Arabidopsis NITROGEN LIMITATION ADAPTATION regulates ORE1 homeostasis during senescence induced by nitrogen deficiency

Park, Bong Soo; Yao, Tao; Seo, Jun Sung; Wong, Eriko Chi Cheng; Mitsuda, Nobutaka; Huang, Chung‐Hao; Chua, Nam‐Hai

doi:10.1038/s41477-018-0269-8

Cited by 74 publications

(73 citation statements)

References 35 publications

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“…A second mechanism has been proposed for the GS enzyme in mammals, wherein the increase in glutamine levels drives ubiquitination and proteasome degradation of the protein [49,50]. In plants, ubiquitination-dependent proteolysis also plays a role in N metabolism during plant adaptation to N starvation [51,52].…”

Section: Discussionmentioning

confidence: 99%

Inorganic Nitrogen Form Determines Nutrient Allocation and Metabolic Responses in Maritime Pine Seedlings

Ortigosa

Valderrama‐Martín

Urbano-Gámez

et al. 2020

Plants

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Nitrate and ammonium are the main forms of inorganic nitrogen available to plants. The present study aimed to investigate the metabolic changes caused by ammonium and nitrate nutrition in maritime pine (Pinus pinaster Ait.). Seedlings were grown with five solutions containing different proportions of nitrate and ammonium. Their nitrogen status was characterized through analyses of their biomass, different biochemical and molecular markers as well as a metabolite profile using 1 H-NMR. Ammonium-fed seedlings exhibited higher biomass than nitrate-fed-seedlings. Nitrate mainly accumulated in the stem and ammonium in the roots. Needles of ammonium-fed seedlings had higher nitrogen and amino acid contents but lower levels of enzyme activities related to nitrogen metabolism. Higher amounts of soluble sugars and L-arginine were found in the roots of ammonium-fed seedlings. In contrast, L-asparagine accumulated in the roots of nitrate-fed seedlings. The differences in the allocation of nitrate and ammonium may function as metabolic buffers to prevent interference with the metabolism of photosynthetic organs. The metabolite profiles observed in the roots suggest problems with carbon and nitrogen assimilation in nitrate-supplied seedlings. Taken together, this new knowledge contributes not only to a better understanding of nitrogen metabolism but also to improving aspects of applied mineral nutrition for conifers.

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Section: Discussionmentioning

confidence: 99%

Inorganic Nitrogen Form Determines Nutrient Allocation and Metabolic Responses in Maritime Pine Seedlings

Ortigosa

Valderrama‐Martín

Urbano-Gámez

et al. 2020

Plants

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“…Such fine-tuning of ORE1 levels gives plants the flexibility to adjust rapidly to the fluctuating nitrogen levels in the environment. The identification of key regulators of ORE1 reported before (Park et al, 2018) Fig. 8 UBP12 and UBP13 regulate ORE1 during leaf senescence under nitrogen-deficient (ÀN) conditions.…”

Section: Multiple Functions Of Ubp12 and Ubp13mentioning

confidence: 93%

“…ligase as PHO2 and NLA, respectively (Park et al, 2018). The rapid degradation of ORE1 allows a faster recovery of nitrogenstressed plants when nitrogen becomes available in the environment (Fig.…”

Section: Ubp12 and Ubp13 Counteract The Effects Of Nlamentioning

confidence: 99%

“…ORE1 interacts with NLA and UBP12/ UBP13. ORE1 is first polyubiquitinated by the E3/E2 enzyme complex, NLA/PHO2, and then degraded by 26S proteasomes leading to delayed leaf senescence (Park et al, 2018). When plants are exposed to nitrogendeficient conditions (ÀN) UBP12 and UBP13 antagonize the effects of NLA E3 ligase by promoting the deubiquitination of polyubiquitinated-ORE1 and rescue ORE1 from being degraded.…”

