Abstract
Soil pH not only plays a regulatory role in seed germination but also influences seedling development, flowering, and crop yield. The study investigated the germination characteristics of sorghum [Sorghum bicolor (L.) Moench.] under varying pH to understand the potential ameliorative effects of seed priming using plant growth-promoting substances. Seeds were sown in Petri dishes with pH moistened solutions at 1, 3, 5, 7, 9, 11, and 13 respectively. These were replicated five times in the second stage, viable seeds were first primed in 150 ppm indole-3-acetic acid, gibberellic acid, and vitamin C before sowing in pH solutions. The experiment showed no significant changes in morphology or physiology of primed and unprimed seeds and no germination at extreme pH. However, there was a significant difference in the activity of enzymes, germination time, and speed as well as germination percentages of both primed and unprimed seeds. Although chemo-priming did not reverse the effect of pH, it was observed however that vitamin C had a significant effect on germination percentage at higher pH. Germination was observed to be impaired at extreme pH. Seeds did not respond to germination capacity suggesting an optimal pH range of 3 and 11 for germination without priming. However, priming did not show any improved germinability index. Seeds primed in the presence of light showed enhanced germination at pH 7. Generally, the germination index without priming showed better germination characteristics than primed seeds, which suggests pH interactions with primers may be a limiting factor.
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Introduction
The nutritional composition of Sorghum bicolor (L.) Moench. (Poaceae) makes it a common staple food in many food-insecure countries. However, the growth of sorghum is regulated by environmental conditions like soil pH. pH (the level of alkalinity or acidity in the soil) has a critical role in seed germination and plant development (Yue et al. 2021). Plant responses to soil pH vary, as do their responses to all other environmental conditions. Some plants benefit from low pH (acidic soils), whereas others grow in higher pH (basic soil) environments (Ebrahimi and Eslamo 2012; Ikhajiagbe et al. 2021). Soil pH has been shown to greatly alter plant morphological features such as height, lateral spread, biomass, flower size, and even the number of flowers generated (Gentili et al. 2018). For example, S. bicolor has a low telorance of acidic soils due to high seed and seedling mortality, as well as reduced grain yield (Butchee et al. 2012). Some seeds, on the other hand, are unaffected by pH shifts, making them a very dominating plant that can grow practically anywhere regardless of soil pH profiles (Ebrahimi and Eslami 2012). It is worth noting that, even though soil pH has such a large influence on plant growth and development, crop responses to variable soil pH are not uniform (Yazdi et al. 2013; Ikhajiagbe et al. 2014, 2021).
Seed priming is a technique that promotes seed germination regardless of environmental conditions (Gebeyaw 2020). Hydropriming, osmopriming, chemical priming, halopriming, solid matrix priming, nutrient priming, vitamin C (ascorbate) priming, and hormone priming are some of the seed priming strategies that have been utilized under diverse environmental stresses (Rakshit and Singh 2018; Mamun et al. 2018; Rhaman et al. 2020). However, regardless of the priming method used, some other key physical and chemical components (osmotic potential, temperature, presence or absence of light, aeration, and seed condition) influence the priming process and determine the eventual germination rate and time, seedling vigour, and subsequent plant development (Rhaman et al. 2020; Musa et al. 2022). Farooq et al. (2013) showed that priming wheat seedlings with ascorbic acid can improve seedling emergence, growth, yield, and crop water status under low water stress.
