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Characterization of STP4 promoter in Indian mustard Brassica juncea for use as an aphid responsive promoter

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Abstract

Objective

Brassica juncea, a major oilseed crop, suffers substantial yield losses due to infestation by mustard aphids (Lipaphis erysimi). Unavailability of resistance genes within the accessible gene pool underpins significance of the transgenic strategy in developing aphid resistance. In this study, we aimed for the identification of an aphid-responsive promoter from B. juncea, based on the available genomic resources.

Results

A monosaccharide transporter gene, STP4 in B. juncea was activated by aphids and sustained increased expression as the aphids colonized the plants. We cloned the upstream intergenic region of STP4 and validated its stand-alone aphid-responsive promoter activity. Further, deletion analysis identified the putative cis-elements important for the aphid responsive promoter activity.

Conclusion

The identified STP4 promoter can potentially be used for driving high level aphid-inducible expression of transgenes in plants. Use of aphid-responsive promoter instead of constitutive promoters can potentially reduce the metabolic burden of transgene-expression on the host plant.

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References

  • Aguayo MF, Ampuero D, Mandujano P, Parada R, Munoz R, Gallart M, Altabella T, Cabrera R, Stange C, Handford M (2013) Sorbitol dehydrogenase is a cytosolic protein required for sorbitol metabolism in Arabidopsis thaliana. Plant Sci 205:63–75

    PubMed  Google Scholar 

  • Ali S, Kim W-C (2019) A fruitful decade using synthetic promoters in the improvement of transgenic plants. Front Plant Sci 10:1433

    PubMed  PubMed Central  Google Scholar 

  • Aluri S, Büttner M (2007) Identification and functional expression of the Arabidopsis thaliana vacuolar glucose transporter 1 and its role in seed germination and flowering. Proc Natl Acad Sci USA 104:2537–2542

    CAS  PubMed  PubMed Central  Google Scholar 

  • Appel HM, Fescemyer H, Ehlting J, Weston D, Rehrig E, Joshi T, Xu D, Bohlmann J, Schultz J (2014) Transcriptional responses of Arabidopsis thaliana to chewing and sucking insect herbivores. Front Plant Sci 5:565

    PubMed  PubMed Central  Google Scholar 

  • Ascencio-Ibáñez JT, Sozzani R, Lee TJ, Chu TM, Wolfinger RD, Cella R, Hanley-Bowdoin L (2008) Global analysis of Arabidopsis gene expression uncovers a complex array of changes impacting pathogen response and cell cycle during gemini virus infection. Plant Physiol 148:436–454

    PubMed  PubMed Central  Google Scholar 

  • Atri C, Kumar B, Kumar H, Kumar S, Sharma S, Banga SS (2012) Development and characterization of Brassica juncea-fruticulosa introgression lines exhibiting resistance to mustard aphid (Lipaphis erysimiKalt). BMC Genet 13:104

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bakhetia DRC (1987) Insect pests of rapeseed-mustard and their management. In: Rao MV, Sithanathan S (eds) Plant protection in field crops. Rajendranagar, PPAI, Irving, pp 249–259

    Google Scholar 

  • Bandopadhyay L, Basu D, Sikdar SR (2013) Identification of genes involved in wild crucifer Rorippa indica resistance response on mustard aphid Lipaphis erysimi challenge. PLoS ONE 8:e73632

    CAS  PubMed  PubMed Central  Google Scholar 

  • Barah P, Winge P, Kusnierczyk A, Tran DH, Bones AM (2013) Molecular signatures in Arabidopsis thaliana in response to insects’ attack and bacterial infection. PLoS ONE 8:e58987

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bhadoria NS, Jakhmola SS, Dhamdhere SV (1995) Relative susceptibility of mustard cultivars to Lipaphis erysimi in North West Madhya Pradesh (India). J Entomol Res 19:143–146

