Leaf cells undergo two main developmental events; i.e., cell proliferation and cell differentiation, before maturation. These events occur sequentially at specific positions and with specific timing during leaf development. To understand the transition from cell proliferation to cell differentiation of rice leaves, we analyzed rice leaves from both morphological and molecular viewpoints. The results of anatomical, morphological, and histochemical analyses indicated that P4 leaf primordium is the stage when dynamic transition of the cellular state from immature to mature along the proximal-distal axis of the leaf occurs. We screened for marker genes showing a dynamic expression pattern along the proximal-distal axis of the P4 leaf, and applied them to expression analysis in wild-type and various morphogenetic mutants. The changes in expression pattern of the marker genes varied between developmental stages and between mutants. Our analysis reinforced previous data regarding the developmental transition of wild-type rice leaves and indicated that the transition can be monitored using our molecular markers. The results of this study indicate that expression analysis using these molecular markers would be valuable for understanding the genetic effects on leaf development in various leaf morphogenetic mutants.
Endo, M., Nakayama, S., Umeda-Hara, C., Ohtsuki, N., Saika, H., Umeda, M. and Toki, S. (2012) CDKB2 Is Involved in Mitosis and DNA Damage Response in Rice. Plant Journal, 69, 967-977. http://dx.doi.org/10.1111/j.1365-313X.2011.04847.x
Lee, J., Das, A., Yamaguchi, M., Hashimoto, J., Tsutsumi, N., Uchimiya, H. and Umeda, M. (2003) Cell Cycle Function of a Rice B2-Type Cyclin Interacting with a B-Type Cyclin-Dependent Kinase. Plant Journal, 34, 417-425. http://dx.doi.org/10.1046/j.1365-313X.2003.01736.x
Gonzalez, N., Vanhaeren, H. and Inzé, D. (2012) Leaf Size Control: Complex Coordination of Cell Division and Expansion. Trends in Plant Science, 17, 332-340. http://dx.doi.org/10.1016/j.tplants.2012.02.003
Verkest, A., Manes, C.L., Vercruysse, S., Maes, S., Schueren, E.V.D., Beeckman, T., Genschik, P., Kuiper, M, Inzé, D. and Veyldera, L.D. (2005) The Cyclin-Dependent Kinase Inhibitor KRP2 Controls the Onset of the Endoreduplication Cycle during Arabidopsis Leaf Development through Inhibition of Mitotic CDKA;1 Kinase Complexes. Plant Cell, 17, 1723-1736. http://dx.doi.org/10.1105/tpc.105.032383
Li, C., Potuschak, T., Colon-Carmona, A., Gutiérrez, R.A. and Doerner, P. (2005) Arabidopsis TCP20 Links Regulation of Growth and Cell Division Control Pathways. Proceedings of the National Academy of Sciences of the United States of America, 102, 12978-12983. http://dx.doi.org/10.1073/pnas.0504039102
Kim, J.H., Choi, D. and Kende, H. (2003) The AtGRF Family of Putative Transcription Factors Is Involved in Leaf and Cotyledon Growth in Arabidopsis. Plant Journal, 36, 94-104. http://dx.doi.org/10.1046/j.1365-313X.2003.01862.x
Liu, D., Song, Y., Chen, Z., and Yua, D. (2009). Ectopic Expression of miR396 Suppresses GRF Target Gene Expression and Alters Leaf Growth in Arabidopsis. Physiologia Plantarum, 136, 223-236. http://dx.doi.org/10.1111/j.1399-3054.2009.01229.x
Mecchia, M.A., Debernardi, J.M., Rodriguez, R.E., Schommer, C. and Palatnik, J.F. (2013) MicroRNA miR396 and RDR6 Synergistically Regulate Leaf Development. Mechanisms of Development, 130, 2-13. http://dx.doi.org/10.1016/j.mod.2012.07.005
Rodriguez, R.E., Mecchia, M.A., Debernardi, J.M., Schommer, C., Weigel, D. and Palatnik, J.F. (2010) Control of Cell Proliferation in Arabidopsis thaliana by microRNA miR396. Development, 137, 103-112. http://dx.doi.org/10.1242/dev.043067
