Abstract
Main conclusion
This review summarizes the current understanding, future challenges and ongoing quest on sugar metabolic alterations that influence the outcome of plant–pathogen interactions.
Intricate cellular and molecular events occur during plant–pathogen interactions. They cause major metabolic perturbations in the host and alterations in sugar metabolism play a pivotal role in governing the outcome of various kinds of plant–pathogen interactions. Sugar metabolizing enzymes and transporters of both host and pathogen origin get differentially regulated during the interactions. Both plant and pathogen compete for utilizing the host sugar metabolic machinery and in turn promote resistant or susceptible responses. However, the kind of sugar metabolism alteration that is beneficial for the host or pathogen is yet to be properly understood. Recently developed tools and methodologies are facilitating research to understand the intricate dynamics of sugar metabolism during the interactions. The present review elaborates current understanding, future challenges and ongoing quest on sugar metabolism, mobilization and regulation during various plant–pathogen interactions.
This is a preview of subscription content, access via your institution.




References
Agudelo-Romero P, Erban A, Rego C et al (2015) Transcriptome and metabolome reprogramming in Vitis vinifera cv. Trincadeira berries upon infection with Botrytis cinerea. J Exp Bot 66:1769–1785. https://doi.org/10.1093/jxb/eru517
Ali A, Alexandersson E, Sandin M et al (2014) Quantitative proteomics and transcriptomics of potato in response to Phytophthora infestans in compatible and incompatible interactions. BMC Genom 15:497. https://doi.org/10.1186/1471-2164-15-497
Aliferis KA, Jabaji S (2012) FT-ICR/MS and GC-EI/MS metabolomics networking unravels global potato sprout’s responses to Rhizoctonia solani infection. PLoS One 7(8):e42576. https://doi.org/10.1371/journal.pone.0042576
Aliferis KA, Faubert D, Jabaji S (2014) A metabolic profiling strategy for the dissection of plant defense against fungal pathogens. PLoS One 9:e111930. https://doi.org/10.1371/journal.pone.0111930
Allwood JW, Clarke A, Goodacre R, Mur LAJ (2010) Dual metabolomics: a novel approach to understanding plant–pathogen interactions. Phytochemistry 71:590–597. https://doi.org/10.1016/j.phytochem.2010.01.006
Allwood JW, Heald J, Lloyd AJ et al (2012) Separating the inseparable: the metabolomic analysis of plant–pathogen interactions. Methods Mol Biol 860:31–49. https://doi.org/10.1007/978-1-61779-594-7_3
Alves MS, Dadalto SP, Gonçalves AB et al (2013) Plant bZIP transcription factors responsive to pathogens: a review. Int J Mol Sci 14:7815–7828. https://doi.org/10.3390/ijms14047815
Antony G, Zhou J, Huang S et al (2010) Rice xa13 recessive resistance to bacterial blight is defeated by induction of the disease susceptibility gene Os-11N3. Plant Cell 22:3864–3876. https://doi.org/10.1105/tpc.110.078964
Berger S, Papadopoulos M, Schreiber U et al (2004) Complex regulation of gene expression, photosynthesis and sugar levels by pathogen infection in tomato. Physiol Plant 122:419–428. https://doi.org/10.1111/j.1399-3054.2004.00433.x
Berger S, Benediktyová Z, Matous K et al (2007a) Visualization of dynamics of plant–pathogen interaction by novel combination of chlorophyll fluorescence imaging and statistical analysis: differential effects of virulent and avirulent strains of P. syringae and of oxylipins on A. thaliana. J Exp Bot 58:797–806. https://doi.org/10.1093/jxb/erl208
Berger S, Sinha AK, Roitsch T (2007b) Plant physiology meets phytopathology: plant primary metabolism and plant pathogen interactions. J Exp Bot 58:4019–4026. https://doi.org/10.1093/jxb/erm298
Bezrutczyk M, Yang J, Eom JS et al (2018) Sugar flux and signaling in plant–microbe interactions. Plant J 93(4):675–685. https://doi.org/10.1111/tpj.13775
Bolouri Moghaddam MR, Van den Ende W (2012) Sugars and plant innate immunity. J Exp Bot 63:3989–3998. https://doi.org/10.1093/jxb/ers129
Bolouri Moghaddam MR, Van Den Ende W (2013) Sweet immunity in the plant circadian regulatory network. J Exp Bot 64:1439–1449
Bolton MD (2009) Primary metabolism and plant defense—fuel for the fire. Mol Plant Microbe Interact 22:487–497. https://doi.org/10.1094/MPMI-22-5-0487
Bonfig KB, Schreiber U, Gabler A et al (2006) Infection with virulent and avirulent P. syringae strains differentially affects photosynthesis and sink metabolism in Arabidopsis leaves. Planta 225:1–12. https://doi.org/10.1007/s00425-006-0303-3
