Neofunctionalization of Toll Signaling in Insects: From Immunity to Dorsoventral Patterning

Literature Cited

1. Akiyama-Oda Y, Oda H. 2006. Axis specification in the spider embryo: dpp is required for radial-to-axial symmetry transformation and sog for ventral patterning. Development 133:2347–57
   [Google Scholar]
2. Almudi I, Martin-Blanco CA, Garcia-Fernandez IM, Lopez-Catalina A, Davie K, Aerts S, Casares F 2019. Establishment of the mayfly Cloeon dipterum as a new model system to investigate insect evolution. EvoDevo 10:6
   [Google Scholar]
3. Anderson KV, Bokla L, Nüsslein-Volhard C. 1985a. Establishment of dorsal-ventral polarity in the Drosophila embryo: the induction of polarity by the Toll gene product. Cell 42:791–98
   [Google Scholar]
4. Anderson KV, Jurgens G, Nüsslein-Volhard C. 1985b. Establishment of dorsal-ventral polarity in the Drosophila embryo: genetic studies on the role of the Toll gene product. Cell 42:779–89
   [Google Scholar]
5. Anderson KV, Nüsslein-Volhard C. 1984. Information for the dorsal-ventral pattern of the Drosophila embryo is stored as maternal mRNA. Nature 311:223–27
   [Google Scholar]
6. Anthoney N, Foldi I, Hidalgo A. 2018. Toll and Toll-like receptor signalling in development. Development 145:9dev156018
   [Google Scholar]
7. Araujo H, Bier E. 2000. sog and dpp exert opposing maternal functions to modify Toll signaling and pattern the dorsoventral axis of the Drosophila embryo. Development 127:3631–44
   [Google Scholar]
8. Benton MA. 2018. A revised understanding of Tribolium morphogenesis further reconciles short and long germ development. PLOS Biol. 16:e2005093
   [Google Scholar]
9. Benton MA, Frey N, Nunes da Fonseca R, von Levetzow C, Stappert D et al. 2019. Fog signaling has diverse roles in epithelial morphogenesis in insects. eLife 8:e47346
   [Google Scholar]
10. Benton MA, Pechmann M, Frey N, Stappert D, Conrads KH et al. 2016. Toll genes have an ancestral role in axis elongation. Curr. Biol. 26:1609–15
    [Google Scholar]
11. Berni M, Fontenele MR, Tobias-Santos V, Caceres-Rodrigues A, Mury FB et al. 2014. Toll signals regulate dorsal-ventral patterning and anterior-posterior placement of the embryo in the hemipteran Rhodnius prolixus. EvoDevo 5:38
    [Google Scholar]
12. Berni M, Mota J, Bressan D, Ribeiro L, Martins G et al. 2023. A pro-BMP function exerted by Rhodnius prolixus Short gastrulation reveals great diversity in the role of BMP modulators during embryonic development. Open Biol. 13:230023
    [Google Scholar]
13. Bier E, De Robertis EM. 2015. BMP gradients: a paradigm for morphogen-mediated developmental patterning. Science 348:aaa5838
    [Google Scholar]
14. Brennan JJ, Gilmore TD. 2018. Evolutionary origins of Toll-like receptor signaling. Mol. Biol. Evol. 35:1576–87
    [Google Scholar]
15. Buchta T, Özüak O, Stappert D, Roth S, Lynch JA. 2013. Patterning the dorsal–ventral axis of the wasp Nasonia vitripennis. Dev. Biol. 381:189–202
    [Google Scholar]
16. Büning J. 1994. The Insect Ovary New York: Springer
17. Cheatle Jarvela AM, Trelstad CS, Pick L 2023. Anterior-posterior patterning of segments in Anopheles stephensi offers insights into the transition from sequential to simultaneous segmentation in holometabolous insects. J. Exp. Zool. B Mol. Dev. Evol. 340:116–30
    [Google Scholar]
18. Chen G, Handel K, Roth S 2000. The maternal NF-κB/dorsal gradient of Tribolium castaneum: dynamics of early dorsoventral patterning in a short-germ beetle. Development 127:5145–56
    [Google Scholar]
19. Chen Y-T. 2015. The role of Toll signaling in dorsoventral axis formation in the milkweed bug Oncopeltus fasciatus PhD Thesis Univ. Cologne Cologne, Ger:.
