Arabidopsis, tobacco, nightshade and elm take insect eggs as herbivore alarm and show similar transcriptomic alarm responses.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
01 10 2020
01 10 2020
Historique:
received:
25
05
2020
accepted:
08
09
2020
entrez:
2
10
2020
pubmed:
3
10
2020
medline:
5
1
2021
Statut:
epublish
Résumé
Plants respond to insect eggs with transcriptional changes, resulting in enhanced defence against hatching larvae. However, it is unknown whether phylogenetically distant plant species show conserved transcriptomic responses to insect eggs and subsequent larval feeding. We used Generally Applicable Gene set Enrichment (GAGE) on gene ontology terms to answer this question and analysed transcriptome data from Arabidopsis thaliana, wild tobacco (Nicotiana attenuata), bittersweet nightshade (Solanum dulcamara) and elm trees (Ulmus minor) infested by different insect species. The different plant-insect species combinations showed considerable overlap in their transcriptomic responses to both eggs and larval feeding. Within these conformable responses across the plant-insect combinations, the responses to eggs and feeding were largely analogous, and about one-fifth of these analogous responses were further enhanced when egg deposition preceded larval feeding. This conserved transcriptomic response to eggs and larval feeding comprised gene sets related to several phytohormones and to the phenylpropanoid biosynthesis pathway, of which specific branches were activated in different plant-insect combinations. Since insect eggs and larval feeding activate conserved sets of biological processes in different plant species, we conclude that plants with different lifestyles share common transcriptomic alarm responses to insect eggs, which likely enhance their defence against hatching larvae.
Identifiants
pubmed: 33004864
doi: 10.1038/s41598-020-72955-y
pii: 10.1038/s41598-020-72955-y
pmc: PMC7530724
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
16281Références
Dicke, M., Agrawal, A. A. & Bruin, J. Plants talk, but are they deaf?. Trends Plant Sci. 8, 403–405 (2003).
pubmed: 13678903
doi: 10.1016/S1360-1385(03)00183-3
pmcid: 13678903
Heil, M. & Silva Bueno, J. C. Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc. Natl. Acad. Sci. USA 104, 5467–5472 (2007).
pubmed: 17360371
doi: 10.1073/pnas.0610266104
pmcid: 17360371
Karban, R., Yang, L. H. & Edwards, K. F. Volatile communication between plants that affects herbivory: A meta-analysis. Ecol. Lett. 17, 44–52 (2014).
pubmed: 24165497
doi: 10.1111/ele.12205
Pashalidou, F. G. et al. Plant volatiles induced by herbivore eggs prime defences and mediate shifts in the reproductive strategy of receiving plants. Ecol. Lett. https://doi.org/10.1111/ele.13509 (2020).
doi: 10.1111/ele.13509
pubmed: 32314512
Helms, A. M., De Moraes, C. M., Mescher, M. C. & Tooker, J. F. The volatile emission of Eurosta solidaginis primes herbivore-induced volatile production in Solidago altissima and does not directly deter insect feeding. BMC Plant Biol. 14, 173 (2014).
pubmed: 24947749
pmcid: 4071026
doi: 10.1186/1471-2229-14-173
Helms, A. M. et al. Identification of an insect-produced olfactory cue that primes plant defenses. Nat. Commun. 8, 337 (2017).
pubmed: 28835618
pmcid: 5569085
doi: 10.1038/s41467-017-00335-8
Hilker, M. & Fatouros, N. E. Resisting the onset of herbivore attack: Plants perceive and respond to insect eggs. Curr. Opin. Plant Biol. 32, 9–16 (2016).
pubmed: 27267276
doi: 10.1016/j.pbi.2016.05.003
pmcid: 27267276
Engelberth, J., Contreras, C. F., Dalvi, C., Li, T. & Engelberth, M. Early transcriptome analyses of Z-3-hexenol-treated Zea mays revealed distinct transcriptional networks and anti-herbivore defense potential of green leaf volatiles. PLoS ONE 8, e77465 (2013).
pubmed: 24155960
pmcid: 3796489
doi: 10.1371/journal.pone.0077465
Ye, M., Glauser, G., Lou, Y., Erb, M. & Hu, L. Molecular dissection of early defense signaling underlying volatile-mediated defense regulation and herbivore resistance in rice. Plant Cell 31, 687–698 (2019).