Botanga CJ, Bethke G, Chen Z et al (2012) Metabolite profiling of Arabidopsis inoculated with Alternaria brassicicola reveals that ascorbate reduces disease severity. Mol Plant Microbe Interact 25:1628–1638. https://doi.org/10.1094/MPMI-07-12-0179-R
Brzin J, Petrovič N, Ravnikar M, Kovač M (2011) Induction of sucrose synthase in the phloem of phytoplasma infected maize. Biol Plant 55:711–715. https://doi.org/10.1007/s10535-011-0173-9
Buhtz A, Witzel K, Strehmel N et al (2015) Perturbations in the primary metabolism of tomato and Arabidopsis thaliana plants infected with the soil-borne fungus Verticillium dahliae. PLoS One 10(9):e0138242. https://doi.org/10.1371/journal.pone.0138242
Cabello S, Lorenz C, Crespo S et al (2014) Altered sucrose synthase and invertase expression affects the local and systemic sugar metabolism of nematode-infected Arabidopsis thaliana plants. J Exp Bot 65:201–212. https://doi.org/10.1093/jxb/ert359
Carolan JC, Caragea D, Reardon KT et al (2011) Predicted effector molecules in the salivary secretome of the pea aphid (Acyrthosiphon pisum): a dual transcriptomic/proteomic approach. J Proteome Res 10:1505–1518. https://doi.org/10.1021/pr100881q
Ceusters J, Van de Poel B (2018) Update: ethylene exerts species-specific and age-dependent control of photosynthesis. Plant Physiol 176(4):2601–2612. https://doi.org/10.1104/pp.17.01706
Cevallos-Cevallos JM, Futch DB, Shilts T et al (2012) GC–MS metabolomic differentiation of selected citrus varieties with different sensitivity to citrus huanglongbing. Plant Physiol Biochem 53:69–76. https://doi.org/10.1016/j.plaphy.2012.01.010
Chandran D, Inada N, Hather G et al (2010) Laser microdissection of Arabidopsis cells at the powdery mildew infection site reveals site-specific processes and regulators. Proc Natl Acad Sci USA 107:460–465. https://doi.org/10.1073/pnas.0912492107
Chang Q, Liu J, Lin X et al (2017) A unique invertase is important for sugar absorption of an obligate biotrophic pathogen during infection. New Phytol 215:1548–1561. https://doi.org/10.1111/nph.14666
Chen J-G, Jones AM (2004) AtRGS1 function in Arabidopsis thaliana. Methods Enzymol 389:338–350. https://doi.org/10.1016/S0076-6879(04)89020-7
Chen L-Q, Hou B-H, Lalonde S et al (2010) Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468:527–532. https://doi.org/10.1038/nature09606
Chen HY, Huh JH, Yu YC et al (2015) The Arabidopsis vacuolar sugar transporter SWEET2 limits carbon sequestration from roots and restricts Pythium infection. Plant J 83:1046–1058. https://doi.org/10.1111/tpj.12948
Cho Y-H, Yoo S-D, Sheen J (2006) Regulatory functions of nuclear hexokinase1 complex in glucose signaling. Cell 127:579–589. https://doi.org/10.1016/j.cell.2006.09.028
Chong J, Piron M-C, Meyer S et al (2014) The SWEET family of sugar transporters in grapevine: VvSWEET4 is involved in the interaction with Botrytis cinerea. J Exp Bot 65:6589–6601. https://doi.org/10.1093/jxb/eru375
Chou HM, Bundock N, Rolfe S, Scholes JD (2000) Infection of Arabidopsis thaliana leaves with Albugo candida (white blister rust) causes a reprogramming of host metabolism. Mol Plant Pathol 1:99–113. https://doi.org/10.1046/j.1364-3703.2000.00013.x
Chu Z, Yuan M, Yao J et al (2006) Promoter mutations of an essential gene for pollen development result in disease resistance in rice. Genes Dev 20:1250–1255. https://doi.org/10.1101/gad.1416306
Cohn M, Bart RS, Shybut M et al (2014) Xanthomonas axonopodis virulence is promoted by a transcription activator-like effector-mediated induction of a SWEET sugar transporter in cassava. Mol Plant Microbe Interact 27:1186–1198. https://doi.org/10.1094/MPMI-06-14-0161-R
Copley TR, Aliferis KA, Kliebenstein DJ, Jabaji SH (2017) An integrated RNAseq-1H NMR metabolomics approach to understand soybean primary metabolism regulation in response to Rhizoctonia foliar blight disease. BMC Plant Biol 17:84. https://doi.org/10.1186/s12870-017-1020-8
Dao TTH, Linthorst HJM, Verpoorte R (2011) Chalcone synthase and its functions in plant resistance. Phytochem Rev 10:397–412. https://doi.org/10.1007/s11101-011-9211-7
De Cremer K, Mathys J, Vos C et al (2013) RNAseq-based transcriptome analysis of Lactuca sativa infected by the fungal necrotroph Botrytis cinerea. Plant, Cell Environ 36:1992–2007. https://doi.org/10.1111/pce.12106
de Torres Zabala M, Littlejohn G, Jayaraman S et al (2015) Chloroplasts play a central role in plant defence and are targeted by pathogen effectors. Nat Plants 1:15074. https://doi.org/10.1038/nplants.2015.74
