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Revista Chapingo. Serie horticultura

versión On-line ISSN 2007-4034versión impresa ISSN 1027-152X

Rev. Chapingo Ser.Hortic vol.29 no.3 Chapingo sep./dic. 2023  Epub 26-Ene-2024

https://doi.org/10.5154/r.rchsh.2022.11.016 

Review article

Sugar transporters in plant-beneficial endophytic fungus and plant-phytopathogenic nematode interactions

Luis Yobani Gayosso-Rosales1 

Reyna Isabel Rojas-Martínez1 

Stefan de Folter2 

Daniel Leobardo Ochoa-Martínez1 

Manuel Silva-Valenzuela1 

Emma Zavaleta-Mejía1 

1 Colegio de Postgraduados, Posgrado en Fitosanidad-Fitopatología. Carretera México-Texcoco km 36.5, Montecillo, Texcoco, Estado de México, C. P. 56230, MÉXICO.

2 Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (CINVESTAV-IPN), Unidad de Genómica Avanzada (UGA-LANGEBIO). Libramiento Norte León km 9.6, Irapuato, Guanajuato, C. P. 36824, MÉXICO.


Abstract

The transport of sugars, a product of photosynthesis, involves the distribution of carbohydrates from synthesis organs, such as leaves, to the tissues of demand organs such as roots, stems, flowers, fruits and seeds. Their mobilization occurs through the plasmodesmata or apoplast by means of membrane transporters, which are proteins encoded by the so-called sugar transporter genes. Their expression in plants is modified by the presence of microorganisms that colonize them. Studies on their expression in plant-nematode interactions are relatively recent, and in plant-beneficial endophyte fungus interactions they have been carried out mainly with arbuscular mycorrhizal fungi. In this review, information on the current state of knowledge of sugar transporters in plant-endophyte fungus and plant-nematode interactions is summarized.

Keywords: Sugars will eventually be exported transporters (SWEET); sucrose transporter (SUT); tonoplast monosaccharide transporter (TMT); vacuolar glucose transporter (VGT); Meloidogyne incognita; Heterodera schachtii; arbuscular mycorrhizal fungi

Resumen

El transporte de azúcares, producto de la fotosíntesis, implica la distribución de los carbohidratos desde los órganos de síntesis, como las hojas, hasta los tejidos de órganos de demanda como raíces, tallos, flores, frutos y semillas. Su movilización ocurre a través de los plasmodesmos o del apoplasto mediante transportadores de membrana, que son proteínas codificadas por los denominados genes transportadores de azúcares. Su expresión en las plantas es modificada por la presencia de los microorganismos que las colonizan. Los estudios sobre su expresión en las interacciones planta-nematodos son relativamente recientes, y en las interacciones planta-hongos endófitos benéficos se han realizado principalmente con hongos micorrícicos arbusculares. En esta revisión, se resume la información sobre el estado actual del conocimiento de los transportadores de azúcares en la interacción planta-hongos endófitos y planta-nematodos.

Palabras clave: Transportadores de azúcares (SWEET); transportador de sacarosa (SUT); transportador de monosacáridos del tonoplasto (TMT); transportador de glucosa vacuolar (VGT); Meloidogyne incognita; Heterodera schachtii; hongos micorrícicos arbusculares

Introduction

Depending on the metabolic demand in plant organ tissues, sugars produced by photosynthesis can be translocated over long distances in the form of sucrose to demand organs, stored locally in cell vacuoles or stored as starch mainly in chloroplasts (Weise, Schrader, Kleinbeck, & Sharkey, 2006; Guo et al., 2014). The plant root is a demand organ that imports sugars from leaf tissue to be used and stored in its different tissues (Salmeron-Santiago et al., 2021). Transport of sugars in plants occurs through the plasmodesmata or apoplast via membrane transporters, which are gene-encoded proteins generally known as sugar transporter genes (Williams, Lemoine, & Sauer, 2000; Gill et al., 2021; Singh et al., 2022). In roots, some of these carbohydrates are exuded and utilized by microorganisms colonizing the rhizoplane and rhizosphere (Hennion et al., 2019).

