Heme, a Plastid-Derived Regulator of Nuclear Gene Expression in<i>Chlamydomonas</i>

Gromoff, Erika Donner von; Alawady, Ali; Meinecke, Linda; Grimm, Bernhard; Beck, Christoph F.

doi:10.1105/tpc.107.054650

Cited by 107 publications

(115 citation statements)

References 67 publications

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“…This notion is consistent with the reduced levels of chlorophyll intermediates in glk1 glk2 mutants, a metabolic state that could perturb the tetrapyrrole pool and thus influence the GUN pathway (Mochizuki et al, 2008;Moulin et al, 2008;von Gromoff et al, 2008).…”

Section: Glk Transcript Levels Are Regulated By Feedback From the Plasupporting

confidence: 67%

GLK Transcription Factors Coordinate Expression of the Photosynthetic Apparatus in Arabidopsis

et al. 2009

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Chloroplasts of photosynthetic organisms harness light energy and convert it into chemical energy. In several land plants, GOLDEN2-LIKE (GLK) transcription factors are required for chloroplast development, as glk1 glk2 double mutants are pale green and deficient in the formation of the photosynthetic apparatus. We show here that glk1 glk2 double mutants of Arabidopsis thaliana accumulate abnormal levels of chlorophyll precursors and that constitutive GLK gene expression leads to increased accumulation of transcripts for antenna proteins and chlorophyll biosynthetic enzymes. To establish the primary targets of GLK gene action, an inducible expression system was used in combination with transcriptome analysis. Following induction, transcript pools were substantially enriched in genes involved in chlorophyll biosynthesis, light harvesting, and electron transport. Chromatin immunoprecipitation experiments confirmed the direct association of GLK1 protein with target gene promoters, revealing a putative regulatory cis-element. We show that GLK proteins influence photosynthetic gene expression independently of the phyB signaling pathway and that the two GLK genes are differentially responsive to plastid retrograde signals. These results suggest that GLK genes help to coregulate and synchronize the expression of a suite of nuclear photosynthetic genes and thus act to optimize photosynthetic capacity in varying environmental and developmental conditions.

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Section: Glk Transcript Levels Are Regulated By Feedback From the Plasupporting

confidence: 67%

GLK Transcription Factors Coordinate Expression of the Photosynthetic Apparatus in Arabidopsis

et al. 2009

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“…Heme turnover also will be facilitated by PCYA, which converts BV to PCB. We thus propose that PCB is the bilin signal responsible for induction of a photoprotective transcriptional program, because the genes regulated by exogenous heme treatment in darkness differ from those observed here (51)(52)(53). Our studies demonstrate that cells that lack HMOX1 are poorly equipped to deal with the transition from dark to light because they cannot produce bilins.…”

Section: Discussionmentioning

confidence: 50%

Retrograde bilin signaling enables Chlamydomonas greening and phototrophic survival

