Different soybean cultivars respond differentially to damage in a herbivore-specific manner and decreas herbivore performance
Tóm tắt
This study demonstrates that soybean cultivars respond differentially to damage in a herbivore-specific manner, and trigger responses decreasing herbivore performance. Soybean crops are affected by a great number of insect herbivores, resulting in devastating yield losses. Secondary metabolites like proteinase inhibitors and phenolic compounds are part of plants’ defense mechanisms against insect pests. However, the specificity of soybean defense responses to different attacking herbivores is poorly known. To investigate species-specific foliage responses to herbivory, we used two different commercial soybean cultivars (DM 4210 and DM 5.8i) widely used in Argentina with diverse susceptibility to insects’ attack and two species of phytophagous insects, thrips (Caliothrips phaseoli; Thysanoptera) and lepidopteran larvae (Spodoptera frugiperda; Lepidoptera) with a different way of feeding. Benzoic acid derivative levels were increased by damage of both insect species in the foliage of the field-grown soybean cultivars, whereas trypsin protease inhibitors activity was induced in cultivar (cv) DM 4210 by fall armyworm damage and malonyl genistein content in cv DM 5.8i after thrips’ attack. Although survivorship and mass of fall armyworm larvae were not differentially affected in field conditions by soybean cultivars, larvae reared in the laboratory that fed on cv DM 5.8i gained more mass than those on DM 4210. Conversely, thrips performance, natural colonization, and preference of feeding were higher on cv DM 4210 than on cv DM 5.8i. The differential effects of soybean cultivars on insectspecies’ performance were explained not only by induced defenses, but also by differences of constitutive defenses between cultivars. This study demonstrated that soybean cultivars responded differentially to damage in a herbivore-specific manner, and triggered responses decreased herbivore performance.
Tài liệu tham khảo
Acevedo FE, Rivera-Vega LJ, Chung SH et al (2015) Cues from chewing insects—the intersection of DAMPs, HAMPs, MAMPs and effectors. Curr Opin Plant Biol 26:80–86. https://doi.org/10.1016/j.pbi.2015.05.029
Annadana S, Peters J, Gruden K et al (2002) Effects of cysteine protease inhibitors on oviposition rate of the western flower thrips, Frankliniella occidentalis. J Insect Physiol 48:701–706. https://doi.org/10.1016/S0022-1910(02)00093-8
Appel HM, Fescemyer H, Ehlting J et al (2014) Transcriptional responses of Arabidopsis thaliana to chewing and sucking insect herbivores. Front Plant Sci 5:1–20. https://doi.org/10.3389/fpls.2014.00565
Barros EM, Torres JB, Ruberson JR, Oliveira MD (2010) Development of Spodoptera frugiperda on different hosts and damage to reproductive structures in cotton. Entomol Exp Appl 137:237–245. https://doi.org/10.1111/j.1570-7458.2010.01058.x
Bingham RA, Agrawal AA (2010) Specificity and trade-offs in the induced plant defence of common milkweed Asclepias syriaca to two lepidopteran herbivores. J Ecol 98:1014–1022. https://doi.org/10.1111/j.1365-2745.2010.01681.x
Birkett MA, Pickett JA (2014) Prospects of genetic engineering for robust insect resistance. Curr Opin Plant Biol 19:59–67. https://doi.org/10.1016/j.pbi.2014.03.009
Carrao-Panizzi MC, Kitamura K (1995) Isoflavone content in brazilian soybean cultivars. Breed Sci. https://doi.org/10.1270/jsbbs1951.45.295
Childers C, Achor DS (1995) Thrips feeding and oviposition injuries to economic plants, subsequent damage, and host responses to infestation. In: Parker BL, Skinner M, Lewis T (eds) Thrips biology and management. Plenum Press, New York, pp 31–51
Childers CC, Bullock RC (1999) Controlling Frankliniella bispinosa (Thysanoptera: Thripidae) on florida citrus during bloom and increased fruit set on navel and ‘Valencia’ oranges. Florida Entomol 82(3):410
Chisholm IF, Lewis T (1984) A new look at thrips (Thysanoptera) mouthparts, their action and effects of feeding on plant tissue. Bull Entomol Res 74:663–675. https://doi.org/10.1017/S0007485300014048
da Graça JP, Ueda TE, Janegitz T et al (2016) The natural plant stress elicitor cis-jasmone causes cultivar-dependent reduction in growth of the stink bug, Euschistus heros and associated changes in flavonoid concentrations in soybean, Glycine max. Phytochemistry 131:84–91. https://doi.org/10.1016/j.phytochem.2016.08.013