Genes encoding for the synthesis of sugar transporter proteins have been detected and characterized in plants (Huang, Hu, Liu, Zhou, & Liu, 2020), nematodes (Berninsone, Hwang, Zemtseva, Horvitz, & Hirschberg, 2001), bacteria (Henderson, 1990), oomycetes (Wang et al., 2009) and fungi (Schüßler, Martin, Cohen, Fitz, & Wipf, 2006; Dai et al., 2021), among other organisms. Plant roots are colonized by various organisms, including endophytic fungi and plant-parasitic nematodes (Baron & Rigobelo, 2022). Some of the genes encoding sugar transporter proteins in plants, such as sucrose transporters (SUTs, sucrose import and export), vacuolar glucose transporters (VGTs, vacuole glucose importers), tonoplast monosaccharide transporters (MSTs, monosaccharide importers), and sugars will eventually be exported transporters (SWEETs, importers and exporters of sucrose, glucose, and fructose), are known to play an important role in nematode parasitism (Zhao et al., 2018) and in the colonization of endophytic fungi (Doidy et al., 2012a; Rani, Jogawat, & Loha, 2021).

Plant-parasitic nematodes cause global losses in vegetables, which are estimated at $US80 billion per year (Jones et al., 2013). A few studies on sugar transporters in plant-nematode interaction have been conducted using the model plant Arabidopsis thaliana inoculated with Meloidogyne incognita or Heterodera schachtii.

On the other hand, since the discovery of endophytic fungi in the 1970s, these microorganisms have been studied as biocontrol agents (Clay, 1989). Recent studies show that beneficial endophytic fungi can activate defense mechanisms against pathogens (Adeleke, Ayilara, Akinola, & Babalola, 2022), aid nutrient acquisition (Verma et al., 2021) and promote abiotic stress tolerance (Bilal et al., 2020) in the plants they colonize. However, at present, research on endophytic fungi is focused on the study of bioactive molecules produced by endophytes for agricultural and pharmacological use or as biocontrol agents (Yan et al., 2019).

It has been documented that colonization of plants by beneficial endophytic fungi can reduce infection by plant-parasitic nematodes (Zhou, Wheeler, Starr, Valencia, & Sword, 2018; Miao, Han, Zhang, Wang, & Wang, 2019). These fungi have great potential as pathogen controllers (Siddiqui & Mahmood, 1996) since they can parasitize them (Yan, Sikora, & Zheng, 2011), produce secondary metabolites with nematicidal, nematostatic, and repellent properties (such as 4-hydroxybenzoic acid, indole-3-acetic acid, gibepirone D [Bogner et al., 2017], cyclopiazonic acid [Nguyen et al., 2021], verrucarin A and roridin A [Nguyen et al., 2018]), induce plant defense mechanisms (Ghahremani, Escudero, Saus, Gabaldón, & Sorribas, 2019) and compete with nematodes for nutrients inside the plant (Sikora et al., 2008). However, knowledge about the last mechanism is limited.

In studies on plant-beneficial endophytic fungus interaction, it is reported that arbuscular mycorrhizal fungi (AMF) can modulate the expression of genes encoding sugar transporter proteins in their hosts (Requena, Tamayo, Figueira-Galán, & Manck-Götzenberger, 2022). This literature review aims to present advances that have been made regarding the characterization and function of sugar transporters in plant-endophyte and plant-nematode interactions.

Methodology for the bibliographic information search

The search for scientific articles was carried out in the PubMed (NCBI), Europe PMC, Google Scholar, Springer Link and Science Research databases. To filter the information, the following keywords were used: transporter sugars in plants, sugars will eventually be exported transporters (SWEET), sucrose transporter (SUT), tonoplast monosaccharide transporter (TMT), vacuolar glucose transporter (VGT), soluble sugars in plants, plant- parasitic nematodes, endophytic fungi in plants, sugar transporter gene, regulation of plant sugar transporters by pathogens, regulation of plant sugar transporters by nematodes, regulation of plant sugar transporters by mycorrhizal fungi and CRISPR-Cas9 system in plants. The articles consulted were those related to sugar transport by sugar translocator proteins in plant-nematode and plant-beneficial endophyte fungus interactions.

Sugar transporters

Sugar transporters are proteins that have a common structure, with 7 or 12 transmembrane domains connected by hydrophilic loops that function as H+/sugar symporters across membranes (Hofmann et al., 2009; Doidy et al., 2012a; Chen, 2014; Reuscher et al., 2014). They are found in the membranes of both eukaryotic and prokaryotic cells (Chen, Cheung, Feng, Tanner, & Frommer, 2015), and have been identified in plants (Julius, Leach, Tran, Mertz, & Braun, 2017), nematodes (Berninsone et al., 2001), bacteria (Henderson, 1990), oomycetes (Wang et al., 2009), fungi (Schüßler et al., 2006), humans (Caulfield et al., 2008) and mice (Hiraoka et al., 2007). In mammals, there are hexose transporters (HXT), glucose transporters (GLUT, SGLT and GLUT) and Na+-dependent glucose transporters (NaGLT1).

