ABNORMAL SHOOT IN YOUTH, a Homolog of Molybdate Transporter Gene, Regulates Early Shoot Development in Rice

Ken-Ichiro Hibara, Wataru Hosoki, Tsuneo Hakoyama, Yoshihiro Ohmori, Toru Fujiwara, Jun-Ichi Itoh, Yasuo Nagato

Graduate School of Agricultural and Life Sciences, University of Tokyo, Tokyo, Japan..

DOI: 10.4236/ajps.2013.45A001                

Abstract

We analyzed the abnormal shoot in youth (asy) mutant to understand the phase-specific regulation of shoot development. asy showed various shoot abnormalities, including small leaves due to the precocious termination of cell division, defects in leaf blade-sheath boundary formation, and abnormal shoot apical meristem maintenance at the early vegetative stage. These defects recovered with advanced development. ASY encodes a DUF791 domain protein, which is part of the major facilitator superfamily. Despite stage-specific phenotypes, the ASY expression level was roughly constant throughout development. A paralog of ASY, ASL, exists in the rice genome and is supposed to have redundant functions. ASL expression was relatively low in early-stage embryos but increased at later stages. Thus, asy phenotypes were limited to the stage when ASL expression was suppressed. A homology search revealed that ASY is a homolog of the Chlamydomonas CrMoT2 gene, which encodes a molybdate transporter. ASY was suggested to encode a molybdate transporter based on its sequence similarity with CrMoT2 and predicted transmembrane topology. This is the first report of a CrMOT2-type molybdate transporter in higher plants.

Keywords

ABNORMAL SHOOT IN YOUTH; Early Vegetative Stage; Shoot Meristem; Rice; Molybdenum; Transporter

