A high-quality carrot genome assembly provides new insights into carotenoid accumulation and asterid genome evolution

Nature Genetics

Volumn 48, Issue 6, 2016, Pages 657-666

  Iorizzo, Massimo ^a,l   Ellison, Shelby ^a   Senalik, Douglas ^a,b   Zeng, Peng ^c   Satapoomin, Pimchanok ^a   Huang, Jiaying ^c   Bowman, Megan ^d   Iovene, Marina ^e   Sanseverino, Walter ^f   Cavagnaro, Pablo ^g,h   Yildiz, Mehtap ⁱ   Macko Podgórni, Alicja ^j   Moranska, Emilia ^j   Grzebelus, Ewa ^j   Grzebelus, Dariusz ^j   Ashrafi, Hamid ^k,l   Zheng, Zhijun ^c   Cheng, Shifeng ^c   Spooner, David ^a,b   Van Deynze, Allen ^k   Simon, Philipp ^a,b   more..

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b U S DAIRY FORAGE RESEARCH CENTER   (United States)

^c BGI SHENZHEN   (China)

^d MICHIGAN STATE UNIVERSITY   (United States)

^e Institute of Biosciences and Bioresources   (Italy)

^f Sequentia Biotech   (Spain)

^g Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^h Instituto Nacional de Tecnolog'a Agropecuaria (INTA)   (Argentina)

ⁱ YUZUNCU YIL UNIVERSITY   (Turkey)

^j UNIVERSITY OF AGRICULTURE IN KRAKOW   (Poland)

^k UNIVERSITY OF CALIFORNIA   (United States)

^l NORTH CAROLINA STATE UNIVERSITY   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CAROTENOID; PIGMENT; GENETIC MARKER;

ARTICLE; ASTERID; CARROT; CHROMOSOME STRUCTURE; CLADISTICS; DISEASE RESISTANCE; FLAVOR; FLOWERING; GENE SEQUENCE; GENETIC VARIABILITY; MOLECULAR EVOLUTION; NONHUMAN; PEST RESISTANCE; PLANT GENOME; POLYPLOIDY; PRIORITY JOURNAL; REGULATOR GENE; CLASSIFICATION; EVOLUTION; GENETIC LINKAGE; GENETIC MARKER; GENETICS; METABOLISM; PHYLOGENY; PLANT ROOT;

BIOLOGICAL EVOLUTION; CAROTENOIDS; DAUCUS CAROTA; GENES, REGULATOR; GENETIC LINKAGE; GENETIC MARKERS; GENOME, PLANT; PHYLOGENY; PLANT ROOTS;

EID: 84966671734     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.3565     Document Type: Article

References (130)

