Effects of sand burial on survival and growth of Artemisia
halodendron and its physiological response
HaLin Zhao 1*, Hao Qu 1, RuiLian Zhou 2, (given name before family name)
1. Cold and Arid Regions Environmental and Engineering Research Institute, Chinese Academy of Sciences, Lanzhou,
Gansu 730000, China
2. Faculty of Life Sciences, Ludong University, Yantai, Shandong 264025, China
*Correspondence to: HaLin Zhao, Professor of Cold and Arid Regions Environmental and Engineering Research Institute, Chinese Academy of Sciences. No. 320, West Donggang Road, Lanzhou, Gansu 730000, China. E-mail:
zhaohalin9988@hotmail.com
ABSTRACT
There is a great deal of literature on the effects of sand burial upon the survival and growth of desert plants, but the
physiological adaption mechanisms of desert plants to sand burial have as yet rarely been studied. Artemisia halodendron
is widely distributed in the semi-arid deserts of China and is a dominant species in semi-moving dune vegetation. The
growth and physiological properties of A. halodendron seedlings under different sand burial depths were studied in 2010
and 2011 in the Horqin Sand Land, Inner Mongolia, to better understand the ability and physiological mechanism by which
desert plants withstand sand burial. The results showed that A. halodendron as a prammophyte species had a stronger
ability to withstand sand burial compared to non-prammophytes, with some plants still surviving even if buried to a depth
reaching 225% of seedling height. Although seedling growth was inhibited significantly once the depth of sand burial
reached 50% of the seedling height, seedling survival did not decrease significantly until the burial depth exceeded 100%
of the seedling height. Sand burial did not result in significant water stress or MDA (Malondialdehyde) accumulation in the
seedlings, but membrane permeability increased significantly when the burial depth exceeded 100% of the seedling height.
After being subjected to sand burial stress, POD (Peroxidase) activity and proline content increased significantly, but SOD
(Superoxide Dismutase) and POD activities and soluble sugar content did not. The primary mechanism resulting in increased mortality and growth inhibition were that cell membranes were damaged and photosynthetic area decreased when
subjected to the severe stress of sand burial, while proline and POD played key roles in osmotic adjustment and protecting
cell membranes from damage, respectively.
Keywords: desert shrub; sand burial; survival rate; growth; physiological response
1 Introduction
In coastal and lake shoreline dunes, as well as in inland dunes and desertified areas, sand burial is a common environmental stress encountered by plants (Maun and Lapierre, 1984; Sykes and Wilson, 1990). Plants living in these
areas may experience various degrees of sand burial, including partial or complete burial (Brown, 1997; Maun, 1998).
Only species with special adaptations to sand burial can survive (Maun and Lapierre, 1984; Zhao, 2012). Thus, sand
burial is considered an important factor controlling the distribution and composition of vegetation in sand dune
communities (Shi et al., 2004; Li and Zhao, 2006). The seedling stage is the most vulnerable period in a plant’s life
history, and thus the most vulnerable to the hazards of sand burial (Shi et al., 2004; Ma et al., 2007). The ability of
seedlings to withstand sand burial is crucial for successful establishment and population maintenance by dune vegetation species (Maun, 1998; Owen et al., 2004).
There is considerable literature on how sand burial impacts desert plants, which has focused on the effects of
sand burial on seed germination, emergence, seedling survival and growth, biological yield, and biomass allocation
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(Maun and Lapierre, 1984; Brown, 1997; Li and Zhao, 2006; Wang et al., 2011). A number of studies have
demonstrated that sand burial may modify the physiology and morphology of plants and affect their survival and
growth (Maun and Riach, 1981; Maun, 1998) because sand burial may change abiotic and biotic conditions such as
photosynthetically active radiation, soil temperature, moisture, organic matter, rhizosphere oxygen content, and the
activities of soil microorganism (D’Hertefeldt and van der Putten, 1998; Zhou, 2001; Zhao et al., 2004). Some
studies have indicated that the effects of sand burial on plants may change with the depth of burial (Sykes and
Wilson, 1990; Brown, 1997). Low levels of burial tend to stimulate plant growth, but high levels of burial are
inhibitory (Brown, 1997; Maun, 1998). Therefore, there is a threshold of sand burial that maximizes a plant’s vigor.
