Introduction
Plant cell wall is a net structure
composed of various substances, such as cellulose, pectin, hemicellulose, and
so on (McCormick 2018; Zheng et al. 2018). Cell wall
components support plant cells, tissues, and corpus (Barnes and Anderson 2018). The mechanical strength of plants
corresponds to the physical property of their cell wall, which also helps crops
adapt to different cultivation environments. The inflorescence stem of some
herbaceous peony varieties exhibits a poor mechanical strength, and this
negative trait is manifested as a bending stem on a few days after budding
(DAB), which condition strongly affects the cut-flower production and
ornamental values of herbaceous peony. Therefore, breeders of herbaceous peony
aim to breed cut-flower cultivars with a starched stem (Varu and
Barad 2016; Xue et al. 2018).
The
variations and forms of the mechanical strength of a plant stem are related to
the variation of cell wall components. The main chemical components of the cell
wall are cellulose, pectin, and lignin, which exhibit synergic interactions in
different growth stages; these components mechanically support the entire plant
by affecting the strength of the cell wall of a plant stem (El Hage et al. 2018;
Hatfield et al. 2018). Therefore, the
composition and content of these substances could improve the mechanical
strength of plants. Cellulose is the main component of the cell wall of plants,
and this component provides support for plants (Kotake
et al. 2011). High cellulose content
yields tough plant tissues and improve their rupture strength (Liu et al. 2016). In African daisy (Gerbera jamesonii
Bolus), the stem contains less crude fiber than the other plant parts; as a
consequence, a curving stem is formed (Hamedan et al. 2019). Lignin is cross-linked with cell wall components via
a covalent bond; thus, the mechanical strength of the cell wall is enhanced (Salmén et al.
2016). For instance, cell wall components, such as lignin, of a brittle culm
mutant are significantly lower than those of wild-type brittle culm; as such,
the mutant exhibits a low mechanical strength and easily breaks than the
wild-type plant (Zhang et al. 2016;
Hirano et al. 2017). Pectin is mainly
distributed in the intercellular layer, and this component not only binds cells
together but also solidifies and reinforces tissues. Pectin is present in the
intercellular layer in two forms, namely, water-soluble pectin and
water-insoluble proto-pectin (Bethke et al. 2016). Fruit firmness decreases
as fruit maturity increases; the concentration of proto-pectin, which is
alkali-soluble pectin, decreases as the concentration of water-soluble pectin
increases (Szatanik-Kloc et al. 2017). Therefore, the main cell wall components, such as
cellulose, lignin, and pectin, are related to the mechanical strength of plant
stem. However, studies have rarely described the relationship between the
mechanical strength of the stem of herbaceous peony and its cell wall
components.
In this
study, stems of ‘Da Fugui’, ‘Yangfei
Chuyu’, and ‘Hong Yinzhen’
varieties of herbaceous peony (Paeonia officinalis Pall.) were used as test materials in
Yangzhou area. These varieties exhibit different mechanical strengths. The
mechanical strength, growth index, and content of cell wall components of each
stem were determined within 35 DAB, and the last determination was during
blooming stage. The morphological characteristics and the vibration of the
mechanical strength of the cell wall of each stem were compared. The
relationship of the cell wall components with the mechanical strength of the
stem was also examined from the budding stage to the blooming stage. This study
aimed to discuss the morphological and physiological mechanisms of the
variation in the mechanical strength of the stem of herbaceous peony during
development. Our results provided a theoretical basis of breeding herbaceous
peony with a high mechanical strength.
Materials and Methods
Test materials and experimental details
The test was conducted in
Herbaceous Peony Germplasm Resources Garden of the Gardening and Plant
Protection College in Yangzhou University from March 2013 to May 2013. The
growth status of three selected varieties, namely, ‘Da Fuigui’,
‘Yangfei Chuyu’, and ‘Hong Yinzhen’, was relatively uniform. Samples were collected
every seven days from the budding stage to the blooming stage. Stems, which
grew and developed consistently with each other, were randomly harvested. The inflorescence stems were
cut and separated into three segments, 5 cm length from the upper apex or
distal of the stem as the top segment, the same length from the proximal and
the midst as the bottom and the middle one, respectively. Stems from 3 plants
corresponding to each variety were tested for the
experiment. Plant height was measured with a
tape; parts of the basal stem were clipped and
then brought to the lab. Flower buds and leaves were washed; afterward, 10 cm
of upper stem, middle stem, and basal stem was clipped to determine the
morphological index and mechanical strength. After the samples were treated with
liquid nitrogen, the stems were placed in an ultra-cold storage freezer at -80°C.
