The Research Progress of Plant Arginase and the Roles in Stresses  

Xiaoxu Zhang1 , Xinxin Zhang1 , Tetsuo Takano2 , Shenkui Liu1 , Yuanyuan Bu1
1. Key Laboratory of Saline-alkali Vegetation Ecology Restoration in Oil Field (SAVER), Ministry of Education, Alkali Soil Natural Environmental Science Center (ASNESC), Northeast Forestry University, Harbin 150040, China
2. Asian Natural Environmental Science Center (ANESC), The University of Tokyo, Tokyo 188-0002, Japan
Author    Correspondence author
Cell Biology and Biophysics, 2014, Vol. 3, No. 1   doi: 10.5376/cbb.2014.03.0001
Received: 03 Mar., 2014    Accepted: 05 Apr., 2014    Published: 28 May, 2014
© 2014 BioPublisher Publishing Platform
This is an open access article published under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Preferred citation for this article:

Zhang et al., 2014, The Research Progress of Plant Arginase and the Roles in Stresses, Cell Biology and Biophysics, Vol.3, No.1 1-6 (doi: 10.5376/cbb.2014.03.0001)

Abstract

The arginase is responsible for catalyzing L-arginine into L-ornithine and urea, and it is one of the key enzymes of polyamine cycle and urea cycle. In this paper, we reviewed the function analysis and the roles of plant arginase in stress resistance. It is clearly that arginase plays an important role in the response of adversity stress, but the mechanism of arginase gene regulating the plant tolerance is still need to research.

Keywords
Argianse; Stress; Ammonia toxication

Introduction
Arginine (ARG) is one of the nonessential amino acids, and it plays multiple roles in plant. Arginine is not only a part of protein, but is also the medium of Nitrogen transport and storage (Micallef et al., 1989). Moreover, it is the precursor of polyamines and proline synthesis (Brauc et al., 2012; Flores et al., 2008; Jenkinson et al., 1996). During the seed germination and early seeding growth, proteins are the major form of nitrogen storage. At this period, plants need to accomplish a lot of metabolic activity to complete the normal growth and development. The redistribution of storage protein is very important for plant regeneration, such as the seed germination (Rentsch et al., 2007). It has been reported that the main form of storage protein in seed is arginine (Chatthai et al., 1998; King et al., 1997). For example, during the seed germination in loblolly pine (Pinus taeda L.) , the storage protein in macrogametophyte is degradated with a large increase of amino acid in the seeding, and the most abundant amino acid is arginine (Todd et al., 2001), which makes up about almost half of nitrogen stored in the macrogametophyte storage proteins (King et al., 1997). Therefore, arginine plays an important role in the process of nitrogen metabolism during early seeding development, which is also the main source of nitrogen for polyamine biosynthesis and other nitrogen-containing compounds (Todd et al., 2001).

The earliest reports about arginine transport was found in animals and fungi (Freedland et al., 1984; Yu et al., 1992), then, the researcher found that arginine is transported into mitochondria and is degradated by arginase in chick kidney cells (Kadowaki et al., 1976). Similarly, the arginine is degraded in mitochondria by arginase, but the exact mechanism is not clear (Goldraij et al., 1999). As far as we know, arginine can be broken down by three different enzymes in vivo, namely arginase (or arginine amidohydrolase, ARGAH), arginine decarboxylase (ADC) and nitric oxide synthetase (NOS). Among them, arginase is the enzyme that can catalyze L-arginine into L-ornithine and urea specifically. As we know, L-ornithine is the precursor of polyamine synthesis, and urea is involved in the nitrogen metabolic cycle, which is also the precursor of nitrite, nitrate and NO synthesis (Brownfield et al., 2008a). Polyamine is the scavenger of reactive oxygen species (Wimalasekera et al., 2011), and also is the stress signal in plants, regulating plant growth and a series of biotic and abiotic stress (Wang et al., 2011; Wu et al., 1998). Urea participates in the metabolic cycle (Zonia et al., 1995), and nitrogen is the basic nutrition, which is necessary for plant development and growth. Therefore arginase plays an important role in plant resistance to stress, at the same time, the genetic improvement of crops focusing on arginase is important for molecular breeding (Figure 1).

 

 

Figure 1 The pathway of Arginine Metabolism in plant

 
Function Analysis of Arginase under Stresses in Plants
According to a large number of previous studies we know that the majority of environmental stress, such as chilling, dehydration, high salt and other stresses will lead to excessive accumulation of ROS rapidly in the vivo of plants. The homeostasis for ROS is very important for the defense of stress in plants. The accumulation of excess ROS products leads to oxidative stress and may cause cell death (Apel et al., 2004; Mittler et al., 2004; Zhu et al., 2002). Studies have shown that polyamines and NO in plants are stress signals that can regulate plant development and a range of biotic and abiotic stress responses (Chen et al., 2004; Lozano-Juste et al., 2010; Neill et al., 2008; Wang et al., 2011; Zhao et al., 2007). Under abiotic stress conditions, the accumulation of ROS in ARGAHs mutant of Arabidopsis is significantly reduced, suggesting that inhibition of the expression of Arabidopsis ARGAHs can increase the tolerance to the dehydration, high salt and chilling. And the result of arginase gene overexpression lines shows opposite characteristics.