Below a certain threshold level of burial, the growth of plant species is stimulated by sand burial in terms of plant
height and biomass (Zhang et al., 2002; Ma et al., 2007). As the level of burial increases over the threshold, the
response of plants might deteriorate in terms of growth and vigor until survival is impossible (Maun, 1998; Yang et
al., 2007). However, so far, the physiological adaption mechanisms of plants to sand burial are not clear because
few studies have tested for physiological changes in plants affected by sand burial (Wang et al., 2012; Zhao, 2012).
Artemisia halodendron is a very important sub-shrub species in the deserts of China and is widely distributed in
the country’s northern semi-arid regions (Horqin Sand Land, Maowusu Sand Land, Hulunbeir Sand Land, and
Songnen Sand Land). A. halodendron is a preferred plant in local biological sand-fixing projects because it is strongly
adapted to the dune environment (Zhao et al., 2004; Zhao, 2012). The objectives of this paper are: (1) to examine
changes in survival rate, plant height, osmotic regulation substances, protective enzyme activities, and membrane
permeability of A. halodendron at different sand burial depths; and (2) to analysis the ability and mechanism of A.
halodendron as a psammophyte to withstand sand burial.
2 Material and methods
2.1 Study area
The study area is located in Naiman County (42°15'N, 120°42'E, 345 m a.s.l.), within the Horqin Sandy Land in
the eastern part of Inner Mongolia, China. This region is characterized by a temperate continental semi-arid
monsoon climate regime in the temperate zone. Mean annual precipitation is 364 mm, mean annual potential
evaporation is 1,920 mm, and mean annual temperature is 6.3 °C. The annual frost-free period is approximately
141 days. The average annual wind speed is 3.4–4.5 m/s and mean wind speed in the wind erosion season (spring)
is 5.0–6.0 m/s. The landscape in this region is characterized by dunes alternating with lowland areas. Most of the
lowland area is reclaimed cropland and the dunes are used for pasture. The soils are identified as degraded sandy
Chestnut soils according to the Chinese soil classification system, which are equivalent to Orthi-Sandic Entisols in
the FAO-UNESCO system. The sandy soil consists mainly of coarse sand and silt. The natural vegetation consists
mainly of A. halodendron, Caragana microphylla, Lespedeza davurica, Agriophyllum squarrosum, Setaria viridis,
and Corispermum marocarpum (Zhao et al., 2004).
2.2 Experimental design
A field experiment was conducted from April to August in 2010. The experiment was set up in a water balance
3
field of the Naiman Desertification Research Station (NDRS) in the Chinese Ecosystem Research Network, which
consisted of a number of 2m×2m×2m bottomless cement pools filled with sandy soil. Seeds of A. halodendron
were collected in August 2009 from sand dune areas near NDRS. The seeds were sown in the pools in rows 20 cm
apart in April 2010. After germination, the seedlings were thinned out to avoid death due to competition. One
hundred seedlings having similar growth were left and marked in each cement pool. The seedlings were kept vertical after thinning, and the average height for the seedlings in mid-May, when they were buried in sand, was 8.0 ±
0.2 cm. There were 10 burial treatments: buried to 0% (CK, no burial), 25% (A), 50% (B), 75% (C), 100% (D),
125% (E), 150% (F), 175% (G), 200% (H), and 225% (I) of seedling height. Every treatment consisted of four
replicates, and there were 40 cement pools in total. Unmarked seedlings that emerged after sand burial were removed. No additional water or fertilizer were added at any time during the experiment, in order to keep the soil
condition as close to natural conditions as possible.
2.3 Data collection and analysis
At 10 days of sand burial, leaves from 10 live seedlings were sampled randomly in each treatment to measure
enzyme activities (SOD, POD, and CAT), lipid peroxidation, and membrane permeability (measured in terms of
MDA content and REL (relative electric conductivity)), as well as content of osmotic substances (soluble sugar and
free proline) (Zhang and Zhai, 2003). The survival rate, plant height, and aboveground biomass were measured in
August, 2010.
All data were analyzed using the SPSS program for Windows v. 11.5. Multiple-comparison and one-way
analysis of variance (ANOVA) procedures were used to compare differences among the treatments. Least significant difference (LSD) tests were performed to determine pairwise significant differences among the treatment
means at P<0.05. Pearson correlation coefficients were used to evaluate relationships between the corresponding
variables.
