Abstract
Herbivore identity and intensity are important in mediating plant defense responses, but the effects of their interaction on the plant metabolome have not yet been fully explored. Here, gas chromatography mass spectrometry was utilized to detect the metabolic changes in leaves, stems and roots of the common reed Phragmites australis infested with different intensity combinations of leaf-chewing Laelia coenosa and stem piercing-sucking Dimorphopterus pallipes. The supervised partial least squares-discriminant analysis showed that feeding by the two insects distinctly changed the metabolic profiles of all plant tissues. Furthermore, different intensities of the two herbivores resulted in significantly different metabolites in leaves. Only a high intensity of D. pallipes activated a distinct metabolic profile in roots, whereas there was no difference in stem metabolites in response to different herbivore intensities. Significant combined feeding effects of the two herbivores on plant metabolic composition was only detected in leaves infested with high herbivore intensity. Generally, D. pallipes feeding had a stronger effect on metabolite contents in different tissues compared to L. coenosa feeding. There was mostly a linear relationship between responses of leaf metabolites and herbivore intensity, whereas root metabolites generally showed non-linear responses to herbivore intensity. Additionally, there were significant interactions during simultaneous feeding of the two herbivores in leaves, which tended to be antagonistic. In general, our study suggested that plant responses to herbivory vary among tissues and are affected differently based on herbivore identity and intensity, which may vary in their interactions on plant metabolites at the whole-plant level.
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References
Appel HM et al (2014) Transcriptional responses of Arabidopsis thaliana to chewing and sucking insect herbivores. Front Plant Sci 5:565. https://doi.org/10.3389/fpls.2014.00565
Bennett RN, Wallsgrove RM (1994) Secondary metabolites in plant defence mechanisms. New Phytol 127:617–633. https://doi.org/10.1111/j.1469-8137.1994.tb02968.x
Chambers RM, Meyerson LA, Saltonstall K (1992) Expansion of Phragmites australis into tidal wetlands of North America. Aquat Bot 64:261–273. https://doi.org/10.1016/s0304-3770(99)00055-8
Chung SH, Felton GW (2011) Specificity of induced resistance in tomato against specialist lepidopteran and coleopteran species. J Chem Ecol 37:378–386. https://doi.org/10.1007/s10886-011-9937-0
Copolovici L, Kannaste A, Remmel T, Vislap V, Niinemets U (2011) Volatile emissions from Alnus glutionosa induced by herbivory are quantitatively related to the extent of damage. J Chem Ecol 37:18–28. https://doi.org/10.1007/s10886-010-9897-9
Cronin JT, Bhattarai GP, Allen WJ, Meyerson LA (2015) Biogeography of a plant invasion: plant-herbivore interactions. Ecology 96:1115–1127. https://doi.org/10.1890/14-1091.1
Detling JK, Painter EL (1983) Defoliation responses of western wheatgrass populations with diverse histories of prairie dog grazing. Oecologia 57:65–71. https://doi.org/10.2307/4216929
Doares SH, Narváez-Vásquez J, Conconi A, Ryan CA (1995) Salicylic acid inhibits synthesis of proteinase inhibitors in tomato leaves induced by systemin and jasmonic acid. Plant Physiol 108:1741–1746. https://doi.org/10.2307/4276766
El-Khawas SAM, El-Khawas MAM (2008) Interactions between Aphis gossypii (Glov.) and the common predators in eggplant and squash fields, with evaluating the physiological and biochemical aspects of biotic stress induced by two different aphid species, infesting squash and cabbage plants. Aust J Basic Appl Sci 2:183–193
Fabisch T, Gershenzon J, Unsicker SB (2019) Specificity of herbivore defense responses in a woody plant, black poplar (Populus nigra). J Chem Ecol 45:162–177. https://doi.org/10.1007/s10886-019-01050-y
Gómez S, Steinbrenner AD, Osorio S, Schueller M, Ferrieri RA, Fernie AR, Orians CM (2012) From shoots to roots: transport and metabolic changes in tomato after simulated feeding by a specialist lepidopteran. Entomol Exp Appl 144:101–111. https://doi.org/10.1111/j.1570-7458.2012.01268.x
Haslam SM (1972) Phragmites Communis Trin. (Arundo Phragmites L.,? Phragmites australis (Cav.) Trin. ex Steudel). J Ecol 60:585–610. https://doi.org/10.2307/2258363
Hendricks LG, Mossop HE, Kicklighter CE (2011) Palatability and chemical defense of Phragmites australis to the marsh periwinkle snail Littoraria irrorata. J Chem Ecol 37:838–845. https://doi.org/10.1007/s10886-011-9990-8
Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335. https://doi.org/10.1086/417659
