Skip to main content

Ecological Genomics of Plant-Insect Interactions: The Case of Wasp-Induced Galls

  • Chapter
  • First Online:
Evolutionary Ecology of Plant-Herbivore Interaction

Abstract

Plant-insect interactions are central to understand ecological and evolutionary dynamics that shaped phenotypes and genotypes. Although the interaction between host plants and insect herbivores has been widely assessed, the molecular mechanisms behind it are largely unknown. Here, we discuss the significance of the ecological genomics for the study of nonmodel species in the context of specialized herbivore interactions. First, we provide an overview of ecological genomics and review functional genomic studies addressing plant responses to herbivores. Second, using the oak-wasp interaction as a framework, we addressed the molecular mechanisms involved in the response of host plants to specialized phytophagous insects. We present a functional study of gene expression along the development of oak galls induced by cynipid insects. The transcriptomic profiles depicted show changes in gene regulation related to metabolism and cell cycle, which are consistent with the developmental trajectory of growing larvae. These findings suggest phenotype manipulation of the host plant by the wasp larvae and support the adaptive role of galls as a life history trait of insects. Our study provides insight of how the ecological genomics approach can contribute to elucidate the genetic bases of organism’s response to their environment and thus help to better understand species interactions and adaptation. In order to unravel the genetic control of natural variation, we suggest that future research should encompass applied ecology and evolution, molecular biology, and bioinformatic and genomic tools.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Abrahamson WG, Melika G, Scrafford R, Csóka G (1998) Gall- inducing insects provide insights into plant systematic relationships. Am J Bot 85:1159–1165

    Article  CAS  PubMed  Google Scholar 

  • Allison SD, Schultz JC (2005) Biochemical responses of chestnut oak to a galling cynipid. J Chem Ecol 31:151–166

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Askew RR (1984) The biology of gall wasps. In: Ananthakrishnan N (ed) Biology of gall insects. Edward Arnold, London, pp 223–271

    Google Scholar 

  • Barbehenn RV, Constabel PC (2011) Tannins in plant-herbivore interactions. Phytochemistry 72:1551–1565

    Article  CAS  PubMed  Google Scholar 

  • Bengston SE, Dahan RA, Donaldson Z, Phelps SM, Van Oers K, Sih A, Bell AM (2018) Genomic tools for behavioural ecologists to understand repeatable individual differences in behaviour. Nat Ecol Evol 2:944–955

    Article  PubMed  Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Broekgaarden C, Poelman EH, Steenhuis G, Voorrips RE, Dicke M, Vosman B (2007) Genotypic variation in genome-wide transcription profiles induced by insect feeding: Brassica oleracea – Pieris rapae interactions. BMC Genomics 8:239

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Broekgaarden C, Poelman EH, Voorrips RE, Dicke M, Vosman B (2010) Intraspecific variation in herbivore community composition and transcriptional profiles in field-grown Brassica oleracea cultivars. J Exp Bot 61:807–819

    Article  CAS  PubMed  Google Scholar 

  • Bronner R (1977) Contribution a l'etude histochimique des tissue nourriciers des zoocecidies. Marcellia 40:1–134

    CAS  Google Scholar 

  • Brooks SE, Shorthouse JD (1997) Biology of the rose stem galler Diplolepis nodulosa (Hymenoptera: Cinipidae) and its associated component community in Central Ontario. Can Entomol 129:1121–1140

    Article  Google Scholar 

  • Brooner R (1992) The role of nutritive cells in the nutrition of cynipids and cecidomyiids. In: Shorthouse JD, Rohfritsch O (eds) Biology of insect-induced galls. Oxford University Press, pp 118–140

    Google Scholar 

  • Buron-Moles G, Wisniewski M, Viñas I, Teixidó N, Usall J, Droby S, Torres R (2015) Characterizing the proteome and oxi-proteome of apple in response to a host (Penicillium expansum) and a non-host (Penicillium digitatum) pathogen. J Proteomics 114:136–151

    Article  CAS  PubMed  Google Scholar 

  • Civelek M, Lusis AJ (2014) Systems genetics approaches to understand complex traits. Nat Rev Genet 15:34–48

