Spatially and genetically distinct control of seed germination by phytochromes A and B

Lee, Keun Pyo; Piskurewicz, Urszula; Turečková, Veronika; Carat, Solenne; Chappuis, Richard; Strnad, Miroslav; Fankhauser, Christian; Lopez‐Molina, Luis

doi:10.1101/gad.194266.112

Cited by 117 publications

(157 citation statements)

References 36 publications

(85 reference statements)

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“…Moreover, abscisic acid (ABA) signaling interferes with phyA-dependent seed germination (Lee et al, 2012). On the other hand, phyA synergistically coordinates with ABA to inhibit root elongation under white light (Jiang et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

Arabidopsis Phytochrome A Directly Targets Numerous Promoters for Individualized Modulation of Genes in a Wide Range of Pathways

Chen

et al. 2014

Plant Cell

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The far-red light (FR) photoreceptor phytochrome A (phyA) contains no DNA binding domain but associates with the CHALCONE SYNTHASE promoter through its chaperone FAR-RED ELONGATED HYPOCOTYL1 and transcription factors. Here, we performed a genome-wide identification of phyA targets using a combination of phyA chromatin immunoprecipitation and RNA sequencing methods in Arabidopsis thaliana. Our results indicate that phyA signaling widely affects gene promoters involved in multiple FR-modulated aspects of plant growth. Furthermore, we observed an enrichment of hormone-and stressresponsive elements in the phyA direct target promoters, indicating that a much broader than expected range of transcription factors is involved in the phyA signaling pathway. To verify our hypothesis that phyA regulates genes other than light-responsive ones through the interaction with corresponding transcription factors, we examined the action of phyA on one of its direct target genes, NAC019, which encodes an abscisic acid-dependent transcription factor. The phyA signaling cascade not only targets two G-boxes on the NAC019 promoter for subsequent transcriptional regulation but also positively coordinates with the abscisic acid signaling response for root elongation inhibition under FR. Our study provides new insight into how plants rapidly fine-tune their growth strategy upon changes in the light environment by escorting photoreceptors to the promoters of hormone-or stress-responsive genes for individualized modulation.

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Section: Introductionmentioning

confidence: 99%

Arabidopsis Phytochrome A Directly Targets Numerous Promoters for Individualized Modulation of Genes in a Wide Range of Pathways

Chen

et al. 2014

Plant Cell

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“…During the initial phase of seed imbibition, the protein level of phyA is very low, therefore, seed germination is dependent on the red light activation of phyB (phyB-dependent germination) (Shinomura et al, 1994;Seo et al, 2009). After prolonged incubation in the dark (e.g., 48 h), phyA accumulates to high levels and mediates canopy light (FR) induced-seed germination, promoting germination to very low fluence response and FR high irradiation response (Shinomura et al, 1996;Kneissl et al, 2009;Seo et al, 2009;Lee et al, 2012). Recent study showed that canopy light suppresses phyB-dependent germination in the endosperm and activates phyA-dependent germination in the embryo, which involves spatial abscisic acid (ABA) signaling responses (Lee et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

“…Upon red light irradiation, the Pr form of phytochrome is converted to the Pfr form to initiate red lightregulated plant development (Quail, 2002;Chen et al, 2004). PhyA and phyB are the main receptors of light-induced seed germination and other PHYs (phyC to E) also play minor roles during the process (Lee et al, 2012). PhyA mediates far-red light (FR), whereas PhyB mediates red light (R)-induced seed germination processes.…”

Section: Introductionmentioning

confidence: 99%

“…After prolonged incubation in the dark (e.g., 48 h), phyA accumulates to high levels and mediates canopy light (FR) induced-seed germination, promoting germination to very low fluence response and FR high irradiation response (Shinomura et al, 1996;Kneissl et al, 2009;Seo et al, 2009;Lee et al, 2012). Recent study showed that canopy light suppresses phyB-dependent germination in the endosperm and activates phyA-dependent germination in the embryo, which involves spatial abscisic acid (ABA) signaling responses (Lee et al, 2012). The different roles of phyA and phyB are important for the plant's ability to adapt to different light conditions during germination.…”