Ichihashi, Y., Kawade, K., Usami, T., Horiguchi, G., Takahashi, T. and Tsukaya, H. (2011) Key Proliferative Activity in the Junction between the Leaf Blade and Leaf Petiole of Arabidopsis. Plant Physiology, 157, 1151-1162. http://dx.doi.org/10.1104/pp.111.185066
i>
GRF<
/i>
(<
i>
GROWTH-REGULATING FACTOR<
/i>
)
Li, P., Ponnala, L., Gandotra, N., Wang, L., Si, Y., Tausta, S.L., Kebrom, T.H., Provart, N., Patel, R., Myers, C.R., Reidel, E.J., Turgeon, R., Liu, P., Sun, Q., Nelson, T. and Brutnell, T.P. (2010) The Developmental Dynamics of the Maize Leaf Transcriptome. Nature Genetics, 42, 1060-1067. http://dx.doi.org/10.1038/ng.703
Nelson, T. (2011) The Grass Leaf Developmental Gradient as a Platform for a Systems Understanding of the Anatomical Specialization of C4 Leaves. Journal of Experimental Botany, 62, 3039-3048. http://dx.doi.org/10.1093/jxb/err072
Wang, L., Czedik-Eysenberg, A., Mertz, R.A., Si, Y., Tohge, T., Nunes-Nesi, A., Arrivault, S., Dedow, L.K., Bryant, D.W., Zhou, W., Xu, J., Weissmann, S., Studer, A., Li, P., Zhang, C., LaRue, T., Shao, Y., Ding, Z., Sun, Q., Patel, R.V., Turgeon, R., Zhu, X., Provart, N.J., Mockler, T.C., Fernie, A.R., Stitt, M., Liu, P. and Brutnell, T.P. (2014) Comparative Analyses of C4 and C3 Photosynthesis in Developing Leaves of Maize and Rice. Nature Biotechnology, 32, 1158-1165. http://dx.doi.org/10.1038/nbt.3019
Itoh, J.I., Nonomura, K.-I., Ikeda, K., Yamaki, S., Inukai, Y., Yamagishi, H., Kitano, H. and Nagato, Y. (2005) Rice Plant Development: From Zygote to Spikelet. Plant and Cell Physiology, 46, 23-47. http://dx.doi.org/10.1093/pcp/pci501
Lea, P.J. and Leegood II, R.C. (1999) Plant Biochemistry and Molecular Biology. John Wiley& Sons, Inc., New York, 364 p.
Boudet, A.M. (2000) Lignins and Lignification: Selected Issues. Plant Physiology and Biochemistry, 38, 81-96. http://dx.doi.org/10.1016/S0981-9428(00)00166-2
Evert III, R.F. (2006) Esau’s Plant Anatomy: Meristems, Cells, and Tissues of the Plant Body: Their Structure, Function, and Development. John Wiley&Sons, Inc., Hoboken, 601 p. http://dx.doi.org/10.1002/0470047380
Smith, R.A., Schuetz, M., Roach, M., Mansfield, S.D., Ellis, B. and Samuels, L. (2013) Neighboring Parenchyma Cells Contribute to Arabidopsis Xylem Lignification, While Lignification of Interfascicular Fibers Is Cell Autonomous. Plant Cell, 25, 3988-3999. http://dx.doi.org/10.1105/tpc.113.117176
Wang, Y., Chantreau, M., Sibout, R. and Hawkins, S. (2013) Plant Cell Wall Lignification and Monolignol Metabolism. Frontiers in Plant Science, 4, 1-14.
Morita, K., Hatanaka, T., Misoo, S. and Fukayama, H. (2014) Unusual Small Subunit That Is Not Expressed in Photosynthetic Cells Alters the Catalytic Properties of Rubisco in Rice. Plant Physiology, 164, 69-79. http://dx.doi.org/10.1104/pp.113.228015
Ogawa, S., Suzuki, Y., Yoshizawa, R., Kanno, K. and Makino, A. (2012) Effect of Individual Suppression of RBCS Multigene Family on Rubisco Contents in Rice Leaves. Plant, Cell & Environment, 35, 546-553. http://dx.doi.org/10.1111/j.1365-3040.2011.02434.x
Suzuki, Y., Ohkubo, M., Hatakeyama, H., Ohashi, K., Yoshizawa, R., Kojima, S., Hayakawa, T., Yamaya, T., Mae, T. and Makino, A. (2007) Increased Rubisco Content in Transgenic Rice Transformed with the “Sense” rbcS Gene. Plant and Cell Physiology, 48, 626-637. http://dx.doi.org/10.1093/pcp/pcm035
Sharma, R., Kapoor, M., Tyagi, A.K. and Kapoor, S. (2010) Comparative Transcript Profiling of TCP Family Genes Provide Insight into Gene Functions and Diversification in Rice and Arabidopsis. Journal of Plant Molecular Biology and Biotechnology, 1, 24-38.