1. Simon, P.W., et al. in Carrot. Handbook of Plant Breeding, Vegetables II (eds. Prohens, J., & Nuez, F) 327-357 (Springer, 2008
2. Zagorodskikh, P. New data on the origin and taxonomy of the cultivated carrot. C.R. (Doklady) Acad. Sci. USSR 25, 522-525 (1939
3. Iorizzo, M., et al. Genetic structure and domestication of carrot (Daucus carota subsp. sativus) (Apiaceae). Am. J. Bot. 100, 930-938 (2013
4. Simon, P.W. Domestication, historical development, and modern breeding of carrot. Plant Breed. Rev. 19, 157-190 (2000
5. Arscott, S.A., & Tanumihardjo, S.A. Carrots of many colors provide basic nutrition and bioavailable phytochemicals acting as a functional food. Compr. Rev. Food Sci. Food Saf. 9, 223-239 (2010
6. Simon, P.W. Plant breeding for human nutritional quality. Plant Breed. Rev. 31, 325-392 (2009
7. Rubatzky, V.E., Quiros, C.F., & Simon, P.W. Carrots and Related Vegetable Umbelliferae (CABI, 1999
8. Bremer, B. in Asterids.The Timetree of Life (eds. Hedges, S.B., & Kumar, S) 177-178 (Oxford University Press, 2009
9. Peng, Y., et al. De novo genome assembly of the economically important weed horseweed using integrated data from multiple sequencing platforms. Plant Physiol. 166, 1241-1254 (2014
10. Scaglione, D., et al. The genome sequence of the outbreeding globe artichoke constructed De novo incorporating a phase-aware low-pass sequencing strategy of F1 progeny. Sci. Rep. 6, 19427 (2016
11. Arumuganathan, K., & Earle, E.D. Nuclear DNA content of some important plant species. Plant Mol. Biol. Rep. 9, 208-218 (1991
12. Potato Genome Sequencing Consortium. Genome sequence and analysis of the tuber crop potato. Nature 475, 189-195 (2011
13. Kim, S., et al. Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species. Nat. Genet. 46, 270-278 (2014
14. Iorizzo, M., et al. De novo assembly and characterization of the carrot transcriptome reveals novel genes, new markers, and genetic diversity. BMC Genomics 12, 389 (2011
15. Parra, G., Bradnam, K., & Korf, I. CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 23, 1061-1067 (2007
16. Chain, P.S., et al. Genome project standards in a new era of sequencing. Science 326, 236-237 (2009
17. International Rice Genome Sequencing Project. The map-based sequence of the rice genome. Nature 436, 793-800 (2005
18. Grzebelus, D., Yau, Y.-Y., & Simon, P.W. Master: A novel family of PIF/Harbinger-like transposable elements identified in carrot (Daucus carota L). Mol. Genet. Genomics 275, 450-459 (2006
19. Macko-Podgorni, A., Nowicka, A., Grzebelus, E., Simon, P.W., & Grzebelus, D. DcSto: carrot Stowaway-like elements are abundant, diverse, and polymorphic. Genetica 141, 255-267 (2013
20. Santiago, N., Herráiz, C., Goñi, J.R., Messeguer, X., & Casacuberta, J.M. Genome-wide analysis of the Emigrant family of MITEs of Arabidopsis thaliana. Mol. Biol. Evol. 19, 2285-2293 (2002
21. Miga, K.H., et al. Centromere reference models for human chromosomes X and Y satellite arrays. Genome Res. 24, 697-707 (2014
22. Novák, P., Neumann, P., Pech, J., Steinhaisl, J., & Macas, J. RepeatExplorer: a Galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads. Bioinformatics 29, 792-793 (2013
23. Iovene, M., et al. Comparative FISH mapping of Daucus species (Apiaceae family). Chromosome Res. 19, 493-506 (2011
24. Spalik, K., et al. Amphitropic amphiantarctic disjunctions in Apiaceae subfamily Apioideae. J. Biogeogr. 37, 1977-1994 (2010
25. Nei, M., & Li, W.-H. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc. Natl. Acad. Sci. USA 76, 5269-5273 (1979
26. Rong, J., et al. New insights into domestication of carrot from root transcriptome analyses. BMC Genomics 15, 895 (2014
27. Arbizu, C., Reitsma, K.R., Simon, P.W., & Spooner, D.M. Morphometrics of Daucus (Apiaceae): a counterpart to a phylogenomic study. Am. J. Bot. 101, 2005-2016 (2014
28. Welch, J.E., & Grimball, E.L. Jr. Male sterility in the carrot. Science 106, 594 (1947
29. Weir, B.S., & Cockerham, C.C. Estimating F-statistics for the analysis of population structure. Evolution 38, 1358 (1984
30. Vanneste, K., Baele, G., Maere, S., & Van De Peer, Y. Analysis of 41 plant genomes supports a wave of successful genome duplications in association with the Cretaceous-Paleogene boundary. Genome Res. 24, 1334-1347 (2014
31. Truco, M.J., et al. An ultra-high-density, transcript-based, genetic map of lettuce. G3 3, 617-631 (2013
32. Argout, X., et al. The genome of Theobroma cacao. Nat. Genet. 43, 101-108 (2011