Determination of stem thickness and fresh weight and mechanical
strength
The thickness of the stem was
measured by using a Vernier caliper; the fresh weight was determined by using
electronic scales. The mechanical strength (in Newton [N]) of the stem 5 cm underneath the flower was determined with the
method of Li et al. (2015) using a
strength tester (NK-2, Hangzhou Zhejiang). Each group was composed of three
herbaceous peonies, and measurement was repeated thrice.
Content determination of the main
cell wall components of herbaceous peony stem
The cell wall components of the
stem of herbaceous peony were determined in accordance with a previously
described method (Rose et al. 1998).
Briefly, the stems were ground into fine powder in liquid nitrogen and
extracted with 95% alcohol, then washed twice with boiling alcohol and methyl
alcohol: chloroform (1:1 v/v), respectively. Finally, the cell wall residues
were dried overnight at 50℃ and used for analysis. The experiment was
performed in triplicate. Pectin was
extracted in accordance with Majumder and Mazumdar (2002). Different methods
were applied to determine the contents of the following cell wall components:
sulfate-carbazole method for the water-soluble pectin together with the
proto-pectin content (Blumenkrantz and Asboe-hansen 1973), anthrone-sulfuric acid method for cellulose content (Updegraff 1969) and Müsel et al. (1997) method for lignin content.
Data
processing
The mechanical strength and the morphological
characteristics of the stem were evaluated by using SPSS 16.0. The contents of
each cell wall component in different development stages were also compared and
subjected to correlation analysis in SPSS 16.0. Differences in each parameter
among the three varieties were analyzed by LSD test at 5% significance level
using one-way ANOVA. The graphical presentation of data was done using
Microsoft Excel 2003.
Results
Changes
in mechanical strength, stem thickness, fresh weight
and plant height during development
Mechanical strength: The
changes of the three varieties were similar (Fig. 1). In particular, it
gradually increased and reached its maximum value on 35 DAB. Among
the three varieties, ‘Da Fugui’ yielded the highest
mechanical strength; by contrast, ‘Hong Yinzhen’
exhibited the lowest. The strength of stem with different parts was different.
The top stem of ‘Da Fugui’ was
16.46 N, which was 1.07 times stronger than the two other varieties. At the same time, the middle
stem of ‘Da Fugui’ was 73.22 N, which was 1.13 and 6.60 times stronger than ‘Yangfei
Chuyu’ and ‘Hong Yinzhen’,
respectively. While the basal stem of ‘Da Fugui’ was
171.78 N, which was 1.11 and 2.16
times stronger than ‘Yangfei Chuyu’
and ‘Hong Yinzhen’, respectively.
%20255-262_files/image002.png)
Fig 1: Changes in inflorescence stem mechanical strength of three herbaceous peony cultivars (A: upper stem; B: middle stem; C: bottom stem
%20255-262_files/image004.png)
Fig 2: Changes in inflorescence stem
thickness of three herbaceous peony cultivars
Stem thickness: The changes of the three varieties were also similar
with gradually increasing trend (Fig. 2). ‘Yangfei Chuyu’ was higher than that of ‘Da Fugui’
and ‘Hong Yinzhen’. The top stem of ‘Yangfei Chuyu’ was 0.50 cm on 35
DAB, was 1.02 and 1.67 times thicker than those of ‘Da Fugui’
and ‘Hong Yinzhen’, respectively. The middle stem of
‘Yangfei Chuyu’ was 0.99
cm, revealing that was 1.01 and 2.36 times thicker than those of ‘Da Fugui’ and ‘Hong Yinzhen’,
respectively. The basal stem of ‘Yangfei Chuyu’ was 1.23 cm; showing that 1.03 and 1.43 times
thicker than those of ‘Da Fugui’ and ‘Hong Yinzhen’, respectively.
