Abstract
The present study investigated the feeding behaviour and life-table parameters of the grain aphid Sitobion miscanthi in response to being fed on transgenic wheat lines expressing Pinellia ternata agglutinin (PTA) and Arisaema heterophyllum agglutinin (AHA), both of which originate from Chinese medicinal plants. The findings revealed that the feeding behaviour of S. miscanthi on transgenic wheat lines was negatively affected. The aphids that feed on the PTA and AHA transgenic wheat lines had longer total non-probing (np) periods than the aphids that feed on non-transformed lines but exhibited shorter durations of salivation (E1), phloem sap ingestion phase (E2) and sustained ingestion (E2 > 10 min). Moreover, aphids feeding on the 171 line, which expresses PTA, displayed a significant increase in the number of np patterns and time taken to initiate the first probe. Furthermore, the lifespan of S. miscanthi feeding on any of the wheat lines expressing PTA and AHA was found to reduce significantly. The maximum fecundity of the aphids on the AHA-expressing wheat lines was significantly lower than that of the control group. The net reproductive rate (R0) and intrinsic rate of increase (rm) were also significantly lower for the aphids feeding on the PTA and AHA transgenic wheat than for the aphids feeding on the non-transformed control plants. These findings indicate successful detection of resistance to S. miscanthi in the PTA- and AHA-expressing wheat lines, providing a new option for engineering protection against crop pests by expressing unique proteins that occur naturally in medicinal plants.
Similar content being viewed by others
Data Availability
The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.
References
Agra-Neto AC, Napoleão TH, Pontual EV, Santos ND, Luz Lde A, de Oliveira CM, de Melo-Santos MA, Coelho LC, Navarro DM, Paiva PM (2014) Effect of Moringa oleifera lectins on survival and enzyme activities of Aedes aegypti larvae susceptible and resistant to organophosphate. Parasitol Res 113:175–184
Alvarez AE, Tjallingii WF, Garzo E, Vleeshouwers V, Dicke D, Vosman B (2006) Location of resistance factors in the leaves of potato and wild tuber-bearing Solanum species to the aphid Myzus persicae. Entomol Exp Appl 121:145–157
Bensky D, Clavey S, Stoger E, Gamble A (2004) Chinese herbal medicine: materia medica, 3rd edn. Eastland Press, Seattle
Birch ANE, Geoghegan IE, Majerus MEN, McNicol JW, Hackett CA, Gatehouse AMR, Gatehouse JA (1999) Tri-trophic interactions involving pest aphids, predatory two-spot ladybirds and transgenic potatoes expressing snowdrop lectin for aphid resistance. Mol Breed 5:75–83
Blackman R, Eastop V (2000) Aphids on the world’s crops: an identification and information guide. Wiley, London
Chakraborti D, Sarkar A, Mondal HA, Das S (2009) Tissue specific expression of potent insecticidal, Allium sativum leaf agglutinin (ASAL) in important pulse crop, chickpea (Cicer arietinum L.) to resist the phloem feeding Aphis craccivora. Transgenic Res 18:529–544
Chen JL, Sun JR, Ding HJ, Ni HX, Li XF (1997) The resistant patterns and mechanism of biochemical resistance in various wheat cultivars (lines). Acta Entomol Sin 40:190–195
Chougule NP, Bonning BC (2012) Toxins for transgenic resistance to hemipteran pests. Toxins 4:405–429
Coelho MB, Marangoni S, Macedo MLR (2007) Insecticidal action of Annona coriacea lectin against the flour moth Anagasta kuehniella and the rice moth Corcyra cephalonica (Lepidoptera: Pyralidae). Comp Biochem Physiol Part C Toxicol Pharmcol 146:406–414
