1932

Abstract

Maize occupies dual roles as both () one of the big-three grain species (along with rice and wheat) responsible for providing more than half of the calories consumed around the world, and () a model system for plant genetics and cytogenetics dating back to the origin of the field of genetics in the early twentieth century. The long history of genetic investigation in this species combined with modern genomic and quantitative genetic data has provided particular insight into the characteristics of genes linked to phenotypes and how these genes differ from many other sequences in plant genomes that are not easily distinguishable based on molecular data alone. These recent results suggest that the number of genes in plants that make significant contributions to phenotype may be lower than the number of genes defined by current molecular criteria, and also indicate that syntenic conservation has been underemphasized as a marker for gene function.

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2015-04-29
2024-06-21
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Literature Cited

  1. 1. Arabidopsis Genome Initiat 2000. Analysis of the genome sequence of the flowering plant. Arabidopsis thaliana Nature 408:796–815 [Google Scholar]
  2. Barbaglia AM, Klusman KM, Higgins J, Shaw JR, Hannah LC, Lal SK. 2.  2012. Gene capture by helitron transposons reshuffles the transcriptome of maize. Genetics 190:965–75 [Google Scholar]
  3. Baucom RS, Estill JC, Chaparro C, Upshaw N, Jogi A. 3.  et al. 2009. Exceptional diversity, non-random distribution, and rapid evolution of retroelements in the B73 maize genome. PLOS Genet. 5:e1000732 [Google Scholar]
  4. Bekaert M, Edger PP, Pires JC, Conant GC. 4.  2011. Two-phase resolution of polyploidy in the Arabidopsis metabolic network gives rise to relative and absolute dosage constraints. Plant Cell 23:1719–28 [Google Scholar]
  5. Bennetzen JL, Buckler E, Chandler V, Doebley J, Dorweiler J. 5.  et al. 2001. Genetic evidence and the origin of maize. Lat. Am. Antiq. 12:84–86 [Google Scholar]
  6. Bennetzen JL, Coleman C, Liu R, Ma J, Ramakrishna W. 6.  2004. Consistent over-estimation of gene number in complex plant genomes. Curr. Opin. Plant Biol. 7:732–36 [Google Scholar]
  7. Bennetzen JL, Freeling M. 7.  1993. Grasses as a single genetic system: genome composition, collinearity and compatibility. Trends Genet. 9:259–61 [Google Scholar]
  8. Bennetzen JL, Freeling M. 8.  1997. The unified grass genome: synergy in synteny. Genome Res. 7:301–6 [Google Scholar]
  9. Bennetzen JL, Ma J, Devos KM. 9.  2005. Mechanisms of recent genome size variation in flowering plants. Ann. Bot. 95:127–32 [Google Scholar]
  10. Berhan AM, Hulbert SH, Butler LG, Bennetzen JL. 10.  1993. Structure and evolution of the genomes of Sorghum bicolor and Zea mays. Theor. Appl. Genet. 86:598–604 [Google Scholar]
  11. Birchler JA, Riddle NC, Auger DL, Veitia RA. 11.  2005. Dosage balance in gene regulation: biological implications. Trends Genet. 21:219–26 [Google Scholar]
  12. Birchler JA, Veitia RA. 12.  2007. The gene balance hypothesis: from classical genetics to modern genomics. Plant Cell 19:395–402 [Google Scholar]
  13. Birchler JA, Veitia RA. 13.  2010. The gene balance hypothesis: implications for gene regulation, quantitative traits and evolution. New Phytol. 186:54–62 [Google Scholar]
