The role of sugar signaling in plant defense responses against fungal pathogens

• Autorzy: Morkunas I. , Ratajczak L.
• Języki publikacji: EN

Abstrakty

EN

In most fungal pathogen–plant systems, a high level of sugars in plant tissues enhances plant resistance. Several hypotheses have been proposed to explain the mechanisms of ‘‘high-sugar resistance’’. Sugars constitute the primary substrate providing energy and structural material for defense responses in plants, while they may also act as signal molecules interacting with the hormonal signaling network regulating the plant immune system. Sugars enhance oxidative burst at early stages of infection, increasing lignification of cell walls, stimulate the synthesis of flavonoids and induce certain PR proteins. Some sugars act as priming agents inducing higher plant resistance to pathogens.

• Wydawca: -
• Czasopismo: Acta Physiologiae Plantarum
• Rocznik: 2014
• Tom: 36
• Numer: 07
• Opis fizyczny: p.1607-1619,fig.,ref.

Twórcy

autor

Morkunas I.

• Department of Plant Physiology, Faculty of Horticulture and Landscape Architecture, Poznan University of Life Sciences, Wolynska 35, 60-637 Poznan, Poland

autor

Ratajczak L.

• Department of Plant Physiology, Faculty of Biology, Adam Mickiewicz University, Umultowska 89, 61-614 Poznan, Poland

