Axillary meristem formation in rice requires the WUSCHEL ortholog TILLERS ABSENT1open

Plant Cell

Volumn 27, Issue 4, 2015, Pages 1173-1184

  Tanaka, Wakana ^a   Ohmori, Yoshihiro ^a   Ushijima, Tomokazu ^a,b   Matsusaka, Hiroaki ^a,b   Matsushita, Tomonao ^a,b   Kumamaru, Toshihiro ^a,b   Kawano, Shigeyuki ^a   Hirano, Hiro Yuki ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS THALIANA; ORYZA SATIVA;

PLANT PROTEIN; PROTEIN BINDING;

GENE EXPRESSION REGULATION; GENETICS; MERISTEM; METABOLISM; ORYZA;

GENE EXPRESSION REGULATION, PLANT; MERISTEM; ORYZA; PLANT PROTEINS; PROTEIN BINDING;

EID: 84928946710     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.15.00074     Document Type: Article

References (57)

1. Aichinger, E., Kornet, N., Friedrich, T., and Laux, T. (2012). Plant stem cell niches. Annu. Rev. Plant Biol. 63: 615–636.
2. Arber, A. (1923). Leaves of the Gramineae. Bot. Gaz. 76: 374–388.
3. Barton, M.K. (2010). Twenty years on: The inner workings of the shoot apical meristem, a developmental dynamo. Dev. Biol. 341: 95–113.
4. Bommert, P., Lunde, C., Nardmann, J., Vollbrecht, E., Running, M., Jackson, D., Hake, S., and Werr, W. (2005). thick tassel dwarf1 encodes a putative maize ortholog of the Arabidopsis CLAVATA1 leucine-rich repeat receptor-like kinase. Development 132: 1235–1245.
5. Bossinger, G., Lundqvist, U., Rohde, W., and Salamini, F. (1992). Genetics of plant development in barley. In Barley Genetics, Vol. 6, L. Munck, ed (Copenhagen: Munksgaard lnternational Publishers), pp. 989–1022.
6. Daum, G., Medzihradszky, A., Suzaki, T., and Lohmann, J.U. (2014). A mechanistic framework for noncell autonomous stem cell induction in Arabidopsis. Proc. Natl. Acad. Sci. USA 111: 14619–14624.
7. Domagalska, M.A., and Leyser, O. (2011). Signal integration in the control of shoot branching. Nat. Rev. Mol. Cell Biol. 12: 211–221.
8. Esau, K. (1977). Anatomy of Seed Plants, 2nd ed. (New York: Wiley).
9. Gallavotti, A., Zhao, Q., Kyozuka, J., Meeley, R.B., Ritter, M.K., Doebley, J.F., Pè, M.E., and Schmidt, R.J. (2004). The role of barren stalk1 in the architecture of maize. Nature 432: 630–635.
10. Greb, T., Clarenz, O., Schafer, E., Muller, D., Herrero, R., Schmitz, G., and Theres, K. (2003). Molecular analysis of the LATERAL SUPPRESSOR gene in Arabidopsis reveals a conserved control mechanism for axillary meristem formation. Genes Dev. 17: 1175–1187.
11. Ha, C.M., Jun, J.H., and Fletcher, J.C. (2010). Shoot apical meristem form and function. Curr. Top. Dev. Biol. 91: 103–140.
12. Hiei, Y., Ohta, S., Komari, T., and Kumashiro, T. (1994). Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J. 6: 271–282.
13. Hirakawa, Y., Kondo, Y., and Fukuda, H. (2011). Establishment and maintenance of vascular cell communities through local signaling. Curr. Opin. Plant Biol. 14: 17–23.
14. Hoshikawa, K. (1989). Growing the Rice Plant: An Anatomical Monograph. (Tokyo: Nobunkyo).
15. Itoh, J.-I., Kitano, H., Matsuoka, M., and Nagato, Y. (2000). Shoot organization genes regulate shoot apical meristem organization and the pattern of leaf primordium initiation in rice. Plant Cell 12: 2161–2174.
16. Jackson, D., Veit, B., and Hake, S. (1994). Expression of maize KNOTTED1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot. Development 120: 405–413.
17. Johnston, R., Candela, H., Hake, S., and Foster, T. (2010). The maize milkweed pod1 mutant reveals a mechanism to modify organ morphology. Genesis 48: 416–423.
18. Keller, T., Abbott, J., Moritz, T., and Doerner, P. (2006). Arabidopsis REGULATOR OF AXILLARY MERISTEMS1 controls a leaf axil stem cell niche and modulates vegetative development. Plant Cell 18: 598–611.
