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 non-photosynthetic maize mutants and compared them to transcriptomes of stages of normal leaf development. The transcriptomes of two albino mutants lacking plastid ribosomes resembled transcriptomes at very early stages of normal leaf development, whereas the transcriptomes of two chlorotic mutants with thylakoid targeting or plastid transcription defects resembled those at a slightly later stage. We identified ∼2,700 differentially expressed genes, which fall into six major categories based on the polarity and mutant-specificity of the change. Downregulated genes were generally expressed late in normal development and were enriched in photosynthesis genes, whereas upregulated genes act early and were enriched for functions in chloroplast biogenesis and cytosolic translation. We showed further that TOR signaling was elevated in mutants lacking plastid ribosomes and declined in concert with plastid ribosome buildup during normal leaf development. Our results implicate three plastid signals as coordinators of 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, the consumption of nutrients by developing chloroplasts, represses TOR, promoting termination of cell proliferation during leaf development.

GhCTSF1, a short PPR protein with a conserved role in chloroplast development and photosynthesis, participates in intron splicing of rpoC1 and ycf3-2 transcripts in cotton

“…Ribosome enrichment in GhCTSF1 -silenced plants reflects crosstalk between the nucleus and chloroplast. In addition, photosynthetic damage signals that originate from the plastids influence nuclear gene expression ( Kendrick et al., 2022 ; Zhang et al., 2023a ).…”

Co-expression network of heat-response transcripts: A glimpse into how splicing factors impact rice basal thermotolerance

“…This hypothesis is particularly interesting in light of recent studies on chloroplast retrograde signals (CRS), which is a plastid-to-nucleus signalling mechanism that can regulate nuclear gene expression, especially in response to stress, including HS ( Song et al, 2021 ). CRS was shown to regulate AS of splicing factor AtSR30 ( Petrillo et al, 2014 ) and transcription of ZmGLK1 ( Kendrick et al, 2022 ). The rice orthologues of both SR30 and GLK are present in our robust splicing network, as well as many other chloroplast-related genes, which, if taken together with the information on CRS, allow us to suggest the existence of an important AS- and CRS-dependent feedback loop of HS responses between the chloroplast and the nucleus.…”