Fresh weight: In particular, the fresh weight of the stems gradually
increased, reaching its maximum at 35 DAB. The stem of ‘Da Fugui’
was heavier than the two other varieties. The top stem of ‘Da Fugui’ was 1.80 g, which was 1.16 and 2.28 times heavier
than those of ‘Yangfei Chuyu’
and ‘Hong Yinzhen’. The middle stem of ‘Da Fugui’ was 3.07 g,which
was 1.02 and 3.41 times heavier than those ‘Yangfei Chuyu’ and ‘Hong Yinzhen’. The
basal stem of ‘Da Fugui’ was 4.75 g, which was 1.08
and 2.70 times heavier than those of ‘Yangfei Chuyu’ and ‘Hong Yinzhen’ (Fig.
3).
Plant height: The
height of these varieties gradually increased, while ‘Yangfei
Chuyu’ was significantly taller than the two other
varieties (Fig. 4). All three varieties reached their maximum height at 35 DAB.
‘Yangfei Chuyu’ was 78.8
cm, ‘Da Fugui’ and ‘Hong Yinzhen’
was 56.7 and 66.8 cm respectively. Likewise, the changes in the stems of the
three varieties were similar.
Dynamic
change in cell wall components of stem during development
%20255-262_files/image006.png)
Fig 3: Changes in inflorescence stem fresh
weight of three herbaceous peony cultivars
%20255-262_files/image008.png)
Fig 4: Changes in plant height of three
herbaceous peony cultivars
Cellulose:
The cellulose content of the three varieties
initially increased, but subsequently decreased, and reached the lowest value
on day 35 of budding (Fig. 5A). The lowest cellulose content of 154.64 μg·mg−1
was detected in ‘Hong Yinzhen’. This value was 45.33
and 35.55% in ‘Da Fugui’, and ‘Yangfei
Chuyu’, respectively. The cellulose contents of the
middle stem were also different among the three varieties. The cellulose
contents of ‘Da Fugui’ and ‘Yangfei
Chuyu’ decreased on days 0–35 of budding,
while the cellulose content of ‘Hong Yinzhen’
initially increased and then decreased (Fig. 5B). The lowest cellulose content
of 173.10 μg·mg−1 was found in the middle stem of
‘Hong Yinzhen’ on day 35 of budding; this
finding was 53.58% of the cellulose content of ‘Da Fugui’
and 39.84% of the cellulose content of ‘Yangfei Chuyu’. The cellulose contents of the basal stem of the
three varieties decreased (Fig. 5C). Among the three varieties, ‘Hong Yinzhen’ yielded the lowest cellulose content of 293.24 μg·mg−1
on day 35 of budding; this finding was 76.18% of the cellulose
content of ‘Da Fugui’ and 67.13% of the cellulose
content of ‘Yangfei Chuyu’.
Lignin:
The changes in the lignin content of the stem of
the three varieties were almost the same on 0–35 DAB (Fig. 6). In
particular, the lignin content gradually increased. The lignin content of ‘Da Fugui’ was higher than that of the two other varieties. The
lignin content of the top stem of ‘Da Fugui’ reached
113.59 μg·mg−1, which was 1.19 and 1.70
times higher than those of ‘Yangfei Chuyu’ and ‘Hong Yinzhen’,
respectively. The lignin content of the middle stem of ‘Da Fugui’
reached 117.85 μg·mg−1, which was 1.18
and 2.40 times higher than those of ‘Yangfei Chuyu’ and ‘Hong Yinzhen’,
respectively. The lignin content of the basal stem of ‘Da Fugui’
reached 126.21 μg·mg−1, which was 1.22
and 1.55 times higher than those of ‘Yangfei Chuyu’ and ‘Hong Yinzhen’,
respectively.
