Skip to main content
SpringerLink
Log in

Pea aphid infestation induces changes in flavonoids, antioxidative defence, soluble sugars and sugar transporter expression in leaves of pea seedlings

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

The perception of aphid infestation induces highly coordinated and sequential defensive reactions in plants at the cellular and molecular levels. The aim of the study was to explore kinetics of induced antioxidative defence responses in leaf cells of Pisum sativum L.cv. Cysterski upon infestation of the pea aphid Acyrthosiphon pisum at varying population sizes, including accumulation of flavonoids, changes of carbon metabolism, and expression of nuclear genes involved in sugar transport. Within the first 96 h, after A. pisum infestation, flavonoid accumulation and increased peroxidase activity were observed in leaves. The level of pisatin increased after 48 h of infestation and reached a maximum at 96 h. At this time point, a higher concentration of flavonols was observed in the infested tissue than in the control. Additionally, strong post-infestation accumulation of chalcone synthase (CHS) and isoflavone synthase (IFS) transcription products was also found. The levels of sucrose and fructose in 24-h leaves infested by 10, 20, and 30 aphids were significantly lower than in the control. Moreover, in leaves infested by 30 aphids, the reduced sucrose level observed up to 48 h was accompanied by a considerable increase in the expression level of the PsSUT1 gene encoding the sucrose transporter. In conclusion, A. pisum infestation on pea leads to stimulation of metabolic pathways associated with defence.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Abbreviations

ABTS+ :

The 2,2'-azino-bis-(3-ethylbenzthiazoline-6-sulphonic acid) cation

CHS:

Chalcone synthase

DPBA:

Diphenylboric acid 2-aminoethyl ester

G:

Gram

Hpi:

Hours post infestation

IFS:

Isoflavone synthase

LC/UV/ESI/MS/MS:

Liquid chromatography/ultraviolet detection/electrospray/mass spectrometry (tandem mass spectrometry)

POX:

Peroxidase

ROS:

Reactive oxygen species

SUT1:

Sucrose transporter

SUF1, SUF4:

Sucrose facilitators

SWEETs:

Sugar efflux carriers

TAC:

Total antioxidant capacity

References

  • Akerström B, Maghzal GJ, Winterbourn CC, Kettle AJ (2007) The lipocalin 1-microglobulin has radical scavenging activity. J Biol Chem 282(43):31493–31503

    Article  PubMed  Google Scholar 

  • Allison SD, Schultz JC (2004) Differential activity of peroxidase isozymes in response to wounding, gypsy moth, and plant hormones in northern red oak (Quercus rubra L.). J Chem Ecol 30(7):1363–137

    Article  CAS  PubMed  Google Scholar 

  • Ateyyat M, Abu-Romman S, Abu-Darwish M, Ghabeish I (2012) Impact of flavonoids against woolly apple aphid, Eriosoma lanigerum (Hausmann) and its sole parasitoid, Aphelinus mali (Hald.). J Agric Sci 4(2):227–236

    Google Scholar 

  • Berthier A, Desclos M, Amiard V, Morvan-Bertrand A, Demmig-Adams B, Adams WW 3rd, Turgeon R, Prud'homme MP, Noiraud-Romy N (2009) Activation of sucrose transport in defoliated Lolium perenne L.: an example of apoplastic phloem loading plasticity. Plant Cell Physiol 50(7):1329–1344

    Article  CAS  PubMed  Google Scholar 

  • Bitterlich M, Krügel U, Boldt-Burisch K, Franken P, Kühn C (2014) The sucrose transporter SlSUT2 from tomato interacts with brassinosteroid functioning and affects arbuscular mycorrhiza formation. Plant J 78(5):877–89

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bourdon E, Blache D (2001) The importance of proteins in defense against oxidation. Antioxid Redox Signal 3(2):293–311

    Article  CAS  PubMed  Google Scholar 

  • Bradford M (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Chen S, Li XQ, Zhao A, Wang L, Li X, Shi Q, Chen M, Guo J, Zhang J, Qi D, Liu G (2009) Genes and pathways induced in early response to defoliation in rice seedlings. Curr Issues Mol Biol 11(2):81–100