Duanmu

Casero

Dent

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

111

172

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The maintenance of functional chloroplasts in photosynthetic eukaryotes requires real-time coordination of the nuclear and plastid genomes. Tetrapyrroles play a significant role in plastid-tonucleus retrograde signaling in plants to ensure that nuclear gene expression is attuned to the needs of the chloroplast. Well-known sites of synthesis of chlorophyll for photosynthesis, plant chloroplasts also export heme and heme-derived linear tetrapyrroles (bilins), two critical metabolites respectively required for essential cellular activities and for light sensing by phytochromes. Here we establish that Chlamydomonas reinhardtii, one of many chlorophyte species that lack phytochromes, can synthesize bilins in both plastid and cytosol compartments. Genetic analyses show that both pathways contribute to iron acquisition from extracellular heme, whereas the plastid-localized pathway is essential for light-dependent greening and phototrophic growth. Our discovery of a bilin-dependent nuclear gene network implicates a widespread use of bilins as retrograde signals in oxygenic photosynthetic species. Our studies also suggest that bilins trigger critical metabolic pathways to detoxify molecular oxygen produced by photosynthesis, thereby permitting survival and phototrophic growth during the light period.biliverdin | heme oxygenase | iron homeostasis | oxidative stress | RNA-Seq analysisT he daily light-dark cycle requires all oxygenic photosynthetic species to survive the repeated transition from prolonged darkness to phototrophic metabolism at dawn. Most plants are unable to synthesize chlorophyll in darkness and therefore accumulate photosensitizing chlorophyll precursors at night (1). Sunrise induces an oxidative burst as photosynthesis resumes, so the transition to daylight requires careful coordination of many lightdependent processes. Multiple photoreceptors perform such roles in plants, the most notable being the red-sensing, linear tetrapyrrole (bilin)-based phytochromes and the blue-sensing, flavin-based cryptochromes and phototropins (2-5). Bilins are well-established plant retrograde signals, synthesized in plastids but enabling light sensing by cytosolic phytochromes. Phytochrome photoconversion then triggers nuclear translocation to positively regulate photosynthesis-associated nuclear gene (PhANG) expression (6, 7).Genetic studies suggest that plastids also export negative retrograde signals, metabolites that suppress nuclear gene networks targeted by phytochromes (8-10). Among these metabolites are abscisic acid (ABA) (11), tetrapyrroles (12-14), 3′-phosphoadenosine 5′-phosphate (PAP) (15), β-cyclocitral (16), and methylerythritol cyclodiphosphate (MEcPP) (17). Although hypothetical export of a negative tetrapyrrole signal has received considerable support, biochemical evidence for such a retrograde signal remains equivocal in plants (18)(19)(20). Chlorophyte algae diverged from the streptophyte plant lineage over 500 million years ago but share a common chlorophyll a/b-based photosynthetic lightharvesting app...

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“…In mammals and yeast, heme has several important signaling roles. It has been identified that heme functions in cellular signal transductions, such as transcription (Guarente and Mason 1983;Shan et al 2004;Sun et al 2004;von Gromoff et al 2008;Zitomer and Lowry 1992), translation (Joshi et al 1995), posttranslational protein modification (Chen et al 1989), translocation (Lathrop and Timko 1993), and ion-channel function (Tang et al 2003). Other tetrapyrroles have also been linked with signaling functions.…”

Section: Signaling Function Of Tetrapyrrolesmentioning

confidence: 99%

Tetrapyrrole Metabolism inArabidopsis thaliana

Tanaka

Kobayashi²,

Masuda

2011

The Arabidopsis Book

226

232

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This manuscript is dedicated to Prof. Mamoru Mimuro of Kyoto University who passed away in Februay 2011.Higher plants produce four classes of tetrapyrroles, namely, chlorophyll (Chl), heme, siroheme, and phytochromobilin. In plants, tetrapyrroles play essential roles in a wide range of biological activities including photosynthesis, respiration and the assimilation of nitrogen/sulfur. All four classes of tetrapyrroles are derived from a common biosynthetic pathway that resides in the plastid. In this article, we present an overview of tetrapyrrole metabolism in Arabidopsis and other higher plants, and we describe all identified enzymatic steps involved in this metabolism. We also summarize recent findings on Chl biosynthesis and Chl breakdown. Recent advances in this field, in particular those on the genetic and biochemical analyses of novel enzymes, prompted us to redraw the tetrapyrrole metabolic pathways. In addition, we also summarize our current understanding on the regulatory mechanisms governing tetrapyrrole metabolism. The interactions of tetrapyrrole biosynthesis and other cellular processes including the plastid-to-nucleus signal transduction are discussed.

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Heme, a Plastid-Derived Regulator of Nuclear Gene Expression inChlamydomonas

Cited by 107 publications

References 67 publications

GLK Transcription Factors Coordinate Expression of the Photosynthetic Apparatus in Arabidopsis

GLK Transcription Factors Coordinate Expression of the Photosynthetic Apparatus in Arabidopsis

Retrograde bilin signaling enables Chlamydomonas greening and phototrophic survival

Tetrapyrrole Metabolism inArabidopsis thaliana

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