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卷 65, 编号 4 (2018)

Reviews

Chloroplasts: Structure and Expression of the Plastid Genome

Kusnetsov V.

摘要

During the last two decades much success in studying plastid genome structure and expression was achieved. The primary sequence of hundreds of plant plastid genomes has been determined, which allows us to understand basic laws of plastome structure. Novel chloroplast nuclear-encoded RNA-polymerases and sigma-factors have been discovered. Mechanisms responsible for posttranscriptional regulation of plastid genes' expression, including splicing and editing, are actively being studied. Increasingly more data on the most important role of nucleoids in chloroplast biogenesis is emerging. Much attention is presently given to studying the proteins associated with bacterial type RNA-polymerase. Determination of the primary sequence of genomes for a number of higher plants has produced new information on the exchange of genetic material between cell organelles. At present, interorganelle signaling in plant cells is a subject of active study. In the review, a wide range of issues is quite briefly discussed, including some elements of chloroplast evolution and nuclear-plastid signaling. Certain features of chloroplast genetic material organization are described. In addition, basic stages of plastid genome expression are discussed.

Russian Journal of Plant Physiology. 2018;65(4):465-476
pages 465-476 views

Nitrate Signaling in Plants: Introduction to the Problem

Izmailov S., Nikitin A., Rodionov V.

摘要

The review discusses ecological aspects of nitrate pools in the soil as an evolutionary basis of emergency and manifestation of the nitrate’s signaling function in plants. The historiography and modern state of the problem of signaling are considered in respect to such processes as sensing, consumption, transport, and storage of nitrate as well as regulation of nitrogen, carbon, and secondary metabolisms.

Russian Journal of Plant Physiology. 2018;65(4):477-489
pages 477-489 views

Research Papers

Substrate Specificity of Acyl-Lipid Δ9-Desaturase from Cyanobacterium sp. IPPAS B-1200, a Cyanobacterium with Unique Fatty Acid Composition

Starikov A., Usserbaeva A., Mironov K., Sidorov R., Zayadan B., Bedbenov V., Sinetova M., Los D.

摘要

Cyanobacterium sp. IPPAS B-1200 is characterized by a high content of rare fatty acids (FAs), both myristic (14:0–30%) and myristoleic (14:1Δ9–10%) in the membrane lipids. Thus, short-chain FAs reach 40% of the sum of all FAs in cells, which is unusual for Cyanobacteria. Monounsaturated palmitoleic acids (16:1Δ9) also reach 40% of the sum of the FAs. We determined the complete nucleotide sequence of the genome of this cyanobacterium and found the only gene for the acyl-lipid Δ9-desaturase, desC1. We cloned this gene and characterized its specificity to the length of the substrate using heterologous expression in Escheriсhia coli. The results show that DesC1 nonspecifically generates olefin bond in FAs with a length of 14, 16, and 18 carbon atoms. This finding confirms that all monoesterifed FAs in Cyanobacterium sp. IPPAS B-1200 are generated by one acyl-lipid Δ9-desaturase.

Russian Journal of Plant Physiology. 2018;65(4):490-497
pages 490-497 views

Role of CLE41 Peptide in the Development of Root Storage Parenchyma in Species of the Genus Raphanus L.

Gancheva M., Dodueva I., Lutova L.

摘要

CLE peptides (CLAVATA3/ENDOSPERM SURROUNDING REGION) are signal molecules or plant peptide hormones that play an important role in regulation of development of various meristems governing the expression of WOX (WUSCHEL-RELATED HOMEOBOX) genes. In particular, CLE peptides belonging to a small TDIF (Tracheary Element Differentiation Inhibitory Factor) group are responsible for the operation of gene WOX4 controlling the development of cambium and the conducting system. We looked into the role of CLE41 peptide from the TDIF group in the development of storage root in two species of the genus Raphanus: cultivated radish (Raphanus sativus var. radicula Pers.) that is a popular root crop with a storage root and its ancestor wild radish (Raphanus raphanistrum L.) where storage parenchyma of the root is poorly developed. It was shown that overexpression of gene RsCLE41 and plant treatment with exogenous peptide CLE41 influenced the development of cambium and xylem in the roots of R. sativus and R. raphanistrum and affected expression of the genes from different groups. One could say that peptide CLE41 activates expression of the genes whose homologues in arabidopsis play a key role in the maintenance of cambium (RsWOX4, RsWOX14, RsHAM4, and RsCYCD3). In the storage root of radish, peptide CLE41 activates proliferation of cambium cells reducing the amount of one of the xylem’s elements (lignified parenchyma). The obtained results point to an important role of CLE41 in the development of storage root in radish.

