The possible interaction of ammonium and auxin polar transport on root system architectures in the two ecotypes of Arabidopsis thaliana

Plant growth requires mineral nutrients from soil environment. It is important for plant to develop its root to import mineral nutrient from environment. Both inorganic nitrogen source and plant hormone auxin influence the root system architecture (RSA). Previous study indicated that polar auxin transport is partly involved in ammonium-inhibition of primary root in an Arabidopsis ecotype, Columbia 0 (Col-0); however, the effect of auxin in other ecotypes remains unclear. The purpose of this study is to describe and examine the effect of TIBA, an inhibitor for the auxin polar transport, in ammonium supply-dependent changes of root development. Two Arabidopsis ecotypes, Col-0 and Landsberg erecta 2 (Ler-2), were used due to their different response to ammonium supply. The changes of the RSA in response to ammonium supply on vertical agar medium containing three levels of TIBA and four levels of ammonium were determined in two ecotypes. The primary root length of Ler-2 was markedly shortened by increasing ammonium concentration in the medium, while that of Col-0 was relatively insensitive to ammonium. Conversely, the lateral root length of Ler-2 was increased by ammonium supply. Both primary and lateral root of Col-0 were more sensitive to TIBA than those of Ler-2. ANOVA indicated the significant interaction of TIBA and ammonium in Col-0; however, no interaction in Ler-2. These results suggested the genetic diversity in the interactive effect of auxin and ammonium.     

不同生态型拟南芥耐铵毒害差异的生理机制

【目的】 利用拟南芥生态型群体研究拟南芥耐铵毒害的生理机制,为挖掘耐铵基因提供生理基础及理论指导。 【方法】 共收集了95份生态型拟南芥材料,采用水培实验方法,将拟南芥幼苗移栽后在正常培养液(2 mmol/L NO₃–-N处理)中培养8天,然后转移至含有1 mmol/L (NH₄)₂SO₄的营养液(2 mmol/L NH₄+-N处理)中培养8天,收获后,测定植株全氮量、地上部游离铵含量,以及谷氨酰胺合成酶 (GS) 活性;培养3天后取样,采用RT-PCR技术分析根部主要的铵态氮转运蛋白基因AMT1;1和AMT1;2的表达水平;拟南芥幼苗移栽后在正常培养液中培养8天,转移至丰度为5%的1 mmol/L (15NH₄)₂SO₄中培养,分别处理3 h、6 h和24 h取样,用于同位素分析。 【结果】 2 mmol/L铵态氮处理下拟南芥群体地上部的生长被显著抑制,并且大量游离铵离子累积于地上部,铵态氮下拟南芥群体体内铵含量是对照硝态氮下的1.5倍以上,其中Si-0生态型在铵态氮下铵含量为19.17 μmol/g, FW,是对照的20倍。在硝态氮培养条件下,内源铵的含量与拟南芥地上部生长呈显著负相关,铵态氮培养条件下,地上部生长与铵含量同样呈较高的负相关性,因此内源铵含量少的生态型拟南芥在铵态氮下亦耐铵,所以本研究以拟南芥群体组织内铵含量为主因子,筛选出耐铵拟南芥生态型Or-1、Ta-0,HSM和铵敏感拟南芥生态型Rak-2、Lpv-18、Hi-0,结果表明铵敏感生态型在硝态氮下铵含量是耐铵生态型的1.7倍至10倍。耐铵拟南芥生态型铵转运蛋白基因AMT1;1和AMT1;2的表达水平较铵敏感拟南芥高,植株全氮和地上部15N标记试验结果表明,耐铵拟南芥铵态氮吸收速率高于敏感型。并且耐铵拟南芥生态型在两种氮形态下其谷氨酰胺合成酶 (GS) 活性均显著高于铵敏感生态型,在硝态氮培养条件下GS活性是铵敏感生态型的1.1～1.8倍,在铵态氮培养条件下是1.2～1.6倍,说明耐铵拟南芥生态型的铵同化能力强于敏感型。 【结论】 耐铵生态型拟南芥是通过更高的谷氨酰胺合成酶 (GS) 活性将大量的游离铵同化以减少植株体内游离铵含量,从而减轻植株铵毒害;而不是通过减少铵态氮的吸收。      

Identification of genomic regions regulating ammonium-dependent inhibition of primary root length in Arabidopsis thaliana

