RNA sequencing of laser-capture microdissected compartments of the maize kernel identifies regulatory modules associated with endosperm cell differentiation

Plant Cell

Volumn 27, Issue 3, 2015, Pages 513-531

  Zhan, Junpeng ^a   Thakare, Dhiraj ^a   Ma, Chuang ^a,c   Lloyd, Alan ^b   Nixon, Neesha M ^b   Arakaki, Angela M ^b   Burnett, William J ^b   Logan, Kyle O ^b   Wang, Dongfang ^a,d   Wang, Xiangfeng ^a,e   Drews, Gary N ^b   Yadegari, Ramin ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF UTAH   (United States)

^c NORTHWEST A F UNIVERSITY   (China)

^d SPELMAN COLLEGE   (United States)

^e CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

MAGNOLIOPHYTA; ZEA MAYS;

MESSENGER RNA;

CELL COMPARTMENTALIZATION; CELL DIFFERENTIATION; CYTOLOGY; EMBRYOLOGY; ENDOSPERM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; GENOME IMPRINTING; LASER CAPTURE MICRODISSECTION; MAIZE; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE MOTIF; NUCLEOTIDE SEQUENCE; PLANT GENE; POLLINATION; PRINCIPAL COMPONENT ANALYSIS; PROCEDURES; SEQUENCE ANALYSIS; TIME FACTOR; TWO HYBRID SYSTEM;

BASE SEQUENCE; CELL COMPARTMENTATION; CELL DIFFERENTIATION; ENDOSPERM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENE REGULATORY NETWORKS; GENES, PLANT; GENOMIC IMPRINTING; LASER CAPTURE MICRODISSECTION; MOLECULAR SEQUENCE DATA; NUCLEOTIDE MOTIFS; POLLINATION; PRINCIPAL COMPONENT ANALYSIS; RNA, MESSENGER; SEQUENCE ANALYSIS, RNA; TIME FACTORS; TWO-HYBRID SYSTEM TECHNIQUES; ZEA MAYS;

EID: 84927714543     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.114.135657     Document Type: Article

References (100)