  14. Birchler JA, Yao H, Chudalayandi S. 14.  2007. Biological consequences of dosage dependent gene regulatory systems. Biochim. Biophys. Acta 1769:422–28 [Google Scholar]
  15. Blanc G, Wolfe KH. 15.  2004. Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 16:1667–78 [Google Scholar]
  16. Bolot S, Abrouk M, Masood-Quraishi U, Stein N, Messing J. 16.  et al. 2009. The “inner circle” of the cereal genomes. Curr. Opin. Plant Biol. 12:119–25 [Google Scholar]
  17. Bomblies K, Doebley JF. 17.  2005. Molecular evolution of FLORICAULA/LEAFY orthologs in the Andropogoneae (Poaceae). Mol. Biol. Evol. 22:1082–94 [Google Scholar]
  18. Bomblies K, Wang R-L, Ambrose BA, Schmidt RJ, Meeley RB, Doebley J. 18.  2003. Duplicate FLORICAULA/LEAFY homologs zfl1 and zfl2 control inflorescence architecture and flower patterning in maize. Development 130:2385–95 [Google Scholar]
  19. Bouché N, Bouchez D. 19.  2001. Arabidopsis gene knockout: phenotypes wanted. Curr. Opin. Plant Biol. 4:111–17 [Google Scholar]
  20. Chia J-M, Song C, Bradbury PJ, Costich D, de Leon N. 20.  et al. 2012. Maize HapMap2 identifies extant variation from a genome in flux. Nat. Genet. 44:803–7 [Google Scholar]
  21. Christin P-A, Spriggs E, Osborne CP, Strömberg CAE, Salamin N, Edwards EJ. 21.  2014. Molecular dating, evolutionary rates, and the age of the grasses. Syst. Biol. 63:153–65 [Google Scholar]
  22. Clark LG, Zhang W, Wendel JF. 22.  1995. A phylogeny of the grass family (Poaceae) based on ndhF sequence data. Syst. Bot. 20:436–60 [Google Scholar]
  23. Davidson RM, Gowda M, Moghe G, Lin H, Vaillancourt B. 23.  et al. 2012. Comparative transcriptomics of three Poaceae species reveals patterns of gene expression evolution. Plant J. 71:492–502 [Google Scholar]
  24. Dewey CN. 24.  2011. Positional orthology: putting genomic evolutionary relationships into context. Brief. Bioinform. 12:401–12 [Google Scholar]
  25. Doebley JF, Gaut BS, Smith BD. 25.  2006. The molecular genetics of crop domestication. Cell 127:1309–21 [Google Scholar]
  26. Eichten SR, Swanson-Wagner RA, Schnable JC, Waters AJ, Hermanson PJ. 26.  et al. 2011. Heritable epigenetic variation among maize inbreds. PLOS Genet. 7:e1002372 [Google Scholar]
  27. Emrich SJ, Li L, Wen T-J, Yandeau-Nelson MD, Fu Y. 27.  et al. 2007. Nearly identical paralogs: implications for maize (Zea mays L.) genome evolution. Genetics 175:429–39 [Google Scholar]
  28. Ezkurdia I, Juan D, Rodriguez JM, Frankish A, Diekhans M. 28.  et al. 2014. Multiple evidence strands suggest that there may be as few as 19 000 human protein-coding genes. Hum. Mol. Genet. 23:5866–78 [Google Scholar]
  29. Ferguson AA, Zhao D, Jiang N. 29.  2013. Selective acquisition and retention of genomic sequences by pack-mutator-like elements based on guanine-cytosine content and the breadth of expression. Plant Physiol. 163:1419–32 [Google Scholar]
  30. Fitch WM. 30.  1970. Distinguishing homologous from analogous proteins. Syst. Biol. 19:99–113 [Google Scholar]
  31. Foster T, Yamaguchi J, Wong BC, Veit B, Hake S. 31.  1999. Gnarley1 is a dominant mutation in the knox4 homeobox gene affecting cell shape and identity. Plant Cell 11:1239–52 [Google Scholar]
  32. Franken P, Niesbach-Klösgen U, Weydemann U, Maréchal-Drouard L, Saedler H, Wienand U. 32.  1991. The duplicated chalcone synthase genes C2 and Whp (white pollen) of Zea mays are independently regulated; evidence for translational control of Whp expression by the anthocyanin intensifying gene in. EMBO J. 10:2605–12 [Google Scholar]
