Polyamines in Vigna radiata (L.) Wilczek plant growth and development

 

Urmi Roy1, Ushri Roy2

1Department of Botany, Vijaygarh Jyotish Ray College, 8/2, Bijoygarh, Jadavpur, Kolkata, West Bengal 700032.

2Department of Botany, Bhairab Ganguly College, Belgharia, 2, Feeder Rd, Beehive Garden,

Belghoria, Kolkata, West Bengal 700056.

*Corresponding Author E-mail: royushri@gmail.com

 

ABSTRACT:

Polyamines (PA) are found in all organisms. Polyamines are small aliphatic amines that have more than two amine groups. There are three main polyamines that are found in plants namely putrescine, spermidine and spermine. They can exist in both free and combined forms. In the regulation of growth, development, polyamines have regulatory roles. Polyamines also help plants in biotic and abiotic stress. Being positively charged, polyamines have the ability to interact with negatively charged sites in molecules such as nucleic acids, proteins, and lipids. Polyamines correlate with numerous vital biochemical functions, including protein regulation, regulation of chemiosmosis, and photoprotection in chloroplasts, ATP synthesis, ion channeling, and membrane fluidity. Through various studies it has been observed that exogenous PA application not only helped the plant to tolerate but also gave the plant resistance to several abiotic stresses (e.g. salinity, drought, water logging, osmotic stress, heavy metals, and extreme temperatures). Vigna radiata is native to India and is known as mung bean, mung dal, moong dal, mash bean, green gram, golden gram, and green soy. It is a major supplement of protein in vegetarian diets. Essential amino acids are present in good quantities among which Arginine, Phenylalanine, Leucine, Lysine are noteworthy. Vigna radiata is also a good source of vitamin, mineral and trace element as well as dietary fibres. Some varieties of mung bean possess excellent aroma and are called Sona mung (B1 variety). The present investigators have used the Sona mung for the study of polyamine in Vigna radiata along with other four different varieties, during the growth and development.

 

KEYWORDS: Polyamines, Putrescine, Spermidine, Spemins, Vigna, mung, Thin Layer Chromatography.

 

 


INTRODUCTION:

Plants produce different kinds of chemical compounds along with the regular hormones to regulate their physical and metabolic activities. Different methods are used to extract and estimate the active constituents and the effect of the compounds on plant metabolism and growth are observed1,2. Polyamines are cationic molecules found in every living cell. They not only play roles in plant growth and development, but also help the plant to adapt to environmental stresses. In plant cells, the diamine putrescine (Put), triamine spermidine (Spd) and tetramine spermine (Spm) constitute the major PAs. They can exist in both free and combined forms3.

 

In the combined forms they are either conjugated to small molecules such as coumaroyl, ferulic or hydroxycinnamic acids and are perchloric acid (PCA) soluble or bound to larger molecules such as lipids, nucleic acids or proteins and are PCA- insoluble4,5. The appropriate levels of free PAs during developmental processes are maintained by interconversion between free and combined PAs6,7. Many cellular functions including transcription and translation are influenced by PAs8. On the basis of polyamines, the synthesis, structure and properties of aminoquinoid redox polymers have been developed and studied9.

 

Changes in free and conjugated PAs and their biosynthetic enzymes have been found to occur during developmental processes. Authors had thoroughly investigated and reviewed PA biosynthetic pathways in plants10-14. In higher plants PAs are synthesized either directly from ornithine (one-step process) or indirectly from arginine (multi-step process) by ornithine decarboxylase and arginine decarboxylase respectively to produce putrescine. Putrescine is further converted to spermidine and spermine by successive transfers of aminopropyl groups from decarboxylated S-adenosylmethionine (dcSAM) to putrescine, catalysed by specific spermidine synthase and spermine synthase. Methionine is first converted to S-adenosylmethionine (SAM) and then decarboxylated in a reaction catalyzed by SAM decarboxylase (SAMDC). The resulting dcSAM is utilized as an aminopropyl donor. SAM is a common precursor for both PAs and ethylene and SAMDC is involved in the regulation of both biosynthetic pathways.

 

From the earlier experimental data it was shown that increase in PAs and their biosynthetic enzymes were associated with rapid cell division in many plant systems such as in carrot embryogenesis, tomato ovaries, tobacco ovaries, and also in fruit development. Similar results have been reported for many other plant species15-20.

