Sucrose Mobilization and Catabolism in Arbuscular Mycorrhizal Plants: History
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Subjects: Agriculture, Dairy & Animal Science
Contributor:
Ana Chávez-Bárcenas
,
Isaac A. Salmeron-Santiago
,
Juan Jose Valdez Alarcon
,
Martha Elena Pedraza-Santos
,
Gustavo Santoyo
,
Maria J. Pozo

Arbuscular mycorrhizal fungi (AMF) are obligate biotrophs that supply mineral nutrients to the host plant in exchange for carbon derived from photosynthesis. Sucrose is the end-product of photosynthesis and the main compound used by plants to translocate photosynthates to non-photosynthetic tissues. AMF alter carbon distribution in plants by modifying the expression and activity of key enzymes of sucrose biosynthesis, transport, and/or catabolism. 

  • arbuscular mycorrhiza
  • mycorrhizal plants
  • sucrose catabolism

1. Introduction

Arbuscular mycorrhiza (AM) is a mutualistic association between fungi from the Glomeromycotina group and plants from most phylogenetic clades [1][2]. The mutualistic nature of arbuscular mycorrhizae implies a bidirectional flow of nutrients between plant roots and arbuscular mycorrhizal fungi (AMF). The plant gives up part of its photoassimilates to the fungus, an obligate symbiont with a heterotrophic metabolism that grows and develops in the internal root tissues [3]. One key benefit for the host plants from this biological interaction is the improved acquisition of water and mineral nutrients, in particular phosphorus (P) [4][5][6]. The regulation of this resource exchange between the plant and fungal partners is key for the functioning of symbiosis, as it determines the net outcome of the interaction. Major research efforts have been devoted in the last few decades to an understanding of the trading of resources between the plant and fungal symbiont [7][8].