Bibliografia

• Afoufa-Bastien D, Anna Medici A, Jeauffre J, Coutos-Thévenot P, Lemoine R, Atanassova R, Laloi M (2010) The Vitis vinifera sugar transporter gene family: phylogenetic overview and macroarray expression profiling. BMC Plant Biol 10:245
• Ahmad S, Gordon-Weeks R, Pickett J, Ton J (2010) Natural variation in priming of basal resistance: from evolutionary origin to agricultural exploitation. Mol Plant Pathol 11:817–827
• Andersen QM, Markham KR (2006) Flavonoids. Chemistry, biochemistry and applications. CRC Press/Taylor & Francis Group/LLC CRC Press. Boca Raton/London/New York
• Ash GJ, Brown JF (1991) Effect of nitrogen nutrition of the host on the epidemiology of Puccinia striiformis f.sp. tritici and crop yield in wheat. Australas Plant Pathol 20:108–114
• Asselbergh B, De Vleesschauwer D, Hofte M (2008) Global switches and fine-tuning: ABA modulates plant pathogen defense. Mol Plant Microbe Interact 21:709–719
• Baena-Gonzalez E (2010) Energy signaling in the regulation of gene expression during stress. Mol Plant 3:300–313
• Baena-Gonzalez E, Sheen J (2008) Convergent energy and stress signaling. Trends Plant Sci 13:474–482
• Baena-Gonzalez E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448:938–942
• Ballaré CL, Mazza CA, Austin AT, Pierik R (2012) Canopy light and plant health. Plant Physiol 160:145–155
• Bancal MO, Hansart A, Sache I, Bancall P (2012) Modelling fungal sink competitiveness with grains for assimilates in wheat infected by a biotrophic pathogen. Ann Bot 110(1):113–123
• Bednarek P, Osbourn A (2009) Plant–microbe interactions: chemical diversity in plant defense. Science 324:746–748
• Berger S, Papadopoulos M, Schreiber U, Kaiser W, Roitsch T (2004) Complex regulation of gene expression, photosynthesis and sugar levels by pathogen infection in tomato. Physiol Plant 122:419–428
• Berger S, Sinha AK, Roitsch T (2007) Plant physiology meets phytopathology: plant primary metabolism and plant–pathogen interaction. J Exp Bot 58:4019–4026
• Biemelt S, Sonnewald U (2006) Plant–microbe interactions to probe regulation of plant carbon metabolism. J Plant Physiol 163:307–318
• Boddu J, Cho S, Kruger WM, Muehlbauer GJ (2006) Transcriptome analysis of the barley-Fusarium graminearum interaction. Mol Plant Microbe Interact 19:407–417
• Boller T, He SY (2009) Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324:742–744
• Bolouri-Moghaddam MR, Van den Eden W (2012) Sugars and plant innate immunity. J Exp Bot 63(11):3989–3998
• Bolouri-Moghaddam MR, Le Roy K, Xiang L, Rolland F, Van den Ende W (2010) Sugar signalling and antioxidant network connections in plant cells. FEBS J 277:2022–2037
• Bolton MD (2009) Primary metabolism and plant defense-fuel for the fire. Mol Plant Microbe Interact 22:487–497
• Bonfig KB, Schreiber U, Gabler A, Roitsch T, Berger S (2006) Infection with virulent and avirulent P. syringae strains differentially affects photosynthesis and sink metabolism in Arabidopsis leaves. Planta 225:1–12
• Cao FY, Yoshioka K, Desveaux D (2011) The roles of ABA in plant–pathogen interactions. J Plant Res 124:489–499
• Cerrudo I, Keller MM, Cargnel MD, Demkura PV, de Wit M, Patitucci MS, Pierik R, Pieterse CMJ, Ballaré CL (2012) Low red/far-red ratios reduce Arabidopsis resistance to Botrytis cinerea and jasmonate responses via a COI1-JAZ10-dependent, salicylic acid-independent mechanism. Plant Physiol 158:2042–2052
• Chen LQ, Hou BH, Lalonde S, Takanaga H, Hartung ML, Qu XQ, Guo WJ, Kim JG, Underwood W, Chaudhuri B et al (2010) Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468:527–532
• Chinnusamy V, Zhu JK, Sunkar R (2006) Gene regulation during cold acclimation in plants. Methods Mol Biol 639:39–55
• Cho YH, Yoo SD, Sheen J (2006) Regulatory functions of nuclear hexokinase1 complex in glucose signaling. Cell 127:579–589