Plant roots grow into the soil for efficient acquisition of various nutrients, such as inorganic nitrogen, ammonium, and nitrate. A previous study has revealed the genetic diversity of foliar functions of Arabidopsis thaliana ecotypes in an environment containing ammonium; however, the function of roots remains unclear. This work focuses on the root system architecture (RSA) of Arabidopsis ecotypes to investigate the genetic factors regulating ammonium-dependent RSA changes. Arabidopsis ecotypes were grown on vertical agar medium containing ammonium as a major nitrogen source, and root growth and RSA were determined. Arabidopsis ecotypes showed differential sensitivity to ammonium. The shoot dry weight of some ecotypes decreased, whereas that of other ecotypes increased in ammonium medium. The RSA changes also varied among the different ecotypes in response to ammonium. The total root length, measured as the sum of primary root and lateral root length, of some ecotypes was reduced, whereas that of other ecotypes showed no significant difference in ammonium medium. Compared with lateral roots, the primary roots showed a sharp response to ammonium supply. Notably, the RSA showed a partial correlation with shoot dry weight in ammonium medium. Because Col-4 and Ler-0 showed opposite RSA responses to ammonium supply, these two ecotypes were selected for further genetic analysis. Quantitative trait locus (QTL) analysis of recombinant inbred lines of Col and Ler showed the involvement of several genetic factors in ammonium-dependent RSA changes. Moreover, QTL analysis revealed that the primary structure of nitrogen-related enzymes do not account for changes in RSA in response to ammonium supply.     

Nitrogen Assimilatory Enzymes and Amino Acid Content in Inoculated Foliar Fertilized Pea Plants Grown at Reduced Molybdenum Concentration

ABSTRACT

A possibility to improve nitrogen assimilation in nitrogen fixing Molybdenum (Mo) deficient pea plants was shown. The influence of foliar supplied nutrients in addition to root nutrition resulted in reducing the unfavorable effects of inorganic nitrogen on nodule function and Mo deficiency on the nitrogen assimilatory enzymes. Inoculated pea plants were grown on liquid nutrient solution both with and without Mo. The following variants were tested: Mo supplied plants with root nutrition (F1 + Mo); Mo supplied plants with root and foliar nutrition (F2 + Mo); Mo deficient plants with root nutrition (F1 ? Mo); and Mo deficient plants with root and foliar nutrition (F2 ? Mo). Foliar application of nutrients had a positive effect on the glutamine synthetase and glutamate synthase enzyme activities in the roots and nodules of Mo deficient plants. It was found that the foliar fertilization reduced the inhibitory effect of Mo shortage on the aspartate/asparagine content in the pea shoots.     

Carbon skeletons for amide synthesis during ammonium nutrition in tomato and wheat roots

Heavy application of ammonium nitrogen to plant roots results in the conversion of ammonium nitrogen to the nitrogen of amides, glutamine, and asparagine, which are stored in roots or translocated to shoot. Since the net synthesis of such amides requires the supply of corresponding carbon skeletons, the carbon metabolism in amide synthesis in response to ammonium supply was investigated in tomato and wheat roots. The content of major primary amino acids was determined in tomato and wheat roots during a 4-d period of ammonium nutrition after 1-d culture in nitrogen-free nutrient solution. Ammonium supply led to a continuous increase in the asparagine content in wheat roots, whereas in tomato roots, the glutamine content increased 1 d after ammonium supply and thereafter the glutamine content was higher than the asparagine content. The amounts of amino acids synthesized from glucose-¹⁴C increased while the amounts of organic acids decreased in tomato roots by the supply of ammonium nitrogen for 1 d, compared to the roots that did not receive nitrogen. In tomato roots, the proportion of labeled glutamine was higher than that of labeled asparagine and the C5 amino acids were more strongly labeled than the C4 amino acids. These findings were different from the previous ones in wheat roots where the proportion of asparagine was found to be extremely high (Koga and Ikeda 2000: J. Fac. Agr. Kyushu Univ45, 7–13). To examine the in vivo asparagine synthesis, aspartate-'4C was fed to the roots. The labeling of asparagine, which was the most strongly labeled amino acid among the free amino acids, was remarkably strong in wheat roots whereas the labeling of glutamine was also pronounced in tomato roots. These results indicate that the ability to replenish carbon skeletons for amide synthesis in ammonium nutrition is different between tomato and wheat roots.     