In the same way, plant growth regulators play crucial functions in plants facing abiotic stress and demonstrate an appreciable ability to boost a plant’s adaptation to an unstable, ever-changing environment through the modulation of the plant’s growth, development, and nutrient use (Rakshit and Singh 2018; Musa et al. 2022). Plant growth hormones are produced in vivo by plants in negligible concentrations to regulate physiological and morphological processes in plants necessary for their survival (Mundiyara et al. 2020; Khan 2021; Opik et al. 2005). These plant growth regulators include both synthetic (salicylic acid, brassinosteroids, and jasmonates) and naturally occurring growth hormones (gibberellic acid (GA), abscisic acid, ethylene, auxins, and cytokinins (Rakshit and Singh 2018). They adjust the plant's response to the stressed plant's physiological and molecular reaction resulting in the plant's improved chance of survival. Auxins (for example indole-3-acetic acid [IAA]) is a plant growth hormone with multiple functions. It is unarguably a life-sustaining component of plants facing stress conditions (Kazan 2013; Mundiyara et al. 2020). Gibberellins stimulate the germination of seeds, cause leaf expansion, elongate stems, promote the development of fruits, and are important when plants are facing abiotic stresses as they improve their response and profitable adaptation (Yamaguchi 2008; Colebrook et al. 2014; Somorro et al. 2020). Gibberellins also work with other plant growth influencers in many processes involving response to stimuli (Munteanu et al. 2014). Ascorbic acid is the chief antioxidant present in plant cells. It supports other membrane-indentured antioxidants in its role as a cellular protector (Horemans et al. 2000; Nunes et al. 2020). A lot of research is currently being carried out on the benefits of vitamin C in the alleviation of biotic and abiotic stress. It has been observed that vitamin C promotes the germination, growth, and development of seedlings of plants such as potatoes, beans, sorghum and tomato (Zhang et al. 2015, 2019) even amid salinity and drought (Nunes et al. 2020).
The present study investigates the effects of varying pH levels on the germinability of sorghum. The study did also attempt to use chemo-priming to remediate the effects of pH by incorporating growth-promoting chemicals like indole-3-acetic acid, ascorbic acid and gibberellic acid. The study will provide supporting evidence of whether intermediate pH levels can promote germination and significant growth without priming.
Materials and method
Experimental area
The study was conducted in the Postgraduate laboratory, Mushroom building of the department of Plant biology and biotechnology, University of Benin, Benin City, Edo state. The experiment was carried in vitro in the laboratory for germination study.
Seed collection
The seeds of Sorghum bicolor were obtained and subjected to viability test. The viability of the seeds was ensured using the floatation viability seed testing described by Ogwu et al. (2014) and Daneshvar et al. (2017).
The experiment was divided into two stages. Number 42 Whatman filter paper was placed in different Petri dishes and soaked with 10 ml of different levels pH solution in preparation for the seeds. The experiment was then divided into two stages.
Stage 1 Germination study (no priming)
20 viable seeds were placed in the Petri dishes at replicates of five for each pH level without priming. Growth parameters were measured for 7 days of the germination study.
Stage 2 Germination study (with priming)
The viable seeds were initially primed in 10 ml of 150 ppm concentration of IAA, GA, ascorbic acid (Vitamin C), and water for one hour before being introduced into the Petri dishes.
Germination percentage
The number of germinants was recorded twice daily at 15 h intervals for phase 1 and 10 h intervals for phase 2 before being terminated after 7 days. The germination percentage is calculated as:
Seedling vigor
The seedling vigor was determined using the formula below:
where FGP (i.e., the final germination percentage) is the germination percentage attained by the plant. SVI (I) = Seedling length × FGP. SVI (II) = (Root length + Shoot length) × FGP. SVI (III) = Seedling dry weight × FGP.
Enzyme activity
The samples were homogenized with a phosphate buffer (PO32−) to maintain the optimal activity of the enzymes. The analytes were then centrifuged at 4000 rpm for 10 min and stored in 0 °C for 24 h.
Catalase
Catalase (CAT) activity was estimated by the method described by Cohen et al. (1970) using two reagents hydrogen peroxidase (H2O2) and sulphuric acid (6 M) H2SO4. 0.01 M KMnO4 was prepared by dissolving 0.158 g of KMnO4 in 100 ml of distilled water. Phosphate buffer (pH 7.4) 0.426 g of NaHPO4 and 0.240 g of NaH2PO4 was weighed and dissolved in 100 ml of distilled water. 6 M H2SO4 and 32.3 ml of concentrated H2SO4 were added to 66.7 ml of distilled water. To a known volume of plasma (0.5 ml), 5.0 ml of H2O2 was added. This was mixed by inversion and allowed to stand for 30 min. The reaction was stopped by adding 1.5 ml of 6 M H2SO4 and 7 ml of 0.01 M KMnO4. These were mixed by inversion and allowed to stand for 10 min. The absorbance was read at 480 nm within 30–60 s against distilled water. The enzyme blank was run simultaneously with 1.0 ml of distilled water instead of hydrogen peroxide. The enzyme activity was expressed as µ moles of H2O2 decomposed/min/mg/protein and calculated using the formula:
where OD = Absorbance, L = Light path, V = Total volume of reaction sample, M = Molar coefficeint of H2O2 (40/m/cm), V = Volume of sample, Y = mg protein in the sample.
