Maize plant expresses SWEET transporters differently when interacting with Trichoderma asperellum and Fusarium verticillioides, two fungi with different lifestyles.

Most Trichoderma species are beneficial fungi that promote plant growth and resistance, while Fusarium genera cause several crop damages. During the plant-fungi interaction there is a competition for sugars in both lifestyles. Here we analyzed the plant growth promotion and biocontrol activity of T. asperellum against F. verticillioides and the effect of both fungi on the expression of the maize diffusional sugar transporters, the SWEETs. The biocontrol activity was done in two ways, the first was by observing the growth capacity of both fungus in a dual culture. The second one by analyzing the infection symptoms, the chlorophyl content and the transcript levels of defense genes determined by qPCR in plants with different developmental stages primed with T. asperellum conidia and challenged with F. verticillioides. In a dual culture, T. asperellum showed antagonist activity against F. verticillioides. In the primed plants a delay in the infection disease was observed, they sustained chlorophyll content even after the infection, and displayed upregulated defense-related genes. Additionally, the T. asperellum primed plants had longer stems than the nonprimed plants. SWEETs transcript levels were analyzed by qPCR in plants primed with either fungus. Both fungi affect the transcript levels of several maize sugar transporters differently. T. asperellum increases the expression of six SWEETs on leaves and two at the roots and causes a higher exudation of sucrose, glucose, and fructose at the roots. On the contrary, F. verticillioides reduces the expression of the SWEETs on the leaves, and more severely when a more aggressive strain is in the plant. Our results suggest that the plant is able to recognize the lifestyle of the fungi and respond accordingly by changing the expression of several genes, including the SWEETs, to establish a new sugar flux.

Moonlighting Proteins: The Case of the Hexokinases.

Moonlighting proteins are defined as proteins with two or more functions that are unrelated and independent to each other, so that inactivation of one of them should not affect the second one and vice versa. Intriguingly, all the glycolytic enzymes are described as moonlighting proteins in some organisms. Hexokinase (HXK) is a critical enzyme in the glycolytic pathway and displays a wide range of functions in different organisms such as fungi, parasites, mammals, and plants. This review discusses HXKs moonlighting functions in depth since they have a profound impact on the responses to nutritional, environmental, and disease challenges. HXKs' activities can be as diverse as performing metabolic activities, as a gene repressor complexing with other proteins, as protein kinase, as immune receptor and regulating processes like autophagy, programmed cell death or immune system responses. However, most of those functions are particular for some organisms while the most common moonlighting HXK function in several kingdoms is being a glucose sensor. In this review, we also analyze how different regulation mechanisms cause HXK to change its subcellular localization, oligomeric or conformational state, the response to substrate and product concentration, and its interactions with membrane, proteins, or RNA, all of which might impact the HXK moonlighting functions.

Trichoderma atroviride-emitted volatiles improve growth of Arabidopsis seedlings through modulation of sucrose transport and metabolism.

Plants host a diverse microbiome and differentially react to the fungal species living as endophytes or around their roots through emission of volatiles. Here, using divided Petri plates for Arabidopsis-T. atroviride co-cultivation, we show that fungal volatiles increase endogenous sugar levels in shoots, roots and root exudates, which improve Arabidopsis root growth and branching and strengthen the symbiosis. Tissue-specific expression of three sucrose phosphate synthase-encoding genes (AtSPS1F, AtSPS2F and AtSPS3F), and AtSUC2 and SWEET transporters revealed that the gene expression signatures differ from those of the fungal pathogens Fusarium oxysporum and Alternaria alternata and that AtSUC2 is largely repressed either by increasing carbon availability or by perception of the fungal volatile 6-pentyl-2H-pyran-2-one. Our data point to Trichoderma volatiles as chemical signatures for sugar biosynthesis and exudation and unveil specific modulation of a critical, long-distance sucrose transporter in the plant.

SWEET Transporters for the Nourishment of Embryonic Tissues during Maize Germination.

In maize seed germination, the endosperm and the scutellum nourish the embryo axis. Here, we examined the mRNA relative amount of the SWEET protein family, which could be involved in sugar transport during germination since high [14-C]-glucose and mainly [14-C]-sucrose diffusional uptake were found in embryo tissues. We identified high levels of transcripts for SWEETs in the three phases of the germination process: ZmSWEET4c, ZmSWEET6b, ZmSWEET11, ZmSWEET13a, ZmSWEET13b, ZmSWEET14b and ZmSWEET15a, except at 0 h of imbibition where the abundance of each ZmSWEET was low. Despite the major sucrose (Suc) biosynthesis capacity of the scutellum and the high level of transcripts of the Suc symporter SUT1, Suc was not found to be accumulated; furthermore, in the embryo axis, Suc did not decrease but hexoses increased, suggesting an efficient Suc efflux from the scutellum to nourish the embryo axis. The influx of Glc into the scutellum could be mediated by SWEET4c to take up the large amount of transported sugars due to the late hydrolysis of starch. In addition, sugars regulated the mRNA amount of SWEETs at the embryo axis. These results suggest an important role for SWEETs in transporting Suc and hexoses between the scutellum and the embryo axis, and differences in SWEET transcripts between both tissues might occur because of the different sugar requirements and metabolism.