Insights into the maize pan-genome and pan-transcriptome

Plant Cell

Volumn 26, Issue 1, 2014, Pages 121-135

  Hirsch, Candice N ^a,d   Foerster, Jillian M ^b,e   Johnson, James M ^b,f   Sekhon, Rajandeep S ^b   Muttoni, German ^b,g   Vaillancourt, Brieanne ^a   Peñagaricano, Francisco ^b   Lindquist, Erika ^c   Pedraza, Mary Ann ^c   Barry, Kerrie ^c   de Leon, Natalia ^b   Kaeppler, Shawn M ^b   Robin Buell, C ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c DOE JOINT GENOME INSTITUTE   (United States)

^d UNIVERSITY OF MINNESOTA   (United States)

^e Pioneer Dupont   (United States)

^f AgReliant Genetics LLC   (United States)

^g MONSANTO COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTOME;

GENE LINKAGE DISEQUILIBRIUM; GENETICS; MAIZE; PLANT CHROMOSOME; PLANT GENOME; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM;

CHROMOSOMES, PLANT; GENOME, PLANT; LINKAGE DISEQUILIBRIUM; POLYMORPHISM, SINGLE NUCLEOTIDE; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, RNA; TRANSCRIPTOME; ZEA MAYS;

EID: 84896808010     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.119982     Document Type: Article

References (84)

