Abstract
MEAM1 (Middle East-Asia Minor 1) and MED (Mediterranean), two cryptic species of the Bemisia tabaci species complex, are highly destructive herbivores worldwide. Attack by herbivorous insects often induces plant defense responses that deter herbivores, recruit natural enemies, or warn other plants of possible herbivore attack. However, recent studies found that herbivores can manipulate and suppress plant defenses for their own benefit. These responses, which differ depending on the herbivore and the plant species, may mediate the preference and performance of later-arriving con- and heterospecific herbivores that attack the same plant. Here, we found that MEAM1 whiteflies preferred to settle and oviposit on MED-infested pepper and avoided conspecific-infested pepper plants. In contrast, MED whiteflies preferred to settle and oviposit on non-infested rather than on MEAM1-infested pepper. MEAM1 infestation significantly increased the contents of JA in pepper plants, which coincided with the increased expression of the following genes in the JA biosynthesis pathway: FAD, LOX6, OPR3, and PDF1.2. MED infestation significantly increased the contents of ABA in pepper plants and reduced the expression of PR1 and NPR1 in the SA biosynthesis pathway. Although MEAM1 infestation increased the transcript levels of C4H, 4CL1, CHS, and CHI3 in the phenylpropanoid biosynthesis pathway, total phenol levels did not increase. The reduction of the total phenols in pepper previously infested by MED, probably contributed to the settling and oviposition preference of the later-arriving heterospecific MEAM1. Overall, these results demonstrate that previous infestation by MEAM1 and MED whiteflies induces different responses in pepper plants that shape the host preference and performance of the later-arriving con- and heterospecific whiteflies.
Similar content being viewed by others
Availability of data and materials
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Agrawal AA, Weber MG (2015) On the study of plant defence and herbivory using comparative approaches: how important are secondary plant compounds. Ecol Lett 18:985–991. https://doi.org/10.1111/ele.12482
Alba JM, Schimmel BCJ, Glas JJ, Ataide LMS, Pappas ML, Villarroel CA, Schuurink RC, Sabelis MW, Kant MR (2015) Spider mites suppress tomato defenses downstream of jasmonate and salicylate independently of hormonal crosstalk. New Phytol 205:828–840. https://doi.org/10.1111/nph.13075
Ali JG, Agrawal AA (2012) Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci 17:293–302
Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, Ehlert C, Maclean DJ, Ebert PR, Kazan K (2004) Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 16:3460–3479. https://doi.org/10.1105/tpc.104.025833
Arimura G, Matsui K, Takabayashi J (2009) Chemical and molecular ecology of herbivore-induced plant volatiles: proximate factors and their ultimate functions. Plant Cell Physiol 50:911–923. https://doi.org/10.1093/pcp/pcp030
Awmack CS, Leather SR (2002) Host plant quality and fecundity in herbivorous insects. Annu Rev Entomol 47:817–844. https://doi.org/10.1146/annurev.ento.47.091201.145300
Bai YC, Yang CQ, Halitschke R, Paetz C, Kessler D, Burkard K, Gaquerel E, Baldwin IT, Li DP (2022) Natural history-guided omics reveals plant defensive chemistry against leafhopper pests. Science. https://doi.org/10.1126/science.abm2948