    CAS  PubMed  Google Scholar 

  • Chen LQ, Qu XQ, Hou BH, Sosso D, Osorio S, Fernie AR, Frommer WB (2012) Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science 335:207–211

    Article  CAS  PubMed  Google Scholar 

  • Chen LQ, Lin IW, Qu XQ, Sosso D, McFarlanec HE, Londoñoa A, Samuelsc AL, Frommer WB (2015) A cascade of sequentially expressed sucrose transporters in the seed coat and endosperm provides nutrition for the Arabidopsis embryo. Plant Cell 27(3):607–619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chincinska IA, Liesche J, Krugel U, Michalska J, Geigenberger P, Grimm B, Kühn C (2008) The sucrose transporter StSUT4 from Solanum tuberosum affects flowering, tuberization and shade avoidance response. Plant Physiol 146:515–528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christensen JH, Bauw G, Welinder KG, Van Montagu M, Boerjan W (1998) Purification and characterization of peroxidases correlated with lignification in poplar xylem. Plant Physiol 118(1):125–135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dao TT, Linthorst HJ, Verpoorte R (2011) Chalcone synthase and its functions in plant resistance. Phytochem Rev 10(3):397–412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dibley K (2012) The functional characterisation of novel sucrose transporters. Dissertation. The University of Newcastle

  • 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(7):413–422

    Article  CAS  PubMed  Google Scholar 

  • Douglas AE (2006) Phloem-sap feeding by animals: problems and solutions. J Exp Bot 57(4):747–754

    Article  CAS  PubMed  Google Scholar 

  • Dubey NK, Idris A, Verma AK, Chandrashekar K, Pandey KD (2013) Expression pattern of sucrose transporters in Arabidopsis thaliana during aphid (Myzus persiace) infestation. Am J Plant Sci 4:47–51

    Article  CAS  Google Scholar 

  • Endler A, Meyer S, Schelbert S, Schneider T, Weschke W, Peters SW, Keller F, Baginsky S, Martinoia E, Schmidt UG (2006) Identification of a vacuolar sucrose transporter in Barley and Arabidopsis mesophyll cells by a tonoplast proteomic approach. Plant Physiol 141:196–207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferrieri AP, Arce CC, Machado RA, Meza-Canales ID, Lima E, Baldwin IT, Erb M (2015) A Nicotiana attenuata cell wall invertase inhibitor (NaCWII) reduces growth and increases secondary metabolite biosynthesis in herbivore-attacked plants. New Phytol. doi:10.1111/nph.13475

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Formela M, Samardakiewicz S, Marczak Ł, Nowak W, Narożna D, Bednarski W, Kasprowicz-Maluśki A, Morkunas I (2014) Effects of endogenous signals and Fusarium oxysporum on the mechanism regulating genistein synthesis and accumulation in yellow lupine and their impact on plant cell cytoskeleton. Molecules 19(9):13392–13421

    Article  PubMed  Google Scholar 

  • 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(2):821–829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gould KS, Lister C (2006) Flavonoid functions in plants. In: Andersen ØM, Markham KR (eds) Flavonoids: chemistry, biochemistry and applications. CRC Press, London, New York, Boca Raton, pp 397–441

    Google Scholar 

  • Harborne JB, Williams CA (2000) Advances in flavonoid research since 1992. Phytochemistry 55(6):481–504

    Article  CAS  PubMed  Google Scholar 

  • Hernández I, Alegre L, Van Breusegem F, Munné-Bosch S (2009) How relevant are flavonoids as antioxidants in plants? Trends Plant Sci 14:125–132

    Article  PubMed  Google Scholar 

  • Hodge S, Ward JL, Beale MH, Bennett M, Mansfield JW, Powell G (2013) Aphid-induced accumulation of trehalose in Arabidopsis thaliana is systemic and dependent upon aphid density. Planta 237:1057–1064