3 Results
3.1 Changes in survival rate and seedling height
The survival rates of the seedlings fluctuated and decreased with increasing sand burial depth (Figure 1), decreasing by 48.9%–64.0% in treatments A to C compared with CK, but the differences between them were not significant (P>0.05). The survival rate diminished sharply when the burial depth exceeded 100% of seedling height,
decreasing 90.3%–96.9% in treatments E to H compared with CK. Seedling height decreased gradually with increasing sand burial depth, and was significantly lower in all the sand burial treatments compared to CK (P<0.05)
except for treatment A.
Figure 1 Changes in survival rate (a) and height (b) of A. halodendron seedlings affected by sand burial. Bars represent means ± SD.
Values with the same letters are not significantly different at P<0.05
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3.2 Changes in RWC, MDA, membrane permeability
Leaf relative water content (RWC) fluctuated and decreased with increasing burial depth, and was lower in all
the sand burial treatments than in CK except for treatment F (Figure 2), but the differences between them were not
significant (P>0.05) except for treatment E. In comparison with CK, MDA content was significant lower in all the
sand burial treatments (P<0.05) except for treatments F and A, where it was higher. Membrane permeability first
decreased and then increased with increasing burial depth, being lower in treatments B and C and significantly
higher in treatments D to H compared to CK (P<0.05).
Figure 2 Changes in FWC (a), MDA (b), and membrane permeability (c) of A. halodendron seedlings affected by sand burial. Bars
represent means ± SD. Values with the same letters are not significantly different at P<0.05
3.3 Changes in activities of protective enzymes
The activities of SOD, POD, and CAT all fluctuated violently with increasing sand burial depth (Figure 3). In
comparison with CK, SOD activity was lower in all the sand burial treatments, except that it was significantly higher in
treatments D and E (P<0.05). POD activity was higher in all the sand burial treatments except for treatment D. CAT
activity was significantly higher in treatments C and D and significantly lower in treatment E compared with CK
(P<0.05). Although CAT activity was lower in the other sand burial treatments than in CK, the differences were not
significant (P>0.05).
Figure 3 Changes in activity of SOD (a), POD (b), and CAT (c) in A. halodendron seedlings affected by sand burial. Bars represent
means ± SD. Values with the same letters are not significantly different at P<0.05
3.4 Changes in free proline and soluble sugar
Free proline content fluctuated and increased with increasing depth of sand burial (Figure 4). The free proline
content was significantly higher in treatment C and in treatments F to H compared to CK, while the difference was
not significantly different from CK in the other treatments (P>0.05). The soluble sugar content also fluctuated with
increasing sand burial depth. The differences were not significant in most treatments compared to CK (P>0.05),
except for significantly lower levels in treatments B, C, and F.
Figure 4 Changes in proline (a) and soluble sugar (b) affected by sand burial. Bars represent means ± SD. Values with the same
letters are not significantly different at P<0.05
3.5 Correlation analysis for biological characteristics
The results from the correlation analysis showed that survival rate and seedling height had a positive correlation with RWC and a negative correlation with MDA content and membrane permeability (Table 1), but the correlation only reached a significant level between survival rate, height, and membrane permeability (P<0.05). MDA
content had a negative correlation with free proline, soluble sugar, and CAT activity, and a positive correlation with
5
SOD and POD activities, but none of the correlations reached a level of significance (P>0.05). Membrane permeability had a positive correlation with SOD and POD and a negative correlation with CAT, but the correlations
again did not reach the level of significance (P>0.05).
Table 1 Correlation analysis among plant growth properties and physiological indices
Item
Survival rate
Height
Proline
Sugar
SOD
CAT
POD
Height
0.844**
1
Proline
−0.446
−0.441
1
Sugar
0.191
0.195
0.379
1
SOD
−0.081
−0.134
0.708*
0.31
1
CAT
0.28
0.063
0.454
0.155
0.189
1
POD
−0.355
0.173
−0.451
−0.751*
−0.322
−0.690*
1
MDA
−0.221
−0.173
−0.024
−0.548
0.445
−0.289
0.504
MP
−0.771*
−0.825**
0.512
0.085
0.520
−0.284
0.106
RWC
0.443
0.335
0.051
−0.294
0.491
0.277
−0.036
*: P<0.05; **: P<0.01; MP: membrane permeability.
