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Review Article

PEPCK Gene for Enhanced Photosynthesis and Salinity Stress Tolerance in Rice: A Review

Suchismita Prusty1, Ranjan Kumar Sahoo1,*
1Department of Biotechnology, Centurion University of Technology and Management, R. Sitapur-761 211, Odisha, India.

ABSTRACT

Phosphoenolpyruvate carboxykinase (PEPCK) is an enzyme of the lyase family utilized in the gluconeogenesis pathway in plants. It converts oxaloacetate into Phosphoenolpyruvate (PEP) and carbon dioxide. PEPCK acts as a prime decarboxylase cytosolic enzyme and may have exhibited a positive response against salinity (main abiotic stress) stress in certain plants. Transgenic plants (C3) with high-level expression of C4 enzymes PEPC or PEPCK can serve as a perfect example for increasing the crop photosynthetic capacity through genetic engineering. In this review, we have focused on the recent advances in the utilization of the PEPCK gene and its role in increasing photosynthesis as well as in abiotic stress tolerance.

INTRODUCTION

Phosphoenolpyruvate carboxykinase (PEPCK) is a protein which acts as a prime decarboxylase cytosolic enzyme. Involvement of PEPCK has been reported in the gluconeogenesis, TCA cycle, metabolism of malate, nitrogen sugar, organic acid and amino acid along with maintaining pH stability (Liu et al., 2021). Besides metabolism, PEPCK has been involved in different stress tolerance activities. PEPCK gene’s role in C4 and CAM type photosynthetic plants is well recognized, along with other roles it plays in biosynthetic and energy metabolism in non-photosynthetic tissues of C4 plants (Aubry et al., 2011). The main reason behind crop loss is environmental stress (abiotic and biotic) which hampers the growth of the plant by interfering with its morphology, physiology and biochemistry. Various environmental parameters, including heat, cold, drought and salinity have a substantial impact on crop yield, resulting in yield loss for more than 50% of total quantity (Haggag et al., 2015). Previous studies have shown that, among abiotic stresses, salinity stress preoccupies the second rank after drought (Ghosh et al., 2012). Saline terrain makes for 20% (900 million hectares) of irrigated agricultural land and 6% farming land (Ismail and Horie, 2017). Moreover, the stressed area is expected to grow to 50% of irrigated land by 2050 (Kumar et al., 2020). India accounts for about 8.4 million hectares of affected areas (Ghosh et al., 2012). Each year, salinity deteriorates around 1% of the world’s agricultural land (2 million hectares), resulting in lower or no crop output (Yadav et al., 2020).

Rice (Oryza sativa L.) is second major staple crops, consumed by more than half of the World’s population (Feist and Sitko, 2018). Being a glycophyte, rice is prone to salt stress (Sahi et al., 2006). The net yield loss due to salinity is nearly about 30-50% of total yield. It has previously been reported that salt stress inhibits grain yield significantly more than it does to vegetative development in rice (Joseph and Mohanan, 2013). In some plants, it is observed that salinity stress results in the accumulation of glucose, sucrose, citrate, glutamate and malate. The Phosphoenolpyruvate carboxykinase (PEPCK) gene induction and functional significance in abiotic and biotic stress tolerance have been proven in various investigations (Song et al., 2021). According to some theories, PEPCK may have exhibited a positive response against salinity stress in certain plants but the mechanism of action on rice is still unclear (Huang et al., 2015).  This article is based upon different roles and uses of PEPCK gene and its possible biochemical, morphological and physiological effects on rice plant while conferring the mechanism of salinity tolerance and enhancing the photosynthetic activity in the plant.
 