 

Polyamines are redox polymers and were used in polarography research to observe the absorption and adsorption of Cr (VI) ions21. Authors investigated general properties and relative activities of polyamine biosynthetic enzymes in mung bean (Vigna radiata L.) tissues22. Two years later Put, Spd and Spm were found in proportions depending on the state of maturation in the mung-bean hypocotyls23. Put was the major polyamine detected, whereas Spm was present in trace amounts in xylem exudates from stems and in phloem sap of mung bean plants (Vigna radiata L Wilczek)24.

 

In the 20th century there were several reports on polyamines in many plant species, regulating different developmental processes. The transcript levels and activities of the polyamine biosynthetic enzymes and free polyamine titers, throughout the growth stages of peach fruit (Prunus persica L. Batsch cv. Redhaven) grown under field conditions and a sharp increase in spermidine titers in corns of Polianthes tuberosa (cv. Double) at the early floral initiation stage25,26. On the contrary polyamines also showed an inhibitory effect on the activity of endopeptidase in mung bean cotyledons27.

 

Investigation of polyamine titers during different stages of fruit development proved the relationship between polyamine and fruit development28. In the early stage of fruit development the polyamines were maintained at a high level, followed by decline with fruit development processing29.

 

From very ancient times, plants have been used for their medicinal values. Plants are being used as antipyretic agents, antimicrobial agents30-32. In India mung bean (Vigna radiata) has been cultivated throughout the plains. It has high nutritional value (protein 21%–28% and carbohydrate 69.2%). The dark seed colour of mung bean contains anthocyanins which is an 'anti-aging' agent or antioxidant. Like many other plant sources, pulses are also used as an anti-cancer diet.

 

In the present investigation the polyamine content of Vigna radiata seeds in relation to dormancy breaking through the imbibition period was analyzed. Dormancy was characterized by very low levels of PAs, hormones, DNA, RNA and protein metabolism and high levels of ABA. Release from dormancy giving rise to sprouting was related to dramatic perturbation in cell morphology and metabolism. A sharp and rapid increase of PA biosynthesis was observed after breaking of dormancy (the early G1 phase) followed by the degradation and the new synthesis of protein, RNA and non-chromosomal DNA. Inhibitors of PA biosynthesis affect both DNA replication and cell cycling. Tuber dormancy was broken up by PA application33. Similar results were obtained in N. tabacum cell suspension cultures34.

 

Imbibition was efficient in breaking dormancy in plant species, promoting germination. Seed imbibition is the first step in seed germination or sprouting. The polyamine content of Vigna seeds differing in imbibition condition would put light in the mobilization of polyamines in Vigna seeds.

 

The endogenous PA titre may have a fundamental role in seed development and maturation along with different plant hormones. In the present study the PA levels of immature and mature pods were studied in Vigna radiata to understand the role of PA during Vigna seed development. PA was extracted from five different varieties of mung bean. The endogenous polyamine titers in field grown plants of Vigna radiata leaves were estimated to correlate polyamine synthesis during growth. A comparative study has been made in five different varieties of Vigna radiata.

 

MATERIAL AND METHOD:

Plant Material preparation:

Five varieties of Vigna seeds (namely B1, TM 99, TARM 2, PDM 84 and TM 98) were collected from Baharampur Pulse and Oilseed Research Centre, W.B. Seeds were sowed during the month of November. Seedlings were maintained in earthen pots containing a commercial soil rite and soil mix (in a ratio of 1:1). Plants were allowed to grow in a greenhouse where the photoperiod was maintained for 16 h. The average day temperature was 250C with a night temperature maintained at 150C. The emergences of pods was observed after 2 months of sowing and the seeds matured in less than 3 months i.e. 1st week of January of next year.

 

For observing the effect of imbibition on polyamine content, seeds were imbibed with differing imbibition periods after sterilization. For comparative study of polyamine content during plant growth, polyamine content was estimated from leaves, immature pods and mature pods of these five varieties grown in the greenhouse.

 

For observing the polyamine content in seeds of Vigna differing in imbibition period, seeds of the 5 varieties were sterilized in 10% sodium hypochlorite solution (NaOCl, v/v). The sterilized seeds were allowed to imbibe water. Three sets were maintained for each with the imbibition period for 24h (1 day), 48h (2 days), and 72h (3 days) in t conical flasks, with 50ml autoclaved distilled water.

