Genomic dissection of an extended phenotype: Oak galling by a cynipid gall wasp

1. Meyer J, Maresquelle HJ. Anatomie des galles. Berlin: Gebrüder Borntraeger; 1983.

2. Rohfritsch O, Shorthouse JD, Braun AC, Kahl G, Schell JS. Insect galls. Academic Press; 1982.

3. Dorchin N, Cramer MD, Hoffmann JH. Photosynthesis and sink activity of wasp-induced galls in Acacia pycnantha. Ecology. Wiley Online Library; 2006;87: 1781–1791. doi: 10.1890/0012-9658(2006)87[1781:pasaow]2.0.co;2 16922327

4. Larson KC, Whitham TG. Manipulation of food resources by a gall-forming aphid: the physiology of sink-source interactions. Oecologia. Springer; 1991;88: 15–21. doi: 10.1007/BF00328398 28312726

5. Abrahamson WG, McCrea KD. Nutrient and biomass allocation in Solidago altissima: effects of two stem gallmakers, fertilization, and ramet isolation. Oecologia. Springer; 1986;68: 174–180. doi: 10.1007/BF00384784 28310124

6. Oates CN, Denby KJ, Myburg AA, Slippers B, Naidoo S. Insect gallers and their plant hosts: from omics data to systems biology. Int J Mol Sci. Multidisciplinary Digital Publishing Institute; 2016;17: 1891.

7. Poole P, Ramachandran V, Terpolilli J. Rhizobia: from saprophytes to endosymbionts. Nat Rev Microbiol. Nature Publishing Group; 2018;16: 291. doi: 10.1038/nrmicro.2017.171 29379215

8. Martinson EO, Hackett JD, Machado CA, Arnold AE. Metatranscriptome Analysis of Fig Flowers Provides Insights into Potential Mechanisms for Mutualism Stability and Gall Induction. PLoS One. 2015;10: e0130745. doi: 10.1371/journal.pone.0130745 26090817

9. Cook JM, Rasplus J-Y. Mutualists with attitude: coevolving fig wasps and figs. Trends Ecol Evol. Elsevier; 2003;18: 241–248.

10. Cook JM, West SA. Figs and fig wasps. Curr Biol. Elsevier; 2005;15: R978—R980. doi: 10.1016/j.cub.2005.11.057 16360672

11. Wesemael W, Viaene N, Moens M. Root-knot nematodes (Meloidogyne spp.) in Europe. Nematology. Brill; 2011;13: 3–16.

12. Csóka G, Stone GN, Melika G. Non-native gall-inducing insects on forest trees: a global review. Biol Invasions. Springer; 2017;19: 3161–3181.

13. Escobar MA, Dandekar AM. Agrobacterium tumefaciens as an agent of disease. Trends Plant Sci. Elsevier; 2003;8: 380–386. doi: 10.1016/S1360-1385(03)00162-6 12927971

14. Hoffmann JH, Impson FAC, Moran VC, Donnelly D. Biological control of invasive golden wattle trees (Acacia pycnantha) by a gall wasp, Trichilogaster sp.(Hymenoptera: Pteromalidae), in South Africa. Biol Control. Elsevier; 2002;25: 64–73.

15. Story JM, Smith L, Corn JG, White LJ. Influence of seed head-attacking biological control agents on spotted knapweed reproductive potential in western Montana over a 30-year period. Environ Entomol. Oxford University Press Oxford, UK; 2008;37: 510–519.

16. Lacroix B, Citovsky V. Pathways of DNA Transfer to Plants from Agrobacterium tumefaciens and Related Bacterial Species. Annu Rev Phytopathol. Annual Reviews; 2019;57: 231–251. doi: 10.1146/annurev-phyto-082718-100101 31226020

17. Le Fevre R, Evangelisti E, Rey T, Schornack S. Modulation of host cell biology by plant pathogenic microbes. Annu Rev Cell Dev Biol. Annual Reviews; 2015;31: 201–229. doi: 10.1146/annurev-cellbio-102314-112502 26436707

18. Abad P, Gouzy J, Aury J-M, Castagnone-Sereno P, Danchin EGJ, Deleury E, et al. Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nat Biotechnol. 2008;26: 909–15. doi: 10.1038/nbt.1482 18660804

19. Mejias J, Truong NM, Abad P, Favery B, Quentin M. Plant proteins and processes targeted by parasitic nematode effectors. Front Plant Sci. Frontiers Media SA; 2019;10.

20. Rehman S, Gupta VK, Goyal AK. Identification and functional analysis of secreted effectors from phytoparasitic nematodes. BMC Microbiol. BioMed Central; 2016;16: 48. doi: 10.1186/s12866-016-0632-8 27001199

21. Stuart JJ, Chen M-S, Shukle R, Harris MO. Gall midges (Hessian flies) as plant pathogens. Annu Rev Phytopathol. 2012;50: 339–57. doi: 10.1146/annurev-phyto-072910-095255 22656645

22. Chen M-S, Fellers JP, Zhu YC, Stuart JJ, Hulbert S, El-Bouhssini M, et al. A super-family of genes coding for secreted salivary gland proteins from the Hessian fly, Mayetiola destructor. J Insect Sci. 2006;6: 12. doi: 10.1673/2006.06.12.1 19537963

23. Zhao C, Shukle R, Navarro-Escalante L, Chen M, Richards S, Stuart JJ. Avirulence gene mapping in the Hessian fly (Mayetiola destructor) reveals a protein phosphatase 2C effector gene family. J Insect Physiol. 2016;84: 22–31. doi: 10.1016/j.jinsphys.2015.10.001 26439791

24. Aggarwal R, Subramanyam S, Zhao C, Chen M-S, Harris MO, Stuart JJ. Avirulence effector discovery in a plant galling and plant parasitic arthropod, the Hessian fly (Mayetiola destructor). PLoS One. Public Library of Science; 2014;9: e100958. doi: 10.1371/journal.pone.0100958 24964065

25. Schultz JC, Edger PP, Body MJA, Appel HM. A galling insect activates plant reproductive programs during gall development. Sci Rep. 2019;9: 1833. doi: 10.1038/s41598-018-38475-6 30755671

26. Nabity PD, Haus MJ, Berenbaum MR, DeLucia EH. Leaf-galling phylloxera on grapes reprograms host metabolism and morphology. Proc Natl Acad Sci. National Acad Sciences; 2013;110: 16663–16668. doi: 10.1073/pnas.1220219110 24067657

27. Raman A, Schaefer CW, Withers TM, others. Biology, ecology, and evolution of gall-inducing arthropods. Boca Raton: CRC Press; 2005.