pubmed: 30760558
pmcid: 6482627
doi: 10.1105/tpc.18.00569
Hilker, M. & Fatouros, N. E. Plant responses to insect egg deposition. Annu. Rev. Entomol. 60, 493–515 (2015).
pubmed: 25341089
doi: 10.1146/annurev-ento-010814-020620
Bittner, N., Trauer-Kizilelma, U. & Hilker, M. Early plant defence against insect attack: Involvement of reactive oxygen species in plant responses to insect egg deposition. Planta 245, 993–1007 (2017).
pubmed: 28175992
doi: 10.1007/s00425-017-2654-3
Geuss, D., Stelzer, S., Lortzing, T. & Steppuhn, A. Solanum dulcamara’s response to eggs of an insect herbivore comprises ovicidal hydrogen peroxide production. Plant Cell Environ. 40, 2663–2677 (2017).
pubmed: 28667817
doi: 10.1111/pce.13015
Fatouros, N. E. et al. Synergistic effects of direct and indirect defences on herbivore egg survival in a wild crucifer. Proc. R. Soc. Biol. Sci. 281, 20141254 (2014).
doi: 10.1098/rspb.2014.1254
Gouhier-Darimont, C., Schmiesing, A., Bonnet, C., Lassueur, S. & Reymond, P. Signalling of Arabidopsis thaliana response to Pieris brassicae eggs shares similarities with PAMP-triggered immunity. J. Exp. Bot. 64, 665–674 (2013).
pubmed: 23264520
pmcid: 3542055
doi: 10.1093/jxb/ers362
Rondoni, G. et al. Vicia faba plants respond to oviposition by invasive Halyomorpha halys activating direct defences against offspring. J. Pest Sci. 2004(91), 671–679 (2018).
doi: 10.1007/s10340-018-0955-3
Bonnet, C. et al. Combined biotic stresses trigger similar transcriptomic responses but contrasting resistance against a chewing herbivore in Brassica nigra. BMC Plant Biol. 17, 127 (2017).
pubmed: 28716054
pmcid: 5513356
doi: 10.1186/s12870-017-1074-7
Lortzing, V. et al. Insect egg deposition renders plant defense against hatching larvae more effective in a salicylic acid-dependent manner. Plant Cell Environ. 42, 1019–1032 (2019).
pubmed: 30252928
doi: 10.1111/pce.13447
Kim, J., Tooker, J. F., Luthe, D. S., De Moraes, C. M. & Felton, G. W. Insect eggs can enhance wound response in plants: A study system of tomato Solanum lycopersicum L. and Helicoverpa zea Boddie. PLoS ONE 7, e37420 (2012).
pubmed: 22616005
pmcid: 3352884
doi: 10.1371/journal.pone.0037420
Bandoly, M., Grichnik, R., Hilker, M. & Steppuhn, A. Priming of anti-herbivore defence in Nicotiana attenuata by insect oviposition: Herbivore-specific effects. Plant Cell Environ. 39, 848–859 (2016).
pubmed: 26566692
doi: 10.1111/pce.12677
Bandoly, M., Hilker, M. & Steppuhn, A. Oviposition by Spodoptera exigua on Nicotiana attenuata primes induced plant defence against larval herbivory. Plant J. 83, 661–672 (2015).
pubmed: 26096574
doi: 10.1111/tpj.12918
Drok, S., Bandoly, M., Stelzer, S., Lortzing, T. & Steppuhn, A. Moth oviposition shapes the species-specific transcriptional and phytohormonal response of Nicotiana attenuata to larval feeding. Sci. Rep. 8, 10249 (2018).
pubmed: 29980784
pmcid: 6035172
doi: 10.1038/s41598-018-28233-z
Geuss, D., Lortzing, T., Schwachtje, J., Kopka, J. & Steppuhn, A. Oviposition by Spodoptera exigua on Solanum dulcamara alters the plant’s response to herbivory and impairs larval performance. Int. J. Mol. Sci. 19, 4008 (2018).
pmcid: 6321313
doi: 10.3390/ijms19124008
pubmed: 6321313
Luo, W., Friedman, M. S., Shedden, K., Hankenson, K. D. & Woolf, P. J. GAGE: Generally applicable gene set enrichment for pathway analysis. BMC Bioinform. 10, 161 (2009).
