The expression of cyanobacterial glycolate–decarboxylation pathway genes improves biomass accumulation in Arabidopsis thaliana

Bilal, Misbah; Abbasi, Anum Zeb; Khurshid, Ghazal; Yiotis, Charilaos; Hussain, Jamshaid; Shah, Mohammad Maroof; Naqvi, Tatheer Alam; Kwon, Suk‐Yoon; Park, Youn‐Il; Ahmad, Raza

doi:10.1007/s11816-019-00548-x

Cited by 7 publications

(13 citation statements)

References 23 publications

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“…Previous studies reported that integration of photorespiratory bypass enhances the rate of carboxylation due to higher concentration of C i in the vicinity of Rubisco and reduction in levels of photorespiratory intermediates [22][23][24]27,56 . Our model also exhibited an enhanced rate of carboxylation which resulted in an increase in levels of phosphoglycerate (PGA) and a concomitant decrease in Ribulose 1,5 bisphosphate (RuBP) concentration (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…Cyanobacterial glycolate decarboxylation pathway, which employs single gene coded glycolate dehydrogenase (GDH) to catabolize GCA 25 , 26 , 48 has become an attractive target for bypassing photorespiration in C 3 plants. Engineering of cyanobacterial GDH in C 3 plants has also resulted in enhanced biomass production 8 , 27 . Therefore, a systematic evaluation of cyanobacterial decarboxylation pathway using systems biology approach can help to further elucidate its potential in improvement of photosynthesis.…”

Section: Discussionmentioning

confidence: 99%

“…Note that just like the modified Maier et al ’s bypass, cyanobacterial glycolate decarboxylation pathway also yields two molecule of CO 2 as a result of GCA catabolism 24 , 25 . Transformation of individual genes of cyanobacterial glycerate and glycolate decarboxylation pathways in chloroplast of potato and Arabidopsis catabolized GCA and exhibited promising results 8 , 27 .…”

Section: Introductionmentioning

confidence: 99%

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A cyanobacterial photorespiratory bypass model to enhance photosynthesis by rerouting photorespiratory pathway in C3 plants

Khurshid

Abbassi

Khalid

et al. 2020

Sci Rep

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Plants employ photosynthesis to produce sugars for supporting their growth. During photosynthesis, an enzyme Ribulose 1,5 bisphosphate carboxylase/oxygenase (Rubisco) combines its substrate Ribulose 1,5 bisphosphate (RuBP) with CO2 to produce phosphoglycerate (PGA). Alongside, Rubisco also takes up O2 and produce 2-phosphoglycolate (2-PG), a toxic compound broken down into PGA through photorespiration. Photorespiration is not only a resource-demanding process but also results in CO2 loss which affects photosynthetic efficiency in C3 plants. Here, we propose to circumvent photorespiration by adopting the cyanobacterial glycolate decarboxylation pathway into C3 plants. For that, we have integrated the cyanobacterial glycolate decarboxylation pathway into a kinetic model of C3 photosynthetic pathway to evaluate its impact on photosynthesis and photorespiration. Our results show that the cyanobacterial glycolate decarboxylation bypass model exhibits a 10% increase in net photosynthetic rate (A) in comparison with C3 model. Moreover, an increased supply of intercellular CO2 (Ci) from the bypass resulted in a 54.8% increase in PGA while reducing photorespiratory intermediates including glycolate (− 49%) and serine (− 32%). The bypass model, at default conditions, also elucidated a decline in phosphate-based metabolites including RuBP (− 61.3%). The C3 model at elevated level of inorganic phosphate (Pi), exhibited a significant change in RuBP (+ 355%) and PGA (− 98%) which is attributable to the low availability of Ci. Whereas, at elevated Pi, the bypass model exhibited an increase of 73.1% and 33.9% in PGA and RuBP, respectively. Therefore, we deduce a synergistic effect of elevation in CO2 and Pi pool on photosynthesis. We also evaluated the integrative action of CO2, Pi, and Rubisco carboxylation activity (Vcmax) on A and observed that their simultaneous increase raised A by 26%, in the bypass model. Taken together, the study potentiates engineering of cyanobacterial decarboxylation pathway in C3 plants to bypass photorespiration thereby increasing the overall efficiency of photosynthesis.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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A cyanobacterial photorespiratory bypass model to enhance photosynthesis by rerouting photorespiratory pathway in C3 plants

Khurshid

Abbassi

Khalid

et al. 2020

Sci Rep

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“…Moreover, the artificial pathways could simply not operate at a significant level. This might be even more likely in light of the fact that growth improvements similar to those noted above were achieved by the plastidal overexpression of E. coli glycolate dehydrogenase alone, omitting the two glycerate pathway enzymes, in the chloroplast of Arabidopsis (Kebeish et al , ; Bilal et al , ), potato (Nölke et al , ; Ahmad et al , ) and camelina (Dalal et al , ). Similarly, the strong impairments seen after overexpression of glycolate oxidase only in the chloroplast (Fahnenstich et al , ) and which can be cured by concomitant catalase overexpression (Maier et al , ) strongly suggest that the first step of the introduced glycolate oxidation pathway functions as intended.…”

Section: Tailored Photorespiration For Better Crops?mentioning

confidence: 93%

Wasteful, essential, evolutionary stepping stone? The multiple personalities of the photorespiratory pathway