Russian Journal of Plant Physiology. 2018;65(4):498-511
pages 498-511 views

Stomatal Behaviours of Aspen (Populus tremuloides) Plants in Response to Low Root Temperature in Hydroponics

Chen Z., Feng J., Wan X.

摘要

Hydroponic-grown seedlings of aspen (Populus tremuloides Michx.) were used to investigate how low root temperatures (5°C) affect stomatal conductance and water relations. An isohydric manner of the stomatal behaviour was found with the seedlings when their roots were subjected to the low temperature. Stomatal conductance rapidly and dramatically reduced in response to the low root temperature, while the xylem water potential did not significantly alter. Under the low root temperature, pH value of the xylem sap increased from 6.15 to 6.72 within the initial 4 h, while abscisic acid (ABA) concentration increased by the eighth hour of treatment. K+ concentration of the xylem sap significantly decreased within the 8th h and then reversed by the 24th h. The ion change was accompanied by a decrease and then an increase in the electrical conductivity, and an increase and then a decrease in the osmotic potential. The tempo of physiological responses to the low root temperature suggests that the rapid pH change of the xylem sap was the initial factor which triggered stomatal closure in low temperature-treated seedlings, and that the role of the more slowly accumulating ABA was likely to reinforce the stomatal closure. Xylem sap from the seedlings subjected low root temperature affected stomatal aperture on leaf discs when they were floated on the sap solution. The stomatal aperture correlated (P = 0.006) with the changed pattern of [K+] in the sap while the range of pH or ABA found in the xylem sap did not influence stomatal aperture of leaf discs in solution. The effect of xylem sap on stomatal aperture on leaf discs was different from on stomatal conductance in the intact seedlings. Comparison was made with previous study with the soil-grown seedlings.

Russian Journal of Plant Physiology. 2018;65(4):512-517
pages 512-517 views

Closure of Stomata in Water-Stressed Pine Needles Results from the Decreased Water Potential of the Mesophyll Apoplast in the Substomatal Cavity

Voronin P., Rakhmankulova Z., Tarnopolskaya E., Kuznetsov V.

摘要

Pine (Pinus sylvestris L.) seedlings grown under controlled conditions were subjected to water deficit (external water potentials ranging from–0.15 to–1.5 MPa) by adding polyethylene glycol 6000 (PEG) to the nutrient solution. Following this treatment, the dry weights of plant shoots and roots, as well as the ratio of variable to maximum chlorophyll fluorescence (Fv/Fm), nonphotochemical quenching (NPQ) of chlorophyll excitations, photosynthetic CO2/H2O exchange, dark respiration of needles, and water potential of mesophyll apoplast in the substomatal cavity of pine needles, were measured. The imposed water deficit was followed by the inhibition of seedling growth, suppression of photosynthesis and transpiration, and by the decreased content of photosynthetic pigments. It is shown for the first time that the closure of stomata in the needles of water-stressed pine seedlings falls into the physiological reaction norm and is caused by the reduction of water potential in the mesophyll apoplast of the substomatal cavity.

Russian Journal of Plant Physiology. 2018;65(4):518-523
pages 518-523 views

Temperature Responses of Photosynthesis and Respiration of Maize (Zea mays) Plants to Experimental Warming

Zheng Y., Li R., Guo L., Hao L., Zhou H., Li F., Peng Z., Cheng D., Xu M.

摘要

Understanding the key processes and mechanisms of photosynthetic and respiratory acclimation of maize (Zea mays L.) plants in response to experimental warming may further shed lights on the changes in the carbon exchange and Net Primary Production (NPP) of agricultural ecosystem in a warmer climate regime. In the current study, we examined the temperature responses and sensitivity of foliar photosynthesis and respiration for exploring the mechanisms of thermal acclimation associated with physiological and biochemical processes in the North China Plain (NCP) with a field manipulative warming experiment. We found that thermal acclimation of An as evidenced by the upward shift of An-T was determined by the maximum velocity of Rubisco carboxylation (Vcmax), the maximum rate of electron transport (Jmax), and the stomatal- regulated CO2 diffusion process (gs), while the balance between respiration and photosynthesis (Rd/Ag), and/or regeneration of RuBP and the Rubisco carboxylation (Jmax/Vcmax) barely affected the thermal acclimation of An. We also found that the temperature response and sensitivity of Rd was closely associated with the changes in foliar N concentration induced by warming. These results suggest that the leaf-level thermal acclimation of photosynthesis and respiration may mitigate or even offset the negative impacts on maize from future climate warming, which should be considered to improve the accuracy of process-based ecosystem models under future climate warming.

