Biomass digestibility is predominantly affected by three factors of wall polymer features distinctive in wheat accessions and rice mutants
- Zhiliang Wu†1, 2, 3,
- Mingliang Zhang†1, 2, 3,
- Lingqiang Wang1, 2, 3Email author,
- Yuanyuan Tu1, 2, 3,
- Jing Zhang1, 2, 3,
- Guosheng Xie1, 2, 3,
- Weihua Zou1, 2, 3,
- Fengcheng Li1, 2, 3,
- Kai Guo1, 2, 4,
- Qing Li1, 2, 5,
- Chunbao Gao6 and
- Liangcai Peng1, 2, 3Email author
© Wu et al.; licensee BioMed Central Ltd. 2013
Received: 4 September 2013
Accepted: 26 November 2013
Published: 16 December 2013
Wheat and rice are important food crops with enormous biomass residues for biofuels. However, lignocellulosic recalcitrance becomes a crucial factor on biomass process. Plant cell walls greatly determine biomass recalcitrance, thus it is essential to identify their key factors on lignocellulose saccharification. Despite it has been reported about cell wall factors on biomass digestions, little is known in wheat and rice. In this study, we analyzed nine typical pairs of wheat and rice samples that exhibited distinct cell wall compositions, and identified three major factors of wall polymer features that affected biomass digestibility.
Based on cell wall compositions, ten wheat accessions and three rice mutants were classified into three distinct groups each with three typical pairs. In terms of group I that displayed single wall polymer alternations in wheat, we found that three wall polymer levels (cellulose, hemicelluloses and lignin) each had a negative effect on biomass digestibility at similar rates under pretreatments of NaOH and H2SO4 with three concentrations. However, analysis of six pairs of wheat and rice samples in groups II and III that each exhibited a similar cell wall composition, indicated that three wall polymer levels were not the major factors on biomass saccharification. Furthermore, in-depth detection of the wall polymer features distinctive in rice mutants, demonstrated that biomass digestibility was remarkably affected either negatively by cellulose crystallinity (CrI) of raw biomass materials, or positively by both Ara substitution degree of non-KOH-extractable hemicelluloses (reverse Xyl/Ara) and p-coumaryl alcohol relative proportion of KOH-extractable lignin (H/G). Correlation analysis indicated that Ara substitution degree and H/G ratio negatively affected cellulose crystallinity for high biomass enzymatic digestion. It was also suggested to determine whether Ara and H monomer have an interlinking with cellulose chains in the future.
Using nine typical pairs of wheat and rice samples having distinct cell wall compositions and wide biomass saccharification, Ara substitution degree and monolignin H proportion have been revealed to be the dominant factors positively determining biomass digestibility upon various chemical pretreatments. The results demonstrated the potential of genetic modification of plant cell walls for high biomass saccharification in bioenergy crops.
KeywordsCell wall Cellulose crystallinity Arabinose substitution degree p-coumaryl alcohol proportion Biomass digestibility Chemical pretreatment Wheat Rice
Lignocellulosic biomass has been considered as one of the most important renewable sources for biofuels and other chemical products . As the second generation of biofuels, biomass conversion into bioethanol principally involves three major steps: physical and chemical pretreatments for cell-wall disassociation, enzymatic digestion towards soluble sugar release, and yeast fermentation resulting in ethanol production . However, biomass conversion is currently a costly process due to lignocellulosic recalcitrance [3, 4]. Many factors such as cell wall compositions, wall polymer features, and wall network styles, determine the lignocellulosic recalcitrance [5–9]. Therefore, it becomes essential to sort out the major factors of plant cell walls that affect sugar release upon various pretreatments and sequential enzymatic hydrolysis .