Dias Peruca R, Coelho RG, da Silva GG et al (2018) Impacts of soybean-induced defenses on Spodoptera frugiperda (Lepidoptera: Noctuidae) development. Arthropod Plant Interact 12:257–266. https://doi.org/10.1007/s11829-017-9565-x
Diaz Napal GN, Palacios SM (2015) Bioinsecticidal effect of the flavonoids pinocembrin and quercetin against Spodoptera frugiperda. J Pest Sci 88:629–635. https://doi.org/10.1007/s10340-014-0641-z
Dillon FM, Chludil HD, Zavala JA (2017) Solar UV-B radiation modulates chemical defenses against Anticarsia gemmatalis larvae in leaves of field-grown soybean. Phytochemistry 141:27–36. https://doi.org/10.1016/j.phytochem.2017.05.006
Dillon FM, Tejedor MD, Ilina N et al (2018a) Solar UV-B radiation and ethylene play a key role in modulating effective defenses against Anticarsia gemmatalis larvae in field-grown soybean. Plant Cell Environ 41:383–394. https://doi.org/10.1111/pce.13104
Dillon FM, Chludil HD, Reichelt M et al (2018b) Field-grown soybean induces jasmonates and defensive compounds in response to thrips feeding and solar UV-B radiation. Environ Exp Bot 156:1–7. https://doi.org/10.1016/j.envexpbot.2018.08.022
Fehr WR, Caviness CE, Burmood DT, Pennington JS (1971) Stage of development descriptions for soybean Glycine max (L.) Merrill. Crop Sci 11:929–931
Giacometti R, Barneto J, Barriga LG, Sardoy PM, Balestrasse K, Andrade AM, Pagano EA, Alemano SG, Zavala JA (2016) Early perception of stink bug damage in developing seeds of field-grown soybean induces chemical defenses, and decreases bug attack. Pest Manag Sci 72:1585–1594
Gosset V, Harmel N, Göbel C et al (2009) Attacks by a piercing-sucking insect (Myzus persicae Sultzer) or a chewing insect (Leptinotarsa decemlineata Say) on potato plants (Solanum tuberosum L.) induce differential changes in volatile compound release and oxylipin synthesis. J Exp Bot 60:1231–1240. https://doi.org/10.1093/jxb/erp015
Groves C, German T, Dasgupta R et al (2016) Seed transmission of soybean vein necrosis virus: The first tospovirus implicated in seed transmission. PLoS ONE 11:1–14. https://doi.org/10.5061/dryad.b1pg3.Funding
Hoffmann-Campo CB, Harborne JB, McCaffery AR (2001) Pre-ingestive and post-ingestive effects of soya bean extracts and rutin on Trichoplusia ni growth. Entomol Exp Appl 98(2):181–194
Jongsma MA, Bakker PL, Peters J, Bosch D, Stiekema WJ (1995) Adaptation of Spodoptera exigua larvae to plant proteinase inhibitors by induction of gut proteinase activity insensitive to inhibition. Proc Nat Acad Sci 92(17):8041–8045
Kirk WDJ (1995) Feeding behavior and nutritional requirements. In: Parker BL, Skinner M, Lewis T (eds) Thrips biology and management. Plenum Press, New York, pp 21–29
Lattanzio V, Arpaia S, Cardinali A et al (2000) Endogenous flavonoids in resistance mechanism of Vigna role to aphids. J Agric Food Chem 48:5316–5320. https://doi.org/10.1021/jf000229y
Leiss KA, Choi YH, Verpoorte R, Klinkhamer PGL (2011) An overview of NMR-based metabolomics to identify secondary plant compounds involved in host plant resistance. Phytochem Rev 10:205–216. https://doi.org/10.1007/s11101-010-9175-z
Leitner M, Boland W, Mithöfer A (2005) Direct and indirect defences induced by piercing-sucking and chewing herbivores in Medicago truncatula. New Phytol 167:597–606
Marques LH, Santos AC, Castro BA et al (2018) Impact of transgenic soybean expressing Cry1Ac and Cry1F proteins on the non-target arthropod community associated with soybean in Brazil. PLoS ONE 13:1–23. https://doi.org/10.1371/journal.pone.0191567
Moritz G (1997) Structure, growth and development. In: Lewis T (ed) Thrips as crop pests. CAB International, New York, pp 15–63
Mouden S, Sarmiento KF, Klinkhamer PGL, Leiss KA (2017) Integrated pest management in western flower thrips: past, present and future. Pest Manag Sci 73:813–822. https://doi.org/10.1002/ps.4531
Neven LG (2000) Physiological responses of insects to heat. Postharvest Biol Technol 21:103–111. https://doi.org/10.1016/S0925-5214(00)00169-1
Oerke EC (2006) Crop losses to pests. J Agric Sci 144:31–43. https://doi.org/10.1017/S0021859605005708