    Google Scholar 

  • Bhatia V, Uniyal P, Bhattacharya R (2011) Aphid resistance in Brassica crops: challenges, biotechnological progress and emerging possibilities. Biotechnol Adv 29:879

    PubMed  Google Scholar 

  • Boughton AJ, Hoover K, Felton GW (2006) Impact of chemical elicitor applications on greenhouse tomato plants and population growth of the green peach aphid, Myzus persicae. Entomol Exp Appl 120:175–188

    CAS  Google Scholar 

  • Brini F, Yamamoto A, Jlaiel L, Takeda S, Hobo T, Dinh HQ (2011) Pleiotropic effects of the wheat dehydrin DHN-5 on stress responses in Arabidopsis. Plant Cell Physiol 52:676–688

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Cho MH, Lim H, Shin DH, Jeon JS, Bhoo SH, Park YI, Hahn TR (2011) Role of the plastidic glucose translocator in the export of starch degradation products from the chloroplasts in Arabidopsis thaliana. New Phytol 190:101–112

    CAS  PubMed  Google Scholar 

  • Cipollini D, Purrington CB, Bergelson J (2003) Costs of induced responses in plants. BAS Appl Ecol 4:79–85

    Google Scholar 

  • Couldridge C, Newbury HJ, Ford-Lloyd B, Bale J, Pritchard J (2007) Exploring plant responses to aphid feeding using a full Arabidopsis microarray reveals a small number of genes with significantly altered expression. Bull Entomol Res 97:523–532

    CAS  PubMed  Google Scholar 

  • Das A, Ghosh P, Das S (2018) Expression of Colocasia esculenta tuber agglutinin in Indian mustard provides resistance against Lipaphis erysimi and the expressed protein is non-allergenic. Plant Cell Rep 37:849

    CAS  PubMed  Google Scholar 

  • Davuluri RV, Sun H, Palaniswamy SK, Matthews N, Molina C, Kurtz M, Grotewold E (2003) AGRIS: Arabidopsis gene regulatory information server, an information resource of Arabidopsiscis-regulatory elements and transcription factors. BMC Bioinform 4:25

    Google Scholar 

  • de Ilarduya MO, Xie QG, Kaloshian I (2003) Aphid-induced defence responses in Mi-1-mediated compatible and incompatible tomato interactions. Mol Plant Microbe Interact 16:699–708

    Google Scholar 

  • De Vos M, Jander G (2009) Myzus persicae (green peach aphid) salivary components induce defense responses in Arabidopsis thaliana. Plant Cell Environ 32:1548–1560

    CAS  PubMed  Google Scholar 

  • De Vos M, Van-Oosten VR, Van-Poecke RMP, Van-Pelt JA, Pozo MJ, Mueller MJ (2005) Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol Plant Microbe Interact 18:923–937

    CAS  PubMed  Google Scholar 

  • Divol F, Vilaine F, Thibivilliers S, Amselem J, Palauqui JC, Kusiak C, Dinant S (2005) Systemic response to aphid infestation by Myzus persicae in the phloem of Apium graveolens. Plant Mol Biol 57:517–540

    CAS  PubMed  Google Scholar 

  • Donahue JL, Alford SR, Torabinejad J, Kerwin RE, Nourbakhsh A, Ray WK, Hernick M, Huang X, Lyons BM, Hein PP, Gillaspy GE (2010) The Arabidopsis thaliana Myo-Inositol 1-phosphate synthase1 gene is required for Myo-inositol synthesis and suppression of cell death. Plant Cell 22:888–890

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dorschner KW, Ryan JD, Johnson RC, Eikenbary RD (1987) Modification of host nitrogen levels by the greenbug (Homoptera: Aphididae): its role in resistance of winter wheat to aphids. Environ Entomol 16:1007–1011

    Google Scholar 

  • DRMR (2015) Vision 2050. https://www.drmr.res.in/publication/DRMR%2520Rajasthan-(Vision2050)-Final.pdf

