Comparative transcriptomics as a tool for the identification of root branching genes in maize

Plant Biotechnology Journal

Volumn 11, Issue 9, 2013, Pages 1092-1102

  Jansen, Leentje ^a,b   Hollunder, Jens ^a,b   Roberts, Ianto ^a,b   Forestan, Cristian ^c   Fonteyne, Philippe ^a,b   Van Quickenborne, Charlotte ^a,b   Zhen, Rui Guang ^d   Mckersie, Bryan ^d   Parizot, Boris ^a,b   Beeckman, Tom ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c UNIVERSITY OF PADOVA   (Italy)

^d BASF CORPORATION   (United States)

Author keywords

Arabidopsis thaliana; Auxin; Comparative transcriptomics; Lateral root initiation; Maize

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; MAGNOLIOPHYTA; ZEA MAYS;

AUXIN; INDOLEACETIC ACID; INDOLEACETIC ACID DERIVATIVE; VEGETABLE PROTEIN;

ARABIDOPSIS; ARABIDOPSIS THALIANA; ARTICLE; CELL CYCLE; CELL DIVISION; COMPARATIVE STUDY; COMPARATIVE TRANSCRIPTOMICS; CYTOLOGY; DRUG EFFECT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LATERAL ROOT INITIATION; MAIZE; PLANT ROOT;

ARABIDOPSIS THALIANA; AUXIN; COMPARATIVE TRANSCRIPTOMICS; LATERAL ROOT INITIATION; MAIZE;

ARABIDOPSIS; CELL CYCLE; CELL DIVISION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; INDOLEACETIC ACIDS; PLANT PROTEINS; PLANT ROOTS; ZEA MAYS;

EID: 84888138095     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12104     Document Type: Article

References (65)

