A novel bioinformatics pipeline to discover genes related to arbuscular mycorrhizal symbiosis based on their evolutionary conservation pattern among higher plants

BMC Plant Biology

Volumn 14, Issue 1, 2014, Pages

  Favre, Patrick ^a,c   Bapaume, Laure ^a   Bossolini, Eligio ^a,d   Delorenzi, Mauro ^b,c   Falquet, Laurent ^a,c   Reinhardt, Didier ^a  

^a UNIVERSITY OF FRIBOURG   (Switzerland)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^d Bayer Cropscience Belgium   (Belgium)

Author keywords

Arbuscular mycorrhiza; Bioinformatics; Common SYM gene; Conservation; Gene clustering; Proteome analysis; Symbiosis; Symbiosis signaling

Indexed keywords

VEGETABLE PROTEIN;

ANGIOSPERM; BIOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGY; MOLECULAR EVOLUTION; MYCORRHIZA; PHYLOGENY; PHYSIOLOGY; PROMOTER REGION; SYMBIOSIS;

ANGIOSPERMS; COMPUTATIONAL BIOLOGY; EVOLUTION, MOLECULAR; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; MYCORRHIZAE; PHYLOGENY; PLANT PROTEINS; PROMOTER REGIONS, GENETIC; SYMBIOSIS;

EID: 84964313509     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/s12870-014-0333-0     Document Type: Article

References (87)