SWEETs are present in archaeobacteria, plants and humans (Chen et al., 2012). SUTs have been characterized in plants (Reinders, Sivitz, & Ward, 2012), algae (Schilling & Oesterhelt, 2007), fungi (Reinders & Ward, 2001) and bacteria (Silva et al., 2005). MSTs are present in humans (Büttner & Sauer, 2000), mycorrhizal fungi (Helber et al., 2011), bacteria (Horler et al., 2009), nematodes (Berninsone et al., 2001) and algae (Schilling & Oesterhelt, 2007). In plants, VGTs have also been reported (Williams et al., 2000; Chen et al., 2012; Hennion et al., 2019). Table 1 presents the sugar transporters that have been reported both in plants and in beneficial microorganisms and pathogens associated with them.

Table 1 Sugar transporters in plants, and beneficial microorganisms and pathogens. 

Family Function Reference
Plants
SWEET Importers and exporters of hexoses (glucose and fructose) and sucrose Chen et al. (2010), Chen et al. (2012), Feng & Frommer (2015)
VGT Vacuolar glucose transporter Aluri & Büttner (2007), Doidy et al. (2012a), Williams et al. (2000)
TMT/MST Importer of monosaccharides (glucose, fructose, galactose and xylose) Wormit et al. (2006), Schulz et al. (2011), Doidy et al. (2012a), Zhao et al. (2018)
SUC/SUT Importer and exporter of sucrose Reinders et al. (2012), Chen et al. (2015), Hennion et al. (2019)
HT Importer of hexoses (fructose and glucose) and sucrose Wang et al. (2020)
Brittle Proteins (BT) Sugar transporter to mitochondria Kirchberger et al. (2007), Linka & Weber (2010)
Fungi
SUC/SUT Importer and exporter of sucrose Reinders & Ward (2001), Fang & Leger (2010), Vargas, Crutcher, & Kenerley (2011)
TMT/MST Importer of monosaccharides (glucose, fructose, galactose and xylose) Schüßler et al. (2006), Helber et al. (2011)
HXT Hexose importers Rani et al. (2016)
FRT1 Fructose transporter Doehlemann, Molitor, & Hahn, (2005)
Nematodes
TMT/MST Monosaccharide importer Berninsone et al. (2001)
SQV-7 Import of UDP-glucuronic acid, UDP-GalNAc acetylgalactosamine and UDP-galactose Berninsone et al. (2001)
SRF-3 Transmembrane transport of UDP-N-acetylglucosamine and galactose Caffaro, Hirschberg, & Berninsone (2007)
CO3H5.2 Transporter of UDP-GlcNAc and UDP-GalNAc Caffaro et al. (2007)
Bacteria
PTS Importer of glucose, mannose, fructose and lactose Siebold, Flükiger, Beutler, & Erni (2001)
SWEET Importers and exporters of hexoses (glucose and fructose) and sucrose Chen et al. (2012), Xu et al. (2014), Feng & Frommer (2015)
ABC Importers and exporters of maltose, arabinose, xylose and galactose Oldham, Khare, Quiocho, Davidson, & Chen (2007), Ferreira & de Sá-Nogueira (2010), Oldham & Chen (2011a), Oldham & Chen (2011b)
SUC/SUT Importer and exporter of sucrose Silva et al. (2005)
TMT/MST Monosaccharide importer Horler et al. (2009)

Sugar transporters in the translocation of photosynthates in plants

Plant sugars are synthesized during the photosynthesis process, which takes place in the chloroplasts of metabolically active leaf mesophyll cells during atmospheric carbon fixation CO2 (Yamada & Osakabe, 2018). They are the main source of carbon and energy through ATP synthesis via the oxidative phosphorylation process in plants (Hennion et al., 2019; Saleem, Fariduddin, & Janda, 2021). These metabolites are involved in most metabolic and signaling pathways that control growth, development, and tolerance to stress by biotic and abiotic factors (Williams et al., 2000; Aluri & Büttner, 2007; Hennion et al., 2019). In addition, they may interact with the hormonal signaling network during plant defense responses against pathogens by regulating the oxidative burst in the early stages of infection, increasing cell wall lignification, stimulating flavonoid synthesis and inducing certain pathogenesis-related proteins (Morkunas & Ratajczak, 2014).

Photosynthates produced during photosynthesis are transported mainly as sucrose to developing meristems and organs (such as leaves, roots, stems, flowers, fruits, and young seeds) (Rolland, Moore, & Sheen, 2002; Yamada & Osakabe, 2018). The transport and distribution of sugars from phototrophic leaves (source) to heterotrophic organs (demand) occurs via the phloem (Rolland et al., 2002; Chen, 2014; Julius et al., 2017).