19. Komatsu, K., Maekawa, M., Ujiie, S., Satake, Y., Furutani, I., Okamoto, H., Shimamoto, K., and Kyozuka, J. (2003). LAX and SPA: Major regulators of shoot branching in rice. Proc. Natl. Acad. Sci. USA 100: 11765–11770.
20. Kouchi, H., and Hata, S. (1993). Isolation and characterization of novel nodulin cDNAs representing genes expressed at early stages of soybean nodule development. Mol. Gen. Genet. 238: 106–119.
21. Lau, S., Slane, D., Herud, O., Kong, J., and Jürgens, G. (2012). Early embryogenesis in flowering plants: Setting up the basic body pattern. Annu. Rev. Plant Biol. 63: 483–506.
22. Laux, T., Mayer, K.F.X., Berger, J., and Jürgens, G. (1996). The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122: 87–96.
23. Li, X., et al. (2003). Control of tillering in rice. Nature 422: 618–621.
24. Lin, H., Niu, L., McHale, N.A., Ohme-Takagi, M., Mysore, K.S., and Tadege, M. (2013). Evolutionarily conserved repressive activity of WOX proteins mediates leaf blade outgrowth and floral organ development in plants. Proc. Natl. Acad. Sci. USA 110: 366–371.
25. Long, J., and Barton, M.K. (2000). Initiation of axillary and floral meristems in Arabidopsis. Dev. Biol. 218: 341–353.
26. Long, J.A., Moan, E.I., Medford, J.I., and Barton, M.K. (1996). A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379: 66–69.
27. Mayer, K.F., Schoof, H., Haecker, A., Lenhard, M., Jürgens, G., and Laux, T. (1998). Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95: 805–815.
28. Müller, D., Schmitz, G., and Theres, K. (2006). Blind homologous R2R3 Myb genes control the pattern of lateral meristem initiation in Arabidopsis. Plant Cell 18: 586–597.
29. Nagasaki, H., Itoh, J., Hayashi, K., Hibara, K., Satoh-Nagasawa, N., Nosaka, M., Mukouhata, M., Ashikari, M., Kitano, H., Matsuoka, M., Nagato, Y., and Sato, Y. (2007). The small interfering RNA production pathway is required for shoot meristem initiation in rice. Proc. Natl. Acad. Sci. USA 104: 14867–14871.
30. Nakata, M., and Okada, K. (2013). The leaf adaxial-abaxial boundary and lamina growth. Plants 2: 174–202.
31. Nardmann, J., and Werr, W. (2006). The shoot stem cell niche in angiosperms: Expression patterns of WUS orthologues in rice and maize imply major modifications in the course of mono- and dicot evolution. Mol. Biol. Evol. 23: 2492–2504.
32. Nardmann, J., and Werr, W. (2013). Symplesiomorphies in the WUSCHEL clade suggest that the last common ancestor of seed plants contained at least four independent stem cell niches. New Phytol. 199: 1081–1092.
33. Nardmann, J., Reisewitz, P., and Werr, W. (2009). Discrete shoot and root stem cell-promoting WUS/WOX5 functions are an evolutionary innovation of angiosperms. Mol. Biol. Evol. 26: 1745–1755.
34. Nardmann, J., Zimmermann, R., Durantini, D., Kranz, E., and Werr, W. (2007). WOX gene phylogeny in Poaceae: A comparative approach addressing leaf and embryo development. Mol. Biol. Evol. 24: 2474–2484.
35. Ohmori, Y., Tanaka, W., Kojima, M., Sakakibara, H., and Hirano, H.-Y. (2013). WUSCHEL-RELATED HOMEOBOX4 is involved in meristem maintenance and is negatively regulated by the CLE gene FCP1 in rice. Plant Cell 25: 229–241.
36. Oikawa, T., and Kyozuka, J. (2009). Two-step regulation of LAX PANICLE1 protein accumulation in axillary meristem formation in rice. Plant Cell 21: 1095–1108.
37. Pautler, M., Tanaka, W., Hirano, H.Y., and Jackson, D. (2013). Grass meristems I: Shoot apical meristem maintenance, axillary meristem determinacy and the floral transition. Plant Cell Physiol. 54: 302–312.
38. Sato, Y., Hong, S.K., Tagiri, A., Kitano, H., Yamamoto, N., Nagato, Y., and Matsuoka, M. (1996). A rice homeobox gene, OSH1, is expressed before organ differentiation in a specific region during early embryogenesis. Proc. Natl. Acad. Sci. USA 93: 8117–8122.
