A genotypic difference in primary root length is associated with the inhibitory role of transforming growth factor-beta receptor-interacting protein-1 on root meristem size in wheat

Plant Journal

Volumn 77, Issue 6, 2014, Pages 931-943

  He, Xue ^a   Fang, Jingjing ^a,b   Li, Jingjuan ^a,c   Qu, Baoyuan ^a   Ren, Yongzhe ^a,d   Ma, Wenying ^a   Zhao, Xueqiang ^a   Li, Bin ^a   Wang, Daowen ^a   Li, Zhensheng ^a   Tong, Yiping ^a  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b INSTITUTE OF PLANT PROTECTION   (China)

^c SHANDONG PEANUT RESEARCH INSTITUTE   (China)

^d SHANGQIU NORMAL UNIVERSITY   (China)

Author keywords

brassinosteroid; peroxidase; primary root length; proteomics; reactive oxygen species; root meristem size; TGF beta receptor interacting protein 1; Triticum aestivum L.

Indexed keywords

GENE EXPRESSION; MOLECULAR BIOLOGY; OXYGEN; PLANTS (BOTANY);

BRASSINOSTEROIDS; PEROXIDASE; PRIMARY ROOT LENGTHS; PROTEOMICS; REACTIVE OXYGEN SPECIES; ROOT MERISTEM; TGF-BETA RECEPTOR-INTERACTING PROTEIN-1; TRITICUM AESTIVUM L;

PROTEINS;

ARABIDOPSIS; TRITICUM AESTIVUM;

BRASSINOLIDE; BRASSINOSTEROID; HETEROCYCLIC STEROID; MESSENGER RNA; PEROXIDASE; PHYTOHORMONE; PLANT RNA; REACTIVE OXYGEN METABOLITE; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; CARBOHYDRATE METABOLISM; COMPARATIVE STUDY; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MERISTEM; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGY; PLANT ROOT; PRIMARY ROOT LENGTH; PROTEOMICS; QUANTITATIVE TRAIT LOCUS; ROOT MERISTEM SIZE; SIGNAL TRANSDUCTION; TGF-BETA RECEPTOR-INTERACTING PROTEIN-1; TRITICUM AESTIVUM L.; TWO HYBRID SYSTEM; WHEAT;

BRASSINOSTEROID; PEROXIDASE; PRIMARY ROOT LENGTH; PROTEOMICS; REACTIVE OXYGEN SPECIES; ROOT MERISTEM SIZE; TGF-BETA RECEPTOR-INTERACTING PROTEIN-1; TRITICUM AESTIVUM L.;

ARABIDOPSIS; BRASSINOSTEROIDS; CARBOHYDRATE METABOLISM; GENE EXPRESSION REGULATION, PLANT; MERISTEM; OXIDATION-REDUCTION; PEROXIDASE; PLANT GROWTH REGULATORS; PLANT PROTEINS; PLANT ROOTS; PROTEOMICS; QUANTITATIVE TRAIT LOCI; REACTIVE OXYGEN SPECIES; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; RNA, MESSENGER; RNA, PLANT; SIGNAL TRANSDUCTION; STEROIDS, HETEROCYCLIC; TRITICUM; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84895925471     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12449     Document Type: Article

References (76)

