Abstract
Lipaphis erysimi is a key pest of rapeseed-mustard in Indian subcontinent. Although chemical control is the basis of its management, the unsustainability of this approach has accelerated global research efforts to find alternate solutions. Host plant resistance is one among these. A set of introgression lines were developed using Brassica fruticulosa previously found to be resistant to L. erysimi. Rigorous screening over the years led to the identification of 3 introgression lines (I8, I79, and I82) for field resistance to aphids. We evaluated these introgression lines under field and laboratory conditions along with B. fruticulosa (resistant parent), B. juncea var. PBR-210 (susceptible parent) to elucidate the mechanism of resistance. Significantly a smaller number of aphids settled on circular leaf discs of B. fruticulosa, I8 and I82 compared to that on PBR-210 after 24 and 48 h of release. A similar trend was observed in free choice field experiment with significantly less aphid colonization on B. fruticulosa, I8, I79 and I82 compared to PBR-210 indicating lower aphid preference for these genotypes. Further, no choice experiments revealed significant negative effects of these genotypes on aphid demographic parameters (nymphal survival, development period, fecundity and longevity). Tolerance may not be a mechanism of resistance as aphid population failed to develop on these genotypes. Thus, resistance in these introgression lines may be attributed to a synergistic combination of antixenosis and antibiosis mechanisms.
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Adhab M, Finke D, Schoelz J (2019) Turnip aphids (Lipaphis erysimi) discriminate host plants based on the strain of cauliflower mosaic virus infection. Emirates J Food Agric 31:69–75. https://doi.org/10.9755/ejfa.2019.v31.i1.1903
Adhab M, Schoelz JE (2015) Report of the turnip aphid, Lipaphis erysimi (Kaltenbach, 1843) from Missouri, USA. J Plant Prot Res 55(3):327–328. https://doi.org/10.1515/jppr-2015-0035
Agrawal N, Gupta M, Atri C, Akhatar J, Kumar S, Heslop-Harrison JS, Banga SS (2021) Anchoring alien chromosome segment substitutions bearing gene(s) for resistance to mustard aphid in Brassica juncea-B. fruticulosa introgression lines and their possible disruption through gamma irradiation. Theor Appl Genet. https://doi.org/10.1007/s00122-021-03886-z
Ahuja I, Rohloff J, Bones AM (2010) Defence mechanisms of brassicaceae: implications for plant-insect interactions and potential for integrated pest management-a review. Agron Sustain Dev 30:311–348. https://doi.org/10.1051/agro/2009025
Alvarez AE, Tjallingii WF, Garzo E, Vleeshouwers V, Dicke M, 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. https://doi.org/10.1111/j.1570-8703.2006.00464.x
Angadi SP, Singh JP, Anand IJ (1987) Inheritance of non-waxiness and tolerance to aphids in Indian mustard. J Oilseeds Res 4:265–267
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 erysimi Kalt). BMC Genet 13:104. https://doi.org/10.1186/1471-2156-13-104
Bakehetia DRC, Sandhu RS (1973) Differential response of Brassica species/varieties to the aphid (Lipaphis erysimi Kalt.) infestation. J Res PAU 10:272–279
Bakhetia DRC (1983) Losses in rapeseed and mustard due to Lipaphis erysimi (Kalt.) in India- a literature study. Proc Int Rapeseed Conf 6:16–22
Bhatia V, Uniyal PL, Bhattacharya RC (2011) Aphid resistance in Brassica crops: challenges, biotechnological progress and emerging possibilities. Biotechnol Adv 29:879–888. https://doi.org/10.1016/j.biotechadv.2011.07.005
Blackman RL, Eastop VF (1984) Aphids on the World’s Crops. John Wiley, Chichester, UK, p 466p
Canassa VF, Baldin ELL, Lourenção AL, Barros DRP, Lopes NP, Sartori MMP (2020) Feeding behavior of Brevicoryne brassicae in resistant and susceptible collard greens genotypes: interactions among morphological and chemical factors. Entomol Exp Appl 168:228–239. https://doi.org/10.1111/eea.12897
Canassa VF, Baldin ELL, Sacilotto MG, Barros DRP, Lopes NP, Sartori MMP (2021) Assessing the resistance of collard greens genotypes to the cabbage aphid (Brevicoryne brassicae) (Hemiptera: Aphididae). Phytoparasitica. https://doi.org/10.1007/s12600-021-00882-3