Pectin:
The changes in the water-soluble pectin content of
the three varieties were almost the same as the lignin (Fig. 7). In general,
the water-soluble pectin contents decreased. The content of ‘Da Fugui’ was significantly lower than that of the two other
varieties (P < 0.01). The content of the top stem of ‘Da Fugui’
on day 35 of budding was 11.07 μg·mg−1, which was
63.69% of ‘Yangfei Chuyu’
and 32.13% of ‘Hong Yinzhen’. The pectin content of
the middle stem of ‘Da Fugui’ was 9.76 μg·mg−1,
which was 34.75% of ‘Yangfei Chuyu’
and 23.78% of ‘Hong Yinzhen’. The content of the
basal stem was 17.22 μg·mg−1, which was 47.09% of
‘Yangfei Chuyu’ and 28.09%
of ‘Hong Yinzhen’. For the proto-pectin, in general,
the change of contents was contrast with that of water-soluble pectin (Fig. 8).
The content of ‘Da Fugui’ was significantly higher
than that of the two other varieties on day 35 of budding (P <
0.01). The content of the top stem of ‘Da Fugui’ was
132.69 μg·mg−1, which was 1.07 and 1.97 times
higher than those of ‘Yangfei Chuyu’
and ‘Hong Yinzhen’, respectively. The content of the
middle stem of ‘Da Fugui’ was 143.12 μg·mg−1,
which was 1.10 and 1.47 times higher than those of ‘Yangfei
Chuyu’ and ‘Hong Yinzhen’, respectively. The content of the basal stem of
‘Da Fugui’ was 177.94 μg·mg−1,
which was 1.37 and 1.65 times higher than those of ‘Yangfei
Chuyu’ and ‘Hong Yinzhen’,
respectively.
%20255-262_files/image010.png)
Fig 5: Changes in cellulose contents in
the inflorescence stems of three herbaceous peony cultivars
%20255-262_files/image012.png)
Fig 6: Changes in lignin contents in the
inflorescence stems of three herbaceous peony cultivars
(A: upper stem; B: middle stem; C: bottom stem.)
Correlation
analysis of the factors affecting mechanical strength of stem
Mechanical
strength of the top stem of the three varieties exhibited a highly significant
positive correlation with plant height, stem thickness, and stem fresh weight (Table 1). The mechanical
strength of the stem showed a significant negative correlation with the
cellulose and water-soluble pectin contents of the cell wall. The mechanical
strength of the stems of all varieties exhibited a highly significant positive
correlation with the lignin content of the cell wall.
The
correlation coefficients of the mechanical strength of the stem of herbaceous
peony at different developmental stages and the main physical and chemical
characteristics of this species are presented in Table 2. On 0–7 DAB, the
mechanical strength of the stem was positively correlated with plant height,
stem thickness and fresh weight, cellulose and pectin contents. The mechanical
strength of the stem was also significantly correlated with plant height, stem
thickness, and fresh weight, but was not correlated with the cellulose and
pectin contents. Furthermore, the mechanical strength of the stem was
negatively correlated with the lignin and proto-pectin contents. Among the
parameters correlated with the mechanical strength, the stem thickness yielded
the highest correlation (Table 2). On 14–21 DAB, the mechanical
strength of the stem was positively correlated with plant height, stem
thickness, and stem fresh weight, cellulose content, and water-soluble pectin
content. The mechanical strength of stem also exhibited a highly significant
correlation with stem thickness and stem fresh weight. Furthermore, the
mechanical strength of the stem was significantly correlated with plant height.