    Article  CAS  PubMed  Google Scholar 

  • Jeandet P, Clément C, Courot E, Cordelier S (2013) Modulation of phytoalexin biosynthesis in engineered plants for disease resistance. Int J Mol Sci 14(7):14136–14170

    Article  PubMed  PubMed Central  Google Scholar 

  • Jeandet P, Hébrard C, Deville MA, Cordelier S, Dorey S, Aziz A, Crouzet J (2014) Deciphering the role of phytoalexins in plant-microorganism interactions and human health. Molecules 19(11):18033–18056

    Article  PubMed  Google Scholar 

  • Kempema LA, Cui X, Holzer FM, Walling LL (2007) Arabidopsis transcriptome changes in response to phloem-feeding silver leaf whitefly nymphs. Similarities and distinctions in responses to aphids. Plant Physiol 143(2):849–865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koch K (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7:235–246

    Article  CAS  PubMed  Google Scholar 

  • Kotkar HM, Mendki PS, Sadan SV, Jha SR, Upasani SM, Maheshwari VL (2002) Antimicrobial and pesticidial activity of partially purified flavonoids of Annona squamos. Pest Manag Sci 58(1):33–37

    Article  CAS  PubMed  Google Scholar 

  • Kühn C (2010) Sucrose transporters in plant development. In: Geisler M, Venema K (ed) Signaling and Communication in Plants: Transporters and pumps in plant signaling, Springer Verlag Heidelberg, pp. 225-251

  • Kühn C, Grof CP (2010) Sucrose transporters of higher plants. Curr Opin Plant Biol 13(3):288–298

    Article  PubMed  Google Scholar 

  • Kühn C, Hajirezaei MR, Fernie AR, Roessner-Tunali U, Czechowski T, Hirner B, Frommer WB (2003) The sucrose transporter StSUT1 localizes to sieve elements in potato tuber phloem and influences tuber physiology and development. Plant Physiol 131:102–113

    Article  PubMed  PubMed Central  Google Scholar 

  • Kuśnierczyk A, Winge P, Jørstad TS, Trończyska J, Rossiter JT, Bones AM (2008) Towards global understanding of plant defense against aphids—timing and dynamics of early Arabidopsis defense responses to cabbage aphid (Brevicoryne brassicae) attack. Plant Cell Environ 31(8):1097–1115

    Article  PubMed  Google Scholar 

  • Lammens W, Le Roy K, Van Laere A, Rabijns A, Van den Ende W (2008) Crystal structures of Arabidopsis thaliana cell-wall invertase mutants in complex with sucrose. J Mol Biol 377(2):378–385

    Article  CAS  PubMed  Google Scholar 

  • Lattanzio V, Arpaia S, Cardinali A, di Venere D, Linsalata V (2000) Role of endogenous flavonoids in resistance mechanism of Vigna to aphids. J Agric Food Chem 48:5316–5320

    Article  CAS  PubMed  Google Scholar 

  • Lemoine R, La Camera S, Atanassova R, Dédaldéchamp F, Allario T, Portau N, Bonnemain J-L, Laloi M, Coutos-Thiévenot P, Maurousset L, Faucher M, Girousse C, Lemonnier P, Parrilla J, Durand M (2013) Source-to-sink transport of sugar and regulation by environmental factors. Front Plant Sci 4(272):1–21

    Google Scholar 

  • Lev-Yadun S, Gould KS (2009) Role of anthocyanins in plant defense. In: Gould KS, Davies KM, Winefield C (ed) Life's colorful solutions: the biosynthesis, functions and applications of anthocyanins, Springer-Verlag Berlin, pp. 21–48

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔC T method. Methods 25(4):402–408

    Article  CAS  PubMed  Google Scholar 

  • Mai VC, Bednarski W, Borowiak-Sobkowiak B, Wilkaniec B, Samardakiewicz S, Morkunas I (2013) Oxidative stress in pea seedling leaves in response to Acyrthosiphon pisum infestation. Phytochemistry 93:49–62