Section: Multiple Functions Of Ubp12 and Ubp13mentioning

confidence: 99%

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Arabidopsis ubiquitin‐specific proteases UBP12 and UBP13 shape ORE1 levels during leaf senescence induced by nitrogen deficiency

et al. 2019

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Summary Nitrogen deficiency (−N) in plants triggers leaf senescence which is regulated by the transcription factor ORE1. Little is known about post‐translational regulation of ORE1 in this process. Here, we show that UBP12/UBP13 (ubiquitin‐specific protease 12/13) antagonize the action of NLA (nitrogen limitation adaptation) E3 ligase to maintain ORE1 homeostasis. In vitro pull‐down and in vivo co‐immunoprecipitation assays demonstrated specific binding between UBP12/UBP13 and ORE1. We further analyzed in various genotypes total Chl content and expression levels of senescence‐related genes under −N conditions. We found that UBP12/UBP13 can deubiquitinate polyubiquitinated ORE1 in vitro and increase the stability of ORE1 in vivo in MG132/cycloheximide‐chase experiments. Plants overexpressing UBP12/UBP13 display accelerated leaf senescence which is reversed by the ore1 mutation. By contrast, the senescence phenotype of plants overexpressing ORE1 is exacerbated by UBP12/UBP13 overexpression. The expression of senescence‐related genes tracks the senescence phenotype. ORE1 protein levels can be elevated by UBP12/UBP13 overexpression but decreased in ubp12‐2w/13‐3. In conclusion, UBP12/UBP13 deubiquitinate ORE1 to stabilize this transcription factor and promote its activity as a positive regulator for leaf senescence under −N conditions. Our study shows that UBP12/UBP13 counteracts the effect of NLA E3 ligase to accelerate leaf senescence under nitrogen starvation.

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“…The rice NLP3, a key transcription factor for nitrogen responses, is controlled by OsSPX4, which is in New Phytologist (2020) 225: 637-652 Ó 2019 The Authors New Phytologist Ó 2019 New Phytologist Trust www.newphytologist.com turn ubiquitinated and degraded in a nitrogen-dependent manner (Hu et al, 2019). Moreover, the Ub E3-ligase NLA, which contains an N-terminal SPX domain, controls nitrogen transport and nitrogen-dependent senescence by regulating the Ub-mediated degradation of nitrogen transporters and ORE1 (a key transcription factor for leaf senescence) (Peng et al, 2007;Liu et al, 2017;Park et al, 2018). Interestingly, NLA also controls the concentration of Pi transporters (Lin et al, 2013;Park et al, 2014;Yue et al, 2017), making it a hub that integrates signaling for both of these nutrients (Fig.…”

Section: Inositol Pyrophosphate Signaling In Plantsmentioning

confidence: 99%

Identity and functions of inorganic and inositol polyphosphates in plants

2019

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Inorganic polyphosphates (polyPs) and inositol pyrophosphates (PP-InsPs) form important stores of inorganic phosphate and can act as energy metabolites and signaling molecules. Here we review our current understanding of polyP and inositol phosphate (InsP) metabolism and physiology in plants. We outline methods for polyP and InsP detection, discuss the known plant enzymes involved in their synthesis and breakdown, and summarize the potential physiological and signaling functions for these enigmatic molecules in plants.

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Arabidopsis NITROGEN LIMITATION ADAPTATION regulates ORE1 homeostasis during senescence induced by nitrogen deficiency

Cited by 74 publications

References 35 publications

Inorganic Nitrogen Form Determines Nutrient Allocation and Metabolic Responses in Maritime Pine Seedlings

Inorganic Nitrogen Form Determines Nutrient Allocation and Metabolic Responses in Maritime Pine Seedlings

Arabidopsis ubiquitin‐specific proteases UBP12 and UBP13 shape ORE1 levels during leaf senescence induced by nitrogen deficiency

Identity and functions of inorganic and inositol polyphosphates in plants

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