2. Sucrose Transporters and Sucrose Mobilization in Mycorrhizal Plants

To achieve carbon loading in non-photosynthetic tissues, Suc synthesized in mesophyll cells reaches the apoplast adjacent to the phloem, where phloem loading is mediated by SUT [9]. The SUT proteins form a small three clade family divided into types I, II, and III; SUT types I and II are found in the phloem tissues and they import Suc into the phloem for the mobilization of carbon from the source to the sink tissues. The transporters of the type III clade are located in the tonoplast membrane where they transiently load Suc into the tonoplast [10].
A semiquantitative RT-PCR transcriptional analysis of SUT transporters in tomato (S. lycopersicum) plants colonized by Glomus caledonium or G. intraradices estimated the down-regulation of SlSUT1 in the source tissues of mycorrhizal S. lycopersicum, and its expression was not influenced by the availability of P, but it was related to the presence of the AMF in the roots [11]. Further quantitative RT-PCR (qRT-PCR) studies in F. mosseae colonized S. lycopersicum plants revealed an up-regulation of SlSUT1 (type I), SlSUT2 (type II), and SlSUT4 (type III) in the leaves. While SlSUT1 and SlSUT4 were up-regulated in the roots, SlSUT2 was not [12].
In M. truncatula, the increased expression of MtSUT1-1, MtSUT2, and MtSUT4-1 (orthologous to SlSUT1, SlSUT2, and SlSUT4, respectively) was described by qRT-PCR in the leaves and roots of plants grown at low P concentrations (NaH2PO4, 0.13 mM); the expression of those genes in the leaves was even higher under Rhizophagus sp. colonization, suggesting that AMF induces carbon flux from the source tissues to the phloem [13]. The roots also showed more MtSUT1-1 transcript accumulation in low P when plants were mycorrhized; however, MtSUT2 and MtSUT4-1 were similar in mycorrhizal and non-mycorrhizal plants [13].
According to the studies reported above, the S. lycopersicum and M. truncatula SUT orthologous from the same divergent clades exhibit similar expression patterns in the source and sink tissues in response to mycorrhizal colonization. While genes from the three SUT types were up-regulated in the leaves of both plant species, only type I and III transporters were transcriptionally up-regulated in mycorrhized roots. Thus, we propose that the enhanced expression of SUT orthologous genes in the source and sink tissues in response to mycorrhizal colonization in angiosperms of divergent lineages is the result of a conserved molecular mechanism to supply carbon to AMF in which the Suc flow mediated by SUT transporters is a common trait in higher plants.
The enhanced SUT expression observed in mycorrhizal S. lycopersicum correlated with Suc and Fru accumulation and the decrease in Glc in the roots [12]. These results suggest that the carbon delivered to the roots as Suc is catabolized to generate Glc that is preferably used to supply carbon to the AMF, thus contributing to Fru accumulation in the root tissues [12]. In M. truncatula, lower concentrations of Suc, Glc, and Fru in the leaves of mycorrhizal plants was proposed to be a consequence of higher sugar transport activity in source tissues [13].
The heterologous expression of the spinach (Spinacia oleracea) SUT1 transporter gene (SoSUT1) fused to the constitutive CaMV 35S promoter led to an increase in the colonization capacity of R. irregularis in S. tuberosum, despite high P levels in the soil. This high P concentration strongly inhibited AMF colonization in the wild-type genotype and in a silenced SUT1 mutant that was also tested under the same conditions, supporting the claim that the carbon supply exerted by the source tissues controls AMF colonization [14]. Plants inoculated with R. irregularis at a low P content showed similar levels of colonization in the wild type and the overexpressing and the silenced SUT1 S. tuberosum mutants; therefore, it was hypothesized that when phloem loading is impaired due to SUT1 silencing, plants tend to prioritize carbon delivery to sustain the mycorrhizal symbiosis. In agreement with this hypothesis, mycorrhized silenced SUT1 plants showed a lower biomass accumulation [14].