20. Church SH, Donoughe S, de Medeiros BAS, Extavour CG. 2019. Insect egg size and shape evolve with ecology but not developmental rate. Nature 571:58–62
    [Google Scholar]
21. Clark E, Peel AD, Akam M. 2019. Arthropod segmentation. Development 146:18dev170480
    [Google Scholar]
22. da Fonseca RN, van der Zee M, Roth S. 2010. Evolution of extracellular Dpp modulators in insects: the roles of tolloid and twisted-gastrulation in dorsoventral patterning of the Tribolium embryo. Dev. Biol. 345:80–93
    [Google Scholar]
23. da Fonseca RN, von Levetzow C, Kalscheuer P, Basal A, van der Zee M, Roth S. 2008. Self-regulatory circuits in dorsoventral axis formation of the short-germ beetle Tribolium castaneum. Dev. Cell 14:605–15
    [Google Scholar]
24. Daigneault J, Klemetsaune L, Wasserman SA. 2013. The IRAK homolog Pelle is the functional counterpart of IκB kinase in the Drosophila Toll pathway. PLOS ONE 8:e75150
    [Google Scholar]
25. Deignan L, Pinheiro MT, Sutcliffe C, Saunders A, Wilcockson SG et al. 2016. Regulation of the BMP signaling-responsive transcriptional network in the Drosophila embryo. PLOS Genet. 12:e1006164
    [Google Scholar]
26. Dobreva MP, Camacho J, Abzhanov A. 2022. Time to synchronize our clocks: Connecting developmental mechanisms and evolutionary consequences of heterochrony. J. Exp. Zool. B Mol. Dev. Evol. 338:87–106
    [Google Scholar]
27. Donoughe S, Hoffmann J, Nakamura T, Rycroft CH, Extavour CG. 2022. Nuclear speed and cycle length co-vary with local density during syncytial blastoderm formation in a cricket. Nat. Commun. 13:3889
    [Google Scholar]
28. El-Sherif E, Lynch JA, Brown SJ. 2012. Comparisons of the embryonic development of Drosophila, Nasonia, and Tribolium. Wiley Interdiscip. Rev. Dev. Biol. 1:16–39
    [Google Scholar]
29. Ferrandon D, Imler JL, Hetru C, Hoffmann JA. 2007. The Drosophila systemic immune response: sensing and signalling during bacterial and fungal infections. Nat. Rev. Immunol. 7:862–74
    [Google Scholar]
30. Fitzgerald KA, Kagan JC. 2020. Toll-like receptors and the control of immunity. Cell 180:1044–66
    [Google Scholar]
31. Gavin-Smyth J, Wang YC, Butler I, Ferguson EL. 2013. A genetic network conferring canalization to a bistable patterning system in Drosophila. Curr. Biol. 23:2296–302
    [Google Scholar]
32. Genikhovich G, Fried P, Prunster MM, Schinko JB, Gilles AF et al. 2015. Axis patterning by BMPs: cnidarian network reveals evolutionary constraints. Cell Rep. 10:101646–54
    [Google Scholar]
33. Gorman MJ, Kankanala P, Kanost MR. 2004. Bacterial challenge stimulates innate immune responses in extra-embryonic tissues of tobacco hornworm eggs. Insect Mol. Biol. 13:19–24
    [Google Scholar]
34. Handel K, Grünfelder CG, Roth S, Sander K. 2000. Tribolium embryogenesis: a SEM study of cell shapes and movements from blastoderm to serosal closure. Dev. Genes Evol. 210:167–79
    [Google Scholar]
35. Hartenstein V. 1993. Atlas of Drosophila Development. Cold Spring Harbor, NY: Cold Spring Harb. Lab. Press
36. Haskel-Ittah M, Ben-Zvi D, Branski-Arieli M, Schejter ED, Shilo BZ, Barkai N. 2012. Self-organized shuttling: generating sharp dorsoventral polarity in the early Drosophila embryo. Cell 150:1016–28
    [Google Scholar]
37. Hilker M, Meiners T, eds. 2002. Chemoecology of Insect Eggs and Egg Deposition Oxford, UK: Blackwell
38. Hinton HE. 1981. The Biology of Insect Eggs Oxford, UK: Pergamon
39. Hong JW, Hendrix DA, Papatsenko D, Levine MS. 2008. How the Dorsal gradient works: insights from postgenome technologies. PNAS 105:20072–76
    [Google Scholar]
40. Hughes CL, Liu PZ, Kaufman TC. 2004. Expression patterns of the rogue Hox genes Hox3/zen and fushi tarazu in the apterygote insect Thermobia domestica. Evol. Dev. 6:393–401