    Article  CAS  PubMed  Google Scholar 

  • Mai VC, Drzewiecka K, Jeleń H, Narożna D, Rucińska-Sobkowiak R, Kęsy J, Floryszak-Wieczorek J, Gabryś B, Morkunas I (2014) Differential induction of Pisum sativum defense signaling molecules in response to pea aphid infestation. Plant Sci 221–222:1–12

    Article  PubMed  Google Scholar 

  • Moran PJ, Thompson GA (2001) Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. Plant Physiol 125:1074–1085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moran PJ, Cheng Y, Cassell JL, Thompson GA (2002) Gene expression profiling of Arabidopsis thaliana in compatible plant–aphid interactions. Arch Insect Biochem Physiol 51:182–203

    Article  CAS  PubMed  Google Scholar 

  • Morkunas I, Gmerek J (2007) The possible involvement of peroxidase in defence of yellow lupine embryo axes against Fusarium oxysporum. J Plant Physiol 164(2):185–194

    Article  CAS  PubMed  Google Scholar 

  • Morkunas I, Ratajczak L (2014) The role of sugar signaling in plant defense responses against fungal pathogens. Acta Physiol Plant 36(7):1607–1619

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Morkunas I, Mai VC, Gabryś B (2011a) Phytohormonal signaling in plant responses to aphid feeding. Acta Physiol Plant 33(6):2057–2073

    Article  CAS  Google Scholar 

  • Morkunas I, Narożna D, Nowak W, Samardakiewicz S, Remlein-Starosta D (2011b) 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

    Article  CAS  PubMed  Google Scholar 

  • Morkunas I, Formela M, Floryszak-Wieczorek J, Marczak Ł, Narożna D, Nowak W, Bednarski W (2013) Cross-talk interactions of exogenous nitric oxide and sucrose modulates phenylpropanoid metabolism in yellow lupine embryo axes infected with Fusarium oxysporum. Plant Sci 211:102–121

    Article  CAS  PubMed  Google Scholar 

  • Mutti NS, Louis J, Pappan L, Pappan K, Begum K, Chen M-S, Park Y, Dittmer N, Marshall J, Reese JC, Reeck GR (2008) A protein from the salivary glands of the pea aphid, Acyrthosiphon pisum, is essential in feeding on a host plant. Proc Natl Acad Sci U S A 105(29):9965–9969

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Payyavula RS, Tay KHC, Tsai C-J, Harding SA (2011) The sucrose transporter family in Populus: the importance of a tonoplast PtaSUT4 to biomass and carbon partitioning. Plant J 65:757–770w

    Article  CAS  PubMed  Google Scholar 

  • Peer WA, Murphy AS (2006) Flavonoid as signal molecules: targets of flavonoids action. In: Grotewold E (ed) The science of flavonoids. Springer, Berlin, pp 239–268

    Chapter  Google Scholar 

  • Pourcel L, Routaboul JM, Cheynier V, Lepiniec L, Debeaujon I (2007) Flavonoid oxidation in plants: from biochemical properties to physiological functions. Trends Plant Sci 12(1):29–36

    Article  CAS  PubMed  Google Scholar 

  • Price DR, Gatehouse JA (2014) Genome-wide annotation and functional identification of aphid GLUT-like sugar transporters. BMC Genomics 15:647

    Article  PubMed  PubMed Central  Google Scholar 

  • Proels RK, Huckelhoven R (2014) Cell-wall invertases, key enzymes in the modulation of plant metabolism during defence responses. Mol Plant Pathol 15(8):858–64

    Article  CAS  PubMed  Google Scholar 

  • Quiroga M, Guerrero C, Botella MA, Barceló A, Amaya I, Medina MI, Alonso FJ, de Forchetti SM, Tigier H, Valpuesta V (2000) A tomato peroxidase involved in the synthesis of lignin and suberin. Plant Physiol 122(4):1119–1128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reinders A, Sivitz AB, Starker CG, Gantt JS, Ward JM (2008) Functional analysis of LjSUT4, a vacuolar sucrose transporter from Lotus japonicus. Plant Mol Biol 68:289–299