By contrast, the mechanical strength of the stem was not significantly
correlated with the cellulose and water-soluble pectin Table 1: Correlation coefficients of mechanical strength and some physical and
chemical characteristics of herbaceous peony inflorescence stems in different
parts
|
Correlation index |
Top stem |
||
|
‘Dafuigui’ |
‘Yangfei CHuyu’ |
‘Hong Yinzhen’ |
|
|
Stem thickness |
0.977** |
0.982** |
0.981** |
|
Stem fresh weight |
0.956** |
0.973** |
0.987** |
|
Plant height |
0.949** |
0.964** |
0.975** |
|
Cellulose contents |
-0.761** |
-0.822** |
-0.740** |
|
Lignin contents |
0.784** |
0.885** |
0.814** |
|
Soluble pectin contents |
-0.726** |
-0.829** |
-0.821** |
|
Proto-pectin contents |
0.728** |
0.808** |
0.824** |
%20255-262_files/image014.png)
Fig 7: Changes in soluble pectin contents in the inflorescence stems of three herbaceous peony cultivars
contents. The
mechanical strength was negatively correlated with the lignin and proto-pectin
contents. Among the parameters correlated with the mechanical strength, stem
thickness (R = 0.900**) exhibited the
largest correlation coefficient. On 28–35 DAB, the mechanical
strength of the stem was positively correlated with stem thickness, stem fresh
weight, lignin content, and proto-pectin content. The mechanical strength of
the stem exhibited a highly significant correlation with stem thickness and stem
fresh weight. The mechanical strength of the stem was significantly correlated
with the lignin content, but was not significantly correlated with the
proto-pectin content. Stem thickness (R =
0.961**) showed the largest correlation coefficient. Moreover, the
mechanical strength of the stem was negatively correlated with plant height,
cellulose content, and water-soluble pectin
%20255-262_files/image016.png)
Fig 8: Changes in proto-pectin contents in
the inflorescence stems of three herbaceous peony cultivars
content.
However, the negative correlation of the mechanical strength with the
water-soluble pectin was not significant.
Plant stem growth indexes, such as
length, thickness, and fresh weight, are the main factors affecting tissue
mechanical strength (Jeon et al. 2016; Wu et al.
2017). Our study indicated that plant height was significantly
correlated with the mechanical strength of the top stem of herbaceous peony
(Table 1); however, this finding is not consistent with that observed in rice
(Yang et al. 2011), wheat (Wang et al. 2006). In our study, plant height
was positively correlated with the mechanical strength of the stem on 0–7 DAB
and 14–21 DAB; however, on 28–35 DAB, plant height was negatively
correlated with the mechanical strength of the stem (Table 2). That is to say
that the mechanical strength gradually increased as the stem grew after the
budding stage of herbaceous peony. On 28–35 DAB, although the stem
stopped growth, the stem thickness was highly and significantly correlated with
the mechanical strength of the different parts of the stem of herbaceous peony
and at different developmental stages. This finding is consistent with that
observed in maize (Xu et al. 2017).
Table 2: Correlation
coefficients of mechanical strength and some physical and chemical
characteristics of herbaceous peony inflorescence stems in different stages
|
Index |
Correlation
index |
||
|
0–7 days after budding |
14–21 days after budding |
28–35 days after budding |
|
|
Stem diameter |
0.516** |
0.863** |
0.944** |
|
Stem fresh weight |
0.486** |
0.900** |
0.961** |
|
Plant height |
0.446** |
0.273* |
-0.055 |
|
Cellulose contents |
0.063 |
0.269 |
-0.203 |
|
Lignin contents |
-0.333 |
-0.220 |
0.499* |
|
Soluble pectin contents |
0.051 |
0.133 |
-0.554* |
|
Proto-pectin contents |
-0.496* |
-0.255 |
0.439 |
In our experiment, the fresh weight of the
stem was gradually increased to the maximum. This also implied the carbohydrate was abundant in the stem, which ensures that
the stem of herbaceous peony can support flowers with sufficient mechanical
strength in the full-bloom stage (Table 2). So, the fresh weight of the stem of
herbaceous peony was significantly correlated with the mechanical strength of
the different parts of the stem and different
developmental stages.
Plant
cell wall can provide mechanical strength for cells, tissues, and the entire plant,
and this part is composed of several substances, including cellulose, lignin
and pectin (Padayachee et al. 2017).
It was showed that the excessive cellulose content was closely related to
curvature of stems, and it was consistent with that found in hemp fibers (Liu et al. 2015), but inconsistent with that
observed in rice (Li et al. 2003) and
wheat (Wang et al. 2006). It is
possibly caused by the differences in the stalk structures of herbaceous peony,
rape, and members of the grass family. We believe that high cellulose content
is favorable for the maintenance of erectness at early developmental stage.