• Cho J, Ryoo N, Eom J, Lee D, Kim H, Jeong S, Lee Y, Kwon Y, Cho M, Bhoo SH et al (2009) Role of the rice hexokinases OsHXK5 and OsHXK6 as glucose sensors. Plant Physiol 149:745–759
• Cho YH, Hong JW, Kim EC, Yoo SD (2012) Regulatory functions of SnRK1 in stress-responsive gene expression and in plant growth and development. Plant Physiol 158:1955–1964
• Chołuj D, Moliszewska EB (2012) The influence of Aphanomyces cochlioides on selected physiological processes in sugar beet leaves and yield parameters. Eur J Plant Pathol 132:59–70
• Chou H, Bundock N, Rolfe S, Scholes J (2000) Infection of Arabidopsis thaliana leaves with Albugo candida causes a reprogramming of host metabolism. Mol Plant Pathol 1:99–111
• Chujo T, Miyamoto K, Shimogawa T, Shimizu T, Otake Y, Yokotani N, Nishizawa Y, Shibuya N, Nojiri H, Yamane H, Minami E, Okada K (2013) OsWRKY28, a PAMP-responsive transrepressor, negatively regulates innate immune responses in rice against rice blast fungus. Plant Mol Biol 82:23–37
• Conrath U (2011) Molecular aspects of defence priming. Trends Plant Sci 16:524–531
• Danial DL, Parlevliet JE (1995) Effects of nitrogen fertilization on disease severity and infection type of yellow rust on wheat genotypes varying in quantitative resistance. J Phytopathol 143:679–681
• Delatte TL, Sedijani P, Kondou Y, Matsui M, de Jong GJ, Somsen GW, Wiese-Klingenberg A, Primavesi LF, Paul MJ, Schluepmann H (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
• Doehlemann G, Wahl R, Horst RJ, Voll LM, Usadel B, Poree F, Stitt M, Pons-Kühnemann J, Sonnewald U, Kahmann R, Kämper J (2008) Reprogramming a maize plant: transcriptional and metabolic changes induced by the fungal biotroph Ustilago maydis. Plant J 56:181–195
• Doidy J, Grace E, Kühn C, Simon-Plas F, Casieri L, Wipf D (2012) Sugar transporters in plants and in their interactions with fungi. Trends Plant Sci 17:413–422
• Douglas CJ (1996) Phenylpropanoid metabolism and lignin biosynthesis: from weeds to trees. Trends Plant Sci 1:171–178
• Ehlert A, Weltmeier F, Wang X, Mayer CS, Smeekens S, Vicente-Carbajosa J, Droge-Laser W (2006) Two-hybrid protein–protein interaction analysis in Arabidopsis protoplasts: establishment of a heterodimerization map of group C and group S bZIP transcription factors. Plant J 46:890–900
• Ehness R, Ecker M, Godt DE, Roitsch T (1997) Glucose and stress independently regulate source and sink metabolism and defense mechanisms via signal transduction pathways involving protein phosphorylation. Plant Cell 9:1825–1841
• Essmann J, Schmitz-Thom I, Schon H, Sonnewald S, Weis E, Scharte J (2008) RNA interference-mediated repression of cell wall invertase impairs defense in source leaves of tobacco. Plant Physiol 147:1288–1299
• Ferri M, Tassoni A, Franceschetti M, Righetti L, Naldrett MJ, Bagni N (2009) Chitosan treatment induces changes of protein expression profile and stilbene distribution in Vitis vinifera cell suspensions. Proteomics 9:610–624
• Ferri M, Righetti L, Tassoni A (2011) Increasing sucrose concentrations promote phenylpropanoid biosynthesis in grapevine cell cultures. J Plant Physiol 168:189–195
• Floryszak-Wieczorek J, Arasimowicz M, Milczarek G, Jeleń H, Jackowiak H (2007) Only an early nitric oxide burst and the following wave of secondary nitric oxide generation enhanced effective defence responses of pelargonium to a necrotrophic pathogen. New Phytol 175:718–730
• Forlani G (2010) Differential in vitro responses of rice cultivars to Italian lineages of the blast pathogen Pyricularia grisea. 2. Aromatic biosynthesis. J Plant Physiol 167:928–932
• Fotopoulos V, Gilbert MJ, Pittman JK, Marvier AC, Buchanan AJ, Sauer N, Hall JL, Williams LE (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