    Article  CAS  PubMed  Google Scholar 

  • Reinders A, Sivitz A, Ward J (2012) Evolution of plant sucrose uptake transporters. Front Plant Sci 3:1–12

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Salunke BK, Kotkar HM, Mendki PS, Upasani SM, Maheshwari VL (2005) Efficacy of flavonoids in controlling Callosobruchus chinensis (L.) (Coleoptera: Bruchidae), a post-harvest pest of grain legumes. Crop Prot 24(10):888–893

    Article  CAS  Google Scholar 

  • Sauer N (2007) Molecular physiology of higher plant sucrose transporters. FEBS Lett 581(12):2309–2317

    Article  CAS  PubMed  Google Scholar 

  • Schaarschmidt S, Roitsch T, Hause B (2006) Arbuscular mycorrhiza induces gene expression of the apoplastic invertase LIN6 in tomato (Lycopersicon esculentum) roots. J Exp Bot 57(15):4015–23

    Article  CAS  PubMed  Google Scholar 

  • Scheidt HA, Pampel A, Nissler L, Gebhardt R, Huster D (2004) Investigation of the membrane localization and distribution of flavonoids by high-resolution magic angle spinning NMR spectroscopy. Biochim Biophys Acta 1663(1-2):97–107

    Article  CAS  PubMed  Google Scholar 

  • Sherson SM, Alford HL, Forbes SM, Wallace G, Smith SM (2003) Roles of cell-wall invertases and monosaccharide transporters in the growth and development of Arabidopsis. J Exp Bot 54(382):525–531

    Article  CAS  PubMed  Google Scholar 

  • Shiratake K (2007) Genetics of sucrose transporter in plants. Genes, Genomes and Genomics Global Science Books 1(1):73-80

  • Simmonds MSJ (2003) Flavonoid–insect interactions: recent advances in our knowledge. Phytochemistry 6:21–30

    Article  Google Scholar 

  • Simmonds MSJ, Stevenson PC (2001) Effects of isoflavonoids from Cicer on larvae of Helicoverpa armigera. J Chem Ecol 27(5):965–977

    Article  CAS  PubMed  Google Scholar 

  • Singh V, Louis J, Ayre BG, Reese JC, Shah J (2011) TREHALOSE PHOSPHATE SYNTHASE11-dependent trehalose metabolism promotes Arabidopsis thaliana defense against the phloem-feeding insect Myzus persicae. Plant J 67(1):94–104

    Article  CAS  PubMed  Google Scholar 

  • Sivitz AB, Reinders A, Johnson ME, Krentz AD, Grof CPL, Perroux JM, Ward JM (2007) Arabidopsis sucrose transporter AtSUC9. High affinity transport activity, intragenic control of expression and early-flowering mutant phenotype. Plant Physiol 143:188–198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith CM, Chuang WP (2014) Plant resistance to aphid feeding: behavioral, physiological, genetic and molecular cues regulate aphid host selection and feeding. Pest Manag Sci 70(4):528–540

    Article  PubMed  Google Scholar 

  • Solfanelli C, Poggi A, Loreti E, Alpi A, Perata P (2006) Sucrose-specific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant Physiol 140:637–646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stobiecki M, Wojtaszek P, Gulewicz K (1997) Application of solid phase extraction for profiling of quinolisidine alkaloids and phenolic compounds in Lupinus albus. Phytochem Anal 8:153–158

    Article  CAS  Google Scholar 

  • Tjallingi WF (2006) Salivary secretions by aphids interacting with proteins of phloem wound responses. J Exp Bot 57(4):739–745

    Article  Google Scholar 

  • Upasani SM, Kotkar HM, Mendki PS, Maheshwari VL (2003) Partial characterization and insecticidal properties of Ricinus communis L. foliage flavonoids. Pest Manag Sci 59(12):1349–1354