28. Rohfritsch O. Patterns in gall development. In: Shorthouse JD, Rohfritsch O, editors. Biology of insect-induced galls. Oxford University Press: New York; 1992. pp. 60–86.

29. Stone GN, Schönrogge K. The adaptive significance of insect gall morphology. Trends Ecol Evol. 2003;18: 512–522. doi: 10.1016/S0169-5347(03)00247-7

30. Dawkins R. The Extended Phenotype. Oxford: Oxford University Press; 1989.

31. Crespi B, Worobey M. Comparative Analysis of Gall Morphology in Australian Gall Thrips: The Evolution of Extended Phenotypes. Evolution (N Y). 1998; 1686–1696.

32. Stone GN, Cook JM. The structure of cynipid oak galls: patterns in the evolution of an extended phenotype. Proc R Soc B Biol Sci. 1998;265. doi: 10.1098/rspb.1998.0387

33. Kutsukake M, Meng X-Y, Katayama N, Nikoh N, Shibao H, Fukatsu T. An insect-induced novel plant phenotype for sustaining social life in a closed system. Nat Commun. Nature Publishing Group; 2012;3: 1187. doi: 10.1038/ncomms2187 23149732

34. Stern DL. Phylogenetic evidence that aphids, rather than plants, determine gall morphology. Proc R Soc London Ser B Biol Sci. The Royal Society London; 1995;260: 85–89.

35. Giron D, Huguet E, Stone GN, Body M. Insect-induced effects on plants and possible effectors used by galling and leaf-mining insects to manipulate their host-plant. J Insect Physiol. 2015;84: 70–89. doi: 10.1016/j.jinsphys.2015.12.009 26723843

36. Tooker JF, Helms AM. Phytohormone Dynamics Associated with Gall Insects, and their Potential Role in the Evolution of the Gall-Inducing Habit. J Chem Ecol. 2014;40: 742–753. doi: 10.1007/s10886-014-0457-6 25027764

37. Csóka G, Stone GN, Melika G. The biology, ecology and evolution of Gall-inducing Cynipidae. In: Raman C, Schaefer W, Withers TM, editors. Biology, ecology and evolution of gall inducing insects. Boca Raton: CRC Press; 2005. pp. 573–642.

38. Bailey R, Schönrogge K, Cook JM, Melika G, Csóka G, Thúroczy C, et al. Host niches and defensive extended phenotypes structure parasitoid wasp communities. PLoS Biol. 2009;7: e1000179. doi: 10.1371/journal.pbio.1000179 19707266

39. Ronquist F, Liljeblad J. Evolution of the gall wasp—host plant association. Evolution (N Y). 2001;55: 2503–2522.

40. Shorthouse JD, Leggo JJ, Sliva MD, Lalonde RG. Has egg location influenced the radiation of Diplolepis (Hymenoptera: Cynipidae) gall wasps on wild roses? Basic Appl Ecol. 2005;6: 423–434. doi: 10.1016/j.baae.2005.07.006

41. Hough JS. Studies on the common spangle gall of oak. New Phytol. 1953;52: 149–177.

42. Stone GN, Hernandez-Lopez A, Nicholls JA, di Pierro E, Pujade-Villar J, Melika G, et al. Extreme host plant conservatism during at least 20 million years of host plant pursuit by oak gallwasps. Evolution (N Y). 2009;63: 854–869.

43. Hough JS. Studies on the common spangle gall of oak: II. A general consideration of past work on gall induction. New Phytol. 1953;52: 218–228.

44. Rey L. La galle de Biorhiza pallida Bosc. Sur la racine de Quercus pedunculata Ehrh.: observation de la ponte et de les premières réactions de l’hôte. Comptes rendus l’Académie des Sci. 1967;264: 2891–2894.

45. Rey L. La galle de Biorhiza pallida Ol. Etude préliminaire du bourgeon de Quercus pedunculata Ehrh. au moment de l’attaque du parasite. Bull la Société Bot Fr. 1966;113: 503–514.

46. Garbin L, Durfort M, Diaz NB, Pujade-Villar J. Histological Modifications on Quercus suber Twigs (Fagaceae) Caused by the Gallwasp Plagiotrochus suberi (Hymenoptera: Cynipidae). Entomol Gen. 2005;28: 91–102.