In grafting experiments in which S. lycopersicum SUT2-silenced mutants and wild-type genotypes were combined, Bitterlich et al. (2014) demonstrated a reproducible increase in root colonization by F. mosseae or R. irregularis when inoculated independently in silenced SlSUT2 root stocks, indicating a root-specific function of SUT2 in the carbon flux to AMF. Furthermore, the positive growth response to AMF colonization was abolished in SlSUT2 antisense plants [15]. Remarkably, the SUT2 transporter was specifically immunolocalized in the periarbuscular membrane in cortical cells, suggesting that SUT2 transports Suc from the periarbuscular matrix back to the cytoplasm of the plant cell. Thus, SUT2 exerts an important influence on carbon distribution between symbionts in mycorrhizal associations, regulating the amount of Suc in the periarbuscular space and controlling the carbon supplied to the fungal symbiont [15]. The phenotype of S. lycopersicum SUT2-silenced plants can be partially rescued by the exogenous application of brassinosteroids, suggesting that the biosynthetic/signaling pathway of this plant growth regulator is linked to the Suc–carbon partitioning pathway, mediated by SUT2. Therefore, it is possible that brassinosteroids may be involved in carbon distribution to AMF during the arbuscular mycorrhizal interaction [15][16].
The most recently discovered plant carbohydrate transporter proteins are the SWEET transporters [17]. They are encoded by a multigenic family that clusters four subgroups classified by their affinity for carbohydrates. In S. lycopersicum, the four groups are subsequently separated into Class I transporters that mediate Glc and Fru transport, and Class II transporters, which have a higher affinity for Glc and Suc [18]. SWEET transporters function as Suc exporters, releasing Suc to the apoplast, and their function is essential for phloem loading [19]. Several events of plant development such as the embryonic and reproductive tissue development in A. thaliana, Glycine max, and Petunia axillaris have been related to the carbohydrate transport activity of SWEET proteins [20][21][22].
Increasing evidence indicates that SWEET transporters play major roles in the mutualistic and pathogenic interactions of plants with microorganisms [23][24][25][26]. The differential regulation of some SWEET genes has been demonstrated. For example, the genome of Lotus japonicus contains 13 SWEET codifying genes. The transcriptional analysis of this gene family during symbiosis revealed that only LjSWEET3 is up-regulated in nodules formed by Mesorhizobium loti, and its expression was also increased in roots colonized by R. irregularis [25]. The expression level of the 35 SWEET genes in the S. tuberosum genome was analyzed in roots inoculated with R. irregularis in three temporally defined stages of mycorrhizal development, and 22 of these genes were differentially expressed in at least two of the three stages studied [23]. The study led to the identification of three SWEET genes from divergent clades in the transporter family that were induced by the mycorrhiza. The promoter of these three genes was subsequently fused to the β-glucuronidase gene to characterize their expression in non-mycorrhized and mycorrhized M. truncatula plants. In all cases, the reporter gene expression was specifically detected in the cortical cells containing arbuscules. In particular, the promoter of StSWEET2a, a putative Suc transporter, controlled the expression of the reporter gene only at the root apex of non-mycorrhized plants. According to these authors, the induced specific expression of StSWEET2a in the arbusculated cortical cells supports the claim that Suc is an important source that helps the carbon demands of the fungal symbiont in arbuscular mycorrhizal interactions to be met [23]. This transcriptional analysis of SWEET genes in S. tuberosum showed that StWEET1a, StSWEET1b, and StWEET7a are genes that are up-regulated in mycorrhized plants [23]. Their putative orthologs in M. trucatula, MtSWEET1b, and MtSWEET6 also showed higher expression levels in mycorrhizal plants [27]. Remarkably, the simultaneous colonization of M. truncatula by R. irregularis and Ensifer meliloti in a tripartite association led to a reduction in mycorrhizal colonization, the down-regulation of MtSWEET1b and MtSWEET6 expression in the roots, and the up-regulation of MtSWEET15d in the root nodules. Accordingly, the authors concluded that MtSWEET1b and MtSWEET6 play a key role in the specific carbon transfer to the AMF [27]. An et al. (2019) further characterized this mycorrhiza-upregulated MtSWEET1b as a Glc transporter located in the periarbuscular membrane [28]. Phylogenetically, MtSWEET1b shares its origin with MtSWEET1a, as both are homologous to the A. thaliana gene AtSWEET1, a bidirectional uniporter facilitator of Glc that is highly expressed in flowers and pollen tubes, but with a weak expression in the roots [28][29]. There are at least two SWEET genes homologous to AtSWEET1 in the genome of plants that belong to both lineages of angiosperms such as O. sativa, L. japonicus, and S. tuberosum, and as reported for M. truncatula, at least one of those genes showed an up-regulation in mycorrhized plants [28].
