Evaluation of nanoparticles for promoting seed germination ...ejtafs.mardi.gov.my/jtafs/45-1/nanoparticles.pdf · pertumbuhan pada biji benih padi MR263 dan MR269) M.S. Nur Azura1,

J. Trop. Agric. and Fd. Sc. 45(1)(2017): 13 – 24

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Article history Received: 20.4.16 Accepted: 26.4.16

Authors’ full names: Nur Azura Mohd Said, Zamri Ishak, Rashid Mat Rani, Mohd Shahrin Ghazali, Rafidah Abdul Rahman, Mohammad Rejab Ismail, Azima Azmi, Suria Mohd Saad and Amyita Witty Ugap E-mail: [email protected] ©Malaysian Agricultural Research and Development Institute 2017

Evaluation of nanoparticles for promoting seed germination and growth rate in MR263 and MR269 paddy seeds (Penilaian partikel nano untuk menggalakkan germinasi biji benih dan kadar pertumbuhan pada biji benih padi MR263 dan MR269) M.S. Nur Azura1, I. Zamri1, M.R. Rashid1, G. Mohd Shahrin1, A.R. Rafidah1, I. Mohammad Rejab1, A. Azima1, M.S. Suria1 and W.U. Amyita2

1Biotechnology and Nanotechnology Research Centre, MARDI Headquarters, Persiaran MARDI-UPM, 43400 Serdang, Selangor, Malaysia 2Gene Bank and Seed Centre, MARDI Headquarters, Persiaran MARDI-UPM 43400 Serdang, Selangor, Malaysia

Abstract Effects of various selected nanoparticles on seed germination and growth rate of two different paddy varieties, MR263 and MR293 were studied. Different types of nanoparticles with different sizes were selected, i.e. carbon-based materials [10 – 20 nm single-walled carbon nanotubes (SWCNTs) and multi-walled carbon nanotubes (MWCNTs)], ~100 nm nanosilicon and nanoscale metal oxides (70 – 100 nm CuO). Germination rate was evaluated on the second and seventh day; while both root length and shoot length were measured on the seventh day. MR263 paddy seeds treated with 1 mg/ml nanosilicon particles exhibited the highest germination rate. Germination rate of paddy seeds treated with nanosilicon increased from 13% (second day) up to 95% (seventh day). In terms of growth rate, nanosilicon, SWCNTs and MWCNTs exhibited 34 – 41% root length growth for MR263 variety compared to controlled (untreated) seeds. Germination rate for MR269 however was not greatly affected by nanoparticles treatment, with only 7 – 9% root growth measured. CuO nanoparticle was found to inhibit and suppress the paddy seeds growth from both varieties, presumably due to its toxicity property. It was concluded that smaller nanoparticles produced better germination rate as they are able to penetrate the seeds’ pores better and subsequently increase the seeds water uptake. Keywords: nanoparticles, germination rate, carbon nanotubes, nanosilicon, copper oxide and paddy seeds

Introduction Nanomaterials are defined as particles with size less than 100 nm in at least one dimension (Roco 2013); and are gaining vast interests in recent decades. According to US Nanotechnology White Paper (2005), engineered nanomaterials can be divided into four types, i.e. (i) carbon based materials, (ii) metal-based materials and nanoscale metal oxides; (iii) dendrimers/nano-sized polymers and (iv) composites (combination of nanoparticles).

The first two types are the most common nanomaterials that are often studied. Owing to the nano-size and their outstanding properties, nanoparticless have lent themselves well in wide applications ranging from electronics, medicine, sensing, defense, food industry and agriculture (Aitken et al. 2006). However, in the latter application, the use of nanoparticles is relatively new and still has not been fully explored.

