Sugar flux and signaling in plant–microbe interactions

Bezrutczyk, Margaret; Yang, Jungil; Eom, Joon-Seob; Prior, Matthew J.; Sosso, Davide; Hartwig, Thomas; Szurek, Boris; Oliva, Ricardo; Vera-Cruz, C.; White, Frank F.; Yang, Bing; Frommer, Wolf B.

doi:10.1111/tpj.13775

Cited by 180 publications

(168 citation statements)

References 103 publications

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“…So far, all the functionally characterized SWEET family members from different plant species were confirmed to have both sugar efflux and influx activity (Chen et al, 2010(Chen et al, , 2012Lin et al, 2014;Eom et al, 2015). As uniporters, SWEETs transport sugars along a concentration gradient, which raises the question whether MtSWEET1b exports glucose towards the fungus, or whether it imports glucose in competition with the fungus to support the high metabolic activity of arbuscule-containing cells or to avoid defence responses caused by high levels of glucose in the apoplast (Schaarschmidt et al, 2007;Helber et al, 2011;Moore et al, 2015;Bezrutczyk et al, 2018). Several studies indicate that arbuscules-containing cells form a strong sink for hexoses.…”

Section: Researchmentioning

confidence: 99%

A Medicago truncatula SWEET transporter implicated in arbuscule maintenance during arbuscular mycorrhizal symbiosis

Zeng

et al. 2019

New Phytologist

112

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Summary Plants form a mutualistic symbiosis with arbuscular mycorrhizal (AM) fungi, which facilitates the acquisition of scarce minerals from the soil. In return, the host plants provide sugars and lipids to its fungal partner. However, the mechanism by which the AM fungi obtain sugars from the plant has remained elusive. In this study we investigated the role of potential SWEET family sugar exporters in AM symbiosis in Medicago truncatula. We show that M. truncatula SWEET1b transporter is strongly upregulated in arbuscule‐containing cells compared to roots and localizes to the peri‐arbuscular membrane, across which nutrient exchange takes place. Heterologous expression of MtSWEET1b in a yeast hexose transport mutant showed that it mainly transports glucose. Overexpression of MtSWEET1b in M. truncatula roots promoted the growth of intraradical mycelium during AM symbiosis. Surprisingly, two independent Mtsweet1b mutants, which are predicted to produce truncated protein variants impaired in glucose transport, exhibited no significant defects in AM symbiosis. However, arbuscule‐specific overexpression of MtSWEET1bY57A/G58D, which are considered to act in a dominant‐negative manner, resulted in enhanced collapse of arbuscules. Taken together, our results reveal a (redundant) role for MtSWEET1b in the transport of glucose across the peri‐arbuscular membrane to maintain arbuscules for a healthy mutually beneficial symbiosis.

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Section: Researchmentioning

confidence: 99%

A Medicago truncatula SWEET transporter implicated in arbuscule maintenance during arbuscular mycorrhizal symbiosis

Zeng

et al. 2019

New Phytologist

112

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“…7). It is believed that depletion of carbohydrates enhances plant susceptibility to a pathogen infection (Morkunas and Ratajczak 2014, Bezrutczyk et al 2018, Kanwar and Jha 2018. A decrease in the content of total sugars and reducing sugars in B. juncea during progressive A. brassicae infection (Mathpal et al 2011) and Albugo candida infection (Mishra et al 2009) was reported.…”

Section: Black Spot Disease Influences Brassica Juncea Primary Metabomentioning

confidence: 99%

Leaf position‐dependent effect of Alternaria brassicicola development on host cell death, photosynthesis and secondary metabolites in Brassica juncea

Macioszek

Wielanek

Morkunas

et al. 2019

Physiologia Plantarum

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During the first 24 hours of infection, Alternaria brassicicola developmental parameters such as conidial germination, germ tubes and appressoria formation on each of the five mature Brassica juncea leaves, correlated with a leaf position showing stronger development of the pathogen on older leaves than on young ones. As a consequence of fungal development, the black spot disease was observed during 96 hours of infection on a macroscopic scale, as well as via confocal microscopy. Degradation of the chloroplast thylakoids and plastoglobule appearance during infection, followed by the decrease in chlorophyll a fluorescence parameters i.e. maximum quantum yield of PSII (Fv/Fm), non‐photochemical quenching (NPQ) and chlorophyll a:b ratio, have been observed. Also, after an initial increase of carbohydrates (glucose, fructose and sucrose), content far below the respective control values was found. The content of secondary metabolites such as flavonoids and glucosinolates increased in a leaf position‐dependent manner in infected leaves, with a lower level in older leaves than in younger ones. Although, the total phenolic compounds (TPCs) content did not differ significantly in infected leaves compared to control leaves, TPCs level in both control and infected leaves was leaf position‐dependent. To the best of our knowledge, this is the first report on leaf position‐dependent effect on the B. juncea biochemical response to A. brassicicola infection.

