Abstract
Background
The nonstructural carbohydrates (NSCs) of plants are posited to be crucial traits for the resistance and resilience of plants to climate change-induced drought and flooding. However, the potential effects of persistent drought and waterlogging on the dynamics of the NSCs and the underlying mechanisms are still poorly understood.
Methods
We measured the NSCs concentrations and pool size, photosynthetic rate and biomass of Robinia pseudoacacia L. seedlings for both 2015 and 2016 under five soil water treatments: 3%, 8%, 17%, 24% and 34% soil water content, representing extreme drought (ED), moderate drought (MD), the control group (CG), field capacity (FC) and waterlogging (WL) stresses, respectively. We observed the relationship between the pool size of NSCs and the survival of seedlings under water stress (drought and waterlogging) for 30 days in greenhouse.
Results
Compared with CG, the net photosynthetic rate decreased 91%, 67%, 34% and 71%, and the biomass decreased by 37%, 15%, 16% and 33% under ED, MD, FC and WL, respectively. The total NSC (TNSC) concentration was significantly increased by 154% under ED after 10 days and sharply decreased by 50% under ED after 30 days. The concentrations of soluble sugars (SS) were significantly increased by 100% under MD after 10 days and sharply decreased by 60% under ED after 30 days. Compared with GC, the response of NSCs, photosynthetic rate and biomass under ED were more dramatic than that under WL. The pool sizes of fructose and sucrose were larger under ED and WL, but the maximum pool size of starch occurred under the CG. The depletion of NSCs was not observed under ED at the end of the experiments in both 2015 and 2016.
Conclusions
Our results indicate that the dynamics of NSCs is an important physiological feature of plant adaptation and resistance to drought and waterlogging. In addition, high sugars concentrations are beneficial for the plants during the short-term extreme drought and the longer term mild drought or waterlogging.
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Background
Extreme event-induced tree mortality occurs globally and is likely to be exaggerated by future climate change, particularly drought and flood (Patz et al. 2005; Bréda et al. 2006; Huntington et al. 2006; Adams et al. 2009; Allen et al. 2010; Pachauri et al. 2014). As is well known, the events of extreme drought and floods will affect forest ecosystems along with rising temperatures, heat waves, and changing interactions between pests/pathogens and hosts (Bonan 2008; Allen et al. 2010). However, the underlying mechanisms of drought-induced tree mortality remain unclear (McDowell et al. 2008a, b; Sala 2009; Sala et al. 2010). In ideal condition over the time, tree mechanism is largely governed by the increasing stand level competition and social status on an individual tree (Saud et al. 2016, 2018), but under drought stress, trees are vulnerable to carbon starvation. Previous studies suggested that trees were vulnerable to carbon starvation under drought stress (Parker and Patton 1975; Bréda et al. 2006; McDowell et al. 2008a, b; Adams et al. 2009; Sala et al. 2010). However, there are the elusive and complex phenomena of nonstructural carbohydrates (NSCs) in plants in response to drought that are induced by different drought features (i.e., intensity and duration) and tree species, size, age and tissues (Sala et al. 2012; Hartmann et al. 2013; Palacio et al. 2014). Therefore, the lack of consensus among these studies on the effect of water availability on the NSC dynamics suggests that further studies are necessary to elucidate the underlying mechanisms (McDowell et al. 2008a, b; O’Grady et al. 2013).
Although studies on the effect of drought on NSCs is extensive, there has been few studies focusing on the effect of waterlogging (Board 2008; Parent et al. 2008; Nguyen et al. 2018). Sala et al. (2012) and Palacio et al. (2014) reported the manner in which we think about modeling tree growth and reviewed the literature on the minimum thresholds of nonstructural carbohydrates (NSC) under multiple environmental stresses. Some studies found that there was lack of direct evidence for the carbon-starvation hypothesis to explain water-induced mortality in plant (Sala 2009; Sala et al. 2010, 2012). Moreover, approximately 16% of land has been affected by waterlogging, resulting in severe economic losses (Luan et al. 2018). The assessment of the relationship between plant waterlogging and changes in NSCs concentration and allocation is very limited.
Some previous research suggested that different drought intensities induced different physiological responses of plants (Ditmarova et al. 2010; Osakabe et al. 2014) which may induce various NSC dynamics in trees to resist and survive under different water-stressed conditions (McDowell et al. 2008a, b). According to the previous hypothesis, mild drought stress may not result in the exhaustive depletion of NSCs, which may occur under severe drought stress, and trees may die from irreversible xylem cavitation (McDowell et al. 2011). However, there is a lack of research on the underlying mechanisms of NSC dynamics, particularly under drought (McDowell et al. 2008a, b) and waterlogging conditions.