Plant cell walls are composed primarily of cellulose, hemicelluloses, lignin and pectic polysaccharides with minor structural proteins . Cellulose is one of the most abundant biopolymers in nature , and has a straight carbohydrate polymer chain composed of β-1, 4-glucans [13, 14]. Cellulose crystallinity has been reported as a negative factor in biomass enzymatic digestibility [15–17]. Hemicelluloses are a class of heterogeneous polysaccharides, and xylans are the major components in the mature tissues of grass plants. It has been reported that hemicelluloses can negatively affect lignocellulose crystallinity for high biomass-digestibility in plants . In particular, arabinose substitution degree of xylans is a positive factor in biomass enzymatic saccharification upon various chemical pretreatments in Miscanthus.
Lignin is a very stable and complex waterproofing phenolic polymer composed mainly of p-coumaryl alcohol (H), coniferyl alcohol (G), and sinapyl alcohol (S) [19–22]. Due to its structural diversity and heterogeneity, lignin can greatly contribute to lignocellulosic recalcitrance [23, 24]. Recent reports have suggested that lignin may play dual roles in biomass enzymatic digestion, but much remains unknown in different plants [20, 24, 25].
Wheat and rice are the major food crops and can provide enormous biomass residues over the world [26–29]. Despite various physical, chemical, and biological pretreatments having been used for wheat and rice straw digestion [30–34], little is known about the key factors of plant cell-wall structures that greatly influence biomass enzymatic saccharification in both plants. Due to the complicated cell-wall structures and diverse biological functions, however, it remains technically difficult to find out the factors that remarkably affect biomass process [35, 36]. Hence, in this study we selected the representative wheat and rice samples from the 115 wheat accessions collected in China and the 46 rice mutants generated from T-DNA insertion mutagenesis pools . The selected wheat accessions and rice mutants can exhibit the characteristic cell-wall compositions that lead to sorting out three major factors of wall polymers on biomass enzymatic digestibility under various chemical pretreatments.
Results and discussion
Analysis of cell-wall composition in wheat and rice
Cell wall composition (% dry matter) of biomass residues in wheat samples
27.53 ± 0.98**
32.63 ± 0.34
21.76 ± 0.49*
35.89 ± 0.70
32.30 ± 0.11
23.08 ± 0.31
30.76 ± 1.35
29.66 ± 0.20**
21.56 ± 0.30*
32.71 ± 0.77
34.15 ± 0.79
20.45 ± 0.28
29.32 ± 0.15
29.68 ± 0.91
19.28 ± 0.17**
31.59 ± 0.97
29.92 ± 0.28
24.48 ± 0.05
Cell wall composition (% dry matter) of biomass residues in wheat samples
30.76 ± 1.35
29.66 ± 0.20
21.56 ± 0.30
30.19 ± 0.38
30.40 ± 0.24
22.45 ± 0.46
29.32 ± 0.15
29.68 ± 0.91
19.28 ± 0.17
29.38 ± 1.15
29.85 ± 0.96
19.70 ± 1.29
33.76 ± 0.56
33.70 ± 0.56
20.94 ± 0.33
32.71 ± 0.77
34.15 ± 0.79
20.45 ± 0.28
Cell wall composition (% cell wall) of biomass residues in wheat and rice samples
35.26 ± 0.29
38.71 ± 0.55*
26.03 ± 0.59
36.36 ± 0.20
36.61 ± 0.52
27.03 ± 0.38
37.43 ± 0.76
36.73 ± 0.94
25.84 ± 0.64
37.09 ± 0.36
37.17 ± 0.51
25.75 ± 0.43
33.30 ± 0.34
39.27 ± 1.05
27.43 ± 0.75
33.60 ± 0.80
39.84 ± 0.35
26.56 ± 0.79
Determination of biomass digestibility in wheat
Due to the alternations of cell-wall composition in group I (Table 1), we found that reducing single-wall polymer levels (cellulose, hemicellulose, lignin) at three pairs (I-1, I-2, I-3) caused considerably increased biomass enzymatic digestibility by 1.2- to 2.0-fold (hexose yields) under NaOH and H2SO4 pretreatments with three concentrations (Figure 1A, Additional files 1 and 2). Notably, although the wheat sample (TaLq1) in pair I-2 showed the reduced hemicellulose level than its paired sample (Talq47) by 15.1%, the TaLq1 sample displayed a much higher biomass enzymatic saccahrification, similar to the samples in pairs I-1 and I-3 with the cellulose and lignin level changed by 30.4% and 27.0%, respectively. The results indicated that hemicelluloses, such as cellulose and lignin, may negatively affect biomass digestibility in wheat, which was similar to the findings in wood and corn [38, 39], but was in contrast to Miscanthus.
