Abstract

During maize (Zea mays) C(4) 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 C(3) 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 C(4) 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 C(4) photosynthesis.

Highlights

  • 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

  • The Zmhcf136 mutant was first identified in sand bench screens of an Ac-mutagenized population as a recessive hcf seedling-lethal mutant

  • Initial BLAST searches revealed that this fragment has significant similarity to the Arabidopsis (Arabidopsis thaliana) gene HCF136, suggesting the Ac inserted into an exon of a maize Hcf136 homolog

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Summary

Introduction

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. 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. M cells contain both PSII and PSI activities and perform linear photosynthetic electron transport (PET). M celldefective mutants that lack PSII are unable to generate electron flow and likely result in overly oxidized linear PET chains. Both of these mutant classes will fail to accumulate soluble sugars due to the absence of photosynthesis. Mutations that disrupt the cellular environments of M and BS cells may provide useful tools for probing the differentiation process

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