47. Derory J, Léger P, Garcia V, Schaeffer J, Hauser MT, Salin F, et al. Transcriptome analysis of bud burst in sessile oak (Quercus petraea). New Phytol. 2006;170: 723–738. doi: 10.1111/j.1469-8137.2006.01721.x 16684234

48. Plomion C, Aury J-M, Amselem J, Leroy T, Murat F, Duplessis S, et al. Oak genome reveals facets of long lifespan. Nat Plants. Nature Publishing Group; 2018;4: 440. doi: 10.1038/s41477-018-0172-3 29915331

49. Cambier S, Ginis O, Moreau SJM, Gayral P, Hearn J, Stone GN, et al. Gall wasp transcriptomes unravel potential effectors involved in molecular dialogues with oak and rose bushes. Front Physiol. 2019;10: 926. doi: 10.3389/fphys.2019.00926 31396099

50. Hearn J, Stone GN, Bunnefeld L, Nicholls JA, Barton NH, Lohse K. Likelihood-based inference of population history from low-coverage de novo genome assemblies. Mol Ecol. 2014;3643: 198–211. doi: 10.1111/mec.12578 24188568

51. Bunnefeld L, Hearn J, Stone GN, Lohse K. Whole-genome data reveal the complex history of a diverse ecological community. Proc Natl Acad Sci. 2018;115: E6507–E6515. doi: 10.1073/pnas.1800334115 29946026

52. Nicholls JA, Melika G, Stone GN. Sweet Tetra-Trophic Interactions: Multiple Evolution of Nectar Secretion, a Defensive Extended Phenotype in Cynipid Gall Wasps. Am Nat. 2017;189: 67–77. doi: 10.1086/689399 28035894

53. Cook JM, Rokas A, Pagel M, Stone GN. Evolutionary shift between host oak section and host-plant organs in Andricus gallwasps. Evolution (N Y). 2002;56: 1821–1830.

54. Ronquist F, Nieves-Aldrey J-L, Buffington ML, Liu Z, Liljeblad J, Nylander JAA. Phylogeny, evolution and classification of gall wasps: the plot thickens. PLoS One. 2015;10: e0123301. doi: 10.1371/journal.pone.0123301 25993346

55. Phylogeny Ronquist F., classification and evolution of the Cynipoidea. Zool Scr. 1999;28: 139–164. doi: 10.1046/j.1463-6409.1999.00022.x

56. Beyerinck MW. Beobachtungen ueber die ersten Entwicklungsphasen einiger Cynipidengallen. Amsterdam: Mueller; 1882;

57. Brooks SE, Shorthouse JD. Developmental morphology of stem galls of Diplolepis nodulosa (Hymenoptera: Cynipidae) and those modified by the inquiline Periclistus pirata (Hymenoptera: Cynipidae) on Rosa blanda (Rosaceae). Can J Bot. NRC Research Press; 1998;76: 365–381.

58. Rey L. Particular aspects of the endoplasmic reticulum observed during the evolution of the nutrient cells of the gall caused by Biorhiza pallida [Quercus]. Comptes Rendus Hebd des Seances l’Academie des Sci Ser D. 1975;

59. Harper LJ, Schönrogge K, Lim KY, Francis P, Lichtenstein CP. Cynipid galls: insect-induced modifications of plant development create novel plant organs. Plant Cell Environ. 2004;27: 327–335.

60. Schönrogge K, Harper LJ, Lichtenstein CP. The protein content of tissues in cynipid galls (Hymenoptera: Cynipidae): Similarities between cynipid galls and seeds. Plant Cell Environ. 2000;23: 215–222.

61. Atkinson RJ, Brown GS, Stone GN. Skewed sex ratios and multiple founding in galls of the oak apple gall wasp Biorhiza pallida. Ecol Entomol. 2003;28: 14–24.

62. Folliot R. Les insectes cécidogènes et la cécidogenèse. Trait Zool Anat systématique, Biol. 1977;8: 389–429.

63. Bronner R. The role of nutritive cells in the nutrition of cynipids and cecidomyiids. In: Shorthouse JD, Rohfritsch O, editors. Biology of insect-induced galls. New York: Oxford University Press; 1992. pp. 118–140.

64. Shorthouse JD, Rohfritsch O. Biology of insect-induced galls. New York, USA: Oxford University Press; 1992.

65. Bagatto G, Paquette LC, Shorthouse JD. Influence of galls of Phanacis taraxaci on carbon partitioning within common dandelion, Taraxacum officinale. Entomol Exp Appl. 1996;79: 111–117.

66. Rey L. La galle de Biorhiza pallida Ol.: stades ultérieurs de développement. Marcellia. 1971;37: 193–218.

67. Sinclair FH, Stone GN, Nicholls JA, Cavers S, Gibbs M, Butterill P, et al. Impacts of local adaptation of forest trees on associations with herbivorous insects: implications for adaptive forest management. Evol Appl. Wiley Online Library; 2015;8: 972–987. doi: 10.1111/eva.12329 26640522

68. Hartley SE, Lawton JH. Host-plant manipulation by gall-insects: a test of the nutrition hypothesis. J Anim Ecol. JSTOR; 1992; 113–119.

69. Allison SD, Schultz JC. Biochemical responses of chestnut oak to a galling cynipid. J Chem Ecol. 2005;31: 151–166. 15839487

70. Elborough K, Winz R, Deka R, Markham J, White A, Rawsthorne S, et al. Biotin carboxyl carrier protein and carboxyltransferase subunits of the multi-subunit form of acetyl-CoA carboxylase from Brassica napus: cloning and analysis of expression during oilseed rape embryogenesis. Biochem J. 1996;315: 103–112. doi: 10.1042/bj3150103 8670092

71. Wilhelm E. Somatic embryogenesis in oak (Quercus spp.). Vitr Cell Dev Biol—Plant. 2000;36: 349–357. doi: 10.1007/s11627-000-0062-y

72. Gibson CM, Hunter MS. Extraordinarily widespread and fantastically complex: Comparative biology of endosymbiotic bacterial and fungal mutualists of insects. Ecol Lett. 2010;13: 223–234. doi: 10.1111/j.1461-0248.2009.01416.x 20015249

73. Kaiser W, Huguet E, Casas J, Commin C, Giron D. Plant green-island phenotype induced by leaf-miners is mediated by bacterial symbionts. Proc R Soc B Biol Sci. 2010;277: 2311–2319. doi: 10.1098/rspb.2010.0214 20356892