Chandra A, Gupta ML, Banga SS, Banga SK (2004) Production of an interspecific hybrid between Brassica fruticulosa and B. rapa. Plant Breed 123:497–498. https://doi.org/10.1111/j.1439-0523.2004.01007.x
Chatterjee SD, Sengupta K (1987) Observations on reaction of mustard aphid to white petal and glossy plants of Indian mustard. J Oilseeds Res 4:125–127
Chongtham R, Waikhom S, Kumar A, Goel S, Agarwal M, Jagannath A (2017) Evaluation of different hosts and laboratory conditions for rearing of the mustard aphid (Lipaphis erysimi) and their use for screening of aphid resistant transgenic plants of the oilseed crop, Brassica juncea (Indian mustard). Vegetos (spl Issue). 30:185–190. https://doi.org/10.5958/2229-4473.2017.00058.1
Cole RA (1994) Locating a resistance mechanism to the cabbage aphid in two wild Brassicas. Entomol Exp Appl 71:23–31. https://doi.org/10.1111/j.1570-7458.1994.tb01766.x
Dosdall LM, Kott LS (2006) Introgression of resistance to cabbage seed pod weevil to canola from yellow mustard. Crop Breed Genet 46:2437–2445. https://doi.org/10.2135/cropsci2006.02.0132
Ellis PR, Farrell JA (1995) Resistance to cabbage aphid (Brevicoryne brassicae) in six Brassica accessions in New Zealand. New Zealand J Crop Hortic Sci 23:25–29. https://doi.org/10.1080/01140671.1995.9513864
El-Wakeil, Gaafar N, Sallam A, Volkmar C (2013) Side effects of insecticides on natural enemies and possibility of their integration in plant protection strategies. In: Stanislav Trdan (Ed.) Insecticides: Development of safer and more effective technologies. IntechOpen. Doi https://doi.org/10.5772/54199
Giordanengo P, Brunissen L, Rusterucci C, Vincent C, van Bel A, Dinant S, Girousse C, Faucher M, Bonnemain JL (2010) Compatible plant-aphid interactions: how aphids manipulate plant responses. C R Biol 333(6–7):516–523. https://doi.org/10.1016/j.crvi.2010.03.007
Girousse C, Bournoville R (1994) Role of phloem sap quality and exudation characteristics on performance of pea aphid grown on lucerne genotypes. Entomol Exp Appl 70:227–235. https://doi.org/10.1111/j.1570-7458.1994.tb00751.x
Goggin FL (2007) Plant-aphid interactions: molecular and ecological perspectives. Curr Opin Plant Biol 10:399–408. https://doi.org/10.1016/j.pbi.2007.06.004
Gupta M, Banga SS (2020) Exploiting alien genetic variation for germplasm enhancement in Brassica oilseeds. In: Kang MS (ed) Quantitative genetics, genomics and plant breeding. CABI Publishing Wallingford, Oxon, pp 338–384. https://doi.org/10.1079/9781789240214.0338
Heil M (2014) Herbivore induced plant volatiles: targets, perception and unanswered questions. New Phytol 204:297–306. https://doi.org/10.1111/nph.12977
Hondelmann P, Paul C, Schreiner M, Meyhofer R (2020) Importance of antixenosis and antibiosis resistance to the cabbage whitefly (Aleyrodes prolettela) in Brussels sprout cultivars. Insects 11:56. https://doi.org/10.3390/insects11010056
Jaouannet M, Rodriguez PA, Thorpe P, Lenoir CJG, MacLeod R, Martinez CE, Bos JIB (2014) Plant immunity in plant-aphid interactions. Front Plant Sci. https://doi.org/10.3389/fpls.2014.00663
Kalra VK, Singh H, Rohilla HR (1987) Influence of various genotypes of Brassica juncea on biology of mustard aphid, Lipaphis erysimi (Kalt.). Indian J Agric Sci 57:277–279
Kennedy JS, Day MF, Eastop VF (1962) A conspectus of aphids as vectors of plant viruses. Commonwealth Institute of Entomology, London, UK
Klingauf FA (1987) Host plant finding and acceptance. In: Minks AK, Harrewijn P (eds) Aphids: Their biology, natural enemies and control, vol 2A. Elsevier, Amsterdam, pp 209–223
Kloth KJ, ten Broeke CJM, Thoen MPM, van den Brink MH, Wiegers GL, Krips OE, Noldus LPJJ, Dicke M, Jongsma MA (2015) High-throughput phenotyping of plant resistance to aphids by automated video tracking. Plant Methods 11:4. https://doi.org/10.1186/s13007-015-0044-z
Kuhlmann F, Opitz SEW, Inselsbacher E, Ganeteg U, Nasholm T, Ninkovic V (2013) Exploring the nitrogen ingestion of aphids-a new method using electrical penetration graph and 15N labelling. PLoS ONE. 2013;8:e83085 doi:https://doi.org/10.1371/journal.pone.0083085