Beckers GJM, Spoel SH (2006) Fine-tuning plant defence signalling: salicylate versus jasmonate. Plant Biol 8:1–10. https://doi.org/10.1055/s-2005-872705
Beran F, Köllner TG, Gershenzon J, Tholl D (2019) Chemical convergence between plants and insects: biosynthetic origins and functions of common secondary metabolites. New Phytol 223:52–67. https://doi.org/10.1111/nph.15718
Boeckler GA, Gershenzon J, Unsicker SB (2011) Phenolic glycosides of the Salicaceae and their role as anti-herbivore defenses. Phytochemistry 72:1497–1509. https://doi.org/10.1016/j.phytochem.2011.01.038
Borevitz JO, Xia YJ, Blount J, Dixon RA, Lamb C (2000) Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell 12:2383–2393. https://doi.org/10.1105/tpc.12.12.2383
Chen MS (2008) Inducible direct plant defense against insect herbivores: a review. Insect Sci 15:101–114. https://doi.org/10.1111/j.1744-7917.2008.00190.x
Chu D, Liu GX, Fan ZX, Tao YL, Zhang YJ (2007) Genetic differentiation of different geographical populations of Bemisia tabaci (Gennadius) complex. Agricultural Sciences in China 6:696–705. https://doi.org/10.1016/S1671-2927(07)60102-3
Cui HY, Guo LT, Wang SL, Xie W, Jiao XG, Wu QJ, Zhang YJ (2017) The ability to manipulate plant glucosinolates and nutrients explains the better performance of Bemisia tabaci Middle East-Asia Minor 1 than Mediterranean on cabbage plants. Ecol Evol 7:6141–6150. https://doi.org/10.1002/ece3.2921
Daglia M (2012) Polyphenols as antimicrobial agents. Curr Opin Biotech 23:174–181. https://doi.org/10.1016/j.copbio.2011.08.007
De Barro PJ, Liu SS, Boykin LM, Dinsdale AB (2011) Bemisia tabaci: a statement of species status. Annu Rev Entomol 56:1–19. https://doi.org/10.1146/annurev-ento-112408-085504
De Geyter N, Gholami A, Goormachtig S, Goossens A (2012) Transcriptional machineries in jasmonate-elicited plant secondary metabolism. Trends Plant Sci 17:349–359. https://doi.org/10.1016/j.tplants.2012.03.001
De Vos M, Van Oosten VR, Van Poecke RMP, Van Pelt JA, Pozo MJ, Mueller MJ, Buchala AJ, Métraux J, Van Loon LC, Dicke M, Pieterse CMJ (2005) Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol Plant Microbe Interact 18:923–937. https://doi.org/10.1094/MPMI-18-0923
de Oliveira EF, Pallini A, Janssen A (2016) Herbivores with similar feeding modes interact through the induction of different plant responses. Oecologia 180:1–10. https://doi.org/10.1007/s00442-015-3344-0
Dinsdale A, Cook L, Riginos C, Buckley YM, De Barro P (2010) Refined global analysis of Bemisia tabaci (Hemiptera: Sternorrhyncha: Aleyrodoidea: Aleyrodidae) mitochondrial cytochrome oxidase 1 to identify species level genetic boundaries. Ann Entomol Soc Am 103:196–208. https://doi.org/10.1603/AN09061
Dudareva N, Klempien A, Muhlemann JK, Kaplan I (2013) Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytol 198:16–32. https://doi.org/10.1111/nph.12145
Eisenring M, Glauser G, Meissle M, Romeis J (2018) Differential impact of herbivores from three feeding guilds on systemic secondary metabolite induction, phytohormone levels and plant-mediated herbivore interactions. J Chem Ecol 44:1178–1189. https://doi.org/10.1007/s10886-018-1015-4
Erb M, Robert CAM, Hibbard BE, Turlings TCJ (2011) Sequence of arrival determines plant-mediated interactions between herbivores. J Ecol 99:7–15. https://doi.org/10.1111/j.1365-2745.2010.01757.x
Erb M, Meldau S, Howe GA (2012) Role of phytohormones in insect-specific plant reactions. Trends Plant Sci 17:250–259. https://doi.org/10.1016/j.tplants.2012.01.003