1. Aida, M., Beis, D., Heidstra, R., Willemsen, V., Blilou, I., Galinha, C.R., Nussaume, L., Noh, Y.-S., Amasino, R., and, Scheres, B., (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell, 119, 109-120.
2. An, D.G., Su, J.Y., Liu, Q.Y., Zhu, Y.G., Tong, Y.P., Li, J.M., Jing, R.L., Li, B., and, Li, Z.S., (2006) Mapping QTLs for nitrogen uptake in relation to the early growth of wheat (Triticum aestivum L.). Plant Soil, 284, 73-84.
3. Asano, K., Kinzy, T.G., Merrick, W.C., and, Hershey, J.W., (1997) Conservation and diversity of eukaryotic translation initiation factor eIF3. J. Biol. Chem., 272, 1101-1109.
4. Beemster, G.T., and, Baskin, T.I., (1998) Analysis of cell division and elongation underlying the developmental acceleration of root growth in Arabidopsis thaliana. Plant Physiol., 116, 1515-1526.
5. Benková, E., and, Hejátko, J., (2009) Hormone interactions at the root apical meristem. Plant Mol. Biol., 69, 383-396.
6. - radicals. J. Physiol. Chem., 84, 830-833.
7. Bishopp, A., Ursache, R., and, Helariutta, Y., (2012) Plant development: how long is a root? Curr. Biol., 22, R919-R921.
8. Burks, E.A., Bezerra, P.P., Le, H., Gallie, D.R., and, Browning, K.S., (2001) Plant initiation factor 3 subunit composition resembles mammalian initiation factor 3 and has a novel subunit. J. Biol. Chem., 276, 2122-2131.
9. Cakmak, I., Strbac, D., and, Marschner, H., (1993) Activities of hydrogen peroxide-scavenging enzymes in germinating wheat seeds. J. Exp. Bot., 44, 127-132.
10. Chen, S.X., and, Schopfer, P., (1999) Hydroxyl-radical production in physiological reactions-A novel function of peroxidase. Eur. J. Biochem., 260, 726-735.
11. Chen, R.H., Miettinen, P.J., Maruoka, E.M., Choy, L., and, Derynck, R., (1995) A WD-domain protein that is associated with and phosphorylated by the type II TGF-beta receptor. Nature, 377, 548-552.
12. Chen, Z., Zeng, M., Song, B., et al. (2012) Dufulin activates HrBP1 to produce antiviral responses in tobacco. PLoS ONE, 7, e37944.
13. Chory, J., Nagpal, P., and, Peto, C.A., (1991) Phenotypic and genetic analysis of det2, a new mutant that affects light-regulated seedling development in Arabidopsis. Plant Cell, 3, 445-459.
14. Clouse, S.D., (2011) Brassinosteroid signal transduction: from receptor kinase activation to transcriptional networks regulating plant development. Plant Cell, 23, 1219-1230.
15. Clouse, S.D., Langford, M., and, McMorris, T.C., (1996) A brassinosteroid-insensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development. Plant Physiol., 111, 671-678.
16. De Dorlodot, S., Forster, B., Pages, L., Price, A., Tuberosa, R., and, Draye, X., (2007) Root system architecture: opportunities and constraints for genetic improvement of crops. Trends Plant Sci., 12, 474-481.
17. De Tullio, M.C., Jiang, K., and, Feldman, L.J., (2010) Redox regulation of root apical meristem organization: connecting root development to its environment. Plant Physiol. Biochem., 48, 328-336.
18. Dello Ioio, R., Nakamura, K., Moubayidin, L., Perilli, S., Taniguchi, M., Morita, M.T., Aoyama, T., Costantino, P., and, Sabatini, S., (2008) A genetic framework for the control of cell division and differentiation in the root meristem. Science, 322, 1380-1384.
19. Duan, K., Li, L., Hu, P., Xu, S.P., Xu, Z.H., and, Xue, H.W., (2006) A brassinolide-suppressed rice MADS-box transcription factor, OsMDP1, has a negative regulatory role in BR signaling. Plant J., 47, 519-531.
20. Dunand, C., Crèvecoeur, M., and, Penel, C., (2007) Distribution of superoxide and hydrogen peroxide in Arabidopsis root and their influence on root development: possible interaction with peroxidases. New Phytol., 174, 332-341.