Generally, the employment of nanoparticles in agriculture envisages that

Evaluation of nanoparticles in paddy seeds

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these particles will impart some beneficial effects to the crops. In the seed industry, it has proven that the nanoparticles could improve both plant germination and growth rate of the seeds (Khot et al. 2012). Unlike seed dormancy which is undesirable in agricultural crops, rapid germination and growth are required hence the study incorporating nanoparticles. However, reports related to understanding nanoparticle and plant interactions are still limited and sometimes contradictory. In terms of seed industry itself, the global seed industry is valued at USD 7.67 billion in 2009. As for Malaysia, the total imports are valued at USD 3.8 millions and export at USD 0.7 millions (Madom et al. 2013). These values are relatively low and another concern is that the supply of high quality seed or planting materials in Malaysia is still insufficient and inconsistent. Among the vegetable, ornamentals, cover crops and fruits’ seeds, only rice seed industry is well developed and established in Malaysia with MARDI as the producer, breeder and foundation seeds.

The effects of nanoparticles on various seeds have been studied by researchers in recent years. The most widely reported nanoparticles are carbon nanomaterials namely single walled carbon nanotubes (SWCNTs) and multi walled carbon nanotubes (MWCNTs). Their effects have been studied in seeds such as tobacco (Khodakovskayaa et al. 2012), tomato (Khodakovskayaa et al. 2011), barley, corn, soybeans (Lahiani et al. 2013), cotton (Nalwade and Neharkar 2013) and maize (Tiwari et al. 2014), to name a few. Meanwhile for the paddy/rice seeds, apart from MWCNTs (Nair et al. 2010), effects from silver nanoparticles (Thuesombat et al. 2014), ZnO and TiO nanoparticles (Boonyanitipong et al. 2011) also have been investigated. These studies are important in understanding the nature of interactions between nanomaterials and plants in order to comprehend the impact of nanotechnology

in agriculture particularly its toxicity concerns, plant disease treatment and genetic engineering. Certain types of nanoparticles were found to either activate or inhibit specific physiological processes of the seedlings growth, depending on the concentrations.

In this study, we examined the effects of selected nanoparticles on local breed paddy seeds of two different varieties (MR263 and MR269). Different types of nanoparticles with different sizes were selected, namely SWCNTs and MWCNTs of 10 – 20 nm, 100 nm nanosilicon and ~70 – 100 nm CuO. The latter nanoparticle (CuO) was selected due to its well-known antibacterial properties. This study will provide us the information regarding comparisons of different classes of nanoparticles’ effects towards the paddy seeds’ root development (including number of roots) in addition to the effects on seed germination and root elongation of rice. This approach helps to enhance our understanding of the phytotoxicity effect posed from the different nanoparticles on this plant species. Materials and methods Seed material Paddy seeds of MR263 and MR269 varieties breed were obtained from Rice and Paddy Research Centre, MARDI Seberang Perai. Both paddy seeds varieties was launched by MARDI in 2010 and 2013 respectively. Nanoparticles solution preparation CuO, silicon nanoparticles, SWCNTs and MWCNTs were all purchased from SkySpring Nanomaterial, USA with purity of 95 – 99%. All nanomaterials solutions were prepared in 25 ml distilled water (DW) with three different concentrations, i.e. 0.25, 0.5 and 1 mg/ml. The nanoparticle suspensions were sonicated for 45 minutes prior use. Pure distilled water (DW) was used and accounted for control study in each nanoparticle treatments.

M.S. Nur Azura, I, Zamri, M.R. Rashid, G. Mohd Shahrin, A.R. Rafidah, I. Mohammad Rejab, A. Azima, M.S. Suria and W.U. Amyita

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Microscopic characterisation Scanning electron microscopy (SEM) were carried out using Phenom Pro-X SEM with EDX Analysis Desktop (Phenom-World B.V., The Netherlands) at Crest Nanosolutions (M) Sdn. Bhd., Puchong Business Park, Selangor. Transmission electron microscopy (TEM) (Hitachi H-7100) was done in Microscopic Unit, Institute of Bioscience, Universiti Putra Malaysia (UPM). Nanoparticles treatment Seeds sterilisation was carried out by soaking 180 – 200 seeds in 5.25% sodium hypochlorite (Sigma Aldrich) for 10 min. The seeds were then placed on Buchner filter funnel, rinsed 3 – 5 times with DW and dried on filter paper for 20 – 30 min. Subsequently, the seeds were soaked in 25 ml nanoparticles solutions of different concentrations (0.25, 0.5 and 1 mg/ml) for two h. A total of twenty seeds were then transferred onto soaked filter paper in a round container with distance