  33. Freeling M. 33.  2009. Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition. Annu. Rev. Plant Biol. 60:433–53 [Google Scholar]
  34. Freeling M, Lyons E, Pedersen B, Alam M, Ming R, Lisch D. 34.  2008. Many or most genes in Arabidopsis transposed after the origin of the order Brassicales. Genome Res. 18:1924–37 [Google Scholar]
  35. Freeling M, Woodhouse MR, Subramaniam S, Turco G, Lisch D, Schnable JC. 35.  2012. Fractionation mutagenesis and similar consequences of mechanisms removing dispensable or less-expressed DNA in plants. Curr. Opin. Plant Biol. 15:131–39 [Google Scholar]
  36. Fu H, Dooner HK. 36.  2002. Intraspecific violation of genetic colinearity and its implications in maize. PNAS 99:9573–78 [Google Scholar]
  37. Gaut BS, Doebley JF. 37.  1997. DNA sequence evidence for the segmental allotetraploid origin of maize. PNAS 94:6809–14 [Google Scholar]
  38. Gerstein MB, Bruce C, Rozowsky JS, Zheng D, Du J. 38.  et al. 2007. What is a gene, post-ENCODE? History and updated definition. Genome Res. 17:669–81 [Google Scholar]
  39. Goff SA, Ricke D, Lan T-H, Presting G, Wang R. 39.  et al. 2002. A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296:92–100 [Google Scholar]
  40. Gore MA, Chia J-M, Elshire RJ, Sun Q, Ersoz ES. 40.  et al. 2009. A first-generation haplotype map of maize. Science 326:1115–17 [Google Scholar]
  41. 41. Grass Phylogeny Work. Group 2001. Phylogeny and subfamilial classification of the grasses (Poaceae). Ann. Mo. Bot. Gard. 88:373–457 [Google Scholar]
  42. 42. Grass Phylogeny Work. Group 2012. New grass phylogeny resolves deep evolutionary relationships and discovers C4 origins. New Phytol. 193:304–12 [Google Scholar]
  43. Gupta S, Gallavotti A, Stryker GA, Schmidt RJ, Lal SK. 43.  2005. A novel class of helitron-related transposable elements in maize contain portions of multiple pseudogenes. Plant Mol. Biol. 57:115–27 [Google Scholar]
  44. Hillier LW, Coulson A, Murray JI, Bao Z, Sulston JE, Waterston RH. 44.  2005. Genomics in C. elegans: so many genes, such a little worm. Genome Res. 15:1651–60 [Google Scholar]
  45. Hirsch CN, Foerster JM, Johnson JM, Sekhon RS, Muttoni G. 45.  et al. 2014. Insights into the maize pan-genome and pan-transcriptome. Plant Cell 26:121–35 [Google Scholar]
  46. Hufford MB, Lubinksy P, Pyhäjärvi T, Devengenzo MT, Ellstrand NC, Ross-Ibarra J. 46.  2013. The genomic signature of crop-wild introgression in maize. PLOS Genet. 9:e1003477 [Google Scholar]
  47. Jia Y, Lisch DR, Ohtsu K, Scanlon MJ, Nettleton D, Schnable PS. 47.  2009. Loss of RNA-dependent RNA polymerase 2 (RDR2) function causes widespread and unexpected changes in the expression of transposons, genes, and 24-nt small RNAs. PLOS Genet. 5:e1000737 [Google Scholar]
  48. Jiang N, Bao Z, Zhang X, Eddy SR, Wessler SR. 48.  2004. Pack-MULE transposable elements mediate gene evolution in plants. Nature 431:569–73 [Google Scholar]
  49. Kawabe A, Hansson B, Hagenblad J, Forrest A, Charlesworth D. 49.  2006. Centromere locations and associated chromosome rearrangements in Arabidopsis lyrata and A. thaliana. Genetics 173:1613–19 [Google Scholar]
  50. Kellogg EA. 50.  2000. The grasses: a case study in macroevolution. Annu. Rev. Ecol. Syst. 31:217–38 [Google Scholar]
  51. Kuromori T, Wada T, Kamiya A, Yuguchi M, Yokouchi T. 51.  et al. 2006. A trial of phenome analysis using 4000 Ds-insertional mutants in gene-coding regions of Arabidopsis. Plant J. 47:640–51 [Google Scholar]