1. Andrews, S. (2010). FastQC: A quality control tool for high-throughput sequence data. (http://www.bioinformatics.babraham.ac.uk/projects/fastqc).
2. Bailey, T.L. and Elkan, C. (1994). Fitting a Mixture Model by Expectation Maximization to Discover Motifs in Bipolymers. (San Diego, CA: University of California).
3. Balandín, M., Royo, J., Gómez, E., Muniz, L.M., Molina, A., and Hueros, G. (2005). A protective role for the embryo surrounding region of the maize endosperm, as evidenced by the characterisation of ZmESR-6, a defensin gene specifically expressed in this region. Plant Mol. Biol. 58: 269-282.
4. Baranowskij, N., Frohberg, C., Prat, S., and Willmitzer, L. (1994). A novel DNA binding protein with homology to Myb oncoproteins containing only one repeat can function as a transcriptional activator. EMBO J. 13: 5383-5392.
5. Barrero, C., Muñiz, L.M., Gómez, E., Hueros, G., and Royo, J. (2006). Molecular dissection of the interaction between the transcriptional activator ZmMRP-1 and the promoter of BETL-1. Plant Mol. Biol. 62: 655-668.
6. Becraft, P.W. (2001). Cell fate specification in the cereal endosperm. Semin. Cell Dev. Biol. 12: 387-394.
7. Becraft, P.W., and Gutierrez-Marcos, J. (2012). Endosperm development: dynamic processes and cellular innovations underlying sibling altruism. Dev. Biol. 1: 579-593.
8. Berger, F., Grini, P.E., and Schnittger, A. (2006). Endosperm: an integrator of seed growth and development. Curr. Opin. Plant Biol. 9: 664-670.
9. Blauth, S.L., Kim, K.-N., Klucinec, J., Shannon, J.C., Thompson, D., and Guiltinan, M. (2002). Identification of Mutator insertional mutants of starchbranching enzyme 1 (sbe1) in Zea mays L. Plant Mol. Biol. 48: 287-297.
10. Bolger, A.M., Lohse, M., and Usadel, B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30: 2114-2120.
11. Bonello, J.F., Opsahl-Ferstad, H.G., Perez, P., Dumas, C., and Rogowsky, P.M. (2000). Esr genes show different levels of expression in the same region of maize endosperm. Gene 246: 219-227.
12. Brink, R.A., and Cooper, D.C. (1947). The endosperm in seed development. Bot. Rev. 13: 479-541.
13. Brugière, N., Humbert, S., Rizzo, N., Bohn, J., and Habben, J.E. (2008). A member of the maize isopentenyl transferase gene family, Zea mays isopentenyl transferase 2 (ZmIPT2), encodes a cytokinin biosynthetic enzyme expressed during kernel development. Cytokinin biosynthesis in maize. Plant Mol. Biol. 67: 215-229.
14. Charlton, W.L., Keen, C.L., Merriman, C., Lynch, P., Greenland, A.J., and Dickinson, H.G. (1995). Endosperm development in Zea mays; implication of gametic imprinting and paternal excess in regulation of transfer layer development. Development 121: 3089-3097.
15. Chen, J., Zeng, B., Zhang, M., Xie, S., Wang, G., Hauck, A., and Lai, J. (2014). Dynamic transcriptome landscape of maize embryo and endosperm development. Plant Physiol. 166: 252-264.
16. Cheng, W.-H., Taliercio, E.W., and Chourey, P.S. (1996). The Miniature1 seed locus of maize encodes a cell wall invertase required for normal development of endosperm and maternal cells in the pedicel. Plant Cell 8: 971-983.
17. Chourey, P.S., and Nelson, O.E. (1979). Interallelic complementation at the sh locus in maize at the enzyme level. Genetics 91: 317-325.
18. Commuri, P.D., and Keeling, P.L. (2001). Chain-length specificities of maize starch synthase I enzyme: studies of glucan affinity and catalytic properties. Plant J. 25: 475-486.
19. Conesa, A., and Götz, S. (2008). Blast2GO: A comprehensive suite for functional analysis in plant genomics. Int. J. Plant Genomics 2008: 619832.
20. Conesa, A., Götz, S., García-Gómez, J.M., Terol, J., Talón, M., and Robles, M. (2005). Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674-3676.