Role of PEPCK
 
Phosphoenolpyruvate carboxykinase (PEPCK) is an ubiquitous, ATP-dependent cytosolic enzyme, present in the bundle sheath cells of almost all flowering plants, operating as a core decarboxylase agent where the activation occurs by dephosphorylation (Fig 1). PEPCK acts as the prime factor for CO2 concentration regulation via RuBisCo (Brown et al., 2016). PS II activity is maintained in both the mesophyll and bundle sheath cells of C4 plants, consisting of two types of C4 cycles. The first cycle is a carbon cycle comprising aspartate and PEPCK and the second is a malate cycle encompassing NAD-ME, which generates NADH, which when oxidized, facilitates the production of ATP for the PEPCK reaction. The carbon dioxide so produced as a by-product from the PEPCK and NAD-ME reaction is utilized in the dark reaction by means of RuBisCo. The affinity of the PEPCK gene for substrates including CO2 is highly affected by the concentration of metal ions and the ratio of ATP:ADP. PEPCK1 is a crucial protein-coding gene which participates in gluconeogenesis, metabolism of malate and TCA cycle (by catalysing the conversion of OAA to PEP) which is essential for closure of stomata in total dark condition (Fig  2). PEPCK2 mainly encodes a mitochondrial enzyme that catalyses the conversion of OAA to PEP, involved in the adipocytokine signalling pathway and glucose metabolism (Stockebrand, 2016). Several reports suggested about its involvement in fermentation pathways, in providing innate and adaptive immunity and acting against low temperature, salinity as well as flooding stress (Wang et al., 2021).

Fig 1: Photosynthetic metabolism showing role of PEPCK.



Fig 2: (a) Probable occurrences happening in guard cell during stomatal closure.



Various attempts have been made for the incorporation of the single cell, showing C4 cycle-like pathway into the parenchyma cells of C3 plants (Miyao et al., 2011). In the C3 plants like rice, PEPCK acts as a decarboxylating agent of C4 acids through a partially occurring C4 cycle inside its vascular system (Martin et al., 2011). Rice leaves express PEPCK in their vascular parenchyma, hydathodes and stomata. It may facilitate the retrieval of Asparagine (Asn) from the xylem in hydathodes and vascular cells. Among the poaceae family, two of its subfamilies named as Chloridoideae and Panicoideae have shown evolvement of the PEPCK cycle pathway. The mutated PEPCK1 plants exhibits enhanced stomatal conduciveness and moderate responses to darkness by stomata in comparison to the wild type in the course of the light-dark transient period, implying that stomata are getting squeezed in the open position (Penfield et al., 2012). Through this we can control and diminish the transpiration rate that would result in enhancement of water content and reduction in photorespiration which as a result would ensure more absorption of carbon-dioxideas well as elevate the photosynthetic rate and increase the vitality of plants that is open to variety of environmental stresses (especially salt stress), improving the productivity of plant along with prompting its high yielding.
 
Stress on plants
 
The growth and maturity of plants are highly affected by environmental stresseslike drought, salinity, heat, cold and heavy metal. These stresses lead to photosynthetic depletion, reduction in germination percentage, biomass curtailment amplification in the reactive oxygen species (ROS). This provokes the changes of biochemical as well as the molecular level of plants that results in morphological and physiological variation in important crops like rice (Hadiarto and Tran, 2011) (Fig 3). The guesstimated value in yield diminution due to negative outcomes of abiotic stresses on rice is calculated to be approximately 70% (Hasanuzzaman et al., 2019). For adaptation to these kinds of environmental stresses, the plant promotes innumerable genes such as PEPCK, PEPC etc. at the transcriptional level and escalates its endurance capacity. This is a much involute process reliant on the extremity of stress, determining the cell or organ reaction along with the developmental stage during stress (Claeys and Inze, 2013). Some adaptation methods to stress by plants include revampingin soluble sugar level (trehalose, sucrose and fructans), sterols and accumulation of several substances like amino acids and/or its derivatives (tryptophan and proline), alcohol, ammonium compounds (glycinebetaine, polyamines) and others in the plant (Wewer et al., 2011). An increase in carbohydrate metabolism also allows the plant to successfully resume photosynthesis and cope up with stress (Bailey-serres and Voesenek, 2010).

Fig 3: Effects and results of different biotic and abiotic stress on the physiological, morphological and biochemical of rice plant.