Esterhuizen LL, Mabasa KG, van Heerden SW, Czosnek H, Brown JK, van Heerden H, Rey MEC (2013) Genetic identification of members of the Bemisia tabaci cryptic species complex from South Africa reveals native and introduced haplotypes. J Appl Entomol 137:122–135. https://doi.org/10.1111/j.1439-0418.2012.01720.x
Ferrero M, Pagliarani C, Novák O, Ferrandino A, Cardinale F, Visentin I, Schubert A (2018) Exogenous strigolactone interacts with abscisic acid-mediated accumulation of anthocyanins in grapevine berries. J Exp Bot 69:2391–2401. https://doi.org/10.1093/jxb/ery033
Florencio-Ortiz V, Novák O, Casas JL (2020) Phytohormone responses in pepper (Capsicum annuum L.) leaves under a high density of aphid infestation. Physiol Plant 170:519–527. https://doi.org/10.1111/ppl.13188
Frost CJ, Mescher MC, Carlson JE, De Moraes CM (2008) Plant defense priming against herbivores: getting ready for a different battle. Plant Physiol 146:818–824. https://doi.org/10.1104/pp.107.113027
Fu ZQ, Dong XN (2013) Systemic acquired resistance: turning local infection into global defense. Annu Rev Plant Biol 64:839–863. https://doi.org/10.1146/annurev-arplant-042811-105606
Glas JJ, Alba JM, Simoni S, Villarroel CA, Stoops M, Schimmel BCJ, Schuurink RC, Sabelis MW, Kant MR (2014) Defense suppression benefits herbivores that have a monopoly on their feeding site but can backfire within natural communities. BMC Biol 12:1–14. https://doi.org/10.1186/s12915-014-0098-9
Hilker M, Meiners T (2010) How do plants “notice” attack by herbivorous arthropods? Biol Rev 85:267–280. https://doi.org/10.1111/j.1469-185X.2009.00100.x
Hillwig MS, Chiozza M, Casteel CL, Lau ST, Hohenstein J, Hernández E, Jander G, MacIntosh GC (2016) Abscisic acid deficiency increases defence responses against Myzus persicae in Arabidopsis. Mol Plant Pathol 17:225–235. https://doi.org/10.1111/mpp.12274
Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66. https://doi.org/10.1146/annurev.arplant.59.032607.092825
Hu J, Lu JT, Yang NN, Liu BM, Fu PY, Yang JJ, Zhang YJ, Jiao XG (2022) Avoidance of previously infested cabbage by MEAM1 cryptic species of Bemisia tabaci species complex. J Pest Sci. https://doi.org/10.1007/s10340-022-01480-w
Huang W, Siemann E, Xiao L, Yang XF, Ding JQ (2014) Species-specific defence responses facilitate conspecifics and inhibit heterospecifics in above-belowground herbivore interactions. Nat Commun 5:1–9. https://doi.org/10.1038/ncomms5851
Huang J, Reichelt M, Chowdhury S, Hammerbacher A, Hartmann H (2017) Increasing carbon availability stimulates growth and secondary metabolites via modulation of phytohormones in winter wheat. J Exp Bot 68:1251–1263. https://doi.org/10.1093/jxb/erx008
Inbar M, Gerling D (2008) Plant-mediated interactions between whiteflies, herbivores, and natural enemies. Annu Rev Entomol 53:431–448. https://doi.org/10.1146/annurev.ento.53.032107.122456
Jassbi AR, Gase K, Hettenhausen C, Schmidt A, Baldwin IT (2008) Silencing geranylgeranyl diphosphate synthase in Nicotiana attenuata dramatically impairs resistance to tobacco hornworm. Plant Physiol 146:974–986. https://doi.org/10.1104/pp.107.108811
Ji R, Fu JM, Shi Y, Li J, Jing MF, Wang L, Yang SY, Tian T, Wang LH, Ju JF, Guo HF, Liu B, Dou DL, Hoffmann AA, Zhu-Salzman K, Fang JC (2021) Vitellogenin from planthopper oral secretion acts as a novel effector to impair plant defenses. New Phytol 232:802–817. https://doi.org/10.1111/nph.17620