• Gibertia S, Berteab CM, Narayanab R, Maffeib ME, Forlani G (2012) Two phenylalanine ammonia lyase isoforms are involved in the elicitor-induced response of rice to the fungal pathogen Magnaporthe oryzae. J Plant Physiol 169:249–254
• Gissot L, Polge C, Jossier M, Girin T, Bouly JP, Kreis M, Thomas M (2006) AKINbc contributes to SnRK1 heterotrimeric complexes and interacts with two proteins implicated in plant pathogen resistance through its KIS/GBD sequence. Plant Physiol 142:931–944
• Goellner K, Conrath U (2008) Priming: it’s all the world to induced disease resistance. Eur J Plant Pathol 121:233–242
• Gómez-Ariza J, Campo S, Rufat M, Estopa` M, Messeguer J, San Segundo B, Coca M (2007) Sucrose-mediated priming of plant defense responses and broad-spectrum disease resistance by overexpression of the maize pathogenesis-related PRms protein in rice plants. Mol Plant Microbe Interact 20:832–842
• Gould KS, Lister C (2006) Flavonoid functions in plants. In: Andersen OM, Markham KR, editors. Flavonoids: chemistry, biochemistry and applications. CRC Press/Taylor & Francis Group/LLC CRC Press. Boca Raton/London/New York, pp 397–441
• Grigston JC, Osuna D, Scheible WR, Liu C, Stitt M, Jones AM (2008) D-Glucose sensing by a plasma membrane regulator of G signaling protein, AtRGS1. FEBS Lett 582:3577–3584
• Halford NG, Hey SJ (2009) Snf1-related protein kinases (SnRKs) act within an intricate network that links metabolic and stress signalling in plants. Biochem J 419:247–259
• Hammerschmidt R (1984) Rapid deposition of lignin in potato tuber tissue as a response to fungi non-pathogenic on potato. Physiol Plant Pathol 24:33–42
• Hanson J, Smeekens S (2009) Sugar perception and signaling—an update. Curr Opin Plant Biol 12:562–567
• Hanson J, Hanssen M, Wiese A, Hendriks MM, Smeekens S (2008) The sucrose regulated transcription factor bZIP11 affects amino acid metabolism by regulating the expression of Asparagine Synthetase1 and Proline Dehydrogenase. Plant J 53:935–949
• Hao L, Wang H, Sunter G, Bisaro DM (2003) Geminivirus AL2 and L2 proteins interact with and inactivate SNF1 kinase. Plant Cell 15:1034–1048
• Hayes MA, Davies C, Dry IB (2007) Isolation, functional characterization, and expression analysis of grapevine (Vitis vinifera L.) hexose transporters: differential roles in sink and source tissues. J Exp Bot 58:1985–1997
• 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
• He C, Hsiang T, Wolyn DJ (2001) Activation of defense responses to Fusarium infection in Asparagus densiflorus. Eur J Plant Pathol 107:473–483
• Heisterüber D, Schulte P, Moerschbacher BM (1994) Soluble carbohydrates and invertase activity in stem rust-infected, resistant and susceptible near-isogenic wheat leaves. Physiol Mol Plant Pathol 45:111–123
• Hey SJ, Byrne E, Halford NG (2010) The interface between metabolic and stress signaling. Ann Bot 105:197–203
• Horsfall JG, Diamond AE (1957) Interactions of tissue sugar, growth substances, and disease susceptibility. Z Pflanzenkr Pflanzenschutz 64:415–421
• Howard DD, Chambers AY, Logan J (1994) Nitrogen and fungicide effects on yield components and disease severity in wheat. J Prod Agric 7:448–454
• Huang J, Taylor JP, Chen JG, Uhrig JF, Schnell DJ, Nakagawa T, Korth KL, Jones AM (2006) The plastid protein thylakoid formation1 and the plasma membrane G protein GPA1 interact in a novel sugar-signaling mechanism in Arabidopsis. Plant Cell 18:1226–1238
• Huber DM, Thompson IA (2007) Nitrogen and plant disease. In: Datnoff LE, Elmer WH, Huber DM (eds) Mineral nutrition and plant disease. APS, St Paul, pp 31–44
• Hummel M, Rahmani F, Smeekens S, Hanson J (2009) Sucrose-mediated translational control. Ann Bot 104:1–7
• Jobic C, Boisson AM, Gout E, Rascle C, Fevre M, Cotton P, Bligny R (2007) Metabolic processes and carbon nutrient exchanges between host and pathogen sustain the disease development during sunflower infection by Sclerotinia sclerotiorum. Planta 226:251–265