21. Dunbabin, V., Diggle, A., and, Rengel, Z., (2003) Is there an optimal root architecture for nitrate capture in leaching environments? Plant, Cell Environ., 26, 835-844.
22. Ehsan, H., Ray, W.K., Phinney, B., Wang, X., Huber, S.C., and, Clouse, S.D., (2005) Interaction of Arabidopsis BRASSINOSTEROID-INSENSITIVE 1 receptor kinase with a homolog of mammalian TGF-beta receptor interacting protein. Plant J., 43, 251-261.
23. Ferguson, B.J., Ross, J.J., and, Reid, J.B., (2005) Nodulation phenotypes of gibberellin and brassinosteroid mutants of pea. Plant Physiol., 138, 2396-2405.
24. Fukaki, H., and, Tasaka, M., (2009) Hormone interactions during lateral root formation. Plant Mol. Biol., 69, 437-449.
25. Galinha, C., Hofhuis, H., Luijten, M., Willemsen, V., Blilou, I., Heidstra, R., and, Scheres, B., (2007) PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature, 449, 1053-1057.
26. Gao, Y., Wang, S., Asami, T., and, Chen, J.G., (2008) Loss-of-function mutations in the Arabidopsis heterotrimeric G-protein alpha subunit enhance the developmental defects of brassinosteroid signaling and biosynthesis mutants. Plant Cell Physiol., 49, 1013-1024.
27. González-García, M.P., Vilarrasa-Blasi, J., Zhiponova, M., Divol, F., Mora-García, S., Russinova, E., and, Caño-Delgado, A.I., (2011) Brassinosteroids control meristem size by promoting cell cycle progression in Arabidopsis roots. Development, 138, 849-859.
28. Guo, H.Q., Li, L., Aluru, M., Aluru, S., and, Yin, Y.H., (2013) Mechanisms and networks for brassinosteroid regulated gene expression. Curr. Opin. Plant Biol., 16, 545-553.
29. Hacham, Y., Holland, N., Butterfield, C., Ubeda-Tomas, S., Bennett, M.J., Chory, J., and, Savaldi-Goldstein, S., (2011) Brassinosteroid perception in the epidermis controls root meristem size. Development, 138, 839-848.
30. Hacham, Y., Sela, A., Friedlander, L., and, Savaldi-Goldstein, S., (2012) BRI1 activity in the root meristem involves post-transcriptional regulation of PIN auxin efflux carriers. Plant Signaling Behav., 7, 68-70.
31. Hammer, G.L., Dong, Z.S., McLean, G., Doherty, A., Messina, C., Schusler, J., Zinselmeier, C., Paszkiewicz, S., and, Cooper, M., (2009) Can changes in canopy and/or root system architecture explain historical maize yield trends in the US corn belt? Crop Sci., 49, 299-312.
32. Hao, C.Y., Dong, Y.C., Wang, L.F., You, G.X., Zhang, H.N., Ge, H.M., Jia, J.Z., and, Zhang, X.Y., (2008) Genetic diversity and construction of core collection in Chinese wheat genetic resources. Chinese Sci. Bull., 53, 1518-1526.
33. He, J.X., Gendron, J.M., Sun, Y., Gampala, S.S., Gendron, N., Sun, C.Q., and, Wang, Z.Y., (2005) BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses. Science, 307, 1634-1638.
34. Herder, G.D., Van Isterdael, G., Beeckman, T., and, De Smet, I., (2010) The roots of a new green revolution. Trends Plant Sci., 15, 600-607.
35. Hong, Y., Peng, J., Jiang, W., Fu, Z., Liu, J., Shi, Y., Li, X., and, Lin, J., (2011) Proteomic analysis of Schistosoma japonicum schistosomulum proteins that are differentially expressed among hosts differing in their susceptibility to the infection. Mol. Cell. Proteomics, 10 (M110), 006098.
36. Jiang, J., and, Clouse, S.D., (2001) Expression of a plant gene with sequence similarity to animal TGF-beta receptor interacting protein is regulated by brassinosteroids and required for normal plant development. Plant J., 26, 35-45.