1. Abendroth, L.J., Elmore, R.W., Boyer, M.J., and Marlay, S.K. (2011). Corn Growth and Development. (Ames, IA: Iowa State University Extension).
2. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990). Basic local alignment search tool. J. Mol. Biol. 215: 403-410.
3. Bertioli, D.J., et al. (2009). An analysis of synteny of Arachis with Lotus and Medicago sheds new light on the structure, stability and evolution of legume genomes. BMC Genomics 10: 45.
4. Briggs, W.H., McMullen, M.D., Gaut, B.S., and Doebley, J. (2007). Linkage mapping of domestication loci in a large maize teosinte backcross resource. Genetics 177: 1915-1928.
5. Brunner, S., Fengler, K., Morgante, M., Tingey, S., and Rafalski, A. (2005). Evolution of DNA sequence nonhomologies among maize inbreds. Plant Cell 17: 343-360.
6. Buckler, E.S., et al. (2009). The genetic architecture of maize flowering time. Science 325: 714-718.
7. Cao, J., et al. (2011). Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat. Genet. 43: 956-963.
8. Chardon, F., Virlon, B., Moreau, L., Falque, M., Joets, J., Decousset, L., Murigneux, A., and Charcosset, A. (2004). Genetic architecture of flowering time in maize as inferred from quantitative trait loci meta-analysis and synteny conservation with the rice genome. Genetics 168: 2169-2185.
9. Chen, C., DeClerck, G., Tian, F., Spooner, W., McCouch, S., and Buckler, E. (2012). PICARA, an analytical pipeline providing probabilistic inference about a priori candidates genes underlying genome-wide association QTL in plants. PLoS ONE 7: e46596.
10. Chen, F., Mackey, A.J., Vermunt, J.K., and Roos, D.S. (2007). Assessing performance of orthology detection strategies applied to eukaryotic genomes. PLoS ONE 2: e383.
11. Cheung, F., Trick, M., Drou, N., Lim, Y.P., Park, J.Y., Kwon, S.J., Kim, J.A., Scott, R., Pires, J.C., Paterson, A.H., Town, C., and Bancroft, I. (2009). Comparative analysis between homoeologous genome segments of Brassica napus and its progenitor species reveals extensive sequence-level divergence. Plant Cell 21: 1912-1928.
12. Chia, J.M., et al. (2012). Maize HapMap2 identifies extant variation from a genome in flux. Nat. Genet. 44: 803-807.
13. Chuck, G., Cigan, A.M., Saeteurn, K., and Hake, S. (2007). The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. Nat. Genet. 39: 544-549.
14. Clark, R.M., et al. (2007). Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana. Science 317: 338-342.
15. de Leon, N., and Coors, J.G. (2002). Twenty-four cycles of mass selection for prolificacy in the golden glow maize population. Crop Sci. 42: 325-333.
16. Dudley, J.W., and Lambert, R.J. (1992). Ninety generations of selection for oil and protein in maize. Maydica 37: 1-7.
17. Duvick, J., Fu, A., Muppirala, U., Sabharwal, M., Wilkerson, M.D., Lawrence, C.J., Lushbough, C., and Brendel, V. (2008). PlantGDB: A resource for comparative plant genomics. Nucleic Acids Res. 36: D959-D965.
18. Eichten, S.R., et al. (2011). Heritable epigenetic variation among maize inbreds. PLoS Genet. 7: e1002372.
19. Gan, X., et al. (2011). Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature 477: 419-423.
20. Gao, X., Becker, L.C., Becker, D.M., Starmer, J.D., and Province, M.A. (2010). Avoiding the high Bonferroni penalty in genome-wide association studies. Genet. Epidemiol. 34: 100-105.
21. Gao, X., Starmer, J., and Martin, E.R. (2008). A multiple testing correction method for genetic association studies using correlated single nucleotide polymorphisms. Genet. Epidemiol. 32: 361-369.
22. Gene Ontology Consortium (2010). The Gene Ontology in 2010: Extensions and refinements. Nucleic Acids Res. 38: D331-D335.
23. Gish, W., and States, D.J. (1993). Identification of protein coding regions by database similarity search. Nat. Genet. 3: 266-272.
24. Gore, M.A., Chia, J.M., Elshire, R.J., Sun, Q., Ersoz, E.S., Hurwitz, B.L., Peiffer, J.A., McMullen, M.D., Grills, G.S., Ross-Ibarra, J., Ware, D.H., and Buckler, E.S. (2009). A first-generation haplotype map of maize. Science 326: 1115-1117.
25. Hansey, C.N., Johnson, J.M., Sekhon, R.S., Kaeppler, S.M., and de Leon, N. (2010). Genetic diversity of a maize association population with restricted phenology. Crop Sci. 51: 704-715.
26. Hansey, C.N., Vaillancourt, B., Sekhon, R.S., de Leon, N., Kaeppler, S. M., and Buell, C.R. (2012). Maize (Zea mays L.) genome diversity as revealed by RNA-sequencing. PLoS ONE 7: e33071.
27. Hogg, J.S., Hu, F.Z., Janto, B., Boissy, R., Hayes, J., Keefe, R., Post, J.C., and Ehrlich, G.D. (2007). Characterization and modeling of the Haemophilus influenzae core and supragenomes based on the complete genomic sequences of Rd and 12 clinical nontypeable strains. Genome Biol. 8: R103.
28. Iseli, C., Jongeneel, C.V., and Bucher, P. (1999). ESTScan: A program for detecting, evaluating, and reconstructing potential coding regions in EST sequences. Proc. Int. Conf. Intell. Syst. Mol. Biol. 138-148.
