Trichoderma species are free-living fungi that decompose dead organic matter, releasing nutrients that improve soil quality. Also, they are endophytic beneficial fungi that colonize plant roots (Mastouri et al., 2010; Schweiger et al., 2021). During root colonization, Trichoderma enhances the plant absorption of nutrients and releases plant growth-promoting molecules improving plant performance and productivity (Contreras-Cornejo et al., 2009; Mastouri et al., 2010; Vinale et al., 2014; López-Coria et al., 2016). Moreover, Trichoderma induces metabolic changes in plant tissues (Schweiger et al., 2021). Several species of Trichoderma are considered biocontrol agents due to their capacity to antagonize pathogens effectively and to enhance plant defenses against viruses, bacteria, and other fungi (Lorito et al., 2010; Sharma and Sharma, 2020). Trichoderma synthesizes a broad spectrum of molecules to fulfill their role as biocontrol, including those that directly attack pathogens, such as bactericides, volatile antibiotics, cell wall degrading enzymes, and proteases (Benítez et al., 2004; Vinale et al., 2008; Druzhinina et al., 2011; Sharma and Sharma, 2020). Contrary to Trichoderma, most Fusarium species are considered pathogens with detrimental effects on plant development and produce several plant diseases, including Fusarium head blight in wheat (Palacios et al., 2021), oat (Ghimire et al., 2020), and barley (Martínez et al., 2021); root rot in soybean (Hafez et al., 2021) and alfalfa (Li et al., 2021); and stem rot and ear rot in maize (Oldenburg et al., 2017). Thus, crop losses caused by Fusarium species are an important limitation to food security. In addition, they also impact animal and human health since they release toxins such as fumonisins and aflatoxins (Logrieco et al., 2002; Wild and Gong, 2010).

In both cases, extensive metabolic reprogramming occurs for the host and the microorganism to fight back against each other (Lapin and Van den Ackerveken, 2013; Schweiger et al., 2021). The study of plant–fungi interaction deserves much attention due to their impact on plant productivity. One crucial task that the plant must face when interacting with microorganisms is controlling its sugar partitioning to keep its development and productivity. In the multigene family of transporters, sugar will eventually be exported transporters (SWEETs), which codify for proteins that move a massive flux of sugars in the direction of the concentration gradient. Some of them are located in the plasma membrane, vacuole, and endoplasmic reticulum and are potential targets for microorganisms (Eom et al., 2015; Breia et al., 2021). For instance, a set of SWEETs that codify to different sugar specificities located at the plasma membrane are induced in Arabidopsis by Pseudomonas syringae pv. tomato strain DC3000, Golovinomyces cichoracearum, and Botrytis cinerea, which induce expression of different sets of SWEETs (Chen et al., 2010). Enhancement of plasma membrane SWEET expression is a strategy for increasing the sugar cell efflux to ensure a constant nutrient supply to the microorganisms, as the latter acts as a sink of carbon nutrients (Chen et al., 2010; Chen et al., 2012). The bacterial pathogen Xhantomonas oryzae pv. oryzae (Xoo), which causes a severe blight in Oryza sativa plants, requires activating specific Oryza sativa SWEET (OsSWEET) genes to induce the disease’s development (Yang et al., 2006; Antony et al., 2010; Chen et al., 2010; Liu et al., 2011). Plasma membrane sucrose rice transporters, OsSWEET11, OsSWEET13, and OsSWEET14, have promoter regions recognized by the transcription activator-like (TAL) effectors synthesized and injected by Xanthomonas into the plant cell (Chu et al., 2006; Römer et al., 2010). Mutants in the TAL effectors cannot induce the expression of SWEETs, causing the disease (Chu et al., 2006; Liu et al., 2011; Yuan et al., 2011).

SWEETs are also a target of beneficial microorganisms. For instance, the beneficial association of Rhizophagus irregularis with potato roots produces a significant increase in SWEET transcriptional levels. These transporters may be involved in the sugar fluxes that could support mycorrhiza colonization (Manck-Götzenberger and Requena, 2016). In Medicago truncatula, the expression of some SWEETs is induced in roots colonized by arbuscular mycorrhiza (Kafle et al., 2019).

However, not only SWEETs localized at the plasma membrane are regulated during the plant–microorganism interaction, but in rice sweet2 mutant plants, they are more susceptible to Pythium irregulare infection. OsSWEET2 is a rice glucose transporter located at the vacuoles at the roots; its absence in the mutant plant produces an increase in glucose export, a reduction in the plant growth, and limits the spread of the infection for P. irregulare (Chen et al., 2015).