 

Polyamine Extraction and Estimation:

PAs were extracted from imbibed seeds, leaves and immature and mature pods of Vigna plant. 300mg imbibed seeds were weighed and used for extraction. Leaves, immature and mature pods from five different varieties of mung bean, were surface sterilized and 300 mg explants were taken for PA extraction.

 

Explants were frozen in liquid nitrogen and were ground to fine powder using pre-chilled mortar and pestle. The frozen powder was then homogenized in 1 ml ice cold perchloric acid (10%, v/v) solution. The homogenates were incubated at 40C for 30 min and were subjected to centrifugation for 25min at 14000rpm at 40C. The supernatant was collected and aliquot (0.1ml) of each extract was mixed with 50mg sodium bicarbonate and 0.2ml dansyl chloride (10mg/ml). The mixture was incubated at 260C overnight in the dark. Dansylated polyamines were extracted with 0.2ml toluene and centrifuging for 10 min at 10000rpm. The upper aqueous layer of polyamines was collected and was used for polyamine analysis through Thin Layer Chromatographic (TLC) studies. The 0.1ml of standard polyamine stock solutions (10mM Put, 10mM Spd, 10 mM Spm) were also dansylated and were used in Thin Layer Chromatographic studies.

 

Ethyl acetate and cyclohexane were mixed at a ratio of 2:3. Pre-coated TLC plates layered with non-fluorescent 0.2mm thick silica were used and 0.1ml extracted dansylated polyamines from each set was loaded as tiny droplets. The loaded plate was placed into the TLC chamber.

 

The spots of PAs corresponding to standard PAs were scrapped and eluted with acetone vortex mixing followed by centrifugation at 4000rpm for 5 min. The supernatant for each sample was collected and used for biological assay. The relative fluorescence of dansylated PAs was scanned using a Fluorescence Spectrophotometer, excitation at 360nm and emission at 506 nm. Polyamine content was estimated according to the formula given below:

 

Spectral Reading X Correction Factor X Volume of toluene used X Volume of supernatant

 

PA content= --------------------nmoles/g of fresh weight

 

Volume of supernatant charged X Volume of supernatant taken for dansylation X Fresh weight

 

Correction Factors for standard PAs were: Put: 1.77 X 10-5, Spd: 3.41 X 10-5 and Spm: 2 X 10-5

 

The data obtained by the above experiments were statistically analyzed by Student’s t-test using 5% level of significance35. The formula was used for testing the significance of difference between means of two independent samples of small population (30<). The observed difference between means was converted to a t-score using pooled standard deviation. The percentage of significance was observed from a table of the critical values of t for two tailed tests.

 

RESULT:

Changes in free PA titers after 1 day, 2 days and 3 days imbibition period were observed. The PA content increased drastically after 2 days of imbibition than 1 day as shown by quick and stable increase of all three fractions of PAs in all five varieties studied. Spd titers were present in higher content than that of Put and Spm throughout the imbibition period. The Put content was found to be similar in B1 and TM 99 varieties but showed little increase in other thee varieties, after 3 days of imbibition period. The increment in Spd content slowed down after 3 days of imbibition period (except PDM 84). The level of Spm decreased or remained the same after 3 days. The total polyamine content in imbibed seeds reached maximum level in 2 days of imbibition period which did not increase further when seeds were allowed to imbibe more water (Fig 1), only PDM 84 showed little increase in total PAs after 3rd day of imbibition.


 

Fig 1: Polyamine Content of Vigna with Different Imbibition Period

 

Fig 2: Free Polyamine Content immature and mature pods of Vigna radiata

 


The Put, Spd and Spm content of immature pods were analyzed with PA content of mature pods of each variety. In the B1 variety, the Put content decreased significantly together with Spm content in mature pods in comparison to immature pods. But the content of Spd increased in mature pods. The total PA content of immature pod was significantly higher in immature pod than mature pod. The TARM 2 variety showed a similar pattern of PA titre. The total PA was also high together with Put and Spm content in immature pods when compared to mature pods. PDM 84 variety showed a little difference in PA content with B1 and TARM 2 varieties, where total PA content together with all Put, Spd and Spm content was higher significantly in immature pods as compared to mature pods. But TM 98 and TM 99 varieties also showed decreases in Put, Spd and Spm content as well as the total PA content in mature pods with respect to immature pods like PDM 84 variety (Fig 2).