1. Smith SE, Read DJ: Mycorrhizal Symbiosis. 3rd edition. New York: Academic; 2008.
2. Wang B, Qiu YL: Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 2006, 16(5):299-363.
3. Brundrett MC: Coevolution of roots and mycorrhizas of land plants. New Phytol 2002, 154(2):275-304.
4. Gutjahr C, Parniske M: Cell and developmental biology of arbuscular mycorrhiza symbiosis. Annu Rev Cell Dev Biol 2013, 29:593-617.
5. Delaux PM, Sejalon-Delmas N, Bécard G, Ané JM: Evolution of the plant-microbe symbiotic 'toolkit'. Trends Plant Sci 2013, 18(6):298-304.
6. Wang B, Yeun LH, Xue JY, Liu Y, Ane JM, Qiu YL: Presence of three mycorrhizal genes in the common ancestor of land plants suggests a key role of mycorrhizas in the colonization of land by plants. New Phytol 2010, 186(2):514-525.
7. Redecker D, Kodner R, Graham LE: Glomalean fungi from the Ordovician. Science 2000, 289(5486):1920-1921.
8. Kistner C, Parniske M: Evolution of signal transduction in intracellular symbiosis. Trends Plant Sci 2002, 7(11):511-518.
9. Sprent JI, James EK: Legume evolution: Where do nodules and mycorrhizas fit in? Plant Physiol 2007, 144(2):575-581.
10. Sprent JI: 60 Ma of legume nodulation. What's new? What's changing? J Exp Bot 2008, 59(5):1081-1084.
11. Hocher V, Alloisio N, Auguy F, Fournier P, Doumas P, Pujic P, Gherbi H, Queiroux C, Da Silva C, Wincker P, Normand P, Bogusz D: Transcriptomics of actinorhizal symbioses reveals homologs of the whole common symbiotic signaling cascade. Plant Physiol 2011, 156(2):700-711.
12. Svistoonoff S, Benabdoun FM, Nambiar-Veetil M, Imanishi L, Vaissayre V, Cesari S, Diagne N, Hocher V, de Billy F, Bonneau J, Wall L, Ykhlef N, Rosenberg C, Bogusz D, Franche C, Gherbi H: The independent acquisition of plant root nitrogen-fixing symbiosis in fabids recruited the same genetic pathway for nodule organogenesis. Plos One 2013, 8(5):e64515. doi:10.1371/journal.pone.0064515.
13. Oldroyd GED: Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 2013, 11(4):252-263.
14. Oldroyd GED, Downie JA: Nuclear calcium changes at the core of symbiosis signalling. Curr Opin Plant Biol 2006, 9(4):351-357.
15. Singh S, Parniske M: Activation of calcium-and calmodulin-dependent protein kinase (CCaMK), the central regulator of plant root endosymbiosis. Curr Opin Plant Biol 2012, 15(4):444-453.
16. Feddermann N, Duvvuru Muni RR, Zeier T, Stuurman J, Ercolin F, Schorderet M, Reinhardt D: The PAM1 gene of petunia, required for intracellular accommodation and morphogenesis of arbuscular mycorrhizal fungi, encodes a homologue of VAPYRIN. Plant J 2010, 64(3):470-481.
17. Pumplin N, Mondo SJ, Topp S, Starker CG, Gantt JS, Harrison MJ: Medicago truncatula Vapyrin is a novel protein required for arbuscular mycorrhizal symbiosis. Plant J 2010, 61(3):482-494.
18. Feddermann N, Reinhardt D: Conserved residues in the ankyrin domain of VAPYRIN indicate potential protein-protein interaction surfaces. Plant Signaling Behav 2011, 6(5):680-684.
19. Breuillin F, Schramm J, Hajirezaei M, Ahkami A, Favre P, Druege U, Hause B, Bucher M, Kretzschmar T, Bossolini E, Kuhlemeier C, Martinoia E, Franken P, Scholz U, Reinhardt D, Bucher M, Kretzschmar T, Bossolini E, Kuhlemeier C, Martinoia E, Franken P, Scholz U, Reinhardt D: Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning. Plant J 2010, 64:1002-1017.
20. Rich MK, Schorderet M, Reinhardt D: The role of the cell wall compartment in mutualistic symbioses of plants. Front Plant Sci 2014, 5:238.
21. Gobbato E, Marsh JF, Vernie T, Wang E, Maillet F, Kim J, Miller JB, Sun J, Bano SA, Ratet P, Mysore KS, Dénarié J, Schultze M, Oldroyd GE: A GRAS-type transcription factor with a specific function in mycorrhizal signaling. Curr Biol 2012, 22(23):2236-2241.