spacing of 1 cm between the seeds. Each treatment was conducted with three replicates. The seeds were left to germinate in the designated germination room for a week. Seedlings evaluation and data collection The seeds were checked for germinations on the second day while the growth rate was measured on the seventh day following the seeds’ treatment with the nanoparticles solutions. Among the growth parameters that were being studied include the primary root length, shoot length and root numbers. Data were recorded and analysed using t-test statistical method. Results were presented as mean ± SE (standard error of the mean). A significance level of α = 0.05 was used in all analyses. The schematic layout of the whole experimental design was as illustrated as in Figure 1.

Figure 1. A schematic of paddy seeds (MR263 and MR269) treatment with selected nanoparticles. Blank distilled water (DW) was used as control study. Following the nanoparticles treatments and germination/seed growth study, statistical analysis was then performed.


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Results and discussion TEM images for nanoparticles The images for nanoparticles from each class; MWCNTs from carbon nanotube group, nanosilicon and CuO from nano metal oxides, were obtained using transmission electron microscopy (TEM) and their sizes were verified. As can be seen from Plate 1, MWCNTs have width of approximately 10 – 20 nm, whilst nanosilicon and CuO have average diameter of 76.78 ± 20.92 nm and 78.22 ± 19.91 nm. All nanoparticles used in this study were of pristine materials i.e. non-functionalised. Germination rate Seed germination and embryo growth are the most important stages in life cycle of plants. There are different definitions of seed germination according to its root length available. However, the general accepted term of germination commences with the uptake of water by the seed (imbibitions) and once the seeds had shown the emergence of radical or cotyledon from the seed coat (Bewley 1997; Lin and Xing 2007). Water uptake process by a mature seed involves a triphasic step with a rapid initial uptake at the phase I (molecular level), Phase II (plateau phase) and phase III occurs after germination is completed (post-germination) (Bewley 1997) (Figure 2).

The seeds germination were observed on the second day as most of the paddy seeds had full germination on the third day. If the treatment with nanoparticles were successful in inducing the germination rate, then it will mostly happened on the second day post imbibition. As shown in Figure 3, the percentage of germination on the second day post treatment for SWCNTs increased up to 2.78% and 7.22% compared to control study for MR263 and MR269 respectively with 0.25 mg/ml SWCNTs. However treatment with MWCNTs did not show any significant increase in germination rates within the first 2 days (less than 1%). By the

seventh day, only MR263 variety exhibited germination rate up to 5% with 0.25 mg/ml SWCNTs and 1.66% with 1 mg/ml MWCNTs while MR269 variety treated with both CNTs-based nanoparticles exhibited less or as similar as the control study’s germination rate. The highest seed germination rate recorded was from 1 mg/ml nanosilicon for both paddy seeds varieties when compared with the controlled seeds. The percentage of paddy seeds germination rate treated with nanosilicon increased from 13.33% on the second day up to 95% on the seventh day for MR263 and 21.11% (second day) to 98.33% (seventh day) for MR269 variety. However in terms of percentage difference, these values were considered low as they differ only in the range of 2 – 6% when compared to the controlled seeds. For the CuO treatment, the lowest concentration (0.25 mg/ml) were required to increase the germination rate for MR263 (11.67% on second day to 93.33% on the seventh day, with percentage increment of 2.23%). For MR269 on the other hand, 1 mg/ml CuO showed the highest germination percentage of 3.89% difference compared to control study on the second day.