To test the negative effect of three major wall polymers on biomass saccharification, we determined the wheat samples of group II, in which each pair exhibited a very similar cell-wall composition (Table 2). Like group I, the biomass enzymatic digestibility in group II was also much changed by 1.2- to 1.7-fold (hexose yields) between the two samples of each pair (II-1, II-2, II-3) after pretreatments with three concentrations of NaOH (Figure 1B, Additional files 1 and 2). By comparison, the wheat samples pretreated with H2SO4 showed relatively less change by 1.1-1.3 fold than that of NaOH. Hence, the data suggested that the cell wall composition (three major wall polymer levels) was not the major factors on biomass enzymatic digestibility in wheat, in particular, upon NaOH pretreatment.
Comparison of biomass saccharification between wheat and rice
Furthermore, the three rice mutants exhibited much higher hexose yields or total sugar yields than that of all ten wheat samples under NaOH and H2SO4 pretreatments (Additional files 1 and 2). For instance, pretreated with 1% NaOH, three rice mutants (Osfc27, Osfc2 and Osfc32) respectively displayed hexose yields (% cellulose) of 59.6%, 93.4%, and 67.4% or total sugar yields (% cell wall) of 72.3%, 76.9%, and 74.2%, whereas ten wheat samples had hexose yields ranging from 31.4% to 54.5% or total sugar yields ranging from 37.8% to 50.8%. Similarly, the Osfc32 mutant pretreated with 1% H2SO4 displayed the highest hexose and total sugar yields at 74.3% and 86.4%, but Talq27 and Talq107 accessions had the highest hexose or total sugar yields at 50.3% or 55.2%, respectively.
Observation of biomass residue surface
Effects of wall-polymer features on biomass enzymatic digestion
With regard to monosaccharide composition of hemicelluloses, we found that arabinose (Ara) and xylose (Xyl) covered more than 95% of total monosaccharides (Additional file 4), indicating that xylans are the major hemicelluloses in both wheat and rice plants. As the Xyl/Ara ratio has been applied as a negative indicator for the Ara substitution degree of xylans in Miscanthus, we calculated the Xyl/Ara values of both potassium hydroxide (KOH)-extractable and non-KOH-extractable hemicelluloses. In general, the non-KOH-extractable hemicelluloses contained the largest difference in Xyl/Ara values between two samples of each pair (ranging from −18.0% to −148.1%), compared with the KOH-extractable hemicelluloses (−1.6% to −75.9%) and total hemicelluloses (−1.2% to −79%) (Figure 4B, Additional file 4). Like cellulose CrI, the biomass samples with high biomass digestibility had much lower Xyl/Ara values than that of their paired samples in the non-KOH-extractable hemicelluloses, in particular in three pairs of group III. Hence, the data indicated that Ara substitution degree of the non-KOH-extractable xylans positively affected biomass enzymatic digestibility in wheat and rice, similar to the role of Xyl/Ara in Miscanthus.
In terms of three monolignin (H, G, S) constitution, we calculated the ratios (H/G, H/S, S/G) in the KOH-extractable and non-KOH-extractable lignins (Additional file 5). By comparison, H/G values of the KOH-extractable lignin were much more alternated between two samples of each pair than any other monolignin ratios (Figure 4C, Additional file 5). Unlike cellulose CrI or hemicellulose Xyl/Ara, the biomass samples with high biomass-digestibility displayed extremely higher H/G values than that of their paired samples in the KOH-extractable lignin, in particular in three pairs of group III. Thus, this is the first time report of H/G (or the H proportion) as a positive factor in biomass enzymatic saccharification in wheat and rice. On the other hand, although S/G has been reported as a negative factor in Miscanthus and other plants [15, 40–42], the nine pairs of biomass samples exhibited an inconsistent and small alternation of S/G, suggesting that the S/G was not the major factor in wheat and rice.
