, Volume 249, Issue 2, pp 305–318 | Cite as

Alterations in plant sugar metabolism: signatory of pathogen attack

  • Poonam Kanwar
  • Gopaljee JhaEmail author


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.


Source Sink Signaling Photosynthesis Enzymes Transporters 



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.

Supplementary material

425_2018_3018_MOESM1_ESM.docx (22 kb)
Supplementary material 1 (DOCX 22 kb)


  1. 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. Google Scholar
  2. 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. Google Scholar
  3. 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. Google Scholar
  4. Aliferis KA, Faubert D, Jabaji S (2014) A metabolic profiling strategy for the dissection of plant defense against fungal pathogens. PLoS One 9:e111930. Google Scholar
  5. Allwood JW, Clarke A, Goodacre R, Mur LAJ (2010) Dual metabolomics: a novel approach to understanding plant–pathogen interactions. Phytochemistry 71:590–597. Google Scholar
  6. 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. Google Scholar
  7. 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. Google Scholar
  8. 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. Google Scholar
  9. 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. Google Scholar
  10. 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. Google Scholar
  11. Berger S, Sinha AK, Roitsch T (2007b) Plant physiology meets phytopathology: plant primary metabolism and plant pathogen interactions. J Exp Bot 58:4019–4026. Google Scholar
  12. Bezrutczyk M, Yang J, Eom JS et al (2018) Sugar flux and signaling in plant–microbe interactions. Plant J 93(4):675–685. Google Scholar
  13. Bolouri Moghaddam MR, Van den Ende W (2012) Sugars and plant innate immunity. J Exp Bot 63:3989–3998. Google Scholar
  14. Bolouri Moghaddam MR, Van Den Ende W (2013) Sweet immunity in the plant circadian regulatory network. J Exp Bot 64:1439–1449Google Scholar
  15. Bolton MD (2009) Primary metabolism and plant defense—fuel for the fire. Mol Plant Microbe Interact 22:487–497. Google Scholar
  16. 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. Google Scholar
  17. 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. Google Scholar
  18. 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. Google Scholar
  19. 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. Google Scholar
  20. 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. Google Scholar
  21. 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. Google Scholar
  22. Ceusters J, Van de Poel B (2018) Update: ethylene exerts species-specific and age-dependent control of photosynthesis. Plant Physiol 176(4):2601–2612. Google Scholar
  23. 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. Google Scholar
  24. 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. Google Scholar
  25. 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. Google Scholar
  26. Chen J-G, Jones AM (2004) AtRGS1 function in Arabidopsis thaliana. Methods Enzymol 389:338–350. Google Scholar
  27. Chen L-Q, Hou B-H, Lalonde S et al (2010) Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468:527–532. Google Scholar
  28. 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. Google Scholar
  29. Cho Y-H, Yoo S-D, Sheen J (2006) Regulatory functions of nuclear hexokinase1 complex in glucose signaling. Cell 127:579–589. Google Scholar
  30. 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. Google Scholar
  31. 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. Google Scholar
  32. 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. Google Scholar
  33. 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. Google Scholar
  34. 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. Google Scholar
  35. Dao TTH, Linthorst HJM, Verpoorte R (2011) Chalcone synthase and its functions in plant resistance. Phytochem Rev 10:397–412. Google Scholar
  36. 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. Google Scholar
  37. 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. Google Scholar
  38. 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. Google Scholar
  39. 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. Google Scholar
  40. Dixon RA, Paiva NL (1995) Stress-induced phenylpropanoid metabolism. Plant cell 7:1085–1097. Google Scholar
  41. 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. Google Scholar
  42. 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. Google Scholar
  43. Duan G, Christian N, Schwachtje J et al (2013) The metabolic interplay between plants and phytopathogens. Metabolites 3:1–23. Google Scholar
  44. Duran-Flores D, Heil M (2016) Sources of specificity in plant damaged-self recognition. Curr Opin Plant Biol 32:77–87Google Scholar
  45. 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. Google Scholar
  46. 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. Google Scholar
  47. Fagard M, Launay A, Clément G et al (2014) Nitrogen metabolism meets phytopathology. J Exp Bot 65:5643–5656. Google Scholar
  48. Fatima U, Senthil-Kumar M (2015) Plant and pathogen nutrient acquisition strategies. Front Plant Sci 6:750. Google Scholar
  49. 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. Google Scholar
  50. 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. Google Scholar
  51. 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. Google Scholar
  52. 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. Google Scholar
  53. 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. Google Scholar
  54. 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. Google Scholar
  55. 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. Google Scholar
  56. 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. Google Scholar
  57. 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. Google Scholar
  58. 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. Google Scholar
  59. 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. Google Scholar
  60. 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. Google Scholar
  61. Heuberger AL, Robison FM, Lyons SMA et al (2014) Evaluating plant immunity using mass spectrometry-based metabolomics workflows. Front Plant Sci 5:291. Google Scholar
  62. 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. Google Scholar
  63. 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. Google Scholar
  64. 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. Google Scholar
  65. 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. Google Scholar
  66. 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. Google Scholar
  67. Hulsmans S, Rodriguez M, De Coninck B, Rolland F (2016) The SnRK1 energy sensor in plant biotic interactions. Trends Plant Sci 21:648–661. Google Scholar
  68. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329. Google Scholar
  69. 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. Google Scholar
  70. 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. Google Scholar
  71. 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. Google Scholar
  72. 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. Google Scholar
  73. 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. Google Scholar
  74. 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. Google Scholar
  75. 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. Google Scholar
  76. Lalonde S, Boles E, Hellmann H et al (1999) The dual function of sugar carriers. Transport and sugar sensing. Plant Cell 11:707–726. Google Scholar
  77. 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. Google Scholar
  78. 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. Google Scholar
  79. 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. Google Scholar
  80. 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. Google Scholar