29. Johnson, R.C., Nelson, G.W., Troyer, J.L., Lautenberger, J.A., Kessing, B.D., Winkler, C.A., and O'Brien, S.J. (2010). Accounting for multiple comparisons in a genome-wide association study (GWAS). BMC Genomics 11: 724.
30. Kahlke, T., Goesmann, A., Hjerde, E., Willassen, N.P., and Haugen, P. (2012). Unique core genomes of the bacterial family vibrionaceae: Insights into niche adaptation and speciation. BMC Genomics 13: 179.
31. Kane, N.A., Danyluk, J., Tardif, G., Ouellet, F., Laliberté, J.F., Limin, A.E., Fowler, D.B., and Sarhan, F. (2005). TaVRT-2, a member of the StMADS-11 clade of flowering repressors, is regulated by vernalization and photoperiod in wheat. Plant Physiol. 138: 2354-2363.
32. Kikuchi, R., Sage-Ono, K., Kamada, H., Handa, H., and Ono, M. (2008). PnMADS1, encoding an StMADS11-clade protein, acts as a repressor of flowering in Pharbitis nil. Physiol. Plant. 133: 786-793.
33. Kumar, P., Henikoff, S., and Ng, P.C. (2009). Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat. Protoc. 4: 1073-1081.
34. Lai, J., et al. (2010). Genome-wide patterns of genetic variation among elite maize inbred lines. Nat. Genet. 42: 1027-1030.
35. Langmead, B., Trapnell, C., Pop, M., and Salzberg, S.L. (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10: R25.
36. Lauter, N., Kampani, A., Carlson, S., Goebel, M., and Moose, S.P. (2005). MicroRNA172 down-regulates glossy15 to promote vegetative phase change in maize. Proc. Natl. Acad. Sci. USA 102: 9412-9417.
37. Lazakis, C.M., Coneva, V., and Colasanti, J. (2011). ZCN8 encodes a potential orthologue of Arabidopsis FT florigen that integrates both endogenous and photoperiod flowering signals in maize. J. Exp. Bot. 62: 4833-4842.
38. Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., and Durbin, R.1000 Genome Project Data Processing Subgroup (2009). The sequence alignment/map format and SAMtools. Bioinformatics 25: 2078-2079.
39. Li, L., and Stoeckert, C.J., Jr., and Roos, D.S. (2003). OrthoMCL: Identification of ortholog groups for eukaryotic genomes. Genome Res. 13: 2178-2189.
40. Lipka, A.E., Tian, F., Wang, Q., Peiffer, J., Li, M., Bradbury, P.J., Gore, M.A., Buckler, E.S., and Zhang, Z. (2012). GAPIT: Genome association and prediction integrated tool. Bioinformatics 28: 2397-2399.
41. Liu, K., and Muse, S.V. (2005). PowerMarker: An integrated analysis environment for genetic marker analysis. Bioinformatics 21: 2128-2129.
42. Makarevitch, I., Stupar, R.M., Iniguez, A.L., Haun, W.J., Barbazuk, W.B., Kaeppler, S.M., and Springer, N.M. (2007). Natural variation for alleles under epigenetic control by the maize chromomethylase zmet2. Genetics 177: 749-760.
43. Maron, L.G., et al. (2013). Aluminum tolerance in maize is associated with higher MATE1 gene copy number. Proc. Natl. Acad. Sci. USA 110: 5241-5246.
44. McNally, K.L., et al. (2009). Genomewide SNP variation reveals relationships among landraces and modern varieties of rice. Proc. Natl. Acad. Sci. USA 106: 12273-12278.
45. Medini, D., Donati, C., Tettelin, H., Masignani, V., and Rappuoli, R. (2005). The microbial pan-genome. Curr. Opin. Genet. Dev. 15: 589-594.
46. Moose, S.P., and Sisco, P.H. (1996). Glossy15, an APETALA2-like gene from maize that regulates leaf epidermal cell identity. Genes Dev. 10: 3018-3027.
47. Morgante, M., De Paoli, E., and Radovic, S. (2007). Transposable elements and the plant pan-genomes. Curr. Opin. Plant Biol. 10: 149-155.
48. Odhiambo, M.O., and Compton, W.A. (1987). Twenty cycles of divergent mass selection for seed size in Corn1. Crop Sci. 27: 1113-1116.
49. Ossowski, S., Schneeberger, K., Clark, R.M., Lanz, C., Warthmann, N., and Weigel, D. (2008). Sequencing of natural strains of Arabidopsis thaliana with short reads. Genome Res. 18: 2024-2033.
50. Ouyang, S., et al. (2007). The TIGR Rice Genome Annotation Resource: Improvements and new features. Nucleic Acids Res. 35: D883-D887.
51. Paterson, A.H., et al. (2009). The Sorghum bicolor genome and the diversification of grasses. Nature 457: 551-556.
52. Patterson, N., Price, A.L., and Reich, D. (2006). Population structure and eigenanalysis. PLoS Genet. 2: e190.
53. Poethig, R.S. (2009). Small RNAs and developmental timing in plants. Curr. Opin. Genet. Dev. 19: 374-378.
54. Purcell, S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M.A., Bender, D., Maller, J., Sklar, P., de Bakker, P.I., Daly, M.J., and Sham, P.C. (2007). PLINK: A tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81: 559-575.
55. Rogers, J.S. (1972). Measure of genetic similarity and genetic distance. Studies in Genomics. VII. Univ. Tex. Publ. 7213: 145-153.
56. Russell, W.K. (2006). Registration of KLS_30 and KSS_30 populations of maize. Crop Sci. 46: 1405-1406.
57. Saghai-Maroof, M.A., Soliman, K.M., Jorgensen, R.A., and Allard, R.W. (1984). Ribosomal DNA spacer-length polymorphisms in barley: mendelian inheritance, chromosomal location, and population dynamics. Proc. Natl. Acad. Sci. USA 81: 8014-8018.
58. Salvi, S., et al. (2007). Conserved noncoding genomic sequences associated with a flowering-time quantitative trait locus in maize. Proc. Natl. Acad. Sci. USA 104: 11376-11381.