MDA
MP
1
0.400
0.526
1
−0.170
4 Discussion and conclusion
4.1 Effects of sand burial on survival and growth of A. halodendron
In desert areas, sand burial is one of the most important factors affecting plant survival and growth, but the
abilities of different plants to withstand sand burial have obvious differences (Brown, 1997; Li and Zhao, 2006).
For example, in two studies Sophora moocrofiana and Bromus inermis seedlings all died when the sand burial
depth was 100% of seedling height (Yang et al., 2007; Wang et al., 2011), while Hedysarum leave and Caragana
microphylla seedlings all died only when the burial depth was 133% of the seedlings’ height (Zhang et al., 2002;
Zhao et al., 2010). In comparison with these plants, A. halodendron seedlings had a stronger ability to withstand
sand burial and some seedlings still survived until the burial depth was 225% of seedling height.
The stronger ability of A. halodendron to withstand sand burial can be attributed to its unusual properties. A.
halodendron, as a psammophytic sub-shrub, is a pioneer species in sandy vegetation succession and is naturally
distributed in semi-moving sand lands and the lower parts of moving dunes, and has developed characteristics of
drought tolerance, barren resistance, and sand resistance in its long-term natural selection and adaptation process to
the aeolian environment (Li, 1994; Zhao et al., 2004). However, its responses in terms of seedling survival and
growth after sand burial showed significant differences. In comparison with CK, the survival rate decreased by
90.3%–96.9% once the buried depth exceeded 100% of the seedling height, while seedling height only decreased
by 44.7%–68.4%. These results suggest that even with the psammophyte, whose survival and growth could be
inhibited by severe sand burial, sand burial had a greater effect on survival than height of growth (Shi et al., 2004;
Zhao et al., 2004; Zhao, 2012).
Previous studies have shown that with increased depths of sand burial, soil moisture, and soil harnessing increased and soil temperature in the rhizosphere decreased (Zhang et al., 2002; Yang et al., 2007). The present study
showed that, unlike drought stress and salt stress, changes in leaf RWC in A. halodendron were not significant,
suggesting that the major mechanism inhibiting the survival and growth of the seedlings after complete sand burial
was not water stress (Maun, 1998; Yang et al., 2007; Wang et al., 2012). According to the analysis, when subjected
6
to complete burial in sand, increased mortality and growth inhibition of the seedlings resulted mainly from two
reasons. First, a deep burial depth may prevent seedlings from re-emerging above the sand because pre-emergence
mortality results from a cessation of seedling growth before it can reach the soil surface (Li and Zhao, 2006; Wang
et al., 2012). Second, even after emerging from complete sand burial, decreased leaf area and reduced photosynthesis may render the substance and energy obtained by the seedlings insufficient to meet their growth needs
(Zhang et al., 2002; Yang et al., 2007).
4.2 Physiological response of A. halodendron seedlings to sand burial
Previous studies suggested that when subjected to drought, cold, or high temperature stress, the balance between generating and clearing reactive oxygen was destroyed in the cells, causing overproduction of reactive
oxygen and lipid peroxidation, and resulting in MDA accumulation and increased membrane permeability (Monk
et al., 1989; Zhou and Wang, 1999; Zhou et al., 2004). This enhancement in membrane lipid peroxidation was one
of the most important mechanisms causing cell membrane oxidative damage and cell death (Bai et al., 2006; Wang
et al., 2012). The present results showed that the MDA content was significantly lower in the partial sand burial
treatments compared to CK, but membrane permeability did not increase significantly. After being subjected to
complete sand burial, MDA content was still lower in most the treatments compared to CK, except for being higher
in treatment F, while membrane permeability increased significantly with increased depth of burial. These results
suggest that partial burial with sand did not cause lipid peroxidation and cell membrane damage (Zhou, 2001;
Hernández and Almansa, 2002; Chen et al., 2011). Although complete burial with sand did not result in an overt
accumulation of MDA, membrane permeability increased significantly and cell membrane damage was exacerbated with increasing burial depth (Shanahan et al., 1990; Zhou and Wang, 1999; Wang et al., 2012).
