Evaluating the impact of biochar on biomass and nitrogen use efficiency of sugarcane using 15N tracer method

N is an essential nutrient for sugarcane (Saccharum spp. Hybribds) growth. Excess chemical nitrogen fertilizer applied still a serious problem of China sugarcane plant. Biochar has shown promise in improving crop yield and N use efficiency (NEU).However its impact on sugarcane is not well-studied. To investigate how biochar impacts on sugarcane growth and nitrogen N use efficiency (NUE), a glasshouse pot experiment was conducted using the ¹⁵N tracer method. Two cultivars, GT11 and B8, were chosen as test objects and were planted under low N(120 kg N hm^-2) and high N(600 kg N hm^-2)condition, respectively. The effects of low and high biochar application rates (10 t hm^-2 and 20 t hm^-2) on growth, nitrogen uptake, accumulation and distribution as well as NUE in GT11 and B8 were studied. Results showed that sugarcane biomass was not significantly affected by biochar application. N uptake by GT11 was significantly increased 23.91% - 45.42% by C20 and N120 condition at tillering stage and elongation stage. While N uptake by B8 showed a significant response to B10 and B20 with an increase of 27.27% and 30.40% at tillering stage,respectively. Biochar application led to 0.28% - 23.75% and 1.08% - 30.07% increase in NUE of GT11 and B8,respectively. The effect of biochar application of N from fertilizer(FF) was significant,however only C20 treatment shown remarkable response when under low N treatment. Our study suggest that the effects of biochar on sugarcane depend on varieties and the applied rate of biochar and N fertilizer.Biochar application with inorganic N could improve N uptake and N use of sugarcane.

Highlight

1. Biochar improve the biomass of sugarcane genotype with low NUE.

2. Biochar could increase the N uptake and N from fertilizer of sugarcane.

3. High biochar application improve sugarcane take more N from fertilizer.

Introduction

Biochar is a carbon-rich substance prepared under hypoxic or anaerobic, low temperature (<800 °C) conditions (Lehmann et al., 2005). Biochar has shown great application potential in soil improvement (Pan et al., 2021), crop yield increase (Omara et al., 2020), and environmental restoration (AliZahed et al., 2021; Başer et al., 2021). It has received extensive attention from domestic and abroad researchers. Nitrogen is the primary nutrient element for crop production. Numerous studies have focused on the effects of biochar on the N utilization of soil and crops. The raw material source and preparation temperature of biochar will affect its ability to absorb nitrogen N (Liao et al., 2018), as well as the growth and N use efficiency of crops (Shanta et al., 2016; Egamberdieva et al., 2019; Olszyk et al., 2020). Biochar can increase the yield of corn (Omara et al., 2020), wheat (Zee et al., 2017), rice (Huang et al., 2014; Ali et al., 2020), and other crops (Lou et al., 2016; Haque et al., 2019; Li et al., 2021), and increase the utilization rate of N fertilizer. Its short-term effect is more evident under the condition of soil nutrient deficiency; however, its effect on increasing the yield of fertile soil is far from significant or even invalid (Jeffery et al., 2017; Vijay et al., 2021). Huang et al. (2019) experiment with biochar application on rice for six consecutive seasons; the N utilization rate increased by 7%–11% only during the fifth and the sixth seasons, indicating that the application of biochar must be repeated for a long period of time to increase the internal N utilization and yield of rice. The impact of biochar on crop yield and N utilization varies with crop or biochar species, application amount, and time.