21. Cooper, D.C. (1951). Caryopsis development following matings between diploid and tetraploid strains of Zea mays. Am. J. Bot. 38: 702-708.
22. Cord Neto, G., Yunes, J.A., da Silva, M.J., Vettore, A.L., Arruda, P., and Leite, A. (1995). The involvement of Opaque 2 on beta-prolamin gene regulation in maize and Coix suggests a more general role for this transcriptional activator. Plant Mol. Biol. 27: 1015-1029.
23. Costa, L.M., Yuan, J., Rouster, J., Paul, W., Dickinson, H., and Gutierrez-Marcos, J.F. (2012). Maternal control of nutrient allocation in plant seeds by genomic imprinting. Curr. Biol. 22: 160-165.
24. Doan, D.N., Linnestad, C., and Olsen, O.-A. (1996). Isolation of molecular markers from the barley endosperm coenocyte and the surrounding nucellus cell layers. Plant Mol. Biol. 31: 877-886.
25. Drews, G.N. (1998). In situ hybridization. Methods Mol. Biol. 82: 353-371.
26. Etcheverry, T. (1990). Induced expression using yeast copper metallothionein promoter. Methods Enzymol. 185: 319-329.
27. FAO (2012). FAO Statistical Yearbook 2012. (http://www.fao.org/docrep/015/i2490e/i2490e00.htm).
28. Faure, J.-E. (2001). Double fertilization in flowering plants: discovery, study methods and mechanisms. C. R. Acad. Sci. 3 324: 551-558.
29. Gallusci, P., Varotto, S., Matsuoko, M., Maddaloni, M., and Thompson, R.D. (1996). Regulation of cytosolic pyruvate, orthophosphate dikinase expression in developing maize endosperm. Plant Mol. Biol. 31: 45-55.
30. Giroux, M.J., Boyer, C., Feix, G., and Hannah, L.C. (1994). Coordinated transcriptional regulation of storage product genes in the maize endosperm. Plant Physiol. 106: 713-722.
31. Gómez, E., Royo, J., Guo, Y., Thompson, R., and Hueros, G. (2002). Establishment of cereal endosperm expression domains: identification and properties of a maize transfer cell-specific transcription factor, ZmMRP-1. Plant Cell 14: 599-610.
32. Gómez, E., Royo, J., Muñiz, L.M., Sellam, O., Paul, W., Gerentes, D., Barrero, C., López, M., Perez, P., and Hueros, G. (2009). The maize transcription factor myb-related protein-1 is a key regulator of the differentiation of transfer cells. Plant Cell 21: 2022-2035.
33. Götz, S., García-Gómez, J.M., Terol, J., Williams, T.D., Nagaraj, S.H., Nueda, M.J., Robles, M., Talón, M., Dopazo, J., and Conesa, A. (2008). High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res. 36: 3420-3435.
34. Gray, J., et al. (2009). A recommendation for naming transcription factor proteins in the grasses. Plant Physiol. 149: 4-6.
35. Gruis, D.F., Guo, H., Selinger, D., Tian, Q., and Olsen, O.-A. (2006). Surface position, not signaling from surrounding maternal tissues, specifies aleurone epidermal cell fate in maize. Plant Physiol. 141: 898-909.
36. Gupta, S., Stamatoyannopoulos, J.A., Bailey, T.L., and Noble, W.S. (2007). Quantifying similarity between motifs. Genome Biol. 8: R24.
37. Gutiérrez-Marcos, J.F., Costa, L.M., Biderre-Petit, C., Khbaya, B., O’Sullivan, D.M., Wormald, M., Perez, P., and Dickinson, H.G. (2004). Maternally expressed gene1 Is a novel maize endosperm transfer cell-specific gene with a maternal parent-of-origin pattern of expression. Plant Cell 16: 1288-1301.
38. Haig, D., and Westoby, M. (1989). Parent-specific gene expression and the triploid endosperm. Am. Nat. 134: 147-155.
39. Hamamura, Y., Nagahara, S., and Higashiyama, T. (2012). Double fertilization on the move. Curr. Opin. Plant Biol. 15: 70-77.
40. 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.
41. Heidler, S.A., and Radding, J.A. (1995). The AUR1 gene in Saccharomyces cerevisiae encodes dominant resistance to the antifungal agent aureobasidin A (LY295337). Antimicrob. Agents Chemother. 39: 2765-2769.