Effect of root temperature on carob growth: Nitrate versus ammonium nutrition

The response of carob (Ceratonia siliqua L.) seedlings grown at different root zone temperatures affected by nitrate and ammonium nutrition was studied. When root temperatures ranged from 10 to 35°C, ammonium‐fed plants were significantly larger than nitrate‐fed plants. Ammonium‐fed plants displayed toxicity symptoms and were much smaller at 40°C root temperature in comparison with the nitrate‐fed plants grown at the same root temperature. Root/shoot ratio slightly increase with root temperature in ammonium‐ and nitrate‐fed plants in a similar way, and shoot demand per root unit decreased with root temperature between 15 and 25°C. There was a general increase in net photosynthesis with root temperature, though nitrate‐fed plants were more sensitive to low and ammonium‐fed plants to high temperatures. Increasing the root temperature of ammonium fed plants from 10 to 40°C leads to a 30% increase in the amount of photosynthates sent to the roots. The presence of ammonium resulted in the distribution of newly fixed carbon away from carbohydrates and into nitrogen compounds. Potassium, calcium, and nitrogen content of the plants also increased with increasing root temperature.     

Effects of Soil Application of Amino Acids,Ammonium, and Nitrate on Nutrient Accumulation and Growth Characteristics of Sweet Basil

ABSTRACT

The use of organic or reduced form of nitrogen (N) can have various beneficial effects in terms of plant nutrient uptake, metabolism, and environmental issues. In this study, the influence of soil application of reduced N-forms (ammonium, glycine, and glutamine) compared to nitrate and a no fertilizer treatment was evaluated on growth characteristics of sweet basil (Occimum basilicum L.) under a moderate lime soil conditions. The basil growth traits including root and shoot biomass were increased under application of reduced N-forms mainly glycine and glutamine compared to no fertilizer treatment. Application of reduced forms of nitrogen (ammonium, glycine, and glutamine) increased the leaf concentrations of potassium (K), magnesium (Mg), calcium (Ca), iron (Fe) and zinc (Zn), whereas the leaf N concentration was increased by ammonium and nitrate fertilization compared to unfertilized control plants. The results indicate that soil application of reduced N-forms particularly glycine and glutamine is superior to nitrate application.     

Differences in nitrogen‐assimilating enzyme activity in halophyte species are habitat‐related

The chemical form and content of available nitrogen (N) in salt marsh substrates varies considerably. On the western coast of Ireland, habitats designated as Ombrogenic Atlantic salt marshes were formed on ombrogenic peat substrate. The peat substrate in these systems has three times more ammonium than substrate from adjacent salt marsh habitats on sand and mud substrate. This study examined the extent to which the high concentration of ammonium in peat salt marsh substrate influences the N‐ assimilating enzyme activity of halophytes and the extent to which N metabolism differs between species. Specifically, this work investigated whether plants from peat salt marshes are more likely to assimilate ammonium than plants from non‐peat substrates. Four halophyte plant species—Armeria maritima, Aster tripolium, Plantago maritime, and Triglochin maritime—were sampled from various saltmarsh habitats including three sites on peat substrate and three on non‐peat substrate, comprising sand, mud and sand/mud. The activities of N‐metabolising enzymes—glutamine synthetase (GS), glutamate synthase, glutamate dehydrogenase (GDH), and nitrate reductase (NR)—were quantified in shoot and root parts. Root GS activity in Armeria maritima and shoot GS activity in Triglochin maritima were positively correlated with increasing soil ammonium levels. Root NR activity in Aster tripolium and shoot NR activity in Plantago maritima were significantly higher in plants grown on non‐peat substrates than peat substrates. The shoot : root GS activity ratio in Triglochin maritima on peat substrate was more than double the ratio on non‐peat substrates. It is concluded that all species tested displayed differences in N‐metabolising activities depending on the chemical form and/or concentration of N in the substrate, while three out of the four species were capable of taking advantage of the high levels of ammonium in peat substrates.     