    Article  CAS  PubMed  Google Scholar 

  • Cornell HV (1983) The secondary chemistry and complex morphology of galls formed by the Cynipidae (Hymenoptera): why and how? Am Midl Nat 110:225–234

    Article  Google Scholar 

  • Csóka G, Stone GN, Melika G (2005) Biology, ecology and evolution of gall-inducing Cynipidae. In: Raman A, Schaefer CW, Withers TM (eds) Biology, ecology and evolution of gall-inducing arthropods. Science Publishers, New Hampshire, pp 569–636

    Google Scholar 

  • De la Mora M, Piñero D, Oyama K, Farrel B, Mgallón S, Núñez-Farfán J (2018) Evolution of Trichobaris (Curculionidae) in relation to host a plants: geometric morphometrics, phylogeny and phylogeography. Mol Phylogenet Evol 124:37–49

    Google Scholar 

  • De Vos M, Denekamp M, Dicke M, Vuylsteke M, Van Loon LC, Smeekens SCM, Pietersen C (2006) The Arabidopsis thaliana transcription factor AtMYB102 functions in defense against the insect herbivore Pieris rapae. Plant Signal Behav 1:305–311

    Article  PubMed  PubMed Central  Google Scholar 

  • Dicke M, Van Poecke RMP (2002) Signalling in plant-insect interactions: signal transduction in direct and indirect plant defence. In: Sheel C, Wasternack C (eds) Plant signal transduction. Oxford University Press, pp 289–316

    Google Scholar 

  • Edger PP, Heidel-Fischer HM, Bekaert M et al (2015) The butterfly plant arms-race escalated by gene and genome duplications. Proc Natl Acad Sci 112:8362–8366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ehrlich PR, Raven PH (1964) Butterflies and plants: a study in coevolution. Evolution 18:586–608

    Article  Google Scholar 

  • Eulgem T (2005) Regulation of the Arabidopsis defense transcriptome. Trends Plant Sci 10:71–78

    Article  CAS  PubMed  Google Scholar 

  • Feder ME, Mitchell-Olds T (2003) Evolutionary and ecological functional genomics. Nat Rev Genet 4:649–655

    Article  CAS  Google Scholar 

  • Feeny P (1976) Plant apparency and chemical defense. In: Wallace JW, Mansel RL (eds) Biochemical interaction between plants and insects. Plenum Press, New York, pp 1–40

    Google Scholar 

  • Forkner RE, Marquis RJ, Lill JT (2004) Feeny revisited: condensed tannins as anti-herbivore defences in leaf-chewing herbivore communities of Quercus. Ecol Entomol 29:174–187

    Article  Google Scholar 

  • Gibson G, Muse SV (2009) Primer of genome science. Sinauer Associates, Sunderland

    Google Scholar 

  • Gómez-Gómez L, Felix G, Boller T (1999) A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J 18:277–284

    Article  PubMed  Google Scholar 

  • Götz S, García-Gómez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, Robles M, Talon M, Dopazo J, Conesa A (2008) High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 36:3420–3435

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M et al (2011) Function search in a large transcription factor gene family in Arabidopsis: assessing the potential of reverse genetics to identify insertional mutations in R2R3 MYB genes. Nat Biotechnol 29:644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Griffiths AJ, Wessler SR, Lewontin RC, Gelbart WM, Suzuki DT, Miller JH (2005) An introduction to genetic analysis. Macmillan, New York

    Google Scholar 

  • Guzicka M, Karolewski P, Giertych MJ (2017) Structural modification of Quercus petraea leaf caused by Cynips quercusfolii–histological study of galls. J Plant Interact 12:7–13

    Article  CAS  Google Scholar 

  • Hahlbrock K, Scheel D (1989) Hysiology and molecular biology of phenylpropanoid metabolism. Annu Rev Plant Biol 40:347–369

    Article  CAS  Google Scholar 

  • Halitschke R, Baldwin IT (2003) Antisense LOX expression increases herbivore performance by decreasing defense responses and inhibiting growth-related transcriptional reorganization in Nicotiana attenuata. Plant J 36:794–807

    Article  CAS  PubMed  Google Scholar 

  • Hartley SE (1998) The chemical composition of plant galls: are levels of nutrients and secondary compounds controlled by the gall-former? Oecologia 113:492–501

