Drastic Differences in Silicon Concentrations between Roots and Leaves of 10 Different Solanum lycopersicum L. Varieties

in HortScience
View More View Less
  • Department of Biological Sciences, The University of Toledo, 2801 Bancroft Street, Toledo, OH 43606

Silicon (Si) absorption is highly variable among different plant types; however, few studies have examined variations among different cultivars within a single species. In this study, 10 different tomato cultivars, including determinants and indeterminants as well as hybrids and heirlooms, were hydroponically grown in the presence or absence of Si to determine the absorption and distribution of the nutrients in roots, stems, petioles, and leaves. A total elemental analysis revealed that Si concentrations significantly increased with Si treatment, and that root concentrations were significantly higher than those in leaves. Although a few species showed differences in carbon, nitrogen, and calcium concentrations in roots and leaves with Si treatment, many of the macronutrients and micronutrients were unaffected. These data suggest that tomato plants absorb Si within the macronutrient range and restrict its movement from roots to shoots.

Abstract

Silicon (Si) absorption is highly variable among different plant types; however, few studies have examined variations among different cultivars within a single species. In this study, 10 different tomato cultivars, including determinants and indeterminants as well as hybrids and heirlooms, were hydroponically grown in the presence or absence of Si to determine the absorption and distribution of the nutrients in roots, stems, petioles, and leaves. A total elemental analysis revealed that Si concentrations significantly increased with Si treatment, and that root concentrations were significantly higher than those in leaves. Although a few species showed differences in carbon, nitrogen, and calcium concentrations in roots and leaves with Si treatment, many of the macronutrients and micronutrients were unaffected. These data suggest that tomato plants absorb Si within the macronutrient range and restrict its movement from roots to shoots.

Plants vary greatly in their leaf Si concentrations, with angiosperms ranging from 0.005% to 11% (Hodson et al., 2005). Compared with other essential nutrients, this concentration is well within the range of the micronutrients; in many species, Si concentrations in the leaves exceed those of macronutrients (Epstein and Bloom, 2005; Zellner et al., In press). Tomatoes (Solanum lycopersicum L.) have been referred to as Si excluders or nonaccumulators because previous studies showed that Si concentrations in the xylem sap of the upper portion of the plant were lower than those supplied in the nutrient solution (Heine et al., 2005; Mitani and Ma, 2005; Takahashi and Miyake, 1977; and Takahashi et al., 1990). However, this suggests the restriction of Si movement, but not exclusion, because researchers have detected appreciable concentrations of the nutrient at slightly higher concentrations in the root than in the foliar tissue of tomato cultivar King Kong II (Heine et al., 2005). Other studies of foliar Si concentrations in tomato have shown lower values. For instance, Frantz et al. (2008) reported that tomato grown for 3 weeks with 1.0 mm potassium silicate accumulated 747 ppm Si in foliar tissue. Jarosz (2014) reported values of 500 ppm Si in leaves of ‘Cunero F1’ grown in the presence of 100 ppm modified colloidal silica solution and grown in the greenhouse for 8 months.

Tomatoes absorb Si and, more importantly, show beneficial responses to Si treatment. In the absence of Si, Miyake and Takahashi (1978) were able to show deficiency symptoms in ‘Bejiu’ and ‘Giant Fukuju’ that manifested as stunted growth with abnormal pollen and fruit development. The application of Si to tomato ‘Kada Gigante’ at increasing concentrations resulted in higher yields with less cracking (Marodin et al., 2014). More notable are the beneficial responses to environmental and abiotic stresses of tomato plants treated with Si. Silicon has been shown to protect tomatoes against blossom-end rot (Stamatakis et al., 2003). With Si supplementation, tomatoes were less susceptible to osmotic and salt stress (Ali et al., 2018; Li et al., 2015; Romero-Aranda et al., 2006; Shi et al., 2016; Zhang et al., 2018). Researchers have observed protection against biotic disease in tomatoes supplemented with Si and inoculated with bacterial speck, bacterial wilt, Fusarium crown and root rot, powdery mildew, and Pythium root rot (Andrade et al., 2013; Dannon and Wydra, 2004; Garibaldi et al., 2011; Heine et al., 2006; Huang et al., 2011; Kirrika et al., 2013).

This study was designed to test for variable silicon absorption and allocation in different tomato cultivars and how those concentrations affected other macronutrient and micronutrient concentrations within roots, stems, petioles, and leaves. The 10 cultivars included the heirloom indeterminates ‘Beefsteak’, ‘Brandywine Red’, ‘German Pink’, and ‘Old German’, Heinz hybrids ‘H1015’ (early) and ‘H3406’ (late), indeterminant hybrid ‘Early Girl’, and determinant hybrids ‘Mega Bite’, ‘Micro Tom’, and ‘Sweet ‘N Neat’.

Materials and Methods

Solanum lycopersicum L. seeds for ‘Beef Steak’, ‘Brandywine Red’, ‘Early Girl’, ‘German Pink’, ‘H1015’, ‘H3406’, ‘Mega Bite’, ‘Micro Tom’, ‘Old German’, and ‘Sweet ‘N Neat’ were sown in CleanStart® Oasis Medium (No. 5005; Smithers-Oasis Company, Kent, OH), rinsed and saturated with tap water (Toledo, OH), and placed in a growth chamber set at 25 °C with 45% relative humidity. When plants developed three leaves, they were moved into the greenhouse (The University of Toledo, Toledo, OH), which was maintained between 25 and 32 °C throughout the course of this study. When plants developed two or three true leaves, a single plant was transplanted into a silver 4.7-L ring-free pail (01605 Promotional Pail; Encore Plastics Corp., Cambridge, OH). Each pail contained modified Hoagland’s solution with the following nutrient concentrations for the control solution: 2 mm KH2PO4; 2.5 mm KNO3; 2.5 mm Ca(NO3)2; 1 mm MgSO4; 71 μM Fe-DTPA (Sprint 330, BASF); 9 μM MnCl2; 1.5 μM CuCl2; 1.5 μM ZnCl2; 45 μM H3BO3; 0.1 μM MoNa2O4; and 2 mm K2SO4; however, 2 mm K2SiO2 was used for the Si treatments (Frantz et al., 2005). There were four plants per treatment (n = 4), except for the control treatments, for the tomato cultivars: ‘Beefsteak’ (n = 3); ‘German Pink’ (n = 3); ‘H1015’ (n = 3); ‘Mega Bite’ (n = 2); and ‘Micro Tom’ (n = 3); the Si treatment was used for the tomato cultivar ‘Mega Bite’ (n = 3). Potassium silicate was made by adding KOH (P250-500; Fisher Scientific, Waltham, MA) at a concentration of 0.2 M to 18 MΩ H2O and silicic acid (A288–500; Fisher Scientific) at a concentration of 0.1 M and mixing on a magnetic stirrer overnight. Potassium sulfate was added to the control solutions to ensure that equal concentrations of potassium were present in both treatments. The final concentration of sulfur differed between the Si and the control treatments by 1 mm and 3 mm, respectively. Final elemental concentrations were similar for both treatments with the exception of sulfur at 3 mm and 0 mm and Si at 0 mm and 2 mm for the control and Si treatments, respectively (Table 1). Air was introduced to buckets through Tygon S3™ plastic tubing (14-171-104; Fisher Scientific) with a porous rod (F13635-0014; Bel-Art, Wayne, NJ) inserted at the submerged end. Nutrient solution was completely exchanged weekly.