Arabidopsis under ammonium over-supply: Characteristics of ammonium toxicity in relation to the activity of ammonium transporters

Because of highly intensive farming practices, crop plants could suffer relatively long terms of ammonium (NH₄⁺) excess stress introduced by overdose application of nitrogen fertilizers. However, the lack of sufficient understanding of plant responses to NH₄⁺ excess stress impairs the detection of effective solutions to this problem. The present work examined the biological influences of over-supplied NH₄⁺ in Arabidopsis thaliana using two mutant lines each with an ammonium transporter (AMT) gene (AtAMT1;1 or AtAMT1;3) knocked out. Our results indicated that lacking one of the major components of root NH₄⁺ -absorbing systems significantly alleviated the toxicity effects on Arabidopsis plants by reducing the accumulation of free NH₄⁺, suggesting that persistent absorption of NH₄⁺ through AMT was the main cause of excessive accumulation of free NH₄⁺ in the plants. Shading treatment led to a reduced transpirational driving force and thereby constrained the accumulation of toxic NH₄⁺ in the plants, finally resulting in higher NH₄⁺ -promoted growth in the wild type (WT). Under the shading treatment, the amt1;1 and amt1;3 mutant plants acquired insufficient NH₄⁺ and showed reduced growth when compared with the WT. Furthermore, the foliar application of sucrose notably alleviated the inhibitory effects on plant growth in the WT but had no effect on either the amt1;1 or amt1;3 mutant plants, indicating that carbon scarcity associated with NH₄⁺ excess is probably a major cause of NH₄⁺ toxicity in plants. Accordingly, increasing carbon source could be a potentially effective approach that alleviates the inhibition caused by NH₄⁺ excess and increases nitrogen use efficiency under NH₄⁺ over-supply.     

Changes in growth and nitrogen assimilation in barley seedlings under cadmium stress

Barley (Hordeum vulgare L. cv. Martin) plants grown in solution culture, were exposed to increasing cadmium (Cd) concentration (0, 5, 10, 25, 50, and 100 μM) for a duration of 12 days. The sequence of important biochemical steps of nitrate (NO₃) assimilation were studied in roots and shoots as a function of external Cd concentration. Cadmium uptake in roots and shoots increased gradually with Cd concentration in the medium. This Cd accumulation lowered substantially root and shoot biomass. The nitrate reductase (NR, EC 1.6.6.1) and nitrite reductase (NiR, EC 1.6.6.4) activities declined under Cd stress. Concurrently, tissue NO₃ contents and xylem sap NO₃ concentration were also decreased in Cd‐treated plants. These results suggest that Cd could exert an inhibitory effect on the assimilatory NO₃ reducing system (NR and NiR) through a restriction of NO₃ availability in the tissues. We therefore examined, in short‐term experiments (12 h), the impact of Cd on NO₃ uptake and the two reductases in nitrogen (N)‐starved plants that were pretreated or not with Cd. It was found that Cd induced inhibition of both NO₃ uptake and activities of NR and NiR, during NO₃ induction period. The possible mechanisms of Cd action on NO₃ uptake are proposed. Further, in Cd‐grown plants, the glutamine synthetase (GS, EC 6.3.1.2) showed a decreasing activity both in shoots and roots. However, increasing external Cd concentration resulted in a marked enhancement of glutamate dehydrogenase (NADH‐GDH, EC 1.4.1.2) activity, coupled with elevated levels of ammonium (NH₄ in tissues. On the other hand, the total protein content in Cd‐treated plants declined with a progressive and substantial increase of protease activity in the tissues. These findings indicate that under Cd stress the usual pathway of NH₄ assimilation (glutamine synthetase/glutamate synthase) can switch to an alternative one (glutamate dehydrogenase). The changes in all parameters investigated were concentration‐dependent and more marked in roots than shoots. The regulation of N absorption and assimilation by Cd in relation to growth and adaptation to stress conditions are discussed.     

Phosphorus uptake of maize as affected by ammonium and nitrate nitrogen - Measurements and model calculations -