Superoxide dismutase
This was determined according to the methods of Misra and Fridovich (1972). Adrenaline undergoes auto-oxidation rapidly to adrenochrome whose concentration can be determined at 420 nm with the aid of a spectrophotometer. The auto-oxidation of adrenaline depends on the presence of superanions. Superoxide dismutase inhibits the auto-oxidation of adrenaline by catalysing the breakdown of the superoxide anion. The degree of inhibition reflects the activity of SOD which is determined at 420 nm. Carbonate buffer (0.05 M) pH 10.2: This was prepared by dissolving 0.2014 g of Na2CO3, 0.2604 g NaHCO3 and 0.0372 g of EDTA in 100 ml of distilled water. The pH was adjusted to 10.2 using Sodium hydroxide. Hydrochloric acid (0.005 M): This was prepared by adding 0.044 ml concentrate HCL to 99.96mls of distilled water.
Gluthathione peroxidase
This was determined according to Nyman (1959). This is based on the oxidation of pyrogallol to purpurogallin by peroxidase activity, resulting to a deep brown colour disposition, read at 420 nm. Pyrogallol (20 mM): 0.2552 g of pyrogallol was dissolved in 100 ml of distilled water. To an aliquot of plasma (0.2 ml), 2.5 ml of phosphate buffer, 2.5 ml of H2O2, 1.5 ml of distilled water and 2.5 ml of pyrogallol were added. The reaction was allowed to stand for 30 min at room temperature. A deep brown colour was formed which was read at 480 nm.
where OD = Absorbance of test; Vt = Total volume of reaction mixture; Df = Diution factor = 1. E = Molar extinction co-efficient (12/m/cm); Vs = Volume of sample; Y = mg of protein used.
Determination of malondialdehyde
Malondialdehyde was determined using the thiobarbituric acid assay (Buege and Aust 1978). Malondialdehyde which is a product of lipid peroxidation reacts with thiobarbituric acid (TBA) to give a red species. A volume of plasma (1.0 ml) was added to 2.0 ml of TCA-TBA-HCL and mixed thoroughly. The solution was heated for 15 min in a boiling water bath. After cooling, the flocculent precipitate was removed by centrifuging at 1000 g for 10 min. The absorbance was determined using the formular;
A = Absorbance; V = Total volume of reaction mixture; M = Molar extinction coefficient; V = volume of the sample; Y = mg protein.
Statistical analysis
The mean of five determinations was taken using graph pad prism version five. A two-way analysis of variance was performed to determine sources of variability among the treatment used. Germination was assessed using various measurements and indices as earlier described (Timson 1965; Tucker and Wright 1965; Goodchild and Walker 1971; Gordon 1971; Abdul-Baki and Anderson 1973; AOSA 1983; Al-Mudaris 1998; ISTA 1999; Kader 2005; Ranal and Santana 2006). The first day of germination (or germinability) (FDG) was taken as the time when the first germination was recorded. The last day of germination (LDG) was the last day when seed germination was reported. The final germination percentage (FGP) is the germination percentage attained by the plant even beyond the period. The peak period of germination (PPG) or Modal time of germination (MTG) is the time in which the highest frequency of germinated seeds was observed and need not be unique. Median germination time (MeGT), or Days required for 50% germination, T50 i.e. days required for 50% germination.
T50 = Days required for 50% germination of the total number of seeds.