Russian Journal of Plant Physiology. 2018;65(4):524-531
pages 524-531 views

Scale of Physiological Processes Sensitivity to PEG-Induced Water Stress in Scots Pine Seedlings

Ivanov Y., Zlobin I., Kartashov A., Pashkovskiy P., Kuznetsov V.

摘要

The idea that water deficit strengthening induces concerted changes of plant physiological parameters is rather widespread. However, such changes are often difficult to identify due to challenges in establishments and maintenance of required water stress intensities using solid substrates. Therefore, we exposed Scots pine (Pinus sylvestris L.) seedlings to the range of water potentials from–0.15 to–1.5 MPa in PEG-water culture to identify the series of physiological parameters differently sensitive to water stress. We observed that even mild water stress (–0.15 MPa) inhibited root elongation, which could be one of the main pine seedlings vulnerabilities under drought. Active accumulation of osmolytes was already induced by mild water deficit and further increased with water stress severity. Plant fresh biomass growth sensitivity was more related to changes of relative water content (RWC) than to changes in tissue water content or dry weight accumulation. Plants were able to grow and accumulate dry weight down to–0.5 MPa, but lower medium water potentials (–1.0 and–1.5 MPa) suppressed growth and heavily damaged root cells, as judged from many-fold increase of Ca2+ content in roots. Chlorophyll a content was surprisingly sensitive to water stress, while carotenoids level was increased under severe stress conditions. In conclusion, the experimental system with stepwise water potential values allowed us to analyze the sensitivity scale of a range of P. sylvestris physiological processes to water stress. It was largely similar to those described earlier for other plant species, but its peculiarities were high sensitivity of root elongation, marked resistance of biomass growth to water deficit and well-developed ability to osmotic adjustment.

Russian Journal of Plant Physiology. 2018;65(4):532-540
pages 532-540 views

The Soybean GmRACK1 Gene Plays a Role in Drought Tolerance at Vegetative Stages

Li D., Chen F., Li H., Li W., Guo J.

摘要

The receptor for activated C kinase 1 (RACK1) is a versatile scaffold protein that binds to numerous proteins to regulate diverse cellular pathways in Arabidopsis. However, little is known about the function of RACK1 in soybean (Glycine max L.). Here, we show the expression profile and putative function of a soybean RACK1 (GmRACK1). The amino acid sequence of GmRACK1 had seven tryptophan-aspartic acid (WD) repeats, in which there were typical glycine-histidine (GH) and WD dipeptides. Real-time reverse transcription-polymerase chain reaction analysis showed that GmRACK1 was expressed at different levels in all tissues examined and strongly downregulated by abscisic acid and drought stress. We therefore constructed soybean GmRACK1 silenced (RNA interference, RNAi) and overexpressing plants. There were no obvious phenotypic differences between the transgenic seedlings and wild type under normal condition. However, the GmRACK1-RNAi lines showed significantly improved in drought stress tolerance while the overexpressing seedlings were hypersensitive to drought stress when compared to wild type in terms of plant survival rates after 10 days of drought. GmRACK1-RNAi plants were observed to be more sensitive to ABA when seeds germinated and root grew. Furthermore, an enzyme activity analysis indicated that the GmRACK1-RNAi plants had higher superoxide dismutase, peroxidase, and catalase activities but less malondialdehyde content and electrolyte leakage than those of wild type when the plants were exposed to dehydration treatment, indicating a better anti-oxidative stress capability and less membrane damage. This finding was consistent with the accumulation of reactive oxygen species (ROS) and lower expression of ROS-scavenging genes in the GmRACK1-OE lines. We conclude that the GmRACK1 gene plays an important role controlling ABA level and drought stress resistance in soybean.