Hettenhausen C, Baldwin IT, Wu J (2013) Nicotiana attenuata MPK4 suppresses a novel jasmonic acid (JA) signaling-independent defense pathway against the specialist insect Manduca sexta, but is not required for the resistance to the generalist Spodoptera littoralis. New Phytol 199:787–799. https://doi.org/10.1111/nph.12312
Hopkins RJ, Griffiths DW, Birch ANE, McKinlay RG (1998) Influence of increasing herbivore pressure on modification of glucosinolate content of swedes (Brassica napus spp. rapifera). J Chem Ecol 24:2003–2019. https://doi.org/10.1023/a:1020729524818
Inbar M, Doostdar H, Leibee GL, Mayer RT (1999) The role of plant rapidly induced responses in asymmetric interspecific interactions among insect herbivores. J Chem Ecol 25:1961–1979. https://doi.org/10.1023/a:1020998219928
Khattab H (2007) The defense mechanism of cabbage plant against phloem-sucking aphid (Brevicoryne brassicae L.). Aust J Basic Appl Sci 1:56–62
Kroes A, Weldegergis BT, Cappai F, Dicke M, Loon JJAV (2017) Terpenoid biosynthesis in Arabidopsis attacked by caterpillars and aphids. Oecologia 185:699–712. https://doi.org/10.1007/s00442-017-3985-2
Lenssen JPM, Menting FBJ, van der Putten WH (2004) Do competition and selective herbivory cause replacement of Phragmites australis by tall forbs? Aquat Bot 78:217–232. https://doi.org/10.1016/j.aquabot.2003.10.006
Little D, Gouhier-Darimont C, Bruessow F, Reymond P (2007) Oviposition by pierid butterflies triggers defense responses in Arabidopsis. Plant Physiol 143:784–800. https://doi.org/10.1104/pp.106.090837
Liu C et al (2010) Revealing different systems responses to brown planthopper infestation for pest susceptible and resistant rice plants with the combined metabonomic and gene-expression analysis. J Proteome Res 9:6774–6785. https://doi.org/10.1021/pr100970q
Liu DN, He CX, Chang XN, Fu JJ, Min W (2016) Properties of PVC/straw fibers composite. Eng Plastics Appl 44(10):6–11. https://doi.org/10.3969/j.issn.1001-3539.2016.10.002
Magalhães DM, Borges M, Laumann RA, Blassioli Moraes MC (2018) Influence of multiple- and single-species infestations on herbivore-induced cotton volatiles and Anthonomus grandis behaviour. J Pest Sci 91:1019–1032. https://doi.org/10.1007/s10340-018-0971-3
Mal TK, Narine L (2004) The biology of Canadian weeds. 129. Phragmites australis (Cav.) Trin. ex Steud. Can J Plant Sci 84:365–396. https://doi.org/10.4141/P01-172
Martel JW, Malcolm SB (2004) Density-dependent reduction and induction of milkweed cardenolides by a sucking insect herbivore. J Chem Ecol 30:545–561. https://doi.org/10.1023/b:joec.0000018628.48604.79
Moreira X, Zas R, Sampedro L (2012) Differential allocation of constitutive and induced chemical defenses in pine tree juveniles: a test of the optimal defense theory. PLoS ONE 7:e34006. https://doi.org/10.1371/journal.pone.0034006
Nalam VJ, Nachappa P (2014) The role of roots in plant defense responses to aboveground herbivores. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-54276-3_17
Niinemets U, Kannaste A, Copolovici L (2013) Quantitative patterns between plant volatile emissions induced by biotic stresses and the degree of damage. Front Plant Sci 4:262. https://doi.org/10.3389/fpls.2013.00262
Nowak RS, Caldwell MM (1984) A test of compensatory photosynthesis in the field: implications for herbivory tolerance. Oecologia 61:311–318. https://doi.org/10.1007/BF00379627
Orians CM, Thorn A, Gomez S (2011) Herbivore-induced resource sequestration in plants: why bother? Oecologia 167:1–9. https://doi.org/10.1007/s00442-011-1968-2
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
Rhoades DF (1979) Evolution of plant chemical defence against herbivores. In: Janzen DH (ed) Herbivores: their Interaction with secondary plant metabolites. Academic Press, New York, pp 1–55
Rodriguez-Saona CR, Musser RO, Vogel H, Hum-Musser SM, Thaler JS (2010) Molecular, biochemical, and organismal analyses of tomato plants simultaneously attacked by herbivores from two feeding guilds. J Chem Ecol 36:1043–1057. https://doi.org/10.1007/s10886-010-9854-7
Schmidt MH, Lefebvre G, Poulin B, Tscharntke T (2005) Reed cutting affects arthropod communities, potentially reducing food for passerine birds. Biol Conserv 121:157–166. https://doi.org/10.1016/j.biocon.2004.03.032
Schmidt L, Schurr U, Rose US (2009) Local and systemic effects of two herbivores with different feeding mechanisms on primary metabolism of cotton leaves. Plant Cell Environ 32:893–903. https://doi.org/10.1111/j.1365-3040.2009.01969.x
Schultz JC, Appel HM, Ferrieri AP, Arnold TM (2013) Flexible resource allocation during plant defense responses. Front Plant Sci 4:324. https://doi.org/10.3389/fpls.2013.00324