  • Dubey NK, Mishra DK, Idris A, Nigam D, Singh PK, Sawant SV (2018) Whitefly and aphid inducible promoters of Arabidopsis thaliana L. J Genet 97:109–119

    CAS  PubMed  Google Scholar 

  • Dündar E, Bush DR (2009) BAT1, a bidirectional amino acid transporter in Arabidopsis. Planta 229:1047–1056

    PubMed  Google Scholar 

  • Dutta I, Majumder P, Saha K, Ray P, Das S (2005) Constitutive and phloem specific expression of Allium sativum leaf agglutinin (ASAL) to engineer aphid (Lipaphis erysimi) resistance in transgenic Indian mustard (Brassica juncea). Plant Sci 169:996–1007

    CAS  Google Scholar 

  • Ellis C, Karafyllidis I, Turner JG (2002) Constitutive activation of jasmonate signalling in an Arabidopsis mutant correlates with enhanced resistance to Erysiphe cichoracearum, Pseudomonas syringae, and Myzus persicae. Mol Plant Microbe Interact 15:1025–1030

    CAS  PubMed  Google Scholar 

  • Fotopoulos V, Gilbert MJ, Pittman JK, Marvier AC, Buchanan AJ, Sauer N (2003) The monosaccharide transporter gene, AtSTP4, and the cell-wall invertase, Atβfruct1, are induced in Arabidopsis during infection with the fungal biotroph Erysiphe cichoracearum. Plant Physiol 132:821–829

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gallardo K, Job C, Groot SP, Puype M, Demol H, Vandekerckhove J, Job D (2002) Importance of methionine biosynthesis for Arabidopsis seed germination and seedling growth. Physiol Plant 116:238–247

    CAS  PubMed  Google Scholar 

  • Gao LL, Anderson JP, Klingler JP, Nair RM, Edwards OR, Singh KB (2007) Involvement of the octadecanoid pathway in bluegreen aphid resistance in Medicago truncatula. Mol Plant Microbe Interact 20:82–93

    CAS  PubMed  Google Scholar 

  • Gao Y, Jia S, Wang C, Wang F, Wang F, Zhao K (2016) BjMYB1, a transcription factor implicated in plant defence through activating BjCHI1 chitinase expression by binding to a W-box-like element. J Exp Bot 67:4647–4658

    CAS  PubMed  PubMed Central  Google Scholar 

  • Garcia AF, Dyszy F, Munte CE, Demarco R, Beltramini LM, Oliva G, Costa-Filho AJ, Araujo AP (2014) THI1, a protein involved in the biosynthesis of thiamin in Arabidopsis thaliana: structural analysis of THI1 (A140V) mutant. Biochim Biophys Acta 1844:1094–1103

    CAS  PubMed  Google Scholar 

  • Garrido E, Díaz MF, Bernal H, Nustez CE, Thaler J, Jander G, Poveda K (2017) Costs and trade-offs of resistance and tolerance to belowground herbivory in potato. PLoS ONE 12:e0169083

    PubMed  PubMed Central  Google Scholar 

  • Girousse C, Moulia B, Silk W, Bonnemain JL (2005) Aphid infestation causes different changes in carbon and nitrogen allocation in alfalfa stems as well as different inhibitions of longitudinal and radial expansion. Plant Physiol 137:1474–1484

    CAS  PubMed  PubMed Central  Google Scholar 

  • Goggin FL (2007) Plant-Aphid Interactions: molecular and ecological perspectives. Curr Opin Plant Biol 10:399–408

    CAS  PubMed  Google Scholar 

  • Hanada K, Sawada Y, Kuromori T, Klausnitzer R, Saito K, Toyoda T, Shinozaki K, Li WH, Hirai MY (2011) Functional compensation of primary and secondary metabolites by duplicate genes in Arabidopsis thaliana. Mol Biol Evol 28:377–382

    CAS  PubMed  Google Scholar 

  • Heidel AJ, Baldwin IT (2004) Microarray analysis of salicylic acid and jasmonic acid signalling in responses of Nicotiana attenuata to attack by insects from multiple feeding guilds. Plant Cell Environ 27:1362–1373