74. Bansal R, Hulbert S, Schemerhorn B, Reese JC, Whitworth RJ, Stuart JJ, et al. Hessian Fly-Associated Bacteria: Transmission, Essentiality, and Composition. PLoS One. 2011;6: e23170. doi: 10.1371/journal.pone.0023170 21858016

75. Joy JB. Symbiosis catalyses niche expansion and diversification. Proc Biol Sci. 2013;280: 20122820. doi: 10.1098/rspb.2012.2820 23390106

76. Nelson LA, Davies KA, Scheffer SJ, Taylor GS, Purcell MF, Giblin-Davis RM, et al. An emerging example of tritrophic coevolution between flies (Diptera: Fergusoninidae) and nematodes (Nematoda: Neotylenchidae) on myrtaceae host plants. Biol J Linn Soc. 2014;111: 699–718. doi: 10.1111/bij.12237

77. Borkent A, Bissett J. Gall midges (Diptera: Cecidomyiidae) are vectors for their fungal symbionts. Symbiosis (USA). 1985;

78. Joy JB. Symbiosis catalyses niche expansion and diversification. Proc R Soc B Biol Sci. 2013;280.

79. Cornell HV. The Secondary Chemistry and Complex Morphology of Galls Formed by the Cynipinae (Hymenoptera): Why and How? Am Midl Nat. 1983;110: 225–234. doi: 10.2307/2425263

80. Bézier A, Annaheim M, Herbinière J, Wetterwald C, Gyapay G, Bernard-Samain S, et al. Polydnaviruses of Braconid Wasps Derive from an Ancestral Nudivirus. Science (80-). 2009;323: 926–930. doi: 10.1126/science.1166788 19213916

81. Drezen J-M, Leobold M, Bezier A, Huguet E, Volkoff A-N, Herniou EA. Endogenous viruses of parasitic wasps: variations on a common theme. Curr Opin Virol. Elsevier; 2017;25: 41–48. doi: 10.1016/j.coviro.2017.07.002 28728099

82. Rizki RM, Rizki TM. Parasitoid virus-like particles destroy Drosophila cellular immunity. Proc Natl Acad Sci. National Acad Sciences; 1990;87: 8388–8392. doi: 10.1073/pnas.87.21.8388 2122461

83. H R. Von welchen Organen der Gallwespenlarve geht der Reiz zur Bildung der Pflanzengalle aus? Zoologischer Jahrbücher. Abteilung für Syst Geogr und Biol der Tiere. 1904;20: 19–90.

84. Roth P. Beiträge zur Biologie der Gallwespen. Verhandlungen der Naturforscher Gesellschaft Basel. 1949;60: 104–178.

85. Westermann AJ, Gorski SA, Vogel J. Dual RNA-seq of pathogen and host. Nat Rev Microbiol. 2012;10: 618–630. doi: 10.1038/nrmicro2852 22890146

86. Nabity PD. Insect-induced plant phenotypes: Revealing mechanisms through comparative genomics of galling insects and their hosts. Am J Bot. 2016;103: 979–981. doi: 10.3732/ajb.1600111 27257007

87. Zhu C, Shi F, Chen Y, Wang M, Zhao Y, Geng G. Transcriptome Analysis of Chinese Chestnut (Castanea mollissima Blume) in Response to Dryocosmus kuriphilus Yasumatsu Infestation. Int J Mol Sci. Multidisciplinary Digital Publishing Institute; 2019;20: 855.

88. Jia XY, He LH, Jing RL, Li RZ. Calreticulin: Conserved protein and diverse functions in plants. Physiol Plant. 2009;136: 127–138. doi: 10.1111/j.1399-3054.2009.1223.x 19453510

89. Zürcher E, Liu J, di Donato M, Geisler M, Müller B. Plant development regulated by cytokinin sinks. Science (80-). 2016;353: 1027–1030. doi: 10.1126/science.aaf7254 27701112

90. Seo M, Akaba S, Oritani T, Delarue M, Bellini C, Caboche M, et al. Higher Activity of an Aldehyde Oxidase in the Auxin-Overproducing superroot 1 mutant of Arabidopsis thaliana. Plant Physiol. Am Soc Plant Biol; 1998;116: 687–693. doi: 10.1104/pp.116.2.687 9489015

91. Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP. Prediction of plant microRNA targets. Cell. Elsevier; 2002;110: 513–520. doi: 10.1016/s0092-8674(02)00863-2 12202040

92. Iwama A, Yamashino T, Tanaka Y, Sakakibara H, Kakimoto T, Sato S, et al. AHK5 histidine kinase regulates root elongation through an ETR1-dependent abscisic acid and ethylene signaling pathway in Arabidopsis thaliana. Plant cell Physiol. Oxford University Press; 2007;48: 375–380. doi: 10.1093/pcp/pcl065 17202180

93. Tran L-SP, Urao T, Qin F, Maruyama K, Kakimoto T, Shinozaki K, et al. Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc Natl Acad Sci. National Acad Sciences; 2007;104: 20623–20628. doi: 10.1073/pnas.0706547105 18077346

94. Suzuki H, Yokokura J, Ito T, Arai R, Yokoyama C, Toshima H, et al. Biosynthetic pathway of the phytohormone auxin in insects and screening of its inhibitors. Insect Biochem Mol Biol. 2014;53: 66–72. doi: 10.1016/j.ibmb.2014.07.008 25111299

95. Römer P, Hahn S, Jordan T, Strauß T, Bonas U, Lahaye T. Plant pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene. Science (80-). American Association for the Advancement of Science; 2007;318: 645–648.

