Genes involved in floral meristem in tomato exhibit drastically reduced genetic diversity and signature of selection

BMC Plant Biology

Volumn 14, Issue 1, 2014, Pages

  Bauchet, Guillaume ^a,b   Munos, Stéphane ^a,c   Sauvage, Christopher ^a   Bonnet, Julien ^b   Grivet, Laurent ^b   Causse, Mathilde ^a  

^a Researches Center of Avignon   (France)

^b Syngenta Seeds SAS   (France)

^c CNRS   (France)

Author keywords

Meristem; S. lycopersicum; Signature of selection; Tomato

Indexed keywords

ARABIDOPSIS THALIANA; LYCOPERSICON; LYCOPERSICON ESCULENTUM;

CLASSIFICATION; FLOWER; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; MERISTEM; METABOLISM; PLANT GENOME; SINGLE NUCLEOTIDE POLYMORPHISM; TOMATO;

FLOWERS; GENETIC VARIATION; GENOME, PLANT; LYCOPERSICON ESCULENTUM; MERISTEM; POLYMORPHISM, SINGLE NUCLEOTIDE; SELECTION, GENETIC;

EID: 84936748175     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/s12870-014-0279-2     Document Type: Article

References (153)

1. Doebley JF, Gaut BS,Smith BD: The molecular genetics of crop domestication. Cell 2006, 127(7):1309-1321.
2. Burger JC, Chapman MA, Burke JM: Molecular insights into the evolution of crop plants. Am J Bot 2008, 95(2):113-122.
3. Tanksley SD: The genetic, developmental, and molecular bases of fruit size and shape variation in tomato. Plant Cell 2004, 16(Suppl 1):S181-S189.
4. Girin T, Sorefan K, Østergaard L: Meristematic sculpting in fruit development. J Exp Bot 2009, 60(5):1493-1502.
5. Park SJ, Eshed Y, Lippman ZB: Meristem maturation and inflorescence architecture;lessons from the Solanaceae. Curr Opin Plant Biol 2014, 17:70-77.
6. Becker A, Alix K, Damerval C: The evolution of flower development: current understanding and future challenges. Ann Bot 2011, 107(9):1427-1431.
7. Kaufmann K, Pajoro A, Angenent GC: Regulation of transcription in plants: mechanisms controlling developmental switches. Nat Rev Genet 2010, 11(12):830-842.
8. Causier B, Schwarz-Sommer Z, Davies B: Floral organ identity: 20 years of ABCs. Semin Cell Dev Biol 2010, 21(1):73-79.
9. van der Knaap E, Chakrabarti M, Chu YH, Clevenger JP, Illa Berenguer E, Huang Z, Keyhaninejad N, Mu Q, Sun L, Wang Y, Wu S: What lies beyond the eye: the molecular mechanisms regulating tomato fruit weight and shape. Front Plant Sci 2014, 5(227):1-13.
10. Heidstra R, Sabatini S: Plant and animal stem cells: similar yet different. Nat Rev Mol Cell Biol 2014, 15(5):301-312.
11. Perales M, Reddy GV: Stem cell maintenance in shoot apical meristems. Curr Opin Plant Biol 2012, 15(1):10-16.
12. Koornneef M, Meinke D: The development of Arabidopsis as a model plant. Plant J 2010, 61(6):909-921.
13. Irish VF: The flowering of Arabidopsis flower development. Plant J 2010, 61(6):1014-1028.
14. Gillaspy G, Ben-David H, Gruissem W: Fruits: a developmental perspective. Plant Cell Online 1993, 5(10):1439-1451.
15. Xiao H, Radovich C, Welty N, Hsu J, Li D, Meulia T, van der Knaap E: Integration of tomato reproductive developmental landmarks and expression profiles, and the effect of SUN on fruit shape. BMC Plant Biol 2009, 9(1):49.
16. Bertin N, Causse M, Brunel B, Tricon D, Genard M: Identification of growth processes involved in QTLs for tomato fruit size and composition. J Exp Bot 2008, 60(1):237-248.
17. The Tomato Genome Consortium: The tomato genome sequence provides insights into fleshy fruit evolution. Nature 2012, 485(7400):635-641.
18. Ranjan A, Ichihashi Y, Sinha N: The tomato genome: implications for plant breeding, genomics and evolution. Genome Biol 2012, 13(8):167.