42. Holding, D.R., Otegui, M.S., Li, B., Meeley, R.B., Dam, T., Hunter, B.G., Jung, R., and Larkins, B.A. (2007). The maize floury1 gene encodes a novel endoplasmic reticulum protein involved in zein protein body formation. Plant Cell 19: 2569-2582.
43. Hollander, M., and Wolfe, D.A., Chicken, E. (2013). Nonparametric Statistical Methods. (New York: John Wiley & Sons).
44. Hu, Z., Mellor, J., DeLisi, C. (2004). Analyzing networks with VisANT. In Current Protocols in Bioinformatics, Andreas D. Baxevanis, ed (New York: John Wiley & Sons), pp. 881-8824.
45. Hubbard, T., et al. (2002). The Ensembl genome database project. Nucleic Acids Res. 30: 38-41.
46. Hueros, G., Royo, J., Maitz, M., Salamini, F., and Thompson, R.D. (1999). Evidence for factors regulating transfer cell-specific expression in maize endosperm. Plant Mol. Biol. 41: 403-414.
47. Hueros, G., Varotto, S., Salamini, F., and Thompson, R.D. (1995). Molecular characterization of BET1, a gene expressed in the endosperm transfer cells of maize. Plant Cell 7: 747-757.
48. James, M.G., Robertson, D.S., and Myers, A.M. (1995). Characterization of the maize gene sugary1, a determinant of starch composition in kernels. Plant Cell 7: 417-429.
49. Jin, J., Zhang, H., Kong, L., Gao, G., and Luo, J. (2014). PlantTFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors. Nucleic Acids Res. 42: D1182-D1187.
50. Kerk, N.M., Ceserani, T., Tausta, S.L., Sussex, I.M., and Nelson, T.M. (2003). Laser capture microdissection of cells from plant tissues. Plant Physiol. 132: 27-35.
51. Lafon-Placette, C., and Köhler, C. (2014). Embryo and endosperm, partners in seed development. Curr. Opin. Plant Biol. 17: 64-69.
52. Langfelder, P., and Horvath, S. (2008). WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9: 559.
53. Leroux, B.M., Goodyke, A.J., Schumacher, K.I., Abbott, C.P., Clore, A.M., Yadegari, R., Larkins, B.A., and Dannenhoffer, J.M. (2014). Maize early endosperm growth and development: from fertilization through cell type differentiation. Am. J. Bot. 101: 1259-1274.
54. Li, G., et al. (2014). Temporal patterns of gene expression in developing maize endosperm identified through transcriptome sequencing. Proc. Natl. Acad. Sci. USA 111: 7582-7587.
55. Lopes, M.A., and Larkins, B.A. (1993). Endosperm origin, development, and function. Plant Cell 5: 1383-1399.
56. Ma, C., and Wang, X. (2012). Application of the Gini correlation coefficient to infer regulatory relationships in transcriptome analysis. Plant Physiol. 160: 192-203.
57. Ma, C., Xin, M., Feldmann, K.A., and Wang, X. (2014). Machine learning-based differential network analysis: a study of stress-responsive transcriptomes in Arabidopsis. Plant Cell 26: 520-537.
58. Maddaloni, M., Donini, G., Balconi, C., Rizzi, E., Gallusci, P., Forlani, F., Lohmer, S., Thompson, R., Salamini, F., and Motto, M. (1996). The transcriptional activator Opaque-2 controls the expression of a cytosolic form of pyruvate orthophosphate dikinase-1 in maize endosperms. Mol. Gen. Genet. 250: 647-654.
59. Magnard, J.-L., Le Deunff, E., Domenech, J., Rogowsky, P.M., Testillano, P.S., Rougier, M., Risueño, M.C., Vergne, P., and Dumas, C. (2000). Genes normally expressed in the endosperm are expressed at early stages of microspore embryogenesis in maize. Plant Mol. Biol. 44: 559-574.
60. Magnard, J.L., Lehouque, G., Massonneau, A., Frangne, N., Heckel, T., Gutierrez-Marcos, J.F., Perez, P., Dumas, C., and Rogowsky, P.M. (2003). ZmEBE genes show a novel, continuous expression pattern in the central cell before fertilization and in specific domains of the resulting endosperm after fertilization. Plant Mol. Biol. 53: 821-836.
