Phylogenetic analysis and photoregulation of siroheme biosynthesis genes: uroporphyrinogen III methyltransferase and sirohydrochlorin ferrochelatase of Arabidopsis thaliana

Garai, Sampurna; Joshi, Naveen Chandra; Tripathy, Baishnab C.

doi:10.1007/s12298-016-0363-1

Cited by 6 publications

(5 citation statements)

References 31 publications

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“…The promoters of SiR, NII , and NIA2 have light responsive elements (LRE). Interestingly, both siroheme biosynthetic genes i.e., UPM1 and SIRB are also upregulated by light and have LRE in their promoters for interaction with the phytochromes (Garai et al, 2016 ). This demonstrates the pivotal role of light in the regulation of most of the N and S assimilation pathway.…”

Section: Introductionmentioning

confidence: 99%

Alleviation of Nitrogen and Sulfur Deficiency and Enhancement of Photosynthesis in Arabidopsis thaliana by Overexpression of Uroporphyrinogen III Methyltransferase (UPM1)

Garai

Tripathy

2018

Front. Plant Sci.

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Siroheme, an iron-containing tetrapyrrole, is the prosthetic group of nitrite reductase (NiR) and sulfite reductase (SiR); it is synthesized from uroporphyrinogen III, an intermediate of chlorophyll biosynthesis, and is required for nitrogen (N) and sulfur (S) assimilation. Further, uroporphyrinogen III methyltransferase (UPM1), responsible for two methylation reactions to form dihydrosirohydrochlorin, diverts uroporphyrinogen III from the chlorophyll biosynthesis pathway toward siroheme synthesis. AtUPM1 [At5g40850] was used to produce both sense and antisense plants of Arabidopsis thaliana in order to modulate siroheme biosynthesis. In our experiments, overexpression of AtUPM1 signaled higher NiR (NII) and SiR gene and gene product expression. Increased NII expression was found to regulate and enhance the transcript and protein abundance of nitrate reductase (NR). We suggest that elevated NiR, NR, and SiR expression must have contributed to the increased synthesis of S containing amino acids in AtUPM1overexpressors, observed in our studies. We note that due to higher N and S assimilation in these plants, total protein content had increased in these plants. Consequently, chlorophyll biosynthesis increased in these sense plants. Higher chlorophyll and protein content of plants upregulated photosynthetic electron transport and carbon assimilation in the sense plants. Further, we have observed increased plant biomass in these plants, and this must have been due to increased N, S, and C assimilation. On the other hand, in the antisense plants, the transcript abundance, and protein content of NiR, and SiR was shown to decrease, resulting in reduced total protein and chlorophyll content. This led to a decrease in photosynthetic electron transport rate, carbon assimilation and plant biomass in these antisense plants. Under nitrogen or sulfur starvation conditions, the overexpressors had higher protein content and photosynthetic electron transport rate than the wild type (WT). Conversely, the antisense plants had lower protein content and photosynthetic efficiency in N-deficient environment. Our results clearly demonstrate that upregulation of siroheme biosynthesis leads to increased nitrogen and sulfur assimilation, and this imparts tolerance to nitrogen and sulfur deficiency in Arabidopsis thaliana plants.

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Section: Introductionmentioning

confidence: 99%

Alleviation of Nitrogen and Sulfur Deficiency and Enhancement of Photosynthesis in Arabidopsis thaliana by Overexpression of Uroporphyrinogen III Methyltransferase (UPM1)

Garai

Tripathy

2018

Front. Plant Sci.

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“…Siroheme plays a crucial part in the reduction of nitrate and sulfate as a kind of accessorial factor. Since plants can utilize ammonium nitrogen and sulfur amino acid, instead of nitrate and sulfate directly from soil, the Fe 2+ that chelated in the center of siroheme is capable of assisting the electronation of reduction of nitrate and sulfate (Hu et al 2015;Garai et al 2016).…”

Section: Sirohemementioning

confidence: 99%

5-Aminolevulinic acid (ALA) biosynthetic and metabolic pathways and its role in higher plants: a review

et al. 2018

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Crop productivity is restricted by various abiotic stresses such as drought, salinity, heat, and cold. Many efforts have been taken to decrease the inhibition of plant growth by alleviating the abiotic stresses. Exogenous applications of hormones, plant growth regulators, and/or small signaling molecules have been reported as a means to enhance plant resistance to stress. One of the small signaling molecules utilized is 5-aminolevulinic acid (ALA) that has been shown to enhance plant growth under abiotic stress. As a metabolic intermediate in higher plants, ALA is a precursor of all tetrapyrroles such as chlorophyll, heme and siroheme. The pathway towards biosynthesis upstream and the metabolism downstream of ALA contains multiple regulatory points that are affected by positive/negative factors. However, report about the regulatory aspects of the ALA metabolic pathway and the role of ALA in stimulating physiochemical processes in higher plants under stress have not been collated and summarized systematically. In this regard, we summarize recent developments in understanding the mechanisms of plant responses to abiotic stress which are affected by ALA as well as new information on the metabolic pathway of ALA. We find that exogenous application of ALA can enhance some key physiological and biochemical processes in plants such as photosynthesis, nutrient uptake, antioxidant characteristics and osmotic equilibrium, however, more in-depth research on the specific mechanisms are needed.