  52. Lai J, Li R, Xu X, Jin W, Xu M. 52.  et al. 2010. Genome-wide patterns of genetic variation among elite maize inbred lines. Nat. Genet. 42:1027–30 [Google Scholar]
  53. Lai J, Li Y, Messing J, Dooner HK. 53.  2005. Gene movement by helitron transposons contributes to the haplotype variability of maize. PNAS 102:9068–73 [Google Scholar]
  54. Lisch D. 54.  2013. How important are transposons for plant evolution?. Nat. Rev. Genet. 14:49–61 [Google Scholar]
  55. Longley AE. 55.  1941. Chromosome morphology in maize and its relatives. Bot. Rev. 7:263–89 [Google Scholar]
  56. Lynch M, Conery JS. 56.  2000. The evolutionary fate and consequences of duplicate genes. Science 290:1151–55 [Google Scholar]
  57. Lyons E, Pedersen B, Kane J, Freeling M. 57.  2008. The value of nonmodel genomes and an example using SynMap within CoGe to dissect the hexaploidy that predates the rosids. Trop. Plant Biol. 1:181–90 [Google Scholar]
  58. Maeda I, Kohara Y, Yamamoto M, Sugimoto A. 58.  2001. Large-scale analysis of gene function in Caenorhabditis elegans by high-throughput RNAi. Curr. Biol. 11:171–76 [Google Scholar]
  59. Mangelsdorf PC, Reeves RG. 59.  1931. Hybridization of maize, Tripsacum, and Euchlaena. J. Hered. 22:329–43 [Google Scholar]
  60. Mano Y, Omori F, Kindiger B, Takahashi H. 60.  2008. A linkage map of maize × teosinte Zea luxurians and identification of QTLs controlling root aerenchyma formation. Mol. Breed. 21:327–37 [Google Scholar]
  61. Mathews S, Spangler RE, Mason-Gamer RJ, Kellogg EA. 61.  2002. Phylogeny of Andropogoneae inferred from phytochrome B, GBSSI, and ndhF. Int. J. Plant Sci. 163:441–50 [Google Scholar]
  62. Mauro-Herrera M, Wang X, Barbier H, Brutnell TP, Devos KM, Doust AN. 62.  2013. Genetic control and comparative genomic analysis of flowering time in Setaria (Poaceae). G3 3:283–95 [Google Scholar]
  63. Messing J, Bharti AK, Karlowski WM, Gundlach H, Kim HR. 63.  et al. 2004. Sequence composition and genome organization of maize. PNAS 101:14349–54 [Google Scholar]
  64. Mikel MA, Dudley JW. 64.  2006. Evolution of North American dent corn from public to proprietary germplasm. Crop Sci. 46:1193 [Google Scholar]
  65. Moore G, Devos KM, Wang Z, Gale MD. 65.  1995. Cereal genome evolution. Grasses, line up and form a circle. Curr. Biol. 5:737–39 [Google Scholar]
  66. Morgante M, Brunner S, Pea G, Fengler K, Zuccolo A, Rafalski A. 66.  2005. Gene duplication and exon shuffling by helitron-like transposons generate intraspecies diversity in maize. Nat. Genet. 37:997–1002 [Google Scholar]
  67. Murat F, Xu J-H, Tannier E, Abrouk M, Guilhot N. 67.  et al. 2010. Ancestral grass karyotype reconstruction unravels new mechanisms of genome shuffling as a source of plant evolution. Genome Res. 20:1545–57 [Google Scholar]
  68. Nardmann J, Ji J, Werr W, Scanlon MJ. 68.  2004. The maize duplicate genes narrow sheath1 and narrow sheath2 encode a conserved homeobox gene function in a lateral domain of shoot apical meristems. Development 131:2827–39 [Google Scholar]
  69. O'Malley RC, Ecker JR. 69.  2010. Linking genotype to phenotype using the Arabidopsis unimutant collection. Plant J. 61:928–40 [Google Scholar]
  70. Ouyang S, Zhu W, Hamilton J, Lin H, Campbell M. 70.  et al. 2007. The TIGR Rice Genome Annotation Resource: improvements and new features. Nucleic Acids Res. 35:D883–87 [Google Scholar]