For example, Shi and other researchers proved that the negative regulation of ARGAHs in Arabidopsis is based on the regulation of arginase to arginine metabolism and the accumulation of ROS (Shi et al., 2013). Other studies show that the manipulation of ARGAHs expression can change the activities of a variety of antioxidant enzymes, including SOD, CAT, POD, in many kinds of stresses (Shi et al., 2013). Botrytis cinere induces the expression of ARGAH2 and ARGAH2 overexpression lines show an increased in the resistance to Botrytis cinere (Brauc et al., 2012; Brownfield et al., 2008b). Previous studies showed that the lines with Arabidopsis arginase genes knocking out leads to an increase in NO accumulation, while, the overexpression of ARGAH2 gene enhances the development of callus under clubroot infection. Studies have shown that in tomato, LeARG2 was induced by wounding, but LeARG1 won’t (Chen et al., 2004). Therefore, arginase can respond to a variety biotic and abiotic stress by regulating the pathways of arginine and polyamine (Shi et al., 2013).

The Relationship between Arginase and Ammonia Toxicity

Nitrogen is one of the necessary macro-element for plant growth, and it has an important role in plant metabolism, growth and development (Brix et al., 2002; Dyhr et al., 1996; Guo et al., 2007; Romero et al., 1999). The plant gets the nitrogen source by absorption from the soil and the assimilation when growing up. In order to make the crop grow better, fertilizer is usually added into the soil in agriculture. Urea is a kind of effective fertilizer, which is widely used all over the word, and more than 50 percent of nitrogen is provided in the form of urea (Glibert et al., 2006). Furthermore, because of that the urea in soil exists in the form of ammonia ion after hydrolyzation, and ammonia ion loses less nitrogen after denitrogenation under waterlog. The urea is widely used in rice production (Dobermann et al., 2000). Even though, urea is a good fertilizer in agriculture, it can lead to poison to the plants, such as the inhibition of seed germination, a weakness in seeding growth, damage of roots, especially in alkali soil (Bremner et al., 1996; Fan et al., 1995; Haden et al., 2011a). It is pointed out that the adverse effect on plants is caused by the ammonia, which is produced by the hydrolization of areas in soil, and not by the urea itself (Bremner et al., 1989).

The forms of nitrogen that plants can utilize are nitrate, ammonium radical, alkaline air and Nitrogen gas. For most of plants, using NO3- and NH4+ combination is better than providing only one kind of the two compounds as nitrogen source (Chaillou et al., 1991; Claussen et al., 2002; Tylova-Munzarova et al., 2005; Zou et al., 2005). Moreover, the plant growth will be inhibited in the condition that only the NH4+ is offered as a nitrogen source, also plants will display the symptom of NH4+ toxicity, such as the colour change of leaves, the complete suppression of growth and the depression of root stem percentage (Gerendás et al., 1997). Contradictory, the NO3- will be stored in the sap vesicle of plant cells when plant absorbs excess NO3-, and it won’t result in injurious effects on plants (Konnerup et al., 2010).

In the water solution, NH3 and NH4+ are in equilibrium, and the partial pressure of NH3 increases with the raising of pH value (Haden et al., 2011b). The excess accumulation of NH3 in the alkaline saline soil may lead to two kinds of toxicity to plants. One is the NH3 toxicity, which is caused by the directive diffusion of gaseousness or dissolved NH3 into plant cells. It disturbs the regulation of pH value in vivo, and then obstructs the normal metabolic activity leading to poisoning of plant cells (Kosegarten et al., 1997; Wilson et al., 1998). It is found that the ammonia toxicity symptom was observed in many crops including maize, wheat, barley, sorghum and rye (Haden et al., 2011a).

As we know, L-arginine can be specificitly hydrolyzed by argianse into urea and L-ornithin. Urea is hydrolyzed into ammonia and carbamate, while, the carbamate will resolve into carbomdioxide and two molecules of ammonia (Real-Guerra et al., 2013). If there is an overdose of ammonia produced, it can lead to poisoning of the cells. Arginase is one of the key enzymes in the urea cycle, and it is proved to be important in ammonia detoxification. For example, the increase expressions of argianse I and omithine transcarbamylase of human being cut down the ammonia detoxification in HepG2 cells (Mavri-Damelin et al., 2007). Also, it has business with arginase II, glutamate synthase, ASS and so on. The result is consistent with the report that argianse plays a defense function against the cell’ death induced by ammonia in gastric epithelium cells (Tang et al., 2012). However, there are no reports about the relationship between argianse and ammonia toxicity. But we can stipulate that arginase negative regulates the tolerance of plants under ammonia. Nevertheless, a large a mount of reach is required to confirm this.

Prospection
So far, there are lots of studies which focus on the role for arginase in plant responses to stress and scientists have gotten many progresses. But there are still a lot of things unknown about the entire mechanism and pathway of nitrogen metabolism. And the mechanism of arginase response to stress is also not clear. So studies are needed to find out all of these mechanisms. And it is useful to understand the nitrogen metabolism. Furthermore, we can find out a method to enhance the resistance to stress through the study of arginase in the plant.

Acknowledgements
This work was supported by specific fund for forest scientific research in the public welfare (201404220) and Program for Changjiang Scholars and Innovative Research Team (PCSIRT, IRT13053).

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