    [Google Scholar]
41. Inomata H, Shibata T, Haraguchi T, Sasai Y. 2013. Scaling of dorsal-ventral patterning by embryo size-dependent degradation of Spemann's organizer signals. Cell 153:1296–311
    [Google Scholar]
42. Irizarry J, McGehee J, Kim G, Stein D, Stathopoulos A. 2020. Twist-dependent ratchet functioning downstream from Dorsal revealed using a light-inducible degron. Genes Dev. 34:965–72
    [Google Scholar]
43. Jacobs CG, Rezende GL, Lamers GE, van der Zee M. 2013. The extraembryonic serosa protects the insect egg against desiccation. Proc. Biol. Sci. 280:20131082
    [Google Scholar]
44. Jacobs CG, Spaink HP, van der Zee M. 2014. The extraembryonic serosa is a frontier epithelium providing the insect egg with a full-range innate immune response. eLife 3:e04111
    [Google Scholar]
45. Jacobs CGC, van der Hulst R, Chen YT, Williamson RP, Roth S, van der Zee M. 2022. Immune function of the serosa in hemimetabolous insect eggs. Philos. Trans. R. Soc. Lond. B Biol. Sci. 377:20210266
    [Google Scholar]
46. Jacobs CGC, van der Zee M. 2013. Immune competence in insect eggs depends on the extraembryonic serosa. Dev. Comp. Immunol. 41:263–69
    [Google Scholar]
47. Jazwinska A, Rushlow C, Roth S. 1999. The role of brinker in mediating the graded response to Dpp in early Drosophila embryos. Development 126:3323–34
    [Google Scholar]
48. Johnson KP, Dietrich CH, Friedrich F, Beutel RG, Wipfler B et al. 2018. Phylogenomics and the evolution of hemipteroid insects. PNAS 115:12775–80
    [Google Scholar]
49. Klingler M, Bucher G. 2022. The red flour beetle T. castaneum: elaborate genetic toolkit and unbiased large scale RNAi screening to study insect biology and evolution. EvoDevo 13:14
    [Google Scholar]
50. Lemaitre B, Nicolas E, Michaut L, Reichhart JM, Hoffmann JA 1996. The dorsoventral regulatory gene cassette spätzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86:973–83
    [Google Scholar]
51. Lowe CJ, Terasaki M, Wu M, Freeman RM Jr., Runft L et al. 2006. Dorsoventral patterning in hemichordates: insights into early chordate evolution. PLOS Biol. 4:e291
    [Google Scholar]
52. Lynch JA, Peel AD, Drechsler A, Averof M, Roth S. 2010. EGF signaling and the origin of axial polarity among the insects. Curr. Biol. 20:1042–47
    [Google Scholar]
53. Lynch JA, Roth S. 2011. The evolution of dorsal-ventral patterning mechanisms in insects. Genes Dev. 25:107–18
    [Google Scholar]
54. Manning AJ, Rogers SL. 2014. The Fog signaling pathway: insights into signaling in morphogenesis. Dev. Biol. 394:6–14
    [Google Scholar]
55. Masumoto M, Machida R. 2006. Development of embryonic membranes in the silverfish Lepisma saccharina linnaeus (insecta: Zygentoma, Lepismatidae). Tissue Cell 38:159–69
    [Google Scholar]
56. Maxton-Küchenmeister J, Handel K, Schmidt-Ott U, Roth S, Jäckle H. 1999. Toll homolog expression in the beetle Tribolium suggests a different mode of dorsoventral patterning than in Drosophila embryos. Mech. Dev. 83:107–14
    [Google Scholar]
57. Medzhitov R, Preston-Hurlburt P, Janeway CA Jr. 1997. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388:394–97
    [Google Scholar]
58. Misof B, Liu S, Meusemann K, Peters RS, Donath A et al. 2014. Phylogenomics resolves the timing and pattern of insect evolution. Science 346:763–67
    [Google Scholar]
59. Morisato D. 2001. Spätzle regulates the shape of the Dorsal gradient in the Drosophila embryo. Development 128:2309–19
    [Google Scholar]
60. Muhammad MSD. 2018. Large scale RNAi screen in Tribolium reveals novel genes involved in dorsoventral pattern formation PhD Thesis Univ. Cologne Cologne, Ger:.