Cell-to-cell transport of sugars occurs through the plasmodesmata or apoplast via sugar transporter proteins located in cell membranes (Chen, 2014). It has been reported that plant cells exhibit great compartmentalization and require transporters that can take up and release sugars from these compartments (Fettke & Fernie, 2015). Cellular uptake and release of sugars by transporter proteins is of great importance for the distribution of carbon between different cells, tissues and organs of multicellular organisms (Chen et al., 2015). Some transporter proteins translocate sugars into cells (importers), while others take them out of cells (exporters) (Guo et al., 2014; Jeena, Kumar, & Shukla, 2019). It is considered that the storage or release of sugars in the different cellular compartments, by sugar transporters, may be an adaptation strategy against biotic and abiotic stress through dynamic regulation of sugar flow (Yamada & Osakabe, 2018).

Long-distance transfer of sucrose is driven by hydrostatic pressure generated in the phloem (Eom, Choi, Ward, & Jeon, 2012). Two main mechanisms in phloem loading have been identified: symplastic (via plasmodesmata) and apoplastic (via sugar transporters) (Eom et al., 2012). For sucrose to reach the phloem from mesophyll cells, outflow from one cell and subsequent uptake by an adjacent cell is necessary (Julius et al., 2017). In the case of apoplastic loading of the phloem and the transport of sugars from cell to cell, this is carried out by transporter proteins encoded by their respective genes.

Among the main sugar transporters identified in plants are MSTs (which import the glucose and fructose monosaccharides into the vacuoles, and are located in the tonoplast) (Wormit et al., 2006; Zhao et al., 2018), SUT/SUCs (sucrose importers or exporters located in cell membranes, vacuoles and plastids) (Kühn & Grof, 2010), SWEETs (sucrose, glucose, and fructose importers or exporters, and are located in the cell membranes and tonoplasts of root cells) (Chen et al., 2010; Chen et al., 2012; Guo et al., 2014) and VGTs (importers of glucose into the vacuole and are located in the tonoplast) (Aluri & Büttner, 2007; Doidy et al., 2012a; Hennion et al., 2019). Brittle proteins are found in mitochondria, such as ZmBT1 (Zea mays Brittle1) that transports ADP-glucose in maize (Kirchberger et al., 2007) and AtBT1 in A. thaliana capable of transporting AMP, ADP and ATP, but not ADP-glucose (Kirchberger, Tjaden, & Neuhaus, 2008).

SWEET proteins have seven transmembrane domains (TMDs), whereas SUT/SUC sucrose transporters have 12 TMDs. Both SWEETs and SUTs are involved in sucrose loading to the phloem (Jeena et al., 2019; Ji et al., 2022). SWEETs are thought to probably regulate the flow of sucrose from the phloem parenchyma into the phloem apoplasm; subsequently, sucrose is translocated and stored in companion cells and sieve elements through SUTs, a key step in phloem loading (Chen, 2014).

SUTs, also called SUCs (Santiago, Ward, & Sharkey, 2020), can export sucrose out of cells, vacuoles, and plastids; however, they can also import sucrose into cells (Hennion et al., 2019). Sugars transported apoplastically by the phloem are used to form the seed coat, the nutrition of new tissues that will form the seed, and the nutrition of the embryo (Jeena et al., 2019). Plants secrete sugars through their nectaries to attract pollinators, as well as through their roots to feed beneficial microorganisms in the rhizosphere and rhizoplane (Chen, 2014).

Excess sugars in the cytoplasm are stored in the vacuole (Hedrich, Sauer, & Neuhaus, 2015). Vacuolar storage and remobilization involve transporters across the membrane, which play a key role in maintaining cell metabolism, osmoregulation and adaptation to environmental conditions. The main transporters in the vacuole are VGTs and TMTs (monosaccharide transporters) that are found in the tonoplast (Wormit et al., 2006; Jung et al., 2015). Sucrose import into the vacuole is mainly performed by two members grouped in the family of MST monosaccharide transporters (TMT1 and TMT2) (Wormit et al., 2006; Cho et al., 2010). On the other hand, in assays with vacuoles isolated from a hexose-transport-deficient yeast mutant expressing the AtVGT1 gene, active uptake of glucose and fructose was recorded (Aluri & Büttner, 2007). In A. thaliana plants, with the AtVGT1 gene silenced, flowering was delayed and seed size was reduced (Aluri & Büttner, 2007), whereas AtTMT1 overexpression increased seed size and limited vacuolar monosaccharide loading (Wingenter et al., 2010). Cho et al. (2010), through glucose uptake studies using vacuoles isolated from transgenic mutant A. thaliana (tmt1-2-3) expressing OsTMT1 in rice plants, demonstrated that OsTMTs are capable of transporting glucose into vacuoles.