1. Beeckman, T., Burssens, S. and Inzé, D. (2001) The peri-cell-cycle in Arabidopsis. J. Exp. Bot. 52, 403-411.
2. von Behrens, I., Komatsu, M., Zhang, Y., Berendzen, K.W., Niu, X., Sakai, H., Taramino, G. and Hochholdinger, F. (2011) Rootless with undetectable meristem 1 encodes a monocot-specific AUX/IAA protein that controls embryonic seminal and post-embryonic lateral root initiation in maize. Plant J. 66, 341-353.
3. Bell, J.K. and McCully, M.E. (1970) A histological study of lateral root initiation and development in Zea mays. Protoplasma, 70, 179-205.
4. Benjamini, Y. and Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Roy. Statist. Soc. Ser. B (Methodological), 57, 289-300.
5. Berckmans, B., Vassileva, V., Schmid, S.P.C., Maes, S., Parizot, B., Naramoto, S., Magyar, Z., Lessa Alvim Kamei, C., Koncz, C., Bögre, L., Persiau, G., De Jaeger, G., Friml, J., Simon, R., Beeckman, T. and De Veylder, L. (2011) Auxin-dependent cell cycle reactivation through transcriptional regulation of Arabidopsis E2Fa by lateral organ boundary proteins. Plant Cell, 23, 3671-3683.
6. Bolstad, B.M., Irizarry, R.A., Åstrand, M. and Speed, T.P. (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics, 19, 185-193.
7. Brady, S.M., Orlando, D.A., Lee, J.-Y., Wang, J.Y., Koch, J., Dinneny, J.R., Mace, D., Ohler, U. and Benfey, P.N. (2007) A high-resolution root spatiotemporal map reveals dominant expression patterns. Science, 318, 801-806.
8. Casero, P.J., Casimiro, I. and Lloret, P.G. (1995) Lateral root initiation by asymmetrical transverse divisions of pericycle cells in four plant species: Raphanus sativus, Helianthus annuus, Zea mays, and Daucus carota. Protoplasma, 188, 49-58.
9. Chuck, G. and Hake, S. (2005) Regulation of developmental transitions. Curr. Opin. Plant Biol. 8, 67-70.
10. De Bodt, S., Maere, S. and Van de Peer, Y. (2005) Genome duplication and the origin of angiosperms. Trends Ecol. Evol. 20, 591-597.
11. De Smet, I., Vassileva, V., De Rybel, B., Levesque, M.P., Grunewald, W., Van Damme, D., Van Noorden, G., Naudts, M., Van Isterdael, G., De Clercq, R., Wang, J.Y., Meuli, N., Vanneste, S., Friml, J., Hilson, P., Jürgens, G., Ingram, G.C., Inzé, D., Benfey, P.N. and Beeckman, T. (2008) Receptor-like kinase ACR4 restricts formative cell divisions in the Arabidopsis root. Science, 322, 594-597.
12. De Veylder, L., Beeckman, T., Beemster, G.T.S., Krols, L., Terras, F., Landrieu, I., Van Der Schueren, E., Maes, S., Naudts, M. and Inée, D. (2001) Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell, 13, 1653-1667.
13. Dembinsky, D., Woll, K., Saleem, M., Liu, Y., Fu, Y., Borsuk, L.A., Lamkemeyer, T., Fladerer, C., Madlung, J., Barbazuk, B., Nordheim, A., Nettleton, D., Schnable, P.S. and Hochholdinger, F. (2007) Transcriptomic and proteomic analyses of pericycle cells of the maize primary root. Plant Physiol. 145, 575-588.
14. Dolan, L., Janmaat, K., Willemsen, V., Linstead, P., Poethig, S., Roberts, K. and Scheres, B. (1993) Cellular organisation of the Arabidopsis thaliana root. Development, 119, 71-84.
15. Feldman, L. (1994) The maize root. In The Maize Handbook (Freeling, M. and Walbot, V., eds), pp. 29-37. New York: Springer.
16. Finet, C., Berne-Dedieu, A., Scutt, C.P. and Marlétaz, F. (2013) Evolution of the ARF gene family in land plants: old domains, new tricks. Mol. Biol. Evol. 30, 45-56.
17. Fukaki, H., Tameda, S., Masuda, H. and Tasaka, M. (2002) Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J. 29, 153-168.
18. Gentleman, R., Carey, V., Huber, W., Irizarry, R. and Dudoit, S. (2005) Bioinformatics and Computational Biology Solutions Using R and Bioconductor. New York: Springer.
19. Gewin, V. (2010) Food: an underground revolution. Nature, 466, 552-553.
20. Glover, J.D., Cox, C.M. and Reganold, J.P. (2007) Future farming: a return to roots? Sci. Am. 297, 82-89.
21. Hellemans, J., Mortier, G., De Paepe, A., Speleman, F. and Vandesompele, J. (2007) qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol. 8, R19.