61. Marshall, E., Costa, L.M., and Gutierrez-Marcos, J. (2011). Cysteine-rich peptides (CRPs) mediate diverse aspects of cell-cell communication in plant reproduction and development. J. Exp. Bot. 62: 1677-1686.
62. Martínez-García, J.F., Moyano, E., Alcocer, M.J., and Martin, C. (1998). Two bZIP proteins from Antirrhinum flowers preferentially bind a hybrid C-box/G-box motif and help to define a new subfamily of bZIP transcription factors. Plant J. 13: 489-505.
63. Marzábal, P., Gas, E., Fontanet, P., Vicente-Carbajosa, J., Torrent, M., and Ludevid, M.D. (2008). The maize Dof protein PBF activates transcription of gamma-zein during maize seed development. Plant Mol. Biol. 67: 441-454.
64. Massonneau, A., Condamine, P., Wisniewski, J.-P., Zivy, M., and Rogowsky, P.M. (2005). Maize cystatins respond to developmental cues, cold stress and drought. Biochim. Biophys. Acta 1729: 186-199.
65. Mathelier, A., et al. (2014) JASPAR 2014: an extensively expanded and updated open-access database of transcription factor binding profiles. Nucleic Acids Res. 42: D142-D147.
66. Moore, T., and Haig, D. (1991). Genomic imprinting in mammalian development: a parental tug-of-war. Trends Genet. 7: 45-49.
67. Mortazavi, A., Williams, B.A., McCue, K., Schaeffer, L., and Wold, B. (2008). Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5: 621-628.
68. Muñiz, L.M., Royo, J., Gómez, E., Baudot, G., Paul, W., and Hueros, G. (2010). Atypical response regulators expressed in the maize endosperm transfer cells link canonical two component systems and seed biology. BMC Plant Biol. 10: 84.
69. Muñiz, L.M., Royo, J., Gómez, E., Barrero, C., Bergareche, D., and Hueros, G. (2006). The maize transfer cell-specific type-A response regulator ZmTCRR-1 appears to be involved in intercellular signalling. Plant J. 48: 17-27.
70. Niu, X., Helentjaris, T., and Bate, N.J. (2002). Maize ABI4 binds coupling element1 in abscisic acid and sugar response genes. Plant Cell 14: 2565-2575.
71. Olsen, O.A. (2001). Endosperm development: cellularization and cell fate specification. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52: 233-267.
72. Olsen, O.-A. (2004). Nuclear endosperm development in cereals and Arabidopsis thaliana. Plant Cell 16: S214-S227.
73. Olsen, O.-A., and Becraft, P.W. (2013). Endosperm development. In Seed Genomics, P.W. Becraft, ed (New York: John Wiley & Sons), pp. 43-62.
74. Opsahl-Ferstad, H.G., Le Deunff, E., Dumas, C., and Rogowsky, P.M. (1997). ZmEsr, a novel endosperm-specific gene expressed in a restricted region around the maize embryo. Plant J. 12: 235-246.
75. Quinlan, A.R., and Hall, I.M. (2010). BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26: 841-842.
76. Riechmann, J.L., Wang, M., and Meyerowitz, E.M. (1996). DNAbinding properties of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA and AGAMOUS. Nucleic Acids Res. 24: 3134-3141.
77. Royo, J., Gómez, E., Sellam, O., Gerentes, D., Paul, W., and Hueros, G. (2014). Two maize END-1 orthologs, BETL9 and BETL9like, are transcribed in a non-overlapping spatial pattern on the outer surface of the developing endosperm. Front. Plant Sci. 5: 180.
78. Sabelli, P.A., and Larkins, B.A. (2009). The development of endosperm in grasses. Plant Physiol. 149: 14-26.
79. Schel, J., Kieft, H., and Lammeren, A.v. (1984). Interactions between embryo and endosperm during early developmental stages of maize caryopses (Zea mays). Can. J. Bot. 62: 2842-2853.
80. Schmidt, R.J., Burr, F.A., Aukerman, M.J., and Burr, B. (1990). Maize regulatory gene opaque-2 encodes a protein with a “leucine-zipper” motif that binds to zein DNA. Proc. Natl. Acad. Sci. USA 87: 46-50.