In summary, three pairs of wheat and rice samples in group III exhibited much more alternations of CrI, Xyl/Ara and H/G values than that of the other six pairs of wheat samples in groups I and II (Figure 4), consistent with the remarkably high biomass-digestibility in rice mutants.
Correlation among wall-polymer features and biomass digestibility
Potential modification of plant cell walls for high biomass digestibility
The three main wall-polymer features, including cellulose CrI, non-KOH-extractable Xyl/Ara of hemicellulose, and KOH-extractable H/G of lignin, rather than cell-wall composition (wall-polymer levels), have been revealed as predominant factors in biomass enzymatic digestibility upon various chemical pretreatments. It has been indicated that either Ara substitution degree or H monolignin proportion negatively affects CrI for high biomass-saccharification. The results also suggest the potential of cell-wall modifications for biofuel production in wheat, rice and other bioenergy crops.
The 115 wheat accessions were provided by Hubei Agricultural Science Academy in Hubei Province, China. They represent a diversity of winter wheat germplasm adapted to growth in Yangzi River regions in central China. All the wheat samples were collected from Hubei experimental fields in the growing season of 2010. A total of 46 homozygous rice mutants with fragile or high culm phenotypes were originally selected from T-DNA mutant pools as described by Xie et al. 2013 , and their mature culms tissues were collected from the Wuhan experimental fields in 2009 and 2010. The collected samples were dried at 50°C after inactivation at 105°C for 20 minutes. The dried tissues were ground into powder through a 40-mesh screen and stored in a dry container until use.
Plant cell-wall fractionation
The plant cell-wall fractionation method was used to extract cellulose and hemicelluloses, as described by Peng et al., 2000 , and Xu et al., 2012  with minor modification. The soluble sugar, lipids, starch and pectin of the samples were successively removed by potassium phosphate buffer (pH 7.0), chloroform-methanol (1:1, v/v), dimethylsulphoxide (DMSO)-water (9:1, v/v) and 0.5% (w/v) ammonium oxalate. The remaining pellet was extracted with 4 M KOH with 1.0 mg/mL sodium borohydride for 1 h at 25°C, and the combined supernatant with two parallels; one parallel was neutralized, dialyzed and lyophilized as KOH-extractable hemicelluloses monosaccharides, and one parallel was collected for determination of free pentoses as the KOH-extractable hemicelluloses. For the remaining two parallel non-KOH-extractable residues, one parallel was sequentially extracted with trifluoroacetic acid (TFA) for monosaccharides, and one parallel was further extracted with H2SO4 (67%, v/v) for 1 h at 25°C, and the supernatants were collected for determination of free hexoses and pentoses as total cellulose and non-KOH-extractable hemicelluloses. All experiments were carried out in biological triplicate.
Colorimetric assay of hexoses and pentoses
The UV–VIS spectrometer (V-1100D, Shanghai MAPADA Instruments Co., Ltd. Shanghai, China) was used for the absorbance reading. Hexoses were detected using the anthrone/H2SO4 method , and pentoses were tested using the orcinol/HCl method . Anthrone was purchased from Sigma-Aldrich Co. LLC., and ferric chloride and orcinol were obtained from Sinopharm Chemical Reagent Co., Ltd. The standard curves for hexoses and pentoses were drawn using d-glucose and d-xylose as standards (purchased from Sinopharm Chemical Reagent Co., Ltd.) respectively. The total sugar yield from pretreatment and enzymatic hydrolysis was subject to the sum total of hexoses and pentoses. High pentose levels can affect the absorbance reading at 620 nm for hexose content using the anthrone/H2SO4 method, so deduction from the pentose reading at 660 nm was carried out for final hexose calculation. A series of xylose concentrations were analyzed for plotting the standard curve referred to for the deduction, which was verified by gas chromatography–mass spectrometry (GC-MS) analysis. All experiments were carried out in biological triplicate.