Previous studies on nanoparticles and seeds germination rate are very limited and sometimes contradictory, depending on the types of nanoparticles and seeds studies. Nair and co-workers (2010) had reported that the incorporation of both SWCNTs and MWCNTs at 30 µg/ml showed positive effects towards the germination of paddy seeds, however the detailed statistical data has not been published. Besides paddy, 25 µg/ml MWCNTs in suspension form also had proven to increase the germination rate for other crops such as soybean by approximately 10% (Lahiani et al. 2013). CNTs, at the concentration range of 10 – 40 µg/ml when applied to the tomato seeds, exhibited a substantial percentage increment of 20 – 50% when compared to the controlled seeds.


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Plate 1. TEM images for (a) MWCNTs; (b) nanosilicon; and (c) CuO (scale bar 100 nm)

Figure 2. Triphasic process associated with seed germination and postgermination upon water uptake (Bewley 1997)


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The tomato seeds treated with CNTs had started to germinate on the third day while untreated tomato seeds still had not germinate at that time (Khodakovskaya et al. 2009). On the other hand however, seed germinations for radish, rape, lettuce and cucumber were not affected by the 2 mg/ml of MWCNT, Al2O3, ZnO, Al and Zn. Nano-Zn and nano-ZnO were found to inhibit the germination for ryegrass and corn seeds (Lin & Xing 2007).

Overall, the percentage values obtained from the MR263 and MR269 germination rate were relatively very low considering the seeds were not fully germinate within the first 2 days and even on the seventh day, the difference with control study is negligible. This low germination rate could be attributed to the plant seed’s coating. Seed coat plays a very important role in protecting the embryo and have selective permeability towards certain suspensions (Lin & Xing 2007).

In our case, paddy seeds had a hard testa surrounding the seeds (Plate 2) hence this may explain why seed germination in this study was not greatly altered by nanoparticles as the testa may have deterred direct adsorption or caused non-uniform penetration of the nanoparticles suspensions (Wierzbicka and Obidzińska 1998). Seedlings growth rate The growth rate study of paddy variety MR263 (Figure 4) showed both SWCNTs and MWCNTs at concentration of 0.5 mg/ml resulted in the longest primary root length i.e. 48.86 ± 18.26 mm (34.64% cf. control) and 49.70 ± 21.24 mm (40.99% cf. control). For the nanosilicon, the lowest concentration (0.25 mg/ml) produced the longest root length with 49.49 ± 17.56 mm (33.83% cf. control). The percentage increment for root length with nanosilicon is relatively lower

Figure 3. Percentage of paddy seeds germination on the second and seventh day for MR263 and MR269 treated with different concentrations of nanoparticles


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(a)

Plate 2. The paddy seed coat (testa) observed under different magnifying power; (a)paddy seed coat observed under light microscopy (magnification of 40x); (b – d) seed coated surfaced as observed under SEM with magnification of 150x, 600x and 1500x

Figure 4. Effects of various concentrations of SWCNTs, MWCNTs, nanosilicon and CuO towards seedling growth i.e. (a) primary root length, (b) shoot length and (c) root numbers for MR263 variety paddy seeds. Blank control study with no nanoparticles is represented by 0 mg/ml

(b) (c)


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compared to the first two nanoparticles treatments. The treatment with CuO on the other hand, was found to inhibit the growth of the MR263 seed root length by 69.81%. The highest percentage of shoot length recorded is with 0.25 mg/ml MWCNTs with 16.27% cf. control followed by 1 mg/ml of CuO with 10.06% cf. control (Figure 4b). The root numbers however, are not greatly affected by the nanoparticles.

It is interesting to note that growth rate of the seeds inversely proportional to the nanomaterials’ size. In this case, both SWCNTs and MWCNTs have dimensions of 10 – 20 nm in comparison with nanosilicon with calc. ~73.65 ± 29.28 nm. Smaller nanoparticles are able to penetrate the seeds’ pores better and subsequently increase the germination rate by increasing the seeds water uptake (Khot et al. 2012). Nevertheless, the shoot length did not increase greatly with the nanoparticles treatment. We also observed that concentrations of the nanoparticles also influenced both germination and seedling growth rate. High concentration (1 mg/ml) resulted in better germination rate and only low concentration (0.25 mg/ml) of nanoparticle were required to promote the best seedling root length. The concentrations in which MWCNTs gave positive effects to growth were reported in the range of 20 – 500 µg/ml, depending on the the plant species (Lahiani et al. 2013; Tiwari et al. 2014). Higher concentration of MWCNTs may only give harmful result to plant whereby it was previously reported by Begum et al. (2012) that 2 mg/ml of MWCNTs were shown to have adverse effects to the plant growth.