Germination rate index (GRI) was calculated using
where GP1 is germination percentage on the first day, GP2 is germination percent on the second day, GPn is germ percent at n days. GRI reflects the percentage of germination on each day of the germination period.
Corrected germination rate index (GRIcorrected):
The seedling vigor:
Time spread of germination, or Germination distribution (TSG):
This is the time (in days) taken between the first and last germination events.
Germination index, GI:
where S1, S2, S3, Sn are number of seeds that germinated per lot (or Petri dish) at day 1, day 2, day 3 … day n.
Mean daily germination, MDG:
Daily germination speed, DGS:
Mean germination time, MGT:
Mean germination rate, MGR:
Coefficient of velocity of germination, CVG:
where G1, G2, G3, Gn are germination percent per lot (or Petri dish) at day 1, day 2, day 3 … day n. CVG gives an indication of the rapidity of germination.
Germination capacity, GC:
where N is the number of seeds used in the bioassay.
Results
The present study investigated the germination characteristics of Sorghum bicolor under different pH regimes after chemo priming using growth stimulating substances such as indole-acetic acid, gibberellic acid as well as an antioxidant, Vitamin C. The results of germination indices of the text plant before chemopriming is presented in Table 1.
Results showed that germination occurred within the first day after initiation (Supplementary Fig. S1). No germination occurred at extreme pH 1 and pH 13 throughout the 6 days observation period. However, germination occurred between pH 3 and pH 11. The result for germination percentage showed that germination time was significantly enhanced at the alkaline pH of 11 wherein germination percentage attained was 97% within the first 24 h of germination initiation. However, in the control, the first germination percentage which was obtained within the first 24 h was less than 50% (pH 7).
When chemo-priming agents were applied whether in the dark or the presence of light, the result showed that although as earlier reported in Supplementary Fig. S1 wherein a higher germination percentage of 90% was obtained within 24 h of germination initiation, the introduction of chemo-priming significantly reduced germination percentage, particularly at pH 11. Seeds primed with IAA in the dark had germination percent that ranged from 5% on day 1 to 55% on day 7 when seeds were exposed to pH 3 (Supplementary Fig. S2).
The effects of light on the total sugar content of the germinant at 7 days after initiation of germination is presented in Table 2.
Although total sugars in the control was 0.0525 mg/ml, a significant increase in sugar content in the seeds originally exposed to pH changes without any form of chemo-priming significantly reduced at acidic pH (pH 1 to 5); where total sugars range from 0.0314 to 0.0325 mg/ml. However, at a highly basic pH, total sugars in the germinant were significantly high compared to the control (0.0721 to 0.982 mg/ml). It was generally observed that although germination percent was significantly reduced due to pH despite chemo-priming, the accumulation of sugars in the germinating seeds significantly increased by more than 100% irrespective of pH level in so far as the seeds were either primed with ascorbic acid, IAA or GA. In this case, total sugars range from 0.367 to 0.445 mg/ml. Germination performance during priming was computed using germination indices that accessed germination time and germination capacity. However, it took up to 165 h for Sorghum bicolor to complete germination (Supplementary Table S1). The median time of germination stood at 67 h at pH 3, 37 h at pH 7 and pH 11. Mean daily germination ranged from 15.0 at pH 5 to 32.2 at pH 11 whereas germination capacity ranged from 1.5 to 1.7. Considering the variance, however, it was observed that variance was highest in index. Supplementary Table S1 suggest the sources of variation, in this case, were pH levels and germination indices. Since synchronization index is a criterion for determining germination performance, it helps to show the possibility that germination would occur or not occur. Therefore, when the synchronization index is significantly high, the possibility for germination is higher compared to when the synchronization index was low which would indicate that the possibility that germination would not occur would be higher. In this study, the synchronization index was highest at pH 11 (418.22) compared to 223.57 at pH 7 (Suppelmentary Table S2). Similarly, at pH 3, the synchronization index was 5.11. The implication is that at pH 3 and pH 5, germination was most likely to occur under the current experimental conditions compared to pH 7.
The effects of chemo-priming with IAA in the presence of light or dark conditions on germination indices after priming is presented in Table 3.