In addition, not only drought intensity but also drought duration changes the NSC allocation and dynamics (McDowell et al. 2011). In the early stage of drought, the NSC concentrations may increase because the metabolic rate precedes the reduction in the photosynthetic rate (Korner 2003; Osakabe et al. 2014). However, as the drought stress persists, the reduction in the metabolic rate precedes that of the photosynthetic rate (Hsiao 1973; McDowell et al. 2011). Many previous studies focused only on the initial and final stage of the short-term drought manipulation (Regier et al. 2009, 2010; Anderegg and Anderegg 2013). Some previous studies also found that waterlogging as the dominant water stress within tree pits and thus avoidance of waterlogging conditions is required to stimulate increased tree growth (Grey et al. 2018; Ismail 2018). Therefore, it is necessary to understand how the duration of drought (McDowell and Sevanto 2010; Sala et al. 2010) and waterlogging (Sairam et al. 2008) changes the NSC dynamics in plants.
It has been demonstrated that different species have distinct functions and sizes of the NSC pool of different components (e.g., fructose, glucose, sucrose, starch, fructans and lipids) (Hoch et al. 2003; Würth et al. 2005; Millard et al. 2007; Palacio et al. 2014). Recently, there have been studies on the drought-induced allocations in carbon assimilation, transport, and utilization between the above- and below-ground tree tissues (Day et al. 2009; Li et al. 2013a, 2017); 2) We primarily studied the partitioning and dynamics of the TNSC, SS, starch, fructose, glucose and sucrose concentrations on the whole-tree scale. The change status did not use isotope techniques to accurately reveal the NSC allocation mechanisms; 3) we measured photosynthesis and biomass as covariates to clarify the NSC dynamic mechanisms without combining hydraulic characteristics. We should combine carbon starvation with hydraulic failure to explore the response of the trees to drought and waterlogging to understand possible mechanisms, and further research on this direction is urgently needed.
Conclusions
The main conclusions of this study are as follows: 1) the intensity and duration of soil water stress have significant effects on the NSC dynamics of Robinia pseudoacacia seedlings. 2) We observed a significant decrease in NSC concentration under severe drought stress, and the NSC concentration under MD and FC remained high levels. The NSC concentration under WL conditions recovered near the initial value. 3) Drought causes seedlings to preferentially increase NSC in below-ground tissues. While FC and WL can promote the distribution of NSCs mainly in the above-ground tissues. In summary, the dynamic characteristics (for strength and duration) and component types of NSCs in drought and waterlogged are important for elucidating the relationship between NSC dynamics and soil water stress. However, further research is needed to investigate the NSC dynamics during the dormant season, as well as the NSC allocation and storage characteristics of plant tissues under drought and waterlogging stress.
Abbreviations
- An :
-
The net photosynthetic rate
- ANOVA:
-
Analysis of variance
- CG:
-
Control group
- ED:
-
Extreme drought
- FC:
-
Field capacity
- Frc:
-
Fructose
- Glc:
-
Glucose
- HSWT:
-
High soil water treatment (including field capacity and waterlogging)
- MD:
-
Moderate drought
- RAB:
-
The ratios of above- and below-ground
- ROS:
-
Reactive oxygen species
- RSS:
-
The ratio of soluble sugars and starch
- SS:
-
Soluble sugars
- Sta:
-
Starch
- Suc:
-
Sucrose
- TNSC:
-
Total nonstructural carbohydrates
- WL:
-
Waterlogging
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Acknowledgements
We greatly appreciate the help of Dr. Yi Zhang on the implementation of our experiments and seedling culture and water control in the greenhouse.
Funding
This study was mainly funded by the National Key R&D Program of China (2016YFC0500203), Qian Ren program and the Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant. The National Natural Science Foundation of China (41571081) and the National Key R&D Program of China (2016YFC0501804). The National Natural Science Foundation of China (41601098) and the Young Excellence Program for the Teachers of the College of Forestry, Northwest A&F University (Z111021603).
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BY, CP and MW contributed conception and design of the study; BY organized the database; BY performed the statistical analysis; BY wrote the first draft of the manuscript; WL and MD revised the section of the manuscript. All authors contributed to manuscript revision, read and approved the submitted version.
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Additional file 1:
Figure S1. Air temperature. Figure S2. Air humidity. (DOCX 113kb)
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Yang, B., Peng, C., Zhu, Q. et al. The effects of persistent drought and waterlogging on the dynamics of nonstructural carbohydrates of Robinia pseudoacacia L. seedlings in Northwest China. For. Ecosyst. 6, 23 (2019). https://doi.org/10.1186/s40663-019-0181-3
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DOI: https://doi.org/10.1186/s40663-019-0181-3