Delatte TL, Sedijani P, Kondou Y et al (2011) Growth arrest by trehalose-6-phosphate: an astonishing case of primary metabolite control over growth by way of the SnRK1 signaling pathway. Plant Physiol 157:160–174. https://doi.org/10.1104/pp.111.180422
Dhandapani P, Song J, Novak O, Jameson PE (2017) Infection by Rhodococcus fascians maintains cotyledons as a sink tissue for the pathogen. Ann Bot 119(5):841–852. https://doi.org/10.1093/aob/mcw202
Dixon RA, Paiva NL (1995) Stress-induced phenylpropanoid metabolism. Plant cell 7:1085–1097. https://doi.org/10.1105/tpc.7.7.1085
Doehlemann G, Molitor F, Hahn M (2005) Molecular and functional characterization of a fructose specific transporter from the gray mold fungus Botrytis cinerea. Fungal Genet Biol 42:601–610. https://doi.org/10.1016/j.fgb.2005.03.001
Doehlemann G, Wahl R, Horst RJ et al (2008) Reprogramming a maize plant: transcriptional and metabolic changes induced by the fungal biotroph Ustilago maydis. Plant J 56:181–195. https://doi.org/10.1111/j.1365-313X.2008.03590.x
Duan G, Christian N, Schwachtje J et al (2013) The metabolic interplay between plants and phytopathogens. Metabolites 3:1–23. https://doi.org/10.3390/metabo3010001
Duran-Flores D, Heil M (2016) Sources of specificity in plant damaged-self recognition. Curr Opin Plant Biol 32:77–87
Engelsdorf T, Horst RJ, Pröls R et al (2013) Reduced carbohydrate availability enhances the susceptibility of Arabidopsis toward Colletotrichum higginsianum. Plant Physiol 162:225–238. https://doi.org/10.1104/pp.112.209676
Essmann J, Schmitz-Thom I, Schon H et al (2008) RNA interference-mediated repression of cell wall invertase impairs defense in source leaves of tobacco. Plant Physiol 147(3):1288–1299. https://doi.org/10.1104/pp.108.121418
Fagard M, Launay A, Clément G et al (2014) Nitrogen metabolism meets phytopathology. J Exp Bot 65:5643–5656. https://doi.org/10.1093/jxb/eru323
Fatima U, Senthil-Kumar M (2015) Plant and pathogen nutrient acquisition strategies. Front Plant Sci 6:750. https://doi.org/10.3389/fpls.2015.00750
Fernandez D, Tisserant E, Talhinhas P et al (2012) 454-pyrosequencing of Coffea arabica leaves infected by the rust fungus Hemileia vastatrix reveals in planta-expressed pathogen-secreted proteins and plant functions in a late compatible plant–rust interaction. Mol Plant Pathol 13:17–37. https://doi.org/10.1111/j.1364-3703.2011.00723.x
Ferrari S, Galletti R, Denoux C et al (2007) Resistance to Botrytis cinerea induced in Arabidopsis by elicitors is independent of salicylic acid, ethylene, or jasmonate signaling but requires PHYTOALEXIN DEFICIENT3. Plant Physiol 144:367–379. https://doi.org/10.1104/pp.107.095596
Fofana B, Banks TW, McCallum B et al (2007) Temporal gene expression profiling of the wheat leaf rust pathosystem using cDNA microarray reveals differences in compatible and incompatible defence pathways. Int J Plant Genom 2007:17542. https://doi.org/10.1155/2007/17542
Foster AJ, Jenkinson JM, Talbot NJ (2003) Trehalose synthesis and metabolism are required at different stages of plant infection by Magnaporthe grisea. EMBO J 22:225–235. https://doi.org/10.1093/emboj/cdg018
Fotopoulos V, Gilbert MJ, Pittman JK et al (2003) The monosaccharide transporter gene, AtSTP4, and the cell-wall invertase, Atbetafruct1, are induced in Arabidopsis during infection with the fungal biotroph Erysiphe cichoracearum. Plant Physiol 132:821–829. https://doi.org/10.1104/pp.103.021428
Fu Y, Zhang H, Mandal SN et al (2016) Quantitative proteomics reveals the central changes of wheat in response to powdery mildew. J Proteom 130:108–119. https://doi.org/10.1016/j.jprot.2015.09.006
Ghosh S, Kanwar P, Jha G (2017) Alterations in rice chloroplast integrity, photosynthesis and metabolome associated with pathogenesis of Rhizoctonia solani. Sci Rep 7:41610. https://doi.org/10.1038/srep41610
Grigston JC, Osuna D, Scheible W-R et al (2008) D-Glucose sensing by a plasma membrane regulator of G signaling protein, AtRGS1. FEBS Lett 582:3577–3584. https://doi.org/10.1016/j.febslet.2008.08.038
Gyetvai G, Sønderkær M, Göbel U et al (2012) The transcriptome of compatible and incompatible interactions of potato (Solanum tuberosum) with Phytophthora infestans revealed by DeepSAGE analysis. PLoS One 7:e31526. https://doi.org/10.1371/journal.pone.0031526
Halitschke R, Hamilton JG, Kessler A (2011) Herbivore-specific elicitation of photosynthesis by mirid bug salivary secretions in the wild tobacco Nicotiana attenuata. New Phytol 191:528–535. https://doi.org/10.1111/j.1469-8137.2011.03701.x