When IAA was applied at night during the dark, the final germination percent of pH7 was 12.2 compared to 40.0 at pH 9. No germination was recorded at pH 11. However, when IAA was applied in the presence of light, the result showed significant elevation in final germination percent to 5.2 at pH 11. Chemopriming in the dark with IAA implied a peak period of germination at 70 h during exposure to pH 3, 73 h in pH 5, and 40 h in pH 7. This implication meant that as pH increased, chemo-priming during the dark enhanced germination time. The same was observed during the application of IAA in the dark wherein the peak period of germination reduced from 77.2 h at pH 3 to 41.3 h at pH 7. Germination hours ranged generally from 0.3 to 3.0 with the application of IAA whether in the presence or the absence of light.
Gibberellic acid was applied as a chemo-primer in the presence or absence of light (Table 4).
Here, result showed that no germination occurred at pH 1 and 3 irrespective of the light condition and GA as the chemo-primer. However final germination percent ranged from 35.3% at pH 11 to 60.9% at pH 9 when seeds were primed with GA in the presence of light. However, final germination ranged from 40.4% at pH 5, 7, and 11 to 70.6% at pH 3. The peak period of germination also reduced with the application of GA whether in the presence or absence of light from 70.6 h at pH 3 to 40.4 h at pH 9. The germination rate index was lowest at pH 11 (27.08) when GA was applied in the presence of light and 31.67 of germination rate index at pH 11 with the application of GA in the dark. Observably, germination performance in pH 11 which was highest without chemo-priming or exposure of the plant to light or dark conditions was significantly higher. The application of chemo-primers to enhance germination, germinability, and germination capacity at pH 11 has been significantly reduced. The same result are presented in Table 5. Ascorbic acid, SOD activity reduced to 75.3unit/g in pH 1 and 90.85unt/g in pH 9. High SOD activity was reported in pH 13 (95.65unit/g). Chemopriming with IAA and GA did not significantly affect SOD and catalase activities but affected malondialdehyde (MDA) and glutathione peroxidase (Supplementary Fig. S3). On the other hand, chemo-priming in the dark had variable effects on enzyme activities (Supplementray Fig. S4).
Enzyme levels were presented as possible sources of variation (Table 6). For all enzymes assayed, the result showed that the pH levels explained more than 25% of the total variation recorded in the experiment. For treatments, mean square 2.11 SOD, 0.63 for catalase, 202.9 for glutathione peroxidase and 30.5 for malondialdehyde. The implication is that variability was most likely attributed to changes in glutathione peroxidase.
Discussion
Soil pH significantly influences the growth and development of plants during germination. The level of pH affects the plant’s ability to absorb nutrient. Although pH plays a significant role in nutrient availability, depending on the plant extreme pH can cause nutrient deficiency and impair germination (Curtbew 2020). This same trend agrees with an earlier result obtained by Koger et al. (2004) who worked with Caperonia palustris. Koger et al. (2004) observed that germination was optimal within pH 5–9 but at both extremes, germination was retarded. Butchee et al. (2012) studied the effect of soil pH on Sorghum and they observed that the plant is sensitive to pH changes in the soil and that the more acidic the soil becomes, the greater the mortality of the seeds or seedlings. In this study, it was observed that extremes of pH reduced seed germination response. Seeds did not respond to the germination capacity of Sorghum bicolor at less than 24 h at extreme pH. This suggests that pH < 5.5 and pH > 8 fall outside the optimal pH range and pose a challenge in the development of any plant according to Lauchi and Grattan (2016) who reported that most cultivated soils suitable for crop production have pH ranges of 6 to 8. Gregory et al. reported the effect of acidity on the germination of Paulownia tomentosa. No germination occurred at pH < 4. Ion toxicity and nutrient imbalances were among the major causes of germination impairment. All of this research show that germination can either be stimulated or lagged by soil pH. Furthermore, Humphries et al. (2018) working with Nassella trichotoma, observed that despite the range of pH (4–10) the seed was subjected to, germination remained unaffected. Some plants are favoured by acidic pH and others thrive in a higher pH (basic soil) according to Ebrahimi and Eslamo (2012). Quality research has brought to light the understanding that most crop plants have an optimum pH range of 5.5 to 6.5 and unarguably outliers exist that favour pH extremes (Gentili et al. 2018). The extent of control pH has over seed germination, crop growth, and development, cannot be overlooked. In this study, there was a significant observation that aligns with this finding. The rate of germination was significantly higher at intermediate levels of pH between 3 and 11 without the application of chemo-primers. However, the germination percentage was higher for pH above 7 for the first 4 days of germination but on day 7 of observation, there was no significant difference in germination percentage. This suggests that high pH may enhance germination speed under certain conditions. Working with Calymperes erosum C. Mull Gemmaling observed that germination was appreciable within the range of 4 and 5 but at pH lower than 4 or higher than 7, germination was significantly retarded. Working with rape seed (Brassica napus L.) with the same ascorbic acid, Razaji et al. (2014) discovered that it dramatically improved germination, shoot length, root length, vigor index, and even stimulated enzyme activity under drought conditions. Gornik and Lahuta (2017) revealed that seed priming with salicylic acid or jasmonic acid improves sunflower growth, carbohydrate content, and low-temperature resilience (Helianthus annuus L.). Plant growth regulators have been implicated in the drought survival observed in Oryza sativa L (Sasi et al. 2021). The method of application is sometimes to the leaves and other times to the seed by seed priming” (Somorro et al. 2020; Rhaman et al. 2020).
The use of chemo-primers did not make significant changes in germination speed at all levels of pH. Guangu and Tailin (2013) have reported a different observation chemo-priming Cunninghamia lanceolata which showed a significant increase in germination speed after priming with IAA and GA. Although the observations are not similar, it is suggestive that the concentrations of the treatment could have a significant impact on the results. In this study, IAA and GA were applied in much higher concentrations which could have further impaired the rate of germination. Some plants would not germinate unless there is pitch-black darkness and others require low light and if the required condition is altered, delayed germination becomes unavoidable (Drake 1993). Priming seeds in the dark have shown a significant influence in enhancing germination in plants. The presence of light may stunt the germination process. However, priming Sorghum bicolor showed significant improvement in root and shoot length but at lower concentrations (Olorunmaiye and Olatunji 2018). This suggests that the chemo-priming of plants can be influenced by their concentration irrespective of the condition. In this study, it was observed that priming in the presence of light enhanced germination at pH 7 compared with the absence of light. At higher pH, there was improved growth without priming but impaired by the application of IAA and GA. This concurs with Hilay and Emile (1987) observations that chemo-primers uptake could be dependent on the proton gradient across the seed suggesting the influence of pH. IAA and GA could not overturn this concentration gradient even at higher pH or lower pH. At higher pH, however, Ascorbic acid showed a significant level of enhancement in germination.
Conclusion
Sorghum germination is easily affected by pH but only at extremes as shown by the results from this study. However, the fluctuation of pH in most soils could pose a serious threat to the survival of the plant beyond germination. The use of chemo-priming although did not influence germination at any level of pH, and can become a form of respite to ameliorate the challenge of extreme pH at negligible concentrations. The intermediate levels of pH showed significant growth response without priming suggesting that neutralizing soil pH could still be the best practice in overcoming the challenge of pH changes in the soil. The main sources of variation observed in the present study includes light and pH.
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The authors wish to express gratitude to the Head Lab., Mr. B, Ebebeli, for providing space for the study.
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BI conceived and designed the research; OO and MCO collected the data; BI and MCO performed analysis and interpretation of data; BI supervised the study; OO and MCO wrote the first draft; all the authors approved the final draft.
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Onoabhagbe, O., Ogwu, M.C. & Ikhajiagbe, B. Germination characteristics of Sorghum bicolor (L.) Moench. under different pH regimes after chemo-priming. Vegetos (2024). https://doi.org/10.1007/s42535-024-00909-0
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DOI: https://doi.org/10.1007/s42535-024-00909-0