Section: Introductionmentioning

confidence: 99%

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HFR1 Sequesters PIF1 to Govern the Transcriptional Network Underlying Light-Initiated Seed Germination in Arabidopsis

et al. 2013

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Seed germination is the first step for seed plants to initiate a new life cycle. Light plays a predominant role in promoting seed germination, where the initial phase is mediated by photoreceptor phytochrome B (phyB). Previous studies showed that PHYTOCHROME-INTERACTING FACTOR1 (PIF1) represses seed germination downstream of phyB. Here, we identify a positive regulator of phyB-dependent seed germination, LONG HYPOCOTYL IN FAR-RED1 (HFR1). HFR1 blocks PIF1 transcriptional activity by forming a heterodimer with PIF1 that prevents PIF1 from binding to DNA. Our whole-genomic analysis shows that HFR1 and PIF1 oppositely mediate the light-regulated transcriptome in imbibed seeds. Through the HFR1–PIF1 module, light regulates expression of numerous genes involved in cell wall loosening, cell division, and hormone pathways to initiate seed germination. The functionally antagonistic HFR1–PIF1 pair constructs a fail-safe mechanism for fine-tuning seed germination during low-level illumination, ensuring a rapid response to favorable environmental changes. This study identifies the HFR1–PIF1 pair as a central module directing the whole genomic transcriptional network to rapidly initiate light-induced seed germination.

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“…Among them, light plays a major role in initiating seed germination (1-4). Plants perceive light signals through distinct families of photoreceptors, in which the red light photoreceptor phytochrome B (phyB) mediates the initial phase of light-induced seed germination (3,(5)(6)(7)(8). Previous studies showed that in seeds, phyB modulates downstream regulatory networks through one of its interacting factors, phytochrome interacting factor 1 (PIF1) (9-11).…”

mentioning

confidence: 99%

Arabidopsis DET1 degrades HFR1 but stabilizes PIF1 to precisely regulate seed germination

Shi

Wang

et al. 2015

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

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Seed is an essential propagation organ and a critical strategy adopted by terrestrial flowering plants to colonize the land. The ability of seeds to accurately respond to light is vital for plant survival. However, the underlying mechanism is largely unknown. In this study, we reveal a circuit of triple feed-forward loops adopted by Arabidopsis seeds to exclusively repress germination in dark conditions and precisely initiate germination under diverse light conditions. We identify that de-etiolated 1 (DET1), an evolutionarily conserved protein, is a central repressor of light-induced seed germination. Genetic analysis demonstrates that DET1 functions upstream of long hypocotyl in far-red 1 (HFR1) and phytochrome interacting factor 1 (PIF1), the key positive and negative transcription regulators in seed germination. We further find that DET1 and constitutive photomorphogenic 10 (COP10) target HFR1 for protein degradation by assembling a COP10-DET1-damaged DNA binding protein 1-cullin4 E3 ligase complex. Moreover, DET1 and COP10 directly interact with and promote the protein stability of PIF1. Computational modeling reveals that phytochrome B (phyB)-DET1-HFR1-PIF1 and phyB-DET1-Protease-PIF1 are new signaling pathways, independent of the previously identified phyB-PIF1 pathway, respectively mediating the rapid and time-lapse responses to light irradiation. The model-simulated results are highly consistent with their experimental validations, suggesting that our mathematical model captures the essence of Arabidopsis seed germination networks. Taken together, this study provides a comprehensive molecular framework for light-regulated seed germination, improving our understanding of how plants respond to changeable environments.S eed germination is controlled by a wide range of environmental factors to ensure that plants start a new lifecycle in favorable conditions. Among them, light plays a major role in initiating seed germination (1-4). Plants perceive light signals through distinct families of photoreceptors, in which the red light photoreceptor phytochrome B (phyB) mediates the initial phase of light-induced seed germination (3,(5)(6)(7)(8). Previous studies showed that in seeds, phyB modulates downstream regulatory networks through one of its interacting factors, phytochrome interacting factor 1 (PIF1) (9-11). PIF1 is a basic helix-loop-helix (bHLH) transcription factor that plays a primary role in repressing seed germination, and PIF1 proteins are highly accumulated in dark-incubated seeds (9, 10, 12). Under light irradiation, the light-activated phyB interacts with PIF1 to induce PIF1 phosphorylation and degradation via the 26S proteasome (12-16). Our recent study identified long hypocotyl in far-red 1 (HFR1) as a core transcription regulator in seed germination (17). HFR1 positively regulates seed germination by forming heterodimers with PIF1 to sequester PIF1 from binding to its target genes (17). The HFR1-PIF1 pair governs the transcriptional networks of light-initiated seed germination (17). However, how...

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Spatially and genetically distinct control of seed germination by phytochromes A and B

Cited by 117 publications

References 36 publications

Arabidopsis Phytochrome A Directly Targets Numerous Promoters for Individualized Modulation of Genes in a Wide Range of Pathways

Arabidopsis Phytochrome A Directly Targets Numerous Promoters for Individualized Modulation of Genes in a Wide Range of Pathways

HFR1 Sequesters PIF1 to Govern the Transcriptional Network Underlying Light-Initiated Seed Germination in Arabidopsis

Arabidopsis DET1 degrades HFR1 but stabilizes PIF1 to precisely regulate seed germination

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