  81. León P, Sheen J (2003) Sugar and hormone connections. Trends Plant Sci 8:110–116. Google Scholar
  82. 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. Google Scholar
  83. 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. Google Scholar
  84. 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. Google Scholar
  85. 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. Google Scholar
  86. Lopes DB, Berger RD (2001) The effects of rust and anthracnose on the photosynthetic competence of diseased bean leaves. Phytopathology 91:212–220. Google Scholar
  87. 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. Google Scholar
  88. 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. Google Scholar
  89. 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. Google Scholar
  90. 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. Google Scholar
  91. 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. Google Scholar
  92. Morkunas I, Ratajczak L (2014) The role of sugar signaling in plant defense responses against fungal pathogens. Acta Physiol Plant 36:1607–1619. Google Scholar
  93. 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. Google Scholar
  94. Nimchuk Z, Eulgem T, Holt BF, Dangl JL (2003) Recognition and response in the plant immune system. Annu Rev Genet 37:579–609. Google Scholar
  95. 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. Google Scholar
  96. 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. Google Scholar
  97. Oliva R, Quibod IL (2017) Immunity and starvation: new opportunities to elevate disease resistance in crops. Curr Opin Plant Biol 38:84–91. Google Scholar
  98. 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. Google Scholar
  99. Paul MJ, Primavesi LF, Jhurreea D, Zhang Y (2008) Trehalose metabolism and signaling. Annu Rev Plant Biol 59:417–441. Google Scholar
  100. 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. Google Scholar
  101. 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. Google Scholar
  102. Petit A-N, Vaillant N, Boulay M et al (2006) Alteration of photosynthesis in grapevines affected by esca. Phytopathology 96:1060–1066. Google Scholar
  103. Piasecka A, Jedrzejczak-Rey N, Bednarek P (2015) Secondary metabolites in plant innate immunity: conserved function of divergent chemicals. New Phytol 206:948–964Google Scholar
  104. 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. Google Scholar
  105. Pieterse CMJ, Van der Does D, Zamioudis C et al (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28:489–521. Google Scholar
  106. 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. Google Scholar
  107. 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. Google Scholar
  108. Pusztahelyi T, Holb IJ, Pócsi I (2015) Secondary metabolites in fungus–plant interactions. Front Plant Sci 6:573. Google Scholar
  109. 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. Google Scholar
  110. Rolfe SA, Scholes JD (2010) Chlorophyll fluorescence imaging of plant–pathogen interactions. Protoplasma 247:163–175. Google Scholar
  111. 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. Google Scholar
  112. 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. Google Scholar
  113. 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. Google Scholar
  114. 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. Google Scholar
  115. 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. Google Scholar
  116. 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. Google Scholar
  117. Sheen J (1990) Metabolic repression of transcription in higher plants. Plant Cell 2:1027–1038. Google Scholar
  118. Sheen J (2014) Master regulators in plant glucose signaling networks. J Plant Biol 57:67–79. Google Scholar
  119. 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. Google Scholar
  120. 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. Google Scholar
  121. Smith JE, Mengesha B, Tang H et al (2014) Resistance to Botrytis cinerea in Solanum lycopersicoides involves widespread transcriptional reprogramming. BMC Genom 15:334. Google Scholar
  122. Solfanelli C, Poggi A, Loreti E et al (2006) Sucrose-specific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant Physiol 140:637–646. Google Scholar
  123. 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. Google Scholar
  124. 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. Google Scholar
  125. 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. Google Scholar
  126. 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. Google Scholar
  127. 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 29:1061–1076Google Scholar
  128. 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. Google Scholar
  129. 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 15:317–330Google Scholar
  130. Tauzin AS, Giardina T (2014) Sucrose and invertases, a part of the plant defense response to the biotic stresses. Front Plant Sci 5:293. Google Scholar
  131. 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. Google Scholar
  132. 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. Google Scholar
  133. Urano D, Chen J-G, Botella JR, Jones AM (2013) Heterotrimeric G protein signalling in the plant kingdom. Open Biol 3:120186. Google Scholar
  134. VanEtten HD, Mansfield JW, Bailey JA, Farmer EE (1994) Two classes of plant antibiotics: phytoalexins versus “phytoanticipins”. Plant Cell 6:1191–1192. Google Scholar
  135. 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. Google Scholar
  136. 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. Google Scholar
  137. 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. Google Scholar
  138. 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. Google Scholar
  139. 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. Google Scholar
  140. 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. Google Scholar
  141. 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. Google Scholar
  142. 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. Google Scholar
  143. 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. Google Scholar
  144. 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. Google Scholar
  145. Wind J, Smeekens S, Hanson J (2010) Sucrose: metabolite and signaling molecule. Phytochemistry 71:1610–1614. Google Scholar
  146. 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. Google Scholar
  147. 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. Google Scholar
  148. 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. Google Scholar
  149. Xiao W, Sheen J, Jang JC (2000) The role of hexokinase in plant sugar signal transduction and growth and development. Plant Mol Biol 44:451–461Google Scholar
  150. 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. Google Scholar
  151. Yanagisawa S, Yoo S-D, Sheen J (2003) Differential regulation of EIN3 stability by glucose and ethylene signalling in plants. Nature 425:521–525. Google Scholar
  152. 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. Google Scholar
  153. 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. Google Scholar
  154. 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. Google Scholar
  155. 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. Google Scholar
  156. 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. Google Scholar
  157. 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. Google Scholar
  158. 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. Google Scholar
  159. 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. Google Scholar
  160. 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. Google Scholar
  161. 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. Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.National Institute of Plant Genome ResearchNew DelhiIndia

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