Russian Journal of Plant Physiology. 2018;65(4):541-552
pages 541-552 views

Effect of Cadmium on Distribution of Potassium, Calcium, Magnesium, and Oxalate Accumulation in Amaranthus cruentus L. Plants

Osmolovskaya N., Dung V., Kudryashova Z., Kuchaeva L., Popova N.

摘要

Effect of cadmium at concentrations of 1 and 10 μM on biomass increment, mineral nutrient elements (potassium, calcium, and magnesium) accumulation, and oxalic acid pools in organs of Amaranthus cruentus L. plants growing under water culture conditions was investigated. It was established that cadmium in the tested concentrations did not exert any pronounced damage effect on amaranth plants, which was in part shown to be associated with its predominant accumulation in roots and minimization of its transfer into young leaves. It was demonstrated that, in sublethal concentrations, this metal exerted growth response in the above ground amaranth organs expressed in stimulation of young leaves' growth, while simultaneously inhibiting growth processes in mature leaves. The results obtained are discussed in the context of determination of plant growth response to the effect of cadmium by certain metabolic changes whose functional manifestations consisted in carbon metabolism intensification and increase in water-insoluble oxalate content in amaranth leaves. Simultaneous observed increase in Ca2+ and Mg2+ levels in young and mature amaranth leaves is considered as additional evidence in favor of accelerating leaves' ontogenesis pace under the effect of sublethal doses of cadmium.

Russian Journal of Plant Physiology. 2018;65(4):553-562
pages 553-562 views

Responses of Typha orientalis Roots to Pb2+ Stress

Xu X., Hou Y., Xu Y., Ji Y., Jin Y.

摘要

To investigate phytoremediation potential of Typha orientalis Presl in removing Pb2+ from polluted water, relevant experiments were conducted to evaluate responses activated by Pb2+ (0.25–2 mM) in T. orientalis roots over a period of ten days. Pb contents in subcellular fractions decreased in the following order: cell wall > organelle > soluble fraction. Most of Pb was located in cell wall and membrane system. Contents of K and Ca declined in T. orientalis roots under Pb2+ stress, but an opposite effect was noted for some mineral elements (Mg, Cu, Zn, and Fe). H2O2 level increased in a concentration-dependent manner, which induced oxidative stress. However, significant reduction in levels of O2·− and malondialdehyde (MDA) were observed in all Pb2+ treatment groups. Findings indicated toxicity of Pb2+ to T. orientalis in terms of inducing oxidative stress and causing imbalance in mineral elements. However, T. orientalis also resisted Pb2+-induced damage through isolation mechanism, which involves cell wall and membrane systems.

Russian Journal of Plant Physiology. 2018;65(4):563-569
pages 563-569 views

Effect of 24-Epibrassinolide on Antioxidative Defence System Against Lead-Induced Oxidative Stress in The Roots of Brassica juncea L. Seedlings

Dalyan E., Yüzbaşıoğlu E., Akpınar I.

摘要

Lead (Pb) toxicity causes oxidative stress by increasing the production of reactive oxygen species. The aim of the present study was to investigate the role of 24-epibrassinolide (24-EBL) on the antioxidant defence system as a response to Pb stress in Brassica juncea L. Surface-sterilized seeds were exposed to Pb ion (0 and 2 mM) toxicity in Petri dishes and subsequently, the seeds were sprayed with either (i) deionized water or (ii) different concentrations (10–12, 10–10, and 10–8 M) of 24-EBL on alternate days. After nine days, the roots of the B. juncea seedlings were harvested to analyze the heavy metal content, root length, hydrogen peroxide level, lipid peroxidation, total protein content and activities of the antioxidant enzymes (superoxide dismutase, catalase, ascorbate peroxidase, peroxidase, glutathione reductase and glutathione-S-transferase). According to our results, the Pb ions accumulated by the B. juncea roots led to oxidative stress by increasing the level of H2O2 and malondialdehyde, and thus, increased the activity of the antioxidative enzymes (except for catalase) and the growth and total protein content decreased. Whereas, the 24-EBL treatment to the roots of Pb stressed seedlings was able to alleviate the Pb-induced oxidative stress. Upon the application of 24-EBL, a reduction in Pb accumulation, H2O2 and malondialdehyde levels as well as an increased total protein content and activity of antioxidative enzymes detoxifying hydrogen peroxide (catalase, ascorbate peroxidase and peroxidase) were observed. As a result, the stress protective properties of 24-EBL depending on concentration in B. juncea roots were revealed in this study.