96. Field LM, James AA, Plantard O, Rasplus J-Y, Mondor G, Clainche I, et al. Distribution and phylogeny of Wolbachia inducing thelytoky in Rhoditini and Aylacini (Hymenoptera: Cynipidae). Insect Mol Biol. 1999;8: 185–191. 10380102

97. Rokas A, Atkinson RJ, Nieves-Aldrey JL, West SA, Stone GN. The incidence and diversity of Wolbachia in gallwasps (Hymenoptera; Cynipidae) on oak. Mol Ecol. 2002;11: 1815–1829. doi: 10.1046/j.1365-294x.2002.01556.x 12207731

98. Bailey TL, Williams N, Misleh C, Li WW. MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res. 2006;34: 369–373. doi: 10.1093/nar/gkl198 16845028

99. Keeling CI, Henderson H, Li M, Yuen M, Clark EL, Fraser JD, et al. Transcriptome and full-length cDNA resources for the mountain pine beetle, Dendroctonus ponderosae Hopkins, a major insect pest of pine forests. Insect Biochem Mol Biol. 2012;42: 525–36. doi: 10.1016/j.ibmb.2012.03.010 22516182

100. Keeling CI, Yuen MM, Liao NY, Docking TR, Chan SK, Taylor GA, et al. Draft genome of the mountain pine beetle, Dendroctonus ponderosae Hopkins, a major forest pest. Genome Biol. BioMed Central Ltd; 2013;14: R27. doi: 10.1186/gb-2013-14-3-r27 23537049

101. Pauchet Y, Heckel DG. The genome of the mustard leaf beetle encodes two active xylanases originally acquired from bacteria through horizontal gene transfer. Proc Biol Sci. 2013;280: 20131021. doi: 10.1098/rspb.2013.1021 23698014

102. Pauchet Y, Wilkinson P, Chauhan R, Ffrench-Constant RH. Diversity of beetle genes encoding novel plant cell wall degrading enzymes. PLoS One. 2010;5: e15635. doi: 10.1371/journal.pone.0015635 21179425

103. De Lorenzo G, Ferrari S, Giovannoni M, Mattei B, Cervone F. Cell wall traits that influence plant development, immunity, and bioconversion. Plant J. Wiley Online Library; 2019;97: 134–147. doi: 10.1111/tpj.14196 30548980

104. Vallarino JG, Osorio S. Signaling role of oligogalacturonides derived during cell wall degradation. Plant Signal Behav. Landes Bioscience; 2012;7: 1447–1449. doi: 10.4161/psb.21779 22918501

105. Pawłowski TA, Staszak AM, Karolewski P, Giertych MJ. Plant development reprogramming by cynipid gall wasp: proteomic analysis. Acta Physiol Plant. Springer; 2017;39: 114.

106. Takei M, Kogure S, Yokoyama C, Kouzuma Y, Suzuki Y. Identification of an aldehyde oxidase involved in indole-3-acetic acid synthesis in Bombyx mori silk gland. Biosci Biotechnol Biochem. Taylor & Francis; 2019;83: 129–136. doi: 10.1080/09168451.2018.1525275 30286706

107. Zhao CY, Escalante LN, Chen H, Benatti TR, Qu JX, Chellapilla S, et al. A massive expansion of effector genes underlies gall-formation in the wheat pest Mayetiola destructor. Curr Biol. 2015;25. doi: 10.1016/j.cub.2014.12.057 25660540

108. Abe Y, Ide T, Wachi N. Discovery of a New Gall-Inducing Species in the Inquiline Tribe Synergini (Hymenoptera: Cynipidae): Inconsistent Implications from Biology and Morphology. Ann Entomol Soc Am. 2011;104: 115–120. doi: 10.1603/AN10149

109. Stanke M, Morgenstern B. AUGUSTUS: a web server for gene prediction in eukaryotes that allows user-defined constraints. Nucleic Acids Res. Oxford University Press; 2005;33: W465—W467. doi: 10.1093/nar/gki458 15980513

110. Volkenburgh E Van. Leaf expansion—an integrating plant behaviour. Plant Cell Environ. Wiley Online Library; 1999;22: 1463–1473.

111. Maksymowych R. Analysis of leaf development. CUP Archive; 1973.

112. Becraft PW. 1 Development of the Leaf Epidermis. Current topics in developmental biology. Elsevier; 1999. pp. 1–40.

113. Botta R, Sartor C, Torello Marinoni D, Quacchia A, Alma A. Differential gene expression in chestnut buds following infestation by gall-wasp (Dryocosmus kuriphilus Yasumatsu, Hymenoptera: Cynipidae). IV International Chestnut Symposium 844. 2008. pp. 405–410.

114. van Hengel AJ, Tadesse Z, Immerzeel P, Schols H, van Kammen A, de Vries SC. N-acetylglucosamine and glucosamine-containing arabinogalactan proteins control somatic embryogenesis. Plant Physiol. 2001;125: 1880–90. doi: 10.1104/pp.125.4.1880 11299367

115. De Jong AJ, Cordewener J, Lo Schiavo F, Terzi M, Vandekerckhove J, Van Kammen A, et al. A carrot somatic embryo mutant is rescued by chitinase. Plant Cell. 1992;4: 425–33. doi: 10.1105/tpc.4.4.425 1498601

116. Poon S, Heath RL, Clarke AE. A chimeric arabinogalactan protein promotes somatic embryogenesis in cotton cell culture. Plant Physiol. 2012;160: 684–95. doi: 10.1104/pp.112.203075 22858635

117. Fehér A, Pasternak TP, Dudits D. Transition of somatic plant cells to an embryogenic state. Plant Cell, Tissue Organ Cult. 2003;74: 201–228. doi: 10.1023/A:1024033216561

118. Nguema-Ona E, Vicré-Gibouin M, Cannesan M-A, Driouich A. Arabinogalactan proteins in root-microbe interactions. Trends Plant Sci. 2013;18: 440–449. doi: 10.1016/j.tplants.2013.03.006 23623239

119. Van Hengel AJ, Van Kammen A, De Vries SC. A relationship between seed development, Arabinogalactan-proteins (AGPs) and the AGP mediated promotion of somatic embryogenesis. Physiol Plant. 2002;114: 637–644. 11975739

120. Costa ML, Sobral R, Costa MMR, Amorim MI, Coimbra S. Evaluation of the presence of arabinogalactan proteins and pectins during Quercus suber male gametogenesis. Ann Bot. Annals Botany Co; 2014; mcu223.