33. Salse, J., et al. Reconstruction of monocotelydoneous proto-chromosomes reveals faster evolution in plants than in animals. Proc. Natl. Acad. Sci. USA 106, 14908-14913 (2009
34. Lang, D., et al. Genome-wide phylogenetic comparative analysis of plant transcriptional regulation: a timeline of loss, gain, expansion, and correlation with complexity. Genome Biol. Evol. 2, 488-503 (2010
35. Noh, B., et al. Divergent roles of a pair of homologous jumonji/zinc-finger-class transcription factor proteins in the regulation of Arabidopsis flowering time. Plant Cell 16, 2601-2613 (2004
36. Nakamichi, N., et al. Arabidopsis clock-associated pseudo-response regulators PRR9, PRR7 and PRR5 coordinately and positively regulate flowering time through the canonical CONSTANS-dependent photoperiodic pathway. Plant Cell Physiol. 48, 822-832 (2007
37. Levy, Y.Y., Mesnage, S., Mylne, J.S., Gendall, A.R., & Dean, C. Multiple roles of Arabidopsis VRN1 in vernalization and flowering time control. Science 297, 243-246 (2002
38. Sanseverino, W., et al. PRGdb 2.0: towards a community-based database model for the analysis of R-genes in plants. Nucleic Acids Res. 41, D1167-D1171 (2013
39. Simon, P.W., Matthews, W.C., & Roberts, P.A. Evidence for simply inherited dominant resistance to Meloidogyne javanica in carrot. Theor. Appl. Genet. 100, 735-742 (2000
40. Buishand, J.G., & Gabelman, W.H. Investigations on the inheritance of color and carotenoid content in phloem and xylem of carrot roots (Daucus carota L). Euphytica 28, 611-632 (1979
41. Just, B.J., Santos, C.A., Yandell, B.S., & Simon, P.W. Major QTL for carrot color are positionally associated with carotenoid biosynthetic genes and interact epistatically in a domesticated × wild carrot cross. Theor. Appl. Genet. 119, 1155-1169 (2009
42. Just, B.J., et al. Carotenoid biosynthesis structural genes in carrot (Daucus carota): isolation, sequence-characterization, single nucleotide polymorphism (SNP) markers and genome mapping. Theor. Appl. Genet. 114, 693-704 (2007
43. Clotault, J., et al. Expression of carotenoid biosynthesis genes during carrot root development. J. Exp. Bot. 59, 3563-3573 (2008
44. Fuentes, P., et al. Light-dependent changes in plastid differentiation influence carotenoid gene expression and accumulation in carrot roots. Plant Mol. Biol. 79, 47-59 (2012
45. Bowman, M.J., Willis, D.K., & Simon, P.W. Transcript abundance of phytoene synthase 1 and phytoene synthase 2 is associated with natural variation of storage root carotenoid pigmentation in carrot. J. Am. Soc. Hortic. Sci. 139, 63-68 (2014
46. Wang, H., Ou, C.-G., Zhuang, F.-Y., & Ma, Z.-G. The dual role of phytoene synthase genes in carotenogenesis in carrot roots and leaves. Mol. Breed. 34, 2065-2079 (2014
47. Palaisa, K., Morgante, M., Tingey, S., & Rafalski, A. Long-range patterns of diversity and linkage disequilibrium surrounding the maize Y1 gene are indicative of an asymmetric selective sweep. Proc. Natl. Acad. Sci. USA 101, 9885-9890 (2004
48. Wang, R.-L., Stec, A., Hey, J., Lukens, L., & Doebley, J. The limits of selection during maize domestication. Nature 398, 236-239 (1999
49. Ruiz-Sola, M.Á., & Rodríguez-Concepción, M. Carotenoid biosynthesis in Arabidopsis: a colorful pathway. Arabidopsis Book 10, e0158 (2012
50. Cordoba, E., et al. Functional characterization of the three genes encoding 1-deoxy-d-xylulose 5-phosphate synthase in maize. J. Exp. Bot. 62, 2023-2038 (2011
51. Kim, B.R., Kim, S.U., & Chang, Y.J. Differential expression of three 1-deoxy-d-xylulose-5-phosphate synthase genes in rice. Biotechnol. Lett. 27, 997-1001 (2005
52. Saladié, M., Wright, L.P., Garcia-Mas, J., Rodriguez-Concepcion, M., & Phillips, M.A. The 2-C-methylerythritol 4-phosphate pathway in melon is regulated by specialized isoforms for the first and last steps. J. Exp. Bot. 65, 5077-5092 (2014
53. Walter, M.H., Hans, J., & Strack, D. Two distantly related genes encoding 1-deoxy-d-xylulose 5-phosphate synthases: differential regulation in shoots and apocarotenoid-accumulating mycorrhizal roots. Plant J. 31, 243-254 (2002
54. Estévez, J.M., Cantero, A., Reindl, A., Reichler, S., & León, P. 1-Deoxy-d-xylulose-5-phosphate synthase, a limiting enzyme for plastidic isoprenoid biosynthesis in plants. J. Biol. Chem. 276, 22901-22909 (2001
55. Lois, L.M., Rodríguez-Concepción, M., Gallego, F., Campos, N., & Boronat, A. Carotenoid biosynthesis during tomato fruit development: regulatory role of 1-deoxy-d-xylulose 5-phosphate synthase. Plant J. 22, 503-513 (2000
56. Ichikawa, T., et al. The FOX hunting system: an alternative gain-of-function gene hunting technique. Plant J. 48, 974-985 (2006