Table 1.

Final nutrient concentrations in hydroponics solutions.

Table 1.

Plants were maintained under these conditions until the first flowers were present (4–8 weeks, depending on the cultivar), at which time plants were harvested. Tissue from each cultivar was collected on the same day, weighed to determine the fresh weight, and divided into roots, leaves, petioles, and stems; the stems were measured to quantify shoot lengths. The tissue was washed in 0.1 N HCl three times, rinsed in 18 MΩ H2O, placed into brown paper bags (#4 Kraft paper bags; Gordon Food Service, Aberdeen, MD) and dried at 55 °C in a drying oven (Blue M POM-1403C-1; Blue M Electric Co., Blue Island, IL) for at least 3 d. Dried tissue was weighed and ground in mortars with pestles and then placed into plastic snap cap vials (5 dr clear plastic; Thornton Plastics, Salt Lake City, UT). Inductively coupled plasma optical emission spectroscopy (ICP-OES) was performed for tissue to determine the total Si using KOH digestion (Frantz et al., 2008) and the total elemental concentrations using nitric digestion (Frantz et al., 2008; Frantz et al., 2011; Li et al., 2008). Elemental concentrations less than 1 ppm (mg Si/kg tissue) were reported as 0 ppm Si. This was a single exploratory study that was not repeated.

Statistical analysis was performed using R (R Core Team, 2016). Welch’s t test was performed to determine differences in the stem lengths of ‘Beefsteak’ using the ‘t.test(y1,y2)’ code. Analysis of variance (ANOVA) was used to analyze differences in nutrient concentrations of tomato cultivars. Tukey’s honestly significant difference post hoc test was performed using the ‘aov(DV∼T*V)’ code, where DV is the dependent variable, T is the treatment (control or Si), and V is the tomato cultivar. One-way ANOVA was also performed for each cultivar to determine differences using ‘aov(DV∼T)’.

Results

During vegetative growth, ‘Beefsteak’ plants treated with Si were, on average, 5 cm taller than control-treated plants at 12 d and 6 cm taller at 32 d after transplanting (Table 2). Interestingly, compared with the control treatment, the Si treatment resulted in larger sd at both time points. No differences in stem length of the Si-treated and control-treated plants were observed for the other nine cultivars (Table 3). There were differences in the stem lengths of different cultivars, as expected.

Table 2.

Stem lengths of tomato cultivar Beefsteak at 12 d and 32 d.

Table 2.
Table 3.

Effect of silicon on the stem lengths of ‘Beefsteak’ (BS), ‘Brandywine Red’ (BWR), ‘Early Girl’ (EG), ‘German Pink’ (GP), Heinz ‘H1015’ (early) and ‘H3406’ (late), ‘Mega Bite’ (MB), ‘Micro Tom’ (MT), ‘Old German’ (OG), and ‘Sweet ‘N Neat’ (SNN).

Table 3.

The Si treatment had a positive effect on plant fresh weight and dry weight, with the exception of the petiole dry weight (Table 4). Overall, more Si-treated plants than control-treated plants had increased weight. Specifically, ‘Beefsteak’, ‘German Pink’, ‘H1015’, ‘H3406’, and ‘Mega Bite’ had increased dry root weights with Si treatment compared with those of controls. ‘Beefsteak’ and ‘German Pink’ with Si treatment had significantly higher dry weights of all the tissue tested, whereas ‘H3406’ had additional increases in the dry mass of leaves, roots, and stems, but not petioles, and ‘H1015’ Si-treated plants had higher stem weights than the controls.

Table 4.

Effects of silicon on fresh and dry weights of ‘Beefsteak’ (BS), ‘Brandywine Red’ (BWR), ‘Early Girl’ (EG), ‘German Pink’ (GP), Heinz ‘H1015’ (early) and ‘H3406’ (late), ‘Mega Bite’ (MB), ‘Micro Tom’ (MT), ‘Old German’ (OG) and ‘Sweet ‘N Neat’ (SNN).

Table 4.

The Si concentrations were significantly higher in all Si-treated plant tissue, compared to controls (Table 5). The highest Si concentrations were in the roots (range, 0.05% to 4.3% Si), followed by the leaves (0.06% to 3.7% Si), petioles (0.01% to 0.03% Si), and stems (0.009% to 0.02% Si). Based on the leaf Si concentrations, H1015, H3406, and heirloom cultivars had higher concentrations of Si, with ‘Beefsteak’, ‘Early Girl’, ‘Micro Tom’, and ‘Sweet ‘N Neat’ having the lowest Si concentrations. Most interestingly, control plants still had concentrations of more than 35 ppm Si in root tissue, even with no inclusion of Si in the growing media. Many of the cultivars grown in these conditions had no detectable levels of Si in stems and petioles, and a few, including ‘German Pink’, ‘H3406’, and ‘Sweet ‘N Neat’, had no detectable levels within the leaves.

Table 5.

Effect of silicon (Si) treatment on Si concentrations in leaves, roots, stems, and petioles of tomatoes.

Table 5.