Kular JS, Kumar S (2011) Quantification of avoidable yield losses in oilseed Brassica caused by insect pests. J Plant Prot Res 51:38–43. https://doi.org/10.2478/v10045-011-0007-y
Kumar S (2019) Aphid-plant interactions: implications for pest management. In: Manuel Oliveira, Anabela Fernandes-Silva, Feyza Candan (eds.) Plant Communities and their environment. Intech Open UK. doi: https://doi.org/10.5772/intechopen.84302
Kumar S, Atri C, Sangha MK, Banga SS (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. https://doi.org/10.1007/s10681-011-0351-z
Kumar S, Banga SS (2017) Breeding for aphid resistance in rapeseed-mustard. In: R Arora, S Sandhu (eds.) Breeding insect resistant crops for sustainable agriculture. SpringerNature Singapore Pte Ltd, pp 171–199 doi:https://doi.org/10.1007/978-981-10-6056-4_6
Kumar S, Singh YP (2015) Insect Pests. In: Kumar A, Banga SS, Meena PD, Kumar PR (eds) Brassica oilseeds breeding and their management. CABI, UK, pp 193–232
Le Roux V, Dugravot S, Campan E, Dubois F, Vincent C, Giordanengo P (2008) Wild Solanum resistance to aphids: antixenosis or antibiosis? J Econ Entomol 101:584–591. https://doi.org/10.1093/jee/101.2.584
Malik RS, Anand IJ (1984) Effect of aphid infestation on the oil yielding attributes in Brassica. J Oilseeds Res 1:147–155
Mphosi MS, Foster SP (2010) Female preference and larval performance of sunflower moth, Homoeosoma electellum, on sunflower pre-breeding lines. Entomol Exp Appl 134:182–190. https://doi.org/10.1111/j.1570-7458.2009.00949.x
Novak NG, Perez FG, Jones RW, Lawrence SD (2019) Detached leaf assays to simplify gene expression studies in potato during infestation by chewing insect Menduca sexta. J vis Exp 15:147. https://doi.org/10.3791/59153
Palial S (2017) Mechanism of introgressed resistance in Brassica juncea against Lipaphis erysimi (Kaltenbach). MSc Thesis, Punjab Agricultural University, Ludhiana, India, 77p
Palial S, Kumar S, Sharma S (2018) Biochemical changes in Brassica juncea-fruticulosa introgression lines after Lipaphis erysimi (Kaltenbach) infestation. Phytoparasitica 46:499–509. https://doi.org/10.1007/s12600-018-06
Pettersson J, Tjallingii WF, Hardie J (2007) Host-plant selection and feeding. In: van Emden H, Harrington R (eds) Aphids as crop pests. CAB International, Cromwell Press, Trowbridge, UK, pp 87–114. https://doi.org/10.1079/9780851998190.0115
Pink DAC, Kift NB, Ellis PR, Mcclement SJ, Lynn J, Tatchell MG (2008) Genetic control of resistance to the aphid Brevicoryne brassicae in the wild species Brassica fruticulosa. Plant Breed 122:24–29. https://doi.org/10.1046/j.1439-0523.2003.00777.x
Powell G, Tosh CR, Hardie J (2006) Host plant selection by aphids: behavioral, evolutionary, and applied perspectives. Ann Rev Entomol 51:309–330. https://doi.org/10.1146/annurev.ento.51.110104.151107
Rana J (2005) Performance of Lipaphis erysimi (Homoptera: Aphididae) on different Brassica species in a tropical environment. J Pest Sci 78:155–160. https://doi.org/10.1007/s10340-005-0088-3
Rohilla HR, Singh H, Singh R (1999) Evaluation of rapeseed-mustard genotypes against mustard aphid, Lipaphis erysimi (Kalt.): test of agrochemicals and cultivars no. 20. Ann Appl Biol 134:42–43
Santolamazza-Carbone S, Velasco P, Soengas P, Cartea ME (2014) Botton-up and top-down herbivore regulation mediated by glucosinolates in Brassica oleracea var. acephala. Oecologia 174:893–907. https://doi.org/10.1007/s00442-013-2817-2
SAS Institute 2005. SAS/Stat Software: Version 9.1. SAS Institute, Cary, NC
Shankar M, Sharma HC, Babu TR, Sridevi D (2013) Evaluation of no-choice cage, detached leaf and diet incorporation assays to screen chickpeas for resistance to the beet armyworm Spodoptera exigua (Lepidoptera: Noctuidae). Int J Tropical Insect Sci 34(1):22–31. https://doi.org/10.1017/S1742758413000374
Sharma HC, Pampapathy G, Dhillon MK, Ridsdill-Smith JT (2005) Detached leaf assay to screen for host plant resistance to Helicoverpa armigera. J Econ Entomol 98(2):568–576. https://doi.org/10.1093/jee/98.2.568