19. Rodriguez GR, Munos S, Anderson C, Sim SC, Michel A, Causse M, Gardener BBM, Francis D, van der Knaap E: Distribution of SUN, OVATE, LC, and FAS in the Tomato Germplasm and the Relationship to Fruit Shape Diversity. Plant Physiol 2011, 156(1):275-285.
20. Monforte AJ, Diaz AI, Caño-Delgado A, van der Knaap E: The genetic basis of fruit morphology in horticultural crops: lessons from tomato and melon. J Exp Bot 2014, doi:10.1093/jxb/eru017.
21. Frary A, Nesbitt TC, Grandillo S, Knaap E, Cong B, Liu J, Meller J, Elber R, Alpert KB, Tanksley SD: fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 2000, 289(5476):85-88.
22. Liu J, Van Eck J, Cong B, Tanksley SD: A new class of regulatory genes underlying the cause of pear-shaped tomato fruit. Proc Natl Acad Sci U S A 2002, 99(20):13302-13306.
23. Lippman Z, Tanksley SD: Dissecting the genetic pathway to extreme fruit size in tomato using a cross between the small-fruited wild species Lycopersicon pimpinellifolium and L. esculentum var. Giant Heirloom. Genetics 2001, 158(1):413-422.
24. Cong B, Barrero LS, Tanksley SD: Regulatory change in YABBY-like transcription factor led to evolution of extreme fruit size during tomato domestication. Nat Genet 2008, 40(6):800-804.
25. Muños S, Ranc N, Botton E, Bérard A, Rolland S, Duffé P, Carretero Y, Le Paslier M-C, Delalande C, Bouzayen M, Brunel D, Causse M: Increase in tomato locule number is controlled by two single-nucleotide polymorphisms located near WUSCHEL. Plant Physiol 2011, 156(4):2244-2254.
26. Barrero LS, Cong B, Wu F, Tanksley SD: Developmental characterization of the fasciated locus and mapping of Arabidopsis candidate genes involved in the control of floral meristem size and carpel number in tomato. Genome 2006, 49(8):991-1006.
27. Zamir D: Plant breeders go back to nature. Nat Genet 2008, 40(3):269-270.
28. Wilson LM, Whitt SR, Ibáñez AM, Rocheford TR, Goodman MM, Buckler ES: Dissection of maize kernel composition and starch production by candidate gene association. Plant Cell 2004, 16(10):2719-2733.
29. Sterken R, Kiekens R, Coppens E, Vercauteren I, Zabeau M, Inzé D, Flowers J, Vuylsteke M: A Population genomics study of the arabidopsis core cell cycle genes shows the signature of natural selection. Plant Cell Online 2009, 21(10):2987-2998.
30. Korte A, Farlow A: The advantages and limitations of trait analysis with GWAS: a review. Plant Methods 2013, 9(1):29.
31. Mandel JR, Nambeesan S, Bowers JE, Marek LF, Ebert D, Rieseberg LH, Knapp SJ, Burke JM: Association mapping and the genomic consequences of selection in sunflower. PLoS Genet 2013, 9(3):e1003378.
32. Kimura M: A model of a genetic system which leads to closer linkage by natural selection. Evolution 1956, 10(278):87.
33. Ranc N, Muños S, Xu J, Le Paslier M-C, Chauveau A, Bounon R, Rolland S, Bouchet J-P, Brunel D, Causse M: Genome-wide association mapping in tomato (Solanum lycopersicum) is possible using genome admixture of Solanum lycopersicum var. Cerasiforme. G3: Genes|Genomes|Genetics 2012, 2(8):853-864.
34. Xu J, Ranc N, Muños S, Rolland S, Bouchet J-P, Desplat N, Paslier M-C, Liang Y, Brunel D, Causse M: Phenotypic diversity and association mapping for fruit quality traits in cultivated tomato and related species. Theor Appl Genet 2012, 126(3):567-581.
35. Shirasawa K, Fukuoka H, Matsunaga H, Kobayashi Y, Kobayashi I, Hirakawa H, Isobe S, Tabata S: Genome-Wide Association studies using single nucleotide polymorphism markers developed by re-sequencing of the genomes of cultivated tomato. DNA Research 2013, 20(6):593-603.
36. Sim S-C, Van Deynze A, Stoffel K, Douches DS, Zarka D, Ganal MW, Chetelat RT, Hutton SF, Scott JW, Gardner RG, Panthee DR, Mutschler M, Myers JR, Francis DM: High-Density SNP genotyping of tomato reveals patterns of genetic variation due to breeding. PLoS One 2012, 7(9):e45520.
