Exploring structural variation and gene family architecture with De Novo assemblies of 15 Medicago genomes

BMC Genomics

Volumn 18, Issue 1, 2017, Pages

  Zhou, Peng ^a   Silverstein, Kevin A T ^a   Ramaraj, Thiruvarangan ^b   Guhlin, Joseph ^a   Denny, Roxanne ^a   Liu, Junqi ^a   Farmer, Andrew D ^b   Steele, Kelly P ^c   Stupar, Robert M ^a   Miller, Jason R ^d   Tiffin, Peter ^a   Mudge, Joann ^b   Young, Nevin D ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b NATIONAL CENTER FOR GENOME RESOURCES   (United States)

^c ARIZONA STATE UNIVERSITY   (United States)

^d J CRAIG VENTER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BARREL MEDIC; BASE PAIRING; BIOTIC STRESS; COPY NUMBER VARIATION; GENE IDENTIFICATION; GENE SEQUENCE; GENE STRUCTURE; GENETIC ASSOCIATION; GENETIC VARIATION; MAIZE; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE BINDING SITE; ORTHOLOGY; PLANT GENOME; RICE; SINGLE NUCLEOTIDE POLYMORPHISM; SOYBEAN; SPECIES COMPARISON; SYNTENY; CHEMISTRY; COMPARATIVE GENOMIC HYBRIDIZATION; DNA SEQUENCE; GENETICS; HIGH THROUGHPUT SEQUENCING; ISOLATION AND PURIFICATION; METABOLISM; SEQUENCE ALIGNMENT;

HEAT SHOCK PROTEIN; LEUCINE-RICH REPEAT PROTEINS; PLANT PROTEIN; PLANT RNA; PROTEIN;

COMPARATIVE GENOMIC HYBRIDIZATION; DNA COPY NUMBER VARIATIONS; GENOME, PLANT; HEAT-SHOCK PROTEINS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MEDICAGO TRUNCATULA; PLANT PROTEINS; PROTEINS; RNA, PLANT; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA;

EID: 85016145317     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-017-3654-1     Document Type: Article

References (69)