 

To summarize these results, the Put and Spm content was significantly decreased in mature pods in comparison to immature pods of B1 and TARM 2 varieties, but Spd content was increased in mature pods. At the same time in PDM 84, TM 99 and TM 98 varieties, all the fractions of PAs (Put, Spd and Spm) decreased in mature pods. When the total PA content was considered in immature pods with respect to mature pods it was clear that total PA content decreased significantly in all these five varieties of Vigna radiata studied.

 

When polyamines were extracted from these five varieties of mung bean plant leaves, Spd was highest in all these varieties. Data of polyamine content (Put, Spd and Spm) in leaves of five different varieties of Vigna radiata were analyzed by taking B1 as control (Fig 3).

 

The Put content was higher in B1 variety than other varieties except PDM 84 and it differed significantly with all varieties. The Put content was found to be maximum in PDM84. The Spd content was found maximum in B1 variety and it differed significantly with all other four varieties studied. On the contrary, the Spm content was lowest in experimental control, excepting TM 98. The Spm content did not differ significantly with PDM 84 but differed with other varieties. The total PA content of the leaf was higher in the B1 variety except PDM84 where the highest amount of total PA was found.

 

 

Fig 3: Polyamine Content of Leaf in 5 Different varieties of Vigna radiate

 

DISCUSSION:

The studies conducted during the last two decades have explained many aspects of physiology and biochemistry of PAs in plants. A lot of work was done probing the relationship between polyamine and floral and fruit development, which was helpful for elucidating the mechanism of polyamine involvement in these physiological processes. It was clearly understood that polyamines were essential for cell division in the organogenesis and in the early fruit setting stage.

 

The correlation of spermine levels with ovary senescence and with fruit set and development in Pisum sativum L was observed36. The study indicates that changes in spermine levels are involved in the control of ovary senescence and of fruit set and development. In fruiting cuttings of Vitis vinifera L. cv. Cabernet Sauvignon, free, conjugated and wall-bound polyamines were observed37. Polyamine composition differed according to tissue and stage of development. In developing embryos of Pinus taeda, highest polyamine content was found in cotyledonary stage followed by significant decrease in the mature seed38.

 

In dormancy, seed water content decreased to 5-15% depending on the nature of the storage nutrients. The quiescence was reversed by uptake of water through imbibition, by the degradation of storage materials and activating the oxygen-consuming metabolism, synthesizing new enzymes (like ATP-, m-RNA-, protein- and lipid-synthesis), plant growth regulators (like hormones and polyamines) thus preceding growth39.

 

Plants have been used for years for their medicinal values40-42. Mung bean has been grown in India for its nutritional and medicinal value. In the present study the free polyamine content in relation to imbibition period has been carried out in mung bean seeds. The correlation between free polyamines and growth of mung bean plants was also investigated in five different varieties. Change in free and PCA soluble bound polyamines, Put, Spd and Spm was detected during imbibition period and growth in greenhouse-grown plants.

 

For understanding the PA mobilization in relation to the imbibition period followed by germination, PAs were extracted from 1 day, 2 days and 3 days of imbibed germinating seeds. In 2 days-imbibed conditions there was drastic increase in Put, Spd and Spm content increasing the total PA content in comparison to 1 day imbibed seeds. Further imbibition did not show remarkable change in Put and Spd content but Spm content was decreased. The total PA content also remained the same in 3 days of imbibition period when compared with PA content of 2 days of imbibition period in all varieties, except PDM 84 where little increase in total PA was observed. So the free and PCA-soluble PA content showed its maximum level in 2 days imbibed condition in relation to 1 day imbibed condition. The PA content maintained its level even when a more imbibed condition was imposed for 3 days. It can be concluded that water imbibitions induce higher PA level leading to mobilization of nutrients and after an optimum period of imbibition there was no further mobilization of PA.