22. Zhang Q, Blaylock LA, Harrison MJ: Two Medicago truncatula half-ABC transporters are essential for arbuscule development in arbuscular mycorrhizal symbiosis. Plant Cell 2010, 22(5):1483-1497.
23. Harrison MJ, Dewbre GR, Liu JY: A phosphate transporter from Medicago truncatula involved in the acquisiton of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 2002, 14(10):2413-2429.
24. Javot H, Penmetsa RV, Terzaghi N, Cook DR, Harrison MJ: A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci U S A 2007, 104(5):1720-1725.
25. Schreiber F, Sonnhammer ELL: Hieranoid: Hierarchical Orthology Inference. J Mol Biol 2013, 425(11):2072-2081.
26. Murray JD, Duvvuru Muni R, Torres-Jerez I, Tang Y, Allen S, Andriankaja M, Li G, Laxmi A, Cheng X, Wen J, Vaughan D, Schultze M, Sun J, Charpentier M, Oldroyd G, Tadege M, Ratet P, Mysore KS, Chen R, Udvardi MK: Vapyrin, a gene essential for intracellular progression of arbuscular mycorrhizal symbiosis, is also essential for infection by rhizobia in the nodule symbiosis of Medicago truncatula. Plant J 2011, 65(2):244-252.
27. Apweiler R, Bateman A, Martin MJ, O'Donovan C, Magrane M, Alam-Faruque Y, Alpi E, Antunes R, Arganiska J, Casanova EB, Bely B, Bingley M, Bonilla C, Britto R, Bursteinas B, Mun Chan W, Chavali G, Cibrian-Uhalte E, Da Silva A, De Giorgi M, Fazzini F, Gane P, Castro LG, Garmiri P, Hatton-Ellis E, Hieta R, Huntley R, Legge D, Liu W, Luo J, et al: Activities at the Universal Protein Resource (UniProt). Nucleic Acids Res 2014, 42(D1):D191-D198.
28. Groth M, Takeda N, Perry J, Uchida H, Draexl S, Brachmann A, Sato S, Tabata S, Kawaguchi M, Wang TL, Parniske M: NENA, a Lotus japonicus homolog of Sec13, is required for rhizodermal infection by arbuscular mycorrhiza fungi and rhizobia but dispensable for cortical endosymbiotic development. Plant Cell 2010, 22:2509-2526.
29. Kanamori N, Madsen LH, Radutoiu S, Frantescu M, Quistgaard EMH, Miwa H, Downie JA, James EK, Felle HH, Haaning LL, Jensen TH, Sato S, Nakamura Y, Tabata S, Sandal N, Stougaard J: A nucleoporin is required for induction of Ca2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proc Natl Acad Sci U S A 2006, 103(2):359-364.
30. Saito K, Yoshikawa M, Yano K, Miwa H, Uchida H, Asamizu E, Sato S, Tabata S, Imaizumi-Anraku H, Umehara Y, Kouchi H, Murooka Y, Szczyglowski K, Downie JA, Parniske M, Hayashi M, Kawaguchi M: NUCLEOPORIN85 is required for calcium spiking, fungal and bacterial symbioses, and seed production in Lotus japonicus. Plant Cell 2007, 19(2):610-624.
31. Fiorilli V, Catoni M, Miozzi L, Novero M, Accotto GP, Lanfranco L: Global and cell-type gene expression profiles in tomato plants colonized by an arbuscular mycorrhizal fungus. New Phytol 2009, 184(4):975-987.
32. Guether M, Balestrini R, Hannah M, He J, Udvardi M, Bonfante P: Genome-wide reprogramming of regulatory networks, cell wall and membrane biogenesis during arbuscular-mycorrhizal symbiosis in Lotus japonicus. New Phytol 2009, 182(1):200-212.
33. Güimil S, Chang HS, Zhu T, Sesma A, Osbourn A, Roux C, Ionnidis V, Oakeley EJ, Docquier M, Descombes P, Briggs SP, Paszkowski U: Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. Proc Natl Acad Sci U S A 2005, 102(22):8066-8070.
34. Hohnjec N, Vieweg ME, Puhler A, Becker A, Küster H: Overlaps in the transcriptional profiles of Medicago truncatula roots inoculated with two different Glomus fungi provide insights into the genetic program activated during arbuscular mycorrhiza. Plant Physiol 2005, 137(4):1283-1301.
35. Liu JY, Blaylock LA, Endre G, Cho J, Town CD, VandenBosch KA, Harrison MJ: Transcript profiling coupled with spatial expression analyses reveals genes involved in distinct developmental stages of an arbuscular mycorrhizal symbiosis. Plant Cell 2003, 15(9):2106-2123.