In maize, the SWEET family is composed of 24 members (Sosso et al., 2015; Breia et al., 2021; Liu et al., 2022b; Zhu et al., 2022). Some of them have been characterized and play a key role in plant physiology. For instance, ZmSWEET4c is needed during embryogenesis for starch accumulation in the endosperm (Sosso et al., 2015). The triple mutant zmsweet13a, zmsweet13b, and zmsweet13c, is unable to load the phloem with sugars and reduces overall plant growth (Bezrutczyk et al., 2018). ZmSWEET15a, a sucrose transporter, is induced by sucrose and various abiotic stresses. It has been suggested that ZmSWEET15 activity is important for sucrose transport to sink tissues such as the grain, which could be relevant to increasing crop productivity (Liu et al., 2022a). The expression of the ZmSWEET family was recently evaluated during different abiotic stresses such as salt, Cd, and drought (low water potential and ABA) to know the contribution of the SWEETs to the plant fitness since sugars are used to deal with the cell stress (Zhu et al., 2022). However, there is no available information in maize about the effect of beneficial or pathogen fungi on SWEET expression. Therefore, this work is focused on studying the expression of the most expressed SWEETs in the leaves and roots of maize plants (Walley et al., 2016) when interacting with two different fungi lifestyles, Trichoderma asperellum and Fusarium verticillioides, beneficial and pathogen fungi, respectively. This evidence could contribute to the understanding of sugar partitioning during plant–fungi interaction to improve plant growth and defense responses in this crop.

The most common strategies used to control plant fungal diseases are disease-resistant crop cultivation and crop rotation (Savary et al., 2012). However, herbicides like glyphosate also exhibit plant fungal disease control in wheat and soybean glyphosate-resistant plants (Feng et al., 2005; Claus et al., 2023). Extensive evidence, however, demonstrated that pathogen biocontrol using beneficial microorganisms such as Trichoderma species could enhance plant health since the beneficial fungus competes against pathogens in the rhizosphere (Stummer et al., 2022), induces plant immune responses (Sood et al., 2020), and is available to modify the metabolomic plant context (Schweiger et al., 2021). Here, we demonstrated that T. asperellum could promote young maize plants’ growth and act as a biocontrol agent against F. verticillioides, and modify the transcription of several SWEET transporters in roots and leaves and the sugar content at the roots.

Priming seeds with beneficial microorganisms is a pregerminative treatment to enhance plant growth. Some widely used microorganism genera for priming seeds are Aspergillus, Azospirillum, Bacillus, Rizophagus, Glomus, and Trichoderma, among others (Arora et al., 2020). For example, tomato seeds treated with T. harzianum T-22 germinated earlier, and their radicle grew longer even when the fungus did not colonize the seed embryo, meaning that the fungus exudates have growth-promoting activity (Mastouri et al., 2010). Germinated maize seeds primed with T. asperellum show longer mesocotyls and larger radicles with higher root hairs (López-Coria et al., 2016). This increase correlates with the increased activity of a key enzyme that promotes cell elongation, the plasma membrane H⁺-ATPase (López-Coria et al., 2016).

Several secondary metabolites exudating from Trichoderma have been proposed to induce plant growth, such as auxins, harzianic acid, koniginin A, 6-pentyl-α-pyrone (Lorito et al., 2010; Vinale et al., 2014). In addition, T. virens synthesizes indole-3-acetic acid, indole-3-acetaldehyde, and indole-3-ethanol, auxin-related compounds, promoting lateral root and shoot development (Contreras-Cornejo et al., 2009). Trichoderma also affects the transcription of some plant genes (Sood et al., 2020; Schweiger et al., 2021). All the changes in the plant promoted by Trichoderma species could drive a modification in carbon plant allocation, which can be beneficial for both the microorganism and the plant. Here, we observed that priming treatment increases the expression of ZmSWEET17, ZmSWEET4a, ZmSWEET13a, and ZmSWEET13b in the leaves of 14-day-old plants. From them, only the ZmSWEET13 subfamily has been characterized as a plasma membrane sucrose transporter necessary for phloem loading in maize plants (Bezrutczyk et al., 2018). ZmSWEET4a remains as one putative plasma membrane glucose transporter and ZmSWEET17 as one putative vacuolar fructose transporter (Eom et al., 2015). The increase in the transcription levels of SWEET transporters in leaves could lead to a rise in the sugar transport activity that could not only be beneficial for plant growth but could also increase the carbon flux from leaves to roots. The exudated sugars could sustain Trichoderma establishment at the rhizosphere.