Concentrations of macronutrients in the plants were more affected by the cultivar than by the Si treatment. In leaves, carbon (C), nitrogen (N), phosphorus (P), calcium (Ca), and magnesium (Mg) were not significantly different based on their treatment and cultivar (Table 6). The potassium (K) and sulfur (S) levels in leaves were significantly lower in Si-fed plants of five and seven of the 10 cultivars tested, respectively, compared with controls. Scattered throughout the data were individual Si-fed cultivars that were different from controls. For instance, the Ca level was higher in Si-fed ‘Brandywine Red’ and ‘German Pink’ than in controls, and the C level was higher in leaves of the Heinz cultivar and ‘Mega Bite’ Si-fed plants than in those of controls. In roots, there was no significant interaction for Si treatment and cultivar for N, P, Ca, Mg, and S, but differences were observed for C and K. ‘Early Girl’, ‘German Pink’, ‘H1015’, and ‘H3406’ had lower C concentrations in the roots of Si-fed plants compared to controls. ‘Early Girl’, ‘German Pink’, ‘H3406’, and ‘Mega Bite’ also had lower N in the root tissue of Si-fed plants compared to controls. The K levels were higher and lower in roots of Si-fed plants of ‘Early Girl’ and ‘H3406’, respectively.

Table 6.

Effects of silicon (Si) treatment on macronutrient concentrations in leaves and roots of ‘Beefsteak’ (BS), ‘Brandywine Red’ (BWR), ‘Early Girl’ (EG), ‘German Pink’ (GP), Heinz ‘H1015’ (early) and ‘H3406’ (late), ‘Mega Bite’ (MB), ‘Micro Tom’ (MT), ‘Old German’ (OG), and ‘Sweet ‘N Neat’ (SNN).

Table 6.

There were slight differences in macronutrient concentrations in the stems and petioles, with the petioles showing more differences with the Si treatment than with the control treatment (Table 7). Compared with the stem, the petioles showed stronger differences in nitrogen based on the treatment, cultivar, and the combination of cultivar and treatment. Both stems and petioles showed decreased N concentrations in Si-fed plants similar to those in the leaves and roots. Similar to roots and leaves, S levels were also significantly lower in the stems and petioles of five and six of the 10 plants, respectively. ‘German Pink’ and ‘Sweet ‘N Neat’ only showed significantly lower S levels in the petioles of Si-fed plants, but not in the leaves, roots, or stems. The Ca and Mg levels were slightly higher in Si-fed plants than in control plants. There was no significant difference in P concentrations in stems and petioles, and the C level was significantly higher in ‘Mega Bite’ petioles only.

Table 7.

Effects of silicon (Si) treatment on macronutrient concentrations in stems and petioles of ‘Beefsteak’ (BS), ‘Brandywine Red’ (BWR), ‘Early Girl’ (EG), ‘German Pink’ (GP), Heinz ‘H1015’ (early) and ‘H3406’ (late), ‘Mega Bite’ (MB), ‘Micro Tom’ (MT), ‘Old German’ (OG), and ‘Sweet ‘N Neat’ (SNN).

Table 7.

Most of the micronutrients were unaffected by Si treatment. In the leaves and roots, manganese (Mn) levels were lower in Si-fed plants compared with control plants (Table 8). In roots only, the boron (B) level was slightly higher, but the iron (Fe) and zinc (Zn) levels were slightly lower in Si-fed plants than in controls. In stems, the Zn levels were lower in all Si-fed plants except ‘Micro Tom’, which had a higher level, compared to control plants (Table 9). There were no other significant differences in micronutrient concentrations within the stems and petioles, except for a decrease in Mn in ‘German Pink’ stems and an increase in Mn in ‘Old German’ petioles.

Table 8.

Effects of silicon (Si) treatment on micronutrient concentrations in leaves and roots of ‘Beefsteak’ (BS), ‘Brandywine Red’ (BWR), ‘Early Girl’ (EG), ‘German Pink’ (GP), Heinz ‘H1015’ (early) and ‘H3406’ (late), ‘Mega Bite’ (MB), ‘Micro Tom’ (MT), ‘Old German’ (OG), and ‘Sweet ‘N Neat’ (SNN).

Table 8.
Table 9.

Effect of silicon treatment on micronutrient concentrations in stems and petioles of tomato cultivars ‘Beefsteak’ (BS), ‘Brandywine Red’ (BWR), ‘Early Girl’ (EG), ‘German Pink’ (GP), Heinz ‘H1015’ (early) and ‘H3406’ (late), ‘Mega Bite’ (MB), ‘Micro Tom’ (MT), ‘Old German’ (OG), and ‘Sweet ‘N Neat’ (SNN).

Table 9.

Discussion

Silicon supplementation produces differences in phenotypic observations, such as chlorophyll content, plant height, stem thickness/diameter, and tissue mass (Frazao et al., 2020; Kamenidou et al., 2008; Mattson and Leatherwood, 2010; Silva et al., 2012; Song et al., 2014). During this study, we observed that ‘Beefsteak’ had longer stem lengths and a larger sd after Si treatment than after control treatment. However, differences in plant height were not observed for any of the other cultivars tested. This could suggest that plant growth of this cultivar was an indirect response to Si treatment. Other environmental or genetic factors, in addition to Si, may have been responsible for phenotypic changes observed during other studies.

Tomatoes are known to accumulate lower foliar concentrations of Si compared with grains and other dicots, such as cucumber, sunflower, and zinnia (Frantz et al., 2010; Hodson et al., 2005). Previous studies showed similar Si concentrations in roots and leaves of the tomato cultivar ‘King Kong II’ (Heine et al., 2005). During this study, the highest Si concentrations were observed in the roots of Si-fed plants; their levels exceeded the macronutrient concentrations in many of the cultivars. Root Si concentrations were higher than leaf Si concentrations in all cultivars except for ‘Micro Tom’. During the study involving ‘King Kong II’, plants were grown for less than 2 weeks in 1.0 mm Si; however, during this study, plants were grown for 4 to 8 weeks with 2.0 mm Si, thereby allowing more time for more accumulation in plant tissue. The high concentration of Si in roots compared with that in leaves suggests that tomatoes restrict the movement of Si into aboveground tissue of some cultivars. However, this restriction does not suggest exclusion because the Si concentrations in leaves were higher than the Fe concentrations (Tables 48). These data showed that tomato plants accumulate Si and partition the element into different organs, with roots and leaves appearing as Si sinks. Unlike other nutrients amended in excess, there were no observable toxicity symptoms in the plants as the Si levels significantly increased. This suggests that the plants likely have cellular mechanisms for movement and use in root and leaf tissues.