    CAS  Google Scholar 

  • Hogenhout SA, Ammar ED, Whitfield AE, Redinbaugh MG (2008) Insect vector interactions with persistently transmitted viruses. Annu Rev Phytopathol 46:327–359

    CAS  PubMed  Google Scholar 

  • Hossain MA, Maiti MK, Basu A, Sen S, Ghosh AK, Sen SK (2006) Transgenic expression of onion leaf lectin gene in Indian mustard offers protection against aphid colonization. Crop Sci 46:2022–2032

    CAS  Google Scholar 

  • Hu W, Wang Y, Bowers C, Ma H (2003) Isolation, sequence analysis, and expression studies of florally expressed cDNAs in Arabidopsis. Plant Mol Biol 53:545–563

    CAS  PubMed  Google Scholar 

  • Ijaz U, Pervaiz T, Ahmed T, Seemab R, Shahid M, Noman M, Nadeem M, Azeem F (2020) Plant cis-regulatory elements: methods of identification and applications. Asian J Agric Biol 8:207–222

    Google Scholar 

  • Jaouannet M, Rodriguez PA, Thorpe P, Lenoir CJ, MacLeod R, Escudero-Martinez C et al (2014) Plant immunity in plant-aphid interactions. Front Plant Sci 5:663

    PubMed  PubMed Central  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907

    CAS  PubMed  PubMed Central  Google Scholar 

  • Johanson U, Karlsson M, Johansson I, Gustavsson S, Sjövall S, Fraysse L, Weig AR, Kjellbom P (2001) The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants. Plant Physiol 126:1358–1369

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jost R, Pharmawati M, Lapis-Gaza HR, Rossig C, Berkowitz O, Lambers H, Finnegan PM (2015) Differentiating phosphate-dependent and phosphate-independent systemic phosphate-starvation response networks in Arabidopsis thaliana through the application of phosphite. J Exp Bot 66:2501–2514

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kanrar S, Venkateswari J, Kirti P, Chopra VL (2002) Transgenic Indian mustard (Brassica juncea) with resistance to the mustard aphid (Lipaphis erysimi Kalt.). Plant Cell Rep 20:976–981

    CAS  Google Scholar 

  • Kaur A, Pati PK, Pati AM, Nagpal AK (2017) In-silico analysis of cis-acting regulatory elements of pathogenesis-related proteins of Arabidopsis thaliana and Oryza sativa. PLoS ONE 12:e0184523

    PubMed  PubMed Central  Google Scholar 

  • Kaur P, Banga S, Kumar N, Gupta S, Akhtar J, Banga S (2014) Polyphyletic origin of Brassica juncea with B. rapa and B. nigra (Brassicaceae) participating as cytoplasm donor parents in independent hybridization events. Am J Bot 101:1157–1166

    PubMed  Google Scholar 

  • Kim TH, Barrera LO, Qu C, Van Calcar S, Trinklein ND, Cooper SJ, Luna RM, Glass CK, Rosenfeld MG, Myers RM, Ren B (2005) Direct isolation and identification of promoters in the human genome. Genome Res 15:830–839

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kiyosue T, Abe H, Yamaguchi-Shinozaki K, Shinozaki K (1998) ERD6, a cDNA clone for an early dehydration-induced gene of Arabidopsis, encodes a putative sugar transporter. Biochim Biophys Acta 1370:187–191

    CAS  PubMed  Google Scholar 

  • Koramutla MK, Kaur A, Negi M, Venkatachalam P, Bhattacharya R (2014) Elicitation of jasmonate-mediated host defense in Brassica juncea (L.) attenuates population growth of mustard aphid Lipaphis erysimi (Kalt.). Planta 240:177–194