36. Lévy J, Bres C, Geurts R, Chalhoub B, Kulikova O, Duc G, Journet EP, Ané JM, Lauber E, Bisseling T, Dénarié J, Rosenberg C, Debellé F: A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 2004, 303(5662):1361-1364.
37. 2+/calmodulin-dependent protein kinase required for symbiotic nodule development: Gene identification by transcript-based cloning. Proc Natl Acad Sci U S A 2004, 101(13):4701-4705.
38. Nagy F, Karandashov V, Chague W, Kalinkevich K, Tamasloukht M, Xu GH, Jakobsen I, Levy AA, Amrhein N, Bucher M: The characterization of novel mycorrhiza-specific phosphate transporters from Lycopersicon esculentum and Solanum tuberosum uncovers functional redundancy in symbiotic phosphate transport in solanaceous species. Plant J 2005, 42(2):236-250.
39. Rausch C, Daram P, Brunner S, Jansa J, Laloi M, Leggewie G, Amrhein N, Bucher M: A phosphate transporter expressed in arbuscule-containing cells in potato. Nature 2001, 414(6862):462-466.
40. Wegmüller S, Svistoonoff S, Reinhardt D, Stuurman J, Amrhein N, Bucher M: A transgenic dTph1 insertional mutagenesis system for forward genetics in mycorrhizal phosphate transport of Petunia. Plant J 2008, 54(6):1115-1127.
41. Guether M, Neuhauser B, Balestrini R, Dynowski M, Ludewig U, Bonfante P: A mycorrhizal-specific ammonium transporter from Lotus japonicus acquires nitrogen released by arbuscular mycorrhizal fungi. Plant Physiol 2009, 150(1):73-83.
42. Katoh K, Standley DM: MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol Biol Evol 2013, 30(4):772-780.
43. Shaikhali J, Noren L, Barajas-Lopez JD, Srivastava V, Konig J, Sauer UH, Wingsle G, Dietz KJ, Strand A: Redox-mediated mechanisms regulate DNA binding activity of the G-group of basic region leucine zipper (bZIP) transcription factors in Arabidopsis. J Biol Chem 2012, 287(33):27510-27525.
44. Vickers CE, Xue GP, Gresshoff PM: A novel cis-acting element, ESP, contributes to high-level endosperm-specific expression in an oat globulin promoter. Plant Mol Biol 2006, 62(1-2):195-214.
45. Zhou P, Yang F, Yu JJ, Ao GM, Zhao Q: Several cis-elements including a palindrome involved in pollen-specific activity of SBgLR promoter. Plant Cell Rep 2010, 29(5):503-511.
46. Chen AQ, Gu MA, Sun SB, Zhu LL, Hong SA, Xu GH: Identification of two conserved cis-acting elements, MYCS and P1BS, involved in the regulation of mycorrhiza-activated phosphate transporters in eudicot species. New Phytol 2012, 189(4):1157-1169.
47. Lota F, Wegmüller S, Buer B, Sato S, Bräutigam A, Hanf B, Bucher M: The cis-acting CTTC-P1BS module is indicative for gene function of LjVTI12, a Qb-SNARE protein gene that is required for arbuscule formation in Lotus japonicus. Plant J 2013, 74(2):280-293.
48. Radutoiu S, Madsen LH, Madsen EB, Felle HH, Umehara Y, Gronlund M, Sato S, Nakamura Y, Tabata S, Sandal N, Stougaard J: Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 2003, 425(6958):585-592.
49. Markham JE, Lynch DV, Napier JA, Dunn TM, Cahoon EB: Plant sphingolipids: function follows form. Curr Opin Plant Biol 2013, 16(3):350-357.
50. Kutchan TM: Heterologous expression of alkaloid biosynthetic genes-A review. Gene 1996, 179(1):73-81.
51. Govindarajulu M, Pfeffer PE, Jin HR, Abubaker J, Douds DD, Allen JW, Bücking H, Lammers PJ, Shachar-Hill Y: Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 2005, 435(7043):819-823.
52. Tian CJ, Kasiborski B, Koul R, Lammers PJ, Bücking H, Shachar-Hill Y: Regulation of the nitrogen transfer pathway in the arbuscular mycorrhizal symbiosis: Gene characterization and the coordination of expression with nitrogen flux. Plant Physiol 2010, 153(3):1175-1187.