57. Huang, X., Ouyang, X., & Deng, X.W. Beyond repression of photomorphogenesis: role switching of COP/DET/FUS in light signaling. Curr. Opin. Plant Biol. 21, 96-103 (2014
58. Wei, N., & Deng, X.-W. The role of the COP/DET/FUS genes in light control of Arabidopsis seedling development. Plant Physiol. 112, 871-878 (1996
59. Lau, O.S., & Deng, X.W. The photomorphogenic repressors COP1 and DET1: 20 years later. Trends Plant Sci. 17, 584-593 (2012
60. Rodriguez-Concepcion, M., & Stange, C. Biosynthesis of carotenoids in carrot: an underground story comes to light. Arch. Biochem. Biophys. 539, 110-116 (2013
61. Bowman, M.J. Gene Expression and Genetic Analysis of Carotenoid Pigment Accumulation in Carrot (Daucus carota L). PhD thesis, Univ. Wisconsin-Madison, (2012
62. Sherwin, J.C., Reacher, M.H., Dean, W.H., & Ngondi, J. Epidemiology of vitamin A deficiency and xerophthalmia in at-risk populations. Trans. R. Soc. Trop. Med. Hyg. 106, 205-214 (2012
63. Steward, F.C. Growth and organized development of cultured cells. III. Interpretation of the growth from free cell to carrot plant. Am. J. Bot. 45, 709-713 (1958
64. Vogel, G. How does a single somatic cell become a whole plant? Science 309, 86 (2005
65. Huang, S., et al. Draft genome of the kiwifruit Actinidia chinensis. Nat. Commun. 4, 2640 (2013
66. Jiao, Y., et al. A genome triplication associated with early diversification of the core eudicots. Genome Biol. 13, R3 (2012
67. Luo, R., et al. SOAPdenovo2: an empirically improved memory-efficient short-read De novo assembler. Gigascience 1, 18 (2012
68. Van Ooijen, J.W. JoinMap 4: Software for the Calculation of Genetic Linkage Maps in Experimental Populations (Kyazma, 2006
69. Voorrips, R.E. MapChart: software for the graphical presentation of linkage maps and QTLs. J. Hered. 93, 77-78 (2002
70. Schmieder, R., & Edwards, R. Fast identification and removal of sequence contamination from genomic and metagenomic datasets. PLoS One 6, e17288 (2011
71. Elshire, R.J., et al. A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One 6, e19379 (2011
72. Bradbury, P.J., et al. TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23, 2633-2635 (2007
73. Glaubitz, J.C., et al. TASSEL-GBS: a high capacity genotyping by sequencing analysis pipeline. PLoS One 9, e90346 (2014
74. Cavagnaro, P.F., et al. A gene-derived SNP-based high resolution linkage map of carrot including the location of QTL conditioning root and leaf anthocyanin pigmentation. BMC Genomics 15, 1118 (2014
75. Dong, F., et al. Development and applications of a set of chromosome-specific cytogenetic DNA markers in potato. Theor. Appl. Genet. 101, 1001-1007 (2000
76. Iovene, M., Grzebelus, E., Carputo, D., Jiang, J., & Simon, P.W. Major cytogenetic landmarks and karyotype analysis inDaucus carota and other Apiaceae. Am. J. Bot. 95, 793-804 (2008
77. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., & Lipman, D.J. Basic local alignment search tool. J. Mol. Biol. 215, 403-410 (1990
78. Kim, D., et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36 (2013
79. Xu, Z., & Wang, H. LTR-FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res. 35, W265-W268 (2007
80. Gambin, T., et al. TIRfinder: a web tool for mining class II transposons carrying terminal inverted repeats. Evol. Bioinform. Online 9, 17-27 (2013
81. Wicker, T., et al. A unified classification system for eukaryotic transposable elements. Nat. Rev. Genet. 8, 973-982 (2007
82. Darzentas, N. Circoletto: visualizing sequence similarity with Circos. Bioinformatics 26, 2620-2621 (2010
83. Krzywinski, M., et al. Circos: an information aesthetic for comparative genomics. Genome Res. 19, 1639-1645 (2009
84. Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol. Biol. Evol. 30, 2725-2729 (2013
85. Novák, P., Neumann, P., & Macas, J. Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data. BMC Bioinformatics 11, 378 (2010
86. Benson, G. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 27, 573-580 (1999
87. Stanke, M., et al. AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res. 34, W435-W439 (2006
88. Burge, C., & Karlin, S. Prediction of complete gene structures in human genomic DNA. J. Mol. Biol. 268, 78-94 (1997
89. Majoros, W.H., Pertea, M., & Salzberg, S.L. TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders. Bioinformatics 20, 2878-2879 (2004
90. Birney, E., Clamp, M., & Durbin, R. GeneWise and Genomewise. Genome Res. 14, 988-995 (2004
91. Kent, W.J. BLAT-the BLAST-like alignment tool. Genome Res. 12, 656-664 (2002
