Phylloxerids share ancestral carotenoid biosynthesis genes of fungal origin with aphids and adelgids

PLoS ONE

Volumn 12, Issue 10, 2017, Pages

  Zhao, Chaoyang ^a   Nabity, Paul D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAROTENOID; GENOMIC DNA; PHYLLOXERID; UNCLASSIFIED DRUG; INSECT PROTEIN; OXIDOREDUCTASE; PHYTOENE DEHYDROGENASE;

APHID; ARTICLE; BIOSYNTHESIS; CARBOHYDRATE METABOLISM; CONTROLLED STUDY; DNA EXTRACTION; DNA FRAGMENTATION; ENZYME SYNTHESIS; EXON; GENE DUPLICATION; GENE FUNCTION; INTRON; LIPOPHILICITY; NEXT GENERATION SEQUENCING; NONHUMAN; OPEN READING FRAME; PHYLOGENY; POLYMERASE CHAIN REACTION; PROTEIN ANALYSIS; SEQUENCE ALIGNMENT; SYMBIOSIS; TRANSCRIPTOMICS; ANIMAL; CONSERVED SEQUENCE; FUNGUS; GENE; GENE DOSAGE; GENETICS; HEMIPTERA; METABOLISM; NUCLEOTIDE SEQUENCE; STATISTICAL MODEL;

ANIMALS; APHIDS; BASE SEQUENCE; BIOSYNTHETIC PATHWAYS; CAROTENOIDS; CONSERVED SEQUENCE; EXONS; FUNGI; GENE DOSAGE; GENES, INSECT; HEMIPTERA; INSECT PROTEINS; INTRONS; LIKELIHOOD FUNCTIONS; OXIDOREDUCTASES; PHYLOGENY; POLYMERASE CHAIN REACTION;

EID: 85031032125     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0185484     Document Type: Article

References (40)