Phosphorus uptake is often enhanced by ammonium compared to nitrate nitrogen nutrition of plants. A decrease of pH at the soil-root interface is generally assumed as the cause. However, an alteration of root growth and the mobilization of P by processes other than net release of protons induced by the source of nitrogen may also be considered. To study these alternatives a pot experiment was conducted with maize using a fossil Oxisol high in Fe/Al-P with low soil solution P concentration. Three levels of phosphate (0, 50, 200 mg P kg^?1) in combination with either ammonium or nitrate nitrogen (100 mg N kg^?1) were applied. Plants were harvested 7 and 21 d after sowing, P uptake measured and root and shoot growth determined. To assess the importance of factors involved in the P transfer from soil into plants, calculations were made using a model of Barber and Claassen. In the treatments with no and low P supply NH₄-N compared to NO₃-N nutrition increased the growth of the plants by 25 % and their shoot P content by 38 % while their root growth increased by 6 % only. The rhizosphere pH decreased in the NH₄-N treatments by 0.1 to 0.6 units as compared to the bulk soil while in the NO₃-N treatments it increased by 0.1 to 0.5 units. These pH changes had a minor influence on P uptake only, as was demonstrated by artificially altering the soil pH to 4.7 and 6.3 respectively. At the same rhizosphere pH, however, P influx was doubled by the application of NH₄-compared to NO₃-N. It is concluded that in this soil the enhancement of P uptake of maize plants after ammonium application cannot be attributed to the acidification of the rhizosphere but to effects mobilizing soil phosphate or increasing P uptake efficiency of roots. Model calculation showed that these effects accounted for 53 % of the P influx per unit root length in the NO₃-N and 72 % in the NH₄-N supplied plants if no P was applied. With high P application the respective figures were only 18 and 19%.     

Mitigation of ammonium toxicity by silicon in tomato depends on the ammonium concentration

Ammonium toxicity in hydroponically grown crops can affect tomato development. However, it has been shown that the silicon (Si) attenuates ammonium toxicity in plants depending on the plant species, the stage of development and the ammonium concentration in the nutrient solution. Thus, in order to investigate how Si attenuates stress caused by ammonium in tomato, a study was carried out involving plants cultivated up to 40 days after seed germination using nutrient solutions containing ammonium concentrations (1, 2, 4, 6 and 8?mmol?L^?1), in the absence or presence of Si (1?mmol?L^?1). The accumulation and efficiency of nitrogen and Si use, as well as the concentrations of chlorophyll, carotenoids, malondialdehyde, hydrogen peroxide and growth parameters was assessed. At a concentration of 1?mmol?L^?1 ammonium, Si increases the accumulation of nitrogen and Si, the nitrogen use efficiency, the root area and dry biomass of the shoot. At concentrations of 1 and 2?mmol?L^?1 ammonium, Si increases the leaf area and root dry biomass, and in higher concentrations, there was no effect of Si after the supply of ammonium. It was observed that the addition of Si mitigates ammonium toxicity by 1?mmol?L^?1 ammonium, and we can recommend its use in the nutrient solution (Si?=?1?mmol?L^?1) to grow tomato cropsthat employs ammonium concentration of 1?mmol?L^?1.     

Potential Nitrate Leaching Under Common Landscaping Plants

Two Elsholtzia haichowensis S. populations, copper-tolerant (TLS) and non-tolerant (HA) ones were studied in hydroponic experiment for the nitrogen assimilation and plant growth under excess Cu conditions. The results demonstrated that there were surely the differences in nitrogen assimilation and plant growth between the two populations. Excess Cu caused evident decreases in the shoot and root biomass and root/shoot biomass ratio in HA population while no significant changes happened in TLS population. In addition, in HA population, excess Cu also induced apparent declines in activities of nitrate reductase (NR, EC 1.6.6.1) and glutamine synthetase (GS, EC 6.3.1.2) in the leaves and roots as well as the contents of nitrate, ammonium and amino acids in the roots. In TLS population, excess Cu did not significantly affect the NR activities in the leaves and roots and the nitrate content in the roots, and apparently elevated the root ammonium and amino acids contents, although it also clearly reduced the GS activities in the leaves and roots. Besides, with the addition of Cu in the culture solution, the Cu contents in the leaves and roots of the two populations markedly increased. But this increase was significantly lower in TLS population than that in HA population; the fact might be partly responsible for the relative stabilization of nitrogen assimilation in TLS population compared to that in HA population.     