Jiang YJ, Zhang CX, Chen RZ, He SY (2019) Challenging battles of plants with phloem-feeding insects and prokaryotic pathogens. Proc Natl Acad Sci USA 116:23390–23397. https://doi.org/10.1073/pnas.1915396116
Jiao XG, Xie W, Wang SL, Wu QJ, Zhou L, Pan HP, Liu BM, Zhang YJ (2012) Host preference and nymph performance of B and Q putative species of Bemisia tabaci on three host plants. J Pest Sci 85:423–430. https://doi.org/10.1007/s10340-012-0441-2
Jiao XG, Xie W, Guo LT, Liu BM, Wang SL, Wu QJ, Zhang YJ (2014) Differing effects of cabbage and pepper on B and Q putative species of Bemisia tabaci. J Pest Sci 87:629–637. https://doi.org/10.1007/s10340-014-0594-2
Kaplan I, Halitschke R, Kessler A, Sardanelli S, Denno RF (2008) Constitutive and induced defenses to herbivory in above- and belowground plant tissues. Ecology 89:392–406. https://doi.org/10.1890/07-0471.1
Karban R, Agrawal AA (2002) Herbivore offense. Annu Rev Ecol Syst 33:641–664. https://doi.org/10.1146/annurev.ecolsys.33.010802.150443
Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, Chicago. https://doi.org/10.1016/s0169-5347(97)01267-6
Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev Plant Biol 53:299–328. https://doi.org/10.1146/annurev.arplant.53.100301.135207
Kessler A, Kalske A (2018) Plant secondary metabolite diversity and species interactions. Annu Rev Ecol Evol Syst 49:115–138. https://doi.org/10.1146/annurev-ecolsys-110617-062406
Kessler A, Halitschke R, Baldwin IT (2004) Silencing the jasmonate cascade: induced plant defenses and insect populations. Science 305:665–668. https://doi.org/10.1126/science.1096931
Koornneef A, Pieterse CMJ (2008) Cross talk in defense signaling. Plant Physiol 146:839–844. https://doi.org/10.1104/pp.107.112029
Li P, Shu YN, Fu S, Liu YQ, Zhou XP, Liu SS, Wang XW (2017) Vector and nonvector insect feeding reduces subsequent plant susceptibility to virus transmission. New Phytol 215:699–710. https://doi.org/10.1111/nph.14550
Li JC, Halitschke R, Li DP, Paetz C, Su HC, Heiling S, Xu SQ, Baldwin IT (2021) Controlled hydroxylations of diterpenoids allow for plant chemical defense without autotoxicity. Science 371:255–260. https://doi.org/10.1126/science.abe4713
Liu LJ, Sonbol F, Huot B, Gu YN, Withers J, Mwimba M, Yao J, He SY, Dong XN (2016) Salicylic acid receptors activate jasmonic acid signalling through a non-canonical pathway to promote effector-triggered immunity. Nat Commun 7:1–10. https://doi.org/10.1038/ncomms13099
Ma DW, Constabel CP (2019) MYB repressors as regulators of phenylpropanoid metabolism in plants. Trends Plant Sci 24:275–289. https://doi.org/10.1016/j.tplants.2018.12.003
Mauch-Mani B, Baccelli I, Luna E, Flors V (2017) Defense priming: an adaptive part of induced resistance. Annu Rev Plant Biol 68:485–512. https://doi.org/10.1146/annurev-arplant-042916-041132
Mithöfer A, Boland W (2012) Plant defense against herbivores: chemical aspects. Annu Rev Plant Biol 63:431–450. https://doi.org/10.1146/annurev-arplant-042110-103854
Moreira X, Abdala-Roberts L, Castagneyrol B (2018) Interactions between plant defence signalling pathways: Evidence from bioassays with insect herbivores and plant pathogens. J Ecol 106:2353–2364. https://doi.org/10.1111/1365-2745.12987
Mur LAJ, Kenton P, Atzorn R, Miersch O, Wasternack C (2006) The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiol 140:249–262. https://doi.org/10.1104/pp.105.072348