37. Johnson, K.L., and, Ingram, G.C., (2005) Sending the right signals: regulating receptor kinase activity. Curr. Opin. Plant Biol., 8, 648-656.
38. Kim, T.W., and, Wang, Z.Y., (2010) Brassinosteroid signal transduction from receptor kinases to transcription factors. Annu. Rev. Plant Biol., 61, 681-704.
39. Kim, H., Park, P.J., Hwang, H.J., Lee, S.Y., Oh, M.H., and, Kim, S.G., (2006) Brassinosteroid signals control expression of the AXR3/IAA17 gene in the cross-talk point with auxin in root development. Biosci. Biotech. Bioch., 70, 768-773.
40. Kim, T.W., Guan, S., Sun, Y., Deng, Z., Tang, W., Shang, J.X., Burlingame, A.L., and, Wang, Z.Y., (2009) Brassinosteroid signal transduction from cell-surface receptor kinases to nuclear transcription factors. Nat. Cell Biol., 11, 1254-1260.
41. Koka, C.V., Cerny, R.E., Gardner, R.G., Noguchi, T., Fujioka, S., Takatsuto, S., Yoshida, S., and, Clouse, S.D., (2000) A putative role for the tomato genes DUMPY and CURL-3 in brassinosteroid biosynthesis and response. Plant Physiol., 122, 85-98.
42. Li, J.M., (2010) Regulation of the nuclear activities of brassinosteroid signaling. Curr. Opin. Plant Biol., 13, 540-547.
43. Li, J.M., and, Chory, J., (1997) A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell, 90, 929-938.
44. Li, J.M., and, Nam, K.H., (2002) Regulation of brassinosteroid signaling by a GSK3/SHAGGY-like kinase. Science, 295, 1299-1301.
45. Li, J.M., Nam, K.H., Vafeados, D., and, Chory, J., (2001) BIN2, a new brassinosteroid-insensitive locus in Arabidopsis. Plant Physiol., 127, 14-22.
46. Li, J., Wen, J., Lease, K.A., Doke, J.T., Tax, F.E., and, Walker, J.C., (2002) BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell, 110, 213-222.
47. Li, J., Mo, X.R., Wang, J.R., Chen, N.N., Fan, H., Dai, C.Y., and, Wu, P., (2009) BREVIS RADIX is involved in cytokinin-mediated inhibition of lateral root initiation in Arabidopsis. Planta, 229, 593-603.
48. Liang, Q.A., Cheng, X.H., Mei, M.T., Yan, X.L., and, Liao, H., (2010) QTL analysis of root traits as related to phosphorus efficiency in soybean. Ann. Bot., 106, 223-234.
49. Maruta, T., Ichikawa, Y., Mieda, T., Takeda, T., Tamoi, M., Yabuta, Y., Ishikawa, T., and, Shigeoka, S., (2010) The contribution of Arabidopsis homologs of L-gulono-1,4-lactone oxidase to the biosynthesis of ascorbic acid. Biosci. Biotech. Bioch., 74, 1494-1497.
50. Müssig, C., Shin, G.-H., and, Altmann, T., (2003) Brassinosteroids promote root growth in Arabidopsis. Plant Physiol., 133, 1261-1271.
51. Nakamura, A., Fujioka, S., Sunohara, H., et al. (2006) The role of OsBRI1 and its homologous genes, OsBRL1 and OsBRL3, in rice. Plant Physiol., 140, 580-590.
52. Nam, K.H., and, Li, J., (2002) BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell, 110, 203-212.
53. Noctor, G., and, Foyer, C.H., (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu. Rev. Plant Phys., 49, 249-279.
54. Park, C.H., Kim, T.W., Son, S.H., Hwang, J.Y., Lee, S.C., Chang, S.C., Kim, S.H., Kim, S.W., and, Kim, S.K., (2010) Brassinosteroids control AtEXPA5 gene expression in Arabidopsis thaliana. Phytochemistry, 71, 380-387.
55. Ren, Y.Z., He, X., Liu, D.C., Li, J.J., Zhao, X.Q., Li, B., Tong, Y.P., Zhang, A.M., and, Li, Z.S., (2012) Major quantitative trait loci for seminal root morphology of wheat seedlings. Mol. Breeding, 30, 139-148.
56. Russinova, E., Borst, J.W., Kwaaitaal, M., Cano-Delgado, A., Yin, Y., Chory, J., and, de Vries, S.C., (2004) Heterodimerization and endocytosis of Arabidopsis brassinosteroid receptors BRI1 and AtSERK3 (BAK1). Plant Cell, 16, 3216-3229.
