First published online May 7, 2004; 10.1104/pp.103.036996
Plant Physiology 135:471-482 (2004)
© 2004 American Society of Plant Biologists
GENETICS, GENOMICS, AND MOLECULAR EVOLUTION
CHLOROPLAST BIOGENESIS Genes Act Cell and Noncell Autonomously in Early Chloroplast Development1
María de la Luz Gutiérrez-Nava2,3,
C. Stewart Gillmor2,3,
Luis F. Jiménez,
Arturo Guevara-García and
Patricia León*
Departamento de Biología Molecular de Plantas, Instituto de Biotecnología, Universidad Nacional Autónoma de Mexico, Cuernavaca, Morelos 62271, Mexico (M.G.-N., A.G.-G., P.L.); Department of Plant Biology, Carnegie Institution of Washington (C.S.G.) and Department of Biological Sciences (C.S.G.), Stanford University, Stanford, California, 94305; and Laboratorio de Microscopía Electrónica, Facultad de Ciencias, Universidad Nacional Autónoma de Mexico, Mexico D.F. 04510, Mexico (L.F.J.)
In order to identify nuclear genes required for early chloroplast development, a collection of photosynthetic pigment mutants of Arabidopsis was assembled and screened for lines with extremely low levels of chlorophyll. Nine chloroplast biogenesis (clb) mutants that affect proplastid growth and thylakoid membrane formation and result in an albino seedling phenotype were identified. These mutations identify six new genes as well as a novel allele of cla1. clb mutants have less than 2% of wild-type chlorophyll levels, and little or no expression of nuclear and plastid-encoded genes required for chloroplast development and function. In all but one mutant, proplastids do not differentiate enough to form elongated stroma thylakoid membranes. Analysis of mutants during embryogenesis allows differentiation between CLB genes that act noncell autonomously, where partial maternal complementation of chloroplast development is observed in embryos, and those that act cell autonomously, where complementation during embryogenesis is not observed. Molecular characterization of the noncell autonomous clb4 mutant established that the CLB4 gene encodes for hydroxy-2-methyl-2-(E)-butenyl 4-diphosphate synthase (HDS), the next to the last enzyme of the methylerythritol 4-phosphate (MEP) pathway for the synthesis of plastidic isoprenoids. The noncell autonomous nature of the clb4 mutant suggests that products of the MEP pathway can travel between tissues, and provides in vivo evidence that some movement of MEP intermediates exists from the cytoplasm to the plastid. The isolation and characterization of clb mutants represents the first systematic study of genes required for early chloroplast development in Arabidopsis.
1 This work was supported by CONACYT (31791–N), DGAPA IN210200, BASF, and Howard Hughes grants. M.G.-N. was supported by fellowships from CONACYT, SNI, the Wood-Whelan Research Foundation, and by a UNESCO Short-Term Biotechnology Fellowship. C.S.G. was partially supported by a U.S. Department of Energy/National Science Foundation/U.S. Department of Agriculture tri-agency training grant, and by a grant from the U.S. Department of Energy (DE–FG02–97ER20133) to C.R. Somerville (Carnegie Institution of Washington, Department of Plant Biology).
2 These authors contributed equally to the paper.
3 Present address: Applied Biotechnology Center, CIMMYT (International Maize and Wheat Improvement Center), Apartado 6–641, Mexico D.F. 06600, Mexico.
Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.103.036996.
* Corresponding author; e-mail patricia{at}ibt.unam.mx; fax 52–73–139988.
Received November 30, 2003;
returned for revision February 3, 2004;
accepted February 11, 2004.
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