Hayes MA, Feechan A, Dry IB (2010) Involvement of abscisic acid in the coordinated regulation of a stress-inducible hexose transporter (VvHT5) and a cell wall invertase in grapevine in response to biotrophic fungal infection. Plant Physiol 153:211–221. https://doi.org/10.1104/pp.110.154765
Heil M, Ibarra-Laclette E, Adame-Álvarez RM et al (2012) How plants sense wounds: damaged-self recognition is based on plant-derived elicitors and induces octadecanoid signaling. PLoS One 7:e30537. https://doi.org/10.1371/journal.pone.0030537
Heuberger AL, Robison FM, Lyons SMA et al (2014) Evaluating plant immunity using mass spectrometry-based metabolomics workflows. Front Plant Sci 5:291. https://doi.org/10.3389/fpls.2014.00291
Hong Y-S, Martinez A, Liger-Belair G et al (2012) Metabolomics reveals simultaneous influences of plant defence system and fungal growth in Botrytis cinerea-infected Vitis vinifera cv. Chardonnay berries. J Exp Bot 63:5773–5785. https://doi.org/10.1093/jxb/ers228
Horst RJ, Engelsdorf T, Sonnewald U, Voll LM (2008) Infection of maize leaves with Ustilago maydis prevents establishment of C4 photosynthesis. J Plant Physiol 165:19–28. https://doi.org/10.1016/j.jplph.2007.05.008
Hren M, Ravnikar M, Brzin J et al (2009) Induced expression of sucrose synthase and alcohol dehydrogenase I genes in phytoplasma-infected grapevine plants grown in the field. Plant Pathol 58:170–180. https://doi.org/10.1111/j.1365-3059.2008.01904.x
Hu Y, Zhang J, Jia H et al (2014) Lateral organ boundaries 1 is a disease susceptibility gene for citrus bacterial canker disease. Proc Natl Acad Sci USA 111:E521–E529. https://doi.org/10.1073/pnas.1313271111
Hui D, Iqbal J, Lehmann K et al (2003) Molecular interactions between the specialist herbivore Manduca sexta (lepidoptera, sphingidae) and its natural host Nicotiana attenuata: V. microarray analysis and further characterization of large-scale changes in herbivore-induced mRNAs. Plant Physiol 131:1877–1893. https://doi.org/10.1104/pp.102.018176
Hulsmans S, Rodriguez M, De Coninck B, Rolland F (2016) The SnRK1 energy sensor in plant biotic interactions. Trends Plant Sci 21:648–661. https://doi.org/10.1016/j.tplants.2016.04.008
Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329. https://doi.org/10.1038/nature05286
Karve A, Xia X, Moore BD (2012) Arabidopsis Hexokinase-Like1 and Hexokinase1 form a critical node in mediating plant glucose and ethylene responses. Plant Physiol 158:1965–1975. https://doi.org/10.1104/pp.112.195636
Kawahara Y, Oono Y, Kanamori H et al (2012) Simultaneous RNA-seq analysis of a mixed transcriptome of rice and blast fungus interaction. PLoS One 7:e49423. https://doi.org/10.1371/journal.pone.0049423
Kim DS, Hwang BK (2014) An important role of the pepper phenylalanine ammonia-lyase gene (PAL1) in salicylic acid-dependent signalling of the defence response to microbial pathogens. J Exp Bot 65:2295–2306. https://doi.org/10.1093/jxb/eru109
Kocal N, Sonnewald U, Sonnewald S (2008) Cell wall-bound invertase limits sucrose export and is involved in symptom development and inhibition of photosynthesis during compatible interaction between tomato and Xanthomonas campestris pv vesicatoria. Plant Physiol 148:1523–1536. https://doi.org/10.1104/pp.108.127977
Kolbe A, Tiessen A, Schluepmann H et al (2005) Trehalose 6-phosphate regulates starch synthesis via posttranslational redox activation of ADP-glucose pyrophosphorylase. Proc Natl Acad Sci USA 102:11118–11123. https://doi.org/10.1073/pnas.0503410102
Kretschmer M, Croll D, Kronstad JW (2017) Maize susceptibility to Ustilago maydis is influenced by genetic and chemical perturbation of carbohydrate allocation. Mol Plant Pathol 18:1222–1237. https://doi.org/10.1111/mpp.12486
Kumar Y, Zhang L, Panigrahi P et al (2016) Fusarium oxysporum mediates systems metabolic reprogramming of chickpea roots as revealed by a combination of proteomics and metabolomics. Plant Biotechnol J 14:1589–1603. https://doi.org/10.1111/pbi.12522
Lalonde S, Boles E, Hellmann H et al (1999) The dual function of sugar carriers. Transport and sugar sensing. Plant Cell 11:707–726. https://doi.org/10.1105/tpc.11.4.707
Lanubile A, Muppirala UK, Severin AJ et al (2015) Transcriptome profiling of soybean (Glycine max) roots challenged with pathogenic and non-pathogenic isolates of Fusarium oxysporum. BMC Genom 16:1089. https://doi.org/10.1186/s12864-015-2318-2
Lecompte F, Abro MA, Nicot PC (2013) Can plant sugars mediate the effect of nitrogen fertilization on lettuce susceptibility to two necrotrophic pathogens: Botrytis cinerea and Sclerotinia sclerotiorum? Plant Soil 369:387–401. https://doi.org/10.1007/s11104-012-1577-9