Hemicellulose monosaccharide determination by GC-MS
Determination of hemicellulose monosaccharides was described by Li et al., 2013 . The combined supernatants from 4 M KOH fraction were dialyzed for 36 h after neutralization with acetic acid, and the sample from the dialyzed KOH-extractable supernatant or the non-KOH-extractable residue was hydrolyzed by 2 M TFA for free monosaccharide release in a sealed tube at 121°C in an autoclave for 1 h. Myo-inositol (200 μg) was added as the internal standard for GC-MS (SHIMADZU GCMS-QP2010 Plus).
GC-MS was performed using the following: analytical conditions: Restek Rxi-5 ms, 30 m × 0.25 mm ID × 0.25 um df column; carrier gas: helium; injection method: split; injection port: 250°C; interface: 250°C; injection volume: 1.0 μL; temperature program: from 155°C (held for 23 minutes) to 200°C (held for 5 minutes) at 3.8°C/minute, then from 200°C to 300°C (held for 2 minutes) at 20°C/minute; ion source temperature: 200°C; ACQ mode: SIM. The mass spectrometer was operated in the EI mode with ionization energy of 70 ev. Mass spectra were acquired with full scans based on the temperature program from 50 to 500 m/z in 0.45 s. Calibration curves of all analytes routinely yielded correlation coefficients of 0.999 or higher.
Total lignin assay
Total lignin content was determined by the two-step acid hydrolysis method according to Laboratory Analytical Procedure of the National Renewable Energy Laboratory. The lignin includes acid-insoluble and -soluble lignin. The acid-insoluble lignin was calculated gravimetrically after correction for ash, and the acid-soluble lignin was measured by UV spectroscopy.
All experiments were carried out in triplicate.
Lignin monomer detection by high performance liquid chromatography (HPLC)
Lignin monomer determination was as described by Xu et al., 2012 . The standard chemicals, p-Hydroxybenzaldehyde (H), vanillin (G) and syringaldehyde (S) were purchased from Sinopharm Chemical Reagent Co., Ltd. The sample was extracted with benzene-ethanol (2:1, v/v) in a Soxhlet for 4 h, and the remaining pellet was collected as cell-wall residue (CWR). The procedure for nitrobenzene oxidation of lignin was conducted as follows: 0.05 g CWR was added with 5 mL 2 M NaOH and 0.5 mL nitrobenzene, and a stir bar was put into a 25-mL Teflon gasket in a stainless steel bomb. The bomb was sealed tightly and heated at 170°C (oil bath) for 3.5 h and stirred at 20 rpm. Then, the bomb was cooled with cold water. The chromatographic internal standard (ethyl vanillin) was added to the oxidation mixture. This alkaline oxidation mixture was washed three times with 30 mL CH2C12/ethyl acetate mixture (1:1, v/v) to remove nitrobenzene and its reduction by-products. The alkaline solution was acidified to pH 3.0 to 4.0 with 6 M HCl, and then extracted with CH2CI2/ethyl acetate (3 × 30 mL) to obtain the lignin oxidation products, which were in the organic phase. The organic extracts were evaporated to dryness under reduced pressure at 40°C. The oxidation products were dissolved in 10 mL chromatographic pure methanol.
For HPLC analysis the solution was filtered with a membrane filter (0.22 μm). Then, 20 μL solution was injected into the HPLC (Waters 1525 HPLC) column Kromat Universil C18 (4.6 mm × 250 mm, 5 μm) operating at 28°C with CH3OH:H2O:HAc (25:74:1, v/v/v) carrier liquid (flow rate: 1.1 mL/minute). Calibration curves of all analytes routinely yielded correlation coefficients 0.999 or higher, and the detection of the compounds was carried out with a UV-detector at 280 nm.
