall invertase) and sugar transporters including STP (sugar transport protein) and SWEET (sugar will eventually be exported transporters) play important roles in plant-pathogen interactions. However, the information available in the literature comes from diverse systems and often yields contradictory findings and conclusions. To solve this puzzle, we provide here a comprehensive assessment of the topic. Our analyses revealed that the regulation of plant-microbe interactions by CWIN, SWEET, and STP is conditioned by the specific pathosystems involved. The roles of CWINs in plant resistance are largely determined by the lifestyle of pathogens (biotrophs versus necrotrophs or hemibiotrophs), possibly through CWIN-mediated salicylic acid or jasmonic acid signaling and programmed cell death pathways. The up-regulation of SWEETs and STPs may enhance or reduce plant resistance, depending on the cellular sites from which pathogens acquire sugars from the host cells. Finally, plants employ unique mechanisms to defend against viral infection, in part through a sugar-based regulation of plasmodesmatal development or aperture. Our appraisal further calls for attention to be paid to the involvement of microbial sugar metabolism and transport in plant-pathogen interactions, which is an integrated but overlooked component of such interactions.

Keywords: Bacteria; STP; SWEET; fungi; invertase; pathogen; sugar metabolism; sugar signaling; sugar transport; virus.

Fig. 1.

A hypothetical model illustrating how cell wall invertase (CWIN) and sugar transport protein (STP) differentially regulate plant resistance to different pathogens. Plant CWINs inhibit programmed cell death (PCD) and salicylic acid (SA) signaling, and simultaneously promote jasmonic acid (JA) signaling, which collectively contributes to susceptibility to biotrophic pathogens but increases plant resistance to necrotrophic/hemibiotrophic pathogens. Similar to biotrophic fungi and bacteria, viruses also require living tissues. However, in response to viral infection, CWINs and sugar transporters (SWEETS, STPs, and SUTs) appear to enhance resistance to viruses, possibly through inhibiting the formation or opening of plasmodesmata (PD) via modulating callose deposition around PD.

Fig. 2.

A schematic model of the different roles of plant sugar transporters in response to pathogen infection and the involvement of microbial INV and sugar transporters in plant–pathogen interactions. Clade II and III SWEETs export Glc and Suc into the plant apoplasm, respectively. Glc is then directly taken up into bacteria and necrotrophic/hemibiotrophic fungi during the initial infection phase via their own plasmalemma-localized hexose transporters (HXT), whereas Suc is first hydrolyzed into Glc and Fru by plant CWIN or pathogen-secreted INV before being imported into the pathogen cells. Consequently, these SWEETs promote bacterial and necrotrophic/hemibiotrophic fungal growth in the apoplasm. By contrast, Clade I SWEETs can sequester cytosolic Glc into plant cell vacuoles, thereby reducing the availability of Glc in the apoplasm, which starves necrotrophic fungi. The plant STPs facilitate hexose uptake into plant cells, which is subsequently released into the extrahaustorial matrix (EHMx) for uptake by biotrophic fungi via fungal HXT, thus promoting fungal infection. On the other hand, STPs reduce the concentration of Glc at the apoplasm, which inhibits the development of bacteria and necrotrophic/hemibiotrophic fungi. Plant SUTs take up apoplasmic Suc into plant cells and are commonly induced by pathogen infection. Studies in mycorrhizal fungi indicate that SUT (i) may promote the development of biotrophic fungi through increasing the intracellular sugar pool for subsequent import to the EHMx and uptake by Suc transporters such as UmStrt1, and (ii) could inhibit the development of bacteria and necrotrophic/hemibiotrophic fungi by limiting Suc availability in the apoplasm of the plant cell. NB, neckband.