Abstract
Members of the YABBY gene family have a general role that promotes abaxial cell fate in a model eudicot, Arabidopsis thaliana. To understand the function of YABBY genes in monocots, we have isolated all YABBY genes in Oryza sativa (rice), and revealed the spatial and temporal expression pattern of one of these genes, OsYABBY1. In rice, eight YABBY genes constitute a small gene family and are classified into four groups according to sequence similarity, exon–intron structure, and organ-specific expression patterns. OsYABBY1 shows unique spatial expression patterns that have not previously been reported for other YABBY genes, so far. OsYABBY1 is expressed in putative precursor cells of both the mestome sheath in the large vascular bundle and the abaxial sclerenchyma in the leaves. In the flower, OsYABBY1 is specifically expressed in the palea and lemma from their inception, and is confined to several cell layers of these organs in the later developmental stages. The OsYABBY1-expressing domains are closely associated with cells that subsequently differentiate into sclerenchymatous cells. These findings suggest that the function of OsYABBY1 is involved in regulating the differentiation of a few specific cell types and is unrelated to polar regulation of lateral organ development.
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References
Altschul SF, Madden TL, Schäfer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Alvarez J, Smyth DR (1999) CRABS CLAW and SPATULA, two Arabidopsis genes that control carpel development in parallel with AGAMOUS. Development 126:2377–2386
Bommert P, Satoh-Nagasawa N, Jackson D, Hirano HY (2005) Genetics and evolution of inflorescence and flower development in grasses. Plant Cell Physiol 46:69–78
Bowman JL (2000) The YABBY gene family and abaxial cell fate. Curr Opin Plant Biol 3:17–22
Bowman JL, Smyth DR (1999) CRABS CLAW, a gene that regulates carpel and nectary development in Arabidopsis, encodes a novel protein with zinc finger and helix-loop-helix domains. Development 126:2387–2396
Chen Q, Atkinson A, Otsuga D, Christensen T, Reynolds L, Drews GN (1999) The Arabidopsis FILAMENTOUS FLOWER gene is required for flower formation. Development 126:2715–2726
Eshed Y, Baum SF, Bowman JL (1999) Distinct mechanisms promote polarity establishment in carpels of Arabidopsis. Cell 99:199–209
Floyd SK, Bowman JL (2007) The ancestral developmental tool kit of land plants. Int J Plant Sci 168:1–35
Fourquin C, Vinauger-Douard M, Fogliani B, Dumas C, Scutt CP (2005) Evidence that CRABS CLAW and TOUSLED have conserved their roles in carpel development since the ancestor of the extant angiosperms. Proc Natl Acad Sci USA 102:4649–4654
Gleissberg S, Groot EP, Schmalz M, Eichert M, Kölsch A, Hutter S (2005) Developmental events leading to peltate leaf structure in Tropaeolum majus (Tropaeolaceae) are associated with expression domain changes of a YABBY gene. Dev Genes Evol 215:313–319
Golz JF, Roccaro M, Kuzoff R, Hudson A (2004) GRAMINIFOLIA promotes growth and polarity of Antirrhinum leaves. Development 131:3661–3670
Hoshikawa K (1989) Growing the rice plant: an anatomical monograph. Nobunkyo, Tokyo
Jang S, Hur J, Kim SJ, Han MJ, Kim SR, An G (2004) Ectopic expression of OsYAB1 causes extra stamens and carpels in rice. Plant Mol Biol 56:133–143
Juarez MT, Kui JS, Thomas J, Heller BA, Timmermans MCP (2004a) microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 428:84–88
Juarez MT, Twigg RW, Timmermans MCP (2004b) Specification of adaxial cell fate during maize leaf development. Development 131:4533–4544
Kanaya E, Nakajima N, Okada K (2002) Non-sequence-specific DNA binding by the FILAMENTOUS FLOWER protein from Arabidopsis thaliana is reduced by EDTA. J Biol Chem 277:11957–11964
Lee JY, Baum SF, Oh SH, Jiang CZ, Chen JC, Bowman JL (2005) Recruitment of CRABS CLAW to promote nectary development within the eudicot clade. Development 132:5021–5032
Matsuo T, Hoshikawa K (1993) Science of the rice plant. Food and Agriculture Policy Research Center, Tokyo