1. von Wintersdorff CJ, Penders J, van Niekerk JM, Mills ND, Majumder S, van Alphen LB, et al. Dissemination of antimicrobial resistance in microbial ecosystems through horizontal gene transfer. Frontiers in microbiology. 2016; 7.
2. Wybouw N, Pauchet Y, Heckel DG, Van Leeuwen T. Horizontal gene transfer contributes to the evolution of arthropod herbivory. Genome biology and evolution. 2016 Jun 1; 8(6):1785–801. https://doi.org/10.1093/gbe/evw119 PMID: 27307274
3. Werren JH, Richards S, Desjardins CA, Niehuis O, Gadau J, Colbourne JK, NasoniaGenome Working Group. Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science. 2010 Jan 15; 327(5963):343–8. https://doi.org/10.1126/science.1178028 PMID: 20075255
4. Zhu B, Lou MM, Xie GL, Zhang GQ, Zhou XP, Li B, et al. Horizontal gene transfer in silkworm, Bombyx mori. BMC genomics. 2011 May 19; 12(1):248.
5. 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 biology. 2013 Mar 27; 14(3):R27. https://doi.org/10.1186/gb-2013-14-3-r27 PMID: 23537049
6. Terrapon N, Li C, Robertson HM, Ji L, Meng X, Booth W, et al. Molecular traces of alternative social organization in a termite genome. Nature communications. 2014 May 20; 5.
7. Zhao C, Escalante LN, Chen H, Benatti TR, Qu J, Chellapilla S, et al. A massive expansion of effector genes underlies gall-formation in the wheat pest Mayetiola destructor. Current Biology. 2015 Mar 2; 25(5):613–20. https://doi.org/10.1016/j.cub.2014.12.057 PMID: 25660540
8. Benoit JB, Adelman ZN, Reinhardt K, Dolan A, Poelchau M, Jennings EC, et al. Unique features of a global human ectoparasite identified through sequencing of the bed bug genome. Nature communications. 2016 Feb 2; 7.
9. Kanost MR, Arrese EL, Cao X, Chen YR, Chellapilla S, Goldsmith MR, et al. Multifaceted biological insights from a draft genome sequence of the tobacco hornworm moth, Manduca sexta. Insect Biochemistry and Molecular Biology. 2016 Sep 30; 76:118–47. https://doi.org/10.1016/j.ibmb.2016.07.005PMID: 27522922
10. McKenna DD, Scully ED, Pauchet Y, Hoover K, Kirsch R, Geib SM, et al. Genome of the Asian long-horned beetle (Anoplophora glabripennis), a globally significant invasive species, reveals key functional and evolutionary innovations at the beetle—plant interface. Genome Biology. 2016 Nov 11; 17(1):227. https://doi.org/10.1186/s13059-016-1088-8 PMID: 27832824
11. Shelomi M, Danchin EG, Heckel D, Wipfler B, Bradler S, Zhou X, et al. Horizontal gene transfer of pecti-nases from bacteria preceded the diversification of stick and leaf insects. Scientific reports. 2016; 6.
12. Hotopp JC, Clark ME, Oliveira DC, Foster JM, Fischer P, Torres MC, et al. Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science. 2007 Sep 21; 317(5845):1753–6. https://doi.org/10.1126/science.1142490 PMID: 17761848
13. Moran NA, Jarvik T. Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science. 2010 Apr 30; 328(5978):624–7. https://doi.org/10.1126/science.1187113 PMID: 20431015
14. Acuña R, Padilla BE, Flórez-Ramos CP, Rubio JD, Herrera JC, Benavides P, et al. Adaptive horizontal transfer of a bacterial gene to an invasive insect pest of coffee. Proceedings of the National Academy of Sciences. 2012 Mar 13; 109(11):4197–202.
15. Husnik F, Nikoh N, Koga R, Ross L, Duncan RP, Fujie M, et al. Horizontal gene transfer from diverse bacteria to an insect genome enables a tripartite nested mealybug symbiosis. Cell. 2013 Jun 20; 153 (7):1567–78. https://doi.org/10.1016/j.cell.2013.05.040 PMID: 23791183
16. Pauchet Y, Heckel DG. The genome of the mustard leaf beetle encodes two active xylanases originally acquired from bacteria through horizontal gene transfer. Proceedings of the Royal Society of London B: Biological Sciences. 2013 Jul 22; 280(1763):20131021.
17. Sloan DB, Nakabachi A, Richards S, Qu J, Murali SC, Gibbs RA, et al. Parallel histories of horizontal gene transfer facilitated extreme reduction of endosymbiont genomes in sap-feeding insects. Molecular biology and evolution. 2014 Apr 1; 31(4):857–71. https://doi.org/10.1093/molbev/msu004 PMID: 24398322
18. Zhao C, Doucet D, Mittapalli O. Characterization of horizontally transferred β-fructofuranosidase (ScrB) genes in Agrilus planipennis. Insect molecular biology. 2014 Dec 1; 23(6):821–32. https://doi.org/10.1111/imb.12127 PMID: 25224649