Guangxi, a major sugarcane planting province in China, accounts for more than 60% of the country’s planting area and sugar production. The application of N fertilizer is an essential guarantee for increasing sugarcane yield and sugar content (Li et al., 2016). However, the current large-scale application of N fertilizer in sugarcane production has caused problems such as low fertilizer utilization, soil acidification, compaction, toxin accumulation, and reduced fertility (Zeng et al., 2020). Low N utilization efficiency of sugarcane is one of the main problems restricting the increase of sugarcane yield in China. Controlling or reducing the amount of N fertilizer application while continuously increasing sugarcane yield and minimizing the negative impact of excessive nitrogen fertilizer application has always been an important scientific issue for sugarcane-growing countries (Chandrasekaran et al., 2014; Li et al., 2016; Prasara et al., 2019). Previous studies have found that biochar can improve the root characteristics of the sugarcane seedlings and increase their root-shoot ratio (Liu et al., 2015). These effects may be related to the fact that biochar can increase soil pH, reduce N loss in the soil in the early and mid-term growth stages and promote the availability of nitrogen, phosphorus, and potassium in the soil (Liao et al., 2019a). However, these experiments are only the results of a single variety and a single nitrogen treatment and cannot fully reflect the effects of biochar on sugarcane growth and N utilization (Liao et al., 2019b). In this study, we selected two varieties with different nitrogen use efficiency and studied the effects of biochar on sugarcane growth, nitrogen absorption, cumulative distribution, and nitrogen utilization efficiency under different nitrogen treatment conditions using the ¹⁵N tracer method to explore the effects of biochar on sugarcane growth and N utilization. The results provide theoretical and technical references for applying biochar in sugarcane production and reducing the dependence on nitrogen fertilizer.

Materials and methods

Test materials

The sugarcane genotypes, Guitang 11 (GT11, N-inefficient) and B8 (N-efficient), were provided by the Germplasm Resource Garden of Sugarcane Research Institute, Guangxi Academy of Agricultural Sciences. The preliminary test found that the nitrogen use efficiency of the two varieties differed by about 1.0 fold.

Experimental design and treatments combination

The pot experiment was conducted from February 2016 to February 2017 in the greenhouse at Sugarcane Research Institute, Guangxi Academy of Agricultural Science, Nanning, China. Plastic pots of 40 cm in diameter and 40 cm in height were used. Biochar at the rate of 0 g (C0, equivalent to 0 t hm^-2), 70 g (C10, equivalent to 10 t hm^-2), and 141 g (C20, equivalent to 20 t hm^-2) per pot was mixed with soil (30 kg) and incubated. We applied ¹⁵N labeled urea at two rates: 1.8 g (N120, equivalent to 120 kg hm^-2 nitrogen fertilizer) and 9.0 g per pot (N600, equivalent to 600 kg hm^-2 nitrogen fertilizer). Each treatment had six replicates. Two sugarcane plants were planted in each pot. we applied P fertilizer 3.0 g (equivalent to 450 kg P₂O₅·hm^-2) and potassium K fertilizer 2.0 g (equivalent to 225 kg K₂O hm^-2) to each pot, and all the fertilizers were applied only once as base fertilizer when sugarcane is planted. The biochar was mixed and incubated with the aired dry soil one day in advance. The germination, planting, and growth management of the seed stems were the same as the experiment by Liao et al. (2019).

The soil was collected from a depth of 0–20 cm from the sugarcane test field of the Sugarcane Research Institute, Guangxi Academy of Agricultural Sciences. It is classified as Fe-leachi-Stagnic Anthrosols (Cooperative Research Group on Chinese Soil Taxonomy, CRGCST 2001) with a pH of 6.25, electrical conductivity of 42.12 mV, total C content of 0.72 g kg^-1, organic matter content of 15.1 g kg^-1, alkali-hydrolyzable nitrogen (N) of 91.23 mg kg^-1, phosphorus (P) of 43.41 mg kg^-1, and potassium (K) of 152.03 mg·kg^-1.Soil was aired dry and was broken up less than 5 cm with a rubber mallet.

The test biochar was produced from cassava stems using pyrolysis conditions described by Liao et al. (2019). The total C, N, and H of biochar were 67.4%, 0.8%, and 2.18%, respectively. The content of total phosphorus, and potassium were3.53, and 13.40 g·kg^–1. We used ¹⁵N-labeled urea (Shanghai Chemical Plant Ltd.) as the nitrogen fertilizer, with an abundance of 10.18% and a nitrogen content of 46%). Biochar was ground less than 2 mm before mixed and incubated with dry soil.