The lignin content of the stem of herbaceous
peony was significantly correlated with the mechanical strength of the stem
(Table 1), and is consistent with that observed in wheat (Tripathi et al. 2003). On 0–7 DAB and
14–21 DAB, the lignin content of the stem was negatively correlated
with mechanical strength, but this finding was not significant. On 28–35 DAB,
the lignin content of the stem was positively correlated with mechanical
strength. This revealed that low lignin content is favorable for stem growth in
early development stage; in later development stages, high lignin content is
necessary to enhance the mechanical strength of stems to maintain the starched
form of this plant part. This phenomenon is possible because stem growth occurs
as a result of cell differentiation, expansion, and extension at the early
developmental stage (Geitmann and Ortega 2009).
The
content of water-soluble pectin is decreased during pectin degradation in the
cell wall (Cybulska et al.
2015; Chen et al. 2015). In
this process, the pectin lyase disrupts the chemical bond between
polyoxymethylene galacturonic acid and arabinose
(Brown et al. 2005). The decomposition of cell wall components and an
increase in hydrolase activity in the cell wall result in curving stem (Lashermes et al. 2016).
The pectin content of herbaceous peony exhibited a significant negative
correlation with the mechanical strength of the stem. By contrast, the
proto-pectin content showed a positive correlation with the mechanical strength
of the stem (Table 1). Therefore, low water-soluble pectin content and high
proto-pectin content can increase the firmness of the cell wall, and this
condition favors the increase in the mechanical strength of stems. This result
is consistent with that observed in the fruit firmness of pear (Argenta et al. 1981)
and peach (Wahab et al. 2016).
The
optimum time to harvest herbaceous peony cut flowers is the firm budding stage.
In this experiment, this stage was on 28–35 DAB. Correlation
analysis revealed that the most relevant factors that determine the mechanical
strength of the stem of herbaceous peony are stem thickness,
stem fresh weight, lignin content, and water-soluble pectin content (Table 2).
Therefore, the mechanical strength of the stem of herbaceous peony could be
significantly enhanced by increasing stem thickness, stem fresh weight, and
lignin content and by reducing water-soluble pectin content through cultivation
management measures. Moreover, herbaceous peony with stems exhibiting high
mechanical strength, stem fresh weight, and stem thickness could be optimum
models to breed herbaceous peony cut flower.
Conclusion
The mechanical strength of stem was
positively correlated with lignin and proto-pectin contents but was negatively
correlated with cellulose and soluble pectin contents. It is suggested that
enhancing the amount of lignin during the late budding stage in plants by
cultivated measurements, such as increase the thickness as well as improve the
fresh weight of the stem, would be beneficial to improve the mechanical
strength of herbaceous peony stem.
Acknowledgments
This work was supported by the
Natural Science Foundation of China (31772341, 31972448), the Young Talent Support
Project of Jiangsu Provincial Association for Science and Technology, the Fifth
Phase of "Project 333″ Science Funding Program of Jiangsu
Province (BRA2019084), and Jiangsu Modern Agricultural Industrial Technology
System (JATS[2019]374, 448).We thank Dr. Bin Xu of Nanjing Agricultural University for his kind revision
of the manuscript.