39. Satoh, H., Matsusaka, H., and Kumamaru, T. (2010). Use of N-methyl-N-nitrosourea treatment of fertilized egg cells for saturation mutagenesis of rice. Breed. Sci. 60: 475–485.
40. Schmitz, G., Tillmann, E., Carriero, F., Fiore, C., Cellini, F., and Theres, K. (2002). The tomato Blind gene encodes a MYB transcription factor that controls the formation of lateral meristems. Proc. Natl. Acad. Sci. USA 99: 1064–1069.
41. Schoof, H., Lenhard, M., Haecker, A., Mayer, K.F.X., Jürgens, G., and Laux, T. (2000). The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100: 635–644.
42. Schumacher, K., Schmitt, T., Rossberg, M., Schmitz, G., and Theres, K. (1999). The Lateral suppressor (Ls) gene of tomato encodes a new member of the VHIID protein family. Proc. Natl. Acad. Sci. USA 96: 290–295.
43. Sharman, B.C. (1945). Leaf and bud initiation in the Gramineae. Bot. Gaz. 106: 269–289.
44. Suzaki, T., Sato, M., Ashikari, M., Miyoshi, M., Nagato, Y., and Hirano, H.-Y. (2004). The gene FLORAL ORGAN NUMBER1 regulates floral meristem size in rice and encodes a leucine-rich repeat receptor kinase orthologous to Arabidopsis CLAVATA1. Development 131: 5649–5657.
45. Suzaki, T., Toriba, T., Fujimoto, M., Tsutsumi, N., Kitano, H., and Hirano, H.-Y. (2006). Conservation and diversification of meristem maintenance mechanism in Oryza sativa: Function of the FLORAL ORGAN NUMBER2 gene. Plant Cell Physiol. 47: 1591–1602.
46. Suzuki, T., Eiguchi, M., Kumamaru, T., Satoh, H., Matsusaka, H., Moriguchi, K., Nagato, Y., and Kurata, N. (2008). MNU-induced mutant pools and high performance TILLING enable finding of any gene mutation in rice. Mol. Genet. Genomics 279: 213–223.
47. Tabuchi, H., et al. (2011). LAX PANICLE2 of rice encodes a novel nuclear protein and regulates the formation of axillary meristems. Plant Cell 23: 3276–3287.
48. Taguchi-Shiobara, F., Yuan, Z., Hake, S., and Jackson, D. (2001). The fasciated ear2 gene encodes a leucine-rich repeat receptor-like protein that regulates shoot meristem proliferation in maize. Genes Dev. 15: 2755–2766.
49. Tanaka, W., Pautler, M., Jackson, D., and Hirano, H.Y. (2013). Grass meristems II: Inflorescence architecture, flower development and meristem fate. Plant Cell Physiol. 54: 313–324.
50. Uhrig, H., Marocco, A., Döring, H.-P., and Salamini, F. (1997). The clonal origin of the lateral meristem generating the ear shoot of maize. Planta 201: 9–17.
51. Wang, Q., Kohlen, W., Rossmann, S., Vernoux, T., and Theres, K. (2014a). Auxin depletion from the leaf axil conditions competence for axillary meristem formation in Arabidopsis and tomato. Plant Cell 26: 2068–2079.
52. Wang, Y., and Li, J. (2008). Molecular basis of plant architecture. Annu. Rev. Plant Biol. 59: 253–279.
53. Wang, Y., Wang, J., Shi, B., Yu, T., Qi, J., Meyerowitz, E.M., and Jiao, Y. (2014b). The stem cell niche in leaf axils is established by auxin and cytokinin in Arabidopsis. Plant Cell 26: 2055–2067.
54. Yadav, R.K., Perales, M., Gruel, J., Girke, T., Jönsson, H., and Reddy, G.V. (2011). WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Genes Dev. 25: 2025–2030.
55. Yang, F., Wang, Q., Schmitz, G., Müller, D., and Theres, K. (2012). The bHLH protein ROX acts in concert with RAX1 and LAS to modulate axillary meristem formation in Arabidopsis. Plant J. 71: 61–70.
56. Yoshida, A., Suzaki, T., Tanaka, W., and Hirano, H.-Y. (2009). The homeotic gene long sterile lemma (G1) specifies sterile lemma identity in the rice spikelet. Proc. Natl. Acad. Sci. USA 106: 20103–20108.
57. Zhang, X., Zong, J., Liu, J., Yin, J., and Zhang, D. (2010). Genome-wide analysis of WOX gene family in rice, sorghum, maize, Arabi-dopsis and poplar. J. Integr. Plant Biol. 52: 1016–1026.