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“…The AtSirB is responsible for N and S assimilation in plants, and these processes are dependent on light for proper utilization of N and S compounds taken up from the soil (LaBrie and Crawford, 1994;Bork et al, 1998). We have shown that the AtSirB is a lightregulated gene that is present in a minimal amount in etiolated tissues and highly upregulated after light exposure due to light-responsive elements in its promoter (Garai et al, 2016). It may be inferred that similar to the light-regulated expression of apoenzyme, the gene expression of the enzyme required to synthesize the cofactor is also photo-regulated (Becker, Foyer, and Caboche, 1992;Garai et al, 2016;.…”

Section: Discussionmentioning

confidence: 93%

“…The AtSirB is responsible for N and S assimilation in plants, and these processes are dependent on light for proper utilization of N and S compounds taken up from the soil (LaBrie and Crawford, 1994; Bork et al, 1998). We have shown that the AtSirB is a light-regulated gene that is present in a minimal amount in etiolated tissues and highly upregulated after light exposure due to light-responsive elements in its promoter (Garai et al, 2016). It may be inferred that similar to the light-regulated expression of apoenzyme, the gene expression of the enzyme required to synthesize the cofactor is also photo-regulated (Becker, Foyer, and Caboche, 1992; Garai et al, 2016; Rajasekhar and Mohr, 1986).…”

Section: Discussionmentioning

confidence: 99%

“…In addition, the expression of SirB, coding for sirohydrochlorine ferrochelatase (SirB) responsible for synthesizing the cofactor of siroheme that binds to both NiR and SiR, is also light-regulated. The promoter of SirB has light responsive elements (LREs) that photo-modulate SirB expression (Garai et al, 2016). Thus, the expression of both apoprotein and the cofactor of NiR and SiR is light-regulated.…”

Section: Introductionmentioning

confidence: 99%

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Overexpression of Sirohydrochlorin Ferrochelatase Boosts Nitrogen Sulfur and Carbon Utilization inArabidopsis thaliana

Joshi,

Tripathy

2024

Preprint

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Nitrogen deficiency in the soil is a significant agronomic problem, and the application of nitrogenous fertilizers to the soil has environmental concerns, such as sodic soil and the emission of greenhouse gases. To increase the nutrient use efficiency, the cDNA of AtSirB coding for sirohydrochlorin ferrochelatase, responsible for Fe insertion to the tetrapyrrole moiety of sirohydrochlorin, was overexpressed in Arabidopsis thaliana under the control of 35S promoter for increased synthesis of siroheme. The siroheme is a cofactor for the plastidic enzymes nitrite reductase (NiR) and sulfite reductase (SiR), which reduces nitrite and sulfite to ammonium and sulfide, respectively. A three-step process including methylation, oxidation, and ferro-chelation produces siroheme from uroporphyrinogen III, an intermediate of chlorophyll (Chl) biosynthesis. The NiR and SiR gene expression and protein abundance increased in the over-expressers due to the increased AtSirB protein level. It resulted in an increase in N and S assimilation and enhanced protein content of over-expressers. Conversely, the total protein content decreased in antisense plants due to reduced NR and NiR activities. AtSirB over-expressers had higher protein and Chl contents and increased photosynthetic rate and biomass. Under N and S limitation, the protein, Chl, and photosynthetic electron transport rates in AtSirB over-expressers were higher than in WT. Results demonstrate that the SirB that hijacks uroporphyrinogen from the chlorophyll biosynthesis pathway is a crucial player in N and S assimilation. The siroheme is limiting for efficient nitrate and sulfate reduction and utilization. SirB could be genetically manipulated to increase crop productivity for sustainable agriculture.

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Phylogenetic analysis and photoregulation of siroheme biosynthesis genes: uroporphyrinogen III methyltransferase and sirohydrochlorin ferrochelatase of Arabidopsis thaliana

Cited by 6 publications

References 31 publications

Alleviation of Nitrogen and Sulfur Deficiency and Enhancement of Photosynthesis in Arabidopsis thaliana by Overexpression of Uroporphyrinogen III Methyltransferase (UPM1)

Alleviation of Nitrogen and Sulfur Deficiency and Enhancement of Photosynthesis in Arabidopsis thaliana by Overexpression of Uroporphyrinogen III Methyltransferase (UPM1)

5-Aminolevulinic acid (ALA) biosynthetic and metabolic pathways and its role in higher plants: a review

Overexpression of Sirohydrochlorin Ferrochelatase Boosts Nitrogen Sulfur and Carbon Utilization inArabidopsis thaliana

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