Lecompte F, Nicot PC, Ripoll J et al (2017) Reduced susceptibility of tomato stem to the necrotrophic fungus Botrytis cinerea is associated with a specific adjustment of fructose content in the host sugar pool. Ann Bot 119:931–943. https://doi.org/10.1093/aob/mcw240
Lemonnier P, Gaillard C, Veillet F et al (2014) Expression of Arabidopsis sugar transport protein STP13 differentially affects glucose transport activity and basal resistance to Botrytis cinerea. Plant Mol Biol 85:473–484. https://doi.org/10.1007/s11103-014-0198-5
León P, Sheen J (2003) Sugar and hormone connections. Trends Plant Sci 8:110–116. https://doi.org/10.1016/S1360-1385(03)00011-6
Li J, Yang X, Liu X et al (2016) Proteomic analysis of the compatible interaction of wheat and powdery mildew (Blumeria graminis f. sp. tritici). Plant Physiol Biochem 111:234–243. https://doi.org/10.1016/j.plaphy.2016.12.006
Li Y, Wang Y, Zhang H et al (2017) The plasma membrane-localized sucrose transporter IbSWEET10 contributes to the resistance of sweet potato to Fusarium oxysporum. Front Plant Sci 8:197. https://doi.org/10.3389/fpls.2017.00197
Lingner U, Münch S, Deising HB, Sauer N (2011) Hexose transporters of a hemibiotrophic plant pathogen: functional variations and regulatory differences at different stages of infection. J Biol Chem 286:20913–20922. https://doi.org/10.1074/jbc.M110.213678
Liu Q, Yuan M, Zhou Y et al (2011) A paralog of the MtN3/saliva family recessively confers race-specific resistance to Xanthomonas oryzae in rice. Plant Cell Environ 34:1958–1969. https://doi.org/10.1111/j.1365-3040.2011.02391.x
Lopes DB, Berger RD (2001) The effects of rust and anthracnose on the photosynthetic competence of diseased bean leaves. Phytopathology 91:212–220. https://doi.org/10.1094/PHYTO.2001.91.2.212
Lowe RGT, Cassin A, Grandaubert J et al (2014) Genomes and transcriptomes of partners in plant-fungal-interactions between canola (Brassica napus) and two Leptosphaeria species. PLoS One 9:e103098. https://doi.org/10.1371/journal.pone.0103098
Martin K, Singh J, Hill JH et al (2016) Dynamic transcriptome profiling of Bean Common Mosaic Virus (BCMV) infection in common bean (Phaseolus vulgaris L.). BMC Genom 17:613. https://doi.org/10.1186/s12864-016-2976-8
Meyer S, Saccardy-Adji K, Rizza F, Genty B (2001) Inhibition of photosynthesis by Colletotrichum lindemuthianum in bean leaves determined by chlorophyll fluorescence imaging. Plant Cell Environ 24:947–956. https://doi.org/10.1046/j.0016-8025.2001.00737.x
Moore B, Zhou L, Rolland F et al (2003) Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science 300:332–336. https://doi.org/10.1126/science.1080585
Moore JW, Herrera-Foessel S, Lan C et al (2015) A recently evolved hexose transporter variant confers resistance to multiple pathogens in wheat. Nat Genet 47:1494–1498. https://doi.org/10.1038/ng.3439
Morkunas I, Ratajczak L (2014) The role of sugar signaling in plant defense responses against fungal pathogens. Acta Physiol Plant 36:1607–1619. https://doi.org/10.1007/s11738-014-1559-z
Morkunas I, Marczak Ł, Stachowiak J, Stobiecki M (2005) Sucrose-induced lupine defense against Fusarium oxysporum. Sucrose-stimulated accumulation of isoflavonoids as a defense response of lupine to Fusarium oxysporum. Plant Physiol Biochem 43:363–373. https://doi.org/10.1016/j.plaphy.2005.02.011
Nimchuk Z, Eulgem T, Holt BF, Dangl JL (2003) Recognition and response in the plant immune system. Annu Rev Genet 37:579–609. https://doi.org/10.1146/annurev.genet.37.110801.142628
Nunes C, O’Hara LE, Primavesi LF et al (2013) The trehalose 6-phosphate/SnRK1 signaling pathway primes growth recovery following relief of sink limitation. Plant Physiol 162:1720–1732. https://doi.org/10.1104/pp.113.220657
O’Hara LE, Paul MJ, Wingler A (2013) How do sugars regulate plant growth and development? New insight into the role of trehalose-6-phosphate. Mol Plant 6:261–274. https://doi.org/10.1093/mp/sss120
Oliva R, Quibod IL (2017) Immunity and starvation: new opportunities to elevate disease resistance in crops. Curr Opin Plant Biol 38:84–91. https://doi.org/10.1016/j.pbi.2017.04.020
Parker D, Beckmann M, Zubair H et al (2009) Metabolomic analysis reveals a common pattern of metabolic re-programming during invasion of three host plant species by Magnaporthe grisea. Plant J 59:723–737. https://doi.org/10.1111/j.1365-313X.2009.03912.x
Paul MJ, Primavesi LF, Jhurreea D, Zhang Y (2008) Trehalose metabolism and signaling. Annu Rev Plant Biol 59:417–441. https://doi.org/10.1146/annurev.arplant.59.032607.092945
