Light initiates chloroplast biogenesis by activating photosynthesis-associated genes encoded by not only the nuclear but also the plastidial genome, but how photoreceptors control plastidial gene expression remains enigmatic. Here we show that the photoactivation of phytochromes triggers the expression of photosynthesis-associated plastid-encoded genes (
Phytochromes initiate chloroplast biogenesis by activating genes encoding the photosynthetic apparatus, including photosynthesis-associated plastid-encoded genes (
- NSF-PAR ID:
- 10153418
- Publisher / Repository:
- Nature Publishing Group
- Date Published:
- Journal Name:
- Nature Communications
- Volume:
- 10
- Issue:
- 1
- ISSN:
- 2041-1723
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract PhAPG s) by stimulating the assembly of the bacterial-type plastidial RNA polymerase (PEP) into a 1000-kDa complex. Using forward genetic approaches, we identified REGULATOR OF CHLOROPLAST BIOGENESIS (RCB) as a dual-targeted nuclear/plastidial phytochrome signaling component required for PEP assembly. Surprisingly, RCB controlsPhAPG expression primarily from the nucleus by interacting with phytochromes and promoting their localization to photobodies for the degradation of the transcriptional regulators PIF1 and PIF3. RCB-dependent PIF degradation in the nucleus signals the plastids for PEP assembly andPhAPG expression. Thus, our findings reveal the framework of a nucleus-to-plastid anterograde signaling pathway by which phytochrome signaling in the nucleus controls plastidial transcription. -
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Abstract Sigma factor (
SIG ) proteins contribute to promoter specificity of the plastid‐encodedRNA polymerase during chloroplast genome transcription. All six members of theSIG family, that is,SIG 1–SIG 6, are nuclear‐encoded proteins targeted to chloroplasts. Sigma factor 2 (SIG 2) is a phytochrome‐regulated protein important for stoichiometric control of the expression of plastid‐ and nuclear‐encoded genes that impact plastid development and plant growth and development. AmongSIG factors,SIG 2 is required not only for transcription of chloroplast genes (i.e., anterograde signaling), but also impacts nuclear‐encoded, photosynthesis‐related, and light signaling‐related genes (i.e., retrograde signaling) in response to plastid functional status. AlthoughSIG 2 is involved in photomorphogenesis in Arabidopsis, the molecular bases for its role in light signaling that impacts photomorphogenesis and aspects of photosynthesis have only recently begun to be investigated. Previously, we reported thatSIG 2 is necessary for phytochrome‐mediated photomorphogenesis specifically under red (R) and far‐red light, thereby suggesting a link between phytochromes and nuclear‐encodedSIG 2 in light signaling. To explore transcriptional roles ofSIG 2 in R‐dependent growth and development, we performedRNA sequencing analysis to compare gene expression insig2‐2 mutant and Col‐0 wild‐type seedlings at two developmental stages (1‐ and 7‐day). We identified a subset of misregulated genes involved in growth, hormonal cross talk, stress responses, and photosynthesis. To investigate the functional relevance of these gene expression analyses, we performed several comparative phenotyping tests. In these analyses, strongsig2 mutants showed insensitivity to bioactiveGA 3, high intracellular levels of hydrogen peroxide (H2O2) indicative of a stress response, and specific defects in photosynthesis, including elevated levels of cyclic electron flow (CEF ) and nonphotochemical quenching (NPQ ). We demonstrated thatSIG 2 regulates a broader range of physiological responses at the molecular level than previously reported, with specific roles in red‐light‐mediated photomorphogenesis. -
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Premise Light is critical in the ability of plants to accumulate chlorophyll. When exposed to far‐red (
FR ) light and then grown in white light in the absence of sucrose, wild‐type seedlings fail to green in a response known as theFR block of greening (BOG ). This response is controlled by phytochrome A through repression of protochlorophyllide reductase‐encoding (POR ) genes byFR light coupled with irreversible plastid damage. Sigma (SIG ) factors are nuclear‐encoded proteins that contribute to plant greening and plastid development through regulating gene transcription in chloroplasts and impacting retrograde signaling from the plastid to nucleus.SIG s are regulated by phytochromes, and the expression of someSIG factors is reduced in phytochrome mutant lines, includingphyA . Given the association of phyA with theFR BOG and its regulation ofSIG factors, we investigated the potential regulatory role ofSIG factors in theFR BOG response.Methods We examined
FR BOG responses insig mutants, phytochrome‐deficient lines, and mutant lines for several phy‐associated factors. We quantified chlorophyll levels and examined expression of keyBOG ‐associated genes.Results Among six
sig mutants, only thesig6 mutant significantly accumulated chlorophyll afterFR BOG treatment, similar to thephyA mutant.SIG 6 appears to control protochlorophyllide accumulation by contributing to the regulation of tetrapyrrole biosynthesis associated with glutamyl‐tRNA reductase (HEMA 1) function, select phytochrome‐interacting factor genes (PIF4 andPIF6 ), andPENTA1 , which regulatesPORA mRNA translation afterFR exposure.Conclusions Regulation of
SIG6 plays a significant role in plant responses toFR exposure during theBOG response. -
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Abstract Light initiates chloroplast biogenesis in
Arabidopsis by eliminating PHYTOCHROME-INTERACTING transcription FACTORs (PIFs), which in turn de-represses nuclear photosynthesis genes, and synchronously, generates a nucleus-to-plastid (anterograde) signal that activates the plastid-encoded bacterial-type RNA polymerase (PEP) to transcribe plastid photosynthesis genes. However, the identity of the anterograde signal remains frustratingly elusive. The main challenge has been the difficulty to distinguish regulators from the plethora of necessary components for plastid transcription and other essential chloroplast functions, such as photosynthesis. Here, we show that the genome-wide induction of nuclear photosynthesis genes is insufficient to activate the PEP. PEP inhibition is imposed redundantly by multiple PIFs and requires PIF3’s activator activity. Among the nuclear-encoded components of the PEP holoenzyme, we identify four light-inducible, PIF-repressed sigma factors as anterograde signals. Together, our results elucidate that light-dependent inhibition of PIFs activates plastid photosynthesis genes via sigma factors as anterograde signals in parallel with the induction of nuclear photosynthesis genes. -
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SUMMARY Plastids contain their own genomes, which are transcribed by two types of RNA polymerases. One of those enzymes is a bacterial‐type, multi‐subunit polymerase encoded by the plastid genome. The plastid‐encoded RNA polymerase (PEP) is required for efficient expression of genes encoding proteins involved in photosynthesis. Despite the importance of PEP, its DNA binding locations have not been studied on the genome‐wide scale at high resolution. We established a highly specific approach to detect the genome‐wide pattern of PEP binding to chloroplast DNA using plastid chromatin immunoprecipitation–sequencing (ptChIP‐seq). We found that in mature
Arabidopsis thaliana chloroplasts, PEP has a complex DNA binding pattern with preferential association at genes encoding rRNA, tRNA, and a subset of photosynthetic proteins. Sigma factors SIG2 and SIG6 strongly impact PEP binding to a subset of tRNA genes and have more moderate effects on PEP binding throughout the rest of the genome. PEP binding is commonly enriched on gene promoters, around transcription start sites. Finally, the levels of PEP binding to DNA are correlated with levels of RNA accumulation, which demonstrates the impact of PEP on chloroplast gene expression. Presented data are available through a publicly available Plastid Genome Visualization Tool (Plavisto) athttps://plavisto.mcdb.lsa.umich.edu/ .