It was also found out that while SWCNTs, MWCNTs and nanosilicon help to increase the growth rate for MR263 paddy variety, these treatments on MR269 variety has no pronounced effects. Although there are slight increments measured, the percentages are still very low with only

maximum growth of 8.91% cf. control ofr primary root length for the treatment with 0.25 mg/ml MWCNTs (Figure 5a). The shoot growth for MR269 seeds treated with both SWCNTs and MWCNTs were less when compared to control while treatment with 0.5 mg/ml nanosilicon and 0.25 mg/ml gave shoot increment of 2.31% and 16.54% cf. control respectively (Figure 5b). For the root numbers, treatment with 1 mg/ml MWCNTs led to an increment of root numbers by 51.81% (Figure 5c).

The difference between the seedlings growth between the two seed varieties can be related to their unique morphologies and breeding characteristics. MR269 variety which was released by MARDI in 2013 was claimed to be more resistant towards disease compared to the MR263 variety that was launched earlier in 2010 (Saad et al. 2014). In terms of seeds’ morphologies, paddy seed MR263’s testa was found to be covered with short and broad pores while MR269’s pores were long and narrow (Plate 3). Such discrepancies in the pores’ morphologies resulted in different adsorption rate for the nanoparticles suspensions hence MR269 variety was less affected by the nanoparticles treatment due to its smaller pores.

As for CuO nanoparticle, this nanomaterial was found to inhibit and suppress the paddy seeds growth from both varieties. As can be seen from Figure 4(a) and 5(a); and as shown in Plate 4, the paddy seeds treated with CuO has halted the root length when compared to the controlled paddy seeds. Statistical analysis carried out also indicated that these values of root length exposed with CuO are significantly decreased. However, the shoot length for both MR263 and MR269 were seen to increase by 16.5%. These findings were similar as reported by other groups where Cu-based nanoparticle showed reduced length for emerging roots in zucchini (Stampoulis and Sinha 2009) and increase in shoot compared to control plants for lettuce


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seeds (Shah and Belozerova 2009). We presume this could be due to the toxic property of CuO which is more pronounced in the roots hence suppressed the water uptake pathways as the copper entered the cell membrane (Lee et al. 2008). Toxicity of other types of metal-oxide based nanoparticles such as ZnO and TiO2 were also reported and these nanoparticles inhibited the root elongation for paddy seeds (Boonyanitipong et al. 2011).

The aquaporin gene (water channel gene) has been reported to be responsible for the root elongation process of the seeds when they are exposed to the nanoparticles treatment. Apart from that, a number of other genes related to plant stress also were found to be up-regulated in the seedlings (Khodakovskaya et al. 2012). In order to

elucidate the water uptake mechanism, we will be studying the biological mechanisms and reactions via molecular techniques. Other future work will also incorporate toxicity assessment study of the exposed seedlings.

Overall, these findings suggest that nanoparticles exerted either positive germination and growth rate or toxicity on seeds depending on their chemical composition, size, concentrations and types of plants/varieties of seeds. Specific types of nanoparticles in low doses was not harmful to plants but instead are capable of activating specific physiological processes.