The Si concentrations in petioles were significantly higher than those in stems, possibly suggesting that this tissue is a larger sink for the nutrient as it moves into the leaves. Both tissues, however, had small fractions of total Si compared with roots and shoots. Because sap analyses using petiole tissue are becoming more frequent for nutrient analysis, the quantification technique needs to be sensitive enough to detect Si in these ranges.

Interestingly, Si concentrations in tissue varied widely with cultivar. ‘Micro Tom’ had the lowest Si concentrations when compared with the other nine varieties in this study, and it had a higher concentration in leaves than in roots, which was opposite of what was observed for the other species tested. This cultivar is a small, determinate plant that has been used for genomic information. This could suggest that different uptake/partitioning strategies for this plant are involved, and that the use of ‘Micro Tom’, in contrast to Heinz, may provide insight regarding Si regulation. Additionally, Heinz and heirloom cultivars accumulated the highest concentration of Si within tissue. This suggests that they have a larger draw on the silicic acid pool in the media and would require a higher dose of Si in the growing media.

The first criterion for nutrient essentiality in plants states that in the absence of the nutrient or element in question, a plant cannot complete its lifecycle (Arnon and Stout, 1939). Previous studies reported the use of copper stills to produce mineral-free water. During this study, ultra-purified water was used with laboratory-grade chemicals, but there were still detectable concentrations of Si in the roots. The source of Si contamination in this study was unknown. This exemplifies the problem of testing Si essentiality in plants using criteria developed in 1939, requiring that the nutrient be absent from the growing media (Arnon and Stout, 1939). Epstein and Bloom (2005) recognized this limitation and revised the criterion stating that a nutrient is essential if depletion of the element in question from the growing media leads to reduced plant performance. It may be time to reconsider that the essentiality of Si in plants is strongly supported by this adapted definition when considering the role of this element in plant health.

There were few differences in the nutrient compositions of the tomato cultivars between Si-fed and control plants. Differences in K and S concentrations were not too surprising because control plants were fed with K2SO4 to provide equal concentrations of K in the growing media, and this difference was more likely caused by the nutrient solution than by a direct effect of Si absorption by the plant. The amount of nutrients provided in the hydroponics system, including Si, were supplied at a rate at which no nutrient would be limiting to the growth of the plants. This is likely why only slight differences were observed for a few of the nutrients of Si-fed and control plants.

This is not the first study to show differences in Si accumulation among different cultivars. Several studies of rice have shown distinct differences in Si accumulation in different cultivars (Deren et al., 1992; Ma et al., 1992). Arsenault-Labrecque et al. (2012) reported that Si concentrations ranged from 0.4% to 1.3% in different soybean cultivars. Most recently, reports of varying Si contents in eight petunia cultivars were reported (Boldt and Altland, 2021). It is likely that as more plant cultivars are tested, this list will continue to grow.

Because of our knowledge of the benefits of Si against stress and the high demand that is placed on tomato plants during hydroponic production, the incorporation of Si into fertilizer programs is warranted. During this study, a high Si concentration was incorporated in a deep-water hydroponic system. Based on these data, it could be suggested that a higher concentration of Si is needed when growing certain heirlooms than when growing hybrids and determinates. A few studies have examined the effects of Si on hydroponic tomato production. Costan et al. (2020) showed an increase in fruit firmness and vitamin C content. Foliar sprays comprising a combination of Si and B increased the shelf life, vitamin C, and firmness of tomato fruit (Islam et al., 2018). Barreto et al. (2016) showed that Si in hydroponic tomato production can also protect against ammonium toxicity. During hydroponic production, fertilization programs tend to be closely monitored, but research regarding how Si may alter the balance of other nutrients is lacking.

During this study, ample amounts of essential nutrients, including Si, were provided so that no nutrient was limiting to the growth of the 10 tomato cultivars. To understand the role of Si in a balanced nutrient plan for tomatoes, further studies of the effects or interactions of varying Si concentrations and low or limiting amounts of other nutrients, including N, P, and Ca, should be performed. In conclusion, tomatoes accumulate Si at macronutrient concentrations in leaves and do not exclude Si from the media; however, the movement of Si into foliar tissue is restricted when it and other nutrients are supplied in significant ranges.

Literature Cited

  • Ali, N., Schwarzenberg, A., Yvin, J.C. & Hosseini, S.A. 2018 Regulatory role of silicon in mediating differential stress tolerance responses in two contrasting tomato genotypes under osmotic stress Front. Plant Sci. 9 1475 doi: https://doi.org/10.3389/fpls.2018.01475

    • Search Google Scholar
    • Export Citation
  • Andrade, C.C.L., Resende, R.S., Rodrigues, F.A., Ferraz, H.G.M., Moreira, W.R., Oliveira, J.R. & Mariano, R.L.R. 2013 Silicon reduces bacterial speck development on tomato leaves Trop. Plant Pathol. 38 436 442 doi: https://doi.org/10.1590/S1982-56762013005000021

    • Search Google Scholar
    • Export Citation
  • Arnon, D.I. & Stout, P.R. 1939 The essentiality of certain elements in minute quantity for plants with special reference to copper Plant Physiol. 14 371 375 doi: https://doi.org/10.1104/pp.14.2.371

    • Search Google Scholar
    • Export Citation
  • Arsenault-Labrecque, G., Menzies, J.G. & Belanger, R.R. 2012 Effect of silicon absorption on soybean resistance to Phakopsora pachyrhizi in different cultivars Plant Dis. 96 37 42 doi: https://doi.org/10.1094/PDIS-05-11-0376

    • Search Google Scholar
    • Export Citation
  • Barreto, R.F., Prado, R.M., Leal, A.J.F., Troleis, M.J.B., Silva, G.B. Jr., Monteiro, C.C., Santos, L.C.N. & Carvalho, R.F. 2016 Mitigation of ammonium toxicity by silicon in tomato depends on the ammonium concentration Acta Agr. Schandinavica, Section B. 66 483 488 doi: https://doi.org/10.1080/09064710.2016.1178324

    • Search Google Scholar
    • Export Citation
  • Boldt, J.K. & Altland, J.E. 2021 Petunia (Petunia x hybrida) cultivars vary in silicon accumulation and distribution HortScience 56 305 312 doi: https://doi.org/10.21273/HORTSCI15486-20

    • Search Google Scholar
    • Export Citation
  • Bryson, G.M., Mills, H.A., Sasseville, D.N., Jones, J.B. & Barker, A.V. 2014 Plant analysis handbook III: A guide to sampling, preparation, analysis and interpretation for agronomic and horticultural crops C. Micro Macro Publishing Athens, GA