Meister RJ, Kotow LM, Gasser CS (2002) SUPERMAN attenuates positive INNER NO OUTER autoregulation to maintain polar development of Arabidopsis ovule outer integuments. Development 129:4281–4289
Navarro C, Efremova N, Golz JF, Rubiera R, Kuckenberg M, Castillo R, Tietz O, Saedler H, Schwarz-Sommer Z (2004) Molecular and genetic interactions between STYLOSA and GRAMINIFOLIA in the control of Antirrhinum vegetative and reproductive development. Development 131:3649–3659
Olsen AN, Ernst HA, Lo Leggio L, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10:79–87
Prasad K, Parameswaran S, Vijayraghavan U (2005) OsMADS1, a rice MADS-box factor, controls differentiation of specific cell types in the lemma and palea and is an early-acting regulator of inner floral organs. Plant J 43:915–928
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Sawa S, Ito T, Shimura Y, Okada K (1999a) FILAMENTOUS FLOWER controls the formation and development of Arabidopsis inflorescences and floral meristems. Plant Cell 11:69–86
Sawa S, Watanabe K, Goto K, Kanaya E, Morita EH, Okada K (1999b) FILAMENTOUS FLOWER, a meristem and organ identity gene of Arabidopsis, encodes a protein with a zinc finger and HMG-related domains. Genes Dev 13:1079–1088
Siegfried KR, Eshed Y, Baum SF, Otsuga D, Drews GN, Bowman JL (1999) Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development 126:4117–4128
Suzaki T, Sato M, Ashikari M, Miyoshi M, Nagato Y, 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
Tanabe Y, Hasebe M, Sekimoto H, Nishiyama T, Kitani M, Henschel K, Munster T, Theissen G, Nozaki H, Ito M (2005) Characterization of MADS-box genes in charophycean green algae and its implication for the evolution of MADS-box genes. Proc Natl Acad Sci USA 102:2436–2441
Theissen G, Becker A, Di Rosa A, Kanno A, Kim JT, Munster T, Winter KU, Saedler H (2000) A short history of MADS-box genes in plants. Plant Mol Biol 42:115–149
Toki S, Hara N, Ono K, Onodera H, Tagiri A, Oka S, Tanaka H (2006) Early infection of scutellum tissue with Agrobacterium allows high-speed transformation of rice. Plant J 47:969–976
Villanueva JM, Broadhvest J, Hauser BA, Meister RJ, Schneitz K, Gasser CS (1999) INNER NO OUTER regulates abaxial- adaxial patterning in Arabidopsis ovules. Genes Dev 13:3160–3169
Watanabe K, Okada K (2003) Two discrete cis elements control the abaxial side-specific expression of the FILAMENTOUS FLOWER gene in Arabidopsis. Plant Cell 15:2592–2602
Yamada T, Ito M, Kato M (2003) Expression pattern of INNER NO OUTER homologue in Nymphaea (water lily family, Nymphaeaceae). Dev Genes Evol 213:510–513
Yamada T, Ito M, Kato M (2004) YABBY2-homologue expression in lateral organs of Amborella trichopoda (Amborellaceae). Int J Plant Sci 165:917–924
Yamaguchi T, Hirano HY (2006) Function and diversification of MADS-box genes in rice. TSW Dev Embryol 1:99–108
Yamaguchi T, Nagasawa N, Kawasaki S, Matsuoka M, Nagato Y, Hirano H-Y (2004) The YABBY gene DROOPING LEAF regulates carpel specification and midrib development in Oryza sativa. Plant Cell 16:500–509
Zhao W, Su HY, Song J, Zhao XY, Zhang XS (2006) Ectopic expression of TaYAB1, a member of YABBY gene family in wheat, causes the partial abaxialization of the adaxial epidermises of leaves and arrests the development of shoot apical meristem in Arabidopsis. Plant Sci 170:364–371
Acknowledgments
We thank K. Ohsawa for technical assistance. This research was partly supported by Grants-in-Aid for Scientific Research (14036265, 17027009, 17208002) from the Ministry of Education, Culture, Sports, Science and Technology.
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Communicated by R. Hagemann.
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Toriba, T., Harada, K., Takamura, A. et al. Molecular characterization the YABBY gene family in Oryza sativa and expression analysis of OsYABBY1 . Mol Genet Genomics 277, 457–468 (2007). https://doi.org/10.1007/s00438-006-0202-0
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DOI: https://doi.org/10.1007/s00438-006-0202-0