22. Hemerly, A., Bergounioux, C., Van Montagu, M., Inzé, D. and Ferreira, P. (1992) Genes regulating the plant cell cycle: isolation of a mitotic-like cyclin from Arabidopsis thaliana. Proc. Natl Acad. Sci. USA, 89, 3295-3299.
23. Himanen, K., Boucheron, E., Vanneste, S., de Almeida Engler, J., Inzé, D. and Beeckman, T. (2002) Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell, 14, 2339-2351.
24. Himanen, K., Vuylsteke, M., Vanneste, S., Vercruysse, S., Boucheron, E., Alard, P., Chriqui, D., Van Montagu, M., Inzé, D. and Beeckman, T. (2004) Transcript profiling of early lateral root initiation. Proc. Natl Acad. Sci. USA, 101, 5146-5151.
25. Hirota, A., Kato, T., Fukaki, H., Aida, M. and Tasaka, M. (2007) The auxin-regulated AP2/EREBP gene PUCHI is required for morphogenesis in the early lateral root primordium of Arabidopsis. Plant Cell, 19, 2156-2168.
26. Hochholdinger, F., Park, W.J. and Feix, G.H. (2001) Cooperative action of SLR1 and SLR2 is required for lateral root-specific cell elongation in maize. Plant Physiol. 125, 1529-1539.
27. Hochholdinger, F., Park, W.J., Sauer, M. and Woll, K. (2004a) From weeds to crops: genetic analysis of root development in cereals. Trends Plant Sci. 9, 42-48.
28. Hochholdinger, F., Woll, K., Sauer, M. and Dembinsky, D. (2004b) Genetic dissection of root formation in maize (Zea mays) reveals root-type specific developmental programmes. Ann. Bot. 93, 359-368.
29. Irizarry, R.A., Hobbs, B., Collin, F., Beazer-Barclay, Y.D., Antonellis, K.J., Scherf, U. and Speed, T.P. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics, 4, 249-264.
30. Ito, K., Tanakamaru, K., Morita, S., Abe, J. and Inanaga, S. (2006) Lateral root development, including responses to soil drying, of maize (Zea mays) and wheat (Triticum aestivum) seminal roots. Physiol. Plant. 127, 260-267.
31. Jansen, L., Roberts, I., De Rycke, R. and Beeckman, T. (2012) Phloem-associated auxin response maxima determine radial positioning of lateral roots in maize. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367, 1525-1533.
32. Jansen, L., Parizot, B. and Beeckman, T. (2013) Inducible system for lateral roots in Arabidopsis thaliana and maize. Methods Mol. Biol. 959, 149-158.
33. Kang, N.Y., Lee, H.W. and Kim, J. (2013) The AP2/EREBP gene PUCHI coacts with LBD16/ASL18 and LBD18/ASL20 downstream of ARF7 and ARF19 to regulate lateral root development in Arabidopsis. Plant Cell Physiol. doi: 10.1093/pcp/pct081.
34. Katiyar, A., Smita, S., Lenka, S.K., Rajwanshi, R., Chinnusamy, V. and Bansal, K.C. (2012) Genome-wide classification and expression analysis of MYB transcription factor families in rice and Arabidopsis. BMC Genomics, 13, 544.
35. Laplaze, L., Benkova, E., Casimiro, I., Maes, L., Vanneste, S., Swarup, R., Weijers, D., Calvo, V., Parizot, B., Herrera-Rodriguez, M.B., Offringa, R., Graham, N., Doumas, P., Friml, J., Bogusz, D., Beeckman, T. and Bennett, M. (2007) Cytokinins act directly on lateral root founder cells to inhibit root initiation. Plant Cell, 19, 3889-3900.
36. Levesque, M.P., Vernoux, T., Busch, W., Cui, H., Wang, J.Y., Blilou, I., Hassan, H., Nakajima, K, Matsumoto, N., Lohmann, J.U., Scheres, B. and Benfey, P.N. (2006) Whole-genome analysis of the SHORT-ROOT developmental pathway in Arabidopsis. PLoS Biol. 4, e143.
37. Li, L., Stoeckert Jr, C.J. and Roos, D.S. (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13, 2178-2189.
38. Liu, Y., Lamkemeyer, T., Jakob, A., Mi, G., Zhang, F., Nordheim, A. and Hochholdinger, F. (2006) Comparative proteome analyses of maize (Zea mays L.) primary roots prior to lateral root initiation reveal differential protein expression in the lateral root initiation mutant rum1. Proteomics, 6, 4300-4308.
39. Liu, Y., von Behrens, I., Muthreich, N., Schütz, W., Nordheim, A. and Hochholdinger, F. (2010) Regulation of the pericycle proteome in maize (Zea mays L.) primary roots by RUM1 which is required for lateral root initiation. Eur. J. Cell Biol. 89, 236-241.
