Arbuscular mycorrhiza Symbiosis Induces a Major Transcriptional Reprogramming of the Potato SWEET Sugar Transporter Family

Abstract

Biotrophic microbes feeding on plants must obtain carbon from their hosts without killing the cells. The symbiotic Arbuscular mycorrhizal (AM) fungi colonizing plant roots do so by inducing major transcriptional changes in the host that ultimately also reprogram the whole carbon partitioning of the plant. AM fungi obtain carbohydrates from the root cortex apoplast, in particular from the periarbuscular space that surrounds arbuscules. However, the mechanisms by which cortical cells export sugars into the apoplast for fungal nutrition are unknown. Recently a novel type of sugar transporter, the SWEET, able to perform not only uptake but also efflux from cells was identified. Plant SWEETs have been shown to be involved in the feeding of pathogenic microbes and are, therefore, good candidates to play a similar role in symbiotic associations. Here we have carried out the first phylogenetic and expression analyses of the potato SWEET family and investigated its role during mycorrhiza symbiosis. The potato genome contains 35 SWEETs that cluster into the same four clades defined in Arabidopsis. Colonization of potato roots by the AM fungus Rhizophagus irregularis imposes major transcriptional rewiring of the SWEET family involving, only in roots, changes in 22 of the 35 members. None of the SWEETs showed mycorrhiza-exclusive induction and most of the 12 induced genes belong to the putative hexose transporters of clade I and II, while only two are putative sucrose transporters from clade III. In contrast, most of the repressed transcripts (10) corresponded to clade III SWEETs. Promoter-reporter assays for three of the induced genes, each from one cluster, showed re-localization of expression to arbuscule-containing cells, supporting a role for SWEETs in the supply of sugars at biotrophic interfaces. The complex transcriptional regulation of SWEETs in roots in response to AM fungal colonization supports a model in which symplastic sucrose in cortical cells could be cleaved in the cytoplasm by sucrose synthases or cytoplasmic invertases and effluxed as glucose, but also directly exported as sucrose and then converted into glucose and fructose by cell wall-bound invertases. Precise biochemical, physiological and molecular analyses are now required to profile the role of each potato SWEET in the arbuscular mycorrhizal symbiosis.

Differential effects of varied potassium and magnesium nutrition on production and partitioning of photoassimilates in potato plants

“…However, as an alternative scenario, it is feasible that an impaired function of H + ‐ATPases already affects an earlier step of sucrose transport. This is the efflux of sucrose from mesophyll cells into the apoplast what is carried out via SUGARS WILL EVENTUALLY BE EXPORTED TRANSPORTERS (SWEETs; Manck‐Götzenberger and Requena ). We hypothesize that these SWEET transporters are forced to reduce the export of sucrose from the mesophyll into the apoplast because of a reduced activity of H + /sucrose symporters.…”

Nutrient demand and fungal access to resources control the carbon allocation to the symbiotic partners in tripartite interactions of Medicago truncatula

“…We also determined the expression of six SWEETs in the roots of M. truncatula after colonization with different root symbionts. SWEETs can not only catalyse the efflux of carbohydrates but also their uptake (Chen, ), and it has recently been suggested that members of the SWEET family could be involved in the symbiotic C flux (Kryvoruchko et al, ; Manck‐Götzenberger & Requena, ; Sugiyama et al, ). In contrast to MtSWEET11 that is specifically expressed in root nodules, none of the other SWEETs we tested showed a mycorrhiza‐restricted induction, but three of the SWEETs, MtSWEET1b , MtSWEET6 , and MtSWEET15d , were upregulated in AM roots compared with control roots (Figure S5).…”

“…In contrast to MtSWEET11 that is specifically expressed in root nodules, none of the other SWEETs we tested showed a mycorrhiza‐restricted induction, but three of the SWEETs, MtSWEET1b , MtSWEET6 , and MtSWEET15d , were upregulated in AM roots compared with control roots (Figure S5). According to the M. truncatula gene expression atlas (http://mtgea.noble.org/v3), MtSWEET1b and MtSWEET6 are highly expressed in arbusculated cells, and their putative orthologues StSWEET1a , StSWEET1b , and StSWEET 7a from potato also show high transcript levels in mycorrhizal roots (Manck‐Götzenberger & Requena, ). Although MtSWEET1b and MtSWEET6 are also highly expressed in rhizobial roots, the downregulation of both transporters in the tripartite interactions of Experiment 1 (Figure ), in which a suppression of the AM colonization by rhizobia was observed (Figure S2a), is an agreement with a potential role of both transporters for the sugar transport in arbusculated cells.…”

Sugars en route to the roots. Transport, metabolism and storage within plant roots and towards microorganisms of the rhizosphere

“…So far, only a single study focused on SWEET transporters in mycorrhizal systems. Manck‐Gotzenberger and Requena () showed that the SWEET family in potato comprises 35 StSWEET and that 22 StSWEET genes were differentially regulated in response to AM symbiosis. Both plasma membrane (StSWEET7a and StSWEET12a) and tonoplastic (StSWEET2c) transporters are specifically relocalized in plant cells colonized by fungal arbuscules.…”