    Article  CAS  PubMed  Google Scholar 

  • Heil M, Greiner S, Meimberg H, Kruger R, Noyer JL, Heubl G, Lisenmair KE, Boland W (2004) Evolutionary change from induced to constitutive expression of an indirect plant resistance. Nature 430:205–208

    Article  CAS  PubMed  Google Scholar 

  • Hernández-Soto P (2019) Transciptómica de la ontogenia presentada por la agalla inducida por Amphibolips michacaensis (Hymenoptera: Cynipidae) sobre su planta hospedera Quercus castanea. PhD Thesis, Universidad Nacional Autónoma de México

    Google Scholar 

  • Hernández-Soto P, Lara-Flores M, Agredano-Moreno L, Jiménez-García L, Cuevas-Reyes P, Oyama K (2015) Developmental morphology of bud galls induced on the vegetative meristems of Quercus castanea by Amphibolips michoacaensis (Hymenoptera: Cynipidae). Bot Sci 93:685–693

    Article  Google Scholar 

  • Holeski LM, Chase-Alone R, Kelly JK (2010) The genetics of phenotypic plasticity in plant defense: trichome production in Mimulus guttatus. Am Nat 175:391–400

    Article  PubMed  Google Scholar 

  • Holliday JA, Aitken SN, Cooke JE, Fady B, González-Martínez SC, Heuertz M, Plomion C (2017) Advances in ecological genomics in forest trees and applications to genetic resources conservation and breeding. Mol Ecol 26:706–717

    Article  PubMed  Google Scholar 

  • Horton MW, Bodenhausen N, Beilsmith K et al (2014) Genome-wide association study of Arabidopsis thaliana leaf microbial community. Nat Commun 5:5320

    Article  PubMed  Google Scholar 

  • Howe GA (2004) Jasmonates as signals in the wound response. J Plant Growth Regul 23:223–237

    Article  CAS  Google Scholar 

  • Howles PA, Sewalt VJH, Paiva NL, Elkind Y, Bate NJ, Lamb C, Dixon RA (1996) Overexpression of L-phenylalanine ammonia-lyase in transgenic tobacco plants reveals control points for flux into phenylpropanoid biosynthesis. Plant Physiol 112:1617–1624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jansen-González S, de Padua TS, Kjellberg F, Pereira RAS (2014) Same but different: larval development and gall-inducing process of a non-pollinating fig wasp compared to that of pollinating fig-wasps. Acta Oecol 57:44–50

    Article  Google Scholar 

  • Kariñho-Betancourt E, Hernández-Soto P, Rendón-Anaya M, Calderón-Cortés N, Oyama K (2019) Differential expression of genes associated with phenolic compounds in galls of Quercus castanea induced by Amphibolips michoacaensis. J Plant Interact 14:177–186

    Article  CAS  Google Scholar 

  • Kliebenstein DJ, Kroymann J, Brown PD, Figuth A, Pedersen D, Gershenzon J, Mitchell-Olds T (2001) Genetic control of natural variation in Arabidopsis glucosinolate accumulation. Plant Physiol 126:811–825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kliebenstein DJ, Pedersen D, Barker B, Mitchell-Olds T (2002) Comparative analysis of quantitative trait loci controlling glucosinolates, myrosinase and insect resistance in Arabidopsis thaliana. Genetics 161:325–332

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koes RE, Quattrocchio F, Mol JNM (1994) The flavonoid biosynthetic pathway in plants: function and evolution. BioEssays 16:123–132

    Article  CAS  Google Scholar 

  • Liljeblad J, Ronquist F (1998) A phylogenetic analysis of higher-level gall wasp relationships (Hymenoptera: Cynipidae). Syst Entomol 23:229–252

    Article  Google Scholar 

  • Luo J, Xia W, Cao P, Xiao ZA, Zhang Y, Liu M et al (2019) Integrated transcriptome analysis reveals plant hormones jasmonic acid and salicylic acid coordinate growth and defense responses upon fungal infection in poplar. Biomol Ther 9:12

    Google Scholar 

  • Martin C, Smith AM (1995) Strach biosynthesis. Plant Cell 7:971–985

    CAS  PubMed  PubMed Central  Google Scholar 

  • Martin GB, Bogdanove AJ, Sessa G (2003) Understanding the functions of plant disease resistance proteins. Annu Rev Plant Biol 54:23–61