    CAS  PubMed  Google Scholar 

  • Krapp A, David LC, Chardin C, Girin T, Marmagne A, Leprince AS, Chaillou S, Ferrario-Méry S, Meyer C, Daniel-Vedele F (2014) Nitrate transport and signalling in Arabidopsis. J Exp Bot 65:789–798

    CAS  PubMed  Google Scholar 

  • Kumar S, Atri C, Sangha M, Banga S (2011) Screening of wild crucifers for resistance to mustard aphid, Lipaphis erysimi (Kaltenbach) and attempt at introgression of resistance gene(s) from Brassica-fruticulosa to Brassica juncea. Euphytica 179:461–470

    Google Scholar 

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

    PubMed  Google Scholar 

  • Ladwig F, Stahl M, Ludewig U, Hirner AA, Hammes UZ, Stadler R, Harter K, Koch W (2012) Siliques are Red1 from Arabidopsis acts as a bidirectional amino acid transporter that is crucial for the amino acid homeostasis of siliques. Plant Physiol 158:1643–1655

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee YH, Tegeder M (2004) Selective expression of a novel high-affinity transport system for acidic and neutral amino acids in the tapetum cells of Arabidopsis flowers. Plant J 40:60–74

    CAS  PubMed  Google Scholar 

  • Lemoine R, Camera SL, Atanassova R, Dédaldéchamp F, Allario T, Pourtau N, Bonnemain JJ, Laloi M, Coutos-Thévenot 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

    PubMed  PubMed Central  Google Scholar 

  • Lezhneva L, Kiba T, Feria-Bourrellier AB, Lafouge F, Boutet-Mercey S, Zoufan P, Hitoshi Sakakibara H, Daniel-Vedele F, Krapp A (2014) The Arabidopsis nitrate transporter NRT2.5 plays a role in nitrate acquisition and remobilization in nitrogen-starved plants. Plant J 80:230–241

    CAS  PubMed  Google Scholar 

  • Li J, Shan L, Zhou JM, Tang X (2002) Overexpression of Pto induces a salicylate-independent cell death but inhibits necrotic lesions caused by salicylate-deficiency in tomato plants. Mol Plant Microbe Interact 15:654–661

    CAS  PubMed  Google Scholar 

  • Liu H, Zhang H, Yang Y, Li G, Yang Y, Wang X, Basnayake BM, Li D, Song F (2008) Functional analysis reveals pleiotropic effects of rice RING-H2 finger protein gene OsBIRF1 on regulation of growth and defence responses against abiotic and biotic stresses. Plant Mol Biol 68:17–30

    CAS  PubMed  Google Scholar 

  • Liu TY, Aung K, Tseng CY, Chang TY, Chen YS, Chiou TJ (2011) Vacuolar Ca2+/H+ transport activity is required for systemic phosphate homeostasis involving shoot-to-root signalling in Arabidopsis. Plant Physiol 156:1176–1189

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lothier J, Gaufichon L, Sormani R, Lemaître T, Azzopardi M, Morin H, Chardon F, Reisdorf-Cren M, Avice JC, Masclaux-Daubresse C (2011) The cytosolic glutamine synthetase GLN1;2 plays a role in the control of plant growth and ammonium homeostasis in Arabidopsis rosettes when nitrate supply is not limiting. J Exp Bot 62:1375–1390

    CAS  PubMed  Google Scholar 

  • Louvet R, Cavel E, Gutierrez L, Guénin S, Roger D, Gillet F, Guerineau F, Pelloux J (2006) Comprehensive expression profiling of the pectin methylesterase gene family during silique development in Arabidopsis thaliana. Planta 224:782–791

    CAS  PubMed  Google Scholar 

  • Lu H, Yang P, Xu Y, Luo L, Zhu J, Cui N, Kang L, Cui F (2016) Performances of survival, feeding behavior, and gene expression in aphids reveal their different fitness to host alteration. Sci Rep 6:19344