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“…The influence of sugars on the expression of genes (including those controlling the growth processes) is often modified by environmental factors, such as changes in the intensity of irradiation or in the access to minerals. The sugars accumulated under drought or cold mainly play the role of osmoregulators and cryoprotectans, but also as a stored source of carbon for later use (when the stress factor ceases to exist); they can also act as regulators modulating plant growth under new conditions [10,12,15,17,18,69]. Soluble sugars (such as, disaccharides, raffinose family oligosaccharides, and fructans) are strongly related to the accumulation of reactive oxygen species under stress conditions.…”

Section: Introductionmentioning

confidence: 99%

“…The following strategies were used in order to select the appropriate mutants: (i) if high sugar concentrations in the medium inhibited germination and seedling development, then the seedlings showing development were nonsusceptible to sugars (for example, gin -glucose insensitive, rsr -reduced sugar response, sis -sucrose insensitive, or migmannose insensitive germination); (ii) seeds incapable of germinating (and growing) on media containing sugar concentrations that did not inhibit the development of other plants were mutants that were excessively sensitive to sugars (for example, gss -glucose super sensitive, sss -sucrose super sensitive, or hsr -high sugar-response). During the last decades, a huge progress has been made in understanding the physiological roles of sugar-metabolizing enzymes or sugar transporters, mainly by using transgenic/ mutational approaches [2,9,18,55,56,75,76]. The use of novel mutants (and transgenic plants) that specifically react to different sugars, as well as hormonal mutants, will certainly be helpful in subsequent studies on the regulatory role of sugars throughout plant development and in the elucidation of crosstalk with other signaling pathways.…”

Section: Introductionmentioning

confidence: 99%

Regulatory roles of sugars in plant growth and development

Ciereszko

2018

Acta Soc Bot Pol

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In recent years, several studies have focused on the factors and mechanisms that regulate plant growth and development, as well as the functioning of signaling pathways in plant cells, unraveling the involvement of sugars in the processes regulating such growth and development. Saccharides play an important role in the life of plants: they are structural and storage substances, respiratory substrates, and intermediate metabolites of many biochemical processes. Sucrose is the major transport form of assimilates in plants. Sugars can also play an important role in the defense reactions of plants. However, it has been shown that glucose, sucrose, or trehalose-6-phosphate (Tre6P) can regulate a number of growth and metabolic processes, acting independently of the basal functions; they can also act as signaling molecules. Changes in the concentration, qualitative composition, and transport of sugars occur continuously in plant tissues, during the day and night, as well as during subsequent developmental stages. Plants have developed an efficient system of perception and transmission of signals induced by lower or higher sugar availability. Changes in their concentration affect cell division, germination, vegetative growth, flowering, and aging processes, often independently of the metabolic functions. Currently, the mechanisms of growth regulation in plants, dependent on the access to sugars, are being increasingly recognized. The plant growth stimulating system includes hexokinase (as a glucose sensor), trehalose-6-phosphate, and TOR protein kinase; the lack of Tre6P or TOR kinase inhibits the growth of plants and their transition to the generative phase. It is believed that the plant growth inhibition system consists of SnRK1 protein kinases and C/S1 bZIP transcription factors. The signal transduction routes induced by sugars interact with other pathways in plant tissues (for example, hormonal pathways) creating a complex communication and signaling network in plants that precisely controls plant growth and development.

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Sugar flux and signaling in plant–microbe interactions

Cited by 180 publications

References 103 publications

A Medicago truncatula SWEET transporter implicated in arbuscule maintenance during arbuscular mycorrhizal symbiosis

A Medicago truncatula SWEET transporter implicated in arbuscule maintenance during arbuscular mycorrhizal symbiosis

Leaf position‐dependent effect of Alternaria brassicicola development on host cell death, photosynthesis and secondary metabolites in Brassica juncea

Regulatory roles of sugars in plant growth and development

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