  71. Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J. 71.  et al. 2009. The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–56 [Google Scholar]
  72. Pennisi E. 72.  2003. A low number wins the GeneSweep pool. Science 300:1484 [Google Scholar]
  73. Prasad V, Strömberg CAE, Leaché AD, Samant B, Patnaik R. 73.  et al. 2011. Late Cretaceous origin of the rice tribe provides evidence for early diversification in Poaceae. Nat. Commun. 2:480 [Google Scholar]
  74. Reeves RG, Mangelsdorf PC. 74.  1942. A proposed taxonomic change in the tribe Maydeae (family Gramineae). Am. J. Bot. 29:815–17 [Google Scholar]
  75. Ross-Macdonald P, Coelho PS, Roemer T, Agarwal S, Kumar A. 75.  et al. 1999. Large-scale analysis of the yeast genome by transposon tagging and gene disruption. Nature 402:413–18 [Google Scholar]
  76. Russell WA. 76.  1972. Registration of B70 and B73 parental lines of maize (reg. nos. PL16 and PL17). Crop Sci. 12:721 [Google Scholar]
  77. Sakai H, Lee SS, Tanaka T, Numa H, Kim J. 77.  et al. 2013. Rice annotation project database (RAP-DB): an integrative and interactive database for rice genomics. Plant Cell Physiol. 54:e6 [Google Scholar]
  78. Salse J, Abrouk M, Bolot S, Guilhot N, Courcelle E. 78.  et al. 2009. Reconstruction of monocotelydoneous proto-chromosomes reveals faster evolution in plants than in animals. PNAS 106:14908–13 [Google Scholar]
  79. Salse J, Piégu B, Cooke R, Delseny M. 79.  2004. New in silico insight into the synteny between rice (Oryza sativa L.) and maize (Zea mays L.) highlights reshuffling and identifies new duplications in the rice genome. Plant J. 38:396–409 [Google Scholar]
  80. Scannell DR, Byrne KP, Gordon JL, Wong S, Wolfe KH. 80.  2006. Multiple rounds of speciation associated with reciprocal gene loss in polyploid yeasts. Nature 440:341–45 [Google Scholar]
  81. Schnable JC, Freeling M. 81.  2011. Genes identified by visible mutant phenotypes show increased bias toward one of two subgenomes of maize. PLOS ONE 6:e17855 [Google Scholar]
  82. Schnable JC, Freeling M, Lyons E. 82.  2012. Genome-wide analysis of syntenic gene deletion in the grasses. Genome Biol. Evol. 4:265–77 [Google Scholar]
  83. Schnable JC, Pedersen BS, Subramaniam S, Freeling M. 83.  2011. Dose-sensitivity, conserved noncoding sequences and duplicate gene retention through multiple tetraploidies in the grasses. Front. Plant Genet. Plant Genomics 2:2 [Google Scholar]
  84. Schnable JC, Springer NM, Freeling M. 84.  2011. Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss. PNAS 108:4069–74 [Google Scholar]
  85. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F. 85.  et al. 2009. The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–15 [Google Scholar]
  86. Sémon M, Wolfe KH. 86.  2007. Reciprocal gene loss between tetraodon and zebrafish after whole genome duplication in their ancestor. Trends Genet. 23:108–12 [Google Scholar]
  87. Song R, Llaca V, Linton E, Messing J. 87.  2001. Sequence, regulation, and evolution of the maize 22-kD α zein gene family. Genome Res. 11:1817–25 [Google Scholar]
  88. Springer NM, Ying K, Fu Y, Ji T, Yeh C-T. 88.  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 [Google Scholar]
  89. Swanson-Wagner RA, Eichten SR, Kumari S, Tiffin P, Stein JC. 89.  et al. 2010. Pervasive gene content variation and copy number variation in maize and its undomesticated progenitor. Genome Res 20:1689–99 [Google Scholar]
  90. Swidan F, Rocha EPC, Shmoish M, Pinter RY. 90.  2006. An integrative method for accurate comparative genome mapping. PLOS Comput. Biol. 2:e75 [Google Scholar]
