Ethylene-orchestrated circuitry coordinates a seedling’s response to soil cover and etiolated growth

Zhong, Shangwei; Shi, Hui; Xue, Chang; Wei, Ning; Guo, Hongwei; Deng, Xing Wang

doi:10.1073/pnas.1402491111

Cited by 153 publications

(161 citation statements)

References 66 publications

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“…Light is the energy resource and a critical environmental cue for plant development and growth (5,(32)(33)(34)(35). The ability of seeds to rapidly and precisely respond to light is vital for plant survival.…”

Section: Discussionmentioning

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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Section: Discussionmentioning

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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“…Dark-grown Arabidopsis seedlings follow the skotomorphogenic developmental program, which is characterized by long hypocotyls, apical hooks, and closed cotyledons; in contrast, light-grown seedlings undergo photomorphogenesis and display short hypocotyls, no apical hooks, and greening and expanded cotyledons (2,3). It is vital for plants to correctly switch from skotomorphogenesis to photomorphogenesis upon emerging above ground (4). After illumination, the cotyledons quickly open and expand whereas hypocotyls reduce their elongation rate.…”

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confidence: 99%

Arabidopsis SAURs are critical for differential light regulation of the development of various organs

Sun

Wang

Gao

et al. 2016

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

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During deetiolation of Arabidopsis seedlings, light promotes the expansion of cotyledons but inhibits the elongation of hypocotyls. The mechanism of this differential regulation of cell enlargement is unclear. Our organ-specific transcriptomic analysis identified 32 Small Auxin Up RNA (SAUR) genes whose transcripts were light-induced in cotyledons and/or repressed in hypocotyls. We therefore named these SAURs as lirSAURs. Both overexpression and mutation analyses demonstrated that lirSAURs could promote cotyledon expansion and opening and enhance hypocotyl elongation, possibly by inhibiting phosphatase activity of D-clade type 2C protein phosphatases (PP2C-Ds). Light reduced auxin levels to down-regulate the expression of lirSAURs in hypocotyls. Further, phytochrome-interacting factors (PIFs) were shown to directly bind the genes encoding these SAURs and differentially regulate their expression in cotyledons and hypocotyls. Together, our study demonstrates that light mediates auxin levels and PIF stability to differentially regulate the expression of lirSAURs in cotyledons and hypocotyls, and these lirSAURs further mediate the differential growth of these two organs.light signal | seedling development | SAURs | auxin | PIFs

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“…When elongated hypocotyls encounter mechanical obstacles during seedling extrusion from the soil, inhibition of rapid etiolated hypocotyl elongation is required to optimize the seedling's ability to push through the soil without damaging its shoot meristem. Disturbing this physiological process significantly affects seedling emergence from the soil and survival (Zhong et al, 2014). The phytohormone ethylene plays a crucial role in the negative regulation of hypocotyl elongation in the dark.…”

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Ethylene Regulates the Arabidopsis Microtubule-Associated Protein WAVE-DAMPENED2-LIKE5 in Etiolated Hypocotyl Elongation

Sun

Mao

2015

Plant Physiol.

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The phytohormone ethylene plays crucial roles in the negative regulation of plant etiolated hypocotyl elongation. The microtubule cytoskeleton also participates in hypocotyl cell growth. However, it remains unclear if ethylene signaling-mediated etiolated hypocotyl elongation involves the microtubule cytoskeleton. In this study, we functionally identified the previously uncharacterized microtubuleassociated protein WAVE-DAMPENED2-LIKE5 (WDL5) as a microtubule-stabilizing protein that plays a positive role in ethyleneregulated etiolated hypocotyl cell elongation in Arabidopsis (Arabidopsis thaliana). ETHYLENE-INSENSITIVE3, a key transcription factor in the ethylene signaling pathway, directly targets and up-regulates WDL5. Etiolated hypocotyls from a WDL5 loss-of-function mutant (wdl5-1) were more insensitive to 1-aminocyclopropane-1-carboxylic acid treatment than the wild type. Decreasing WDL5 expression partially rescued the shorter etiolated hypocotyl phenotype in the ethylene overproduction mutant eto1-1. Reorganization of cortical microtubules in etiolated hypocotyl cells from the wdl5-1 mutant was less sensitive to 1-aminocyclopropane-1-carboxylic acid treatment. These findings indicate that WDL5 is an important participant in ethylene signaling inhibition of etiolated hypocotyl growth. This study reveals a mechanism involved in the ethylene regulation of microtubules through WDL5 to inhibit etiolated hypocotyl cell elongation.Skotomorphogenesis occurs as buried seedlings fully elongate their hypocotyls upward in search of the soil surface. When elongated hypocotyls encounter mechanical obstacles during seedling extrusion from the soil, inhibition of rapid etiolated hypocotyl elongation is required to optimize the seedling's ability to push through the soil without damaging its shoot meristem. Disturbing this physiological process significantly affects seedling emergence from the soil and survival (Zhong et al., 2014). The phytohormone ethylene plays a crucial role in the negative regulation of hypocotyl elongation in the dark. Ethylene functions through five membrane-bound receptors (ETHYLENE RESPONSE1 ) complexes and degraded in the absence of ethylene (Guo and Ecker, 2003;Potuschak et al., 2003). One of the most widely documented ethylene responses in etiolated seedlings is the triple response, including a short, thickened hypocotyl when darkgrown Arabidopsis (Arabidopsis thaliana) seedlings are treated with ethylene or its biosynthetic precursor 1-aminocyclopropane-1-carboxylic acid (ACC; Bleecker et al., 1988;Ecker, 1995). Ethylene and ACC stimulate hypocotyl elongation in the light but suppress etiolated hypocotyl elongation in the dark, largely due to the concomitant activation of two contrasting pathways (Ecker, 1995;Zhong et al., 2012). Genetic evidence has shown that ethylene-overproduced or constitutive ethylene-response mutants generally display defective etiolated hypocotyl cell growth phenotypes. For example, the ethylene-overproducing mutant eto1-1 and the CONSTITUTIVE TRIPLE RESPONSE1 (CTR1)...

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Ethylene-orchestrated circuitry coordinates a seedling’s response to soil cover and etiolated growth

Cited by 153 publications

References 66 publications

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

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

Arabidopsis SAURs are critical for differential light regulation of the development of various organs

Ethylene Regulates the Arabidopsis Microtubule-Associated Protein WAVE-DAMPENED2-LIKE5 in Etiolated Hypocotyl Elongation

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