Collar JL, Fereres A (1998) Nonpersistent virus transmission efficiency determined by aphid probing behavior during intracellular punctures. Environ Entomol 27:583–591
Down R, Gatehouse AMR, Hamilton WDO, Gatehouse JA (1996) Snowdrop lectin inhibits development and fecundity of the glasshouse potato aphid (Aulacorthum solani) when administered in vitro and via transgenic plants, both in laboratory and glasshouse trials. J Insect Physiol 42:1035–1045
Down RE, Ford L, Woodhouse SD, Davison GM, Majerus MEN, Gatehouse JA, Gatehouse AMR (2003) Tritrophic interactions between transgenic potato expressing snowdrop lectin (GNA), an aphid pest (peach-potato aphid; Myzus persicae Sulz.) and a beneficial predator (2-spot ladybird; Adalia bipunctata L.). Transgenic Res 12:229–241
Du J, Foissac X, Carss A, Gatehouse AMR, Gatehouse JA (2000) Ferritin acts as the most abundant binding protein for snowdrop lectin in the midgut of rice brown planthoppers (Nilaparvata lugens). Insect Biochem Mol Biol 30:297–305
Duan XL, Hou QL, Liu GY, Pang XM, Niu ZL, Wang X, Zhang YF, Li BY, Liang RQ (2018) Expression of Pinellia pedatisecta lectin gene in transgenic wheat enhances resistance to wheat aphids. Molecules 23:748
Francis F, JlL C, Liu Y, Bosquee E (2020) Aphid feeding on plant lectins falling virus transmission rates: a multicase study. J Econ Entomol 113:1635–1639
Gatehouse AMR, Down RE, Powell KS, Sauvion N, Rahb Y, Newell CA, Merryweather A, Boulter D, Gatehouse JA (1996) Effects of GNA-expressing transgenic potato plants on peachpotato aphid, Myzus persicae. Entomol Exp Appl 79:295–307
Huang DF, Pan YH, Zhang SX, Cao JP, Yang XM, Zhang J, Yi WZ (1997) The discovery of insecticidal protein against aphids from Pinellia pedatisecta and P. ternata. Sci Agric Sin 30:94–96
Jiang X, Zhang Q, Qin YG, Yin H, Zhang SY, Li Q, Zhang Y, Fan J, Chen JL (2019) GigaScience 8:101
Jin SX, Zhang XL, Daniell H (2012) Pinellia ternate agglutinin expression in chloroplasts confers broad spectrum resistance against aphid, whitefly, lepidopteran insects, bacterial and viral pathogens. Plant Biotechnol J 10:313–327
Koch MS, Ward JM, Levine SL, Baum JA, Vicini JL, Hammond BG (2015) The food and environmental safety of Bt crops. Front Plant Sci 6:283
Konrad R, Ferry N, Gatehouse AMR, Babendreier D (2008) Potential effects of oilseed rape expressing oryzacystatin-1 (OC-1) and of purified insecticidal proteins on larvae of the solitary bee Osmia bicornis. PLoS ONE 3:e2664
Lehrman A (2007) Does pea lectin expressed transgenically in oilseed rape (Brassica napus) influence honey bee (Apis mellifera) larvae? Environ Biosafety Res 6:1–8
Li RZ, Gao WJ, Ji DP, Li CX (2000) Isolation of agglutinin from A. consarguieum and analysis on its resistance to Aphis gossypii. Acta Gossypii Sin 12:54
Macedo M, Das Graças M, Freire M, Da Silva M, Coelho L (2007) Insecticidal action of Bauhinia monandra leaf lectin (BmoLL) against Anagasta kuehniella (Lepidoptera: Pyralidae), Zabrotes subfasciatus and Callosobruchus maculatus (Coleoptera: Bruchidae). Comput Biochem Physiol A Comput Physiol 146:486–498
Macedo ML, Oliveira CF, Oliveira CT (2015) Insecticidal activity of plant lectins and potential application in crop protection. Molecules 20:2014–2033
Meihls LN, Handrick V, Glauser G, Barbier H, Kaur H, Haribal MM, Lipka AE, Gershenzon J, Buckler ES, Erb M, Köllner TG, Jander G (2013) Natural variation in maize aphid resistance is associated with 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one glucoside methyltransferase activity. Plant Cell 25:2341–2355