Nitrogen form and the seasonal root and shoot response of creeping bentgrass

Abstract

The form of nitrogen can affect root and shoot growth of plants. This study was conducted to determine the effects of ammonium and nitrate nitrogen on root length and number and shoot color and quality of creeping bentgrass (Agrostis palustris Huds. ‘Penncross'). The study was conducted in the University of Georgia rhizotron facility. Turf was grown in an 80/20 sand/peat rooting medium and maintained under putting green conditions for 12 months. Two forms of nitrogen, ammonium and nitrate, utilizing the nitrogen sources of urea and calcium nitrate, respectively, were applied in the following ammonium: nitrate ratios: 100: 0, 75: 25, 50: 50, 25: 75, and 0: 100. A modified Hoagland's solution provided all other macronutrients and micronutrients. Root length, root number, shoot color, and shoot quality data were collected weekly for 12 months. The 100% nitrate treatment resulted in 30% more roots during the fall compared to the 100% ammonium treatment The 100% ammonium treatment had 26% greater root length in the spring compared to the two highest nitrate treatments. The 50: 50 treatment produced greater root length during the spring and summer compared to the high nitrate treatments (0: 100 and 25: 75) and at least 30% greater root number during the summer compared to all treatments. All treatments resulted in a decrease in root length for the summer compared to the spring. The 50: 50 treatment provided higher ratings for shoot color for each season and higher quality ratings for the winter and spring. A fertilizer program that contains a portion of its nitrogen as nitrate would be more beneficial certain times of the year than one containing ammonium or nitrate alone.     

Response of wheat and maize to different nitrogen sources: II. Nitrate reductase and glutamine synthetase enzyme activities,and plastid pigment content

Glutamine synthetase and nitrate reductase enzyme activities occurred both in roots and leaves of maize (Zea mays L., hybrid Pioneer 3737) and wheat (Triticum aestivum L., cultivar Jantar) plants grown on different nitrogen (N) sources. Enzyme activities and plastid pigment content in maize plants were higher in the treatments with a mixture of nitrate (NO₃) and ammonium (NH₄) than with either N source alone. In wheat plants, plastid pigment content, nitrate reductase activity, and root glutamine snynthetase activity were higher in the treatments where NO₃ alone was applied to the nutrient medium.     

Uptake,Transport, and Concentration of Chloride and Sodium in Three Citrus Rootstock Seedlings

ABSTRACT

Aspects of ammonium (NH₄ ⁺) toxicity in cucumber (Cucumis sativus L.) were investigated following growth with different N sources [nitrate (NO₃ ^?), NH₄ ⁺, or NH₄NO₃] supplied in concentrations of 1, 5, 10, or 15 mM. Plant dry weights and root: shoot ratios were lower with NH₄ ⁺-fed plants than with NO₃ ^?-fed plants. Ammonium accumulated strongly in leaves, stem, and roots when the concentration in the growth medium exceeded 1 mM. The increase in tissue NH₄ ⁺ coincided with saturation of glutamine synthetase activity and accumulation of glutamine and arginine. Low tissue levels of calcium and magnesium in the NH₄ ⁺-fed plants constituted part of the NH₄ ⁺-toxicity syndrome. Additions of small amounts of NH₄ ⁺ to NO₃ ^? -grown cucumber plants markedly increased the growth.     

氮素不同形态配比对菠菜体内游离氨基酸含量和相关酶活性的影响

采用溶液培养试验,研究了氮素不同形态配比对菠菜茎叶中游离氨基酸含量及3种主要氮代谢酶活性的影响。结果表明:1)随着营养液中铵硝比(NH4+-N/NO3--N)的降低,菠菜茎叶中游离氨基酸的总量呈下降趋势。在全硝营养下(NH4+-N/NO3--N=0∶100)下,菠菜茎叶中游离氨基酸的总量只有全铵营养(NH4+-N/NO3--N=100∶0)的34.4%。2)在全铵营养下,菠菜茎叶中游离氨基酸的主要组分是谷氨酰胺、精氨酸和谷氨酸,三者占游离氨基酸总量的百分比依次为39.8%、20.2%和8.9%;在全硝营养下,菠菜茎叶中游离氨基酸以谷氨酸、天冬氨酸和丝氨酸为主,三者占游离氨基酸总量的百分比分别为30.3%1、8.6%和8.5%。3)提高营养液中硝态氮的比例,可以显着提高菠菜茎叶中硝酸还原酶(NR)的活性,同时降低了谷氨酸脱氢酶(GDH)的活性,谷氨酰胺合成酶(GS)活性则呈现先升后降的抛物线状变化规律。4)菠菜茎叶中NR活性与谷胺酰胺含量之间存在着显著负相关关系(r=-0.968)。