59. Scheet, P., and Stephens, M. (2006). A fast and flexible statistical model for large-scale population genotype data: Applications to inferring missing genotypes and haplotypic phase. Am. J. Hum. Genet. 78: 629-644.
60. Schnable, J.C., Springer, N.M., and Freeling, M. (2011). Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss. Proc. Natl. Acad. Sci. USA 108: 4069-4074.
61. Schnable, P.S., et al. (2009). The B73 maize genome: Complexity, diversity, and dynamics. Science 326: 1112-1115.
62. Schulz, M.H., Zerbino, D.R., Vingron, M., and Birney, E. (2012). Oases: Robust de novo RNA-seq assembly across the dynamic range of expression levels. Bioinformatics 28: 1086-1092.
63. Sekhon, R.S., Briskine, R., Hirsch, C.N., Myers, C.L., Springer, N.M., Buell, C.R., de Leon, N., and Kaeppler, S.M. (2013). Maize gene atlas developed by RNA sequencing and comparative evaluation of transcriptomes based on RNA sequencing and microarrays. PLoS ONE 8: e61005.
64. Sekhon, R.S., Lin, H., Childs, K.L., Hansey, C.N., Buell, C.R., de Leon, N., and Kaeppler, S.M. (2011). Genome-wide atlas of transcription during maize development. Plant J. 66: 553-563.
65. Sentoku, N., Kato, H., Kitano, H., and Imai, R. (2005). OsMADS22, an STMADS11-like MADS-box gene of rice, is expressed in nonvegetative tissues and its ectopic expression induces spikelet meristem indeterminacy. Mol. Genet. Genomics 273: 1-9.
66. Springer, N.M., et al. (2009). Maize inbreds exhibit high levels of copy number variation (CNV) and presence/absence variation (PAV) in genome content. PLoS Genet. 5: e1000734.
67. Stupar, R.M., and Springer, N.M. (2006). Cis-transcriptional variation in maize inbred lines B73 and Mo17 leads to additive expression patterns in the F1 hybrid. Genetics 173: 2199-2210.
68. Suzek, B.E., Huang, H., McGarvey, P., Mazumder, R., and Wu, C.H. (2007). UniRef: Comprehensive and non-redundant UniProt reference clusters. Bioinformatics 23: 1282-1288.
69. Swanson-Wagner, R.A., Eichten, S.R., Kumari, S., Tiffin, P., Stein, J.C., Ware, D., and Springer, N.M. (2010). Pervasive gene content variation and copy number variation in maize and its undomesticated progenitor. Genome Res. 20: 1689-1699.
70. Swanson-Wagner, R.A., Jia, Y., DeCook, R., Borsuk, L.A., Nettleton, D., and Schnable, P.S. (2006). All possible modes of gene action are observed in a global comparison of gene expression in a maize F1 hybrid and its inbred parents. Proc. Natl. Acad. Sci. USA 103: 6805-6810.
71. Tettelin, H., et al. (2005). Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: Implications for the microbial "pan-genome". Proc. Natl. Acad. Sci. USA 102: 13950-13955.
72. Tettelin, H., Riley, D., Cattuto, C., and Medini, D. (2008). Comparative genomics: The bacterial pan-genome. Curr. Opin. Microbiol. 11: 472-477.
73. Trapnell, C., Pachter, L., and Salzberg, S.L. (2009). TopHat: Discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111.
74. Trapnell, C., Williams, B.A., Pertea, G., Mortazavi, A., Kwan, G., van Baren, M.J., Salzberg, S.L., Wold, B.J., and Pachter, L. (2010). Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28: 511-515.
75. VanRaden, P.M. (2008). Efficient methods to compute genomic predictions. J. Dairy Sci. 91: 4414-4423.
76. Wang, J.W., Park, M.Y., Wang, L.J., Koo, Y., Chen, X.Y., Weigel, D., and Poethig, R.S. (2011). miRNA control of vegetative phase change in trees. PLoS Genet. 7: e1002012.
77. Weigel, D., and Mott, R. (2009). The 1001 genomes project for Arabidopsis thaliana. Genome Biol. 10: 107.
78. Wu, T.D., and Watanabe, C.K. (2005). GMAP: A genomic mapping and alignment program for mRNA and EST sequences. Bioinformatics 21: 1859-1875.
79. Xu, J., Liu, Y., Liu, J., Cao, M., Wang, J., Lan, H., Xu, Y., Lu, Y., Pan, G., and Rong, T. (2012). The genetic architecture of flowering time and photoperiod sensitivity in maize as revealed by QTL review and meta analysis. J. Integr. Plant Biol. 54: 358-373.
80. Yu, J., Pressoir, G., Briggs, W.H., Vroh Bi, I., Yamasaki, M., Doebley, J.F., McMullen, M.D., Gaut, B.S., Nielsen, D.M., Holland, J.B., Kresovich, S., and Buckler, E.S. (2006). A unified mixedmodel method for association mapping that accounts for multiple levels of relatedness. Nat. Genet. 38: 203-208.
81. Zdobnov, E.M., and Apweiler, R. (2001). InterProScan-An integration platform for the signature-recognition methods in InterPro. Bioinformatics 17: 847-848.
82. Zerbino, D.R., and Birney, E. (2008). Velvet: Algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18: 821-829.
83. Zhang, Z., Ersoz, E., Lai, C.Q., Todhunter, R.J., Tiwari, H.K., Gore, M.A., Bradbury, P.J., Yu, J., Arnett, D.K., Ordovas, J.M., and Buckler, E.S. (2010). Mixed linear model approach adapted for genome-wide association studies. Nat. Genet. 42: 355-360.
84. Zhao, Q., Weber, A.L., McMullen, M.D., Guill, K., and Doebley, J. (2011). MADS-box genes of maize: Frequent targets of selection during domestication. Genet. Res. 93: 65-75.