• Jones JD, Dangle JL (2006) The plant immune system. Nature 444:323–329
• Jones OAH, Maguire ML, Griffin JL, Jung YH, Shibato J, Rakwal R, Agrawal GK, Jwa NS (2011) Using metabolic profiling to assess plant–pathogen interactions: an example using rice (Oryza sativa) and the blast pathogen Magnaporthe grisea. Eur J Plant Pathol 129:539–554
• Kaminaka H, Nake C, Epple P, Dittgen J, Schütze K, Chaban C, Holt BF, Merkle T, Schafer E, Harter K, Dangl J (2006) bZIP10-LSD1 antagonism modulates basal defense and cell death in Arabidopsis following infection. EMBO J 25:4400–4411
• Kang SG, Price J, Lin PC, Hong JC, Jang JC (2010) The Arabidopsis bZIP1 transcription factor is involved in sugar signaling, protein networking, and DNA binding. Mol Plant 3:361–373
• Kangasjärvi S, Neukermans J, Li S, Aro EM, Noctor G (2012) Photosynthesis, photorespiration, and light signalling in defence responses. J Exp Bot 63:1619–1636
• Kawakami A, Yoshida M (2012) Graminan breakdown by fructan exohydrolase induced in winter wheat inoculated with snow mold. Plant Physiol 169:294–302
• Kazan K, Manners JM (2011) The interplay between light and jasmonate signalling during defence and development. J Exp Bot 62:4087–4100
• Kim M, Lim JH, Ahn CS, Park K, Kim GT, Kim WT, Pai HS (2006) Mitochondria-associated hexokinases play a role in the control of programmed cell death in Nicotiana benthamiana. Plant Cell 18:2341–2355
• Kühn C, Grof CP (2010) Sucrose transporters of higher plants. Curr Opin Plant Biol 13:288–298
• Kürschner E, Bonman JM, Garrity DP, Tamisin MM, Pabale D, Estrada BA (1992) Effects of nitrogen timing and split application on blast disease in upland rice. Plant Dis 76:384–389
• Kuźniak E, Kornas A, Gabara B, Ullrich C, Skłodowska M, Miszalski Z (2010) Interaction of Botrytis cinerea with the intermediate C3-CAM plant Mesembryanthemum crystallinum. Environ Exp Bot 69:137–147
• Kuźniak E, Gabara B, Skłodowska M, Libik-Konieczny M, Miszalski Z (2011) Effects of NaCl on the response of Mesembryanthemum crystallinum callus to Botrytis cinerea infection. Biol Plant 55:423–430
• Lanubilea A, Bernardi J, Battilani P, Logriecoc A, Marocco A (2012) Resistant and susceptible maize genotypes activate different transcriptional responses against Fusarium verticillioides. Physiol Mol Plant Pathol 77:52–59
• Last FT (1953) Some effects of temperature and nitrogen supply on wheat powdery mildew. Ann Appl Biol 40:312–322
• Łaźniewska J, Macioszek VK, Lawrence ChB, Kononowicz AK (2010) Fight to the death: Arabidopsis thaliana defense response to fungal necrotrophic pathogens. Acta Physiol Plant 32:1–10
• Libik-Konieczny M, Surówka E, Kuźniak E, Nosek M, Miszalski Z (2011) Effects of Botrytis cinerea and Pseudomonas syringae infection on the antioxidant profile of Mesembryanthemum crystallinum C3/CAM intermediate plant. J Plant Physiol 168(10):1052–1059
• Libik-Konieczny M, Surówka E, Nosek M, Goraj S, Miszalski Z (2012) Pathogen-induced changes in malate content and NADP dependent malic enzyme activity in C3 or CAM performing Mesembryanthemum crystallinum L. plants. Acta Physiol Plant 34:1471–1477
• Long DH, Lee FN, TeBeest DO (2000) Effect of nitrogen fertilization on disease progress of rice blast on susceptible and resistant cultivars. Plant Dis 84:403–409
• Morkunas I, Bednarski W (2008) Fusarium oxysporum induced oxidative stress and antioxidative defenses of yellow lupine embryo axes with different level of sugars. J Plant Physiol 165:262–277
• Morkunas I, Gmerek J (2007) The possible involvement of peroxidase in defense of yellow lupine embryo axes against Fusarium oxysporum. J Plant Physiol 164:185–194
• Morkunas I, Garnczarska M, Bednarski W, Ratajczak W, Waplak S (2003) Metabolic and ultrastructural responses of lupine embryo axes to sugar starvation. J Plant Physiol 160:311–319