121. De Jong AJ, Heidstra R, Spaink HP, Hartog MV, Meijer EA, Hendriks T, et al. Rhizobium Lipooligosaccharides Rescue a Carrot Somatic Embryo Mutant. Plant Cell. 1993;5: 615–620. doi: 10.1105/tpc.5.6.615 12271077

122. Röhrig H, Schmidt J, Walden R, Czaja I, Miklaševičs E, Wieneke U, et al. Growth of Tobacco Protoplasts Stimulated by Synthetic Lipo-Chitooligosaccharides. Science (80-). 1995;269: 841–843. doi: 10.1126/science.269.5225.841 17778743

123. Schultze M, Kondorosi A. Regulation of symbiotic root nodule development. Annu Rev Genet. 1998;32: 33–57. doi: 10.1146/annurev.genet.32.1.33 9928474

124. Cannesan M-A, Nguema-Ona E. Arabinogalactan proteins in root–microbe interactions. Trends Plant Sci. 2013;18: 440–449. doi: 10.1016/j.tplants.2013.03.006 23623239

125. Vandenbussche F, Vaseva I, Vissenberg K, Van Der Straeten D. Ethylene in vegetative development: a tale with a riddle. New Phytol. Wiley Online Library; 2012;194: 895–909. doi: 10.1111/j.1469-8137.2012.04100.x 22404712

126. Gresshoff PM, Lohar D, Chan P-K, Biswas B, Jiang Q, Reid D, et al. Genetic analysis of ethylene regulation of legume nodulation. Plant Signal Behav. Taylor & Francis; 2009;4: 818–823. doi: 10.4161/psb.4.9.9395 19847106

127. Tiburcio AF, Altabella T, Bitrián M, Alcázar R. The roles of polyamines during the lifespan of plants: from development to stress. Planta. Springer; 2014;6: 1–18.

128. Volkoff A-N, Jouan V, Urbach S, Samain S, Bergoin M, Wincker P, et al. Analysis of virion structural components reveals vestiges of the ancestral ichnovirus genome. PLoS Pathog. 2010;6: e1000923. doi: 10.1371/journal.ppat.1000923 20523890

129. Webster CL, Waldron FM, Robertson S, Crowson D, Ferrari G, Quintana JF, et al. The discovery, distribution, and evolution of viruses associated with Drosophila melanogaster. PLoS Biol. Public Library of Science; 2015;13: e1002210. doi: 10.1371/journal.pbio.1002210 26172158

130. Quentin M, Abad P, Favery B. Plant parasitic nematode effectors target host defense and nuclear functions to establish feeding cells. Front Plant Sci. 2013;4: 53. doi: 10.3389/fpls.2013.00053 23493679

131. Boulain H, Legeai F, Guy E, Morlière S, Douglas NE, Oh J, et al. Fast Evolution and Lineage-Specific Gene Family Expansions of Aphid Salivary Effectors Driven by Interactions with Host-Plants. Genome Biol Evol. Oxford University Press; 2018;10: 1554–1572. doi: 10.1093/gbe/evy097 29788052

132. Bailey S, Percy DM, Hefer CA, Cronk QCB. The transcriptional landscape of insect galls: psyllid (Hemiptera) gall formation in Hawaiian Metrosideros polymorpha (Myrtaceae). BMC Genomics. 2015;16: 943. doi: 10.1186/s12864-015-2109-9 26572921

133. Tanaka Y, Okada K, Asami T, Suzuki Y. Phytohormones in Japanese Mugwort Gall Induction by a Gall-Inducing Gall Midge. Biosci Biotechnol Biochem. 2013;77: 1942–1948. doi: 10.1271/bbb.130406 24018692

134. Takei M, Yoshida S, Kawai T, Hasegawa M, Suzuki Y. Adaptive significance of gall formation for a gall-inducing aphids on Japanese elm trees. J Insect Physiol. 2015;72: 43–51. doi: 10.1016/j.jinsphys.2014.11.006 25437243

135. Ohkawa M. Isolation of zeatin from larvae of Dryocosmus kuriphilus Yasumatsu [Castanea crenata, gall initiation]. HortScience (USA). 1974;9: 458–459.

136. Percy DM, Page RDM, Cronk QCB. Plant-insect interactions: double-dating associated insect and plant lineages reveals asynchronous radiations. Syst Biol. 2004;53: 120–127. doi: 10.1080/10635150490264996 14965907

137. Wood BW, Payne JA. Growth regulators in chestnut shoot galls infected with oriental chestnut gall wasp, Dryocosmus kuriphilus (Hymenoptera: Cynipidae). Environ Entomol. 1988;17: 915–920.