Sugar transporters in plant-soil microorganism interaction

Plants are in constant association with various microorganisms outside and inside their tissues, usually at the root-soil interface (Zipfel & Oldroyd, 2017). These associations can be beneficial or detrimental to plants (Yan et al., 2019). The most studied beneficial associations in roots are with AMF and rhizobia of the Fabaceae family (Yan et al., 2019). These associations are carried out through the formation of particular organs and new tissues. AMF inhabit specialized compartments of the root cortical cell membrane forming arbuscules, and rhizobia remain in root-derived organs called nodules (Zipfel & Oldroyd, 2017). The formation of these organs enables nutrient transport between plants and microorganisms (Yan et al., 2019). Several studies indicate that endophytic associations also contribute to improving plant response to adverse conditions (Quesada, 2020).

Doidy et al. (2012b) reported that genes encoding for sugar transporter proteins play an important role in the interaction of microorganisms with their host plants. The plant root is an organ that imports sugars from leaf tissue. Part of this carbon source is exuded through the roots and is used by microorganisms colonizing the rhizoplane and rhizosphere (Hennion et al., 2019). Root exudates are a source of nutrients and chemotactic attractants that facilitate adhesion and colonization by microbial populations. Root exudates contain sugars, polysaccharides, amino acids, aromatic acids, aliphatic acids, fatty acids, sterols, phenolic compounds, growth regulators, proteins, and enzymes, and their composition changes as plants develop or respond to exogenous stimuli as part of a plant’s defense system (Pinski, Betekhtin, Hupert-Kocurek, Mur, & Hasterok, 2019).

On the other hand, infection of plants by pathogens causes a reduction in photosynthetic activity. To compensate for the nutrient demand in the infected tissues, nutrient transport from uninfected tissues is necessary (Yamada & Osakabe, 2018). However, pathogens rely on host-derived carbon, so they manipulate plant sugar transporters to easily access sugars, while plants enhance sugar uptake activity to store it in their various cellular compartments and restrict nutrients to pathogens (Yamada & Osakabe, 2018; Liu, Song, & Ruan, 2022). How plants regulate the flow of sugars during pathogen attack has been studied. In wheat, the LR67 gene encodes for a transporter protein of H+/hexoses (mainly glucose), through a dimerization process between the LR67res resistance gene with its homoallele LR67sus (susceptibility gene) blocking glucose uptake from the apoplasm to the host cells, which prevents the development of different biotrophic pathogens of wheat (Moore et al., 2015).

Competition for sugars between plants and the pathogens that colonize them has generated an evolutionary race, in which the plant limits the pathogen's access to nutrients and initiates defense responses, while the pathogen develops adaption strategies to gain access to nutrients and suppress host immunity. During plant infection by pathogens, SWEETs generally facilitate the export of sucrose and hexose out of cells, which increases sugar availability for pathogens colonizing the apoplast (Pommerrenig, Müdsam, Kischka, & Neuhaus, 2020; Breia et al., 2021). SWEETs are very susceptible to being modulated by pathogens to obtain nutrients (Chen et al., 2010; Breia et al., 2021); therefore, these transporters may function as susceptibility factors (Pommerrenig et al., 2020).

Chen et al. (2010) reported that the bacterium Pseudomonas syringae pv. tomato strain DC3000 induced high mRNA levels of AtSWEET4, AtSWEET5, AtSWEET7, AtSWEET8, AtSWEET10, AtSWEET12 and AtSWEET15 in Arabidopsis leaves, while the fungus Golovinomyces cichoracearum promoted the expression of a different set of AtSWEET genes (AtSWEET1, AtSWEET11 and AtSWEET12), being AtSWEET12 in which the highest mRNA levels were found. Likewise, these authors observed that Botrytis cinerea mainly induced the expression of AtSWEET4, AtSWEET15 and AtSWEET17, indicating the specific modulation of SWEET genes by different pathogens.

Sugar transporters in plant-plant-parasitic nematode interaction

There are more than 4,100 species of plant-parasitic nematodes (Jones et al., 2013). Among the most damaging species in agriculture are the root-knot nematodes (Meloidogyne spp. and Nacobbus aberrans), cyst nematodes (Heterodera and Globodera spp.) and lesion nematodes (Pratylenchus spp., Radopholus similis, Ditylenchus dipsaci, Bursaphelenchus xylophilus, Rotylenchulus reniformis, Xiphinema index and Aphelenchoides besseyi) (Jones et al., 2013). Nematode control is mainly carried out by means of chemical products that are highly polluting to the environment; therefore, other ecological alternatives are currently being explored, especially biological control with endophytic microorganisms that are antagonistic to these pathogens.