In roots, ZmSWEET2, ZmSWEET3, ZmSWEET12a, and ZmSWEET14b are the most expressed according to RNAseq analysis (Walley et al., 2016). Our results indicate that SWEETs’ expression levels change throughout the development of roots and show differential responses to priming treatment. The increase in the expression of ZmSWEET2 and ZmSWEET3 in the primed plants does not seem to lead to a significant increase in the sugar content exudated by the 3-day-old roots, which could be explained by the increase in the SUT1 transcription level since SUT1 is a transporter that supports the intracellular accumulation of sucrose (Slewinski et al., 2010), but it could also mean that the microorganism is using the sugar located at the rhizosphere. In addition, as far as we know, there is no information about the intracellular location of ZmSWEET2 and ZmSWEET3. In rice, OsSWEET2 is located at the vacuole (Chen et al., 2015); if that is the case for ZmSWEET2, the increase in its expression could reduce the sugar at the cytoplasm due to the increase of the sugar flux into the vacuole, limiting the available sugars to be exported at the apoplast and used by the microorganisms. In 30-day-old roots, there was a significant increase in soluble sugars exudated by the roots that could be due to ZmSWEET3 and ZmSWEET14b efflux activity. ZmSWEET14b could be a plasma membrane sucrose transporter since it is closely related to the ZmSWEET13 subfamily (Liu et al., 2022b; Zhu et al., 2022); if that is the case, an enhanced transcription could lead to an increase in the protein at the plasma membrane and the rise of the sugar efflux to nourish the fungi at the 30-day-old roots. Nevertheless, since we only evaluated the expression of the SWEET isoforms reported in the root RNAseq study of Walley et al. (2016), it is possible that other SWEET not considered here could be involved in the root sugar secretion, such as ZmSWEET1a, ZmSWEET4a, and ZmSWEET13c, that were found to have high expression in primary roots (Zhu et al., 2022). Also, the amount of SWEET expressed at the membranes remains to be determined. Our results indicate that during the interaction between maize and T. asperellum, the increment of sugars exudated by mature roots can support the fungi nourishment, where ZmSWEET3 and ZmSWEET14b could be involved. As discussed, the expression of SWEETs is not clear in plant–microorganism interactions since, in different scenarios, it was reported an upregulation or downregulation of SWEETs, indicating to be a specie-specific response, and we can also suggest that it is developmentally regulated.

Members of the SWEET family in maize are also susceptible to being altered by abiotic stress. Zhu et al. (2022) analyzed the SWEET family in maize and their expression pattern by abiotic stress, or ABA. Several SWEETs were upregulated by ABA, such as ZmSWEET1a, ZmSWEET4c, ZmSWEET14b, ZmSWEET15b, ZmSWEET16, and ZmSWEET17a, and the other four SWEETs were induced by abiotic stress but not by ABA. Abiotic stress such as drought or high salt concentration alters the intracellular and tissue sugar allocation to deal with the deleterious effect of the stress. These results suggest that the content is vital to the plant in stressful situations (Jeandet et al., 2022).

Several mechanisms have been suggested regarding the biocontrol activity of Trichoderma species against pathogenic fungi. Recognition of the pathogen by the beneficial fungus leads to the exudation of metabolites and enzymes with antibiosis and lytic activities. Such molecules enhance mycoparasitism and the competition for space and nutrients (Köhl et al., 2019; Sharma and Sharma, 2020; Schweiger et al., 2021), which T. asperellum may display when interacting with F. verticillioides since we detected T. asperellum hyphae coiling around the F. verticillioides hyphae, and also the reduction of F. verticillioides growth when both fungi were loaded in the same plate. He et al. (2019) found that T. asperellum-treated soil reduced maize stalk and ear rot produced by Fusarium, and the content of FB1 and deoxynivalenol in the ear and grain was reduced at basal levels. T. asperellum was also able to reduce and select a variety of endophytic microorganisms in a mature plant. The authors suggest that the contribution of T. asperellum to plant fitness was not only to induce the defense response against the pathogen but also to select a specific set of endophytic microorganisms that can also compete with Fusarium. In this work, the study was made with sterile seeds, in which T. asperellum enhances the defense response and reduces F. verticillioides symptoms in the stem and leaves; further work is needed to determine which molecules or microorganisms could synergistically help Trichoderma induce the plant response to a specific pathogen attack.