 
Salinity stress
 
Soil is said to be saline when its pH ranges between 7- 8.5 with electrical conductivity (EC) less than or equal to 4 ds/m i.e., osmosis pressure level is approx. 0.2Mpa and NaCl amount about 40 Mm. High salinity affects almost one billion hectares ofcultivable lands all over the world, hence is a matter of concern and focus (Sahoo et al., 2014) (Fig 4). High-level salinity obstructs the absorption of nutrients as well as water from the soil, hampering the growth of plants and the maturation of seedlings. Rice being a glycophyte is very much sensitive to salinity stress especially during the start of the vegetative stage and late reproductive stage. Most affected organelles due to salinity stress are the mitochondria and the chloroplast, affecting the content of chlorophyll, hence reducing the photosynthetic efficacy of the plant (Robles et al., 2019). It also has an adverse impact on enzymes regulating the Calvin cycle (Bai et al., 2017). Many protrusions in the thylakoid region of chloroplast had been observed resulting in its rupture (Yamane et al., 2018). Transition in the anatomy of the leaf along with shrink in leaf zone has also been observed in rice plants (Wankhade et al., 2010). Salinity stress also results in disorganization of lipid and protein in the plasma membrane, affecting the permeability of membrane as well as leading to ion disproportion and hyperosmotic and/or hyper ionic stresses and toxicity, resulting in the death of the rice plant (Nessim and Kasim, 2019). A remarkable drop in the number of tillers, panicles and spikelet have been observed which may lead to plant sterility resulting in loss of grain production (Joseph and Mohanan, 2013). Moreover, the Reactive Oxygen Species (ROS) productivity is being directly proportional to salinity contents in the soil which increases the risk (Tuteja et al., 2013). In order to protect itself directly or indirectly, the plant up-regulates various genes in retaliation to salinity stress (Tuteja et al., 2013). Induction of specified foreign genes or de-novo genes in the plants may provide a biotic and abiotic stress resistance factor (Jia et al., 2013). The enormous genes from various pathways of biochemical processes including the compartmentalization of sodium ions, signal transduction, oxidative stress protection, carbon metabolism and exclusion transport, etc., are held responsible for toleration of salinity stress. Certain molecular and biochemical machinery as directed by endogenous hormones of the plant also helps them to confer stress tolerance (Osakabe et al., 2013). Through microarray evaluation of the salinity tolerant transgenic rice varieties, we found that metabolic pathways like sugar metabolism, hormone metabolism and other pathways like proline biosynthesis were notably overexpressed which is may be due to playing a part in salinity stress tolerance (Sahoo et al., 2014). Salt stress may be reduced by increasing sugar level which also proffers membrane stability via ROS detoxification and interacting with head groups of phospholipids as delineated in various crops including rice (Cha-um et al., 2009). As stated above that the activity of PEPCK regulates the mechanism of malate, TCA cycle and gluconeogenesis, incorporation of this enzyme could confer salinity tolerance in the rice plant.
 

Fig 4: Effect of salt stress on plant showing its morphological, biochemical and physiological responses and how the crop productivity is affected.



Improvising rice productivity to feed the population
 
Rice (Oryza sativa L.), the monocot species of grasses, is a global predominant cereal crop for being consumed as a major staple food in many countries (Kumar, 2021). It is the basic sustenance for more than half of the planet’s population and is the second most-produced cereal after maize. Although consumption of rice is equally done among all income classes, but the livelihood of penurious people mainly relies on it for sensible diet as well as income. For poverty-stricken people, rice is the principal source of energy laced with many healthful compounds providing them a source of a balanced diet (Chun and Y, 2018). The adaption of novel ways to eradicate the gap between the supply and demand rates is necessary for the achievement of global food security of rice. As per the data by International Rice Research Institute (IRRI) in 2009, the top most rice cultivating countries include (in descending order) China, India, Vietnam, Thailand, Japan and Brazil, which also happens to be top in consuming it (Fig 5). As per the statistics suggested by IRRI, India in 2009, milled rice consumption is about 8,54,30,000 metric tonnes and the amount of rice that is exported is approximately 25,00,000 metric tonnes (Fig 6 and Fig 7).

Fig 5: Data showing major rice producing and consuming countries mainly India and China from year 2006- 2020.



