The Maize Golden2 Gene Defines a Novel Class of Transcriptional Regulators in Plants

In the C4 plant maize, three photosynthetic cell types differentiate: C4 bundle sheath, C4 mesophyll, and C3 mesophyll cells. C3 mesophyll cells represent the ground state, whereas C4 bundle sheath and C4 mesophyll cells are specialized cells that differentiate in response to light-induced positional signals. The Golden2 (G2) gene regulates plastid biogenesis in all photosynthetic cells during the C3 stages of development. However, G2 function is specifically committed to the differentiation of bundle sheath cell chloroplasts in C4 leaf blades. In this article, we report the isolation of G2-like (Glk) genes from maize and rice, providing evidence for a family of Glk genes in plants. The expression profiles of the rice Glk genes suggest that these genes may act redundantly to promote photosynthetic development in this C3 species. In maize, G2 and ZmGlk1 transcripts accumulate primarily in C4 bundle sheath and C4 mesophyll cells, respectively, suggesting a specific role for each gene in C4 differentiation. We show that G2 and ZmGLK1 both can transactivate reporter gene transcription and dimerize in yeast, which supports the idea that these proteins act as transcriptional regulators of cell-type differentiation processes.

[1]  B. Rost PHD: predicting one-dimensional protein structure by profile-based neural networks. , 1996, Methods in enzymology.

[2]  William D. Richardson,et al.  A short amino acid sequence able to specify nuclear location , 1984, Cell.

[3]  M. Freeling A conceptual framework for maize leaf development. , 1992, Developmental biology.

[4]  J. Langdale,et al.  Spatial regulation of photosynthetic development in C4 plants. , 1991, Trends in genetics : TIG.

[5]  J. Drapier,et al.  Biosynthesis of nitric oxide activates iron regulatory factor in macrophages. , 1993, The EMBO journal.

[6]  W. E. Splittstoesser,et al.  Glutamine synthesis in germinating seeds of Cucurbita moschata , 1971 .

[7]  Thomas L. Madden,et al.  Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. , 1997, Nucleic acids research.

[8]  J. Langdale,et al.  bundle sheath defective2, a Mutation That Disrupts the Coordinated Development of Bundle Sheath and Mesophyll Cells in the Maize Leaf. , 1996, The Plant cell.

[9]  G. Edwards,et al.  C3, C4: Mechanisms and Cellular and Environmental Regulation of Photosynthesis , 1983 .

[10]  M. Kanehisa,et al.  A knowledge base for predicting protein localization sites in eukaryotic cells , 1992, Genomics.

[11]  R. Martienssen,et al.  Copying out our ABCs: the role of gene redundancy in interpreting genetic hierarchies. , 1999, Trends in genetics : TIG.

[12]  C. Murre,et al.  Helix-Loop-Helix Proteins: Regulators of Transcription in Eucaryotic Organisms , 2000, Molecular and Cellular Biology.

[13]  W. Brown Leaf Anatomy in Grass Systematics , 1958, Botanical Gazette.

[14]  S. Kirchanski THE ULTRASTRUCTURAL DEVELOPMENT OF THE DIMORPHIC PLASTIDS OF ZEA MAYS L. , 1975 .

[15]  B. Gaut,et al.  DNA sequence evidence for the segmental allotetraploid origin of maize. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[16]  Malmqvist,et al.  Epitope Mapping by Label-Free Biomolecular Interaction Analysis , 1996, Methods.

[17]  T. Mizuno,et al.  Compilation and characterization of Arabidopsis thaliana response regulators implicated in His-Asp phosphorelay signal transduction. , 1999, Plant & cell physiology.

[18]  P. Moore Evolution of photosynthetic pathways in flowering plants , 1982, Nature.

[19]  R. Laskey,et al.  Two interdependent basic domains in nucleoplasmin nuclear targeting sequence: Identification of a class of bipartite nuclear targeting sequence , 1991, Cell.

[20]  T. Aoyama,et al.  Arabidopsis ARR1 and ARR2 response regulators operate as transcriptional activators. , 2000, The Plant journal : for cell and molecular biology.

[21]  S. Dellaporta,et al.  Urea-based Plant DNA Miniprep , 1994 .

[22]  C. Kidner,et al.  bundle sheath defective, a mutation that disrupts cellular differentiation in maize leaves , 1994 .

[23]  R. R. Samaha,et al.  Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. , 2000, Science.

[24]  J. Langdale,et al.  CONTROL OF CELLULAR DIFFERENTIATION IN MAIZE LEAVES , 1995 .

[25]  H. Bono,et al.  Two-component response regulators from Arabidopsis thaliana contain a putative DNA-binding motif. , 1998, Plant & cell physiology.

[26]  S. Mccouch,et al.  Inferences on the genome structure of progenitor maize through comparative analysis of rice, maize and the domesticated panicoids. , 1999, Genetics.

[27]  J. Langdale,et al.  GOLDEN 2: A Novel Transcriptional Regulator of Cellular Differentiation in the Maize Leaf , 1998, Plant Cell.

[28]  W. Brown VARIATIONS IN ANATOMY, ASSOCIATIONS, AND ORIGINS OF KRANZ TISSUE , 1975 .

[29]  J. Langdale,et al.  Cell position and light influence C4 versus C3 patterns of photosynthetic gene expression in maize. , 1988, The EMBO journal.

[30]  J. Langdale,et al.  Cellular pattern of photosynthetic gene expression in developing maize leaves. , 1988, Genes & development.

[31]  A. Grossman,et al.  Psr1, a nuclear localized protein that regulates phosphorus metabolism in Chlamydomonas. , 1999, Proceedings of the National Academy of Sciences of the United States of America.