53. Miyawaki K, Tabata R, Sawa S: Evolutionarily conserved CLE peptide signaling in plant development, symbiosis, and parasitism. Curr Opin Plant Biol 2013, 16(5):598-606.
54. Chen CY, Ané JM, Zhu HY: OsIPD3, an ortholog of the Medicago truncatula DMI3 interacting protein IPD3, is required for mycorrhizal symbiosis in rice. New Phytol 2008, 180(2):311-315.
55. Horvath B, Yeun LH, Domonkos A, Halasz G, Gobbato E, Ayaydin F, Miro K, Hirsch S, Sun JH, Tadege M, Ratet P, Mysore KS, Ané JM, Oldroyd GE, Kaló P: Medicago truncatula IPD3 Is a member of the common symbiotic signaling pathway required for rhizobial and mycorrhizal symbioses. Mol Plant-Microbe Interact 2011, 24(11):1345-1358.
56. Yano K, Yoshida S, Muller J, Singh S, Banba M, Vickers K, Markmann K, White C, Schuller B, Sato S, Asamizu E, Tabata S, Murooka Y, Perry J, Wang TL, Kawaguchi M, Imaizumi-Anraku H, Hayashi M, Parniske M: CYCLOPS, a mediator of symbiotic intracellular accommodation. Proc Natl Acad Sci U S A 2008, 105(51):20540-20545.
57. Scheller HV, Ulvskov P: Hemicelluloses. Annu Rev Plant Biol 2010, 61:263-289.
58. Stein JC, Howlett B, Boyes DC, Nasrallah ME, Nasrallah JB: Molecular cloning of a putative receptor protein kinase gene encoded at the self-incompatibility locus of Brassica oleracea. Proc Natl Acad Sci U S A 1991, 88(19):8816-8820.
59. Nasrallah JB, Nasrallah ME: S-locus receptor kinase signalling. Biochem Soc Trans 2014, 42:313-319.
60. Walker JC, Zhang R: Relationship of a putative receptor protein kinase from maize to the S-locus glycoproteins of Brassica. Nature 1990, 345(6277):743-746.
61. Hernandez-Garcia CM, Finer JJ: Identification and validation of promoters and cis-acting regulatory elements. Plant Sci 2014, 217:109-119.
62. Kim MJ, Ruzicka D, Shin R, Schachtman DP: The Arabidopsis AP2/ERF transcription factor RAP2.11 modulates plant response to low-potassium conditions. Mol Plant 2012, 5(5):1042-1057.
63. Ramkumar G, Madhav MS, Biswal AK, Rama Devi SJS, Sakthivel K, Mohan MK, Umakanth B, Mangrauthia SK, Sundaram RM, Viraktamath BC: Genome-wide identification and characterization of transcription factor binding motifs of NBS-LRR genes in rice and Arabidopsis. J Genomes Exomes 2014, 3:7-15.
64. Cheng MC, Liao PM, Kuo WW, Lin TP: The Arabidopsis ETHYLENE RESPONSE FACTOR1 regulates abiotic stress-responsive gene expression by binding to different cis-acting elements in response to different stress signals. Plant Physiol 2013, 162(3):1566-1582.
65. Hao DY, Yamasaki K, Sarai A, Ohme-Takagi M: Determinants in the sequence specific binding of two plant transcription factors, CBF1 and NtERF2, to the DRE and GCC motifs. Biochemistry 2002, 41(13):4202-4208.
66. Hu FY, Wang D, Zhao XQ, Zhang T, Sun HX, Zhu LH, Zhang F, Li LJ, Li QO, Tao DY, Fu B, Li Z: Identification of rhizome-specific genes by genome-wide differential expression analysis in Oryza longistaminata. BMC Plant Biol 2011, 11:18.
67. Lu X, Jiang WM, Zhang L, Zhang F, Zhang FY, Shen Q, Wang GF, Tang KX: AaERF1 Positively Regulates the Resistance to Botrytis cinerea in Artemisia annua. Plos One 2013, 8(2):e57657. doi:10.1371/journal. pone.0057657.
68. Pirrello J, Prasad BCN, Zhang WS, Chen KS, Mila I, Zouine M, Latche A, Pech JC, Ohme-Takagi M, Regad F, Bouzayen M: Functional analysis and binding affinity of tomato ethylene response factors provide insight on the molecular bases of plant differential responses to ethylene. BMC Plant Biol 2012, 12:190.
69. Shoji T, Mishima M, Hashimoto T: Divergent DNA-Binding Specificities of a Group of ETHYLENE RESPONSE FACTOR Transcription Factors Involved in Plant Defense. Plant Physiol 2013, 162(2):977-990.