Mi XX, Liu X, Yan HL, Liang LN, Zhou XY, Yang JW, Si HJ, Zhang N (2017) Expression of the Galanthus nivalis agglutinin (GNA) gene in transgenic potato plants confers resistance to aphids. C R Biol 340:7–12
Miao J, Wu YQ, Xu WG, Hu L, Yu ZX, Xu QF (2011) The impact of transgenic wheat expressing GNA (snowdrop lectin) on the aphids Sitobion avenae, Schizaphis graminum, and Rhopalosiphum padi. Environ Entomol 40:743–748
Mishra A, Behura A, Mawatwal S, Kumar A, Naik L, Mohanty SS, Manna D, Dokania P, Mishra A, Patra SK, Dhiman R (2019) Structure-function and application of plant lectins in disease biology and immunity. Food Chem Toxicol 134:110827
Mohan Babu R, Sajeena A, Seetharaman K, Reddy MS (2003) Advances in genetically engineered (transgenic) plants in pest management—an over view. Crop Prot 22:1071–1086
Napoleão TH, Pontual EV, Lima TA, Santos NDL, Sá RA, Coelho LCBB, Navarro DMAF, Paiva PMG (2012) Effect of Myracrodruon urundeuva leaf lectin on survival and digestive enzymes of Aedes aegypti larvae. Parasitol Res 110:609–616
Pan L, Farouk MH, Qin GX, Zhao Y, Bao N (2018) The influences of soybean agglutinin and functional oligosaccharides on the intestinal tract of monogastric animals. Int J Mol Sci 19:554
Pan YH, Zhang SX, Cao JP, Huang DF (1998) The isolation, purification of Pinellia pedatisecta lectin and its activity on aphid-resistance. Prog Natl Sci 8:502–505
Parimala P, Ramalakshmi S, Muthuchelian K (2013) Comparative analysis of volatile constituents in Bacillus thuringiensis (Bt) cotton (RCH 2 Bt) and non-Bt cotton by gas chromatography-mass spectrometry. Afr J Agric Res 8:5093–5095
Poulsen M, Schrøder M, Wilcks A, Kroghsbo S, Lindecrona RH, Miller A, Frenzel T, Danier J, Rychlik M, Shu Q, Emami K, Taylor M, Gatehouse A, Engel KH, Knudsen I (2007a) Safety testing of GM-rice expressing PHA-E lectin using a new animal test design. Food Chem Toxicol 45:364–377
Poulsen M, Kroghsbo S, Schrøder M, Wilcks A, Jacobsen H, Miller A, Frenzel T, Danier J, Rychlik M, Shu Q, Emami K, Sudhakar D, Gatehouse A, Engel KH, Knudsen I (2007b) A 90-day safety study in Wistar rats fed genetically modified rice expressing snowdrop lectin Galanthus nivalis (GNA). Food Chem Toxicol 45:350–363
Powell KS (2001) Antimetabolic effects of plant lectins towards nymphal stages of the planthoppers Tarophagous proserpina and Nilaparvata lugens. Entomol Exp Appl 99:71–78
Powell KS, Spence J, Bharathi M, Gatehouse JA, Gatehouse AMR (1998) Immunohistochemical and developmental studies to elucidate the mechanism of action of the snowdrop lectin on the rice brown planthopper, Nilaparvata lugens (Stal). J Insect Physiol 44:529–539
Prado E, Tjallingii WF (1994) Aphid activities during sieve element punctures. Entomol Exp Appl 72:157–165
Rahbe Y, Febway G (1993) Protein toxicity to aphids: an in vitro test on Acyrthosiphon pisum. Entomol Exp Appl 67:149–160
Rahbe Y, Sauvion N, Febway G, Peumans WJ, Gatehouse AMR (1995) Toxocity of lectins and processing of ingested proteins in the pea aphid Acyrthosiphon pisum. Entomol Exp Appl 76:143–155
Sauvion N, Charles H, Febvay G, Rahbe Y (2004) Effects of jackbean lectin (ConA) on the feeding behavior and kinetics of intoxication of the pea aphid, Acyrthosiphon pisum. Entomol Exp Appl 110:31–44
Sauvion N, Rahbe Y, Peumans WJ, Van Damme EJM, Gatehouse JA, Gatehouse AMR (1996) Effects of GNA and other mannose binding lectins on development and fecundity of the peach- potato aphid Myzus persicae. Entomol Exp Appl 79:285–293