Russian Journal of Plant Physiology. 2018;65(4):570-578
pages 570-578 views

Macromolecular Toxins Secreted by Botrytis cinerea Induce Programmed Cell Death in Arabidopsis Leaves

Huo D., Wu J., Kong Q., Zhang G., Wang Y., Yang H.

摘要

Botrytis cinerea causes grey mold disease in crops and horticultural plants. It is suspected to kill plant cells via secreted toxins and to derive nutrients from dead or dying cells. However, whether macromolecular phytotoxins (MPs) secreted by B. cinerea induce necrosis or also trigger a programmed cell death (PCD) remains to be determined. We have previously partially characterized MPs secreted by B. cinerea. Here we isolated MPs from B. cinerea culture and applied them to leaf cells, assessing PCD over the following 120 h. Cell death was assessed by propidium iodide (PI) and 4′,6-diamidino-2-phenylindole (DAPI) staining. Catalase (CAT), peroxidase (POD) activity and the cytochrome c/a ratio were assessed by spectrophotometer. POD isomers were measured using the benzidine acetate method. In Arabidopsis thaliana (L.) Heynh. exposed to B. cinerea MPs, we observed chromatin condensation and marginalization, nuclear substance leakage and accumulation of autofluorescent materials in the cell wall. Furthermore, B. cinerea MPs induced release of cytochrome c from the mitochondria into the cytosol. Moreover, CAT and POD activity was upregulated and the POD isoenzyme pattern was altered. In conclusion, A. thaliana exposed to B. cinerea MPs exhibits multiple hallmarks of PCD, suggesting that B. cinerea induces PCD in host cells through secreted macromolecules.

Russian Journal of Plant Physiology. 2018;65(4):579-587
pages 579-587 views

Activities of Adenylate Cyclase and Changes in cAMP Concentration in Root Cells of Pea Seedlings Infected with Mutualists and Phytopathogens

Lomovatskaya L., Kuzakova O., Romanenko A., Goncharova A.

摘要

Work was carried out on pea (Pisum sativum L.) seedling roots to assess the attachment of the nitrogen-fixing symbiotic bacteria Rhizobium leguminosarum bv. vicea (Rlv) and the bacterial phytopathogens—specific Pseudomonas syringae pv. pisi (Psp) and nonspecific Clavibacter michiganensis ssp. sepedonicus (Cms). Different root zones were examined: (I) the meristem, 2 mm from the root tip; (II) the root hair-free zone, 27 mm; (III) the zone of root hair anlages, 712 mm; (IV) the young root hair zone, 1217 mm; and (V) the zone of root hair that completed the growth, 1722 mm. It was found earlier that the zones differed in their susceptibility to Rlv. In the present work, reactions of particular components of the adenylate cyclase signaling system (ACSS) were estimated, i.e., concentration of cAMP and activities of transmembrane adenylate cyclase (tAC) and soluble adenylate cyclase (sAC) in these zones after different times post inoculation (5, 15, 120, and 360 min). It was revealed that the degree of activation of particular components of ACSS did not depend on the sorption rate of differently specialized bacteria. Upon contact with Rlv, the character of changes in tAC and sAC activities was almost the same in different root zones and resembled the dynamics of the cAMP content. Inoculation with Psp changed the cAMP level similarly to that with Rlv, but the dynamics of tAC and sAC was opposite to each other in most cases. Inoculation with Cms, in spite of the absence of its attachment, elevated the cAMP content and activated tAC and sAC. It is suggested that the above-mentioned changes in ACSS is associated with exometabolites of Rlv, Psp, and Cms, which activate the PAMP-induced immunity of the pea seedling cells. The uniform dynamics of cAMP in different root zones upon the exposure to Rlv and Psp seems to reflect the specific reaction and, presumably, fulfills different functions—regulatory with Rlv and defensive with Psp. Upon short-term contact with Cms, the cAMP dynamics in the same root zones displayed a nonspecific character that might be related to the rate of adsorption of exopolysaccharides by the root hair. The systemic response of ACSS was observed in the hypocotyls of the seedlings exposed to any of the three organisms.

Russian Journal of Plant Physiology. 2018;65(4):588-597
pages 588-597 views

Physiological and Biochemical Responses of Lettuce to Thymol, as Allelochemical

Nasrollahi P., Razavi S., Ghasemian A., Zahri S.