Choi, D., Kim, J.H. and Kende, H. (2004) Whole Genome Analysis of the OsGRF Gene Family Encoding Plant-Specific Putative Transcription Activators in Rice (Oryza sativa L.). Plant and Cell Physiology, 45, 897-904. http://dx.doi.org/10.1093/pcp/pch098
Lee, J., Park, J.-J., Kim, S.L., Yim, J. and An, G. (2007) Mutations in the Rice Liguleless Gene Result in a Complete Loss of the Auricle, Ligule, and Laminar Joint. Plant Molecular Biology, 65, 487-499. http://dx.doi.org/10.1007/s11103-007-9196-1
Yamaguchi, T., Nagasawa, N., Kawasaki, S., Matsuoka, M., Nagato, Y. and Hirano, H.-Y. (2004) The YABBY Gene DROOPING LEAF Regulates Carpel Specification and Midrib Development in Oryza sativa. Plant Cell, 16, 500-509. http://dx.doi.org/10.1105/tpc.018044
Ohmori, Y., Toriba, T., Nakamura, H., Ichikawa, H. and Hirano, H.Y. (2011). Temporal and Spatial Regulation of DROOPING LEAF Gene Expression That Promotes Midrib Formation in Rice. Plant Journal, 65, 77-86. http://dx.doi.org/10.1111/j.1365-313X.2010.04404.x
Sakamoto, T., Kitano, H. and Fujioka, S. (2013) Genetic Background Influences Brassinosteroid-Related Mutant Phenotypes in Rice. American Journal of Plant Sciences, 4, 212-221. http://dx.doi.org/10.4236/ajps.2013.42028
Ueguchi-Tanaka, M., Fujisawa, Y., Kobayashi, M., Ashikari, M., Iwasaki, Y., Kitano, H. and Matsuoka, M. (2000) Rice Dwarf Mutant d1, Which Is Defective in the α Subunit of the Heterotrimeric G Protein, Affects Gibberellin Signal Transduction. Proceedings of the National Academy of Sciences of the United States of America, 97, 11638-11643.
Sakamoto, T., Miura, K., Itoh, H., Tatsumi, T., Ueguchi-Tanaka, M., Ishiyama, K., Kobayashi, M., Agrawal, G.K., Takeda, S., Abe, K., Miyao, A., Hirochika, H., Kitano, H., Ashikari, M. and Matsuoka, M. (2004) An Overview of Gibberellin Metabolism Enzyme Genes and Their Related Mutants in Rice. Plant Physiology, 134, 1642-1653. http://dx.doi.org/10.1104/pp.103.033696
Miyoshi, K., Ahn, B.O., Kawakatsu, T., Ito, Y., Itoh, J.I., Nagato, Y. and Kurata, N. (2004) PLASTOCHRON1, a Timekeeper of Leaf Initiation in Rice, Encodes Cytochrome P450. Proceedings of the National Academy of Sciences of the United States of America, 101, 875-880. http://dx.doi.org/10.1073/pnas.2636936100
Kawakatsu, T., Itoh, J., Miyoshi, K., Kurata, N., Alvarez, N., Veit, B. and Nagato, Y. (2006) PLASTOCHRON2 Regulates Leaf Initiation and Maturation in Rice. Plant Cell, 18, 612-625. http://dx.doi.org/10.1105/tpc.105.037622
Martín-Trillo, M. and Cubas, P. (2010) TCP Genes: A Family Snapshot Ten Years Later. Trends in Plant Science, 15, 31-39. http://dx.doi.org/10.1016/j.tplants.2009.11.003
Yao, X., Ma, H., Wang, J. and Zhang, D. (2007) Genome-Wide Comparative Analysis and Expression Pattern of TCP Gene Families in Arabidopsis thaliana and Oryza sativa. Journal of Integrative Plant Biology, 49, 885-897. http://dx.doi.org/10.1111/j.1744-7909.2007.00509.x
Kieffer, M., Master, V., Waites, R. and Davies, B. (2011) TCP14 and TCP15 Affect Internode Length and Leaf Shape in Arabidopsis. Plant Journal, 68, 147-158. http://dx.doi.org/10.1111/j.1365-313X.2011.04674.x
Liu, H., Guo, S., Xu, Y., Li, C., Zhang, Z., Zhang, D., Xu, S., Zhang, C. and Chong, K. (2014) OsmiR396d-Regulated OsGRFs Function in Floral Organogenesis in Rice through Binding to Their Targets OsJMJ706 and OsCR4. Plant Physiology, 165, 160-174. http://dx.doi.org/10.1104/pp.114.235564
Debernardi, J.M., Rodriguez, R.E., Mecchia, M.A. and Palatnik, J.F. (2012) Functional Specialization of the Plant miR396 Regulatory Network through Distinct microRNA-Target Interactions. PLoS Genetics, 8, e1002419. http://dx.doi.org/10.1371/journal.pgen.1002419
Sunkar, R., Girke, T., Jain, P.K. and Zhu, J.K. (2005) Cloning and Characterization of microRNAs from Rice. Plant Cell, 17, 1397-1411. http://dx.doi.org/10.1105/tpc.105.031682
Nakaya, M., Tsukaya, H., Murakami, N. and Kato, M. (2002) Brassinosteroids Control the Proliferation of Leaf Cells of Arabidopsis thaliana. Plant and Cell Physiology, 43, 239-244. http://dx.doi.org/10.1093/pcp/pcf024
Oki, K., Inaba, N., Kitagawa, K., Fujioka, S., Kitano, H., Fujisawa, Y., Kato, H. and Iwasaki, Y. (2009) Function of the α Subunit of Rice Heterotrimeric G Protein in Brassinosteroid Signaling. Plant and Cell Physiology, 50, 161-172. http://dx.doi.org/10.1093/pcp/pcn182