81. Schmidt, R.J., Ketudat, M., Aukerman, M.J., and Hoschek, G. (1992). Opaque-2 is a transcriptional activator that recognizes a specific target site in 22-kD zein genes. Plant Cell 4: 689-700.
82. 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.
83. Serna, A., Maitz, M., O’Connell, T., Santandrea, G., Thevissen, K., Tienens, K., Hueros, G., Faleri, C., Cai, G., Lottspeich, F., and Thompson, R.D. (2001). Maize endosperm secretes a novel antifungal protein into adjacent maternal tissue. Plant J. 25: 687-698.
84. Shannon, P., Markiel, A., Ozier, O., Baliga, N.S., Wang, J.T., Ramage, D., Amin, N., Schwikowski, B., and Ideker, T. (2003). Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Res. 13: 2498-2504.
85. Shure, M., Wessler, S., and Fedoroff, N. (1983). Molecular identification and isolation of the Waxy locus in maize. Cell 35: 225-233.
86. Sosso, D., Wisniewski, J.-P., Khaled, A.-S., Hueros, G., Gerentes, D., Paul, W., and Rogowsky, P.M. (2010). The Vpp1, Esr6a, Esr6b and OCL4 promoters are active in distinct domains of maize endosperm. Plant Sci. 179: 86-96.
87. Sreenivasulu, N., and Wobus, U. (2013). Seed-development programs: a systems biology-based comparison between dicots and monocots. Annu. Rev. Plant Biol. 64: 189-217.
88. Tailor, R.H., Acland, D.P., Attenborough, S., Cammue, B.P., Evans, I.J., Osborn, R.W., Ray, J.A., Rees, S.B., and Broekaert, W.F. (1997). A novel family of small cysteine-rich antimicrobial peptides from seed of Impatiens balsamina is derived from a single precursor protein. J. Biol. Chem. 272: 24480-24487.
89. Takahashi, H., Kamakura, H., Sato, Y., Shiono, K., Abiko, T., Tsutsumi, N., Nagamura, Y., Nishizawa, N.K., and Nakazono, M. (2010). A method for obtaining high quality RNA from paraffin sections of plant tissues by laser microdissection. J. Plant Res. 123: 807-813.
90. Thompson, R.D., Hueros, G., Becker, H., and Maitz, M. (2001). Development and functions of seed transfer cells. Plant Sci. 160: 775-783.
91. Trapnell, C., Pachter, L., and Salzberg, S.L. (2009). TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111.
92. 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.
93. Trapnell, C., Roberts, A., Goff, L., Pertea, G., Kim, D., Kelley, D.R., Pimentel, H., Salzberg, S.L., Rinn, J.L., and Pachter, L. (2012). Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7: 562-578.
94. Wisniewski, J.-P., and Rogowsky, P.M. (2004). Vacuolar H+-translocating inorganic pyrophosphatase (Vpp1) marks partial aleurone cell fate in cereal endosperm development. Plant Mol. Biol. 56: 325-337.
95. Woo, Y.M., Hu, D.W.N., Larkins, B.A., and Jung, R. (2001). Genomics analysis of genes expressed in maize endosperm identifies novel seed proteins and clarifies patterns of zein gene expression. Plant Cell 13: 2297-2317.
96. Xin, M., et al. (2013). Dynamic expression of imprinted genes associates with maternally controlled nutrient allocation during maize endosperm development. Plant Cell 25: 3212-3227.
97. Xiong, Y., Mei, W., Kim, E.D., Mukherjee, K., Hassanein, H., Barbazuk, W.B., Sung, S., Kolaczkowski, B., and Kang, B.H. (2014). Adaptive expansion of the maize maternally expressed gene (MEG) family involves changes in expression patterns and protein secondary structures of its members. BMC Plant Biol. 14: 204.
98. Yilmaz, A., Nishiyama, M.Y., Jr., Fuentes, B.G., Souza, G.M., Janies, D., Gray, J., and Grotewold, E. (2009). GRASSIUS: a platform for comparative regulatory genomics across the grasses. Plant Physiol. 149: 171-180.
99. Zar, J.H. (1972). Significance testing of the Spearman rank correlation coefficient. J. Am. Stat. Assoc. 67: 578-580.
100. Zhang, B., and Horvath, S. (2005). A general framework for weighted gene co-expression network analysis. Stat. Appl. Genet. Mol. Biol. 4: e17.