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1. Phytochrome activates the plastid-encoded RNA polymerase for chloroplast biogenesis via nucleus-to-plastid signaling

   https://doi.org/10.1038/s41467-019-10518-0  

   Yoo, Chan Yul ; Pasoreck, Elise K. ; Wang, He ; Cao, Jun ; Blaha, Gregor M. ; Weigel, Detlef ; Chen, Meng ( June 2019 , Nature Communications)

   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 (PhAPGs) 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 controlsPhAPGexpression 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 andPhAPGexpression. 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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2. Anterograde signaling controls plastid transcription via sigma factors separately from nuclear photosynthesis genes

   https://doi.org/10.1038/s41467-022-35080-0  

   Hwang, Youra ; Han, Soeun ; Yoo, Chan Yul ; Hong, Liu ; You, Chenjiang ; Le, Brandon H. ; Shi, Hui ; Zhong, Shangwei ; Hoecker, Ute ; Chen, Xuemei ; et al ( December 2022 , Nature Communications)

   Light initiates chloroplast biogenesis inArabidopsisby 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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3. High‐resolution map of plastid‐encoded RNA polymerase binding patterns demonstrates a major role of transcription in chloroplast gene expression

   https://doi.org/10.1111/tpj.15882  

   Palomar, V. Miguel ; Jaksich, Sarah ; Fujii, Sho ; Kuciński, Jan ; Wierzbicki, Andrzej T. ( July 2022 , The Plant Journal)

   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 matureArabidopsis thalianachloroplasts, 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/.

    

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4. Transcriptome and phenotyping analyses support a role for chloroplast sigma factor 2 in red‐light‐dependent regulation of growth, stress, and photosynthesis

   https://doi.org/10.1002/pld3.43  

   Oh, Sookyung ; Strand, Deserah D. ; Kramer, David M. ; Chen, Jin ; Montgomery, Beronda L. ( February 2018 , Plant Direct)

   Sigma factor (SIG) proteins contribute to promoter specificity of the plastid‐encodedRNApolymerase during chloroplast genome transcription. All six members of theSIGfamily, that is,SIG1–SIG6, are nuclear‐encoded proteins targeted to chloroplasts. Sigma factor 2 (SIG2) 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. AmongSIGfactors,SIG2 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. AlthoughSIG2 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 thatSIG2 is necessary for phytochrome‐mediated photomorphogenesis specifically under red (R) and far‐red light, thereby suggesting a link between phytochromes and nuclear‐encodedSIG2 in light signaling. To explore transcriptional roles ofSIG2 in R‐dependent growth and development, we performedRNAsequencing analysis to compare gene expression insig2‐2mutant 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, strongsig2mutants showed insensitivity to bioactiveGA₃, 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 thatSIG2 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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5. Nuclear‐encoded sigma factor 6 ( SIG 6) is involved in the block of greening response in Arabidopsis thaliana

   https://doi.org/10.1002/ajb2.1423  

   Alameldin, Hussien F. ; Oh, Sookyung ; Hernandez, Alexandra P. ; Montgomery, Beronda L. ( January 2020 , American Journal of Botany)

   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 theFRblock of greening (BOG). This response is controlled by phytochrome A through repression of protochlorophyllide reductase‐encoding (POR) genes byFRlight 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.SIGs are regulated by phytochromes, and the expression of someSIGfactors is reduced in phytochrome mutant lines, including phyA. Given the association of phyA with theFR BOGand its regulation ofSIGfactors, we investigated the potential regulatory role ofSIGfactors in theFR BOGresponse.

   We examinedFR BOGresponses insigmutants, phytochrome‐deficient lines, and mutant lines for several phy‐associated factors. We quantified chlorophyll levels and examined expression of keyBOG‐associated genes.

   Among sixsigmutants, only thesig6 mutant significantly accumulated chlorophyll afterFR BOGtreatment, similar to thephyAmutant.SIG6 appears to control protochlorophyllide accumulation by contributing to the regulation of tetrapyrrole biosynthesis associated with glutamyl‐tRNAreductase (HEMA1) function, select phytochrome‐interacting factor genes (PIF4andPIF6), andPENTA1, which regulatesPORAmRNAtranslation afterFRexposure.

   Regulation ofSIG6plays a significant role in plant responses toFRexposure during theBOGresponse.

    

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