    • Export Citation
  • Costan, A., Stamatakis, A., Chrysargyris, A., Petropoulos, S.A. & Tzortzakis, N. 2020 Interactive effects of salinity and silicon application of Solanum lycopersicum growth, physiology and shelf-life of fruit produced hydroponically J. Sci. Food Agr. 100 723 743 doi: https://doi.org/10.1002/jsfa.10076

    • Search Google Scholar
    • Export Citation
  • Dannon, E.A. & Wydra, K. 2004 Interaction between silicon amendment, bacterial wilt development and phenotype of Ralstonia solanacearum in tomato genotypes Physiol. Mol. Plant Pathol. 64 233 243 doi: https://doi.org/10.1016/j.pmpp.2004.09.006

    • Search Google Scholar
    • Export Citation
  • Deren, C.W., Datnoff, L.E. & Snyder, G.H. 1992 Variable silicon content of rice cultivars grown on everglades histosols J. Plant Nutr. 15 2363 2368 doi: https://doi.org/10.1080/01904169209364480

    • Search Google Scholar
    • Export Citation
  • Epstein, E. & Bloom, A.J. 2005 Mineral metabolism 227 231 Mineral nutrition of plants: Principles and perspectives 2nd ed Sinaeur Associates Inc. Sunderland, MA

    • Search Google Scholar
    • Export Citation
  • Frantz, J.M., Pitchay, D.D.S., Locke, J.C., Horst, L.E. & Krause, C.R. 2005 Silicon is deposited in leaves of New Guinea impatiens Plant Health Prog. doi: https://doi.org/10.1094/PHP-2005-0217-01-RS

    • Search Google Scholar
    • Export Citation
  • Frantz, J.M., Locke, J.C., Datnoff, L., Omer, M., Widrig, A., Sturtz, D., Horst, L. & Krause, C.R. 2008 Detection, distribution and quantification of silicon in floricultural crops utilizing three distinct analytical methods Commun. Soil Sci. Plant Anal. 39 2734 2751 doi: https://doi.org/10.1080/00103620802358912

    • Search Google Scholar
    • Export Citation
  • Frantz, J.M., Locke, J.C., Sturtz, D. & Leisner, S. 2010 Silicon in ornamental crops: Detection, delivery, and function 111 134 Rodrigues, F.A. Silicio na agricultura: Anais do V simposio brasileiro sobre silicio na agricultura. Universidade Federal de Vicosa Vicosa, BR

    • Search Google Scholar
    • Export Citation
  • Frantz, J.M., Khandekar, S. & Leisner, S. 2011 Silicon differentially influences copper toxicity response in silicon-accumulator and non-accumulator species J. Amer. Soc. Hort. Sci. 136 329 338 doi: https://doi.org/10.21273/JASHS.136.5.329

    • Search Google Scholar
    • Export Citation
  • Frazao, J.J., Prado, R.M., Souza, J.P. & Rossatto, D.R. 2020 Silicon changes C:N:P stoichiometry of sugarcane and its consequences for photosynthesis, biomass partitioning and plant growth Scientific Rpt. 10 12492 doi: https://doi.org/10.1038/s41598-020-69310-6

    • Search Google Scholar
    • Export Citation
  • Garibaldi, A., Gilardi, G. & Gullino, M.L. 2011 Effect of potassium silicate and electrical conductivity in reducing powdery mildew of hydroponically grown tomato Phytopathol. Mediterr. 50 192 202

    • Search Google Scholar
    • Export Citation
  • Heine, G., Tikum, G. & Horst, W.J. 2005 Silicon nutrition of tomato and bitter gourd with special emphasis on silicon distribution in root fractions J. Plant Nutr. Soil Sci. 168 600 606 doi: https://doi.org/10.1002/jpln.200420508

    • Search Google Scholar
    • Export Citation
  • Heine, G.G., Tikum, G. & Horst, W.J. 2006 The effect of silicon on the infection by and spread of Pythium aphanidermatum in single roots of tomato and bitter gourd J. Expt. Bot. 58 569 577

    • Search Google Scholar
    • Export Citation
  • Hodson, M.J., White, P.J., Mead, A. & Broadley, M.R. 2005 Phylogenetic variation in the silicon composition of plants Ann. Bot. 96 1027 1046 doi: https://doi.org/10.1093/aob/mci255

    • Search Google Scholar
    • Export Citation
  • Huang, C.H., Roberts, P.D. & Datnoff, L.E. 2011 Silicon suppresses fusarium crown and root rot of tomato J. Phytopathol. 159 546 554 doi: https://doi.org/10.1111/j.1439-0434.2011.01803.x

    • Search Google Scholar
    • Export Citation
  • Islam, M.Z., Mele, M.A., Choi, K.Y. & Kang, H.M. 2018 The effect of silicon and boron foliar application on the quality and shelf life of cherry tomatoes Zemdirbyste-Agr. 105 159 164 doi: https://doi.org/10.13080/z-a.2018.105.020

    • Search Google Scholar
    • Export Citation
  • Jarosz, Z. 2014 The effect of silicon application and type of medium on yielding and chemical composition of tomato Acta Sci. Pol. Hortorum Cultus 13 171 183

    • Search Google Scholar
    • Export Citation
  • Kamenidou, S., Cavins, T.J. & Marek, S. 2008 Silicon supplements affect horticultural traits of greenhouse-produced ornamental sunflowers HortScience 43 236 239 doi: https://doi.org/10.21273/HORTSCI.43.1.236

    • Search Google Scholar
    • Export Citation
  • Kirrika, L.M., Stahl, F. & Wydra, K. 2013 Phenotypic and molecular characterization of resistance induction by single and combined application of chitosan and silicon in tomato against Ralstonia solanacearum Physiol. Mol. Plant Pathol. 81 1 12 doi: https://doi.org/10.1016/j.pmpp.2012.11.002

    • Search Google Scholar
    • Export Citation
  • Li, H., Zhu, Y., Hu, Y., Han, W. & Gong, H. 2015 Beneficial effects of silicon in alleviating salinity stress of tomato seedlings grown under sand culture Acta Physiol. Plant. 37 71 doi: https://doi.org/10.1007/s11738-015-1818-7