Additionally, Trichoderma triggers the plant immune system response (Druzhinina et al., 2011). An unknown mechanism disrupts the early response, which leads to the success of the mutualistic plant–Trichoderma interaction. However, a later defense response could be produced when a second infection by a different microorganism, wound (herbivores), or salt stress is perceived (Ankala et al., 2013). Here, we observed that T. asperellum not only triggers the induced immune response (or ISR) by the JA/ethylene pathway but also triggers the SAR response only when F. verticillioides infects the plant. SAR induction has been reported for Trichoderma species when associated with pathogens (Druzhinina et al., 2011). However, it is a response that could be different between plant and fungus species. Chen et al. (2021) found that some isoforms of PAL are not enhanced in dual Trichoderma harzianum and Fusarium oxysporum interaction with Radix pseudostellariae, contrary to PR gene expression. Ben Amira et al. (2017) observed that PAL, PR, and AOC transcripts increase with the interaction of both T. harzianum and F. solani in olive trees. T. asperellum improves maize performance against Fusarium verticillioides and induces maize SWEET sugar transport expression adjustment, resulting in a high sugar root exudation. However, these adjustments do not compromise plant growth, as shown by the chlorophyll content and plant performance.

In relation to the effect of the hemibiotrophic pathogen F. verticillioides on plant performance, we used MY3 and MY5 strains with conidia concentration that keep the plants alive and growing and with a sustained chlorophyll content, features that suggest that both strains are in the biotrophic cycle. However, even though the plants were asymptomatic, they experimented with different reduction profiles of the expression of ZmSWEET1b, ZmSWEET4a, ZmSWEET13a, ZmSWEET13b, and ZmSWEET17 in aerial tissue: higher reduction with the high FB1 producer strain, MY3, and less abrupt reduction with the low FB1 producer strain, MY5. Chong et al. (2014) reported that two biotrophic pathogens, Erysiphe necator and Plasmopara viticola, do not induce the SWEET expression in Vitis vinifera, contrary to the necrotrophic fungus Botrytis cinerea. These results agree with our observations. It is accepted that a biotrophic pathogen’s nutrition strictly depends on the supply of organic carbon and nitrogen metabolites from living host tissue (Divon and Fluhr, 2007), and a necrotrophic organism lives on dead tissues. However, maize plants can detect and change the SWEET expression slightly differently if it is interacting with a high-pathogenic strain or not, even when both are in their biotrophic cycle, suggesting that fungi are expressing different molecules that could be related to their pathogenic potential and the plant can sense and switch on a different set of responses. Therefore, the decrease in ZmSWEET transcripts may reduce the internal plant sugar flux, preparing the defense against the pathogen.

Additionally, the presence of both beneficial and pathogenic fungi at the same time results in high but transitory expression of ZmSWEET13a, a member of the ZmSWEET13 subfamily involved in the apoplastic phloem loading in maize (Bezrutczyk et al., 2018). An increase in ZmSWEET13a expression could be related to the sugar reallocation necessary to support plant–Trichoderma interaction. MtSWEET1b is highly expressed in the peri-arbuscular membrane of roots colonized by the fungus Rhizophagus irregularis, and its overexpression promotes the growth of intraradical mycelium. However, mycorrhization is not affected if the SWEET transporter loses its function (An et al., 2019).

It would be simplistic to point out that microorganisms act only as new sinks for the plant because the plant needs to recognize the fungus interacting with it to set up its biochemical and genetic reprogramming before giving access to its nutrients. Here, we showed that the maize plant is able to modify the SWEET expression differently depending on the lifestyle of the fungi. Still, it could also affect other types of sugar transporters, which are essential to regulating the plant carbon partitioning to continue its plant development.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

ML-C: Conceptualization, Data curation, Formal Analysis, Investigation, Methodology, Writing – original draft. FG-C: Investigation, Formal Analysis, Writing – review & editing. RC-G: Formal Analysis, Investigation, Methodology, Writing – review & editing. DM-C: Formal Analysis, Investigation, Methodology, Writing – review & editing. TS-S: Investigation, Methodology, Writing – review & editing. JA-R: Formal Analysis, Investigation, Methodology, Writing – review & editing. BK-D: Formal Analysis, Methodology, Project administration, Writing – review & editing. SS-N: Conceptualization, Formal Analysis, Funding acquisition, Supervision, Writing – review & editing.