1. Graham PH. Legumes: Importance and Constraints to Greater Use. Plant Physiol. 2003;131:872-7.
2. Lavin M, Herendeen P, Wojciechowski M. Evolutionary Rates Analysis of Leguminosae Implicates a Rapid Diversification of Lineages during the Tertiary. Syst Biol. 2005;54:575-94.
3. Young ND, Udvardi M. Translating Medicago truncatula genomics to crop legumes. Curr Opin Plant Biol. 2009;12:193-201.
4. Ronfort J, Bataillon T, Santoni S, Delalande M, David JL, Prosperi J-M. Microsatellite diversity and broad scale geographic structure in a model legume: building a set of nested core collection for studying naturally occurring variation in Medicago truncatula. BMC Plant Biol. 2006;6:28.
5. Tadege M, Wen J, He J, Tu H, Kwak Y, Eschstruth A, et al. Large-scale insertional mutagenesis using the Tnt1 retrotransposon in the model legume Medicago truncatula. Plant J. 2008;54:335-47.
6. Oldroyd GED, Downie JA. Coordinating Nodule Morphogenesis with Rhizobial Infection in Legumes. Annu Rev Plant Biol. 2008;59:519-46.
7. Tang H, Krishnakumar V, Bidwell S, Rosen B, Chan A, Zhou S, et al. An improved genome release (version Mt4.0) for the model legume Medicago truncatula. BMC Genomics. 2014;15:312.
8. Branca A, Paape TD, Zhou P, Briskine R, Farmer AD, Mudge J, et al. Whole-genome nucleotide diversity, recombination, and linkage disequilibrium in the model legume Medicago truncatula. Proc Natl Acad Sci. 2011;108:E864-70.
9. Stanton-Geddes J, Paape T, Epstein B, Briskine R, Yoder J, Mudge J, et al. Candidate Genes and Genetic Architecture of Symbiotic and Agronomic Traits Revealed by Whole-Genome, Sequence-Based Association Genetics in Medicago truncatula. PLoS One. 2013;8, e65688.
10. Meyers BC. Genome-Wide Analysis of NBS-LRR-Encoding Genes in Arabidopsis. Plant Cell. 2003;15:809-34.
11. Shiu S-H, Bleecker AB. Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci. 2001;98:10763-8.
12. Kuroda H. Classification and Expression Analysis of Arabidopsis F-Box-Containing Protein Genes. Plant Cell Physiol. 2002;43:1073-85.
13. Michelmore RW, Meyers BC. Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res. 1998;8:1113-30.
14. Richly E, Kurth J, Leister D. Mode of Amplification and Reorganization of Resistance Genes During Recent Arabidopsis thaliana Evolution. Mol Biol Evol. 2002;19:76-84.
15. Leister D. Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance genes. Trends Genet. 2004;20:116-22.
16. Shiu S-H, Bleecker AB. Expansion of the Receptor-Like Kinase/Pelle Gene Family and Receptor-Like Proteins in Arabidopsis. Plant Physiol. 2003;132:530-43.
17. Xu G, Ma H, Nei M, Kong H. Evolution of F-box genes in plants: Different modes of sequence divergence and their relationships with functional diversification. Proc Natl Acad Sci. 2009;106:835-40.
18. Meyers BC, Dickerman AW, Michelmore RW, Sivaramakrishnan S, Sobral BW, Young ND. Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily. Plant J. 1999;20:317-32.
19. Padmanabhan M, Cournoyer P, Dinesh-Kumar SP. The leucine-rich repeat domain in plant innate immunity: A wealth of possibilities. Cell Microbiol. 2009;11:191-8.
20. Sung D, Kaplan F, Guy CL. Plant Hsp70 molecular chaperones: protein structure, gene family, expression and function. Physiol Plant. 2001;113:443-51.
21. Graham MA. Computational Identification and Characterization of Novel Genes from Legumes. Plant Physiol. 2004;135:1179-97.
22. Silverstein KAT. Genome Organization of More Than 300 Defensin-Like Genes in Arabidopsis. Plant Physiol. 2005;138:600-10.
23. Silverstein KA, Moskal WA, Wu HC, Underwood BA, Graham MA, Town CD, et al. Small cysteine-rich peptides resembling antimicrobial peptides have been under-predicted in plants. Plant J. 2007;51:262-80.
24. Alunni B, Kevei Z, Redondo-Nieto M, Kondorosi A, Mergaert P, Kondorosi E. Genomic Organization and Evolutionary Insights on GRP and NCR Genes, Two Large Nodule-Specific Gene Families in Medicago truncatula. Mol Plant-Microbe Interact. 2007;20:1138-48.
25. Mergaert P. A Novel Family in Medicago truncatula Consisting of More Than 300 Nodule-Specific Genes Coding for Small, Secreted Polypeptides with Conserved Cysteine Motifs. Plant Physiol. 2003;132:161-73.
26. Farkas A, Maroti G, Durg H, Gyorgypal Z, Lima RM, Medzihradszky KF, et al. Medicago truncatula symbiotic peptide NCR247 contributes to bacteroid differentiation through multiple mechanisms. Proc Natl Acad Sci. 2014;111:5183-8.
27. Young ND, Zhou P, Silverstein KAT. Exploring structural variants in environmentally sensitive gene families. Curr Opin Plant Biol. 2016;30:19-24.
28. Clark RM, Schweikert G, Toomajian C, Ossowski S, Zeller G, Shinn P, et al. Common Sequence Polymorphisms Shaping Genetic Diversity in Arabidopsis thaliana. Science. 2007;317:338-42.
29. Cao J, Schneeberger K, Ossowski S, Günther T, Bender S, Fitz J, et al. Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat Genet. 2011;43:956-63.
30. Schatz MC, Maron LG, Stein JC, Wences A, Gurtowski J, Biggers E, et al. Whole genome de novo assemblies of three divergent strains of rice, Oryza sativa, document novel gene space of aus and indica. Genome Biol. 2014;15:506.
31. Gnerre S, MacCallum I, Przybylski D, Ribeiro FJ, Burton JN, Walker BJ, et al. High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc Natl Acad Sci. 2011;108:1513-8.
32. Smit A, Hubley R, Green P. RepeatMasker Open-4.0. 2013-2015. http://www.repeatmasker.org. 2013. Accessed 24 Mar 2017.