• Morkunas I, Bednarski W, Kozłowska M (2004) Response of embryo axes of germinating seeds of yellow lupine to Fusarium oxysporum. Plant Physiol Biochem 42:493–499
• Morkunas I, Marczak Ł, Stachowiak J, Stobiecki M (2005) Sucrose-stimulated accumulation of isoflavonoids as a defense response of lupine to Fusarium oxysporum. Plant Physiol Biochem 43:363–373
• Morkunas I, Kozłowska M, Ratajczak L, Marczak Ł (2007) Role of sucrose in the development of Fusarium wilt in lupine embryo axes. Physiol Mol Plant Pathol 70:25–37
• Morkunas I, Bednarski W, Kopyra M (2008) Defense strategies of pea embryo axes with different levels of sucrose to Fusarium oxysporum and Ascochyta pisi. Physiol Mol Plant Pathol 72:167–178
• Morkunas I, Stobiecki M, Marczak Ł, Stachowiak J, Narożna D, Remlein-Starosta D (2010) Changes in carbohydrate and isoflavonoid metabolism in yellow lupine in response to infection by Fusarium oxysporum during the stages of seed germination and early seedling growth. Physiol Mol Plant Pathol 75:46–55
• Morkunas I, Narożna D, Nowak W, Samardakiewicz W, Remlein-Starosta D (2011) Cross-talk interactions of sucrose and Fusarium oxysporum in the phenylpropanoid pathway and the accumulation and localization of flavonoids in embryo axes of yellow lupine. J Plant Physiol 168:424–433
• Morkunas I, Formela M, Marczak Ł, Stobiecki M, Bednarski W (2013) The mobilization of defence mechanisms in the early stages of pea seed germination against Ascochyta pisi. Protoplasma 250:63–75
• Muchembled J, Loune’s-Hadj Sahraoui A, Grandmougin- Ferjani A, Sancholle M (2006) Changes in lipid composition of Blumeria graminis f. sp. tritici conidia produced on wheat leaves treated with heptanoyl salicylic acid. Phytochemistry 67:1104–1109
• Naoumkina MA, Zhao QA, Gallego Giraldo L, Dai XB, Zhao PX, Dixon R (2010) Genome-wide analysis of phenylpropanoid defence pathways. Mol Plant Pathol 11:829–846
• Nikraftar F, Taheri P, Rastegar MF, Tarighi S (2013) Tomato partial resistance to Rhizoctonia solani involves antioxidative defense mechanisms. Physiol Mol Plant Pathol 81:74–83
• Nishimura MT, Dangl JL (2010) Arabidopsis and the plant immune system. Plant J 61:1053–1066
• Norholm MH, Nour-Eldin HH, Brodersen P, Mundy J, Halkier BA (2006) Expression of the Arabidopsis high-affinity hexose transporter STP13 correlates with programmed cell death. FEBS Lett 580:2381–2387
• Nunes C, O’Hara LE, Primavesi LF, Delatte TL, Schluepmann H, Somsen GW, Silva AB, Fevereiro PS, Wingler A, Paul MJ (2013a) The trehalose 6-phosphate/SnRK1 signaling pathway primes growth recovery following relief of sink limitation. Plant Physiol 162:1720–1732
• Nunes C, Primavesi LF, Patel MK, Martinez-Barajas E, Powers SJ, Sagar R, Fevereiro PS, Davis BG, Paul MJ (2013b) Inhibition of SnRK1 by metabolites: tissue-dependent 35 effects and cooperative inhibition by glucose 1-phosphate in combination with trehalose 6-phosphate. Plant Physiol Biochem 63:89–98
• Paul MJ, Primavesi LF, Jhurreea D, Zhang Y (2008) Trehalose metabolism and signaling. Annu Rev Plant Biol 59:417–441
• Perfus-Barbeoch L, Jones AM, Assmann SA (2004) Plant heterotrimeric G protein function: insights from Arabidopsis and rice mutants. Curr Opin Plant Biol 7:719–731
• Picman AK, Schneider EF, Picman J (1995) Effect of flavonoids on mycelial growth of Verticillium albo-atrum. Biochem Syst Ecol 23:683–693
• Pieterse CM, Leon-Reyes A, Van der Ent S, Van Wees SC (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308–316
• Płażek A, Żur I (2003) Cold-induced plant resistance to necrotrophic pathogens and antioxidant enzyme activities and cell membrane permeability. Plant Sci 164:1019–1028
• Polge C, Thomas M (2007) SNF1/AMPK/SnRK1 kinases, global regulators at the heart of energy control? Trends Plant Sci 12:20–28
