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GENOME ANALYSIS

Deregulation of Maize C₄ Photosynthetic Development in a Mesophyll Cell-Defective Mutant^{1,[C],[W],[OA]}

Department of Plant Biology (S.C., W.M., K.J.v.W.), and Boyce Thompson Institute for Plant Research (J.M.K., T.P.B.), Cornell University, Ithaca, New York 14853; and Department of Statistics, Iowa State University, Ames, Iowa 50011 (P.L.)

During maize (Zea mays) C₄ differentiation, mesophyll (M) and bundle sheath (BS) cells accumulate distinct sets of photosynthetic enzymes, with very low photosystem II (PSII) content in BS chloroplasts. Consequently, there is little linear electron transport in the BS and ATP is generated by cyclic electron flow. In contrast, M thylakoids are very similar to those of C₃ plants and produce the ATP and NADPH that drive metabolic activities. Regulation of this differentiation process is poorly understood, but involves expression and coordination of nuclear and plastid genomes. Here, we identify a recessive allele of the maize high chlorophyll fluorescence (Hcf136) homolog that in Arabidopsis (Arabidopsis thaliana) functions as a PSII stability or assembly factor located in the thylakoid lumen. Proteome analysis of the thylakoids and electron microscopy reveal that Zmhcf136 lacks PSII complexes and grana thylakoids in M chloroplasts, consistent with the previously defined Arabidopsis function. Interestingly, hcf136 is also defective in processing the full-length psbB-psbT-psbH-petB-petD polycistron specifically in M chloroplasts. To determine whether the loss of PSII in M cells affects C₄ differentiation, we performed cell-type-specific transcript analysis of hcf136 and wild-type seedlings. The results indicate that M and BS cells respond uniquely to the loss of PSII, with little overlap in gene expression changes between data sets. These results are discussed in the context of signals that may drive differential gene expression in C₄ photosynthesis.

² Present address: Department of Plant Pathology, Cornell University, Ithaca, NY 14853.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Thomas P. Brutnell (tpb8{at}cornell.edu).

^[C] Some figures in this article are displayed in color online but in black and white in the print edition.

^[W] The online version of this article contains Web-only data.

^[OA] Open Access articles can be viewed online without a subscription.

www.plantphysiol.org/cgi/doi/10.1104/pp.107.113423

^* Corresponding author; e-mail tpb8{at}cornell.edu.

Received November 18, 2007; accepted February 5, 2008; published February 7, 2008.

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