Shugart H, Ebert T, Gmitter F, Rogers M (2019) The power of electropenetrography in enhancing our understanding of host plant-vector interactions. Insects 10:407
Sprawka I, GołaAwska S, Czerniewicz P, Sytykiewicz H (2011) Insecticidal action of phytohemagglutinin (PHA) against the grain aphid, Sitobion avenae. Pestic Biochem Physiol 99:64–69
Sprawka I, GołAwska S (2010) Effect of the lectin PHA on the feeding behavior of the grain aphid. J Pest Sci 83:149–155
Sprawka I, Goławska S, Goławski A, Chrzanowski G, Czerniewicz P, Sytykiewicz H (2013) Entomotoxic action of jackbean lectin (Con A) in bird cherry-oat aphid through the effect on insect enzymes. J Plant Interact 9:425–433
Sprawka I, Goławska S, Parzych T, Goławski A, Czerniewicz P, Sytykiewicz H (2014) Mechanism of entomotoxicity of the Concanavalin A in Rhopalosiphum padi (Hemiptera: Aphididae). J Insect Sci 14:232
Vandenborre G, Miersch O, Hause B, Smagghe G, Wasternack C, Van Damme EJM (2009) Spodoptera littoralis-induced lectin expression in tobacco. Plant Cell Physiol 50:1142–1155
Van Helden M, Tjallingii WF (1993) Tissue localisation of lettuce resistance to the aphid Nasonovia ribisnigri using electrical penetration graphs. Entomol Exp Appl 68:269–278
Wei SL, Peng ZS (2003) Survey of Pinellia ternata and its adulterants. J Chin Med Mater 26:828–832
Xiao SH, Liu JG, Wu QJ, Di JC, Xu NY, Chen XS, Bai LX (2005) Identification of aphids (Aphis gossypii Glover.) resistant of cotton (Gossypium hirsutum L.) with trans-exogenous agglutinin gene. Cotton Sci 17:72–78
Yao JH, Pang YZ, Qi XH, Wan BL, Zhao XY, Kong WW, Sun XF, Tang KX (2002) Transgenic tobacco expressing Pinellia ternata agglutinin confers enhanced resistance to aphids. Transgenic Res 12:715–722
Yao JH, Zhao XY, Liao ZH, Lin J, Chen ZH, Chen F, Song J, Sun XF, Tang KX (2003) Cloning and molecular characterization of a novel lectin gene from Pinellia ternate. Cell Res 13:301–308
Yao JH, Zhao XY, Qi HX, Wan BL, Chen F, Sun XF, Yu S, Tang KX (2004) Transgenic tobacco expressing an Arisaema heterophyllum agglutinin gene displays enhanced resistance to aphids. Can J Plant Sci 84:785–790
Zhang Y, Yu XD, Tang KX, Xia LQ (2012) Generation of aphid resistant transgenic wheat with aha from Arisaema heterophyllum by Particle Bombardment. Acta Agron Sin 38:1538–1543
Zhao XY, Yao JH, Liao ZH, Zhang HY, Chen F, Wang L, Lu YQ, Sun XF, Yu SQ, Tang KX (2003) Molecular cloning of a novel mannose-binding lectin gene from Arisaema heterophyllum. Plant Sci 165:55–60
Acknowledgements
The test genetically modified wheat lines with agglutinin (PTA, AHA) genes was donated by Prof. Lanqin Xia from the Institute of Crop Sciences, Chinese Academy of Agricultural Sciences.
Funding
This research was supported by National Natural Science Foundation of China (31901881, 31871979), National Key R&D Plan in China (2017YFD0201700, 2017YFD0200900, 2016YFD0300700), State Modern Agricultural Industry Technology System (CARS-22-G-18), and China’s Donation to the CABI Development Fund.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or vertebrates performed by any of the authors.
Additional information
Communicated by Sharon Downes.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zhang, Y., Deng, Q. & Chen, J. Transgenic expression of Pinellia ternata agglutinin (PTA) and Arisaema heterophyllum agglutinin (AHA) in wheat confers resistance against the grain aphid, Sitobion miscanthi. J Pest Sci 94, 1439–1448 (2021). https://doi.org/10.1007/s10340-021-01346-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10340-021-01346-7