138. Brütting C, Crava CM, Schäfer M, Schuman MC, Meldau S, Adam N, et al. Cytokinin transfer by a free-living mirid to Nicotiana attenuata recapitulates a strategy of endophytic insects. Elife. eLife Sciences Publications Limited; 2018;7: e36268. doi: 10.7554/eLife.36268 30014847

139. Bartlett L, Connor EF. Exogenous phytohormones and the induction of plant galls by insects. Arthropod Plant Interact. 2014;8: 339–348. doi: 10.1007/s11829-014-9309-0

140. John M, Röhrig H, Schmidt J, Walden R, Schell J. Cell signalling by oligosaccharides. Trends Plant Sci. Elsevier; 2015;2: 111–115. doi: 10.1016/S1360-1385(97)01005-4

141. Yue J, Hu X, Huang J. Origin of plant auxin biosynthesis. Trends Plant Sci. Elsevier; 2014;19: 764–770. doi: 10.1016/j.tplants.2014.07.004 25129418

142. Nieminen KM, Kauppinen L, Helariutta Y. A weed for wood? Arabidopsis as a genetic model for xylem development. Plant Physiol. Am Soc Plant Biol; 2004;135: 653–659. doi: 10.1104/pp.104.040212 15208411

143. Bar M, Ori N. Leaf development and morphogenesis. Development. 2014;141: 4219–4230. doi: 10.1242/dev.106195 25371359

144. Body MJA, Zinkgraf MS, Whitham TG, Lin C-H, Richardson RA, Appel HM, et al. Heritable Phytohormone Profiles of Poplar Genotypes Vary in Resistance to a Galling Aphid. Mol Plant-Microbe Interact. 2019;32: 654–672. doi: 10.1094/MPMI-11-18-0301-R 30520677

145. Kunieda T, Fujiyuki T, Kucharski R, Foret S, Ament SA, Toth AL, et al. Carbohydrate metabolism genes and pathways in insects: insights from the honey bee genome. Insect Mol Biol. 2006;15: 563–576. doi: 10.1111/j.1365-2583.2006.00677.x 17069632

146. Mckenna DD, Scully ED, Pauchet Y, Hoover K, Kirsch R, Geib SM, et al. Genome of the Asian longhorned beetle (Anoplophora glabripennis), a globally significant invasive species , reveals key functional and evolutionary innovations at the beetle–plant interface. Genome Biol. 2016; 1–18. doi: 10.1186/s13059-015-0866-z

147. Kirsch R, Gramzow L, Theißen G, Siegfried BD, Richard H, Heckel DG, et al. Horizontal gene transfer and functional diversification of plant cell wall degrading polygalacturonases: Key events in the evolution of herbivory in beetles. Insect Biochem Mol Biol. 2014;52: 33–50. doi: 10.1016/j.ibmb.2014.06.008 24978610

148. Kirsch R, Wielsch N, Vogel H, Svatoš A, Heckel DG, Pauchet Y. Combining proteomics and transcriptome sequencing to identify active plant-cell-wall-degrading enzymes in a leaf beetle. BMC Genomics. 2012;13: 587. doi: 10.1186/1471-2164-13-587 23116131

149. Busch A, Danchin EGJ, Pauchet Y. Functional diversification of horizontally acquired glycoside hydrolase family 45 (GH45) proteins in Phytophaga beetles. BMC Evol Biol. 2019;19: 100. doi: 10.1186/s12862-019-1429-9 31077129

150. Brand P, Lin W, Johnson BR. The draft genome of the invasive walking stick, Medauroidea extradendata, reveals extensive Lineage-Specific gene family expansions of Cell wall degrading enzymes in phasmatodea. G3 Genes, Genomes, Genet. 2018;8: 1403–1408.

151. Bronner R. Proprieties lytiques des œufs de Biorrihza pallida. Comptes Rendus l’Académie des Sci. 1973;276: 189–192.

152. Bronner R. Contribution a l’etude histochimique des tissus nourriciers des zoocecidies. Marcellia. 1977;40: 1–134.

153. Rodriguez PA, Stam R, Warbroek T, Bos JIB. Mp10 and Mp42 from the aphid species Myzus persicae trigger plant defenses in Nicotiana benthamiana through different activities. Mol Plant-Microbe Interact. Am Phytopath Society; 2014;27: 30–39. doi: 10.1094/MPMI-05-13-0156-R 24006884

154. Jaouannet M, Rodriguez PA, Thorpe P, Lenoir CJG, MacLeod R, Escudero-Martinez C, et al. Plant immunity in plant–aphid interactions. Front Plant Sci. 2014;5: 663. doi: 10.3389/fpls.2014.00663 25520727

155. Hogenhout SA, Bos JIB. Effector proteins that modulate plant–insect interactions. Curr Opin Plant Biol. 2011;14: 422–428. doi: 10.1016/j.pbi.2011.05.003 21684190

156. Sanchez F, Padilla J E, Perez H, and Lara M. Control of Nodulin Genes in Root-Nodule Development and Metabolism. Annu Rev Plant Physiol Plant Mol Biol. 1991;42: 507–528. doi: 10.1146/annurev.pp.42.060191.002451

157. Ma Y, Yan C, Li H, Wu W, Liu Y, Wang Y, et al. Bioinformatics Prediction and Evolution Analysis of Arabinogalactan Proteins in the Plant Kingdom. Front Plant Sci. 2017;8: 66. doi: 10.3389/fpls.2017.00066 28184232

158. Mashiguchi K, Asami T, Suzuki Y. Genome-Wide Identification, Structure and Expression Studies, and Mutant Collection of 22 Early Nodulin-Like Protein Genes in Arabidopsis. Biosci Biotechnol Biochem. 2009;73: 2452–2459. doi: 10.1271/bbb.90407 19897921

159. Redding NW, Agudelo P, Wells CE. Multiple Nodulation Genes Are Up-Regulated During Establishment of Reniform Nematode Feeding Sites in Soybean. Phytopathology. Am Phytopath Society; 2018;108: 275–291. doi: 10.1094/PHYTO-04-17-0154-R 28945515

160. Domon J-M, Neutelings G, Roger D, David A, David H. A basic chitinase-like protein secreted by embryogenic tissues of Pinus caribaea acts on arabinogalactan proteins extracted from the same cell lines. J Plant Physiol. 2000;156: 33–39.