Fig 6: Data showing worldwide export of produced rice from different countries.



Fig 7: Data showing worldwide import of rice to different countries.



Very crucial major has been taken to deal with possible solutions for accelerating the production of rice by enhancing its photosynthetic efficiency. The prime focus has been high yielding genetically modified rice varieties and utilizing new posts-harvest technologies for loss depletion. Unfortunately, most of the genes that could suppress the activity of stresses are not present in the original genetic pool of rice.

Genetic engineering seems to be the perfect approach as a solution to deal with these problems. We can develop new rice varieties with proper protocols to deal with several issues in the current scenario (Table 1). Evaluation and selection of the resultant clones becomes easy with the help of an efficient reproducible plant regenerating protocols that are available for the target genotypes (Table 2) (Rachmawati and Anzai, 2006). We are gradually progressing towards the C4 rice project by modifying biochemical and anatomical characteristics. In approach to achieve C4 rice, modest amounts of C4 photosynthesis added around existing veins of the plant may offer advantages of enhanced photosynthesis.

Table 1: List of transgenic rice improved for providing tolerance towards abiotic stress.



Table 2: List of transgenic rice improved for providing better yield and increasing grain quality.



The higher ATP demand of C4 photosynthesis can be supplied by an increase in cyclic electron transportation in BS cells. Vein space patterns must be altered such that leaf veins are nearer to each other, including larger chloroplasts and the BS cells must be “modified” for improved photosynthesis, in order to implement Kranz anatomy in rice. Previous studies evidenced that transferring the PEPCK gene from Urochloa panicoides to rice resulted in effective expression. There the carbon flow was changed toward a C4 route, but neither photosynthesis nor growth were noticeably enhanced (Burnell, 2008).

A study to focus on the mechanism for increasing the photosynthetic activity of rice by the over expression of PEPCK gene through models integrating C3 and C4 photosynthetic mechanism could build the gap towards the approach for C4 rice project.
 
Overcoming stress
 
Various morpho-physiological researches aiming for inducing salinity tolerant variants of rice have been carried out where the focus has been to amplify the genetically diversity of the original genotypes, generating de-novo genes. There are transgenic salt-tolerant varieties released in the market for commercial purposes all over the world (Table 3). Halophytic plants are able to aggregate it in the vacuole of the cell which prevents salt accumulation in the cytosol thereby preserving a high cytosolic K+/Na+ ratio. Synthesis of osmolytes, different ion transporters and regulation of the machinery in transcriptional and translational process profferssalinity tolerance (Sahi et al., 2006). Studies have also shown that enhancing the photo synthetic and antioxidant capability may also provide a solution for salinity stress (Tuteja et al., 2013). Aggregation of starch and sugar molecules has proven to prevent the ruinous effect of salt stress by acting as an osmoticum, providing an energy source and checking cell death,improving rice plants’growth and development. For example, tolerant variants’ roots have more sugar content than the susceptible rice variety (Nemati et al., 2011). Enhancing the activity of the C4 type enzyme PEPCK in C3 type rice plant can be used to counteract salinity stress which has been successfully implemented in other species like tomato (C3) sugarcane (C4) etc. This enzyme is involved in the gluconeogenesis which helps to increase the sugar content. Its count in the Krebs cycle which reduces photorespiration and transpiration. Its also included in the malic acid metabolism that hepls in the stomatal conductance. As PEPCK is involved in all the above stated metabolic processes, we can use PEPCK gene incorporated rice plant that would help to confer against stress along with enhancing the photosynthetic ability as well as its vitality. This as a result would increase the productivity and yield through which we can fulfil the demand of population as well as raise the economic welfare.

Table 3: List of genetically engineered transgenic rice improved for providing salinity stress tolerance.

CONCLUSION

Abiotic stress tolerance in plants is a highly complex process that includes multiple biochemical and physiological mechanisms. Many genes can be used to generate transgenic plants providing high-stress tolerance traits. Transgenic plants providing stress tolerance would increase productivity and elevate commercial values, which is crucial for further agricultural and economic advancements.

CONFLICT OF INTEREST

The authors declare that they have no conflict of interest.

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