doi: 10.1186/1471-2105-10-161
Altmann, S. et al. Transcriptomic basis for reinforcement of elm antiherbivore defence mediated by insect egg deposition. Mol. Ecol. 27, 4901–4915 (2018).
pubmed: 30329187
doi: 10.1111/mec.14900
Reymond, P. Perception, signaling and molecular basis of oviposition-mediated plant responses. Planta 238, 247–258 (2013).
pubmed: 23748628
pmcid: 3722449
doi: 10.1007/s00425-013-1908-y
Bittner, N., Hundacker, J., Achotegui-Castells, A., Anderbrant, O. & Hilker, M. Defense of Scots pine against sawfly eggs (Diprion pini) is primed by exposure to sawfly sex pheromones. Proc. Natl. Acad. Sci. USA. 116, 24668–24675 (2019).
pubmed: 31748269
doi: 10.1073/pnas.1910991116
Shapiro, A. M. & DeVay, J. E. Hypersensitivity reaction of Brassica nigra L. (Cruciferae) kills eggs of Pieris butterflies (Lepidoptera: Pieridae). Oecologia 71, 631–632 (1987).
pubmed: 28312240
doi: 10.1007/BF00379310
Clarke, J. D., Liu, Y., Klessig, D. F. & Dong, X. Uncoupling PR gene expression from NPR1 and bacterial resistance: Characterization of the dominant Arabidopsis cpr6-1 mutant. Plant Cell 10, 557–569 (1998).
pubmed: 9548982
pmcid: 144011
doi: 10.1105/tpc.10.4.557
Ding, Y., Shaholli, D. & Mou, Z. A large-scale genetic screen for mutants with altered salicylic acid accumulation in Arabidopsis. Front. Plant Sci. 7, 763 (2015).
Niki, T., Mitsuhara, I., Seo, S., Ohtsubo, N. & Ohashi, Y. Antagonistic effect of salicylic acid and jasmonic acid on the expression of pathogenesis-related (PR) protein genes in wounded mature tobacco leaves. Plant Cell Physiol. 39, 500–507 (1998).
doi: 10.1093/oxfordjournals.pcp.a029397
Fatouros, N. E. et al. Role of Large Cabbage White butterfly male-derived compounds in elicitation of direct and indirect egg-killing defenses in the black mustard. Front. Plant Sci. 6, 794 (2015).
pubmed: 26483811
pmcid: 4586945
doi: 10.3389/fpls.2015.00794
Little, D., Gouhier-Darimont, C., Bruessow, F. & Reymond, P. Oviposition by pierid butterflies triggers defense responses in Arabidopsis. Plant Physiol. 143, 784–800 (2007).
pubmed: 17142483
pmcid: 1803735
doi: 10.1104/pp.106.090837
Wasternack, C. How jasmonates earned their laurels: Past and present. J. Plant Growth Regul. 34, 761–794 (2015).
doi: 10.1007/s00344-015-9526-5
Wasternack, C. & Hause, B. Jasmonates: Biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann. Bot. 111, 1021–1058 (2013).
pubmed: 23558912
pmcid: 3662512
doi: 10.1093/aob/mct067
Diezel, C., von Dahl, C. C., Gaquerel, E. & Baldwin, I. T. Different lepidopteran elicitors account for cross-talk in herbivory-induced phytohormone signaling. Plant Physiol. 150, 1576–1586 (2009).
pubmed: 19458114
pmcid: 2705021
doi: 10.1104/pp.109.139550
Heidel, A. J. & Baldwin, I. T. Microarray analysis of salicylic acid- and jasmonic acid-signalling in responses of Nicotiana attenuata to attack by insects from multiple feeding guilds. Plant Cell Environ. 27, 1362–1373 (2004).
doi: 10.1111/j.1365-3040.2004.01228.x
Nguyen, D. et al. Drought and flooding have distinct effects on herbivore-induced responses and resistance in Solanum dulcamara. Plant Cell Environ. 39, 1485–1499 (2016).
pubmed: 26759219
doi: 10.1111/pce.12708
Caarls, L., Pieterse, C. M. J. & Van Wees, S. C. M. How salicylic acid takes transcriptional control over jasmonic acid signaling. Front. Plant Sci. 6, 170 (2015).