Nahar K, Kyndt T, Nzogela YB, Gheysen G (2012) Abscisic acid interacts antagonistically with classical defense pathways in rice-migratory nematode interaction. New Phytol 196:901–913. https://doi.org/10.1111/j.1469-8137.2012.04310.x
Oliveira MRV, Henneberry TJ, Anderson P (2001) History, current status, and collaborative research projects for Bemisia tabaci. Crop Prot 20:709–723. https://doi.org/10.1016/S0261-2194(01)00108-9
Pan HP, Chu D, Yan WQ, Su Q, Liu BM, Wang SL, Wu QJ, Xie W, Jiao XG, Li RM, Yang NN, Yang X, Xu BY, Brown JK, Zhou XG, Zhang YJ (2012) Rapid spread of tomato yellow leaf curl virus in China is aided differentially by two invasive whiteflies. PLoS ONE 7:e34817. https://doi.org/10.1371/journal.pone.0034817
Pentzold S, Zagrobelny M, Rook F, Bak S (2014) How insects overcome two-component plant chemical defence: plant β-glucosidases as the main target for herbivore adaptation. Biol Rev 89:531–551. https://doi.org/10.1111/brv.12066
Pieterse CMJ, Dicke M (2007) Plant interactions with microbes and insects: from molecular mechanisms to ecology. Trends Plant Sci 12:564–569. https://doi.org/10.1016/j.tplants.2007.09.004
Poelman EH, Dicke M (2014) Plant-mediated interactions among insects within a community ecological perspective. Annu Plant Rev 47:309–337. https://doi.org/10.1111/j.1365-294X.2008.03838.x
Poelman EH, Broekgaarden C, Van Loon JJA, Dicke M (2008) Early season herbivore differentially affects plant defence responses to subsequently colonizing herbivores and their abundance in the field. Mol Ecol 17:3352–3365. https://doi.org/10.1111/j.1365-294X.2008.03838.x
Poreddy S, Mitra S, Schöttner M, Chandran J, Schneider B, Baldwin IT, Kumar P, Pandit SS (2015) Detoxification of hostplant’s chemical defence rather than its anti-predator co-option drives β-glucosidase-mediated lepidopteran counteradaptation. Nat Commun 6:1–13. https://doi.org/10.1038/ncomms9525
Roumani M, Besseau S, Gagneul D, Robin C, Larbat R (2021) Phenolamides in plants: An update on their function, regulation, and origin of their biosynthetic enzymes. J Exp Bot 72:2334–2355. https://doi.org/10.1093/jxb/eraa582
Sarmento RA, Lemos F, Bleeker PM, Schuurink RC, Pallini A, Oliveira MGA, Lima ER, Kant R, Sabelis MW, Janssen A (2011) A herbivore that manipulates plant defence. Ecol Lett 14:229–236. https://doi.org/10.1111/j.1461-0248.2010.01575.x
Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101–1108. https://doi.org/10.1038/nprot.2008.73
Schuman MC, Baldwin IT (2016) The layers of plant responses to insect herbivores. Annu Rev Entomol 61:373–394. https://doi.org/10.1146/annurev-ento-010715-023851
Siemens DH, Garner SH, Mitchell-Olds T, Callaway RM (2002) Cost of defense in the context of plant competition: Brassica rapa may grow and defend. Ecology 83:505–517. https://doi.org/10.1890/0012-9658(2002)083[0505:CODITC]2.0.CO;2
Silva DB, Jiménez A, Urbaneja A, Pérez-Hedo M, Bento JMS (2021) Changes in plant responses induced by an arthropod influence the colonization behavior of a subsequent herbivore. Pest Manag Sci 77:4168–4180. https://doi.org/10.1002/ps.6454
Stam JM, Kroes A, Li YH, Gols R, van Loon JJA, Poelman EH, Dicke M (2014) Plant interactions with multiple insect herbivores: from community to genes. Annu Rev Plant Biol 65:689–713. https://doi.org/10.1146/annurev-arplant-050213-035937