19. Luan JB, Chen W, Hasegawa DK, Simmons AM, Wintermantel WM, Ling KS, et al. Metabolic coevolution in the bacterial symbiosis of whiteflies and related plant sap-feeding insects. Genome biology and evolution. 2015 Sep 1; 7(9):2635–47. https://doi.org/10.1093/gbe/evv170 PMID: 26377567
20. Edge R, McGarvey DJ, Truscott TG. The carotenoids as anti-oxidants—a review. Journal of Photochemistry and Photobiology B: Biology. 1997 Dec 31; 41(3):189–200.
21. Blum MS. Comparative insect physiology, biochemistry and pharmacology, (Kerkut GA and Gilbert LI eds.), 193–224.
22. Vershinin A. Biological functions of carotenoids-diversity and evolution. Biofactors. 1999 Jan 1; 10(2-3):99–104. PMID: 10609869
23. Altincicek B, Kovacs JL, Gerardo NM. Horizontally transferred fungal carotenoid genes in the two-spotted spider mite Tetranychus urticae. Biology letters. 2012 Apr 23; 8(2):253–7. https://doi.org/10.1098/rsbl.2011.0704 PMID: 21920958
24. Cobbs C, Heath J, Stireman JO, Abbot P. Carotenoids in unexpected places: gall midges, lateral gene transfer, and carotenoid biosynthesis in animals. Molecular phylogenetics and evolution. 2013 Aug 31; 68(2):221–8. https://doi.org/10.1016/j.ympev.2013.03.012 PMID: 23542649
25. Hirschberg J, Cohen M, Harker M, Lotan T, Mann V, Pecker I. Molecular genetics of the carotenoid biosynthesis pathway in plants and algae. Pure and applied chemistry. 1997 Jan 1; 69(10):2151–8.
26. Nováková E, Moran NA. Diversification of genes for carotenoid biosynthesis in aphids following an ancient transfer from a fungus. Molecular biology and evolution. 2012 Jan 1; 29(1):313–23. https://doi.org/10.1093/molbev/msr206 PMID: 21878683
27. Nabity PD, Haus MJ, Berenbaum MR, DeLucia EH. Leaf-galling phylloxera on grapes reprograms host metabolism and morphology. Proceedings of the National Academy of Sciences. 2013 Oct 8; 110 (41):16663–8.
28. Nabity PD. Insect-induced plant phenotypes: Revealing mechanisms through comparative genomics of galling insects and their hosts. American journal of botany. 2016 Jun 1; 103(6):979–81. https://doi.org/10.3732/ajb.1600111 PMID: 27257007
29. Sloan DB, Moran NA. Endosymbiotic bacteria as a source of carotenoids in whiteflies. Biology letters. 2012 Dec 23; 8(6):986–9. https://doi.org/10.1098/rsbl.2012.0664 PMID: 22977066
30. Zhao C, Nabity PD. Plant manipulation through gall formation constrains amino acid transporter evolution in sap-feeding insects. BMC Evolutionary Biology. 2017 Jun 27; 17(1):153. https://doi.org/10.1186/s12862-017-1000-5 PMID: 28655293
31. Katoh K, Misawa K, Kuma KI, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic acids research. 2002 Jul 15; 30(14):3059–66. PMID: 12136088
32. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 2000; 17:540–552. PMID: 10742046
33. Le SQ, Gascuel O. An improved general amino acid replacement matrix. Molecular biology and evolution. 2008 Jul 1; 25(7):1307–20. https://doi.org/10.1093/molbev/msn067 PMID: 18367465
34. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular biology and evolution. 2013 Dec 1; 30(12):2725–9. https://doi.org/10.1093/molbev/mst197 PMID: 24132122
35. Mifsud D, Cocquempot C, Mühlethaler R, Wilson M, Streito JC. Other Hemiptera Sternorrhyncha (Aleyrodidae, Phylloxeroidea, and Psylloidea) and Hemiptera Auchenorrhyncha. Chapter 9.4. BioRisk. 2010 Jun 7; 4:511.
36. Blackman RL, Eastop VF. Aphids on the world’s crops: an identification and information guide. John Wiley & Sons Ltd; 2000.
37. Douglas AE. Phloem-sap feeding by animals: problems and solutions. Journal of Experimental Botany. 2006 Mar 1; 57(4):747–54. https://doi.org/10.1093/jxb/erj067 PMID: 16449374
38. Gaupels F, Vlot AC. Plant Defense and Long-Distance Signaling in the Phloem. Phloem: Molecular Cell Biology, Systemic Communication, Biotic Interactions. 2012:227–47.
39. van Bel AJ, Will T. Functional evaluation of proteins in watery and gel saliva of aphids. Frontiers in Plant Science. 2016; 7.
40. Byron A, Kurlovs AH, Dermauw W, Greenhalgh R, Riga M, Grbic M, et al. Disruption of a horizontally transferred phytoene desaturase abolishes carotenoid accumulation and diapause in Tetranychus urticae. Proceedings of the National Academy of Sciences. 2017: 114(29) https://doi.org/10.1073/pnas.1706865114 PMID: 28674017