Sharma HC (2008) Biotechnological approaches for pest management and ecological sustainability. CRC Press, New York, p 526. https://doi.org/10.1201/9781420088489
Singh R, Ellis PR, Pink DAC, Phelps K (1994) An investigation of the resistance to cabbage aphid in brassica species. Ann Appl Biol 125:457–465. https://doi.org/10.1111/j.1744-7348.1994.tb04983.x
Smith CM (2005) Plant resistance to arthropods: molecular and conventional approaches. Springer Press, Dordrecht, The Netherlands, p 413p. https://doi.org/10.1007/1-4020-3702-3
SOPA (2020) India oilseeds-Area, production and productivity. The soybean processors association of India. http://www.sopa.org/india-oilseeds-area-production-and-productivity/ (Date of access: December 5, 2020)
Stapel JO, Cortesero AM, Lew WJ (2000) Disruptive sublethal effects of insecticides on biological control: altered foraging ability and life span of a parasitoid after feeding on extrafloral nectar of cotton treated with systemic insecticides. Bio Con 17:243–249. https://doi.org/10.1006/bcon.1999.0795
Sun M, Voorrips RE, Steenhuis-Broers G, Westende WV, Vosman B (2018) Reduced phloem uptake of Myzus persicae on an aphid resistant pepper accession. BMC Plant Biol 18:138. https://doi.org/10.1186/s12870-018-1340-3
Teotia TPS, Lal OP (1970) Differential response of different varieties and strains of oleiferous brassica to aphid, Lipaphis erysimi (Kalt.). Labdev J Sci Tech 8:219–226
Ulusoy MR, Olmez-Bayhan S (2006) Effect of certain brassica plants on biology of the cabbage aphid Brevicoryne brassicae under laboratory conditions. Phytoparasitica 34:133–138. https://doi.org/10.1007/BF02981313
USDA (2020) Oilseeds: World markets and Trade. United States Department of Agriculture https://www.fas.usda.gov/data/oilseeds-world-markets-and-trade (Date of access: December 5, 2020)
Visser JH, Piron PGM (1997) Olfactory antennal responses to plant volatiles in apterous virginoparae of the vetch aphid Megoura viciae. Ent Exp Appl 77:37–46. https://doi.org/10.1111/j.1570-7458.1995.tb01983.x
White JA, Whitham TG (2000) Associational susceptibility of cottonwood to a box elder herbivore. Ecol 81:1795–1803. https://doi.org/10.1890/0012-9658(2000)081[1795:ASOCTA]2.0.CO;2
Wójcicka A (2015) Surface waxes as a plant defense barrier towards grain aphid. Acta Biol Cracov Ser Bot 57:95–103. https://doi.org/10.1515/abcsb-2015-0012
Xi C, Vosman B, Visser RGF, van der Vlugt RAA, Broekgarden C (2012) High throughput phenotyping for aphid resistance in large plant collections. Plant Methods 8:33. https://doi.org/10.1186/1746-4811-8-33
Yadava AK, Singh H, Yadava TP (1985) Inheritance of nonwaxy trait in Indian mustard and its reaction to aphids. J Oilseeds Res 2:339–342
Zhang F, Batley J (2020) Exploring the application of wild species for crop improvement in a changing climate. Curr Opin Plant Biol 56:218–222. https://doi.org/10.1016/j.pbi.2019.12.013
Zhang K, Zhang W, Zhang S, Wu SF, Ban LF, Su JY, Gao CF (2014a) Susceptibility of Sogatella furcifera and Laodelphax striatellus (Hemiptera: Delphacidae) to six insecticides in China. J Econ Entomol 107:1916–1922. https://doi.org/10.1603/EC14156
Zhang XL, Liu XY, Zhu FX, Li JH, You H, Lu P (2014b) Field evolution of insecticide resistance in the brown plant hopper Nilaparvata lugens (Stal) in China. Crop Prot 58:61–66. https://doi.org/10.1016/j.cropro.2013.12.026
Acknowledgements
The studies were financially supported by the PAU centre of All India Coordinated Research Project on Rapeseed-Mustard. Germplasm used for the studies was developed with financial assistance from Indian Council of Agricultural Research under ICAR National Professor Project “Broadening the genetic base of Indian mustard (Brassica juncea) through alien introgressions and germplasm enhancement”.
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Palial, S., Kumar, S., Atri, C. et al. Antixenosis and antibiosis mechanisms of resistance to turnip aphid, Lipaphis erysimi (Kaltenbach) in Brassica juncea-fruticulosa introgression lines. J Pest Sci 95, 749–760 (2022). https://doi.org/10.1007/s10340-021-01418-8
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DOI: https://doi.org/10.1007/s10340-021-01418-8