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Phytochrome B enhances seed germination tolerance to high temperature by reducing S-nitrosylation of HFR1.

ABSTRACT: Light and ambient high temperature (HT) have opposite effects on seed germination. Light induces seed germination through activating the photoreceptor phytochrome B (phyB), resulting in the stabilization of the transcription factor HFR1, which in turn sequesters the suppressor PIF1. HT suppresses seed germination and triggers protein S-nitrosylation. Here, we find that HT suppresses seed germination by inducing the S-nitrosylation of HFR1 at C164, resulting in its degradation, the release of PIF1, and the activation of PIF1-targeted SOMNUS (SOM) expression to alter gibberellin (GA) and abscisic acid (ABA) metabolism. Active phyB (phyB^Y276H ) antagonizes HFR1 S-nitrosylation and degradation by increasing S-nitrosoglutathione reductase (GSNOR) activity. In line with this, substituting cysteine-164 of HFR1 with serine (HFR1^C164S ) abolishes the S-nitrosylation of HFR1 and decreases the HT-induced degradation of HFR1. Taken together, our study suggests that HT and phyB antagonistically modulate the S-nitrosylation level of HFR1 to coordinate seed germination, and provides the possibility to enhance seed thermotolerance through gene-editing of HFR1.

SUBMITTER: Ying S

PROVIDER: S-EPMC9535752 | biostudies-literature | 2022 Oct

REPOSITORIES: biostudies-literature

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Phytochrome B enhances seed germination tolerance to high temperature by reducing S-nitrosylation of HFR1.

Ying Songbei S Yang Wenjun W Li Ping P Hu Yulan Y Lu Shiyan S Zhou Yun Y Huang Jinling J Hancock John T JT Hu Xiangyang X

EMBO reports 20220905 10

Light and ambient high temperature (HT) have opposite effects on seed germination. Light induces seed germination through activating the photoreceptor phytochrome B (phyB), resulting in the stabilization of the transcription factor HFR1, which in turn sequesters the suppressor PIF1. HT suppresses seed germination and triggers protein S-nitrosylation. Here, we find that HT suppresses seed germination by inducing the S-nitrosylation of HFR1 at C164, resulting in its degradation, the release of PIF ...[more]

PMID: 36062942

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Project description:Seed germination is critical to agricultural productivity because low germination rates and/or asynchronous germination negatively affect stand establishment and subsequent yields. Exposure to high temperatures during seed imbibition can decrease both germination synchrony and rates through an ABA-mediated process called thermoinhibition. Methods to reduce thermoinhibition would be agriculturally valuable, particularly with increasing global mean temperatures. Lettuce seed germination is particularly sensitive to high temperatures and is a classic system for studying thermoinhibition. Extensive evidence using mutants and carotenoid biosynthetic inhibitors (e.g. fluridone) has demonstrated that endogenous abscisic acid (ABA) biosynthesis is required for thermoinhibition in lettuce and Arabidopsis. Although fluridone and related carotenoid biosynthetic inhibitors block thermoinhibition, they are not well-suited for this application due to their herbicidal effects. Here we explore the potential of ABA receptor antagonism to disrupt thermoinhibition using antabactin (ANT), a broad-spectrum high-affinity receptor antagonist. We show low μM ANT treatments (10 μM) during lettuce seed imbibition reduces thermoinhibition at temperatures of up to 40°C, demonstrating that ABA signaling is required for thermoinhibition and that receptor antagonists are well-suited anti-thermoinhibition agents. We further explored interactions between ANT and seed priming, which is used commercially to improve seed germination and reduce thermoinhibition and is achieved by partial hydration and subsequent desiccation of seeds. We show that co-priming with ANT improves germination at elevated temperatures better than priming alone, and thus, the two treatments can be combined to improve germination. Our data demonstrate that ABA antagonists are potentially useful agrochemical leads for mitigating the effects of high temperatures on seed germination and stand establishment that may be of increasing importance due to climate change. More generally, ABA antagonists should be useful in physiological processes where ABA's effects are counterproductive to yield.