• Price J, Laxmi A, St Martin SK, Jang JC (2004) Global transcription profiling reveals multiple sugar signal transduction mechanisms in Arabidopsis. Plant Cell 16:2128–2150
• Rampitsch C, Bykova NV (2012) Proteomics and plant disease: advances in combating a major threat to the global food supply. Proteomics 12:673–690
• Rapacz M, Płazek A, Niemczyk E (2000) Frost de-acclimation of barley (Hordeum vulgare L.) and meadow fescue (Festuca pratensis Huds.). Relationship between soluble carbohydrate content and resistance to frost and the fungal pathogen Bipolaris sorokiniana (Sacc.) Shoem. Ann Bot 86:539–545
• Reignault P, Cojan A, Muchembled J, Sahouri AL, Durand R, Sancholle M (2001) Trehalose induces resistance to powdery mildew in wheat. New Phytol 149:519–529
• Robaglia C, Thomas M, Mayer C (2012) Sensing nutrient and energy status by SnRK1 and TOR kinases. Curr Opin Plant Biol 15:1–7
• Roberts MR, Paul ND (2006) Seduced by the dark side: integrating molecular and ecological perspectives on the influence of light on plant defence against pests and pathogens. New Phytol 170:677–699
• Robert-Seilaniantz A, Grant M, Jones JDG (2011) Hormone crosstalk in plant disease and defense: more than just jasmonate–salicylate antagonism. Ann Rev Phytopathol 49:317–343
• Robert-Seilaniantz A, Navarro L, Bari RJ, Jones JDG (2007) Pathological hormone imbalances. Curr Opin Plant Biol 10:372–379
• 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
• Rook F, Gerrits N, Kortstee A, Kampen Mv, Borrias M, Weisbeek P (1998) Sucrose-specific signalling represses translationof the Arabidopsis ATB2 bZIP transcription factor gene. Plant J 15:253–263
• Rosa M, Prado C, Podazza G, Interdonato R, González JA, Hilal M (2009) Soluble sugars—metabolism, sensing and abiotic stress: a complex network in the life of plants. Plant Signal Behav 4:388–393
• Ruelland E, Zachowski A (2010) How plants sense temperature. Environ Exp Bot 69:225–232
• Scharte J, Schön H, Weis E (2005) Photosynthesis and carbohydrate metabolism in tobacco leaves during an incompatible interaction with Phytophthora nicotianae. Plant Cell Environ 28:1421–1435
• Schenk PM, Carvalhais LC, Kazan K (2012) Unraveling plant–microbe interactions: can multi-species transcriptomics help? Trends Biotechnol 30: 177–184
• Scholes J, Rolfe SA (1996) Photosynthesis in localised regions of oat leaves infected with crown rust (Puccinia coronata): quantitative imaging of chlorophyll fluorescence. Planta 199:573–582
• Sheen J (1990) Metabolic repression of transcription in higher plants. Plant Cell 2:1027–1038
• Slewinski TL (2011) Diverse functional roles of monosaccharide transporters and their homologs in vascular plants: a physiological perspective. Mol Plant 4:641–662
• Smeekens S, Ma J, Hanson J, Rolland F (2010) Sugar signals and molecular networks controlling plant growth. Curr Opin Plant Biol 13:274–279
• Stokes ME, Chattopadhyay A, Wilkins O, Nambara E, Campbell MM (2013) Interplay between sucrose and folate modulates auxin signaling in Arabidopsis. Plant Physiol 162:1552–1565
• Strömberg AS, Brishammar SA (1993) Histological evaluation of induced resistance to Phytophthora infestans (Mont.) de Bary in potato leaves. J Phytopathol 137:15–25
• Sutton P, Gilbert M, Williams L, Hall JL (2007) Powdery mildew infection of wheat leaves changes host solute transport and invertase activity. Physiol Plant 129:787–795
• Svyatyna K, Riemann M (2012) Light-dependent regulation of the jasmonate pathway. Protoplasma 249:S137–S145
• Swarbrick PJ, Schulze-Lefert P, Scholes JD (2006) Metabolic consequences of susceptibility and resistance in barley leaves challenged with powdery mildew. Plant Cell Environ 29:1061–1076
• Taheri P, Tarighi S (2011) A survey on basal resistance and riboflavin-induced defense responses of sugar beet against Rhizoctonia solani. J Plant Physiol 168:1114–1122