pubmed: 25859250
pmcid: 4373269
doi: 10.3389/fpls.2015.00170
Pieterse, C. M. J., Van der Does, D., Zamioudis, C., Leon-Reyes, A. & Van Wees, S. C. M. Hormonal modulation of plant immunity. Annu. Rev. Cell Dev. Biol. 28, 489–521 (2012).
pubmed: 22559264
doi: 10.1146/annurev-cellbio-092910-154055
Bruessow, F., Gouhier-Darimont, C., Buchala, A., Metraux, J.-P. & Reymond, P. Insect eggs suppress plant defence against chewing herbivores. Plant J. 62, 876–885 (2010).
pubmed: 20230509
doi: 10.1111/j.1365-313X.2010.04200.x
Bi, J. L., Murphy, J. B. & Felton, G. W. Does salicylic acid act as a signal in cotton for induced resistance to Helicoverpa zea?. J. Chem. Ecol. 23, 1805–1818 (1997).
doi: 10.1023/B:JOEC.0000006452.81324.b8
Mur, L. A. J., Kenton, P., Atzorn, R., Miersch, O. & Wasternack, C. 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 (2006).
pubmed: 16377744
pmcid: 1326048
doi: 10.1104/pp.105.072348
Kerchev, P. I., Fenton, B., Foyer, C. H. & Hancock, R. D. Plant responses to insect herbivory: Interactions between photosynthesis, reactive oxygen species and hormonal signalling pathways. Plant Cell Environ. 35, 441–453 (2012).
pubmed: 21752032
doi: 10.1111/j.1365-3040.2011.02399.x
Wu, J. & Baldwin, I. T. Herbivory-induced signalling in plants: Perception and action. Plant Cell Environ. 32, 1161–1174 (2009).
pubmed: 19183291
doi: 10.1111/j.1365-3040.2009.01943.x
pmcid: 19183291
Lortzing, T. et al. Transcriptomic responses of Solanum dulcamara to natural and simulated herbivory. Mol. Ecol. Resour. 17, e196–e211 (2017).
pubmed: 28449359
doi: 10.1111/1755-0998.12687
pmcid: 28449359
Oberländer, J., Lortzing, V., Hilker, M. & Kunze, R. The differential response of cold-experienced Arabidopsis thaliana to larval herbivory benefits an insect generalist, but not a specialist. BMC Plant Biol. 19, 338 (2019).
pubmed: 31375063
pmcid: 6679549
doi: 10.1186/s12870-019-1943-3
Wegener, R., Schulz, S., Meiners, T., Hadwich, K. & Hilker, M. Analysis of volatiles induced by oviposition of elm leaf beetle Xanthogaleruca luteola on Ulmus minor. J. Chem. Ecol. 27, 499–515 (2001).
pubmed: 11441441
doi: 10.1023/A:1010397107740
pmcid: 11441441
Nguyen, D. et al. Interactive responses of Solanum dulcamara to drought and insect feeding are herbivore species-specific. Int. J. Mol. Sci. 19, 3845 (2018).
pmcid: 6321310
doi: 10.3390/ijms19123845
Appel, H. M. Phenolics in ecological interactions: The importance of oxidation. J. Chem. Ecol. 19, 1521–1552 (1993).
pubmed: 24249181
doi: 10.1007/BF00984895
pmcid: 24249181
Lattanzio, V., Kroon, P. A., Quideau, S. & Treutter, D. Plant phenolics—Secondary metabolites with diverse functions. Rec. Adv. Polyphenol Res. 1, 1–35 (2009).
Salminen, J. P., Karonen, M. & Sinkkonen, J. Chemical ecology of tannins: Recent developments in tannin chemistry reveal new structures and structure-activity patterns. Chemistry 17, 2806–2816 (2011).
pubmed: 21308809
doi: 10.1002/chem.201002662
Vogt, T. Phenylpropanoid biosynthesis. Mol. Plant 3, 2–20 (2010).
pubmed: 20035037
doi: 10.1093/mp/ssp106
War, A. R. et al. Mechanisms of plant defense against insect herbivores. Plant Signal. Behav. 7, 1306–1320 (2012).
