Overexpression of the Potato Monosaccharide Transporter StSWEET7a Promotes Root Colonization by Symbiotic and Pathogenic Fungi by Increasing Root Sink Strength

Abstract

Root colonization by filamentous fungi modifies sugar partitioning in plants by increasing the sink strength. As a result, a transcriptional reprogramming of sugar transporters takes place. Here we have further advanced in the characterization of the potato SWEET sugar transporters and their regulation in response to the colonization by symbiotic and pathogenic fungi. We previously showed that root colonization by the AM fungus Rhizophagus irregularis induces a major transcriptional reprogramming of the 35 potato SWEETs, with 12 genes induced and 10 repressed. In contrast, here we show that during the early colonization phase, the necrotrophic fungus Fusarium solani only induces one SWEET transporter, StSWEET7a, while represses most of the others (25). StSWEET7a was also induced during root colonization by the hemi-biotrophic fungus Fusarium oxysporum f. sp. tuberosi. StSWEET7a which belongs to the clade II of SWEET transporters localized to the plasma membrane and transports glucose, fructose and mannose. Overexpression of StSWEET7a in potato roots increased the strength of this sink as evidenced by an increase in the expression of the cell wall-bound invertase. Concomitantly, plants expressing StSWEET7a were faster colonized by R. irregularis and by F. oxysporum f. sp. tuberosi. The increase in sink strength induced by ectopic expression of StSWEET7a in roots could be abolished by shoot excision which reverted also the increased colonization levels by the symbiotic fungus. Altogether, these results suggest that AM fungi and Fusarium spp. might induce StSWEET7a to increase the sink strength and thus this gene might represent a common susceptibility target for root colonizing fungi.

Carbohydrate and lipid balances in the positive plant phenotypic response to arbuscular mycorrhiza: increase in sink strength

“…In addition, it has been reported that the constitutive overexpression of StSWEET7a , a Glc and fructose transporter from potato, induces accumulation of StInvCD141 transcripts in non‐mycorrhizal roots and increases the frequency and abundance of mycorrhizal colonization when plants are inoculated with R. irregularis (Tamayo et al, 2022). It was proposed that the overexpression of StSWEET7a depletes the apoplast from monosaccharides, and consequently, the sink strength is increased by the upregulation of cell wall‐bound invertases to promote the unloading of Suc to the apoplast (Tamayo et al, 2022). In tomato, Suc depletion in the periarbuscular space mediated by the SUT2 transporter has been reported as a mechanism to control the supply of C to the AMF.…”

“…Recently, it was reported that the upregulation of a cell wall‐bound invertase gene in potato occurs in parallel with the upregulation of genes coding for SWEET, which are responsible for the mobilization of Suc and monosaccharides (Manck‐Götzenberger & Requena, 2016). In addition, it has been reported that the constitutive overexpression of StSWEET7a , a Glc and fructose transporter from potato, induces accumulation of StInvCD141 transcripts in non‐mycorrhizal roots and increases the frequency and abundance of mycorrhizal colonization when plants are inoculated with R. irregularis (Tamayo et al, 2022). It was proposed that the overexpression of StSWEET7a depletes the apoplast from monosaccharides, and consequently, the sink strength is increased by the upregulation of cell wall‐bound invertases to promote the unloading of Suc to the apoplast (Tamayo et al, 2022).…”

“…Regarding FA, Suc and its catabolic products are the main sources of C that support FA biosynthesis in plant tissues (Lim et al, 2017; Ma et al, 2017). Previous studies have revealed the existence of molecular mechanisms that modulate the mycorrhizal development by controlling the amount of Suc and monosaccharides in the periarbuscular space, mediated by SUT and SWEET transporters (An et al, 2019; Bitterlich et al, 2014; Tamayo et al, 2022).…”

Arabidopsis plants engineered for high root sugar secretion enhance the diversity of soil microorganisms

“…[ 17 ] Moreover, ectopic expression of plasma membrane‐localized SWEET7a increased glucose secretion from roots in potato plants as indicated by increased cell wall invertase levels and arbuscular mycorrhiza colonization. [ 18 ]…”

“…[17] Moreover, ectopic expression of plasma membranelocalized SWEET7a increased glucose secretion from roots in potato plants as indicated by increased cell wall invertase levels and arbuscular mycorrhiza colonization. [18] Increased carbon sink strength, resulting from increased sugar storage, consumption, or secretion, can reduce growth when it cannot be balanced by increased source strength, that is, higher photosynthesis rates. Under non-stressed conditions, plants like Arabidopsis and potato were shown to compensate for increased sugar consumption in sink tissues by increased photosynthesis rates.…”