Oerke EC, Dehne HW (2004) Safeguarding production—losses in major crops and the role of crop protection. Crop Prot 23:275–285. https://doi.org/10.1016/j.cropro.2003.10.001
Oliva MLV, Silva MCC, Sallai RC et al (2010) A novel subclassification for Kunitz proteinase inhibitors from leguminous seeds. Biochimie 92:1667–1673. https://doi.org/10.1016/j.biochi.2010.03.021
Outchkourov NS, De Kogel WJ, Wiegers GL et al (2004) Engineered multidomain cysteine protease inhibitors yield resistance against western flower thrips (Frankliniella occidentalis) in greenhouse trials. Plant Biotechnol J 2:449–458. https://doi.org/10.1111/j.1467-7652.2004.00089.x
Riley DG, Angelella GM, McPherson RM (2011) Pine pollen dehiscence relative to thrips population dynamics. Entomol Exp Appl 138(3):223–233
Rustgi S, Boex-Fontvieille E, Reinbothe C, von Wettstein D, Reinbothe S (2018) The complex world of plant protease inhibitors: insights into a Kunitz-type cysteine protease inhibitor of Arabidopsis thaliana. Commun Integr Biol 11(1):e1368599. https://doi.org/10.1080/19420889.2017.1368599
Ryan CA (1978) Proteinase inhibitors in plant leaves: a biochemical model for pest induced natural plant protection. Trends Biol Sci 3:148–150
Sa VGM, Fonseca BVC, Boregas KGB, Waquil JM (2009) Sobrevivência e Desenvolvimento Larval de S. frugiperda em hospedeiros alternativos. Neotrop Entomol 38:108–115
Selig P, Keough S, Nalam VJ, Nachappa P (2016) Jasmonate-dependent plant defenses mediate soybean thrips and soybean aphid performance on soybean. Arthropod-Plant Interact 10(4):273–282
Schoonhoven LM, van Loon JJA, Dicke M (2005) Insect-plant biology. Oxford University Press, Oxford
Souza CSF, Silveira LCP, Paula DP et al (2018) Transfer of Cry1F from Bt maize to eggs of resistant Spodoptera frugiperda. PLoS ONE 13:1–10. https://doi.org/10.1371/journal.pone.0203791
Steenbergen M, Abd-El-Haliem A, Bleeker P et al (2018) Thrips advisor: exploiting thrips-induced defences to combat pests on crops. J Exp Bot 69:1837–1848. https://doi.org/10.1093/jxb/ery060
Steppuhn A, Baldwin IT (2007) Resistance management in a native plant: nicotine prevents herbivores from compensating for plant protease inhibitors. Ecol Lett 10:499–511. https://doi.org/10.1111/j.1461-0248.2007.01045.x
Underwood N, Morris W, Gross K, Lockwood JR (2000) Induced resistance to Mexican bean beetles in soybean: variation among genotypes and lack of correlation with constitutive resistance. Oecologia 122:83–89. https://doi.org/10.1007/PL00008839
War AR, Paulraj MG, Ignacimuthu S, Sharma HC (2013) Defensive responses in groundnut against chewing and sap-sucking insects. J Plant Growth Regul 32:259–272. https://doi.org/10.1007/s00344-012-9294-4
Wink M (2013) Evolution of secondary metabolites in legumes (Fabaceae). South Afr J Bot 89:164–175. https://doi.org/10.1016/j.sajb.2013.06.006
Wu B, Takahashi T, Kashiwagi T et al (2007) New flavonoid glycosides from the leaves of Solidago altissima. Chem Pharm Bull 55:815–816
Zavala JA, Casteel CL, DeLucia EH, Berenbaum MR (2008a) Anthropogenic increase in carbon dioxide compromises plant defense against invasive insects. Proc Natl Acad Sci 105:5129–5133. https://doi.org/10.1073/pnas.0800568105
Zavala JA, Giri AP, Jongsma MA, Baldwin IT (2008b) Digestive duet: midgut digestive proteinases of Manduca sexta ingesting Nicotiana attenuata with manipulated trypsin proteinase inhibitor expression. PLoS ONE 3:29–31. https://doi.org/10.1371/journal.pone.0002008
Zavala JA, Casteel CL, Nabity PD et al (2009) Role of cysteine proteinase inhibitors in preference of japanese beetles (Popillia japonica) for soybean (Glycine max) leaves of different ages and grown under elevated CO2. Oecologia 161:35–41. https://doi.org/10.1007/s00442-009
Zavala JA, Mazza CA, Dillon FM et al (2015) Soybean resistance to stink bugs (Nezara viridula and Piezodorus guildinii) increases with exposure to solar UV-B radiation and correlates with isoflavonoid content in pods under field conditions. Plant Cell Environ 38:920–928. https://doi.org/10.1111/pce.12368
Zhou J, Tzanetakis IE (2013) Epidemiology of Soybean vein necrosis-associated virus. Phytopathology 103:966–971. https://doi.org/10.1094/phyto-12-12-0322-r
Zuo W, Moses ME, West GB et al (2012) A general model for effects of temperature on ectotherm ontogenetic growth and development. Proc R Soc B 279:1840–1846. https://doi.org/10.1098/rspb.201