Plant yield contents

Samples of sugarcane were collected in three periods: the seedling period (four months after transplanting), the elongation period (seven months after transplanting), and the maturity period (12 months after transplanting). Three pots were collected for each treatment, and samples were classified according to roots, stems, dried leaves, and green leaves, and the fresh weight (FW) data were recorded simultaneously. Dried the collected materials at 60 °Ctill to constant weight, recorded the dry weights (DW, g/pot). The dried samples were ground to determine the total nitrogen content and ¹⁵N abundance.

Determination of plant N content, total N uptake and nitrogen use efficiency

The abundance of ¹⁵N was determined using an isotope mass spectrometer (Thermo Fisher, Waltham, MA, USA). Total N was determined by VAP50 Kjeldahl meter (Gerhardt, Königswinter, Germany). N uptake, Ndff (recovery percentage of plant-derived from ¹⁵N-urea), N uptake from fertilizer, N uptake from the soil, and N use efficiency were calculated using the following equation (Omara et al., 2020):

$$\text{Total N uptake }\left(\text{TN uptake, g/pot}\right)\text{ = total N concentration in plant × total plant DW}$$

$$\text{\% Ndff = }{(}^{15}{\text{N abundance in plant - background}}^{15}\text{N abundance})\text{ / }{(}^{15}{\text{N abundance in fertilizer- background}}^{15}\text{N abundance});{\text{ where, the background}}^{15}\text{N abundance = }\mathrm{0.3663 \%}.$$

$$\text{Ndff }\left(\text{mg/pot}\right)\text{ = Plant DW × N content × \% Ndff}$$

$$\text{N uptake from fertilizer }\left(\text{FF , \% }\right)\text{ = Ndff }\left(\text{mg/pot}\right)\mathrm{ x 100 / plant TN uptake}$$

$$\text{N uptake from soil }\left(\text{FS , \%}\right)=\text{ (total N uptake - N uptake from fertilizer) × 100 / plant TN uptake}$$

$$\text{Nitrogen use efficiency }\left(\text{NUE, \%}\right)\text{ = N uptake} \times \mathrm{100/N applied}$$

Statistical analysis

All data were processed and analyzed using Excel 2007. SPSS19.0 statistical package program was used for the analysis of variance (SPSS Institute, USA). One-way snalysis of variance and the least significant difference test (LSD) were used to assess the statistical differences between the biochar treatments at N120 or N600 level. The level of significance was assessed by 0.05 probability level.

Results

The effect of biochar and N fertilizer treatment on biomass of sugarcane

A considerable difference in the effect of biochar co-treatment with N fertilizer on the biomass of the two varieties was observed, as shown in Table 1. Two varieties were significantly different in the DW of root (p = 0.005), stem (p< 0.001), leaves (p< 0.001), and total DW (p< 0.001). The accumulation of sugarcane biomass was more affected by nitrogen application rate (p< 0.001), with an exception as the root DW (p = 0.208). Biochar could increase the DW of GT11 under low nitrogen conditions (N120). Total DW was 73.05, 195.21, and 347.49 g/pot at tillering stage, elongation stage, and maturation stage without biochar application (C0), respectively. Compared with control C0, total DW increased by 1.38%–16.28%, 4.98%–17.41% (p< 0.05) and 0.25%–6.61% after C10 and C20 treatment, respectively. These were mainly due to DW increases in the stem, green leaf, and root. Biochar application, under N600 treatment, did not show any significant effect of increasing DW of GT11.

TABLE 1

Table 1 Effects of biochar and N fertilizer treatment on dry weight(DW) of two sugarcane varieties.

After biochar was applied, the total DW of B8 was slightly higher than that of the control (C0), mainly under high nitrogen (N600) and high carbon (C20) conditions. Under this condition, the total DW of B8 was 111.24 g/pot, 361.32 g/pot, and 509.47 g/pot at tillering stage, elongation stage, and maturation stage, respectively, which were 0.63%, 12.17%, and 7.28% higher than that of C0 treatment, but did not reach a significant level of difference. These increases are mainly attributable to an enhancement in the stem and leaves DW.