As proposed for SUT transporters, the activity of the SWEET genes described in AM points to a common molecular mechanism for carbon delivery to the fungus in divergent clades of angiosperms, and they appear to play an essential role in plant–microbe interactions. Moreover, the lack of mycorrhizal-responsive homologs of SWEET transporters in A. thaliana suggests that, besides the inability for proper molecular signaling with AMF, non-mycorrhizal plants may have lost the genes required to maintain an efficient carbon efflux to the fungal symbiont (Figure 1). In this regard, it was recently reported that non-mycorrhizal plants are unable to interact with AMF due to the loss or pseudogenization of key genes essential for plant-microbial signaling [30].
In addition to the sugar transporters belonging to the SUT and SWEET families, monosaccharide transporters have also been associated with carbon partitioning to the fungal symbiont in arbuscular mycorrhizal interactions. The first experimental evidence for the induced expression of an M. truncatula hexose transporter (Mtst1) in the roots of M. truncatula and M. sativa colonized by an AMF was presented by Harrison (1996). She also reported the induced expression of Mtst1 in M. truncatula roots colonized by G. versiforme and located its transcripts in arbusculated cortical cells by in-situ hybridization [31].
The S. lycopersicum transporter SlSFP7 (formerly named LeST3) was subsequently identified and characterized by García-Rodríguez et al. (2005) as a hexose transporter of the major facilitator superfamily [32][33]. Its expression level increases in the source tissues in plants colonized by different AMF and by the phytopathogen Phytophthora parasitica, while the level of expression remains constant in the roots. The authors suggested that the up-regulation of this monosaccharide transporter in the leaves is the result of the increased carbon demand imposed by the pathogenic or mutualistic fungal interaction, and its function is to mobilize hexoses from the source tissues to the roots [32]. Ge et al. (2008) also compared the expression of SlSFP7 in plants colonized by AMF. They described that when S. lycopersicum roots were colonized by G. intraradices, the expression level of SlSFP7 increased in the leaves and roots. However, in plants colonized by G. caledonium, the expression levels of this transporter were reduced compared to the control plants, in disagreement with the former hypothesis of SlSFP7 responding to fungal interactions independently of its parasitic or mutualistic behavior, as proposed by García-Rodríguez et al. (2005) [32]. Remarkably, SlSFP7 was the only sugar transporter evaluated by Ge et al. (2008) that showed a transcriptional response to mycorrhization. The contrasting response in the expression of SlSFP7 in S. lycopersicum plants colonized by different AMF species was interpreted as the recruitment of different molecular elements in a single plant species by different AMF species to obtain a carbon supply [11].
The previous studies suggested that different AMF species may exert different levels of carbon sink strength, and thus the level of stimulation of carbon allocation to the symbiotic interphase. A fine-tuned regulation of the expression of plant carbohydrate transporters was also described as involved in the carbon allocation towards the fungal symbiont [13]. Moreover, positive growth responses in mycorrhizal plants showed an up-regulation of SWEET, while non-cooperative mycorrhizal interactions did not [34].
Based on these results, we propose that the ability of AM to impact plant carbon allocation and establish itself as a sink depends in part on the ability of AMF to stimulate the expression and activity of plant carbohydrate transporters, resulting in the amount of carbon received from the host. Consequently, a mycorrhizal interaction that promotes sink stimulation will promote plant growth.
Increased expression of the monosaccharide transporter ZmMST1 was detected in maize roots colonized by G. intraradices. The up-regulation of this gene was observed under conditions of P scarcity and was related to an increase in the concentration of soluble sugars in roots, supporting the role of this transporter in the carbon allocation to AMF [35].
In summary, an analysis of sugar transporters in AMF-colonized plants suggests that to sustain carbon uptake by AMF, sugar is exported to the periarbuscular space through molecular mechanisms controlled by SWEET proteins in the periarbuscular membrane. SWEET proteins have also been proposed as active controllers of the carbon supply by acting as cytoplasmic importers of Suc/hexoses released to the periarbuscular space. The common expression patterns of orthologous genes observed in different model plants upon AMF colonization support the hypothesis of a common molecular mechanism that supplies carbohydrates to the symbiont in vascular plants, in which SUT, SWEET, and monosaccharide transporters have a common role.

