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Expression of Arabidopsis sugar transport protein STP13 differentially affects glucose transport activity and basal resistance to Botrytis cinerea

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Abstract

Botrytis cinerea is the causing agent of the grey mold disease in more than 200 crop species. While signaling pathways leading to the basal resistance against this fungus are well described, the role of the import of sugars into host cells remains to be investigated. In Arabidopsis thaliana, apoplastic hexose retrieval is mediated by the activity of sugar transport proteins (STPs). Expression analysis of the 14 STP genes revealed that only STP13 was induced in leaves challenged with B. cinerea. STP13-modified plants were produced and assayed for their resistance to B. cinerea and glucose transport activity. We report that STP13-deficient plants exhibited an enhanced susceptibility and a reduced rate of glucose uptake. Conversely, plants with a high constitutive level of STP13 protein displayed an improved capacity to absorb glucose and an enhanced resistance phenotype. The correlation between STP13 transcripts, protein accumulation, glucose uptake rate and resistance level indicates that STP13 contributes to the basal resistance to B. cinerea by limiting symptom development and points out the importance of the host intracellular sugar uptake in this process. We postulate that STP13 would participate in the active resorption of hexoses to support the increased energy demand to trigger plant defense reactions and to deprive the fungus by changing sugar fluxes toward host cells.

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Acknowledgments

Pauline Lemonnier and Florian Veillet are supported by Grants from the French Ministry of Higher Education and Research, and the Région Poitou–Charentes, respectively. We are grateful to Vincent Lebeurre and Bruno Faure for helping us producing numerous plants used in this study. Antoine Plasseraud Desgranges is acknowledged for his help in the correction of the manuscript. We would like to thank all our colleagues for inspiring discussions. The CNRS, the University of Poitiers and the Région Poitou–Charentes are gratefully acknowledged for their financial support.

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  1. UMR CNRS 7267 EBI Ecologie et Biologie des Interactions, Equipe “Physiologie Moléculaire du Transport des Sucres chez les végétaux”, Université de Poitiers, Batiment Botanique B31, 3 rue Jacques Fort, TSA 51106, 86073, Poitiers Cedex 9, France

    Pauline Lemonnier, Cécile Gaillard, Florian Veillet, Jérémy Verbeke, Rémi Lemoine, Pierre Coutos-Thévenot & Sylvain La Camera

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  1. Pauline Lemonnier
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Correspondence to Sylvain La Camera.

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11103_2014_198_MOESM1_ESM.tif

Fig. S1. STP13 mRNA accumulation in STP13OE-6 plants. Plants were sprayed with mock solution or B. cinerea suspension (5.104 conidia.ml−1). Healthy (0 hpi) or treated leaves from at least 3 plants were harvested at indicated time points. The STP13 transcript levels were quantified by RT-qPCR. Data are expressed as normalized expression (no unit) to the plant reference gene At4g26410 expression level (Czechowski et al. 2005). Data are mean ± SE from 2 independent experiments. STP13 expression level of B. cinerea infected WT plants (48 hpi) is indicated. B.c.: B. cinerea. hpi: hours post-inoculation (TIFF 7185 kb)

11103_2014_198_MOESM2_ESM.tif

Fig. S2. Disease phenotype of wild-type (WT) and C2-7 plants infected with B. cinerea. A construct including the cDNA corresponding to STP13 mRNA driven by the CaMV35S promoter was introduced into stp13-2. In the resulting plants (named C2-7), leaves of five-week-old plants have been used for inoculation tests. A. Lesion diameters observed on WT and C2-7 plants 3 days after inoculation with 6 µl droplets containing 104 conidia.ml−1. Data represent the mean (± SE) lesion diameter from 4 independent experiments. In each experiment, at least 5 plants per genotype were infected with B. cinerea. No significant difference was determined between WT and C2-7 plants according to a permutation with general scores test (P < 0,05). B. Lesion size distribution observed on WT and C2-7 plants infected with B. cinerea. Plants were drop-inoculated and diameters of necrotic lesions (LD) were measured after 3 days. Lesions were grouped into 3 classes according to their size: small (LD < WT first quartile), medium (LD = WT interquartile range) and large (LD > WT third quartile). The percentage of lesion size distribution from 4 independent experiments is shown. No significant difference between WT and C2-7 was determined by a Chi square test (P < 0,05) (TIFF 5987 kb)

Fig. S3. Six week-old wild-type (WT), stp13-2 and STP13OE-6 plants grown on soil (TIFF 1482 kb)

11103_2014_198_MOESM4_ESM.pdf

Table S2 Table reporting the results of the three-way ANOVA test of PDF1.2 and PAD3 expression. Genotype: wild-type, stp13-2 or STP13OE-6 plants. Time: 0, 24, 48 or 72 h post-treatment. Treatment: mock or B. cinerea (**P < 0,01; ***P < 0,001; nsd: not statistically different)(PDF 18 kb)

Table S1 List of primers used for RT-qPCR analysis (PDF 23 kb)

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Lemonnier, P., Gaillard, C., Veillet, F. et al. Expression of Arabidopsis sugar transport protein STP13 differentially affects glucose transport activity and basal resistance to Botrytis cinerea . Plant Mol Biol 85, 473–484 (2014). https://doi.org/10.1007/s11103-014-0198-5

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