70. Zhou JM, Tang XY, Martin GB: The Pto kinase conferring resistance to tomato bacterial speck disease interacts with proteins that bind a cis-element of pathogenesis-related genes. EMBO J 1997, 16(11):3207-3218.
71. Franken P, Gnädinger F: Analysis of parsley arbuscular endomycorrhiza-Infection, development and messenger-RNA levels of defense-related genes. Mol Plant-Microbe Interact 1994, 7(5):612-620.
72. Gallou A, Declerck S, Cranenbrouck S: Transcriptional regulation of defence genes and involvement of the WRKY transcription factor in arbuscular mycorrhizal potato root colonization. Funct Integr Genom 2012, 12(1):183-198.
73. Wulf A, Manthey K, Doll J, Perlick AM, Linke B, Bekel T, Meyer F, Franken P, Kuster H, Krajinski F: Transcriptional changes in response to arbuscular mycorrhiza development in the model plant Medicago truncatula. Mol Plant-Microbe Interact 2003, 16(4):306-314.
74. Fukai E, Soyano T, Umehara Y, Nakayama S, Hirakawa H, Tabata S, Sato S, Hayashi M: Establishment of a Lotus japonicus gene tagging population using the exon-targeting endogenous retrotransposon LORE1. Plant J 2012, 69(4):720-730.
75. Tadege M, Ratet P, Mysore KS: Insertional mutagenesis: a Swiss army knife for functional genomics of Medicago truncatula. Trends Plant Sci 2005, 10(5):229-235.
76. Vandenbussche M, Janssen A, Zethof J, van Orsouw N, Peters J, van Eijk MJT, Rijpkema AS, Schneiders H, Santhanam P, de Been M, van Tunen A, Gerats T: Generation of a 3D indexed Petunia insertion database for reverse genetics. Plant J 2008, 54(6):1105-1114.
77. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, Claverie JM, Gascuel O: Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 2008, 36:W465-W469.
78. Anisimova M, Gascuel O: Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Syst Biol 2006, 55(4):539-552.
79. Kersey PJ, Staines DM, Lawson D, Kulesha E, Derwent P, Humphrey JC, Hughes DST, Keenan S, Kerhornou A, Koscielny G, Langridge N, McDowall MD, Megy K, Maheswari U, Nuhn M, Paulini M, Pedro H, Toneva I, Wilson D, Yates A, Birney E: Ensembl Genomes: an integrative resource for genome-scale data from non-vertebrate species. Nucleic Acids Res 2012, 40(D1):D91-D97.
80. Junier T, Zdobnov EM: The Newick utilities: high-throughput phylogenetic tree processing in the Unix shell. Bioinformatics 2010, 26(13):1669-1670.
81. Benedito VA, Torres-Jerez I, Murray JD, Andriankaja A, Allen S, Kakar K, Wandrey M, Verdier J, Zuber H, Ott T, Moreau S, Niebel A, Frickey T, Weiller G, He J, Dai X, Zhao P, Tang Y, Udvardi M, Moreau S, Niebel A, Frickey T, Weiller G, He J, Dai X, Zhao P, Tang Y, Udvardi M: A gene expression atlas of the model legume Medicago truncatula. Plant J 2008, 55(3):504-513.
82. He J, Benedito VA, Wang MY, Murray JD, Zhao PX, Tang YH, Udvardi MK: The Medicago truncatula gene expression atlas web server. BMC Bioinformatics 2009, 10:441.
83. Smoot ME, Ono K, Ruscheinski J, Wang PL, Ideker T: Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 2011, 27(3):431-432.
84. Morris JH, Apeltsin L, Newman AM, Baumbach J, Wittkop T, Su G, Bader GD, Ferrin TE: clusterMaker: a multi-algorithm clustering plugin for Cytoscape. BMC Bioinformatics 2011, 12:436.
85. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren JY, Li WW, Noble WS: MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 2009, 37:W202-W208.
86. Rice P, Longden I, Bleasby A: EMBOSS: The European molecular biology open software suite. Trends Genet 2000, 16(6):276-277.
87. Delaux PM, Varala K, Edger PP, Coruzzi GM, Pires JC, Ané JM: Comparative phylogenomics uncovers the impact of symbiotic associations on host genome evolution. PLoS Genet 2014, 10(7):e1004487.