61. Nakamura T, Yoshizaki M, Ogawa S, Okamoto H, Shinmyo Y et al. 2010. Imaging of transgenic cricket embryos reveals cell movements consistent with a syncytial patterning mechanism. Curr. Biol. 20:1641–47
    [Google Scholar]
62. Nie L, Cai SY, Shao JZ, Chen J. 2018. Toll-like receptors, associated biological roles, and signaling networks in non-mammals. Front. Immunol. 9:1523
    [Google Scholar]
63. Nüsslein-Volhard C. 2022. The Toll gene in Drosophila pattern formation. Trends Genet. 38:231–45
    [Google Scholar]
64. O'Connor MB, Umulis D, Othmer HG, Blair SS. 2006. Shaping BMP morphogen gradients in the Drosophila embryo and pupal wing. Development 133:183–93
    [Google Scholar]
65. Ohde T, Takehana Y, Shiotsuki T, Niimi T. 2018. CRISPR/Cas9-based heritable targeted mutagenesis in Thermobia domestica: a genetic tool in an apterygote development model of wing evolution. Arthropod Struct. Dev. 47:362–69
    [Google Scholar]
66. O'Neill LA, Golenbock D, Bowie AG. 2013. The history of Toll-like receptors—redefining innate immunity. Nat. Rev. Immunol. 13:453–60
    [Google Scholar]
67. Özüak O, Buchta T, Roth S, Lynch JA. 2014a. Ancient and diverged TGF-β signaling components in Nasonia vitripennis. Dev. Genes Evol. 224:223–33
    [Google Scholar]
68. Özüak O, Buchta T, Roth S, Lynch JA. 2014b. Dorsoventral polarity of the Nasonia embryo primarily relies on a BMP gradient formed without input from Toll. Curr. Biol. 24:2393–98
    [Google Scholar]
69. Panfilio KA. 2008. Extraembryonic development in insects and the acrobatics of blastokinesis. Dev. Biol. 313:471–91
    [Google Scholar]
70. Pechmann M, Kenny NJ, Pott L, Heger P, Chen YT et al. 2021. Striking parallels between dorsoventral patterning in Drosophila and Gryllus reveal a complex evolutionary history behind a model gene regulatory network. eLife 10:e68287
    [Google Scholar]
71. Pers D, Buchta T, Özüak O, Roth S, Lynch JA. 2022. Expression and function of Toll pathway components in the early development of the wasp Nasonia vitripennis. J. Dev. Biol. 10:17
    [Google Scholar]
72. Pers D, Buchta T, Özüak O, Wolff S, Pietsch JM et al. 2016. Global analysis of dorsoventral patterning in the wasp Nasonia reveals extensive incorporation of novelty in a regulatory network. BMC Biol. 14:63
    [Google Scholar]
73. Pers D, Lynch JA. 2018. Ankyrin domain encoding genes from an ancient horizontal transfer are functionally integrated into Nasonia developmental gene regulatory networks. Genome Biol. 19:148
    [Google Scholar]
74. Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C et al. 1998. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282:2085–88
    [Google Scholar]
75. Reeves GT, Stathopoulos A. 2009. Graded dorsal and differential gene regulation in the Drosophila embryo. Cold Spring Harb. Perspect. Biol. 1:a000836
    [Google Scholar]
76. Rezende GL, Vargas HCM, Moussian B, Cohen E 2016. Composite eggshell matrices: chorionic layers and sub-chorionic cuticular envelopes. Extracellular Composite Matrices in Arthropods E Cohen, B Moussian 325–66. New York: Springer
    [Google Scholar]