Effects of biochar and N fertilizer treatment on nitrogen accumulation and distribution in sugarcane

As shown in Table 2, the N accumulation in stems, green leaves, and senescence leaves of the two varieties was significantly different after treatment (p< 0.001). Both carbon and N treatments significantly affected N accumulation in sugarcane stems, senescence leaves, green leaves, and whole plants (p< 0.001), but there was no significant interaction between carbon and N treatments. Biochar treatment promoted the increase of nitrogen accumulation in stem, and leaves of both varieties at different growth stages.

TABLE 2

Table 2 Effects of biochar and N fertilizer application on N uptake of two sugarcane varieties.

The nitrogen accumulation of GT11 in the whole plant was between 665–4854 mg/pot under low nitrogen conditions. Compared with C0 treatment, the N accumulation of GT11 increased by 7.97%–45.42% after biochar application, while N accumulation of roots, stem, and leaves also increased 2.05%–50.68% in each reproductive period. In particular, C20 treatment significantly increased the nitrogen accumulation of the whole plant in the tillering and elongation stages, which were 23.91% (p< 0.05) and 45.42% (p< 0.05) higher than the control (665 mg/pot and 3338 mg/pot), respectively. Green leaf nitrogen accumulation also increased by 33.74% (p< 0.05) and 43.85% (p< 0.05) compared with the control of 368.81 mg/pot and 453.99 mg/pot, respectively, while 50.68% (p< 0.05) increase in stem and 40.70% (p< 0.05) increase in roots were obtained mainly during the elongation stage.

Under high nitrogen condition, biochar application could boost the N accumulation in the whole plant. In GT11, N accumulation increased by 0.33%–10.43% at the tillering and elongation stages but did not reach a significant difference level. These increases were mainly due to the growth of nitrogen accumulation in roots, stem, and leaves, especially under the C20 treatment in the elongation period. The nitrogen accumulation significantly increased by 25.26%, 10.10%, and 8.25% compared to the respective controls of roots (708.38 mg/pot), stem (4536.27 mg/pot), and leaves (1148.21 mg/pot).

The biochar effect on B8 showed a similar change trend as GT11. The accumulation of whole plant nitrogen of B8 increased by 2.43%–45.23% at each growth stage after biochar was applied, irrespective of N treatment application. At the tilling stage, the nitrogen accumulation after biochar application significantly increased by 27.27%–30.40%, compared with the control (704 mg/pot) at N120 conditions; however, it significantly increased by 36.47% after C20 treatment at N600 condition. Biochar treatment promoted the green leaf nitrogen accumulation of B8 by 8.62%–58.15% at each growth stage. After C10 and C20 treatments, the green leaf nitrogen accumulation reached 634.14–659.57 mg/pot and 841.42–885.62 mg/pot in the tillering and elongation stages, which were significantly higher than C0 by 52.05%–58.15% and 32.45%–39.41%, respectively.

Biochar effect on N from soil and N from fertilizer

As shown in Table 3A, under high and low nitrogen condition without biochar application, the nitrogen in GT11 roots, stem, and leaves in each growth period, was chiefly came from the soil, accounting for 64.62%–82.02%. While the nitrogen from fertilizer (FF) accounted for 17.98%–35.38%. Under low nitrogen conditions, FF of GT11 was between 21.51%–35.03%,which was lower than C0 treatment by 0.02% - 6.32%.The FF of GT11 after C20 treatment was between 43.60%–69.34%,which was higher than C0 by 19.87% - 37.70%.Under high nitrogen conditions, biochar treatment significantly increased FF of GT11 roots, stem, and green leaves with the value between 53.44.22% - 68.87%,which was more than CO by 30.76-40.68%. Further, the value of FF with C10 treatment was higher than that with C20 treatment by 0.03% - 4.31%.

TABLE 3A

Table 3a Effects of biochar and N fertilizer treatment on FF and FS of GT11.