3. Mycorrhizal Symbiosis and Sucrose Catabolism in Plants

The genes encoding the SuSy and invertase enzymes are present in small families in plant genomes [36][37]. Plant invertases are located subcellularly in the cytoplasm, mitochondria, chloroplast, vacuole, and in the cell wall [37]. It has been proposed that in arbuscular mycorrhizal interactions, cell wall invertases, also named apoplastic invertases, hydrolyze Suc in the periarbuscular space and generate the hexoses that will be taken up by AMF. In this regard, promoter analyses and in-situ hybridization studies have revealed the expression of the S. lycopersicum LIN6 promoter activity, which encodes an apoplastic invertase in arbusculated cells [38]. LIN6 transcription was also up-regulated in response to environmental stresses, mechanical stimuli, and by pathogen infection [39].
The experimental evidence obtained for S. lycopersicum and S. tuberosum has led to recent models that describe carbon transfer from the host plant to the fungal symbiont, where apoplastic invertases directly generate hexoses delivered to AMF [38][40][23]. Vacuolar invertase expression is also induced in Phaseolus vulgaris roots colonized by G. intraradices [41], while the specific enzymatic activity of cytosolic invertases increased in G. max, colonized by G. mosseae compared to other types of invertases [42]. This supports the claim that the regulatory cycles of Suc biosynthesis and catabolism in subcellular compartments participate in carbon allocation to AMF during mycorrhizal interaction (Figure 1).
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Figure 1. Carbon flux to the cortical root cells during arbuscular–mycorrhizal interactions. Photosynthates flow through the mycorrhizal plant from the leaves to the arbusculated cortical cells in the roots. The catabolism of Suc in the arbusculated and other cortical cells close to them promotes Suc mass flow and enables the translocation of hexoses, Suc, and lipids to the periarbuscular space towards the fungal arbuscule, imposing a carbon sink (Updated from Wipf et al., 2019; Roth and Paszkowski, 2017; and Manck-Götzenberger and Requena, 2016 [8][43][23]). Blue arrows trace the current carbon flow routes, the discontinued orange arrows show the “futile” cycles of sucrose catabolism and synthesis, the colored barrels designate the carbohydrate transporters. Enzymes are indicated in numbered circles as: (1) Sucrose synthase; (2) Neutral invertase; (3) Apoplastic invertase; (4) Vacuolar invertase; (5) Glycerol-3-phosphate acyl transferase. Numbers in rounded rectangles denote specific metabolic pathways: (1) Suc as a source for aerobic respiration; (2) Glycolytic pathway to render phosphoenolpyruvate; (3) lipid synthesis mediated by the plastid Type I FAS molecular complex. Diamonds indicate potential carbon fluxes as: (1) symplastic and (2) apoplastic routes of hexoses entry to sink cells. Sucrose* indicates the sucrose biosynthesized in the arbusculated cell.
Tobacco plants overexpressing a yeast-derived invertase under the constitutive 35S promoter were inoculated with G. intraradices. Heterozygous lines with different increased invertase levels in the leaves displayed a higher accumulation of hexoses in their source leaves, but no increase in invertase activity or hexose accumulation was observed in the roots, regardless of the activity levels achieved in leaves. The plant lines with higher invertase activity showed lower hexoses content in the roots, together with the up-regulation of the pathogenesis-related (PR) genes PAR1, PR-Q, and PR-1b in the leaves, and reduced levels of root mycorrhization. These results indicated that hexoses accumulated in the leaves activated defense mechanisms potentially with a negative effect on AMF; moreover, they suggest that changes in carbohydrate metabolism in shoots influence the establishment of mycorrhizal interaction in the roots, and that this influence is not exclusively determined by the carbon supply to roots [44]. Interestingly, yeast invertase expression specifically targeted to the tobacco root system increased hexose accumulation, but it did not affect AM colonization [45]. Similarly, the transformed roots of M. truncatula expressing apoplast-, cytosol-, or vacuolar-located yeast-derived invertases accumulated hexoses, but this did not impact mycorrhization [45]. Thus, the authors concluded that the increase in hexose levels did not significantly impact the symbiosis physiology, and that the invertase-controlled carbon supply to the fungus is not a limiting factor. This suggests the existence of other controllers of carbon allocation in the roots [45], as the mechanism previously described regarding SUT transporters [15].
Similar to invertases, Suc synthases (SuSy) are encoded by a small family of genes in most plant species. In M. truncatula, five genes encoding SuSy have been identified in the genome, but only one, MtSucS1, was induced in mycorrhizal roots with G. mosseae. The fusion of specific regions of MtSucS1 to the gusAint reporter gene led to the localization of the chimeric protein in arbusculated cells, but also in the adjacent cells [46]. An analogous pattern of expression of SuSy transcripts in the roots of P. vulgaris colonized by G. intraradices was previously observed by in-situ hybridization [41]. To further analyze mycorrhizal physiology, M. truncatula MtSucS1-antisense lines were inoculated with G. mosseae. The arbuscules in the roots of these plants were early-senescent, did not reach complete differentiation, and colonization was impaired compared to the wild-type phenotype. This aberrant mycorrhizal phenotype was also accompanied by a reduced expression of mycorrhiza-induced plant genes, such as the Pi transporter MtPT4. This led to the conclusion that MtSucS1 is essential to maintain normal arbuscular development and its influence in carbon distribution cannot be replaced solely by invertase activity [47]. Indeed, mycorrhizal colonization-induced genes encoding SuSy and invertases with different subcellular localization, including the LIN6 gene in S. lycopersicum [32]. It has been proposed that SuSy is an important element that generates Suc mobilization gradients to arbusculated cells by maintaining Suc cleavage in the cytoplasm to generate products that could be used to fuel the metabolically active colonized cell, or to export hexoses to the AMF during the interaction [32][41][46].
In summary, it is widely recognized that apoplastic invertase activity generates hexoses from Suc catabolism to be delivered to the fungal partner during mycorrhizal interactions; therefore, its function is to reduce the concentration of Suc in the periarbuscular space to maintain a constant Suc efflux to this zone, while the influx of Suc to the arbusculated cell is also maintained by SuSy and invertases located in other subcellular spaces such as the vacuole and the cytoplasm.

This entry is adapted from the peer-reviewed paper 10.3390/microorganisms10010075

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