The correlation analysis showed that the survival rate and height growth of the seedlings had a significant
negative correlation with changes in membrane permeability, but no significant correlation with changes in MDA
content. This suggests that when subjected to sand burial stress, increased mortality and growth inhibition of the
seedlings should be attributed to membrane damage instead of to membrane peroxidation (Shanahan et al., 1990;
Zhou, 2001). Usually, when subjected to drought, salt, and higher temperature stress, membrane permeability and
MDA content always increase synchronously; the increased mortality and growth inhibition are seen have a significant correlation with both membrane permeability and MDA content (Hernández and Almansa, 2002; Bai et al.,
2006; Chen et al., 2011).
The present results were obviously different from past study results on drought, salt, and higher temperature
stress. One reason may be that drought, salt, and higher temperature stress normally resulted in water stress, which
primarily produced an imbalance between generating and clearing reactive oxygen, with a resulting overproduction
of reactive oxygen and lipid peroxidation (Shanahan et al., 1990; Chen et al., 2011). In contrast, plant RWC did not
significantly increase when subjected to sand burial stress and sand burial did not produce water stress in the
seedlings (Wang et al., 2012; Zhao, 2012). According to the analysis, when a plant is subjected to complete sand
burial, a major mechanism causing decreased MDA content is that the darkness, hypoxia, and low temperature
inhibit production of oxygen free radicals and membrane lipid peroxidation (Zhao, 2012; Wang et al., 2012). As to
why membrane permeability increases in the absence of membrane lipid peroxidation or MDA accumulation, that
feature has yet to be studied further.
7
Many studies have indicated that plants evolve enzymatic coping mechanisms under conditions of long-term
environmental stress. SOD, POD, and CAT, as well as high levels of other anti-oxidative enzymes, may contribute
to withstanding environment stress by increasing their capacity to mount a better protection against oxidative
damage. Thus, anti-oxidative enzymes are usually considered to be critical factors related to stress tolerance (Zhou
and Zhao, 2004; Li et al., 2005; Li et al., 2006; Gao et al., 2008; Wang et al., 2012). The present results showed the
activities of three anti-oxidant enzymes all fluctuated. In general, POD activity increased when the activities of the
SOD and CAT decreased, and SOD and CAT activities increased when POD activity decreased. Compared with
CK, SOD activity was significantly lower in all sand burial treatments except for treatments D and H, POD activity
was higher in all sand burial treatments except treatment D, and CAT activity showed no significant changes with
any of the sand burial treatments except for being elevated in treatments C and D.
Correlation analysis showed that POD activity had a negative correlation with SOD and CAT activities, with
the correlation between POD and CAT reaching a significant level. MDA content had a positive correlation with
SOD and POD and a negative correlation with CAT. These results suggest that when subjected to sand burial stress,
although there was a complementary interplay among the three enzymes, POD played a central role and SOD and
CAT played supporting roles in scavenging active oxygen and minimizing cell membrane damage (Bai et al., 2006;
Wang et al., 2012). This result was not in agreement with other study results on drought, salt, and higher temperature stress. When subjected to severe water stress, the activities of SOD, POD, and CAT usually all decrease
significantly. However, one kind of enzyme activity is always enhanced when these plants were subjected to severe
sand burial stress, which may be an important mechanism by which A. halodendron, as a psammophyte, inhibits
lipid peroxidation under conditions of sand burial stress.
The present results show that when subjected to partial burial with sand, free proline content showed no significant changes and the soluble sugar content decreased significantly compared to CK. After sand burial exceeded
the seedling height, the free proline content increased significantly; the difference from CK did not reach a significant level, although the soluble sugar content increased. Osmotic adjustment is an important function in stress
resistance (Demiral and Türkan, 2005; Trovato et al., 2008). Free proline and soluble sugar accumulation in leaves
under stress conditions is of the utmost importance for plant adaptation during stress (Alia et al., 2001; Wang et al.,
2012). The results suggest that when subjected to the severe stress of sand burial, proline plays a major role and
soluble sugar fails to play an effective role in the osmotic adjustment process (Demiral and Türkan, 2005; Bai et al.,
2006).
Acknowledgments:
The authors are grateful to the anonymous reviewers for their critical review and comments on drafts of this
manuscript. This research was funded by the Chinese National Fund Projects (Nos. 31270752 and 30972422) and
by a Chinese National Support Project of Science and Technology (No. 2011BAC07B02-06).
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