    Article  CAS  PubMed  Google Scholar 

  • May GD (2002) An integrated approach to Medicago functional genomics. In: Romeo JT, Dixon RA (eds) Phytochemistry in the genomics and post-genomics eras. Elsevier Science Ltd, Oxford, pp 179–195

    Chapter  Google Scholar 

  • Meyer J, Maresquelle HJ (1983) Anatomie des Galles. Gebrüder Borntraeger, Berlin

    Google Scholar 

  • Moctezuma C, Hammerbacher A, Heil M, Gershenzon J, Méndez-Alonzo R, Oyama K (2014) Specific polyphenols and tannins are associated with defense against insect herbivores in the tropical oak Quercus oleoides. J Chem Ecol 40:458–467

    Article  CAS  PubMed  Google Scholar 

  • Moyano E, Jouhikainen K, Tammela P, Palazón P, Palazón J, Cusidó RM, Piñol MT, Teeri TH, Oksman-Caldentey KM (2003) Effect of pmt gene overexpression on tropane alkaloid production in transformed root cultures of Datura metel and Hyoscyamus muticus. J Exp Bot 54:203–211

    Article  CAS  PubMed  Google Scholar 

  • Muir SR, Collins GJ, Robinson S, Hughes S, Bovy A, Ric De Vos CH, van Tunen AJ, Verhoeyen ME (2001) Overexpression of petunia chalcone isomerase in tomato results in fruit containing increased levels of flavonols. Nat Biotechnol 19:470–474

    Article  CAS  PubMed  Google Scholar 

  • Nyman T, Julkunen-Tiitto R (2000) Manipulation of the phenolic chemistry of willows by gall-inducing sawflies. Proc Natl Acad Sci 97:13184–13187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Orsucci M, Navajas M, Fellous S (2017) Genotype-specific interactions between parasitic arthropods. Heredity 118:260–265

    Article  CAS  PubMed  Google Scholar 

  • Pascual-Alvarado E, Cuevas-Reyes P, Quesada M, Oyama K (2008) Interactions between galling insects and leaf-feeding insects: the role of plant phenolic compounds and their possible interference with herbivores. J Trop Ecol 24:329–336

    Article  Google Scholar 

  • Pavey SA, Bernatchez L, Aubin-Horth N, Landry CR (2012) What is needed for next-generation ecological and evolutionary genomics? Trends Ecol Evol 27:673–678

    Article  PubMed  Google Scholar 

  • Pearse IS, Hipp AL (2012) Global patterns of leaf defenses in oak species. Evolution 66:2272–2286

    Article  PubMed  Google Scholar 

  • Pevsner J (2015) Bioinformatics and functional genomics. Wiley

    Google Scholar 

  • Philippe R, Hans W, Martine D, Edward EF (2000) Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12:707–719

    Article  Google Scholar 

  • Poland JA, Bradbury PJ, Buckler ES, Nelson RJ (2011) Genome-wide nested association mapping of quantitative resistance to northern leaf blight in maize. Proc Natl Acad Sci 108:6893–6898

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prestidge RA (1992) Population biology and parasitism of Hessian fly (Mayetiola destructor) (Diptera: Cecidomyiidae) on Bromus willdenowii in New Zealand. New Zeal J Agr Res 35:423–428

    Article  Google Scholar 

  • Price PW (2005) Adaptive radiation of gall-inducing insects. Basic Appl Ecol 6:413–421

    Article  Google Scholar 

  • Price PW, Waring GL, Fernandes GW (1986) Hypotheses on the adaptive nature of galls. Proc Entomol Soc Wash 88:361–363

    Google Scholar 

  • Price PW, Fernandes GW, Waring GL (1987) Adaptive nature of insect galls. Environ Entomol 16:15–24

    Article  Google Scholar 

  • R Development Core Team (2014) R: a language and environment for statistical computing (Computer software manual). R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Raman A, Dhileepan K (1999) Qualitative evaluation of damage by Epiblema strenuana (Lepidoptera: Tortricidae) to the weed Parthenium hysterophorus (Asteraceae). Ann Entomol Soc Am 92:717–723