Pereira MF, de Araújo Dos Santos CM, de Araújo EF et al (2013) Beginning to understand the role of sugar carriers in Colletotrichum lindemuthianum: the function of the gene mfs1. J Microbiol 51:70–81. https://doi.org/10.1007/s12275-013-2393-5
Pérez-Bueno ML, Pineda M, Díaz-Casado E, Barón M (2015) Spatial and temporal dynamics of primary and secondary metabolism in Phaseolus vulgaris challenged by Pseudomonas syringae. Physiol Plant 153:161–174. https://doi.org/10.1111/ppl.12237
Petit A-N, Vaillant N, Boulay M et al (2006) Alteration of photosynthesis in grapevines affected by esca. Phytopathology 96:1060–1066. https://doi.org/10.1094/PHYTO-96-1060
Piasecka A, Jedrzejczak-Rey N, Bednarek P (2015) Secondary metabolites in plant innate immunity: conserved function of divergent chemicals. New Phytol 206:948–964
Piazza A, Zimaro T, Garavaglia BS et al (2015) The dual nature of trehalose in citrus canker disease: a virulence factor for Xanthomonas citri subsp. citri and a trigger for plant defence responses. J Exp Bot 66:2795–2811. https://doi.org/10.1093/jxb/erv095
Pieterse CMJ, Van der Does D, Zamioudis C et al (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28:489–521. https://doi.org/10.1146/annurev-cellbio-092910-154055
Prezelj N, Covington E, Roitsch T et al (2016) Metabolic consequences of infection of grapevine (Vitis vinifera L.) cv. “Modra frankinja” with Flavescence Dorée phytoplasma. Front Plant Sci 7:711. https://doi.org/10.3389/fpls.2016.00711
Proels RK, Hückelhoven R (2014) Cell-wall invertases, key enzymes in the modulation of plant metabolism during defence responses. Mol Plant Pathol 15:858–864. https://doi.org/10.1111/mpp.12139
Pusztahelyi T, Holb IJ, Pócsi I (2015) Secondary metabolites in fungus–plant interactions. Front Plant Sci 6:573. https://doi.org/10.3389/fpls.2015.00573
Rojas CM, Senthil-Kumar M, Tzin V, Mysore KS (2014) Regulation of primary plant metabolism during plant–pathogen interactions and its contribution to plant defense. Front Plant Sci 5:17. https://doi.org/10.3389/fpls.2014.00017
Rolfe SA, Scholes JD (2010) Chlorophyll fluorescence imaging of plant–pathogen interactions. Protoplasma 247:163–175. https://doi.org/10.1007/s00709-010-0203-z
Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709. https://doi.org/10.1146/annurev.arplant.57.032905.105441
Rook F, Weisbeek P, Smeekens S (1998) The light-regulated Arabidopsis bZIP transcription factor gene ATB2 encodes a protein with an unusually long leucine zipper domain. Plant Mol Biol 37:171–178. https://doi.org/10.1023/A:1005964327725
Rudd JJ, Kanyuka K, Hassani-Pak K et al (2015) Transcriptome and metabolite profiling of the infection cycle of Zymoseptoria tritici on wheat reveals a biphasic interaction with plant immunity involving differential pathogen chromosomal contributions and a variation on the hemibiotrophic lifestyle def. Plant Physiol 167:1158–1185. https://doi.org/10.1104/pp.114.255927
Scholes J, Rolfe S (1996) Photosynthesis in localised regions of oat leaves infected with crown rust (Puccinia coronata): quantitative imaging of chlorophyll fluorescence. Planta 199:573–582. https://doi.org/10.1007/BF00195189
Scholes J, Rolfe SA (2009) Chlorophyll fluorescence imaging as tool for understanding the impact of fungal diseases on plant performance: a phenomics perspective. Funct Plant Biol 36:880–892. https://doi.org/10.1071/FP09145
Schuler D, Wahl R, Wippel K et al (2015) Hxt1, a monosaccharide transporter and sensor required for virulence of the maize pathogen Ustilago maydis. New Phytol 206:1086–1100. https://doi.org/10.1111/nph.13314
Sheen J (1990) Metabolic repression of transcription in higher plants. Plant Cell 2:1027–1038. https://doi.org/10.1105/tpc.2.10.1027
Sheen J (2014) Master regulators in plant glucose signaling networks. J Plant Biol 57:67–79. https://doi.org/10.1007/s12374-014-0902-7
Shukla N, Yadav R, Kaur P et al (2017) Transcriptome analysis of root-knot nematode (Meloidogyne incognita)-infected tomato (Solanum lycopersicum) roots reveals complex gene expression profiles and metabolic networks of both host and nematode during susceptible and resistance responses. Mol Plant Pathol 19:615–633. https://doi.org/10.1111/mpp.12547
Siemens J, González M-C, Wolf S et al (2011) Extracellular invertase is involved in the regulation of clubroot disease in Arabidopsis thaliana. Mol Plant Pathol 12:247–262. https://doi.org/10.1111/j.1364-3703.2010.00667.x
Smith JE, Mengesha B, Tang H et al (2014) Resistance to Botrytis cinerea in Solanum lycopersicoides involves widespread transcriptional reprogramming. BMC Genom 15:334. https://doi.org/10.1186/1471-2164-15-334