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	M. Aida, T. Ishida, H. Fukaki, H. Fujiwara and M. Tasaka, “Genes Involved in Organ Separation in Arabidopsis: An Analysis of the Cup-Shaped Cotyledon Mutant,” Plant Cell, Vol. 9, No. 6, 1997, pp. 841-857. doi:10.1105/tpc.9.6.841
[2]	M. Aida, T. Ishida and M. Tasaka, “Shoot Apical Meristem and Cotyledon Formation during Arabidopsis Embryogenesis: Interaction among the Cup-Shaped Cotyledon and Shoot Meristemless Genes,” Development, Vol. 126, 1999, pp. 1563-1570.
[3]	J. A. Long, E. I. Moan, J. I. Medford and M. K. Barton, “A Member of the Knotted Class Homeodomain Proteins Encoded by the STM Gene of Arabidopsis,” Nature, Vol. 379, No. 6560, 1996, pp. 66-69. doi:10.1038/379066a0
[4]	H. Nagasaki, J.-I. Itoh, K. Hayashi, K. Hibara, N. Satoh-Nagasawa, M. Nosaka, M. Mukouhata, M. Ashikari, K. Kitano, M. Matsuoka, Y. Nagato and Y. Sato, “Small Interfering RNA Production Pathway Is Required for Shoot Meristem Initiation in Rice,” Proceedings of the National Academy of Sciences of the United States of America, Vol. 104, No. 37, 2007, pp. 14867-14871. doi:10.1073/pnas.0704339104
[5]	M. Abe, T. Yoshikawa, M. Nosaka, H. Sakakibara, Y. Satoh, Y. Nagato and J.-I. Itoh, “Wavy Leaf1, an Ortholog of Arabidopsis HEN1, Regulates Shoot Development by Maintaining microRNA and Trans-Acting siRNA Accumulation in Rice,” Plant Physiology, Vol. 154, No. 3, 2010, pp. 1335-1346. doi:10.1104/pp.110.160234
[6]	U. Brand, J. C. Fletcher, M. Hobe, E. M. Meyerowitz and R. Simon, “Dependence of Stem Cell Fate in Arabidopsis on a Feedback Loop Regulated by CLV3 Activity,” Science, Vol. 289, No. 5479, 2000, pp. 617-619. doi:10.1126/science.289.5479.617
[7]	H. Schoof, M. Lenhard, A. Haecker, K. F. X. Mayer, G. Jurgens and T. Laux, “The Stem Cell Population of Arabidopsis Shoot Meristems Is Maintained by a Regulatory Loop between the Clavata and Wuschel Genes,” Cell, Vol. 100, No. 6, 2000, pp. 635-644. doi:10.1016/S0092-8674(00)80700-X
[8]	H. Kaya, K. I. Shibahara, K. I. Taoka, M. Iwabuchi, B. Stillman and T. Araki, “Fasciata Genes for Chromatin Assembly Factor-1 in Arabidopsis Maintain the Cellularorganization of Apical Meristems,” Cell, Vol. 104, No. 1, 2001, pp. 131-142. doi:10.1016/S0092-8674(01)00197-0
[9]	M. Abe, H. Kuroshita, M. Umeda, J.-I. Itoh and Y. Nagato, “The Rice Flattened Shoot Meristem, Encoding CAF-1 p150 Subunit, Is Required for Meristem Maintenance by Regulating the Cell-Cycle Period,” Developmental Biology, Vol. 319, 2008, pp. 384-393. doi:10.1016/j.ydbio.2008.04.040
[10]	R. S. Poethig, “Phase Change and the Regulation of Shoot Morphogenesis in Plants,” Science, Vol. 250, No. 4983, 1990, pp. 923-930. doi:10.1126/science.250.4983.923
[11]	E. J. Lawson and R. S. Poethig, “Shoot Development in Plants: Time for a Change,” Trends in Genetics, Vol. 11, No. 7, 1995, pp. 263-268. doi:10.1016/S0168-9525(00)89072-1
[12]	K. Asai, N. Satoh, H. Sasaki, H. Satoh and Y. Nagato, “A Rice Heterochronic Mutant, mori1, Is Defective in the Juvenile-Adult Phase Change,” Development, Vol. 12, 2002, pp. 265-273.
[13]	C. Hunter, H. Sun and R. S. Poethig, “The Arabidopsis Heterochronic Gene Zippy Is an Argonaute Family Member,” Genes & Development, Vol. 18, 2003, pp. 2368- 2379.
[14]	G. Chuck, A. M. Cigan, K. Saeteurn and S. Hake, “The Heterochronic Maize Mutant Corngrass1 Results from Over-Expression of a Tandem microRNA,” Nature Genetics, Vol. 39, 2007, pp. 544-549. doi:10.1038/ng2001
[15]	G. Wu, M. Y. Park, S. R. Conway, J. W. Wang, D. Weigel and R. S. Poethig, “The Sequential Action of miR156 and miR172 Regulates Developmental Timing in Arabidopsis,” Cell, Vol. 138, 2009, pp. 750-759. doi:10.1016/j.cell.2009.06.031