161. Arakane Y, Muthukrishnan S. Insect chitinase and chitinase-like proteins. Cell Mol Life Sci. 2010;67: 201–216. doi: 10.1007/s00018-009-0161-9 19816755

162. Zhu Q, Arakane Y, Beeman RW, Kramer KJ, Muthukrishnan S. Functional specialization among insect chitinase family genes revealed by RNA interference. Proc Natl Acad Sci U S A. 2008;105: 6650–5. doi: 10.1073/pnas.0800739105 18436642

163. Taper ML, Case TJ. Interactions between oak tannins and parasite community structure: unexpected benefits of tannins to cynipid gall-wasps. Oecologia. Springer; 1987;71: 254–261. doi: 10.1007/BF00377292 28312253

164. Taper ML, Zimmerman EM, Case TJ. Sources of mortality for a cynipid gall-wasp (Dryocosmus dubiosus (Hymenoptera: Cynipidae)): the importance of the tannin/fungus interaction. Oecologia. Springer; 1986;68: 437–445. doi: 10.1007/BF01036752 28311792

165. Wilson D, Carroll GC. Avoidance of high-endophyte space by gall-forming insects. Ecology. Wiley Online Library; 1997;78: 2153–2163.

166. Wilson D. Fungal endophytes which invade insect galls: insect pathogens, benign saprophytes, or fungal inquilines? Oecologia. Springer; 1995;103: 255–260. doi: 10.1007/BF00329088 28306781

167. Tichomiroff A. Chemische Studien über die Entwicklung der Insecteneier. Zeitschrift für Physiol Chemie. 1885;9: 518–532.

168. Furneaux PJS, Mackay AL. The composition, structure and formation of the chorion and the vitelline membrane of the insect egg-shell. The insect integument. Amsterdam: Elsevier; 1976. pp. 157–176.

169. Moreira MF, Dos Santos AS, Marotta HR, Mansur JF, Ramos IB, Machado EA, et al. A chitin-like component in Aedes aegypti eggshells, eggs and ovaries. Insect Biochem Mol Biol. 2007;37: 1249–61. doi: 10.1016/j.ibmb.2007.07.017 17967344

170. Lohse K, Sharanowski B, Nicholls JA, Blaxter M, Stone GN. Developing EPIC markers for chalcidoid Hymenoptera from EST and genomic data. Mol Ecol Resour. 2011;3: 521–529.

171. Chen S, Zhou Y, Chen Y, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. Cold Spring Harbor Laboratory; 2018;34: i884–i890. doi: 10.1093/bioinformatics/bty560 30423086

172. Andrews S. FastQC: A quality control application for high throughput sequence data. Available at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc. 2010.

173. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotech. 2011;29: 644–652.

174. Patro R, Duggal G, Love MI, Irizarry RA, Kingsford C. Salmon provides fast and bias-aware quantification of transcript expression. Nat Methods. Nature Publishing Group; 2017;14: 417–419. doi: 10.1038/nmeth.4197 28263959

175. Soneson C, Love MI, Robinson MD. Differential analyses for RNA-seq: transcript-level estimates improve gene-level inferences. F1000Research. Faculty of 1000 Ltd; 2015;4.

176. Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc. 2013;8: 1494–1512. doi: 10.1038/nprot.2013.084 23845962

177. Davidson NM, Hawkins ADK, Oshlack A. SuperTranscripts: a data driven reference for analysis and visualisation of transcriptomes. Genome Biol. BioMed Central; 2017;18: 148. doi: 10.1186/s13059-017-1284-1 28778180

178. Li H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics. Oxford University Press; 2018;1: 7.

179. Plomion C, Aury J-M, Amselem J, Alaeitabar T, Barbe V, Belser C, et al. Decoding the oak genome: public release of sequence data, assembly, annotation and publication strategies. Mol Ecol Resour. Wiley Online Library; 2016;16: 254–265. doi: 10.1111/1755-0998.12425 25944057

180. Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods. Nature Publishing Group; 2015;12: 59. doi: 10.1038/nmeth.3176 25402007

181. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. Oxford University Press; 2012;41: D590—D596. doi: 10.1093/nar/gks1219 23193283

182. Simão FA, Waterhouse RM, Ioannidis P, Kriventseva E V, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. Oxford University Press; 2015;31: 3210–3212. doi: 10.1093/bioinformatics/btv351 26059717

183. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-Seq data with DESeq2. Genome Biol. 2014;15: 550. doi: 10.1186/s13059-014-0550-8 25516281

184. Zhu A, Ibrahim JG, Love MI. Heavy-tailed prior distributions for sequence count data: removing the noise and preserving large differences. bioRxiv. Cold Spring Harbor Laboratory; 2018; 303255.

185. Stephens M. False discovery rates: a new deal. Biostatistics. Oxford University Press; 2016;18: 275–294.

186. Alexa A, Rahnenfuhrer J. topGO: Enrichment Analysis for Gene Ontology. Available at: https://bioconductor.org/packages/release/bioc/html/topGO.html. 2016. doi: 10.3390/ijms17030353

187. Supek F, Bošnjak M, Škunca N, Šmuc T. REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS One. 2011;6: e21800. doi: 10.1371/journal.pone.0021800 21789182

188. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19: 455–77. doi: 10.1089/cmb.2012.0021 22506599

189. Zimin A V, Marçais G, Puiu D, Roberts M, Salzberg SL, Yorke JA. The MaSuRCA genome assembler. Bioinformatics. 2013;29: 2669–77. doi: 10.1093/bioinformatics/btt476 23990416

190. Smit AFA HR& GP. RepeatMasker Open-3.0. 1996–2010.

191. Kumar S, Jones M, Koutsovoulos G, Clarke M, Blaxter M. Blobology: exploring raw genome data for contaminants, symbionts and parasites using taxon-annotated GC-coverage plots. Front Genet. Frontiers; 2013;4: 237. doi: 10.3389/fgene.2013.00237 24348509

192. Emms DM, Kelly S. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol. BioMed Central; 2015;16: 157. doi: 10.1186/s13059-015-0721-2 26243257