    • Search Google Scholar
    • Export Citation
  • Li, J., Leisner, S. & Frantz, J. 2008 Alleviation of copper toxicity in Arabidopsis thaliana by silicon addition to hydroponic solutions J. Amer. Soc. Hort. Sci. 133 670 677 doi: https://doi.org/10.21273/JASHS.133.5.670

    • Search Google Scholar
    • Export Citation
  • Ma, J.F., Yamaji, Y.N., Tamai, K. & Mitani, N. 1992 Genotypic difference in silicon uptake and expression of silicon transporter genes in rice Plant Physiol. 145 919 924 doi: https://doi.org/10.1104/pp.107.107599

    • Search Google Scholar
    • Export Citation
  • Marodin, J.C., Resende, J.T.V., Morales, R.F.G., Silva, M.L.S., Galvao, A.G. & Zanin, D.S. 2014 Yield of tomato fruits in relation to silicon sources and rates Hort. Brasileria 32 220 224 doi: https://doi.org/10.1590/S0102-05362014000200018

    • Search Google Scholar
    • Export Citation
  • Mattson, N.S. & Leatherwood, W.R. 2010 Potassium silicate drenches increase leaf silicon content and affect morphological traits of several floriculture crops grown in a peat-based substrate HortScience 45 43 47 doi: https://doi.org/10.21273/HORTSCI.45.1.43

    • Search Google Scholar
    • Export Citation
  • Mitani, N. & Ma, J.F. 2005 Uptake system of silicon in different plant species J. Expt. Bot. 56 1255 1261 doi: https://doi.org/10.1093/jxb/eri121

  • Miyake, Y. & Takahashi, E. 1978 Silicon deficiency of tomato plant Soil Sci. Plant Nutr. 24 175 189 doi: https://doi.org/10.1080/00380768.1978.10433094

    • Search Google Scholar
    • Export Citation
  • R Core Team 2016 R: A language and environment for statistical computing R Foundation for Statistical Computing Vienna, Austria

    • Export Citation
  • Romero-Aranda, M.R., Jurado, O. & Cuartero, J. 2006 Silicon alleviates the deleterious salt effect on tomato plant growth by improving plant water status J. Plant Physiol. 163 847 855 doi: https://doi.org/10.1016/j.jplph.2005.05.010

    • Search Google Scholar
    • Export Citation
  • Shi, Y., Zhang, Y., Han, W., Feng, R., Hu, Y., Guo, J. & Gong, H. 2016 Silicon enhances water stress tolerance by improving root hydraulic conductance in Solanum lycopersicum L Frontiers Plant Sci. 7 196 doi: https://doi.org/10.3389/fpls.2016.00196

    • Search Google Scholar
    • Export Citation
  • Silva, O.N., Lobato, A.K.S., Avila, F.W., Costa, R.C.L., Neto, C.F.O., Filho, B.G.S., Filho, A.P.M., Lemos, R.P., Pinho, J.M., Medeiros, M.B.C.L., Cardoso, M.S. & Andrade, I.P. 2012 Silicon-induced increase in chlorophyll is modulated by leaf water potential in two water-deficient tomato cultivars Plant Soil Environ. 58 481 486 doi: https://doi.org/10.17221/213/2012-PSE

    • Search Google Scholar
    • Export Citation
  • Song, A., Li, P., Fan, F., Li, Z. & Liang, Y. 2014 The effect of silicon on photosynthesis and expression of its relevant genes in rice (Oryza sativa L.) under high-zinc stress PLoS One 9 e113782 doi: https://doi.org/10.1371/journal.pone.0113782

    • Search Google Scholar
    • Export Citation
  • Stamatakis, A., Papadantonakis, N., Savvas, D., Lydakis-Simantiris, N. & Kefalas, P. 2003 Effects of silicon and salinity on fruit yield and quality of tomato grown hydroponically Acta Hort. 609 141 147 doi: https://doi.org/10.17660/ActaHortic.2003.609.18

    • Search Google Scholar
    • Export Citation
  • Takahashi, E. & Miyake, Y. 1977 Silica and plant growth Proc. Intl. Semin. Soil Environ. Fert. Mgt. Intens. Agr. 603 611

  • Takahashi, E., Ma, J.F. & Miyake, Y. 1990 The possibility of silicon as an essential element for higher plants Commun. Agr. Food Chem. 2 99 102

  • Zellner, W., Tubana, B., Rodrigues, R.A. & Datnoff, L.E. 2021 Silicon’s role in plant stress reduction and why this element is not used routinely for managing plant health Plant Dis. (In press) doi: https://doi.org/10.1094/PDIS-08-20-1797-FE

    • Search Google Scholar
    • Export Citation
  • Zhang, Y., Shi, Y., Gong, H., Zhao, H., Li, H., Hu, Y. & Wang, Y. 2018 Beneficial effects of silicon on photosynthesis of tomato seedlings under water stress J. Integr. Agr. 17 2151 2159 doi: https://doi.org/10.1016/S2095-3119(18)62038-6

    • Search Google Scholar
    • Export Citation

If the inline PDF is not rendering correctly, you can download the PDF file here.

Contributor Notes

I acknowledge the work of the U.S. Department of Agriculture-Agricultural Research Service (USDA-ARS) Greenhouse Production Research technicians Douglas Sturtz and Monalisa Banks, who helped with the inductively coupled plasma optical emission spectroscopy analysis, as well as that of Dr. Lindy Lutz and Dr. Sushant Khandekar, who reviewed of the manuscript before submission. Funding for this research was provided by grants from the USDA-ARS and Plant Tuff, Dearborn, MI.

W.L.Z. is the corresponding author. E-mail: wendy.reiner@utoledo.edu.