37. Ranc N, Muños S, Santoni S, Causse M: A clarified position for Solanum lycopersicum var. cerasiforme in the evolutionary history of tomatoes (Solanaceae). BMC Plant Biol 2008, 8(1):130.
38. Long JA, Ohno C, Smith ZR, Meyerowitz EM: TOPLESS regulates apical embryonic fate in Arabidopsis. Science 2006, 312(5779):1520-1523.
39. Zuo J, Niu Q-W, Nishizawa N, Wu Y, Kost B, Chua N-H: KORRIGAN, an Arabidopsis endo-1,4-β-glucanase, localizes to the cell plate by polarized targeting and is essential for cytokinesis. Plant Cell Online 2000, 12(7):1137-1152.
40. Krupková E, Schmülling T: Developmental consequences of the tumorous shoot development1 mutation, a novel allele of the cellulosesynthesizing KORRIGAN1 gene. Plant Mol Biol 2009, 71(6):641-655.
41. Brummell DA, Catala C, Lashbrook CC, Bennett AB: A membrane-anchored E-type endo-1,4-β-glucanase is localized on Golgi and plasma membranes of higher plants. Proc Natl Acad Sci 1997, 94(9):4794-4799.
42. Prigge MJ, Otsuga D, Alonso JM, Ecker JR, Drews GN, Clark SE: Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell Online 2005, 17(1):61-76.
43. Green KA: CORONA, a Member of the Class III Homeodomain Leucine Zipper gene family in Arabidopsis, regulates stem cell specification and organogenesis. Plant Cell Online 2005, 17(3):691-704.
44. Barton MK: Twenty years on: the inner workings of the shoot apical meristem, a developmental dynamo. Dev Biol 2010, 341(1):95-113.
45. Fletcher JC: The ULTRAPETALA gene controls shoot and floral meristem size in Arabidopsis. Development 2001, 128(8):1323-1333.
46. Bai M, Yang G-S, Chen W-T, Mao Z-C, Kang H-X, Chen G-H, Yang Y-H, Xie B-Y: Genome-wide identification of Dicer-like, Argonaute and RNAdependent RNA polymerase gene families and their expression analyses in response to viral infection and abiotic stresses in Solanum lycopersicum. Gene 2012, 501(1):52-62.
47. Kidner CA, Martienssen RA: The role of ARGONAUTE1 (AGO1) in meristem formation and identity. Dev Biol 2005, 280(2):504-517.
48. Bohmert K, Camus I, Bellini C, Bouchez D, Caboche M, Benning C: AGO1 defines a novel locus of Arabidopsis controlling leaf development. EMBO J 1998, 17(1):170-180.
49. Prunet N, Morel P, Thierry AM, Eshed Y, Bowman JL, Negrutiu I, Trehin C: REBELOTE, SQUINT, and ULTRAPETALA1 function redundantly in the temporal regulation of floral meristem termination in Arabidopsis thaliana. Plant Cell Online 2008, 20(4):901-919.
50. Wilkinson MD, Haughn GW: UNUSUAL FLORAL ORGANS controls meristem identity and organ primordia fate in Arabidopsis. Plant Cell Online 1995, 7(9):1485-1499.
51. Hepworth S, Klenz J, Haughn G: UFO in the Arabidopsis inflorescence apex is required for floral-meristem identity and bract suppression. Planta 2006, 223(4):769-778.
52. Allen K, Sussex I: Falsiflora and anantha control early stages of floral meristem development in tomato (Lycopersicon esculentum Mill.). Planta 1996, 200(2):254-264.
53. Lippman ZB, Weigel D, Cohen O, Alvarez JP, Abu-Abied M, Pekker I, Paran I, Eshed Y, Zamir D: The making of a compound inflorescence in tomato and related Nightshades. PLoS Biol 2008, 6(11):e288.
54. Pnueli L, Carmel-Goren L, Hareven D, Gutfinger T, Alvarez J, Ganal M, Zamir D, Lifschitz E: The SELF-PRUNING gene of tomato regulates vegetative to reproductive switching of sympodial meristems and is the ortholog of CEN and TFL1. Development 1998, 125(11):1979-1989.
55. Yeager A: Studies on the inheritance and development of fruit size and shape in the tomato. J Agric Res 1937, 55:141-152.