pubmed: 22895106
pmcid: 3493419
doi: 10.4161/psb.21663
Yamane, H. et al. 4.08—Chemical defence and toxins of plants. in Comprehensive Natural Products II (2010). https://doi.org/10.1016/B978-008045382-8.00099-X
Austel, N., Eilers, E. J., Meiners, T. & Hilker, M. Elm leaves ‘warned’ by insect egg deposition reduce survival of hatching larvae by a shift in their quantitative leaf metabolite pattern. Plant Cell Environ. 39, 366–376 (2016).
pubmed: 26296819
doi: 10.1111/pce.12619
Becerra, J. X. On the factors that promote the diversity of herbivorous insects and plants in tropical forests. Proc. Natl. Acad. Sci. 112, 6098–6103 (2015).
pubmed: 25902509
doi: 10.1073/pnas.1418643112
Ritchie, M. E. et al. Limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 43, e47 (2015).
pubmed: 25605792
pmcid: 4402510
doi: 10.1093/nar/gkv007
Davis, J. W. Bioinformatics and computational biology solutions using R and Bioconductor. J. Am. Stat. Assoc. https://doi.org/10.1198/jasa.2007.s179 (2009).
doi: 10.1198/jasa.2007.s179
Gentleman, R. Bioinformatics and computational biology solutions using R and Bioconductor. J. Am. Stat. Assoc. https://doi.org/10.1007/0-387-29362-0 (2005).
doi: 10.1007/0-387-29362-0
R Core Team. R: A Language and Environment for Statistical Computing 55, 275–286 (2015).
Carlson, M. GO.db: A set of annotation maps describing the entire Gene Ontology. R Packag. version 3.4.0. (2016). https://doi.org/10.1016/j.healthplace.2012.12.005
Huber, W. et al. Orchestrating high-throughput genomic analysis with Bioconductor. Nat. Methods https://doi.org/10.1038/nmeth.3252 (2015).
doi: 10.1038/nmeth.3252
pubmed: 26524241
pmcid: 4629415
D’Agostino, N. et al. Genomic analysis of the native European Solanum species S. dulcamara. BMC Genomics 14, 356 (2013).
pubmed: 23713999
pmcid: 3680029
doi: 10.1186/1471-2164-14-356
Tarca, A. L., Bhatti, G. & Romero, R. A comparison of gene set analysis methods in terms of sensitivity, prioritization and specificity. PLoS ONE 8, e79217 (2013).
pubmed: 24260172
pmcid: 3829842
doi: 10.1371/journal.pone.0079217
Gu, Z., Eils, R. & Schlesner, M. Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics 32, 2847–2849 (2016).
pubmed: 27207943
doi: 10.1093/bioinformatics/btw313
Larson, J. et al. Area-Proportional Euler and Venn Diagrams with circles or ellipses. R Packag. version 4.1.0 (2018).
Geiselhardt, S. et al. Egg laying of Cabbage White butterfly (Pieris brassicae ) on Arabidopsis thaliana affects subsequent performance of the larvae. PLoS ONE 8, e59661 (2013).
pubmed: 23527243
pmcid: 3602411
doi: 10.1371/journal.pone.0059661
Pashalidou, F. G., Lucas-Barbosa, D., van Loon, J. J. A., Dicke, M. & Fatouros, N. E. Phenotypic plasticity of plant response to herbivore eggs: Effects on resistance to caterpillars and plant development. Ecology 94, 702–713 (2013).
pubmed: 23687896
doi: 10.1890/12-1561.1
Pashalidou, F. G. et al. To be in time: Egg deposition enhances plant-mediated detection of young caterpillars by parasitoids. Oecologia 177, 477–486 (2015).
pubmed: 25273955
doi: 10.1007/s00442-014-3098-0
Pashalidou, F. G. et al. Early herbivore alert matters: Plant-mediated effects of egg deposition on higher trophic levels benefit plant fitness. Ecol. Lett. 18, 927–936 (2015).
pubmed: 26147078
doi: 10.1111/ele.12470
Fatouros, N. E. et al. Plant volatiles induced by herbivore egg deposition affect insects of different trophic levels. PLoS ONE 7, e43607 (2012).
pubmed: 22912893
pmcid: 3422343
doi: 10.1371/journal.pone.0043607
Beyaert, I. et al. Can insect egg deposition ‘warn’ a plant of future feeding damage by herbivorous larvae?. Proc. R. Soc. B 279, 101–108 (2012).
pubmed: 21561977
doi: 10.1098/rspb.2011.0468