40. Lynch, J. (1995) Root architecture and plant productivity. Plant Physiol. 109, 7-13.
41. Malamy, J.E. and Benfey, P.N. (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development, 124, 33-44.
42. Marchant, A., Bhalerao, R., Casimiro, I., Eklöf, J., Casero, P.J., Bennett, M. and Sandberg, G. (2002) AUX1 promotes lateral root formation by facilitating indole-3-acetic acid distribution between sink and source tissues in the Arabidopsis seedling. Plant Cell, 14, 589-597.
43. McSteen, P. (2010) Auxin and monocot development. Cold Spring Harb. Perspect. Biol. 2, a001479.
44. Nakazono, M., Qiu, F., Borsuk, L.A. and Schnable, P.S. (2003) Laser-capture microdissection, a tool for the global analysis of gene expression in specific plant cell types: identification of genes expressed differentially in epidermal cells or vascular tissues of maize. Plant Cell, 15, 583-596.
45. Ouyang, S., Zhu, W., Hamilton, J., Lin, H., Campbell, M., Childs, K., Thibaud-Nissen, F., Malek, R.L., Lee, Y., Zheng, L., Orvis, J., Haas, B., Wortman, J. and Buell, C.R. (2007) The TIGR Rice Genome Annotation Resource: improvements and new features. Nucleic Acids Res. 35, D883-D887.
46. Overvoorde, P., Fukaki, H. and Beeckman, T. (2010) Auxin control of root development. Cold Spring Harb. Perspect. Biol. 2, doi: 10.1101/cshperspect.a001537a001537.
47. Parizot, B., Laplaze, L., Ricaud, L., Boucheron-Dubuisson, E., Bayle, V., Bonke, M., De Smet, I., Poethig, S.R., Helariutta, Y., Haseloff, J., Chriqui, D., Beeckman, T. and Nussaume, L. (2008) Diarch symmetry of the vascular bundle in Arabidopsis root encompasses the pericycle and is reflected in distich lateral root initiation. Plant Physiol. 146, 140-148.
48. Parizot, B., De Rybel, B. and Beeckman, T. (2010) VisuaLRTC: a new view on lateral root initiation by combining specific transcriptome data sets. Plant Physiol. 153, 34-40.
49. Parizot, B., Roberts, I., Raes, J., Beeckman, T. and De Smet, I. (2012) In silico analyses of pericycle cell populations reinforce their relation with associated vasculature in Arabidopsis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367, 1479-1488.
50. Paterson, A.H., Bowers, J.E., Bruggmann, R., Dubchak, I., Grimwood, J., Gundlach, H., Haberer, G., Hellsten, U., Mitros, T., Poliakov, A., Schmutz, J., Spannagl, M., Tang, H., Wang, X., Wicker, T., Bharti, A.K., Chapman, J., Feltus, F.A., Gowik, U., Grigoriev, I.V., Lyons, E., Maher, C.A., Martis, M., Narechania, A., Otillar, R.P., Penning, B.W., Salamov, A.A., Wang, Y., Zhang, L., Carpita, N.C., Freeling, M., Gingle, A.R., Hash, C.T., Keller, B., Klein, P., Kresovich, S., McCann, M.C., Ming, R., Peterson, D.G., Mehboob ur, R., Ware, D., Westhoff, P., Mayer, K.F., Messing, J. and Rokhsar, D.S. (2009) The Sorghum bicolor genome and the diversification of grasses. Nature, 457, 551-556.
51. Proost, S., Van Bel, M., Sterck, L., Billiau, K., Van Parys, T., Van de Peer, Y. and Vandepoele, K. (2009) PLAZA: a comparative genomics resource to study gene and genome evolution in plants. Plant Cell, 21, 3718-3731.
52. Rymen, B., Fiorani, F., Kartal, F., Vandepoele, K., Inzé, D. and Beemster, G.T.S. (2007) Cold nights impair leaf growth and cell cycle progression in maize through transcriptional changes of cell cycle genes. Plant Physiol. 143, 1429-1438.
53. Saeed, A.I., Bhagabati, N.K., Braisted, J.C., Liang, W., Sharov, V., Howe, E.A., Li, J., Thiagarajan, M., White, J.A. and Quackenbush, J. (2006) TM4 microarray software suite. Methods Enzymol. 411, 134-193.