References
Argenta LC, JP Mattheis,
X Fan, C Amarante (1981). Managing‘Bartlett’ pear fruit ripening with 1-methylcyclopropene
reapplication during cold storage. Postharvest
Biol Technol 31:125‒130
Barnes WJ, CT Anderson (2018). Release, recycle, rebuild: cell-wall remodeling, autodegradation,
and sugar salvage for new wall biosynthesis during plant development. Mol Plant 11:31‒46
Bethke G, A Thao, G Xiong,
B Li, NE Soltis, H Noriyuki, AH Rachel, K Fumiaki, JK Daniel, P Markus, G Jane
(2016). Pectin biosynthesis is critical for
cell wall integrity and immunity in Arabidopsis
thaliana. Plant Cell 28:537‒556
Blumenkrantz N, G Asboe-Hansen (1973). New method for
quantitative determination of uronic acids. Anal Biochem
54:484‒489
Brown DM, LAH Zeef, J Ellis, R Goodacre, SR
Turner (2005). Identification of novel genes in
Arabidopsis involved in secondary cell wall formation using expression
profiling and reverse genetics. Plant Cell 17:2281‒2295
Chen H, S Cao, X Fang, H Mu, H Yang, W. Wu (2015). Changes in fruit firmness, cell
wall composition and cell wall degrading enzymes in postharvest blueberries
during storage. Sci Hortic
188:44‒48
Cybulska J, A Zdunek,
A Kozioł (2015). The self-assembled network and physiological degradation of pectins in carrot cell walls. Food Hydrocolloid 43:41‒50
El Hage F, D Legland,
N Borrega, MP Jacquemot, Y Griveau, S Coursol, V Mechin, M Reymond (2018). Tissue lignification, cell wall p-coumaroylation
and degradability of maize stems depend on water status. J Agric Food Chem 66:4800‒4808
Geitmann A, JKE Ortega (2009). Mechanics and modeling of plant cell growth. Trends Plant Sci 14:467‒478
Hamedan HJ, MM Sohani, A
Aalami, NM Javad (2019). Genetic engineering of lignin
biosynthesis pathway improved stem bending disorder in cut gerbera (Gerbera jamesonii)
flowers. Sci Hortic
245:274‒279
Hatfield RD, H Jung, JM Marita, H Kim (2018). Cell Wall
Characteristics of a maize mutant selected for decreased ferulates.
Amer J Plant Sci 9:446‒466
Hirano K, R Masuda, W Takase, Y Morinaka, M
Kawamura, Y Takeuchi, H Takagi, H Yaegashi, S Natsume, R Terauchi, T Kotake, Y
Matsushita, T Sazuka (2017). Screening of rice mutants with improved saccharification efficiency
results in the identification of constitutive photomorphogenic 1 and gold hull
and internode 1. Planta 246:61‒74
Jeon HW, JS Cho, EJ Park, KH Han, YI Choi, J Ko (2016). Developing
xylem‐preferential expression of PdGA20ox1, a gibberellin
20‐oxidase 1 from Pinus densiflora, improves woody biomass production in a
hybrid poplar. Plant Biotechnol
J 14:1161‒1170
Kotake T, T Aohara,
K Hirano, A Sato, Y Kaneko, Y Tsumuraya,
H Takatsuji, S Kawasaki (2011). Rice brittle culm 6 encodes a dominant-negative form of CesA protein that perturbs cellulose synthesis in secondary
cell walls. J Exp Bot 62:2053‒2062
Lashermes G, A Gainvors-Claisse, S Recous, I
Bertrand (2016). Enzymatic strategies and carbon
use efficiency of a litter-decomposing fungus grown on maize leaves, stems, and
roots. Front Microbiol 7; Article
1315
Li C, Y Sun, D Zhao, J Tao (2015). Relationship between mechanical
strength and morphological index of inflorescence stem of herbaceous peony (Paeonia lactiflora
Pall.). Acta Agric Zhejiangensis
27:182‒188
Li Y, Q Qian, Y Zhou, M Yan, L Sun, M Zhang, ZM
Fu, YH Wang, B Han, XM Pang, MS Chen, JY Li (2003). BRITTLE CULM
1, which encodes a COBRA-like protein, affects the mechanical properties of
rice plants. Plant Cell 15:2020‒2031
Liu J, N Wu, H Wang, J Sun, B Peng, P Jiang, E Bai
(2016). Nitrogen addition affects chemical
compositions of plant tissues, litter and soil organic matter. Ecology 97:1796‒1806
Liu M, D Fernando, AS
Meyer, B Madsen, G Daniel, A Thygesen
(2015). Characterization
and biological depectinization of hemp fibers
originating from different stem sections. Indust
Crop Prod 76:880‒891
Majumder K, BC Mazumdar (2002). Changes of pectic substances in
developing fruits of cape-gooseberry (Physalis
peruviana L.) in relation to the enzyme activity and evolution of ethylene. Sci Hortic 96:91‒101
McCormick S (2018). Nanoscale imaging of xyloglucan in plant cell walls. Plant J 93:209‒210
Müsel G, T Schindler, R Bergfeld, K Ruel, G Jacquet, C
Lapierre, V Speth, P Schopfer
(1997). Structure and distribution of
lignin in primary and secondary cell walls of maize coleoptiles analyzed by
chemical and immunological probes. Planta 201:146‒159
Padayachee A, L Day, K Howell, MJ Gidley (2017). Complexity and health functionality of plant cell wall
fibers from fruits and vegetables. Crit Rev Food Sci Nutr 57: 59‒81
Rose JKC, KA Hadfield, JM Labavitch,
AB Bennett (1998). Temporal sequence
of cell wall disassembly in rapidly ripening melon fruit. Plant Physiol 117: 345‒361
Salmén L, JS Stevanic, AM
Olsson (2016). Contribution of
lignin to the strength properties in wood fibres
studied by dynamic FTIR spectroscopy and dynamic mechanical analysis (DMA).