Data from Table 3B show that the performance trend of B8, after biochar and nitrogen co-treatment, was similar to that of GT11. In the case of no nitrogen application (C0), the FF of B8 roots, stem, and leaves was between 18.94% to 31.23%, and FS was between 68.77%–81.06%.Under N120 condition, C10 treatment could slightly increase the FF of B8 roots,stem and leaves by 0.16% - 2.07%. With C20 treatment, FF of B8 was increased up to 55.95-72.02% which was higher that C0 by 16.21% - 40.79%.FF of B8 increased corresponding to N fertilizer applied rates. When N fertilizer applied rate reached 600 kg hm^-2,FF of B8 was between 53.17% - 72.03%,that was more 10.00% - 38.43% than C0 treatment. And also observed that FF of B8 with C10 treatment was higher than that with C20 treatment by 0.93% - 15.76%.

TABLE 3B

Table 3b Effects of biochar and N fertilizer treatment on FF and FS of B8.

Statistical analysis showed that biochar and nitrogen treatment significantly affected the FF and FS of roots, stem, and leaves of the two varieties. There were significant differences between different treatment concentrations, and a significant interaction effect existed between biochar and nitrogen treatments.

Biochar effects on nitrogen use efficiency

As shown in Table 4, the NUE of sugarcane was significantly influenced by biochar and nitrogen treatment (p< 0.001). Variety mainly affected the NUE of green leaves (p = 0.002) and senescence leaves (p< 0.001).All in all, Biochar and N fertilizer treatment could increase the whole plant NUE of GT11 and B8 in all growth stages and organs (roots, stem, and leaves).The NUE of GT11 was 0.17%-26.60% higher than that of CK at different growth stages and different organs, B8 also show 0.05%-30.07% higher than CK. Yet two varieties show different response to biochar and N fertilizer applied rate.

TABLE 4

Table 4 Effects of biochar and N fertilizer treatment on N use efficiency of two sugarcane varieties.

Under low nitrogen conditions (N120), the whole plant NUE of GT11 remarkably improved by C20 treatment at tillering and elongated stages. Compared with the C0 treatment, the whole plant NUE of GT11 increased from 21.54% and 47.40% to 45.29% and 74.00% at tillering and elongated stages after C20 treatment, respectively. Under N600 conditions, biochar just significantly improved the whole plant NUE at tillering stages. The whole plant NUE with C10 and C20 treatment was up to 20.60% and 19.98%, that was more than C0 treatment by 12.14% and 11.52%, respectively.

Data from Table 4 shows that the whole plant NUE of B8 was observably increased after biochar applied under N600 conditions. At tillering stage, the whole plant NUE was up to 17.97% and 23.13% from 6.76% by C10 and C20, respectively, and was up to 57.70% and 61.90% from 42.87% at elongated stage, and was up to 48.99% and 46.48% from 18.92% at mature stage. While under N120 conditions, biochar mainly significantly improved the whole plant NUE at tillering stage with C20 treatment.

Discussion

Effects of biochar on sugarcane biomass

In accordance with previous report (Liao, 2019), biochar have little effect on the biomass accumulation of sugarcane. This is in agreement with some studies reported a decline in crop yield with biochar application (Zhu et al., 2014; Jay et al., 2015; Olszyk et al., 2020).Experiment on rice conducted by Xie et al. (2011) showed that grain yield decreased by 2% at first year after wheat straw biochar application. Previous researches seldom concern about different varieties yield response to the biochar impact. In this study, we found that the sugarcane variety GT11 with low NUE could significantly increase the biomass in the elongation period under low nitrogen treatment (N120), this is consistent with many studies which have shown that the effect of biochar on crop yield is not substantial in fertile soil; however, it becomes effective in poor soil (Xie et al., 2013; Omara et al., 2020; Haider et al., 2022). While the variety B8 with slightly higher NUE did not show a significant increase. We speculate that this difference arises from the differences in the response of different sugarcane genotypes to biochar. And this indicated that the impact of biochar on sugarcane yield is very complex.