    Article  Google Scholar 

  • Raman A, Schafer CW, Withers TM (2005) Galls and gall-inducing arthropods: an overview of their biology, ecology, and evolution. In: Biology, ecology, and evolution of gall-inducing arthropods. Science Publishers, Inc., Enfield, pp 1–33

    Google Scholar 

  • Reale L, Tedeschini E, Rondoni G, Ricci C, Bin F, Frenguelli G, Ferranti F (2016) Histological investigation on gall development induced by a worldwide invasive pest, Dryocosmus kuriphilus, on Castanea sativa. Plant Biosyst 150:35–42

    Article  Google Scholar 

  • Redfern M (2011) Plant galls. Collins, London

    Google Scholar 

  • Rendón-Anaya M, Ibarra-Ladette E, Méndez-Bravo A, Lan T, Zheng C, Carretero-Paulet L et al (2019) The avocado genome informs deep angiosperm phylogeny, highlights introgressive hybridization, and reveals pathogen-influenced gene space adaptation. Proc Natl Acad Sci 116:17081–17089

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rey LA (1992) Developmental morphology of two types of hymenopterous galls. In: Shorthouse JD, Rohfritsch O (eds) Biology of insect induced galls. Oxford University Press, Oxford, pp 87–101

    Google Scholar 

  • Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140

    Article  CAS  PubMed  Google Scholar 

  • Roskov Y, Abucay L, Orrell T, Nicolson D, Bailly N, Kirk PM, Bourgoin T, RE DW, Decock W, DeWever A, Nieukerken E v, Zarucchi J, Penev L (eds) (2018) Species 2000 & ITIS catalogue of life, 2018 annual checklist. Digital resource at www.catalogueoflife.org/annual-checklist/2018. Species 2000: Naturalis, Leiden

    Google Scholar 

  • Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15:247–258

    Article  CAS  PubMed  Google Scholar 

  • Salih H, Gong W, He S, Sun G, Sun J, Du X (2016) Genome-wide characterization and expression analysis of MYB transcription factors in Gossypium hirsutum. BMC Genet 17:129

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schultz BB (1992) Insect herbivores as potential causes of mortality and adaptation in gall forming insects. Oecologia 90:297–299

    Article  CAS  PubMed  Google Scholar 

  • Shirley BW (1996) Flavonoid biosynthesis: “new” functions for and “old” pathway. Trends Plant Sci 1:377–382

    Google Scholar 

  • Stafford HA (1990) Flavonoid metabolism. CRC Press, Boca Raton

    Google Scholar 

  • Stone GN, Schönrogge K (2003) The adaptive significance of insect gall morphology. Trends Ecol Evol 18:512–522

    Article  Google Scholar 

  • Stone GN, Schönrogee K, Atkinson RJ, Bellido D, Pujade-Villar J (2002) The population biology of oak gall wasps. Annu Rev Entomol 47:633–668

    Article  CAS  PubMed  Google Scholar 

  • Straalen NM, Roelofs D (2012) An introduction to ecological genomics. Oxford University, Oxford

    Google Scholar 

  • Strong DR, Lawton JH, Southwood SR (1984) Insects on plants. Community patterns and mechanisms. Blackwell Scientific Publicatons, Oxford

    Google Scholar 

  • Taper ML, Case TJ (1987) Oecologia and parasite community structure. Oecologia 71:254–261

    Article  CAS  PubMed  Google Scholar 

  • Tetlow IJ, Morell MK, Emes MJ (2004) Recent developments in understanding the regulation of starch metabolism in higher plants. J Exp Bot 55:2131–2145

    Article  CAS  PubMed  Google Scholar 

  • Thompson GA, Goggin FL (2006) Transcriptomics and functional genomics of plant defence induction by phloem-feeding insects. J Exp Bot 57:755–766

    Article  CAS  PubMed  Google Scholar 

  • Tooker JF, Rohr JR, Abrahamson WG, De Moraes CM (2008) Gall insects can avoid and alter indirect plant defenses. New Phytol 178:657–671

    Article  CAS  PubMed  Google Scholar 

  • Traw B, Bergelson J (2003) Interactive effects of jasmonic acid, salicylic acid, and gibberellin on induction of trichomes in Arabidopsis. Plant Physiol 133:1367–1375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ungerer MC, Johnson LC, Herman MA (2008) Ecological genomics: understanding gene and genome function in the natural environment. Heredity (Edinb) 100:178–183