• Teich AH, Sampson DR, Shugar L, Smid A, Curnoe WE, Kennema C (1987) Yield, quality and disease response of soft white winte wheat cultivars to nitrogen fertilization in Ontario, Canada. Cereal Res Commun 15:265–272
• Thibaud MC, Gineste S, Nussaume L, Robaglia C (2004) Sucrose increases pathogenesis-related PR-2 gene expression in Arabidopsis thaliana through an SA-dependent but NPR1-independent signalling pathway. Plant Physiol Biochem 42:81–88
• Ton J, Flors V, Mauch-Mani B (2009) The multifaceted role of ABA in disease resistance. Trends Plant Sci 14:310–317
• Tronsmo AM (1986) Host water potentials may restrict development of snow mould fungi in low temperature-hardened grasses. Physiol Plant 68:175–179
• Vargas WA, Martin JM, Rech GE, Rivera LP, Benito EP, Diaz-Minguez JM, Thon MR, Sukno SA (2012) Plant defense mechanisms are activated during biotrophic and necrotrophic development of Colletotricum graminicola in maize. Plant Physiol 158:1342–1358
• Vidhyasekaran P (1974) Possible role of sugars in restriction of lesion development in finger millet leaves infected with Helminthosporium tetramera. Physiol Plant Pathol 4:457–467
• Voegele RT, Stuck 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
• Voegele RT, Wirsel S, Möll U, Lechner M, Mendgen K (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
• Walters DR, McRoberts N (2006) Plants and biotrophs: a pivotal role for cytokinins? Trends Plant Sci 11:581–586
• Wasilewska A, Vlad F, Sirichandra C, Redko Y, Jammes F, Valona C et al (2008) An update on abscisic acid signaling in plants and more. Mol Plant 1:198–217
• Weidenbörner M, Hindorf H, Jha HC, Tsotsonos P, Egge H (1990) Antifungal activity of isoflavonoids in different reduced stages of Rhizoctonia solani and Sclerotium rolfsii. Phytochemistry 29:801–803
• Weltmeier F, Rahmani F, Ehlert A, Dietrich K, Schutze K, Wang X, Chaban C, Hanson J, Teige M, Harter K, Vicente-Carbajosa J, Smeekens S, Droge-Laser W (2009) Expression patterns within the Arabidopsis C/S1 bZIP transcription factor network: availability of heterodimerization partners controls gene expression during stress response and development. Plant Mol Biol 69:107–119
• Wind J, Smeekens S, Hanson J (2010) Sucrose: metabolite and signaling molecule. Phytochemistry 71:1610–1614
• Wingler A, Delatte TL, O’Hara LE, Primavesi LF, Jhurreea D, Paul MJ, Schluepmann H (2012) Trehalose 6-phosphate is required for the onset of leaf senescence associated with high carbon availability. Plant Physiol 158:1241–1251
• Wojtaszek P (1997) Mechanisms for the generation of reactive oxygen species in plant defence response. Acta Physiol Plant 19:581–589
• 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
• Xie XZ, Xue YJ, Zhou JJ, Zhang B, Chang H, Takano M (2011) Phytochromes regulate SA and JA signaling pathways in rice and are required for developmentally controlled resistance to Magnaporthe grisea. Mol Plant 4:688–696
• Yoshida M, Nakajima T, Tonooka T (2008) Effect of nitrogen application at anthesis on Fusarium head blight and mycotoxin accumulation in breadmaking wheat in the western part of Japan. J Gen Plant Pathol 74:355–363
• Yu S, Liang C, Liping Z, Diqiu Y (2010) Over expression of OsWRKY72 gene interferes in the abscisic acid signal and auxin transport pathway of Arabidopsis. J Biosci 35:459–471
• Zhang J, Zhou JM (2010) Plant immunity triggered by microbial molecular signatures. Mol Plant 3:783–793
• Zhang Y, Primavesi LF, Jhurreea D, Andralojc PJ, Mitchell RA, Powers SJ, Schluepmann H, Delatte T, Wingler A, Paul MJ (2009) Inhibition of SNF1-related protein kinase1 activity and regulation of metabolic pathways by trehalose-6-phosphate. Plant Physiol 149:1860–1871
• Zipfel C, Robatzek S (2010) Pathogen-associated molecular pattern triggered immunity: veni, vidi…? Plant Physiol 154:551–554

Identyfikatory

DOI

10.1007/s11738-014-1559-z