摘要

Nowadays, allelopathic investigations have focused to identify action mechanisms of this compounds on target organisms in natural habitats. It may tend to introduce new natural herbicides and pesticides for replacing the synthetic ones. In the present study, the allelopathic effects of thymol on lettuce (Lactuca sativa L.) as a model plant were investigated in physiological and biochemical aspects. At the first stage, the effect of different concentrations of thymol on some growth parameters, including seed germination, radicle and plumule growth were evaluated to determine the optimum concentration for the continuation of our experiment. Then, the lettuce seedlings were cultured in pots containing peat and were irrigated with Hoagland nutrient solution supplemented with thymol at the concentration of 50 and 100 μg/mL. The effect of these treatments on physiological, biochemical aspects of the plant were studied following the plant growth. The results showed whereas, the shoot fresh and dry weights and photosynthetic rate in the treated group were decreased significantly compared to the control group at P ≤ 0.05, photochemical efficiency of photosystem II, total protein concentration, proline content and the activity of some antioxidant enzymes such as polyphenol oxidase, ascorbate peroxidase and catalase were increased in treated plants than control ones. However, there was no significantly change in chlorophyll content in treated group than control. It can be concluded that the thymol as an allelochemical caused some physiological and biochemical responses in the lettuce which are much similar to induced responses under abiotic stress. Indeed, it induces a kind of stress named as allelochemical stress.

Russian Journal of Plant Physiology. 2018;65(4):598-603
pages 598-603 views

Identification of Genes Related to Cell Wall Metabolism and Fruit Ripening in Ziziphus jujube Using RNA-seq and Expression Analysis

Hou S., Shen J., Sun Z., Li H.

摘要

The transcriptome of Chinese jujube (Ziziphus jujube Mill.) fruit was characterized to determine which genes were involved in cell wall metabolism and ripening. Based on RNA-seq of fruit pulp, 61.243 contigs (mean length 440 nt) were assembled and 31.725 genes were identified (mean length 842 nt), of which 25.257 were annotated using a non-redundant protein sequence database (Nr). Finally, 8.409 of these genes were classified using the Gene Ontology (GO) functional annotation database into three major categories: cell component, molecular function, and biology process. Comparison of young and mature fruit transcripts showed that 1.206 genes were upregulated while 1.256 genes were downregulated. The 19 candidate genes related to cell wall metabolism and fruit ripening were selected from the differentially expressed genes (DEGs) for further study; qRT-PCR analysis showed that gene expression levels were up- or downregulated significantly at the stages of young and ripe fruit when compared to plant leaves.

Russian Journal of Plant Physiology. 2018;65(4):604-610
pages 604-610 views

Effects of pH on the Submerged Macrophyte Hydrilla verticillata

Song Y., He X., Chen M., Zhang L., Li J., Deng Y.

摘要

Hydrilla verticillata (L.f.) Royle is widely distributed and protects the water environment mainly by serving as a potential heavy metal hyperaccumulator. Hydroponic experiments were performed to investigate the biochemical responses of the leaves and stems of H. verticillata at pH values of 5.5, 6.5, 7.5, 8.5, and 9.5 for 7, 14, and 21 days. The results showed that a weak alkaline environment (pH 8.5) promoted plant growth and that an acidic environment (pH 5.5, 6.5) adversely affected normal metabolism. The malondialdehyde content and three antioxidant enzyme activities changed in a similar pattern after the pH treatments: varying increases occurred following all pH treatments with the exception of pH 8.5. The activities of the three N metabolism enzymes briefly increased in an acidic environment and then sharply decreased compared to the control. The ROS-scavenging mechanisms and N metabolism mechanisms in H. verticillata worked together to respond to pH-induced effects. Based on the interplay between antioxidant enzymes and N metabolism enzymes, H. verticillata could defend against the toxicity induced by an acidic environment for approximately seven days and demonstrate stronger adaptability to the alkaline environment. Depending on the growth status and the synergistic effects of the enzymes, an optimum pH of 8.5 for H. verticillata was found in our experiment. Thus, these characteristics reveal a better understanding of this species so that it can be effectively controlled and better referenced for phytoremediation.

Russian Journal of Plant Physiology. 2018;65(4):611-619
pages 611-619 views