92. Campbell, M.A., Haas, B.J., Hamilton, J.P., Mount, S.M., & Buell, C.R. Comprehensive analysis of alternative splicing in rice and comparative analyses with Arabidopsis. BMC Genomics 7, 327 (2006
93. Trapnell, C., et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562-578 (2012
94. Elsik, C.G., et al. Creating a honey bee consensus gene set. Genome Biol. 8, R13 (2007
95. Zdobnov, E.M., & Apweiler, R. InterProScan-an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17, 847-848 (2001
96. Nawrocki, E.P., & Eddy, S.R. Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 29, 2933-2935 (2013
97. Lowe, T.M., & Eddy, S.R. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25, 955-964 (1997
98. Murray, M.G., & Thompson, W.F. Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res. 8, 4321-4325 (1980
99. Li, H., & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760 (2009
100. Li, H., et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079 (2009
101. McKenna, A., et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297-1303 (2010
102. Pritchard, J.K., Stephens, M., & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945-959 (2000
103. Evanno, G., Regnaut, S., & Goudet, J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14, 2611-2620 (2005
104. Felsenstein, J. PHYLIP-Phylogeny Inference Package (Version 3.2). Cladistics 5, 164-166 (1989
105. Li, L., Stoeckert, C.J. Jr., & Roos, D.S. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13, 2178-2189 (2003
106. Edgar, R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797 (2004
107. Guindon, S., et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307-321 (2010
108. Yang, Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586-1591 (2007
109. Zhang, G., et al. Genome sequence of foxtail millet (Setaria italica) provides insights into grass evolution and biofuel potential. Nat. Biotechnol. 30, 549-554 (2012
110. Paterson, A.H., Bowers, J.E., & Chapman, B.A. Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc. Natl. Acad. Sci. USA 101, 9903-9908 (2004
111. Paterson, A.H., et al. The Sorghum bicolor genome and the diversification of grasses. Nature 457, 551-556 (2009
112. Tomato Genome Consortium. The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485, 635-641 (2012
113. Jaillon, O., et al. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449, 463-467 (2007
114. Wang, Y., et al. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 40, e49 (2012
115. Hasegawa, M., Kishino, H., & Yano, T. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J. Mol. Evol. 22, 160-174 (1985
116. Prüfer, K., et al. FUNC: a package for detecting significant associations between gene sets and ontological annotations. BMC Bioinformatics 8, 41 (2007
117. Dai, X., Sinharoy, S., Udvardi, M., & Zhao, P.-X. PlantTFcat: an online plant transcription factor and transcriptional regulator categorization and analysis tool. BMC Bioinformatics 14, 321 (2013
118. Larkin, M.A., et al. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948 (2007
119. Jones, P., et al. InterProScan 5: genome-scale protein function classification. Bioinformatics 30, 1236-1240 (2014
120. Simon, P.W., & Wolff, X.Y. Carotenes in typical and dark orange carrots. J. Agric. Food Chem. 35, 1017-1022 (1987
121. Simon, P.W., Wolff, X.Y., Peterson, C.E., & Kammerlohr, D.S. High carotene mass carrot population. HortScience 24, 174-175 (1989
122. Bland, J.M., & Altman, D.G. Multiple significance tests: the Bonferroni method. Br. Med. J. 310, 170 (1995
123. Broman, K.W., & Sen, S. A Guide to QTL Mapping with R/qtl (Springer, 2009
124. Leigh, J.W., & Bryant, D. POPART: full-feature software for haplotype network construction. Methods Ecol. Evol. 6, 1110-1116 (2015
125. Barrett, J.C., Fry, B., Maller, J., & Daly, M.J. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21, 263-265 (2005
126. Danecek, P., et al. The variant call format and VCFtools. Bioinformatics 27, 2156-2158 (2011
127. Langfelder, P., & Horvath, S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9, 559 (2008
128. Lamesch, P., et al. The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res. 40, D1202-D1210 (2012
129. Du, Z., Zhou, X., Ling, Y., Zhang, Z., & Su, Z. agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res. 38, W64-W70 (2010
130. Mi, H., Muruganujan, A., & Thomas, P.D. PANTHER in 2013: modeling the evolution of gene function, and other gene attributes, in the context of phylogenetic trees. Nucleic Acids Res. 41, D377-D386 (2013