  • Ali, N., Schwarzenberg, A., Yvin, J.C. & Hosseini, S.A. 2018 Regulatory role of silicon in mediating differential stress tolerance responses in two contrasting tomato genotypes under osmotic stress Front. Plant Sci. 9 1475 doi: https://doi.org/10.3389/fpls.2018.01475

    • Search Google Scholar
    • Export Citation
  • Andrade, C.C.L., Resende, R.S., Rodrigues, F.A., Ferraz, H.G.M., Moreira, W.R., Oliveira, J.R. & Mariano, R.L.R. 2013 Silicon reduces bacterial speck development on tomato leaves Trop. Plant Pathol. 38 436 442 doi: https://doi.org/10.1590/S1982-56762013005000021

    • Search Google Scholar
    • Export Citation
  • Arnon, D.I. & Stout, P.R. 1939 The essentiality of certain elements in minute quantity for plants with special reference to copper Plant Physiol. 14 371 375 doi: https://doi.org/10.1104/pp.14.2.371

    • Search Google Scholar
    • Export Citation
  • Arsenault-Labrecque, G., Menzies, J.G. & Belanger, R.R. 2012 Effect of silicon absorption on soybean resistance to Phakopsora pachyrhizi in different cultivars Plant Dis. 96 37 42 doi: https://doi.org/10.1094/PDIS-05-11-0376

    • Search Google Scholar
    • Export Citation
  • Barreto, R.F., Prado, R.M., Leal, A.J.F., Troleis, M.J.B., Silva, G.B. Jr., Monteiro, C.C., Santos, L.C.N. & Carvalho, R.F. 2016 Mitigation of ammonium toxicity by silicon in tomato depends on the ammonium concentration Acta Agr. Schandinavica, Section B. 66 483 488 doi: https://doi.org/10.1080/09064710.2016.1178324

    • Search Google Scholar
    • Export Citation
  • Boldt, J.K. & Altland, J.E. 2021 Petunia (Petunia x hybrida) cultivars vary in silicon accumulation and distribution HortScience 56 305 312 doi: https://doi.org/10.21273/HORTSCI15486-20

    • Search Google Scholar
    • Export Citation
  • Bryson, G.M., Mills, H.A., Sasseville, D.N., Jones, J.B. & Barker, A.V. 2014 Plant analysis handbook III: A guide to sampling, preparation, analysis and interpretation for agronomic and horticultural crops C. Micro Macro Publishing Athens, GA

    • Export Citation
  • Costan, A., Stamatakis, A., Chrysargyris, A., Petropoulos, S.A. & Tzortzakis, N. 2020 Interactive effects of salinity and silicon application of Solanum lycopersicum growth, physiology and shelf-life of fruit produced hydroponically J. Sci. Food Agr. 100 723 743 doi: https://doi.org/10.1002/jsfa.10076

    • Search Google Scholar
    • Export Citation
  • Dannon, E.A. & Wydra, K. 2004 Interaction between silicon amendment, bacterial wilt development and phenotype of Ralstonia solanacearum in tomato genotypes Physiol. Mol. Plant Pathol. 64 233 243 doi: https://doi.org/10.1016/j.pmpp.2004.09.006

    • Search Google Scholar
    • Export Citation
  • Deren, C.W., Datnoff, L.E. & Snyder, G.H. 1992 Variable silicon content of rice cultivars grown on everglades histosols J. Plant Nutr. 15 2363 2368 doi: https://doi.org/10.1080/01904169209364480

    • Search Google Scholar
    • Export Citation
  • Epstein, E. & Bloom, A.J. 2005 Mineral metabolism 227 231 Mineral nutrition of plants: Principles and perspectives 2nd ed Sinaeur Associates Inc. Sunderland, MA

    • Search Google Scholar
    • Export Citation
  • Frantz, J.M., Pitchay, D.D.S., Locke, J.C., Horst, L.E. & Krause, C.R. 2005 Silicon is deposited in leaves of New Guinea impatiens Plant Health Prog. doi: https://doi.org/10.1094/PHP-2005-0217-01-RS

    • Search Google Scholar
    • Export Citation
  • Frantz, J.M., Locke, J.C., Datnoff, L., Omer, M., Widrig, A., Sturtz, D., Horst, L. & Krause, C.R. 2008 Detection, distribution and quantification of silicon in floricultural crops utilizing three distinct analytical methods Commun. Soil Sci. Plant Anal. 39 2734 2751 doi: https://doi.org/10.1080/00103620802358912

    • Search Google Scholar
    • Export Citation
  • Frantz, J.M., Locke, J.C., Sturtz, D. & Leisner, S. 2010 Silicon in ornamental crops: Detection, delivery, and function 111 134 Rodrigues, F.A. Silicio na agricultura: Anais do V simposio brasileiro sobre silicio na agricultura. Universidade Federal de Vicosa Vicosa, BR

    • Search Google Scholar
    • Export Citation
  • Frantz, J.M., Khandekar, S. & Leisner, S. 2011 Silicon differentially influences copper toxicity response in silicon-accumulator and non-accumulator species J. Amer. Soc. Hort. Sci. 136 329 338 doi: https://doi.org/10.21273/JASHS.136.5.329

    • Search Google Scholar
    • Export Citation
  • Frazao, J.J., Prado, R.M., Souza, J.P. & Rossatto, D.R. 2020 Silicon changes C:N:P stoichiometry of sugarcane and its consequences for photosynthesis, biomass partitioning and plant growth Scientific Rpt. 10 12492 doi: https://doi.org/10.1038/s41598-020-69310-6

    • Search Google Scholar
    • Export Citation
  • Garibaldi, A., Gilardi, G. & Gullino, M.L. 2011 Effect of potassium silicate and electrical conductivity in reducing powdery mildew of hydroponically grown tomato Phytopathol. Mediterr. 50 192 202

    • Search Google Scholar
    • Export Citation
  • Heine, G., Tikum, G. & Horst, W.J. 2005 Silicon nutrition of tomato and bitter gourd with special emphasis on silicon distribution in root fractions J. Plant Nutr. Soil Sci. 168 600 606 doi: https://doi.org/10.1002/jpln.200420508

    • Search Google Scholar
    • Export Citation
  • Heine, G.G., Tikum, G. & Horst, W.J. 2006 The effect of silicon on the infection by and spread of Pythium aphanidermatum in single roots of tomato and bitter gourd J. Expt. Bot. 58 569 577

    • Search Google Scholar
    • Export Citation
  • Hodson, M.J., White, P.J., Mead, A. & Broadley, M.R. 2005 Phylogenetic variation in the silicon composition of plants Ann. Bot. 96 1027 1046 doi: https://doi.org/10.1093/aob/mci255

    • Search Google Scholar
    • Export Citation
  • Huang, C.H., Roberts, P.D. & Datnoff, L.E. 2011 Silicon suppresses fusarium crown and root rot of tomato J. Phytopathol. 159 546 554 doi: https://doi.org/10.1111/j.1439-0434.2011.01803.x

    • Search Google Scholar
    • Export Citation
  • Islam, M.Z., Mele, M.A., Choi, K.Y. & Kang, H.M. 2018 The effect of silicon and boron foliar application on the quality and shelf life of cherry tomatoes Zemdirbyste-Agr. 105 159 164 doi: https://doi.org/10.13080/z-a.2018.105.020