Su Q, Chen G, Mescher MC, Peng ZK, Xie W, Wang SL, Wu QJ, Liu J, Li CR, Wang WK, Zhang YJ (2018) Whitefly aggregation on tomato is mediated by feeding-induced changes in plant metabolites that influence the behaviour and performance of conspecifics. Funct Ecol 32:1180–1193. https://doi.org/10.1111/1365-2435.13055
Su Q, Peng ZK, Tong H, Xie W, Wang SL, Wu QJ, Zhang JM, Li CR, Zhang YJ (2019) A salivary ferritin in the whitefly suppresses plant defenses and facilitates host exploitation. J Exp Bot 70:3343–3355. https://doi.org/10.1093/jxb/erz152
Thaler JS, Humphrey PT, Whiteman NK (2012) Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 17:260–270. https://doi.org/10.1016/j.tplants.2012.02.010
van de Ven WTG, LeVesque CS, Perring TM, Walling LL (2000) Local and systemic changes in squash gene expression in response to silverleaf whitefly feeding. Plant Cell 12:1409–2142. https://doi.org/10.1105/tpc.12.8.1409
VanDoorn A, de Vries M, Kant MR, Schuurink RC (2015) Whiteflies glycosylate salicylic acid and secrete the conjugate via their honeydew. J Chem Ecol 41:52–583. https://doi.org/10.1007/s10886-014-0543-9
Viswanathan DV, Lifchits OA, Thaler JS (2007) Consequences of sequential attack for resistance to herbivores when plants have specific induced responses. Oikos 116:1389–1399. https://doi.org/10.1111/j.0030-1299.2007.15882.x
Walker GP, Perring TM, Freeman TP (2010) Life history, functional anatomy, feeding and mating behavior. In: Stansly PA, Naranjo SE (eds) Bemisia: Bionomics and management of a global pest, 1st edn. Springer, New York, pp 109–160. https://doi.org/10.1007/978-90-481-2460-2_4
Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195–216. https://doi.org/10.1007/s003440000026
Walling LL (2008) Avoiding effective defenses: strategies employed by phloem-feeding insects. Plant Physiol 146:859–866. https://doi.org/10.1104/pp.107.113142
Wang XW, Luan JB, Li JM, Su YL, Xia J, Liu SS (2011) Transcriptome analysis and comparison reveal divergence between two invasive whitefly cryptic species. BMC Genomics 12:458. https://doi.org/10.1186/1471-2164-12-458
Wang XW, Li P, Liu SS (2017) Whitefly interactions with plants. Curr Opin Insect Sci 19:70–75. https://doi.org/10.1016/j.cois.2017.02.001
Wang JJ, Wu DW, Wang YP, Xie DX (2019a) Jasmonate action in plant defense against insects. J Exp Bot 70:3391–3400. https://doi.org/10.1093/jxb/erz174
Wang N, Zhao PZ, Ma YH, Yao XM, Sun YW, Huang XD, Jin JJ, Zhang YJ, Zhu CX, Fang RX, Ye J (2019b) A whitefly effector Bsp9 targets host immunity regulator WRKY33 to promote performance. Philos Trans R Soc Lond B Biol Sci 374:20180313. https://doi.org/10.1098/rstb.2018.0313
Wittstock U, Gershenzon J (2002) Constitutive plant toxins and their role in defense against herbivores and pathogens. Curr Opin Plant Biol 5:300–307. https://doi.org/10.1016/s1369-5266(02)00264-9
Wu JQ, Baldwin IT (2009) Herbivory-induced signalling in plants: perception and action. Plant Cell Environ 32:1161–1174. https://doi.org/10.1111/j.1365-3040.2009.01943.x
Xia JX, Guo ZJ, Yang ZZ, Han HL, Wang SL, Xu HF, Yang X, Yang FS, Wu QJ, Xie W, Zhou XG, Dermauw W, Turlings TCJ, Zhang YJ (2021) Whitefly hijacks a plant detoxification gene that neutralizes plant toxins. Cell 184:1693–1705. https://doi.org/10.1016/j.cell.2021.06.010
Xu J, De Barro PJ, Liu SS (2010) Reproductive incompatibility among genetic groups of Bemisia tabaci supports the proposition that the whitefly is a cryptic species complex. Bull Entomol Res 100:359–366. https://doi.org/10.1017/S0007485310000015
