The nucleoid-associated protein WHIRLY1 is required for the coordinate assembly of plastid and nucleus-encoded proteins during chloroplast development.

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CONCLUSION: Chloroplasts deficient in the major chloroplast nucleoid-associated protein WHIRLY1 have an enhanced ratio of LHCs to reaction centers, indicating that WHIRLY1 is required for a coordinate assembly of the photosynthetic apparatus during chloroplast development. Chloroplast development was found to be delayed in barley plants with an RNAi-mediated knockdown of WHIRLY1 encoding a major nucleoid-associated protein of chloroplasts. The plastids of WHIRLY1 deficient plants had a reduced ribosome content. Accordingly, plastid-encoded proteins of the photosynthetic apparatus showed delayed accumulation during chloroplast development coinciding with a delayed increase in photosystem II efficiency measured by chlorophyll fluorescence. In contrast, light harvesting complex proteins being encoded in the nucleus had a high abundance as in the wild type. The unbalanced assembly of the proteins of the photosynthetic apparatus in WHIRLY1-deficient plants coincided with the enhanced contents of chlorophyll b and xanthophylls. The lack of coordination was most obvious at the early stages of development. Overaccumulation of LHC proteins in comparison to reaction center proteins at the early stages of chloroplast development did not correlate with enhanced expression levels of the corresponding genes in the nucleus. This work revealed that WHIRLY1 does not influence LHC abundance at the transcriptional level. Rather, WHIRLY1 in association with nucleoids might play a structural role for both the assembly of ribosomes and the complexes of the photosynthetic apparatus.