Schwachtje J, Baldwin IT (2008) Why does herbivore attack reconfigure primary metabolism? Plant Physiol 146:845–851. https://doi.org/10.1104/pp.107.112490
Schwachtje J, Minchin PE, Jahnke S, van Dongen JT, Schittko U, Baldwin IT (2006) SNF1-related kinases allow plants to tolerate herbivory by allocating carbon to roots. Proc Natl Acad Sci USA 103:12935–12940. https://doi.org/10.1073/pnas.0602316103
Schweiger R, Heise A-M, Persicke M, Müller C (2014) Interactions between the jasmonic and salicylic acid pathway modulate the plant metabolome and affect herbivores of different feeding types. Plant Cell Environ 37:1574–1585. https://doi.org/10.1111/pce.12257
Silva DB, Weldegergis BT, Van Loon JJ, Bueno VH (2017) Qualitative and quantitative differences in herbivore-induced plant volatile blends from tomato plants infested by either Tuta absoluta or Bemisia tabaci. J Chem Ecol 43:53–65. https://doi.org/10.1007/s10886-016-0807-7
Singh P, Sinhal VK (2011) Effect of aphid infestation on the biochemical constituents of mustard (Brassica juncea) plant. J Phycol 3(8):28–33
Sotelo P, Pérez E, Najar-Rodriguez A, Walter A, Dorn S (2014) Brassica plant responses to mild herbivore stress elicited by two specialist insects from different feeding guilds. J Chem Ecol 40:136–149. https://doi.org/10.1007/s10886-014-0386-4
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
Steinbrenner AD, Gómez S, Osorio S, Fernie AR, Orians CM (2011) Herbivore-induced changes in tomato (Solanum lycopersicum) primary metabolism: a whole plant perspective. J Chem Ecol 37:1294–1303. https://doi.org/10.1007/s10886-011-0042-1
Strong D, Lawton J, Southwood S (1984) Insects on plants. Community patterns and mechanisms. Harvard University Press, Cambridge, MA
Taylor GS, Miles PW (1994) Composition and variability of the saliva of coreids in relation to phytoxicoses and other aspects of the salivary physiology of phytophagous Heteroptera. Entomol Exp Appl 73:265–277. https://doi.org/10.1111/j.1570-7458.1994.tb01864.x
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
Tiffin P (2002) Mechanisms of tolerance to herbivore damage: what do we know? Evol Ecol 14:523–536. https://doi.org/10.1023/a:1010881317261
Tscharntke T (1999) Insects on common reed (Phragmites australis): community structure and the impact of herbivory on shoot growth. Aquat Bot 64:399–410. https://doi.org/10.1016/s0304-3770(99)00066-2
van Dam NM, Oomen MWAT (2014) Root and shoot jasmonic acid applications differentially affect leaf chemistry and herbivore growth. Plant Signal Behav 3:91–98. https://doi.org/10.4161/psb.3.2.5220
van Wees SC, de Swart EA, van Pelt JA, van Loon LC, Pieterse CM (2000) Enhancement of induced disease resistance by simultaneous activation of salicylate- and jasmonate-dependent defense pathways in Arabidopsis thaliana. Proc Natl Acad Sci USA 97:8711–8716. https://doi.org/10.1073/pnas.130425197
Veech RL (2004) Tricarboxylic acid cycle. In: Encyclopedia of biological chemistry. pp 256–262. https://doi.org/10.1016/B978-0-12-378630-2.00608-3
Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195–216. https://doi.org/10.1007/s003440000026
Wang ZD, You LS, Xiong SL (1989) An iconography of pests and natural enemies of Amur silvergrass and reed. China Light Industry Press, Beijing
Zangerl AR (2003) Evolution of induced plant responses to herbivores. Basic Appl Ecol 4:91–103. https://doi.org/10.1078/1439-1791-00135
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/10.2307/40065439
Acknowledgements
We thank Dr. Ruiting Ju (Shanghai Academy of Landscape Architecture Science and Planning) for his support in the greenhouse experiment, as well as Dr. Chengshu Wang and Mr. Wenli Hu (Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences) for their help in metabolomics experiments and data analyses. This research is supported by the Chinese Academy of Sciences (Grant Number CZBZX-1) and the National Natural Science Foundation of China (Grant Number 31770580).
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This research is supported by the Chinese Academy of Sciences (Grant Number CZBZX-1) and the National Natural Science Foundation of China (Grant Number 31770580).
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Pan, S., Zhang, J., Pan, H. et al. Herbivore identity and intensity interact to influence plant metabolic response to herbivory. Arthropod-Plant Interactions 15, 285–298 (2021). https://doi.org/10.1007/s11829-021-09823-7
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DOI: https://doi.org/10.1007/s11829-021-09823-7