Xu HX, Qian LX, Wang XW, Shao RX, Hong Y, Liu SS, Wang XW (2019) A salivary effector enables whitefly to feed on host plants by eliciting salicylic acid-signaling pathway. Proc Natl Acad Sci USA 116:490–495. https://doi.org/10.1073/pnas.1714990116
Yang CH, Guo JY, Chu D, Ding TB, Wei KK, Cheng DF, Wan FH (2017) Secretory laccase 1 in Bemisia tabaci MED is involved in whitefly-plant interaction. Sci Rep 7:1–9. https://doi.org/10.1038/s41598-017-03765-y
Yang JJ, Xie W, Liu BM, Wang SL, Wu QJ, He YC, Zhang YJ, Jiao XG (2020) Phenolics, rather than glucosinolates, mediate host choice of Bemisia tabaci MEAM1 and MED on five cabbage genotypes. J Appl Entomol 144:287–296. https://doi.org/10.1111/jen.12737
Zarate SI, Kempema LA, Walling LL (2007) Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiol 143:866–875. https://doi.org/10.1104/pp.106.090035
Zhang YL, Li X (2019) Salicylic acid: biosynthesis, perception, and contributions to plant immunity. Curr Opin Plant Biol 50:29–36. https://doi.org/10.1016/j.pbi.2019.02.004
Zhang XB, Liu CJ (2015) Multifaceted regulations of gateway enzyme phenylalanine ammonia-lyase in the biosynthesis of phenylpropanoids. Mol Plant 8:17–27. https://doi.org/10.1016/j.molp.2014.11.001
Zhang PJ, Li WD, Huang F, Zhang JM, Xu FC, Lu YB (2013) Feeding by whiteflies suppresses downstream jasmonic acid signaling by eliciting salicylic acid signaling. J Chem Ecol 39:612–619. https://doi.org/10.1007/s10886-013-0283-2
Zhang GF, Lövei GL, Hu M, Wan FH (2014) Asymmetric consequences of host plant occupation on the competition between the whiteflies Bemisia tabaci cryptic species MEAM1 and Trialeurodes vaporariorum (Hemiptera: Aleyrodidae). Pest Manag Sci 70:1797–1807. https://doi.org/10.1002/ps.3713
Zhang PJ, He YC, Zhao C, Ye ZH, Yu XP (2018) Jasmonic acid-dependent defenses play a key role in defending tomato against Bemisia tabaci nymphs, but not adults. Front Plant Sci 9:1065. https://doi.org/10.3389/fpls.2018.01065
Zhang PJ, Wei JN, Zhao C, Zhang YF, Li CY, Liu SS, Dicke M, Yu XP, Turlings TCJ (2019) Airborne host-plant manipulation by whiteflies via an inducible blend of plant volatiles. P Natl Acad Sci USA 116:7387–7396. https://doi.org/10.1073/pnas.1818599116
Zhao HP, Zhang XY, Xue M, Zhang X (2015) Feeding of whitefly on tobacco decreases aphid performance via increased salicylate signaling. PLoS ONE 10:e0138584. https://doi.org/10.1371/journal.pone.0138584
Züst T, Agrawal AA (2016) Mechanisms and evolution of plant resistance to aphids. Nat Plants 2:1–9. https://doi.org/10.1038/nplants.2015.206
Acknowledgements
We thank Jinjian Yang for his devotion on the manuscript and Nina Yang for providing pepper plants for the experiments.
Funding
This study was funded by the National Natural Science Foundation of China (31371941, 31572012), the Key Science and Technology Program of Hubei Tobacco Company of China (027Y2021-005), and the National Tobacco Board project (110202102007).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interests
The authors declare no conflict of interest.
Ethical approval
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Communicated by Rami Horowitz.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Hu, J., Sun, G., Yang, Y. et al. Pepper previously infested by MED facilitates settling and oviposition by MEAM1 of the Bemisia tabaci species complex. J Pest Sci 96, 1019–1034 (2023). https://doi.org/10.1007/s10340-022-01583-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10340-022-01583-4