    Article  CAS  Google Scholar 

  • Valencia S (2004) Diversidad del género Quercus (Fagaceae) en México. B Soc Bot Mex 75:33–35

    Google Scholar 

  • Wen Z, Tan R, Yuan J et al (2014) Genome-wide association mapping of quantitative resistance to sudden death syndrome in soybean. BMC Genomics 15:809

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wickham H (2016) Ggplot2: elegant graphics for data analysis. Springer-Verlag, New York

    Book  Google Scholar 

  • Winkel-Shirley B (1999) Evidence for enzyme complexes in the phenylpropanoid and flavonoid pathways. Physiol Plant 107:142–149

    Article  CAS  Google Scholar 

  • Wise RR (2007) The diversity of plastid form and function. In: Wise RR, Hoober JK (eds) The structure and function of plastids. Springer, Dordrecht, pp 3–26

    Chapter  Google Scholar 

  • Wool D, Aloni R, Ben-Zvi O, Wollberg M (1999) A galling aphid furnishes its home with a built-in pipeline to the host food supply. Entomol Exp Appl 91:183–186

    Article  Google Scholar 

  • Wróblewski T, Spiridon L, Martin EC, Petrescu AJ, Cavanaugh K, Jose-Truco M et al (2018) Genome-wide functional analyses of plant coiled–coil NLR-type pathogen receptors reveal essential roles of their N-terminal domain in oligomerization, networking, and immunity. PLoS Biol 16:e2005821

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yan Y, Zheng X, Apaliya MT, Yang H, Zhang H (2018) Transcriptome characterization and expression profile of defense-related genes in pear induced by Meyerozyma guilliermondii. Postharvest Biol Technol 141:63–70

    Article  CAS  Google Scholar 

  • Yuan YW, Byers KJ, Bradshaw HD Jr (2013) The genetic control of flower–pollinator specificity. Curr Opin Plant Biol 16:422–428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeeman SC, Kossmann J, Smith AM (2010) Starch: its metabolism, evolution, and biotechnological modification in plants. Annu Rev Plant Biol 61:209–234

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Liu CJ (2015) Multifaceted regulations of gateway enzyme phenylalanine ammonia-lyase in the biosynthesis of phenylpropanoids. Mol Plant 8:17–27

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Wang L (2005) The WRKY transcription factor superfamily: its origin in eukaryotes and expansion in plants. BMC Evol Biol 5:1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng S-J, Dicke M (2008) Ecological genomics of plant-insect interactions: from gene to community. Plant Physiol 146:812–817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhong R, Demura T, Ye Z-H (2006) SND1, a NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of Arabidopsis. Plant Cell 18:3158–3170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zipfel C (2008) Pattern-recognition receptors in plant innate immunity. Curr Opin Immunol 20:10–16

    Article  CAS  PubMed  Google Scholar 

  • Züst T, Heichinger C, Grossniklaus U, Harrington R, Kliebenstein DJ, Turnbull LA (2012) Natural enemies drive geographic variation in plant defenses. Science 338:116–119

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

EKB acknowledges the financial support of postdoctoral fellowship by the General Directorate for Academic Development Matters (DGAPA, UNAM). NCC acknowledges the financial support by CONACyT CB-2015-253420 and DGAPA-UNAM, PAPIIT IA200918, IN217420.This project was supported by SEMARNAT-CONACYT grants 2004-C01-97, 2006-23728, CONACYT 38550-V, 2007-80493, CB-2015-253420 and DGAPAUNAM grants IN209108, IN229803 and IV201015.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ken Oyama .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Betancourt, E.K., Soto, P.H., Cortés, N.C., Anaya, M.R., Estrella, A.H., Oyama, K. (2020). Ecological Genomics of Plant-Insect Interactions: The Case of Wasp-Induced Galls. In: Núñez-Farfán, J., Valverde, P. (eds) Evolutionary Ecology of Plant-Herbivore Interaction. Springer, Cham. https://doi.org/10.1007/978-3-030-46012-9_17

Download citation

Publish with us

Policies and ethics