    Article  CAS  PubMed  Google Scholar 

  • Van Bel AJE, Hess PH (2008) Hexoses as phloem transport sugars: the end of a dogma? J Exp Bot 59(2):261–272

    Article  PubMed  Google Scholar 

  • Van den Ende W (2013) Multifunctional fructans and raffinose family oligosaccharides. Front Plant Sci 4(247):1–11

    Google Scholar 

  • Van Loon JJA, Wang CZ, Nielsen JK, Gols R, Qiu YT (2002) Flavonoids from cabbage are feeding stimulants for diamondback moth larvae additional to glucosinolates: chemoreception and behavior. Entomol Exp App 104:27–34

    Article  Google Scholar 

  • Voelckel C, Weisser WW, Baldwin IT (2004) An analysis of plant–aphid interactions by different microarray hybridization strategies. Mol Ecol 13:3187–3195

    Article  CAS  PubMed  Google Scholar 

  • Wahl R, Wippel K, Goos S, Kämper J, Sauer N (2010) A novel high-affinity sucrose transporter is required for virulence of the plant pathogen Ustilago maydis. PLoS Biol 8(2):e1000303

    Article  PubMed  PubMed Central  Google Scholar 

  • Weschke W, Panitz R, Sauer N, Wang Q, Neubohn B, Wobus U (2000) Sucrose transport into barley seeds: molecular characterization of two transporters and implications for seed development and starch accumulation. Plant J 21:455–467

    Article  CAS  PubMed  Google Scholar 

  • Wimmers LE, Turgeon R (1991) Transfer cells and solute uptake in minor veins of Pisum sativum leaves. Planta 186:2–12

    Article  CAS  PubMed  Google Scholar 

  • Zhou Y, Qu H, Dibley KE, Offler CE, Patrick JW (2007) A suite of sucrose transporters expressed in coats of developing legume seeds includes novel pH-independent facilitators. Plant J 49(4):750–64

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The study was supported by the Polish National Science Centre (NCN, grant no. 2011/01/B/NZ9/00074)

Conflict of interest

The authors declare that they have no competing interests.

Author information

Author notes

  1. Van Chung Mai

    Present address: Department of Plant Physiology, Vinh University, Le Duan 182, Vinh city, Vietnam

Authors and Affiliations

  1. Department of Plant Physiology, Poznań University of Life Sciences, Wołyńska 35, 60-637, Poznań, Poland

    Iwona Morkunas, Agnieszka Woźniak, Magda Formela & Van Chung Mai

  2. Institute of Bioorganic Chemistry, Polish Academy of Sciences, Z. Noskowskiego 12/14, 61-704, Poznań, Poland

    Łukasz Marczak

  3. Department of Biochemistry and Biotechnology, Poznań University of Life Sciences, Dojazd 11, 60-632, Poznań, Poland

    Dorota Narożna

  4. Department of Entomology and Environment Protection, Poznań University of Life Sciences, Dąbrowskiego 159, 60-594, Poznań, Poland

    Beata Borowiak-Sobkowiak

  5. Department of Plant Physiology, Institute of Biology, Humboldt University of Berlin, Philippstrasse 13, 10115, Berlin, Germany

    Christina Kühn & Bernhard Grimm

Authors
  1. Iwona Morkunas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Agnieszka Woźniak
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Magda Formela
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Van Chung Mai
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Łukasz Marczak
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dorota Narożna
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Beata Borowiak-Sobkowiak
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Christina Kühn
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Bernhard Grimm
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Iwona Morkunas.

Additional information

Handling Editor: Néstor Carrillo

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Morkunas, I., Woźniak, A., Formela, M. et al. Pea aphid infestation induces changes in flavonoids, antioxidative defence, soluble sugars and sugar transporter expression in leaves of pea seedlings. Protoplasma 253, 1063–1079 (2016). https://doi.org/10.1007/s00709-015-0865-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-015-0865-7

Keywords

Search

Navigation