56. Shannon S, Meeks-Wagner DR: A Mutation in the Arabidopsis TFL1 gene affects inflorescence meristem development. Plant Cell Online 1991, 3(9):877-892.
57. Goldshmidt A, Alvarez JP, Bowman JL, Eshed Y: Signals derived from YABBY gene activities in organ primordia regulate growth and partitioning of arabidopsis shoot apical meristems. Plant Cell Online 2008, 20(5):1217-1230.
58. Huang Z, Houten J, Gonzalez G, Xiao H, Knaap E: Genome-wide identification, phylogeny and expression analysis of SUN, OFP and YABBY gene family in tomato. Mol Genet Genomics 2013, 288(3-4):111-129.
59. Bartholmes C, Hidalgo O, Gleissberg S: Evolution of the YABBY gene family with emphasis on the basal eudicot Eschscholzia californica (Papaveraceae). Plant Biol 2012, 14(1):11-23.
60. Schumacher K, Schmitt T, Rossberg M, Schmitz G, Theres K: The Lateral suppressor (Ls) gene of tomato encodes a new member of the VHIID protein family. Proc Natl Acad Sci 1999, 96(1):290-295.
61. Greb T: Molecular analysis of the LATERAL SUPPRESSOR gene in Arabidopsis reveals a conserved control mechanism for axillary meristem formation. Genes Dev 2003, 17(9):1175-1187.
62. Pysh LD, Wysocka-Diller JW, Camilleri C, Bouchez D, Benfey PN: The GRAS gene family in Arabidopsis: sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. Plant J 1999, 18(1):111-119.
63. McConnell JR, Emery J, Eshed Y, Bao N, Bowman J, Barton MK: Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 2001, 411(6838):709-713.
64. Emery JF, Floyd SK, Alvarez J, Eshed Y, Hawker NP, Izhaki A, Baum SF, Bowman JL: Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr Biol 2003, 13(20):1768-1774.
65. Klucher KM, Chow H, Reiser L, Fischer RL: The AINTEGUMENTA gene of Arabidopsis required for ovule and female gametophyte development is related to the floral homeotic gene APETALA2. Plant Cell Online 1996, 8(2):137-153.
66. Mizukami Y, Fischer RL: Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis. Proc Natl Acad Sci 2000, 97(2):942-947.
67. Nole-Wilson S, Krizek BA: AINTEGUMENTA Contributes to organ polarity and regulates growth of lateral organs in combination with YABBY Genes. Plant Physiol 2006, 141(3):977-987.
68. Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldmann KA, Meyerowitz EM: The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 1990, 346(6279):35-39.
69. Pnueli L, Hareven D, Rounsley SD, Yanofsky MF, Lifschitz E: Isolation of the tomato AGAMOUS gene TAG1 and analysis of its homeotic role in transgenic plants. Plant Cell Online 1994, 6(2):163-173.
70. Hong RL, Hamaguchi L, Busch MA, Weigel D: Regulatory elements of the floral homeotic gene AGAMOUS identified by phylogenetic footprinting and shadowing. Plant Cell Online 2003, 15(6):1296-1309.
71. Pan IL, McQuinn R, Giovannoni JJ, Irish VF: Functional diversification of AGAMOUS lineage genes in regulating tomato flower and fruit development. J Exp Bot 2010, 61(6):1795-1806.
72. Clark SE, Williams RW, Meyerowitz EM: The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 1997, 89(4):575-585.
73. Clark SE, Running MP, Meyerowitz EM: CLAVATA1, a regulator of meristem and flower development in Arabidopsis. Development 1993, 119(2):397-418.
74. Williams RW, Wilson JM, Meyerowitz EM: A possible role for kinaseassociated protein phosphatase in the Arabidopsis CLAVATA1 signaling pathway. Proc Natl Acad Sci 1997, 94(19):10467-10472.
75. Stahl Y, Simon R: Receptor Kinases in Plant Meristem Development. In Receptor-Like Kinases in Plants, Volume 13. Edited by Tax F, Kemmerling B. Berlin Heidelberg: Springer; 2012:23-39.