Figure 5. Effects of various concentrations of SWCNTs, MWCNTs, nanosilicon and CuO towards seedling growth i.e. (a) primary root length, (b) shoot length and (c) root numbers for MR269 variety paddy seeds. Blank control study with no nanoparticles is represented by 0 mg/ml

(a)

(b) (c)


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Conclusion From the studies conducted, we can conclude that in order to attain better germination rate, high concentration (1 mg/ml) of nanoparticles were required whilst lower concentrations (0.25 – 0.5 mg/ml) of nanoparticles were needed to promote the best seedling root length. Smaller nanoparticles were able to penetrate the seeds’ pore better hence stimulating the germination and activate enhanced growth in paddy seeds. However oxygen uptake as indicated by the shoot length measurements did not increase greatly with nanoparticles treatment. MR263 and MR269 exhibited different effects towards nanoparticles treatment which are addressed to the different morphologies between the two varieties. Both SWCNTs and MWCNTs (size 10 – 20 nm) show superior effect on primary root/shoot length followed by silicon nanoparticle (approx 70 nm). Metal-oxide based nanoparticle (CuO) was found to inhibit and suppress the paddy seeds growth from both varieties, which could be due to the toxicity or large nanoparticles

Plate 4. Comparison of growth rate (primary root length) for controlled paddy seed (left); with paddy seed treated with CuO (right)

Plate 3. Paddy seed testa (outer layer) of (a) control MR263 (untreated); and (b) control MR269 (untreated), as observed under SEM (scale bar 50 µm, magnifying power of 1300 – 1500x). The morphologies for both MR263 and MR269 are distinguished by the difference in the seeds’ pore sizes


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size. The positive and encouraging finding on the nanoparticles treatment’s effect on paddy seeds could be the basis in expanding the nanoparticles application to other planting seeds such as tomato and papaya seeds. It is recommended that MWCNTs and nanosilicon with low concentrations (less than 0.5 mg/ml) should be selected for paddy seeds’ future studies taking into account the balance between the germination and seedling growth factors. Acknowledgement Authors would like to thank MARDI for the Development Fund (P-RB-121-1001, Project No. 21003001210001-D) dedicated to this project. References Aitken, R., Chaudhry, M.Q., Boxall, A.B.A. and

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Abstrak Kesan pelbagai partikel nano terpilih terhadap percambahan dan kadar pertumbuhan dua jenis biji benih padi, MR263 dan MR269 dikaji. Partikel-partikel nano daripada pelbagai kumpulan dan saiz yang berbeza telah dipilih, iaitu bahan berasaskan karbon [10 – 20 nm single-walled carbon nanotubes (SWCNTs) dan multi-walled carbon nanotubes (MWCNTs)], silikon nano ~100 nm; dan oksida logam berskala nano (CuO bersaiz 70 – 100 nm). Penilaian kadar percambahan diambil pada hari kedua dan ketujuh, manakala kedua-dua panjang akar dan panjang pucuk diukur pada hari ketujuh. Benih padi (MR263) terawat dengan 1 mg/ml partikel silikon nano menunjukkan kadar percambahan biji benih tertinggi. Peratusan kadar percambahan biji benih padi terawat dengan silikon nano meningkat daripada 13% (hari kedua) sehingga 95% (hari ketujuh). Dari segi kadar pertumbuhan; partikel silikon nano, SWCNTs dan MWCNTs mempamerkan panjang akar sebanyak 34 – 41% untuk biji benih MR263 berbanding dengan biji benih kawalan. Kadar pertumbuhan biji benih MR293 pula didapati kurang dipengaruhi oleh rawatan partikel-partikel nano dengan hanya 7 – 9% pertumbuhan akar dicatatkan. Partikel CuO didapati merencat dan menyekat pertumbuhan kedua-dua jenis varieti biji benih, berkemungkinan disebabkan oleh sifat ketoksikan bahan kimia tersebut. Sebagai rumusan, partikel nano yang bersaiz lebih kecil dapat menghasilkan kadar percambahan yang lebih baik kerana partikel-partikel ini mampu untuk menembusi liang biji benih dengan lebih efektif dan seterusnya meningkatkan kadar percambahan serta kadar pengambilan air.

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Evaluation of nanoparticles for promoting seed germination ...ejtafs.mardi.gov.my/jtafs/45-1/nanoparticles.pdf · pertumbuhan pada biji benih padi MR263 dan MR269) M.S. Nur Azura1,