    • Search Google Scholar
    • Export Citation
  • Jarosz, Z. 2014 The effect of silicon application and type of medium on yielding and chemical composition of tomato Acta Sci. Pol. Hortorum Cultus 13 171 183

    • Search Google Scholar
    • Export Citation
  • Kamenidou, S., Cavins, T.J. & Marek, S. 2008 Silicon supplements affect horticultural traits of greenhouse-produced ornamental sunflowers HortScience 43 236 239 doi: https://doi.org/10.21273/HORTSCI.43.1.236

    • Search Google Scholar
    • Export Citation
  • Kirrika, L.M., Stahl, F. & Wydra, K. 2013 Phenotypic and molecular characterization of resistance induction by single and combined application of chitosan and silicon in tomato against Ralstonia solanacearum Physiol. Mol. Plant Pathol. 81 1 12 doi: https://doi.org/10.1016/j.pmpp.2012.11.002

    • Search Google Scholar
    • Export Citation
  • Li, H., Zhu, Y., Hu, Y., Han, W. & Gong, H. 2015 Beneficial effects of silicon in alleviating salinity stress of tomato seedlings grown under sand culture Acta Physiol. Plant. 37 71 doi: https://doi.org/10.1007/s11738-015-1818-7

    • Search Google Scholar
    • Export Citation
  • Li, J., Leisner, S. & Frantz, J. 2008 Alleviation of copper toxicity in Arabidopsis thaliana by silicon addition to hydroponic solutions J. Amer. Soc. Hort. Sci. 133 670 677 doi: https://doi.org/10.21273/JASHS.133.5.670

    • Search Google Scholar
    • Export Citation
  • Ma, J.F., Yamaji, Y.N., Tamai, K. & Mitani, N. 1992 Genotypic difference in silicon uptake and expression of silicon transporter genes in rice Plant Physiol. 145 919 924 doi: https://doi.org/10.1104/pp.107.107599

    • Search Google Scholar
    • Export Citation
  • Marodin, J.C., Resende, J.T.V., Morales, R.F.G., Silva, M.L.S., Galvao, A.G. & Zanin, D.S. 2014 Yield of tomato fruits in relation to silicon sources and rates Hort. Brasileria 32 220 224 doi: https://doi.org/10.1590/S0102-05362014000200018

    • Search Google Scholar
    • Export Citation
  • Mattson, N.S. & Leatherwood, W.R. 2010 Potassium silicate drenches increase leaf silicon content and affect morphological traits of several floriculture crops grown in a peat-based substrate HortScience 45 43 47 doi: https://doi.org/10.21273/HORTSCI.45.1.43

    • Search Google Scholar
    • Export Citation
  • Mitani, N. & Ma, J.F. 2005 Uptake system of silicon in different plant species J. Expt. Bot. 56 1255 1261 doi: https://doi.org/10.1093/jxb/eri121

  • Miyake, Y. & Takahashi, E. 1978 Silicon deficiency of tomato plant Soil Sci. Plant Nutr. 24 175 189 doi: https://doi.org/10.1080/00380768.1978.10433094

    • Search Google Scholar
    • Export Citation
  • R Core Team 2016 R: A language and environment for statistical computing R Foundation for Statistical Computing Vienna, Austria

    • Export Citation
  • Romero-Aranda, M.R., Jurado, O. & Cuartero, J. 2006 Silicon alleviates the deleterious salt effect on tomato plant growth by improving plant water status J. Plant Physiol. 163 847 855 doi: https://doi.org/10.1016/j.jplph.2005.05.010

    • Search Google Scholar
    • Export Citation
  • Shi, Y., Zhang, Y., Han, W., Feng, R., Hu, Y., Guo, J. & Gong, H. 2016 Silicon enhances water stress tolerance by improving root hydraulic conductance in Solanum lycopersicum L Frontiers Plant Sci. 7 196 doi: https://doi.org/10.3389/fpls.2016.00196

    • Search Google Scholar
    • Export Citation
  • Silva, O.N., Lobato, A.K.S., Avila, F.W., Costa, R.C.L., Neto, C.F.O., Filho, B.G.S., Filho, A.P.M., Lemos, R.P., Pinho, J.M., Medeiros, M.B.C.L., Cardoso, M.S. & Andrade, I.P. 2012 Silicon-induced increase in chlorophyll is modulated by leaf water potential in two water-deficient tomato cultivars Plant Soil Environ. 58 481 486 doi: https://doi.org/10.17221/213/2012-PSE

    • Search Google Scholar
    • Export Citation
  • Song, A., Li, P., Fan, F., Li, Z. & Liang, Y. 2014 The effect of silicon on photosynthesis and expression of its relevant genes in rice (Oryza sativa L.) under high-zinc stress PLoS One 9 e113782 doi: https://doi.org/10.1371/journal.pone.0113782

    • Search Google Scholar
    • Export Citation
  • Stamatakis, A., Papadantonakis, N., Savvas, D., Lydakis-Simantiris, N. & Kefalas, P. 2003 Effects of silicon and salinity on fruit yield and quality of tomato grown hydroponically Acta Hort. 609 141 147 doi: https://doi.org/10.17660/ActaHortic.2003.609.18

    • Search Google Scholar
    • Export Citation
  • Takahashi, E. & Miyake, Y. 1977 Silica and plant growth Proc. Intl. Semin. Soil Environ. Fert. Mgt. Intens. Agr. 603 611

  • Takahashi, E., Ma, J.F. & Miyake, Y. 1990 The possibility of silicon as an essential element for higher plants Commun. Agr. Food Chem. 2 99 102

  • Zellner, W., Tubana, B., Rodrigues, R.A. & Datnoff, L.E. 2021 Silicon’s role in plant stress reduction and why this element is not used routinely for managing plant health Plant Dis. (In press) doi: https://doi.org/10.1094/PDIS-08-20-1797-FE

    • Search Google Scholar
    • Export Citation
  • Zhang, Y., Shi, Y., Gong, H., Zhao, H., Li, H., Hu, Y. & Wang, Y. 2018 Beneficial effects of silicon on photosynthesis of tomato seedlings under water stress J. Integr. Agr. 17 2151 2159 doi: https://doi.org/10.1016/S2095-3119(18)62038-6

    • Search Google Scholar
    • Export Citation
All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 60 60 60
PDF Downloads 26 26 26