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mahoney AK, Anderson EM, Bakker RA, Williams AF, Flood JJ, Sullivan KC, Pillitteri LJ (2016) Functional analysis of the Arabidopsis thaliana MUTE promoter reveals a regulatory region sufficient for stomatal-lineage expression. Planta 243:987–998

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mikkelsen MD, Thomashow MF (2009) A role for circadian evening elements in cold-regulated gene expression in Arabidopsis. Plant J 60:328–339

    CAS  PubMed  Google Scholar 

  • Miles PW (1999) Aphid saliva. Biol Rev 74:41–85

    Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Park SJ, Huang Y, Ayoubi P (2006) Identification of expression profiles of sorghum genes in response to greenbug phloem feeding using cDNA subtraction and microarray analysis. Planta 223:932–947

    CAS  PubMed  Google Scholar 

  • Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP (2004) Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper-Excel-based tool using pair-wise correlations. Biotechnol Lett 26:509–515

    CAS  PubMed  Google Scholar 

  • Pitino M, Hogenhout SA (2012) Aphid protein effectors promote aphid colonization in a plant species-specific manner. Mol Plant Microbe Interact 26:130–139

    Google Scholar 

  • Ram C, Koramutla MK, Bhattacharya R (2017) Identification and comprehensive evaluation of reference genes for RT-qPCR analysis of host gene-expression in Brassica juncea-aphid interaction using microarray data. Plant Physiol Biochem 116:57–67

    CAS  PubMed  Google Scholar 

  • Reddy ASN, Takezawa D, Fromm H, Poovaiah BW (1993) Isolation and characterization of two cDNAs that encode for calmodulin-binding proteins from corn root tips. Plant Sci 94:109–117

    CAS  Google Scholar 

  • Rehill BJ, Schultz JC (2003) Enhanced invertase activities in the galls of Hormaphisham amelidis. J Chem Ecol 29:2703–2720

    CAS  PubMed  Google Scholar 

  • Rodriguez PA, Escudero-Martinez C, Bos JIB (2017) An aphid effector targets trafficking protein VPS52 in a host-specific manner to promote virulence. Plant Physiol 173:1892–1903

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rohilla HR, Singh H, Kalra VK, Kharub SS (1987) Losses caused by mustard aphid, Lipaphis erysimi K. in different Brassica genotype. In: Proceedings of the international rapeseed congress, 11–14 May, 1987, Poland, p. 46

  • Ruta LL, Lin YF, Kissen R, Nicolau I, Neagoe AD, Ghenea S, Bones AM, Farcasanu IC (2017) Anchoring plant metallothioneins to the inner face of the plasma membrane of Saccharomyces cerevisiae cells leads to heavy metal accumulation. PLoS ONE 12:e0178393

    PubMed  PubMed Central  Google Scholar 

  • Sadeghi A (2007) Expression of garlic leaf lectin under the control of the phloem specific promoter Asus1 from Arabidopsis thaliana protects tobacco plants against the tobacco aphids (Myzus nicotianae). Pest Manag Sci 63:1215–1223

    CAS  PubMed  Google Scholar 

  • Saha P, Majumder P, Dutta I, Ray T, Roy SC, Das S (2006) Transgenic rice expressing Allium sativum leaf lectin with enhanced resistance against sap sucking insect pests. Planta 223:1329–1343

    CAS  PubMed  Google Scholar 

  • Sandström J, Telang A, Moran NA (2000) Nutritional enhancement of host plants by aphids—a comparison of three aphid species on grasses. J Insect Physiol 46:33–40

    PubMed  Google Scholar 

  • Santiago JP, Tegeder M (2016) Connecting source with sink: the role of Arabidopsis AAP8 in phloem loading of amino acids. Plant Physiol 171:508–521

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sarkar P, Jana J, Chatterjee S, Sikdar SR (2016) Functional characterization of Rorippa indica defensin and its efficacy against Lipaphis erysimi. SpringerPlus 5:511