 

A similar kind of observation was observed in the polyamine content on the developing fruit and seed of pumpkin (Cucurbita pepo L.)29. Polyamine analyses of the pericarp and the testa tissues showed a higher level of all three polyamines early in development coincident with the period of rapid cell division, differentiation and growth. All three polyamines declined in the testa upon maturity. Spd is the major polyamine metabolite in Paspalum scrobiculatum root/shoot tissues43. Spd elevation in salt stressed seedlings in concentration and time dependent manner was reported.

 

When the PA contents in immature pods and mature pods were measured, the levels of Put and Spm were much higher in immature pods than in mature pods in all these five varieties studied. The total PA content was also higher significantly in immature pods with respect to mature pods. From the above experimental observation it was clear that the content of polyamines was high in immature pods which decreased significantly when the seed matured. So it can be concluded that the polyamines play an important role in Vigna radiata seed development.

 

This result is in accordance with other scientists44. The changes of polyamine metabolism in the process of growth and development of peanuts were reported. At the podding stage polyamine content was the highest then decreased during late stages. In the pericarp of grape berry, the levels of free putrescine and spermidine were higher during early development45. mRNA levels of PA biosynthetic enzyme (spermidine synthase) were high during apple fruit development46.

 

The polyamine content in leaves and a comparison was made among those varieties. Spd content was more prevalent than Put and Spm content. The polyamine content in Vigna radiata differs with respect to the variety. Polyamine compositions of various organs of cucumber plant and they found that spermidine was present at the highest level in rapidly growing tissues implying the involvement of spermidine in the growth and development of young tissues47. The endogenous free polyamine levels among five genotypes of Vigna mungo (L) grown under field conditions were studied48. From flowering to mid-pod development stage, the levels of putrescine, spermidine, and total polyamine showed significant differences amongst the genotypes. Authors also concluded that endogenous free polyamine and putrescine may be considered as genotypic markers for nodule senescence in field grown V. mungo49. The PA concentrations of ovaries of two apricot cultivars, 'S405-17' and 'Bergeron', were collected at three stages of floral development and analyzed51. The PA levels vary with ovary development, depending on the cultivar. Higher concentrations of putrescine, spermidine and spermine were found in S405-17 cultivar than Bergeron cultivar.

 

From the above experimental data and all these examples it is shown that, in the early stage of fruit development, the polyamines are maintained at a high level, followed by decrease in the process of fruit development. During the stage of ripening of fruit the polyamine levels decline. The high polyamine concentrations were related to the high growth rate and active cell division50,51. In the initial stage of fruit development, active cell division occurs, which needs sufficient polyamines. At the later stage of fruit development, cell division gives way to cell enlargement, in which polyamine synthesis is reduced. Decrease in polyamines at the late stage of fruit development has been regarded as a signal for fruit ripening52.

 

Summary:

From the experiment discussed the role of polyamines in breaking the dormancy (through imbibition) and pod development was established in Vigna seeds. At the first stage rapid increase of polyamine content was observed after imbibition, leading to germination of the seeds. But the increase of polyamines was not indefinite. The polyamine content increased maximum after 2 days of imbibition period in comparison to 1 day imbibed condition. But no further increment was found due to more imbibition period. Polyamines also played a significant role in Vigna pod development. The polyamine content was observed maximum in immature pods and the content decreased when the pods matured in all the five varieties studied. It proves that the polyamines played a significant role in breaking Vigna seed dormancy leading to germination by imbibition and also have fundamental role in pod maturation. The polyamine content of leaves varied with respect to varieties but the Spd content was predominant in leaves of all these five varieties.

 

ACKNOWLEDGMENTS:

The authors are sincerely grateful to Prof. Sarmistha Sen Raychaudhuri, Dept of Plant Tissue Culture and Molecular Biology Laboratory, Department of Biophysics, Molecular Biology, and Genetics, University of Calcutta, 92, Acharya Prafulla Chandra Road, Calcutta- 700009, India for her valuable guidance, immense cooperation, and the laboratory facilities. Authors sincerely thank Dr. D. N. Sengupta, Bose Institute, Division of Plant Biology, Kolkata, for his encouragement and guidance for this research work.

 

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Received on 19.05.2021           Modified on 05.07.2021

Accepted on 10.08.2021         © RJPT All right reserved

Research J. Pharm. and Tech. 2022; 15(6):2585-2591.

DOI: 10.52711/0974-360X.2022.00432