Solfanelli C, Poggi A, Loreti E et al (2006) Sucrose-specific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant Physiol 140:637–646. https://doi.org/10.1104/pp.105.072579
Stare T, Ramsak Z, Blejec A et al (2015) Bimodal dynamics of primary metabolism-related responses in tolerant potato–potato virus Y interaction. BMC Genom 16:716. https://doi.org/10.1186/s12864-015-1925-2
Streubel J, Pesce C, Hutin M et al (2013) Five phylogenetically close rice SWEET genes confer TAL effector-mediated susceptibility to Xanthomonas oryzae pv. oryzae. New Phytol 200:808–819. https://doi.org/10.1111/nph.12411
Sun L, Yang D, Kong Y et al (2014) Sugar homeostasis mediated by cell wall invertase GRAIN INCOMPLETE FILLING 1 (GIF1) plays a role in pre-existing and induced defence in rice. Mol Plant Pathol 15:161–173. https://doi.org/10.1111/mpp.12078
Sutton PN, Gilbert MJ, Williams LE, Hall JL (2007) Powdery mildew infection of wheat leaves changes host solute transport and invertase activity. Physiol Plant 129:787–795. https://doi.org/10.1111/j.1399-3054.2007.00863.x
Swarbrick PJ, Schulze-Lefert P, Scholes JD (2006) Metabolic consequences of susceptibility and resistance (race-specific and broad-spectrum) in barley leaves challenged with powdery mildew. Plant Cell Environ 29:1061–1076
Tang JY, Zielinski RE, Zangerl AR et al (2006) The differential effects of herbivory by first and fourth instars of Trichoplusia ni (Lepidoptera: Noctuidae) on photosynthesis in Arabidopsis thaliana. J Exp Bot 57:527–536. https://doi.org/10.1093/jxb/erj032
Tao Y, Xie Z, Chen W et al (2003) Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15:317–330
Tauzin AS, Giardina T (2014) Sucrose and invertases, a part of the plant defense response to the biotic stresses. Front Plant Sci 5:293. https://doi.org/10.3389/fpls.2014.00293
Teixeira PJPL, de Thomazella DP, Reis O et al (2014) High-resolution transcript profiling of the atypical biotrophic interaction between Theobroma cacao and the fungal pathogen Moniliophthora perniciosa. Plant Cell 26:4245–4269. https://doi.org/10.1105/tpc.114.130807
Tonnessen BW, Manosalva P, Lang JM et al (2014) Rice phenylalanine ammonia-lyase gene OsPAL4 is associated with broad spectrum disease resistance. Plant Mol Biol 87:273–286. https://doi.org/10.1007/s11103-014-0275-9
Urano D, Chen J-G, Botella JR, Jones AM (2013) Heterotrimeric G protein signalling in the plant kingdom. Open Biol 3:120186. https://doi.org/10.1098/rsob.120186
VanEtten HD, Mansfield JW, Bailey JA, Farmer EE (1994) Two classes of plant antibiotics: phytoalexins versus “phytoanticipins”. Plant Cell 6:1191–1192. https://doi.org/10.1105/tpc.6.9.1191
Vargas WA, Martín JMS, Rech GE et al (2012) Plant defense mechanisms are activated during biotrophic and necrotrophic development of Colletotrichum graminicola in maize. Plant Physiol 158:1342–1358. https://doi.org/10.1104/pp.111.190397
Versluys M, Tarkowski ŁP, Van den Ende W (2017) Fructans as DAMPs or MAMPs: evolutionary prospects, cross-tolerance, and multistress resistance potential. Front Plant Sci 7:2061. https://doi.org/10.3389/fpls.2016.02061
Voegele RT, Struck C, Hahn M, Mendgen K (2001) The role of haustoria in sugar supply during infection of broad bean by the rust fungus Uromyces fabae. Proc Natl Acad Sci USA 98:8133–8138. https://doi.org/10.1073/pnas.131186798
Voegele RT, Wirsel S, Möll U et al (2006) Cloning and characterization of a novel invertase from the obligate biotroph Uromyces fabae and analysis of expression patterns of host and pathogen invertases in the course of infection. Mol Plant Microbe Interact 19:625–634. https://doi.org/10.1094/MPMI-19-0625
Voll LM, Horst RJ, Voitsik A-M et al (2011) Common motifs in the response of cereal primary metabolism to fungal pathogens are not based on similar transcriptional reprogramming. Front Plant Sci 2:39. https://doi.org/10.3389/fpls.2011.00039
Wahl R, Wippel K, Goos S et al (2010) A novel high-affinity sucrose transporter is required for virulence of the plant pathogen Ustilago maydis. PLoS Biol 8:e1000303. https://doi.org/10.1371/journal.pbio.1000303
Wang X, Liu W, Chen X et al (2010) Differential gene expression in incompatible interaction between wheat and stripe rust fungus revealed by cDNA-AFLP and comparison to compatible interaction. BMC Plant Biol 10:9. https://doi.org/10.1186/1471-2229-10-9
Wiese A, Elzinga N, Wobbes B, Smeekens S (2004) A conserved upstream open reading frame mediates sucrose-induced repression of translation. Plant Cell 16:1717–1729. https://doi.org/10.1105/tpc.019349
Wiese A, Elzinga N, Wobbes B, Smeekens S (2005) Sucrose-induced translational repression of plant bZIP-type transcription factors. Biochem Soc Trans 33:272–275. https://doi.org/10.1042/BST0330272