    PubMed  PubMed Central  Google Scholar 

  • Schneider S, Schneidereit A, Konrad KR, Hajirezaei MR, Gramann M, Hedrich R, Sauer N (2006) Arabidopsis inositol transporter4 mediates high-affinity H+ symport of myoinositol across the plasma membrane. Plant Physiol 141:565–577

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schuler M, Rellán-Álvarez R, Fink-Straube C, Abadía J, Bauer P (2012) Nicotianamine functions in the phloem-based transport of iron to sink organs, in pollen development and pollen tube growth in Arabidopsis. Plant Cell 24:2380–2400

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schwartzberg EG, Tumlinson JH (2014) Aphid honeydew alters plant defence responses. Funct Ecol 28:386–394

    Google Scholar 

  • Sharma M, Sahni R, Kansal R, Koundal KR (2004) Transformation of oilseed mustard B. juncea var. PJK with Snowdrop lectin gene. Indian J Biotechnol 3:97–102

    CAS  Google Scholar 

  • Shekhawat K, Rathore SS, Premi OP, Kandpal BK, Chauhan JS (2012) Advances in agronomic management of Indian mustard (Brassica juncea (L.) Czernj. Cosson): an overview. Intern J Agron 2012:1–14

    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 54:525–531

    CAS  PubMed  Google Scholar 

  • Singh CP, Sachan GC (1994) Assessment of yield losses in yellow sarson due to mustard aphid. Lipaphis erysimi (Kalt). J Oilseeds Res 11:179–184

    Google Scholar 

  • Smith CM, Boyko EV (2007) The molecular bases of plant resistance and defense responses to aphid feeding: current status. Entomol Exp Appl 122:1–16

    CAS  Google Scholar 

  • Sparkes IA, Runions J, Kearns A, Hawes C (2006) Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat Protoc 1:2019–2025

    CAS  PubMed  Google Scholar 

  • Su YH, Frommer WB, Ludewig U (2004) Molecular and functional characterization of a family of amino acid transporters from Arabidopsis. Plant Physiol 136:3104–3113

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sugaya H, Uchimiya S (1992) Deletion analysis of the 5'-upstream region of the Agrobacterium rhizogenes Ri plasmid rolC gene required for tissue-specific expression. Plant Physiol 99:464–467

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sullivan S, Ralet MC, Berger A, Diatloff E, Bischoff V, Gonneau M, Marion-Poll A, North HM (2011) CESA5 is required for the synthesis of cellulose with a role in structuring the adherent mucilage of Arabidopsis Seeds. Plant Physiol 156:1725–1739

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sun C, Palmqvist S, Olsson H, Borén M, Ahlandsberg S, Jansson C (2003) A novel WRKY transcription factor, SUSIBA2, participates in sugar signaling in barley by binding to the sugar-responsive elements of the iso1 promoter. Plant Cell 15:2076–2092

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sunilkumar G, Mohr L, Lopata-Finch E, Emani C, Rathore KS (2002) Developmental and tissue-specific expression of CaMV 35S promoter in cotton as revealed by GFP. Plant Mol Biol 50:463–474

    CAS  PubMed  Google Scholar 

  • TAIR 10. https://www.Arabidopsis.org/index.jsp

  • Tegeder M (2014) Transporters involved in source to sink partitioning of amino acids and ureides: opportunities for crop improvement. J Exp Bot 65:1865–1878

    CAS  PubMed  Google Scholar 

  • Tegeder M, Ward JM (2012) Molecular evolution of plant AAP and LHT amino acid transporters. Front Plant Sci 3:21

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tian S, Wang X, Li P, Wang H, Ji H, Xie J, Qiu Q, Shen D, Dong H (2016) Plant aquaporin AtPIP1;4 links apoplastic H2O2 induction to disease immunity pathways. Plant Physiol 171:1635–1650

    CAS  PubMed  PubMed Central  Google Scholar 

  • Truernit E, Schmid J, Epple P, Illig J, Sauer N (1996) The sink-specific and stress-regulated Arabidopsis STP4 gene: enhanced expression of a gene encoding a monosaccharide transporter by wounding, elicitors, and pathogen challenge. Plant Cell 8:2169–2182