[16]	N. Tanaka, H. Ito, N. Sentoku, M. Kojima, H. Sakakibara, T. Izawa, J.-I. Itoh and Y. Nagato, “The COP1 Ortholog PPS Regulates the Juvenile-Adult and Vegetative-Reproductive Phase Changes in Rice,” Plant Cell, Vol. 23, 2011, pp. 2143-2154. doi:10.1105/tpc.111.083436
[17]	T. Murashige and F. Skoog, “A Revised Medium for Rapid Growth and Bioassays with Tobacco Tissue Cultures,” Physiologia Plantarum, Vol. 15, No. 3, 1962, pp. 473- 497. doi:10.1111/j.1399-3054.1962.tb08052.x
[18]	J. I. Itoh, H. Kitano, M. Matsuoka and Y. Nagato, “Shoot Organization Genes Regulate Shoot Apical Meristem Organization and the Pattern of Leaf Primordium Initiation in Rice,” Plant Cell, Vol. 12, No. 11, 2000, pp. 2161- 2174.
[19]	H. Kouchi and S. Hata, “Isolation and Characterization of Novel Nodulin cDNAs Representing Genes Expressed at Early Stages of Soybean Nodule Development,” Molecular Genetics and Genomics, Vol. 238, No. 1-2, 1993, pp. 106-119.
[20]	Y. Hiei, S. Ohta, T. Komari and T. Kumashiro, “Efficient Transformation of Rice (Oryza sativa L.) Mediated by Agrobacterium and Sequence Analysis of the Boundaries of the T-DNA,” The Plant Journal, Vol. 6, No. 2, 1994, pp. 271-282. doi:10.1046/j.1365-313X.1994.6020271.x
[21]	M. Jain, A. Nijhawan, A. K. Tyagi and J. P. Khurana, “Validation of Housekeeping Genes as Internal Control for Studying Gene Expression in Rice by Quantitative Real-Time PCR,” Biochemical and Biophysical Research Communications, Vol. 345, 2006, pp. 646-651. doi:10.1016/j.bbrc.2006.04.140
[22]	S. S. Pao, I. T. Paulsen and M. H. Saier, “Major Facilitator Superfamily,” Microbiology and Molecular Biology Reviews, Vol. 12, 1998, pp. 1-34.
[23]	M. Tejada-Jiménezl, A. Galván and E. Fernández, “Algae and Humans Share a Molybdate Transporter,” Proceedings of the National Academy of Sciences of the United States of America, Vol.108, No. 16, 2011, pp. 6420-6425. doi:10.1073/pnas.1100700108
[24]	H. Tomatsu, J. Takano, H. Takahashi, A. Watanabe-Takahashi, N. Shibagaki and T. Fujiwara, “An Arabidopsis Thaliana High-Affinity Molybdate Transporter Required for Efficient Uptake of Molybdate from Soil,” Proceedings of the National Academy of Sciences of the United States of America, Vol. 104, No. 47, 2007, pp. 18807-18812. doi:10.1073/pnas.0706373104
[25]	M. Tejada-Jimenez, A. Llamas, E. Sanz-Luque, A. Galvan and E. Fernandez, “A High-Affinity Molybdate Transporter in Eukaryotes,” Proceedings of the National Academy of Sciences of the United States of America, Vol. 104, 2007, pp. 20126-20130. doi:10.1073/pnas.0704646104
[26]	I. Baxter, B. Muthukumar, H. C. Park, P. Buchner, B. Lahner, J. Danku, K. Zhao, J. Lee, M. J. Hawkesford, M. L. Guerinot and D. E. Salt, “Variation in Molybdenum Content across Broadly Distributed Populations of Arabidopsis Thaliana Is Controlled by a Mitochondrial Molybdenum Transporter (MOT1),” PLoS Genetics, Vol. 4, 2008, Article ID: e1000004. doi:10.1371/journal.pgen.1000004
[27]	R. R. Mendel, “Cell Biology of Molybdenum in Plants,” Plant Cell Reports, Vol. 30, Vol. 10, 2011, pp. 1787-1797. doi:10.1007/s00299-011-1100-4
[28]	R. R. Mendel and T. Kruse, “Cell Biology of Molybdenum in Plants and Humans,” Biochimica et Biophysica Acta, Vol. 1823, No. 8, 2012, pp. 1568-1579. doi:10.1016/j.bbamcr.2012.02.007
[29]	Y. Ide, M. Kusano, A. Oikawa, A. Fukushima, H. Tomatsu, K. Saito, M. Yokota Hirai and T. Fujiwara, “Effects of Molybdenum Deficiency and Defects in Molybdate Transporter MOT1 on Transcript Accumulation and Nitrogen/Sulphur Metabolism in Arabidopsis thaliana,” Journal of Experimental Botany, Vol. 62, 2010, pp. 1-15.