76. Ishiguro S, Watanabe Y, Ito N, Nonaka H, Takeda N, Sakai T, Kanaya H, Okada K: SHEPHERD is the Arabidopsis GRP94 responsible for the formation of functional CLAVATA proteins. EMBO J 2002, 21(5):898-908.
77. Scofield S, Dewitte W, Murray JAH: The KNOX gene SHOOT MERISTEMLESS is required for the development of reproductive meristematic tissues in Arabidopsis. Plant J 2007, 50(5):767-781.
78. Chen JJ, Janssen BJ, Williams A, Sinha N: A gene fusion at a homeobox locus: alterations in leaf shape and implications for morphological evolution. Plant Cell Online 1997, 9(8):1289-1304.
79. Uchida N, Townsley B, Chung K-H, Sinha N: Regulation of SHOOT MERISTEMLESS genes via an upstream-conserved noncoding sequence coordinates leaf development. Proc Natl Acad Sci 2007, 104(40):15953-15958.
80. Kwon CS: WUSCHEL is a primary target for transcriptional regulation by SPLAYED in dynamic control of stem cell fate in Arabidopsis. Genes Dev 2005, 19(8):992-1003.
81. Laux T, Mayer KF, Berger J, Jurgens G: The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 1996, 122(1):87-96.
82. Mayer KFX, Schoof H, Haecker A, Lenhard M, Jürgens G, Laux T: Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 1998, 95:805-815.
83. Reinhardt D, Frenz M, Mandel T, Kuhlemeier C: Microsurgical and laser ablation analysis of interactions between the zones and layers of the tomato shoot apical meristem. Development 2003, 130(17):4073-4083.
84. Wang X, Wang X-G, Ren J-P, Ma Y, Yin J: Characterization of Tomato Transcription Factor WUSCHEL and Functional Study in Arabidopsis. J Integrative Agri 2012, 11(8):1257-1265.
85. Moussian B, Schoof H, Haecker A, Jurgens G, Laux T: Role of the ZWILLE gene in the regulation of central shoot meristem cell fate during Arabidopsis embryogenesis. EMBO J 1998, 17(6):1799-809.
86. Kayes JM, Clark SE: CLAVATA2, a regulator of meristem and organ development in Arabidopsis. Development 1998, 125(19):3843-3851.
87. Wang G, Zhang Z, Angenent GC, Fiers M: New aspects of CLAVATA2, a versatile gene in the regulation of Arabidopsis development. J Plant Physiol 2011, 168(4):403-407.
88. Hord CLH: The BAM1/BAM2 Receptor-Like Kinases are important regulators of arabidopsis early anther development. Plant Cell Online 2006, 18(7):1667-1680.
89. DeYoung BJ, Clark SE: BAM receptors regulate stem cell specification and organ development through complex interactions with CLAVATA signaling. Genetics 2008, 180(2):895-904.
90. Lecomte L, Duffe P, Buret M, Servin B, Hospital F, Causse M: Marker-assisted introgression of five QTLs controlling fruit quality traits into three tomato lines revealed interactions between QTLs and genetic backgrounds. TAG Theor Appl Genet 2004, 109(3):658-668.
91. Libault M, Stacey G: Evolution of FW2.2-like (FWL) and PLAC8 genes in eukaryotes. Plant Signal Behav 2010, 5(10):1226-1228.
92. Song W-Y, Hörtensteiner S, Tomioka R, Lee Y, Martinoia E: Common functions or only phylogenetically related? The large family of PLAC8 motif-containing/PCR genes. Mol Cells 2011, 31(1):1-7.
93. Alpert KB, Grandillo S, Tanksley SD: fw2.2:a major QTL controlling fruit weight is common to both red- and green-fruited tomato species. TAG Theor Appl Genet 1995, 91(6):994-1000.
94. Liu J, Cong B, Tanksley SD: Generation and Analysis of an Artificial Gene Dosage Series in Tomato to Study the Mechanisms by Which the Cloned Quantitative Trait Locus fw2.2 Controls Fruit Size. Plant physiology 2003, 132(1):292-299.
95. Cong B, Tanksley SD: FW2.2 and cell cycle control in developing tomato fruit: a possible example of gene co-option in the evolution of a novel organ. Plant Mol Biol 2006, 62(6):867-880.