Detection of cellulose crystallinity
I200 represents both crystalline and amorphous materials while Iam represents amorphous material. The standard error of the CrI method was detected at ± 0.05 to approximately 0.15 using five representative samples in triplicate.
Scanning electron microscopy (SEM) observations
The well-mixed biomass powder samples were pretreated with 1% NaOH or 1% H2SO4, and hydrolyzed with the mixed cellulases. The remaining residues were washed with distilled water until the pH was 7.0. The surface morphology of the sample was sputter-coated with gold and observed by SEM (SEM JSM-6390/LV, Hitachi, Tokyo, Japan) as described by Xu et al., 2012 . Each sample was observed 5 to 10 times and the representative image was used in this study.
Chemical pretreatments were performed as previously described by Huang et al., 2012  with minor modification. For H2SO4 pretreatment, the well-mixed powder of the biomass sample (0.3 g) was added with 6 mL H2SO4 at three concentrations (0.25%, 1%, 4%, v/v). The tube was sealed and heated at 121°C for 20 minutes in an autoclave (15 psi) after mixing well. Then, the tube was shaken at 150 rpm for 2 h at 50°C, and centrifuged at 3,000 g for 5 minutes. The pellet was washed three times with 10 mL distilled water, and stored at −20°C for enzymatic hydrolysis. All supernatants were collected for determination of total sugars (pentoses and hexoses) released from acid pretreatment, and samples with 6 mL distilled water were shaken for 2 h at 50°C as the control. All samples were carried out in biological triplicate.
For NaOH pretreatment, the well-mixed powder of the biomass sample (0.3 g) was added with 6 mL NaOH at three concentrations (0.5%, 1%, 4%, w/v). The tube was shaken at 150 rpm for 2 h at 50°C, and centrifuged at 3,000 g for 5 minutes. The pellet was washed three times with 10 mL distilled water, and stored at −20°C for enzymatic hydrolysis. All supernatants were collected for determination of total sugars released from alkali pretreatment, and samples with 6 mL distilled water were shaken for 2 h at 50°C as the control. All samples were carried out in biological triplicate.
The remaining residues from various pretreatments were washed twice with 10 mL distilled water, and once with 10 mL of mixed-cellulase reaction buffer (0.2 M acetic acid-sodium acetate, pH 4.8). The washed residues were added with 6 mL (1.6 g/L) of mixed cellulases containing β-glucanase (≥2.98 × 104 U), cellulase (≥298 U) and xylanase (≥4.8 × 104 U) from Imperial Jade Bio-technology Co., Ltd) at 0.16% (w/w) concentration for H2SO4- and NaOH- pretreated samples. During the enzymatic hydrolysis, the samples were shaken at 150 rpm at 50°C for 48 h. After centrifugation at 3,000 g for 10 minutes, the supernatants were collected to determine the amounts of pentose and hexose released from enzymatic hydrolysis. The samples with 6 mL of reaction buffer were shaken for 48 h at 50°C as the control. All samples were carried out in biological triplicate.
Statistical calculation of correlation coefficients
Correlation coefficients were generated by performing Spearman rank correlation analysis for all pairs of measured traits across the whole population. This analysis used average values calculated from all original determinations for a given traits pair.
cell wall residue
gas chromatography-mass spectrometer
high performance liquid chromatography
scanning electron microscopy.
We specially thank Dr Qifa Zhang for kindly providing the rice T-DNA mutant pools and Dr Xiwen Cai for reading of the manuscript. This work was supported in part by grants from the 111 Project of Ministry of Education of China (B08032), the National Natural Science Foundation of China (31171524), the Transgenic Plant and Animal Project of Ministry of Agriculture of China (2009ZX08009-119B), the 973 Pre-project of Ministry of Science and Technology of China (2010CB134401), HZAU Changjiang Scholar Promoting Project (52204–07022), and Fundamental Research Funds for the Central Universities (2011PY047).
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