Effects of biochar on nitrogen accumulation in sugarcane

The results from this study demonstrate that biochar could improve the nitrogen accumulation of the two sugarcane varieties under high and low nitrogen conditions, especially in the tillering and elongation stages, where the nitrogen accumulation of the whole sugarcane plant and green leaves significantly increased. Both biochar and nitrogen treatments greatly affected nitrogen accumulation in stem and leaves of the two varieties, but there was no significant interaction between them. These results are consistent with the effect of biochar on nitrogen accumulation in other crops. Huang et al. (2014) found that biochar promoted rice fertilizer nitrogen uptake by about 23%–27%, thus increasing rice grain yield by 6%–8%. Khan et al. (2021) also found that applying biochar under nitrogen reduction conditions can increase the nitrogen absorption of rice by 13%, thus increasing rice grain yield and NUE by 36% and 35%, respectively. Biochar can significantly increase nitrogen accumulation and the proportion of nitrogen obtained by crops from fertilizers or soil. This is probable due to biochar application can effectively improve soil structure, increase soil pH value, and facilitate the release of soil-available nitrogen and other nutrient availability (Frimpon et al., 2021). Our previous studies have also observed (Liao et al., 2018, 2019) that biochar can increase the nitrogen content in the soil and augment the soil nitrogen retention in the early growth stage of sugarcane, which could explain how biochar is capable of promoting the increase of nitrogen accumulation in the early growth stages of sugarcane.

The effect of biochar on sugarcane nitrogen use efficiency

Our experiment found that biochar can indeed improve the nitrogen utilization rate of sugarcane, where the NUE of roots, stem, and leaves increased to a certain extent. Under high and low nitrogen conditions, the nitrogen use efficiency of the whole plant, green leaves, and roots of GT11 was significantly improved, yet B8 got a huge boost under high nitrogen conditions. The positive influence of biochar on NUE is consistent with several reports. Omara et al. (2020) demonstrated that Zea mays L. grain yield, N uptake, and NUE increased by 25%, 28%, and 46%, respectively, with fertilizer N-biochar-combinations treatment compared to N fertilizer single treatment in sandy loam soil. Ye et al. (2020) conducted a three-year fixed-point experiment in stratospheric soil in Northeast China to study the effects of biochar and controlled-release of nitrogen fertilizers on rice yield, nitrogen use efficiency, residual nitrogen, and nitrogen balance in soil-crop systems. Their study found that yield and nitrogen use efficiency increased by 10.2% and 16.5%, respectively, after adding biochar. On the other hand, the experimental results showed that nitrogen accumulation, nitrogen use efficiency, and biomass in leaves were greatly improved, but biochar did not show a significant promoting effect on stem as harvested organs, suggesting that there is a complex transformation relationship in sugarcane ‘source–sink,’ thereby affecting the accumulation of stem biomass, which requires further research in later experiments.

Conclusion

With consistent biochar treatments and growing conditions, two sugarcane varieties varied in response to biochar but with some general patterns. Results showed a positive effect of application of biochar in genotype with low NUE and low N condition. High biochar applied rate could effectively reduce the stress of high N level on the growth of sugarcane. However, this experiment is mainly a barrel planting experiment under greenhouse conditions, and many years of multi-pilot field experiments are still needed in the follow-up tests. Nonetheless, the effect of biochar treatment on the physiological and biochemical indicators of sugarcane will be carried out in the future, and the relationship between the nitrogen balance of the biochar–sugarcane–soil system will be studied to verify and evaluate the effect of biochar on the nitrogen absorption and utilization of sugarcane. Finally, this study provides a theoretical basis for biochar application in sugarcane cultivation and production.

Data availability statement

The original contributions presented in the study are included in the article/Supplementary Material. Further inquiries can be directed to the corresponding authors.

Author contributions

GC: Analyzed and interpreted the data, Wrote the original article. JG: Performed the experiments, Contributed reagents, materials, analysis tools or data. C-XQ: Contributed reagents, materials, analysis tools or data. D-LH: revised the article. FL: Conceived and designed the experiments, Performed the experiments, Wrote the original article. LY: conceived and design the experiments. All authors contributed to the article and approved the submitted version.

Funding

The present study was supported by National Key R&D Program of China (2019YFD1000503, 2020YFD10006054-14), National natural science foundation of China (31560353), Natural Science Foundation of Guangxi Province (2021GXNSFBA075010), and Fund of Guangxi Academy of Agricultural Sciences (GNK2021YT0110,GNK2022JM14).

Acknowledgment

The authors would like to thank Editage (www.editage.cn) for English language editing.

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher’s note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

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