96. Li E, Wang S, Liu Y, Chen JG, Douglas CJ: OVATE FAMILY PROTEIN4 (OFP4) interaction with KNAT7 regulates secondary cell wall formation in Arabidopsis thaliana. The Plant Journal 2011, 67(2):328-341.
97. Hackbusch J, Richter K, Müller J, Salamini F, Uhrig JF: A central role of Arabidopsis thaliana ovate family proteins in networking and subcellular localization of 3-aa loop extension homeodomain proteins. Proc Natl Acad Sci U S A 2005, 102(13):4908-4912.
98. Wang S, Chang Y, Guo J, Zeng Q, Ellis BE, Chen J-G: Arabidopsis Ovate family proteins, a novel transcriptional repressor family, control multiple aspects of plant growth and development. PLoS One 2011, 6(8):e23896.
99. Xiao H, Jiang N, Schaffner E, Stockinger EJ, van der Knaap E: A retrotransposon-mediated gene duplication underlies morphological variation of tomato fruit. Science 2008, 319(5869):1527-1530.
100. Wu S, Xiao H, Cabrera A, Meulia T, van der Knaap E: SUN regulates vegetative and reproductive organ shape by changing cell division patterns. Plant Physiol 2011, 157(3):1175-1186.
101. Kaya H, Shibahara K-I, Taoka K-I, Iwabuchi M, Stillman B, Araki T: FASCIATA genes for chromatin assembly factor-1 in Arabidopsis maintain the cellular organization of apical meristems. Cell 2001, 104(1):131-142.
102. Dennis MD, Browning KS: Differential phosphorylation of plant translation initiation factors by Arabidopsis thaliana CK2 holoenzymes. J Biol Chem 2009, 284(31):20602-20614.
103. Burko Y, Geva Y, Refael-Cohen A, Shleizer-Burko S, Shani E, Berger Y, Halon E, Chuck G, Moshelion M, Ori N: From organelle to organ: ZRIZI MATE-type transporter is an organelle transporter that enhances organ initiation. Plant Cell Physiol 2011, 52(3):518-527.
104. Fonné-Pfister R, Chemla P, Ward E, Girardet M, Kreuz KE, Honzatko RB, Fromm HJ, Schär HP, Grütter MG, Cowan-Jacob SW: The mode of action and the structure of a herbicide in complex with its target: binding of activated hydantocidin to the feedback regulation site of adenylosuccinate synthetase. Proc Natl Acad Sci 1996, 93(18):9431-9436.
105. Lim E, Bowles D: A class of plant glycosyltransferases involved in cellular homeostasis. EMBO J 2004, 23(15):2915-2922.
106. Linder P: Dead-box proteins: a family affair-active and passive players in RNP-remodeling. Nucleic Acids Res 2006, 34(15):4168-4180.
107. Panjabi P, Jagannath A, Bisht N, Padmaja KL, Sharma S, Gupta V, Pradhan A, Pental D: Comparative mapping of Brassica juncea and Arabidopsis thaliana using Intron Polymorphism (IP) markers: homoeologous relationships, diversification and evolution of the A, B and C Brassica genomes. BMC Genomics 2008, 9(1):113.
108. Wicker T, Schlagenhauf E, Graner A, Close TJ, Keller B, Stein N: 454 sequencing put to the test using the complex genome of barley. BMC Genomics 2006, 7:275.
109. Sim S-C, Durstewitz G, Plieske J, Wieseke R, Ganal MW, Van Deynze A, Hamilton JP, Buell CR, Causse M, Wijeratne S, Francis DM: Development of a large SNP genotyping array and generation of high-density genetic maps in tomato. PLoS One 2012, 7(7):e40563.
110. Lucatti A, van Heusden A, de Vos R, Visser R, Vosman B: Differences in insect resistance between tomato species endemic to the Galapagos Islands. BMC Evol Biol 2013, 13(1):175.
111. Van Deynze A, Stoffel K, Buell CR, Kozik A, Liu J, van der Knaap E, Francis D: Diversity in conserved genes in tomato. BMC Genomics 2007, 8(1):465.
112. Miller JC, Tanksley SD: RFLP analysis of phylogenetic relationships and genetic variation in the genus Lycopersicon. TAG Theor Appl Genet 1990, 80(4):437-448.
113. Blanca J, Cañizares J, Cordero L, Pascual L, Diez MJ, Nuez F: Variation revealed by snp genotyping and morphology provides insight into the origin of the tomato. PLoS One 2012, 7(10):e48198.