Project description:In Arabidopsis thaliana, the basic Helix Loop Helix transcription factor, PHYTOCHROME INTERACTING FACTOR1 (PIF1) is known to orchestrate the seed transcriptome such that, ultimately, proteins repressing the completion of germination are produced in darkness. While PIF1-mediated control of abscisic acid (ABA) and gibberellic acid (GA) anabolism/catabolism is indirect, PIF1 action favors ABA while discriminating against GA, firmly establishing ABA's repressive influence on the completion of germination. The result is tissue that is more sensitive to and producing more ABA; and is less responsive to and deficient in GA. Illumination of the appropriate wavelength activates phytochrome which enters the nucleus, and binds to PIF1, initiating PIF1's phosphorylation by diverse kinases, subsequent polyubiquitination, and hydrolysis. One mechanism by which phosphorylated PIF1 is eliminated from the cells of the seed upon illumination involves an F-BOX protein, COLD TEMPERATURE GERMINATING10 (CTG10). Discovered in an unbiased screen of activation tagged lines hastening the completion of seed germination at 10°C, one indirect consequence of CTG10 action in reducing PIF1 titer, should be to enhance the transcription of genes whose products work to increase bioactive GA titer, shifting the intracellular milieu from one that is repressive to, toward one conducive to, the completion of seed germination. We have tested this hypothesis using a variety of Arabidopsis lines altered in CTG10 amounts. Here we demonstrate using bimolecular fluorescence complementation that PIF1 interacts with CTG10 and show that, in light exposed seeds, PIF1 is more persistent in ctg10 relative to WT seeds while it is less stable in seeds over-expressing CTG10. These results are congruent with the relative transcript abundance from three genes whose products are involved in bioactive GA accumulation. We put forth a model of how PIF1 interactions in imbibed seeds change during germination and how a permissive light signal influences these changes, leading to the completion of germination of these positively photoblastic propagules.

Project description:IntroductionHeat stress is a vital factor which restricts rice seed quality and yield. However, the response mechanism to heat stress in the mid filling stage of rice seed is unclear.MethodsIn the present study we integrated phenotypic analysis with biochemical, hormone, and gene expression analysis in order to explore technologies for improving rice seeds heat tolerance and subsequent seed germination.ResultsSpermidine (Spd) application effectively alleviated the damage of heat stress treatment during mid-filling stage (HTM, 12-20 days after pollination) on seed development, promoted subsequent seed germination and seedlings establishment. Spd significantly increased seed dry weight, starch and amylose contents during seed development under heat stress, and improved seed germinate, seedlings establishment and seedling characteristics during germination time. Biochemical analysis indicated that, HTM significantly decreased the activities of several starch synthase enzymes and led to a decrease in starch content. While Spd treatment significantly enhanced the activities of ADP-glucose pyrophosphorylas and granule-bound starch synthase, as well as the corresponding-genes expressions in HTM rice seeds, resulting in the increases of amylose and total starch contents. In addition, Spd significantly increased the catalase and glutathione reductase activities together with corresponding-genes expressions, and lowered the overaccumulation of H2O2 and malondialdehyde in HTM seeds. In the subsequent seed germination process, HTM+Spd seeds exhibited dramatically up-regulated levels of soluble sugars, glucose, ATP and energy charges. Consistently, HTM+Spd seeds showed significantly increased of α-amylose and α-glucosidase activities as well as corresponding-genes expressions during early germination. Moreover, HTM evidently increased the abscisic acid (ABA) content, decreased the gibberellin (GA) content, and accordingly significantly declined the GA/ABA ratio during early rice seeds germination. However, Spd treatment did not significantly affect the metabolism of GA and ABA in seed germination stage.DiscussionThe present study suggested that Spd treatment could effectively alleviate the negative impact of HTM on seed development and the subsequent seed germination, which might be closely correlated with starch synthesis and antioxidant defense during seed filling period, starch decomposition and energy supply in seed germination period.

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Phytochrome B enhances seed germination tolerance to high temperature by reducing S-nitrosylation of HFR1.

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Phytochrome B enhances seed germination tolerance to high temperature by reducing S-nitrosylation of HFR1.

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