77. Roth S. 2004. Gastrulation in other insects. Gastrulation: From Cells to Embryos C Stern 105–21. Cold Spring, NY: Cold Spring Harb. Lab. Press
    [Google Scholar]
78. Roth S, Lynch JA. 2009. Symmetry breaking during Drosophila oogenesis. Cold Spring Harb. Perspect. Biol. 1:a001891
    [Google Scholar]
79. Roth S, Schupbach T. 1994. The relationship between ovarian and embryonic dorsoventral patterning in Drosophila. Development 120:2245–57
    [Google Scholar]
80. Roth S, Stein D, Nüsslein-Volhard C. 1989. A gradient of nuclear localization of the dorsal protein determines dorsoventral pattern in the Drosophila embryo. Cell 59:1189–202
    [Google Scholar]
81. Rousso T, Lynch J, Yogev S, Roth S, Schejter ED, Shilo B-Z. 2010. Generation of distinct signaling modes via diversification of the Egfr ligand-processing cassette. Development 137:3427–37
    [Google Scholar]
82. Rushlow CA, Han K, Manley JL, Levine M. 1989. The graded distribution of the dorsal morphogen is initiated by selective nuclear transport in Drosophila. Cell 59:1165–77
    [Google Scholar]
83. Sachs L, Chen Y-T, Drechsler A, Lynch JA, Panfilio KA et al. 2015. Dynamic BMP signaling polarized by Toll patterns the dorsoventral axis in a hemimetabolous insect. eLife 4:e05502
    [Google Scholar]
84. Sander K. 1971. Pattern formation in longitudinal halves of leaf hopper eggs (Homoptera) and some remarks on the definition of “embryonic regulation. .” Wilhelm Roux Arch. Entwickl. Mech. 167:336–52
    [Google Scholar]
85. Sandmann T, Girardot C, Brehme M, Tongprasit W, Stolc V, Furlong EE. 2007. A core transcriptional network for early mesoderm development in Drosophila melanogaster. Genes Dev. 21:436–49
    [Google Scholar]
86. Schloop AE, Bandodkar PU, Reeves GT. 2020a. Formation, interpretation, and regulation of the Drosophila Dorsal/NF-κB gradient. Curr. Top. Dev. Biol. 137:143–91
    [Google Scholar]
87. Schloop AE, Carrell-Noel S, Friedman J, Thomas A, Reeves GT. 2020b. Mechanism and implications of morphogen shuttling: lessons learned from Dorsal and Cactus in Drosophila. Dev. Biol. 461:13–18
    [Google Scholar]
88. Schmidt-Ott U, Kwan CW. 2022. How two extraembryonic epithelia became one: serosa and amnion features and functions of Drosophila’s amnioserosa. Philos. Trans. R. Soc. Lond. B Biol. Sci. 377:20210265
    [Google Scholar]
89. Schmidt-Ott U, Lynch JA. 2016. Emerging developmental genetic model systems in holometabolous insects. Curr. Opin. Genet. Dev. 39:116–28
    [Google Scholar]
90. Schmitt-Engel C, Schultheis D, Schwirz J, Strohlein N, Troelenberg N et al. 2015. The iBeetle large-scale RNAi screen reveals gene functions for insect development and physiology. Nat. Commun. 6:7822
    [Google Scholar]
91. Shan T, Wang Y, Dittmer NT, Kanost MR, Jiang H. 2022. Serine protease networks mediate immune responses in extra-embryonic tissues of eggs in the tobacco hornworm, Manduca sexta. J. Innate Immun. 15:365–79
    [Google Scholar]
92. Stappert D, Frey N, von Levetzow C, Roth S. 2016. Genome-wide identification of Tribolium dorsoventral patterning genes. Development 143:2443–54
    [Google Scholar]