Holzforschung
70:1155‒1163
Szatanik-Kloc A, J Szerement, J Cybulska,
G Jozefaciuk (2017). Input of different kinds of soluble
pectin to cation binding properties of roots cell walls. Plant Physiol Biochem
120:94‒201
Tripathi SC, KD Sayre, JN Kaul (2003). Growth and morphology of spring
wheat (Triticum aestivum
L.) culms and their association with lodging: Effects of genotypes, N levels and
ethephon. Field Crop Res 8:271‒290
Updegraff DM (1969). Semimicro determination of
cellulose inbiological materials. Anal Biochem 32:420‒424
Varu DK, AV Barad (2016). Effect of stem length and stage
of harvest on vase-life of cut flowers in tuberose (Polianthes tuberosa L.) cv. Double. J Hortic Sci 5:42‒47
Wahab M, Z Ullah, M Sajid, M
Usman, K Sohail, S Nayab, M
Ullah (2016). Effect of calcium sources as
foliar applications on fruit quality of peach cultivars. Prog Hortic 48:167‒172
Wang J, J Zhu, Q Lin, X
Li, N Teng, Z Li, B Li, A Zhang, J Lin (2006). Effects of stem structure and cell wall components on bending strength
in wheat. Chinese Sci Bull 51:815‒823
Wu L, W Zhang, Y Ding, J Zhang, ED Cambula, F Weng, Z Liu, C Ding, S Tang, L Chen, S Wang, G
Li (2017). Shading contributes to the reduction of stem mechanical strength by decreasing cell wall
synthesis in Japonica rice (Oryza sativa
L.). Front Plant Sci 8; Article 881
Xu C, Y Gao, B Tian, J
Ren, Q Meng, P Wang (2017). Effects of edah,
a novel plant growth regulator, on mechanical strength, stalk vascular bundles
and grain yield of summer maize at high densities. Field Crop Res 200:71‒79
Xue J, Y Tang, S
Wang, R Yang, Y Xue, C Wu, X Zhang (2018). Assessment of vase quality and transcriptional regulation of sucrose
transporter and invertase genes in cut peony (Paeonia lactiflora ‘Yang Fei Chu Yu’)
treated by exogenous sucrose. Posthar Biol Technol 143:92‒101
Yang Y, Z Zhu, Y Zhang, T Chen, Q Zhao, L Zhou, S Yao, Y Zhang, S Dong, C
Wang (2011). Relationship
between lodging resistance and stem morphological traits in different rice
varieties (lines). Jiangsu J Agric
Sci 27:231–235
Zhang M, F Wei, K Guo, Z Hu, Y Li, G Xie, Y
Wang, X Cai, L Peng, L Wang (2016). A novel FC116/BC10 mutation
distinctively causes alteration in the expression of the genes for cell wall
polymer synthesis in rice. Front Plant
Sci 7; Article 1366
Zheng Y, W Wang, Y
Chen, E Wagner, DJ Cosgrove (2018). Xyloglucan
in the primary cell wall: assessment by FESEM, selective enzyme digestions and
nanogold affinity tags. Plant J 93:213‒228