57. Ryu, H., Kim, K., Cho, H., and, Hwang, I., (2010) Predominant actions of cytosolic BSU1 and nuclear BIN2 regulate subcellular localization of BES1 in brassinosteroid signaling. Mol. Cells, 29, 291-296.
58. Sakurai, T., Okamoto, H., Kawahara, K., and, Nakahara, A., (1982) Some properties of a blue copper protein 'Plantacyanin' from cucumber peel. FEBS Lett., 147, 220-224.
59. Steele, K.A., Virk, D.S., Kumar, R., Prasad, S.C., and, Witcombe, J.R., (2007) Field evaluation of upland rice lines selected for QTLs controlling root traits. Field Crop Res., 101, 180-186.
60. Subramaniam, K., Ye, Z., Buechley, G., Shaner, G., Solomos, T., and, Ueng, P.P., (1999) Isolation of a Zeta class wheat glutathione S-transferase gene. Bba-Gene Struct. Expr., 1447, 348-356.
61. Sun, Y., Fan, X.Y., Cao, D.M., et al. (2010) Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev. Cell, 19, 765-777.
62. Tang, W., Kim, T.W., Oses-Prieto, J.A., Sun, Y., Deng, Z., Zhu, S., Wang, R., Burlingame, A.L., and, Wang, Z.Y., (2008) BSKs mediate signal transduction from the receptor kinase BRI1 in Arabidopsis. Science, 321, 557-560.
63. Tang, W., Yuan, M., Wang, R., et al. (2011) PP2A activates brassinosteroid-responsive gene expression and plant growth by dephosphorylating BZR1. Nat. Cell Biol., 13, 124-131.
64. Tsukagoshi, H., Busch, W., and, Benfey, P.N., (2010) Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell, 143, 606-616.
65. Tuberosa, R., Sanguineti, M.C., Landi, P., Michela Giuliani, M., Salvi, S., and, Conti, S., (2002) Identification of QTLs for root characteristics in maize grown in hydroponics and analysis of their overlap with QTLs for grain yield in the field at two water regimes. Plant Mol. Biol., 48, 697-712.
66. Vernoux, T., Wilson, R.C., Seeley, K.A., et al. (2000) The ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development. Plant Cell, 12, 97-109.
67. Vert, G., Nemhauser, J.L., Geldner, N., Hong, F., and, Chory, J., (2005) Molecular mechanisms of steroid hormone signaling in plants. Annu. Rev. Cell Dev. Biol., 21, 177-201.
68. Waines, J.G., and, Ehdaie, B., (2007) Domestication and crop physiology: roots of green-revolution wheat. Ann. Bot., 100, 991-998.
69. Walter, M., Chaban, C., Schutze, K., et al. (2004) Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J., 40, 428-438.
70. Wang, X., and, Chory, J., (2006) Brassinosteroids regulate dissociation of BKI1, a negative regulator of BRI1 signaling, from the plasma membrane. Science, 313, 1118-1122.
71. Wang, Z.Y., Nakano, T., Gendron, J., et al. (2002) Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev. Cell, 2, 505-513.
72. Wu, F.H., Shen, S.C., Lee, L.Y., Lee, S.H., Chan, M.T., and, Lin, C.S., (2009) Tape-Arabidopsis Sandwich-a simpler Arabidopsis protoplast isolation method. Plant Methods, 5, 16.
73. Yin, Y., Wang, Z.Y., Mora-Garcia, S., Li, J., Yoshida, S., Asami, T., and, Chory, J., (2002) BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell, 109, 181-191.
74. Yin, Y., Vafeados, D., Tao, Y., Yoshida, S., Asami, T., and, Chory, J., (2005) A new class of transcription factors mediates brassinosteroid-regulated gene expression in Arabidopsis. Cell, 120, 249-259.
75. Yu, X., Li, L., Zola, J., et al. (2011) A brassinosteroid transcriptional network revealed by genome-wide identification of BESI target genes in Arabidopsis thaliana. Plant J., 65, 634-646.
76. Zhao, J., Peng, P., Schmitz, R.J., Decker, A.D., Tax, F.E., and, Li, J.M., (2002) Two putative BIN2 substrates are nuclear components of brassinosteroid signaling. Plant Physiol., 130, 1221-1229.