54. Schnable, P.S., Ware, D., Fulton, R.S., Stein, J.C., Wei, F., Pasternak, S., Liang, C., Zhang, J., Fulton, L., Graves, T.A., Minx, P., Reily, A.D., Courtney, L., Kruchowski, S.S., Tomlinson, C., Strong, C., Delehaunty, K., Fronick, C., Courtney, B., Rock, S.M., Belter, E., Du, F., Kim, K., Abbott, R.M., Cotton, M., Levy, A., Marchetto, P., Ochoa, K., Jackson, S.M., Gillam, B., Chen, W., Yan, L., Higgnbotham, J., Cardenas, M., Waligorski, J., Applebaum, E., Phelps, L., Falcone, J., Kanchi, K., Thane, T., Scimone, A., Thane, N., Henke, J., Wang, T., Ruppert, J., Shah, N., Rotter, K., Hodges, J., Ingenthron, E., Cordes, M., Kohlberg, S., Sgro, J., Delgado, B., Mead, K., Chinwalla, A., Leonard, S., Crouse, K., Collura, K., Kudrna, D., Currie, J., He, R., Angelova, A., Rajasekar, S., Mueller, T., Lomeli, R., Scara, G., Ko, A., Delaney, K., Wissotski, M., Lopez, G., Campos, D., Braidotti, M., Ashley, E., Golser, W., Kim, Y., Lee, S., Lin, J., Dujmic, Z., Kim, W., Talag, J., Zuccolo, A., Fan, C., Sebastian, A., Kramer, M., Spiegel, L., Nascimento, L., Zutavern, T., Miller, B., Ambroise, C., Muller, S., Spooner, W., Narechania, A., Ren, L., Wei, S., Kumari, S., Faga, B., Levy, M.J., McMahan, L., Van Buren, P., Vaughn, M.W., Ying, K., Yeh, C.-T., Emrich, S.J., Jia, Y., Kalyanaraman, A., Hsia, A.-P., Barbazuk, W.B., Baucom, R.S., Brutnell, T.P., Carpita, N.C., Chaparro, C., Chia, J.-M., Deragon, J.-M., Estill, J.C., Fu, Y., Jeddeloh, J.A., Han, Y., Lee, H., Li, P., Lisch, D.R., Liu, S., Liu, Z., Nagel, D.H., McCann, M.C., SanMiguel, P., Myers, A.M., Nettleton, D., Nguyen, J., Penning, B.W., Ponnala, L., Schneider, K.L., Schwartz, D.C., Sharma, A., Soderlund, C., Springer, N.M., Sun, Q., Wang, H., Waterman, M., Westerman, R., Wolfgruber, T.K., Yang, L., Yu, Y., Zhang, L., Zhou, S., Zhu, Q., Bennetzen, J.L., Dawe, R.K., Jiang, J., Jiang, N., Presting, G.G., Wessler, S.R., Aluru, S., Martienssen, R.A., Clifton, S.W., McCombie, W.R., Wing, R.A. and Wilson, R.K. (2009) The B73 maize genome: complexity, diversity, and dynamics. Science, 326, 1112-1115.
55. Smyth, G.K. (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, 1544-6115.
56. Swarup, K., Benková, E., Swarup, R., Casimiro, I., Péret, B., Yang, Y., Parry, G., Nielsen, E., De Smet, I., Vanneste, S., Levesque, M.P., Carrier, D., James, N., Calvo, V., Ljung, K., Kramer, E., Roberts, R., Graham, N., Marillonnet, S., Patel, K., Jones, J.D.G., Taylor, C.G., Schachtman, D.P., May, S., Sandberg, G., Benfey, P., Friml, J., Kerr, I., Beeckman, T., Laplaze, L. and Bennett, M.J. (2008) The auxin influx carrier LAX3 promotes lateral root emergence. Nat. Cell Biol. 10, 946-954.
57. The Arabidopsis Genome Initiative. (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature, 408, 796-815.
58. The International Brachypodium Initiative. (2010) Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature, 463, 763-768.
59. Van Bel, M., Proost, S., Wischnitzki, E., Movahedi, S., Scheerlinck, C., Van de Peer, Y. and Vandepoele, K. (2012) Dissecting plant genomes with the PLAZA comparative genomics platform. Plant Physiol. 158, 590-600.
60. Vanneste, S., De Rybel, B., Beemster, G.T.S., Ljung, K., De Smet, I., Van Isterdael, G., Naudts, M., Iida, R., Gruissem, W., Tasaka, M., Inzé, D., Fukaki, H. and Beeckman, T. (2005) Cell cycle progression in the pericycle is not sufficient for SOLITARY ROOT/IAA14-mediated lateral root initiation in Arabidopsis thaliana. Plant Cell, 17, 3035-3050.
61. Varney, G.T. and Canny, M.J. (1993) Rates of water uptake into the mature root system of maize plants. New Phytol. 123, 775-786.
62. Viaene, T., Delwiche, C.F., Rensing, S.A. and Friml, J. (2013) Origin and evolution of PIN auxin transporters in the green lineage. Trends Plant Sci. 18, 5-10.
63. Waisel, Y., Eshel, A. and Kafkafi, U. (2002) Plant Roots: The Hidden Half. New York: Marcel Dekker, Inc.
64. Wilmoth, J.C., Wang, S., Tiwari, S.B., Joshi, A.D., Hagen, G., Guilfoyle, T.J., Alonso, J.M., Ecker, J.R. and Reed, J.W. (2005) NPH4/ARF7 and ARF19 promote leaf expansion and auxin-induced lateral root formation. Plant J. 43, 118-130.
65. Woll, K., Borsuk, L.A., Stransky, H., Nettleton, D., Schnable, P.S. and Hochholdinger, F. (2005) Isolation, characterization, and pericycle-specific transcriptome analyses of the novel maize lateral and seminal root initiation mutant rum1. Plant Physiol. 139, 1255-1267.