93. Stathopoulos A, Levine M. 2002. Linear signaling in the Toll-Dorsal pathway of Drosophila: activated Pelle kinase specifies all threshold outputs of gene expression while the bHLH protein Twist specifies a subset. Development 129:3411–19
    [Google Scholar]
94. Stein DS, Stevens LM. 2014. Maternal control of the Drosophila dorsal-ventral body axis. Wiley Interdiscip. Rev. Dev. Biol. 3:301–30
    [Google Scholar]
95. Steward R. 1989. Relocalization of the dorsal protein from the cytoplasm to the nucleus correlates with its function. Cell 59:1179–88
    [Google Scholar]
96. Tetreau G, Dhinaut J, Galinier R, Audant-Lacour P, Voisin SN et al. 2020. Deciphering the molecular mechanisms of mother-to-egg immune protection in the mealworm beetle Tenebrio molitor. PLOS Pathog. 16:e1008935
    [Google Scholar]
97. Tomizuka S, Machida R. 2015. Embryonic development of a collembolan, Tomocerus cuspidatus Börner 1909: with special reference to the development and developmental potential of serosa (Hexapoda: Collembola, Tomoceridae). Arthropod Struct. Dev. 44:157–72
    [Google Scholar]
98. True JR, Haag ES. 2001. Developmental system drift and flexibility in evolutionary trajectories. Evol. Dev. 3:109–19
    [Google Scholar]
99. Umetsu D. 2022. Cell mechanics and cell-cell recognition controls by Toll-like receptors in tissue morphogenesis and homeostasis. Fly 16:233–47
    [Google Scholar]
100. van der Zee M, Stockhammer O, von Levetzow C, da Fonseca RN, Roth S. 2006. Sog/Chordin is required for ventral-to-dorsal Dpp/BMP transport and head formation in a short germ insect. PNAS 103:16307–12
     [Google Scholar]
101. Vargas HCM, Panfilio KA, Roelofs D, Rezende GL. 2021. Increase in egg resistance to desiccation in springtails correlates with blastodermal cuticle formation: eco-evolutionary implications for insect terrestrialization. J. Exp. Zool. B. Mol. Dev. Evol. 336:606–19
     [Google Scholar]
102. Vilcinskas A. 2021. Mechanisms of transgenerational immune priming in insects. Dev. Comp. Immunol. 124:104205
     [Google Scholar]
103. Wang YC, Ferguson EL. 2005. Spatial bistability of Dpp-receptor interactions during Drosophila dorsal-ventral patterning. Nature 434:229–34
     [Google Scholar]
104. Wheeler SR, Carrico ML, Wilson BA, Skeath JB. 2005. The Tribolium columnar genes reveal conservation and plasticity in neural precursor patterning along the embryonic dorsal-ventral axis. Dev. Biol. 279:491–500
     [Google Scholar]
105. Wilson MJ, Abbott H, Dearden PK. 2011. The evolution of oocyte patterning in insects: multiple cell-signaling pathways are active during honeybee oogenesis and are likely to play a role in axis patterning. Evol. Dev. 13:127–37
     [Google Scholar]
106. Wilson MJ, Kenny NJ, Dearden PK. 2014. Components of the dorsal-ventral pathway also contribute to anterior-posterior patterning in honeybee embryos (Apis mellifera). EvoDevo 5:11
     [Google Scholar]
107. Wipfler B, Letsch H, Frandsen PB, Kapli P, Mayer C et al. 2019. Evolutionary history of Polyneoptera and its implications for our understanding of early winged insects. PNAS 116:3024–29
     [Google Scholar]