Pathogens have developed the ability to regulate the expression of genes encoding for sugar transporter proteins to gain access to these nutrients. The capture of sugars secreted by plant roots is one of the key mechanisms for the survival and reproduction of pathogenic microorganisms (Chen et al., 2010; Julius et al., 2017). There is evidence that plant-parasitic nematodes can modulate the expression of genes encoding for sugar transporter proteins in the host (Juergensen et al., 2003; Chen, 2014). SUC genes, encoding sucrose transporter proteins, have been identified as having an important role in nematode parasitism (Hammes et al., 2005). The first report on the modification of sugar transporter gene expression was recorded in the A. thaliana-Heterodera schachtii interaction, in which the AtSUC2 gene was overexpressed in root syncytia (Juergensen et al., 2003). Years later, Hammes et al. (2005) found that the vacuole glucose transporters VGT1 and TMT1 were induced by M. incognita in A. thaliana roots, whereas in galls the AtSUC1 gene was highly induced.

In A. thaliana plants, with the AtSUC4 (sucrose transporter) gene silenced, there was a significant reduction in the development of adult H. schachtii females compared to those that developed in wild A. thaliana (Hofmann, Wieczorek, Blöchl, & Grundler, 2007). AtSUC4 has been reported to exhibit high sucrose transport capacity (Weise et al., 2000), while AtSUC2 has a low capacity to transport it (Hofmann et al., 2007). When comparing the expression of these two phloem-specific sucrose transporters (AtSUC4 = AtSUT4 and AtSUC2) in H. schachtii-induced syncytia in A. thaliana, it was observed that AtSUC4 gene expression did not change during H. schachtii development (Hofmann et al., 2007). In contrast, AtSUC2 expression was repressed five days after inoculation with the nematode in root sections containing syncytia. This indicates that the AtSUC4 transporter favors sucrose accumulation in newly formed syncytia, but when the AtSUC4 gene was silenced, it significantly increased male differentiation to the detriment of females, due to a lack of food (Hofmann et al., 2007).

H. schachtii-induced syncytia in A. thaliana have high metabolic activity, which requires high levels of sucrose and starch (Hofmann & Grundler, 2007). This metabolic alteration causes increased demand for water and sugars (Juergensen et al., 2003). The import of soluble sugars (sucrose, glucose, galactose, raffinose, fructose and trehalose) into the syncytium is via the symplastic pathway; therefore, sugar transporters allow intra- and intercellular flow (Hofmann & Grundler, 2006; Hofmann et al., 2007; Hofmann et al., 2009). Hofmann et al. (2009) reported that in H. schachtii-induced syncytia in A. thaliana roots, genes for the sugar transporters STP12 (glucose, galactose, mannose, fructose and xylose importer, located in cytoplasmic membranes) (Rottmann et al., 2018), GTP2 (glucose 6-phosphate importer to the chloroplast and plastids in root cells) (Hofmann et al., 2009; Weise et al., 2019) and MEX1 (maltose importer) were expressed, while genes encoding the sugar transporter protein SFP1, and the hexose transporters STP7 and STP4 were repressed. These researchers also found that silencing the STP12 gene in A. thaliana favored the development of H. schachtii females relative to males.

In tomato roots infected by M. incognita, the expression of nine sugar transporter genes was detected (Shukla et al., 2018). In the same interaction, Zhao et al. (2018) recorded a high expression of three SlTMT and two SlVGT in leaves, while in roots the highest expression corresponded to two SlTMT and two SlVGT; likewise, they observed the expression of three SlSUT and 17 SlSWEET genes in both leaves and roots. In A. thaliana mutant plants of the AtSUC2 gene (sucrose transporter), inoculated with M. incognita, a high expression of β-glucuronidase (which hydrolyzes carbohydrates such as sucrose) was recorded at infection sites and development of the nematodes was arrested, reaching only the J4 stage. On the other hand, it has been reported that SWEET gene mutations impede the flow of sugars to pathogens, which generates resistance in plants (Hennion et al., 2019) and constitutes a possible alternative for the control of plant-parasitic nematodes in different crops.

Sugar transporters in plant-beneficial endophytic fungal interaction

Various soil microorganisms colonize both the surface of the roots and the apoplast of their cells (Hacquard et al., 2015). There is evidence that expression of different genes encoding for sugar transporters occurs in root cells of plants colonized by beneficial fungi (An et al., 2019; Tamayo, Figueira-Galán, Manck-Götzenberger, & Requena, 2022). During root colonization by AMF, both the photosynthate translocation to the root and the photosynthetic rate increase (Tinker, Durall, & Jones, 1994; García-Rodríguez, Pozo, Azcón-Aguilar, & Ferrol, 2005).