Wilson RA, Jenkinson JM, Gibson RP et al (2007) Tps1 regulates the pentose phosphate pathway, nitrogen metabolism and fungal virulence. EMBO J 26:3673–3685. https://doi.org/10.1038/sj.emboj.7601795
Wind J, Smeekens S, Hanson J (2010) Sucrose: metabolite and signaling molecule. Phytochemistry 71:1610–1614. https://doi.org/10.1016/j.phytochem.2010.07.007
Windram O, Madhou P, McHattie S et al (2012) Arabidopsis defense against Botrytis cinerea: chronology and regulation deciphered by high-resolution temporal transcriptomic analysis. Plant Cell 24:3530–3557. https://doi.org/10.1105/tpc.112.102046
Witzel K, Buhtz A, Grosch R (2017) Temporal impact of the vascular wilt pathogen Verticillium dahliae on tomato root proteome. J. Proteom 169:215–224. https://doi.org/10.1016/j.jprot.2017.04.008
Wojakowska A, Muth D, Narożna D et al (2013) Changes of phenolic secondary metabolite profiles in the reaction of narrow leaf lupin (Lupinus angustifolius) plants to infections with Colletotrichum lupini fungus or treatment with its toxin. Metabolomics 9:575–589. https://doi.org/10.1007/s11306-012-0475-8
Xiao W, Sheen J, Jang JC (2000) The role of hexokinase in plant sugar signal transduction and growth and development. Plant Mol Biol 44:451–461
Xu X-H, Wang C, Li S-X et al (2015) Friend or foe: differential responses of rice to invasion by mutualistic or pathogenic fungi revealed by RNAseq and metabolite profiling. Sci Rep 5:13624. https://doi.org/10.1038/srep13624
Yanagisawa S, Yoo S-D, Sheen J (2003) Differential regulation of EIN3 stability by glucose and ethylene signalling in plants. Nature 425:521–525. https://doi.org/10.1038/nature01984
Yang B, Sugio A, White FF (2006) Os8N3 is a host disease-susceptibility gene for bacterial blight of rice. Proc Natl Acad Sci USA 103:10503–10508. https://doi.org/10.1073/pnas.0604088103
Yang F, Melo-Braga MN, Larsen MR et al (2013) Battle through signaling between wheat and the fungal pathogen Septoria tritici revealed by proteomics and phosphoproteomics. Mol Cell Proteom 12:2497–2508. https://doi.org/10.1074/mcp.M113.027532
Yu Y, Streubel J, Balzergue S et al (2011) Colonization of rice leaf blades by an African strain of Xanthomonas oryzae pv. oryzae depends on a new TAL effector that induces the rice nodulin-3 Os11N3 gene. Mol Plant Microbe Interact 24:1102–1113. https://doi.org/10.1094/MPMI-11-10-0254
Yuan M, Chu Z, Li X et al (2009) Pathogen-induced expressional loss of function is the key factor in race-specific bacterial resistance conferred by a recessive R gene xa13 in rice. Plant Cell Physiol 50:947–955. https://doi.org/10.1093/pcp/pcp046
Zangerl AR, Hamilton JG, Miller TJ et al (2002) Impact of folivory on photosynthesis is greater than the sum of its holes. Proc Natl Acad Sci USA 99:1088–1091. https://doi.org/10.1073/pnas.022647099
Zhao D, You Y, Fan H et al (2018) The role of sugar transporter genes during early infection by root-knot nematodes. Int J Mol Sci 19:302. https://doi.org/10.3390/ijms19010302
Zhou J, Peng Z, Long J et al (2015) Gene targeting by the TAL effector PthXo2 reveals cryptic resistance gene for bacterial blight of rice. Plant J Cell Mol Biol 82:632–643. https://doi.org/10.1111/tpj.12838
Zhu Z, An F, Feng Y et al (2011) Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis. Proc Natl Acad Sci USA 108:12539–12544. https://doi.org/10.1073/pnas.1103959108
Zimmerli L, Stein M, Lipka V et al (2004) Host and non-host pathogens elicit different jasmonate/ethylene responses in Arabidopsis. Plant J Cell Mol Biol 40:633–646. https://doi.org/10.1111/j.1365-313X.2004.02236.x
Zou J, Rodriguez-Zas S, Aldea M et al (2005) Expression profiling soybean response to Pseudomonas syringae reveals new defense-related genes and rapid HR-specific downregulation of photosynthesis. Mol Plant Microbe Interact 18:1161–1174. https://doi.org/10.1094/MPMI-18-1161
Acknowledgements
P.K. acknowledges the post-doctoral research fellowship from Department of Biotechnology (DBT, Govt. of India). The research in GJ lab is supported by research funding from DBT, Govt. of India and core research grant of National Institute of Plant Genome Research (NIPGR), New Delhi.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kanwar, P., Jha, G. Alterations in plant sugar metabolism: signatory of pathogen attack. Planta 249, 305–318 (2019). https://doi.org/10.1007/s00425-018-3018-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-018-3018-3
Keywords
- Source
- Sink
- Signaling
- Photosynthesis
- Enzymes
- Transporters