33. Stanke M, Waack S. Gene prediction with a hidden Markov model and a new intron submodel. th a hidden Markov model and a new intron submodel. Bioinformatics. 2003;19:ii215-25.
34. Nielsen R. Molecular Signatures of Natural Selection. Annu Rev Genet. 2005;39:197-218.
35. Conrad DF, Pinto D, Redon R, Feuk L, Gokcumen O, Zhang Y, et al. Origins and functional impact of copy number variation in the human genome. Nature. 2010;464:704-12.
36. Redon R, Ishikawa S, Fitch KR, Feuk L, Perry GH, Andrews TD, et al. Global variation in copy number in the human genome. Nature. 2006;444:444-54.
37. Ye K, Schulz MH, Long Q, Apweiler R, Ning Z. Pindel: A pattern growth approach to detect break points of large deletions and medium sized insertions from paired-end short reads. Bioinformatics. 2009;25:2865-71.
38. Li S, Li R, Li H, Lu J, Li Y, Bolund L, et al. SOAPindel: Efficient identification of indels from short paired reads. Genome Res. 2013;23:195-200.
39. Gore MA, Chia J-M, Elshire RJ, Sun Q, Ersoz ES, Hurwitz BL, et al. A First-Generation Haplotype Map of Maize. Science. 2009;326:1115-7.
40. Lam H-M, Xu X, Liu X, Chen W, Yang G, Wong F-L, et al. Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nat Genet. 2010;42:1053-9.
41. Zheng L-Y, Guo X-S, He B, Sun L-J, Peng Y, Dong S-S, et al. Genome-wide patterns of genetic variation in sweet and grain sorghum (Sorghum bicolor). Genome Biol. 2011;12:R114.
42. Chia J-M, Song C, Bradbury PJ, Costich D, de Leon N, Doebley J, et al. Maize HapMap2 identifies extant variation from a genome in flux. Nat Genet. 2012;44:803-7.
43. Huang X, Kurata N, Wei X, Wang Z-XX, Wang A, Zhao Q, et al. A map of rice genome variation reveals the origin of cultivated rice. Nature. 2012;490:497-501.
44. Gordon SP, Priest H, Des Marais DL, Schackwitz W, Figueroa M, Martin J, et al. Genome diversity in Brachypodium distachyon: deep sequencing of highly diverse inbred lines. Plant J. 2014;79:361-74.
45. Xu X, Liu X, Ge S, Jensen JD, Hu F, Li X, et al. Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes. Nat Biotechnol. 2012;30:105-11.
46. Gan X, Stegle O, Behr J, Steffen JG, Drewe P, Hildebrand KL, et al. Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature. 2011;477:419-23.
47. Li Y, Zhou G, Ma J, Jiang W, Jin L, Zhang Z, et al. De novo assembly of soybean wild relatives for pan-genome analysis of diversity and agronomic traits. Nat Biotechnol. 2014;32:1045-52.
48. Golicz AA, Bayer PE, Barker GC, Edger PP, Kim H, Martinez PA, et al. The pangenome of an agronomically important crop plant Brassica oleracea. Nat Commun. 2016;7:13390.
49. Hirsch CN, Foerster JM, Johnson JM, Sekhon RS, Muttoni G, Vaillancourt B, et al. Insights into the Maize Pan-Genome and Pan-Transcriptome. Plant Cell. 2014;26:121-35.
50. Zhang Q-J, Zhu T, Xia E-H, Shi C, Liu Y-L, Zhang Y, et al. Rapid diversification of five Oryza AA genomes associated with rice adaptation. Proc Natl Acad Sci. 2014;111:E4954-62.
51. Marone D, Russo M, Laidò G, De Leonardis A, Mastrangelo A. Plant Nucleotide Binding Site-Leucine-Rich Repeat (NBS-LRR) Genes: Active Guardians in Host Defense Responses. Int J Mol Sci. 2013;14:7302-26.
52. Yoder JB, Briskine R, Mudge J, Farmer A, Paape T, Steele K, et al. Phylogenetic Signal Variation in the Genomes of Medicago (Fabaceae). Syst Biol. 2013;62:424-38.
53. Murray MG, Thompson WF. Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res. 1980;8:4321-6.
54. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009;25:1105-11.
55. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, et al. Pfam: the protein families database. Nucleic Acids Res. 2014;42:D222-30.
56. Eddy SR. Accelerated Profile HMM Searches. PLoS Comput Biol. 2011;7, e1002195.
57. Ameline-Torregrosa C, Wang B-B, O'Bleness MS, Deshpande S, Zhu H, Roe B, et al. Identification and Characterization of Nucleotide-Binding Site-Leucine-Rich Repeat Genes in the Model Plant Medicago truncatula. Plant Physiol. 2007;146:5-21.
58. Zhou P, Silverstein KA, Gao L, Walton JD, Nallu S, Guhlin J, et al. Detecting small plant peptides using SPADA (Small Peptide Alignment Discovery Application). BMC Bioinformatics. 2013;14:335.
59. DOLEZEL J, Plant DNA. Flow Cytometry and Estimation of Nuclear Genome Size. Ann Bot. 2005;95:99-110.
60. Kent WJ. BLAT - The BLAST-like alignment tool. Genome Res. 2002;12:656-64.
61. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25:2078-9.
62. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, et al. BLAST plus: architecture and applications. BMC Bioinformatics. 2009;10:421.
63. Benson G. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 1999;27:573-80.
64. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403-10.
65. Angiuoli SV, Salzberg SL. Mugsy: Fast multiple alignment of closely related whole genomes. Bioinformatics. 2011;27:334-42.
66. R Development Core Team. R: A Language and Environment for Statistical Computing. R Found. Stat. Comput. Vienna Austria. 2016;0:[ISBN] 3-900051-07-0.
67. Li L. OrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes. Genome Res. 2003;13:2178-89.
68. Cingolani P, Platts A, Wang LL, Coon M, Nguyen T, Wang L, et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w 1118; iso-2; iso-3. Fly. 2012;6:80-92.
69. Chaisson MJ, Tesler G. Mapping single molecule sequencing reads using basic local alignment with successive refinement (BLASR): application and theory. BMC Bioinformatics. 2012;13:238.