The first evidence for carbon transfer from a plant to an AMF was provided by Ho and Trappe (1973). Three steps have been described for photosynthate transport from host plant cells to fungal tissue: 1) release of sucrose into apoplastic space by diffusion through concentration gradients, 2) hydrolysis of sucrose into fructose and glucose by cell wall invertase enzymes, and 3) transport across the fungal membrane into the intra-radical hyphae (Rani et al., 2016). Solaiman and Saito (1997), by exposing hyphae of Gigantea margarita to 14C-labeled glucose, fructose, and sucrose and measuring 14CO2 evolution by radiorespirometry, found that hyphae mainly use glucose as a substrate in respiration.

Different sugar transporters have been characterized in beneficial endophytic fungi, which allow them to take up different sugars from host plants. In the symbiont fungus Geosiphon pyriformis, the glucose transporter GpMST1 was identified (Schüßler et al., 2006), and in Glomus intraradices, the monosaccharide transporter MST2 (Helber et al., 2011). MST2 and PiHXT5 transport glucose efficiently; in addition, they can transport substrates such as xylose, glucuronic acid, galacturonic acid, mannose, and galactose (Helber et al., 2011; Rani et al., 2016). This suggests that certain AMF can feed on cell wall components.

On the other hand, in beneficial endophytic fungi such as Metarhizium robertsii and Trichoderma virens, SUT genes (MRT and TvSUT, respectively), involved in the uptake of sugars from root exudates, have been identified (Fang & Leger, 2010; Vargas et al., 2011). In Glomus intraradices, SUT genes were identified, such as GiSUC1 (Doidy et al., 2012a), and in Geosiphon pyriformis, the GpMST1 gene, which possesses transmembrane domains and functions as a cotransporter with greater affinity for glucose, mannose, galactose, fructose and xylose (Schüßler et al., 2006). In the mycorrhizal fungus Glomus sp., a monosaccharide transporter (MST2) was identified, the expression of which was closely related to that of the mycorrhizal-specific phosphate transporter (PT4). Silencing of the MST2 gene resulted in malformed arbuscules and reduced PT4 gene expression (Helber et al., 2011).

The expression of sugar transporter genes in plants is modified when they are infected by beneficial endophytic fungi. For example, SlSUT1, SlSUT2 and SlSUT4 genes are over-expressed in response to Glomus mosseae in tomato (Boldt et al., 2011), while in potato colonized by Rhizophagus irregularis the expression of some SWEET genes was up-regulated (Manck-Götzenberger & Requena, 2016). Likewise, in mycorrhized rice roots, the expression of the OsSWEET3b gene was induced (Fiorilli et al., 2015), suggesting that SWEETs could regulate sugar export to the symbiotic interface. In Medicago truncatula plants infected with AMF, the MtST1 (monosaccharide importer) gene was overexpressed, and its silencing reduced arbuscule formation (Harrison, 1996; Doidy et al., 2012a). A study on AMF indicated that transgenic tomato plants, with reduced expression of the SlSUT2 gene through an antisense construct, had increased colonization by Funneliformis mosseae and Rhizophagus irregularis due to low sucrose uptake from the apoplast into root cells. This indicates that SUTs can regulate plant-microorganism interactions by regulating sucrose availability in the host apoplast (Bitterlich, Krügel, Boldt‐Burisch, Franken, & Kühn, 2014).

Some of the genes encoding for sugar transporter proteins in plants such as SUTs (sucrose importers and exporters), SWEETs (sucrose, glucose and fructose importers and exporters), VGTs (glucose importers to the vacuole) and TMTs (monosaccharide importers) are known to play an important role in plant interaction with both beneficial endophytic fungi (Doidy et al., 2012a) and plant-parasitic nematodes (Zhao et al., 2018). García-Rodríguez et al. (2005) found that LeST3 (monosaccharide transporter) gene expression was increased in leaves of tomato plants colonized by the AMF Glomus mosseae and Glomus intraradices, as well as by the root pathogen Phytophthora parasítica. This indicates that LeST3 functions as a sugar transporter in tissues colonized by both beneficial microorganisms and pathogens.

Beneficial associations between plants and endophytic fungi are fragile, and can shift to neutral, saprophytic or even pathogenic interactions when stress conditions affect the balance of nutrient exchange and the survival of one of the symbiotic partners is compromised (Mandyam & Jumpponen, 2015).