114. Koenig D, Jiménez-Gómez JM, Kimura S, Fulop D, Chitwood DH, Headland LR, Kumar R, Covington MF, Devisetty UK, Tat AV, Tohge T, Bolger A, Schneeberger K, Ossowski S, Lanz C, Xiong G, Taylor-Teeples M, Brady SM, Pauly M, Weigel D, Usadel B, Fernie AR, Peng J, Sinha NR, Maloof JN: Comparative transcriptomics reveals patterns of selection in domesticated and wild tomato. Proc Natl Acad Sci U S A 2013, 110(28):E2655-E2662.
115. Labate JA, Sheffer SM, Balch T, Robertson LD: Diversity and population structure in a geographic sample of tomato accessions. Crop Sci 2011, 51(3):1068-1079.
116. Gossmann TI, Song B-H, Windsor AJ, Mitchell-Olds T, Dixon CJ, Kapralov MV, Filatov DA, Eyre-Walker A: Genome wide analyses reveal little evidence for adaptive evolution in many plant species.Mol Biol Evol 2010, 27(8):1822-1832.
117. Städler T, Roselius K, Stephan W: Genealogical footprints of speciation processes in wild tomatoes: demography and evidence for historical gene flow. Evolution 2005, 59(6):1268-1279.
118. Charlesworth D, Charlesworth B, Morgan MT: The pattern of neutral molecular variation under the background selection model. Genetics 1995, 141(4):1619-1632.
119. Smith JM, Haigh J: The hitch-hiking effect of a favourable gene. Genet Res 1974, 23(01):23-35.
120. Chakrabarti M, Zhang N, Sauvage C, Muños S, Blanca J, Cañizares J, Diez MJ, Schneider R, Mazourek M, McClead J, Causse M, van der Knaap E: A cytochrome P450 regulates a domestication trait in cultivated tomato. Proc Natl Acad Sci 2013, 110(42):17125-17130.
121. Albrechtsen A, Nielsen FC, Nielsen R: Ascertainment biases in SNP chips affect measures of population divergence. Mol Biol Evol 2010, 27(11):2534-2547.
122. Manrique-Carpintero NC, Tokuhisa JG, Ginzberg I, Holliday JA, Veilleux RE: Sequence diversity in coding regions of candidate genes in the glycoalkaloid biosynthetic pathway of wild potato species. G3: Genes| Genomes|Genetics 2013, 3(9):1467-1479.
123. Sim SC, Robbins MD, Deynze AV, Michel AP, Francis DM: Population structure and genetic differentiation associated with breeding history and selection in tomato (Solanum lycopersicum L.). Heredity 2010, 106(6):927-935.
124. Pavlidis P, Metzler D, Stephan W: Selective sweeps in multilocus models of quantitative traits. Genetics 2012, 192(1):225-239.
125. Chevin L-M, Hospital F: Selective sweep at a quantitative trait locus in the presence of background genetic variation. Genetics 2008, 180(3):1645-1660.
126. Durbak AR, Tax FE: CLAVATA signaling pathway receptors of Arabidopsis regulate cell proliferation in fruit organ formation as well as in meristems. Genetics 2011, 189(1):177-194.
127. Zhong S, Fei Z, Chen Y-R, Zheng Y, Huang M, Vrebalov J, McQuinn R, Gapper N, Liu B, Xiang J, Shao Y, Giovannoni JJ: Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat Biotechnol 2013, 31:154-159.
128. Manning K, Tör M, Poole M, Hong Y, Thompson AJ, King GJ, Giovannoni JJ, Seymour GB: A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat Genet 2006, 38(8):948-952.
129. Brewer MT, Lang L, Fujimura K, Dujmovic N, Gray S, van der Knaap E: Development of a controlled vocabulary and software application to analyze fruit shape variation in tomato and other plant species. Plant Physiol 2006, 141(1):15-25.
130. Roe BA: Shotgun library construction for DNA sequencing. Methods Mol Biol 2004, 255:171-187.
131. Wiley G, Macmil S, Qu C, Wang P, Xing Y, White D, Li J, White JD, Domingo A, Roe BA: Methods for Generating Shotgun and Mixed Shotgun/paired-end Libraries for the 454 dna Sequencer. In Current Protocols in Human Genetics. John Wiley & Sons, Inc; 2001.
132. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen YJ, Chen Z, Dewell Scott B, Du L, Fierro JM, Gomes XV, Godwin BC, He W, Helgesen S, Ho CH, Irzyk GP, Jando SC, Alenquer MLI, Jarvie TP, Jirage KB, Kim JB, Knight JR, Lanza JR, Leamon JH, Lefkowitz SM, Lei M, Li J, Lohman KL, Lu H, Makhijani VB, McDade KE, McKenna MP, Myers EW, Nickerson E, Nobile JR, Plant R, Puc BP, Ronan MT, Roth GT, Sarkis GJ, Simons JF, Simpson JW, Srinivasan M, Tartaro KR, Tomasz A, Vogt KA, Volkmer GA, Wang SH, Wang Y, Weiner MP, Yu P, Begley RF, Rothberg JM: Genome sequencing in microfabricated high-density picolitre reactors. Nature 2005, 437(7057):376-380.
133. Mariette J, Noirot C, Klopp C: Assessment of replicate bias in 454 pyrosequencing and a multi-purpose read-filtering tool. BMC Res Notes 2011, 4(1):149.
134. Burland TG: DNASTAR's Lasergene sequence analysis software. Molecular Methods 1999, 132:71-91.
135. Kent WJ: BLAT-The BLAST-Like alignment tool. Genome Res 2002, 12(4):656-664.
136. Cingolani P, Platts A, Wang L, Coon M, Nguyen T, Wang L, Land S, Ruden D, Lu X: A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 2012, 6(2):1-13.
137. Hamilton JP, Sim S-C, Stoffel K, Van Deynze A, Buell CR, Francis DM: Single Nucleotide polymorphism discovery in cultivated tomato via sequencing by synthesis. Plant Gen 2012, 5(1):17-29.
138. Sauvage C, Segura V, Bauchet G, Stevens R, Thi Do P, Nikoloski Z, Fernie AR, Causse M: Genome Wide Association in tomato reveals 44 candidate loci for fruit metabolic traits. Plant Physiology 2014, pp.114.241521. doi:http://dx.doi.org/10.1104/pp.114.241521.
139. Tajima F: Statistical method for testing the neutral mutation hypothesis by dna polymorphism. Genetics 1989, 123(3):585-595.
140. Librado P, Rozas J: DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25:1451-1452.
141. Hutter S, Vilella A, Rozas J: Genome-wide DNA polymorphism analyses using VariScan. BMC Bioinform 2006, 7(1):409.
142. Yang Z, Bielawski JP: Statistical methods for detecting molecular adaptation. Trends Ecol Evol 2000, 15(12):496-503.
143. Goldman N, Yang Z: A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol 1994, 11(5):725-736.
144. Yang Z: PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 2007, 24(8):1586-1591.
145. Weir BS, Cockerham CC: Estimating F-statistics for the analysis of population structure. Evolution 1984, 38(6):1358-1370.
146. Falush D, Stephens M, Pritchard JK: Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 2007, 7(4):574-578.
147. Evanno G, Regnaut S, Goudet J: Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 2005, 14(8):2611-2620.
148. Porras-Hurtado L, Ruiz Y, Santos C, Phillips C, Carrecedo Á, Lareu M: An overview of STRUCTURE: applications, parameter settings and supporting software. Frontiers in Genetics 2013, 4(98):1-13.
149. Hardy OJ, Vekemans X: SPAGeDI: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2002, 2:618-620.
150. Loiselle BA, Sork VL, Nason J, Graham C: Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Am J Bot 1995, 82:1420-1425.
151. Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES: TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 2007, 23(19):2633-2635.
152. Benjamini Y, Hochberg Y: Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc 1995, 57(1):289-300.
153. Steinbach D, Alaux M, Amselem J, Choisne N, Durand S, Flores R, Keliet A-O, Kimmel E, Lapalu N, Luyten I, Michotey C, Mohellibi N, Pommier C, Reboux S, Valdenaire D, Verdelet D, Quesneville H: GnpIS: an information system to integrate genetic and genomic data from plants and fungi. Database 2013, doi:10.1093/database/bat058.