Fernie

Bauwe

2020

The Plant Journal

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The photorespiratory pathway, in short photorespiration, is a metabolic repair system that enables the CO 2 fixation enzyme Rubisco to sustainably operate in the presence of oxygen, that is, during oxygenic photosynthesis of plants and cyanobacteria. Photorespiration is necessary because an auto-inhibitory metabolite, 2-phosphoglycolate (2PG), is produced when Rubisco binds oxygen instead of CO 2 as a substrate and must be removed, to avoid collapse of metabolism, and recycled as efficiently as possible. The basic principle of recycling 2PG very likely evolved several billion years ago in connection with the evolution of oxyphotobacteria. It comprises the multi-step combination of two molecules of 2PG to form 3-phosphoglycerate. The biochemistry of this process dictates that one out of four 2PG carbons is lost as CO 2 , which is a long-standing plant breeders' concern because it represents by far the largest fraction of respiratory processes that reduce gross-photosynthesis of major crops down to about 50% and less, lowering potential yields. In addition to the ATP needed for recycling of the 2PG carbon, extra energy is needed for the refixation of liberated equal amounts of ammonia. It is thought that the energy costs of photorespiration have an additional negative impact on crop yields in at least some environments. This paper discusses recent advances concerning the origin and evolution of photorespiration, and gives an overview of contemporary and envisioned strategies to engineer the biochemistry of, or even avoid, photorespiration.

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“…Recently, we have reported transgenic Arabidopsis thaliana plants independently expressing novel cyanobacterial decarboxylation pathway genes i.e . GDH, HDH, and ODC (GD, HD, and OX transgenic plants) ( Bilal et al, 2019 ). The resultant transgenic plants showed improved growth and chlorophyll content ( Bilal et al, 2019 ).…”

Section: Introductionmentioning

confidence: 99%

Expression of cyanobacterial genes enhanced CO₂ assimilation and biomass production in transgenic Arabidopsis thaliana

Abbasi

Bilal

Khurshid

et al. 2021

PeerJ

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Background Photosynthesis is a key process in plants that is compromised by the oxygenase activity of Rubisco, which leads to the production of toxic compound phosphoglycolate that is catabolized by photorespiratory pathway. Transformation of plants with photorespiratory bypasses have been shown to reduce photorespiration and enhance plant biomass. Interestingly, engineering of a single gene from such photorespiratory bypasses has also improved photosynthesis and plant productivity. Although single gene transformations may not completely reduce photorespiration, increases in plant biomass accumulation have still been observed indicating an alternative role in regulating different metabolic processes. Therefore, the current study was aimed at evaluating the underlying mechanism (s) associated with the effects of introducing a single cyanobacterial glycolate decarboxylation pathway gene on photosynthesis and plant performance. Methods Transgenic Arabidopsis thaliana plants (GD, HD, OX) expressing independently cyanobacterial decarboxylation pathway genes i.e., glycolate dehydrogenase, hydroxyacid dehydrogenase, and oxalate decarboxylase, respectively, were utilized. Photosynthetic, fluorescence related, and growth parameters were analyzed. Additionally, transcriptomic analysis of GD transgenic plants was also performed. Results The GD plants exhibited a significant increase (16%) in net photosynthesis rate while both HD and OX plants showed a non-significant (11%) increase as compared to wild type plants (WT). The stomatal conductance was significantly higher (24%) in GD and HD plants than the WT plants. The quantum efficiencies of photosystem II, carbon dioxide assimilation and the chlorophyll fluorescence-based photosynthetic electron transport rate were also higher than WT plants. The OX plants displayed significant reductions in the rate of photorespiration relative to gross photosynthesis and increase in the ratio of the photosynthetic electron flow attributable to carboxylation reactions over that attributable to oxygenation reactions. GD, HD and OX plants accumulated significantly higher biomass and seed weight. Soluble sugars were significantly increased in GD and HD plants, while the starch levels were higher in all transgenic plants. The transcriptomic analysis of GD plants revealed 650 up-regulated genes mainly related to photosynthesis, photorespiratory pathway, sucrose metabolism, chlorophyll biosynthesis and glutathione metabolism. Conclusion This study revealed the potential of introduced cyanobacterial pathway genes to enhance photosynthetic and growth-related parameters. The upregulation of genes related to different pathways provided evidence of the underlying mechanisms involved particularly in GD plants. However, transcriptomic profiling of HD and OX plants can further help to identify other potential mechanisms involved in improved plant productivity.

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The expression of cyanobacterial glycolate–decarboxylation pathway genes improves biomass accumulation in Arabidopsis thaliana

Cited by 7 publications

References 23 publications

A cyanobacterial photorespiratory bypass model to enhance photosynthesis by rerouting photorespiratory pathway in C3 plants

A cyanobacterial photorespiratory bypass model to enhance photosynthesis by rerouting photorespiratory pathway in C3 plants

Wasteful, essential, evolutionary stepping stone? The multiple personalities of the photorespiratory pathway

Expression of cyanobacterial genes enhanced CO₂ assimilation and biomass production in transgenic Arabidopsis thaliana

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The expression of cyanobacterial glycolate–decarboxylation pathway genes improves biomass accumulation in Arabidopsis thaliana

Cited by 7 publications

References 23 publications

A cyanobacterial photorespiratory bypass model to enhance photosynthesis by rerouting photorespiratory pathway in C3 plants

A cyanobacterial photorespiratory bypass model to enhance photosynthesis by rerouting photorespiratory pathway in C3 plants

Wasteful, essential, evolutionary stepping stone? The multiple personalities of the photorespiratory pathway

Expression of cyanobacterial genes enhanced CO2 assimilation and biomass production in transgenic Arabidopsis thaliana

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Expression of cyanobacterial genes enhanced CO₂ assimilation and biomass production in transgenic Arabidopsis thaliana