In A. thaliana plants, which are highly colonized by T. harzianum under stress conditions due to low phosphorus availability, a negative regulation of SWEET11 and SWEET12 gene expression, and high expression levels of SUC1 and SWEET2 genes were found. SWEET11 and SWEET12 transporters are mainly responsible for the discharge of apoplastic sugar from the phloem into the roots; therefore, the plants negatively regulate the expression of SWEET11 and SWEET12 to restrict the loss of sugar from the apoplast due to the development of the fungus, which limits hyphal growth due to sugar restriction. Low availability of sugar in the apoplast stimulates sugar uptake by mesophyll root cells by inducing high levels of SUC1 and SWEET2 gene expression in Trichoderma-inoculated plants with phosphorus availability. SUC1 and SUC2 are considered to be the main sugar importers from the apoplast to root cells, whereas SWEET2, located in the tonoplast in mesophyll cells and root epidermis cells, is responsible for the uptake of sugars from the cytoplasm into vacuoles. This suggests that the roots compete with the fungus for apoplastic sucrose through SUC1, and SWEET2 sequesters sucrose in the vacuole of root cells to reduce sugar loss by the fungus (Rouina, Tseng, Nataraja, Uma-Shaanker, & Oelmüller, 2021).

Zhang et al. (2019) reported that during the flowering stage, in A. thaliana plants inoculated with the beneficial fungus Phomopsis liquidambari, jasmonate signaling was activated and the expression of SWEET11 and SWEET12 in rosette leaves, and SUC1 in roots was reduced. Consequently, phloem sugar transport and soluble invertase activity in the root were reduced, resulting in low glucose and fructose concentrations in plant roots, which affected root colonization by P. liquidambari. This suggests that plants utilize available sugars for flower development and restrict hexoses, such as fructose and glucose, to the microorganisms that colonize them.

It is important to note that the development of beneficial and pathogenic microorganisms colonizing plants does not only depend on sugars (Keymer et al., 2017), as they also need other essential nutrients such as fatty acids, minerals, amino acids and organic acids (Jiang et al., 2017; Ma, Hill, Chadwick, Wu, & Jones, 2021; Xing et al., 2021). Jiang et al. (2017) reported that host plants of the AMF Rhizophagus irregularis, which is a fatty acid auxotroph, transfer fatty acids to the fungus to maintain colonization.

Conclusions

The detection and characterization of sugar transport proteins, as well as the identification of the genes that encode them, has allowed us to begin to understand how beneficial and pathogenic microorganisms obtain nutrients. Generally, these genes are overexpressed in plants colonized by plant-parasitic nematodes and beneficial endophytic fungi.

The study of sugar transporters in plant-nematode interactions is a relatively recent area of study. Most research has been conducted on the model plant A. thaliana inoculated with M. incognita or H. schachtii; therefore, there is a need to explore the role of sugar transporters in interactions with other agriculturally important nematodes and economically important plants. In the literature search conducted, it was evident that the emphasis has been on AMF and pathogenic fungi, and that there is little information available on transporters in other beneficial endophytic fungi that promote plant growth and protect them from attack by phytopathogens.

There are still many questions remaining to be answered, such as: What other sugar transporters exist in plants? How is the functioning of the various sugar transporters coordinated in the cell? What are the molecular and cellular mechanisms involved in sugar transport in the plant-nematode and plant-endophytic fungus interaction? How is the expression and functioning of transporters modulated in the plant-nematode-beneficial endophytic fungus interaction? What determines that in the competition for nutrients between the endophyte and the nematode the balance tips in one direction or the other? Would the editing of genes encoding sugar transporter proteins in plants for pathogen control affect the colonization of beneficial microorganisms? How could the functioning of plant sugar transporters be used to facilitate their colonization by beneficial microorganisms? Could this knowledge be used in the design of management strategies for plant-parasitic nematodes? The answers to these and many other questions can be resolved by increasing the number of projects involving researchers from different disciplines.

Currently, there are gene editing tools such as the CRISPR-Cas9 technique which allows point mutations to be made in genes of interest. The use of these tools to mutate sugar transporter genes might allow us to know how determinant they are in the establishment and development of beneficial microorganisms, nematodes and plant-parasitic fungi. The manipulation of sugar transporters by means of molecular techniques in agriculturally important crops could help to improve their association with beneficial microorganisms or interfere with the establishment and development of phytopathogens.

Acknowledgments

The authors thank the National Council of Science and Technology for the scholarship granted to the first author for his postgraduate studies.

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Received: October 19, 2022; Accepted: June 26, 2023

*Corresponding author: zavaleta@colpos.mx, tel. +52 777 192 83 87

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