  91. Swigoňová Z, Lai J, Ma J, Ramakrishna W, Llaca V. 91.  et al. 2004. Close split of sorghum and maize genome progenitors. Genome Res 14:1916–23 [Google Scholar]
  92. Talbert LE, Doebley JF, Larson S, Chandler VL. 92.  1990. Tripsacum andersonii is a natural hybrid involving Zea and Tripsacum: molecular evidence. Am. J. Bot 77:722–26 [Google Scholar]
  93. Tang H, Lyons E, Pedersen B, Schnable JC, Paterson AH, Freeling M. 93.  2011. Screening synteny blocks in pairwise genome comparisons through integer programming. BMC Bioinform 12:102 [Google Scholar]
  94. Tenaillon MI, Hufford MB, Gaut BS, Ross-Ibarra J. 94.  2011. Genome size and transposable element content as determined by high-throughput sequencing in maize and Zea luxurians. Genome Biol. Evol 3:219–29 [Google Scholar]
  95. Tiffin P, Moeller DA. 95.  2006. Molecular evolution of plant immune system genes. Trends Genet 22:662–70 [Google Scholar]
  96. van Heerwaarden J, Doebley J, Briggs WH, Glaubitz JC, Goodman MM. 96.  et al. 2011. Genetic signals of origin, spread, and introgression in a large sample of maize landraces. PNAS 108:1088–92 [Google Scholar]
  97. Wang H, Bennetzen JL. 97.  2012. Centromere retention and loss during the descent of maize from a tetraploid ancestor. PNAS 109:21004–9 [Google Scholar]
  98. Wang W, Zheng H, Fan C, Li J, Shi J. 98.  et al. 2006. High rate of chimeric gene origination by retroposition in plant genomes. Plant Cell 18:1791–802 [Google Scholar]
  99. Wang X, Gowik U, Tang H, Bowers JE, Westhoff P, Paterson AH. 99.  2009. Comparative genomic analysis of C4 photosynthetic pathway evolution in grasses. Genome Biol. 10:R68 [Google Scholar]
  100. Wei F, Coe E, Nelson W, Bharti AK, Engler F. 100.  et al. 2007. Physical and genetic structure of the maize genome reflects its complex evolutionary history. PLOS Genet. 3:e123 [Google Scholar]
  101. Wei F, Zhang J, Zhou S, He R, Schaeffer M. 101.  et al. 2009. The physical and genetic framework of the maize B73 genome. PLOS Genet. 5:e1000715 [Google Scholar]
  102. Whitkus R, Doebley J, Lee M. 102.  1992. Comparative genome mapping of sorghum and maize. Genetics 132:1119–30 [Google Scholar]
  103. Woodhouse MR, Pedersen B, Freeling M. 103.  2010. Transposed genes in Arabidopsis are often associated with flanking repeats. PLOS Genet. 6:e1000949 [Google Scholar]
  104. Woodhouse MR, Schnable JC, Pedersen BS, Lyons E, Lisch D. 104.  et al. 2010. Following tetraploidy in maize, a short deletion mechanism removed genes preferentially from one of the two homeologs. PLOS Biol. 8:e1000409 [Google Scholar]
  105. Xu X, Liu X, Ge S, Jensen JD, Hu F. 105.  et al. 2012. Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes. Nat. Biotechnol. 30:105–11 [Google Scholar]
  106. Zhang P, Chopra S, Peterson T. 106.  2000. A segmental gene duplication generated differentially expressed myb-homologous genes in maize. Plant Cell 12:2311–22 [Google Scholar]
  107. Zhou L, Huang B, Meng X, Wang G, Wang F. 107.  et al. 2010. The amplification and evolution of orthologous 22-kDa α-prolamin tandemly arrayed genes in coix, sorghum and maize genomes. Plant Mol. Biol. 74:631–43 [Google Scholar]
  108. Zhou S, Wei F, Nguyen J, Bechner M, Potamousis K. 108.  et al. 2009. A single molecule scaffold for the maize genome. PLOS Genet. 5:e1000711 [Google Scholar]
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