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Walters D, Heil M (2007) Costs and trade-offs associated with induced resistance. Physiol Mol Plant Pathol 71:3–17

    CAS  Google Scholar 

  • War AR, Paulraj MG, Ahmad T, Buhroo AA, Hussain B, Ignacimuthu S, Sharma HC (2012) Mechanisms of plant defense against insect herbivores. Plant Signal Behav 7:1306–1320

    PubMed  PubMed Central  Google Scholar 

  • Wei PC, Zhang XQ, Zhao P, Wang XC (2011) Regulation of stomatal opening by the guard cell expansin AtEXPA1. Plant Signal Behav 6:740–742

    CAS  PubMed  PubMed Central  Google Scholar 

  • Will T, Tjallingii WF, Thönnessen A, van Bel AJ (2007) Molecular sabotage of plant defense by aphid saliva. Proc Natl Acad Sci USA 104:10536–10541

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu X, Chen C, Fan B, Chen Z (2006) Physical and functional interactions between pathogen-induced Arabidopsis WRKY18, WRKY40, and WRKY60 transcription factors. Plant Cell 18:1310–1326

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu H, Wang X, Zhao H, Liu F (2008) An intensive understanding of vacuum infiltration transformation of pakchoi (Brassica rapa ssp. chinensis). Plant Cell Rep 27:1369–1376

    CAS  PubMed  Google Scholar 

  • Zhu XF, Shi YZ, Lei GJ, Fry SC, Zhang BC, Zhou YH, Braam J, Jiang T, Xu XY, Mao CZ, Pan YJ, Yang JL, Wu P, Zheng SJ (2012) XTH31, Encoding an in vitro xeh/xet-active enzyme, regulates aluminum sensitivity by modulating in vivo xet action, cell wall xyloglucan content, and aluminum binding capacity in Arabidopsis. Plant Cell 24:4731–4747

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu-Salzman K, Salzman RA, Ahn JE, Koiwa H (2004) Transcriptional regulation of sorghum defense determinants against a phloem-feeding aphid. Plant Physiol 134:420–431

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zust T, Agrawal AA (2016) Mechanisms and evolution of plant resistance to aphids. Nat Plants 2:15206

    CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by Post Graduate School, IARI through a Ph.D fellowship to CR and DST-SERB grant (EMR/2017/003463) to RB.

Supporting information

Supplementary Fig. 1 Assay of pCAMBIA-proBjSTP4 construct for bacterial expression. The Agrobacterium cells harbouring the pCAMBIA-proBjSTP4 construct was incubated at 37 °C for 1 h along with GUS assay buffer. Agrobacterium strain harbouring pBI121 (35S::GUS) and pORER2 (35S::GUS) were taken as positive control. Supplementary Table 1 Details of gene-specific primers used for qRT-PCR analysis. Supplementary Table 2 List of primers used for amplification of proBjSTP4 and deletion fragments. Supplementary Table 3 Characteristics features of putative cis-regulatory elements in proBjSTP4.

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Authors and Affiliations

  1. ICAR-National Institute for Plant Biotechnology, ICAR-Indian Agricultural Research Institute Campus, New Delhi, 110012, India

    Chet Ram, Muthuganeshan Annamalai, Murali Krishna Koramutla, Rekha Kansal, Pradeep K. Jain & Ramcharan Bhattacharya

  2. Division of Plant Physiology, ICAR-Indian Agricultural Research Institute Campus, New Delhi, 110012, India

    Ajay Arora

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  1. Chet Ram
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Ram, C., Annamalai, M., Koramutla, M.K. et al. Characterization of STP4 promoter in Indian mustard Brassica juncea for use as an aphid responsive promoter. Biotechnol Lett 42, 2013–2033 (2020). https://doi.org/10.1007/s10529-020-02961-7

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