Correlated retrograde and developmental regulons implicate multiple retrograde signals as coordinators of chloroplast development in maize

Abstract

Signals emanating from chloroplasts influence nuclear gene expression, but roles of retrograde signals during chloroplast development are unclear. To address this gap, we analyzed transcriptomes of four non-photosynthetic maize mutants and interpreted them in the context of transcriptome dynamics during normal leaf development. We analyzed two albino mutants lacking plastid ribosomes and two chlorotic mutants with thylakoid targeting or plastid transcription defects. The ~2700 differentially expressed genes fall into six major categories based on the polarity and mutant-specificity of the change. These distinct retrograde responses correlate with distinct developmental dynamics, with down-regulated genes expressed later in normal development and up-regulated genes acting early. Photosynthesis genes are down-regulated specifically in the albino mutants, whereas up-regulated genes are enriched for functions in chloroplast biogenesis and cytosolic translation. TOR signaling is elevated in plastid ribosome-deficient mutants and declines in concert with plastid ribosome buildup during leaf development. Our results implicate three plastid signals as integral players during photosynthetic differentiation. One signal requires plastid ribosomes and activates photosynthesis genes. A second signal reflects attainment of chloroplast maturity and represses chloroplast biogenesis genes. A third signal responds to nutrient consumption by developing chloroplasts and represses TOR, which down-regulates cell proliferation genes early in leaf development.