Research articleUnderlying mechanism on source-sink carbon balance of grazed perennial grass during regrowth: Insights into optimal grazing regimes of restoration of degraded grasslands in a temperate steppe
Graphical abstract
Introduction
The grassland biome is the largest terrestrial ecosystem; it covers 40% of the world's land area and accounts for 34% of the terrestrial organic carbon (C) stock (Zhou et al., 2018). China's grasslands are an important component of the world's grassland biome, it may play an important role in China's terrestrial C cycle and C sequestration because of its large extension (accounting for 41.7% of the country's land area and 12% of the world's grassland area) and the potential of C stock (Fang et al., 2010).Grazing is a primary land use in China's grassland, and exerts complex effects on plant growth. Grazing directly changes individual plants by removing photosynthetic tissues and changing above- and belowground C allocation, and also affects plants indirectly by changing soil nutrient cycling, canopy openness, and light acquisition (Benot et al., 2019). However, most of China's temperate grasslands are suffering from overgrazing, which has led to widespread degradation and productivity reduction in this ecosystem (Liu et al., 2019a; Niu et al., 2019). The restoration of degraded grasslands depends on optimal grazing regimes that promote rapid compensatory regrowth of the grazed plants and beneficial interactions among the components of the grassland ecosystem (Dong et al., 2020). A plant's ability to survive grazing and continue to develop is an essential mechanism of grazing tolerance, which depends on C fixation, redistribution of C reserves, and development of physiological regulatory mechanisms (Grogan and Zamin, 2018; Liu et al., 2019b). Therefore, knowledge of the compensatory growth and C allocation responses by grazed plants over a range of grazing intensity is required to support the development of sustainable grazing management, particularly in semi-arid grasslands (Tahmasebi et al., 2020).
Plant photosynthetic C fixation and allocation among tissues play important roles in the allocation of photoassimilate to above- and belowground biomass and in ecosystem C cycles (Wang et al., 2019a). The C allocation of plants is driven by C fixation through photosynthesis, and grazing affects photosynthetic C fixation and subsequent C allocation directly by changing photosynthetic and physiological traits, for example the net photosynthetic rate (Pn) increased under moderate grazing but decreased with increasing grazing intensity (Poorter et al., 2012; Liu et al., 2019b; Shen et al., 2019).. Though the effects of grazing on photosynthesis of grassland plants have been described, there is still limited understanding of how C fixation changes. This is an important knowledge gap, since C fixation is the key source of C input in grassland ecosystems, and the mechanisms of its responses to different grazing intensities determine the sustainability of grazing.
C allocation patterns within the perennial grass biomass determine not only plant growth but also the plant's vulnerability to disturbance (e.g., grazing), as they determine the amount of C that is cycled and sequestered by a grassland (Palacio et al., 2020). Grazing could be a decisive factor in determining the change of tissues from a C source to a sink and the C re-allocation between above- and belowground biomass (Hafner et al., 2012). Previous studies usually used a mass-balance approach to estimate the biomass-based C allocation between plants and the soil, but allocation of recently fixed C and non-structural carbohydrates (NSCs) among plant tissues drives long-term biomass accumulation and turnover of C pools (Wu et al., 2010; Wei et al., 2016; Wilson et al., 2018; Weber et al., 2019). Isotope tracer techniques (e.g., 13C) offer a suitable method for quantifying and tracing C flows in terrestrial ecosystems, and this technique has been applied in grasslands and forests (Karlowsky et al., 2018; Mou et al., 2018; Zong et al., 2018). Although previous studies found changes in the dynamics of recently fixed C of grass in temperate grasslands, we still don't fully understand the changes in C fixation and C allocation patterns under different grazing intensities (Wang et al., 2007, 2019abib_Wang_et_al_2007bib_Wang_et_al_2019a). Therefore, determining the C allocation by grassland plants and how this allocation responds to different grazing intensities are of great significance to support the evaluation of C budgets in semi-arid steppes.
Plant C allocation among tissues and physiological processes (growth, storage, and metabolism) allow plants to flexibly meet their demands for resources, especially under C limitation conditions such as those created by grazing (Hussain et al., 2020). The carbohydrates, and especially NSCs (mainly soluble sugars and starch), are supplied from photosynthetic source leaves and function as main substrates in all physiological processes, including transport to sink organs (e.g., roots, stems) to support plant growth and stress adaptation (Rennie and Turgeon, 2009; He et al., 2020). Defoliation by grazing changes source organs to sinks during leaf regrowth, thereby creating imbalances within plants that activate re-allocation of NSC reserves (D'Andrea et al., 2019). Reconfiguration of stored NSCs (e.g., conversion of starch to sucrose) provides important energy that supports rapid recovery of damaged photosynthetic tissues and growth of new leaves (Martinez-Vilalta et al., 2016). Once a new leaf is sufficiently mature to perform net photosynthesis, it changes from a C sink to a source organ (Benot et al., 2019; Guo et al., 2020). In addition, close coordination between photosynthetic activity of source leaves and C demand of sink tissues revealed decreasing Pn combined with decreased C demand by sink organs and NSC accumulation in source leaves (Andersen, 2003; Franck et al., 2006). The source–sink relationship in plants changes because of different response mechanisms under different levels of stress (e.g., drought), but the C fixation and NSC allocation patterns caused by a source–sink imbalance under the C limitation induced by grazing remain unclear (Schöenbeck et al., 2020).
Sucrose is the main NSC form, and is transported over long distances between source and sink organs. However, this involves the conversion of starch to sucrose, since starch is relatively immobile (Wang et al., 2020). Sucrose metabolism is catalyzed by sucrose phosphate synthase (SPS) and sucrose synthase (SS), which both participate in regulatory cycles for the breakdown or synthesis of starch and sucrose from hexoses in different plant tissues (Padhi et al., 2019). Defoliation can affect SPS and SS activities, thereby changing the initial NSC allocation for regrowth, and severe leaf removal results in a low source to sink ratio and increases expression of SPS-related genes (Silva et al., 2017; Mesejo et al., 2019). These findings suggest that source–sink relationships can be modulated by SPS and SS, depending on the amount of stored sucrose and starch, and that a grazing intensity threshold might exist, above which NSC reserves are not used for regrowth (Meuriot et al., 2018). The regulation of the source–sink balance by SPS and SS has been investigated during fruit ripening and grain filling, but the responses of these enzymes to NSC allocation and source–sink dynamics under different grazing intensities is not yet clear.
Plant hormones are involved in a wide range of plant physiological and developmental processes that regulate growth, NSC metabolism, and stress defenses (Savchenko et al., 2019). Recent studies found that abscisic acid (ABA), salicylic acid (SA), and jasmonate are key components of signaling paths that regulate sucrose accumulation and photosynthesis under stress (La et al., 2019; Havko et al., 2020). Regulation of the source–sink balance by plant hormones has been explored in crops and model plants by promoting the growth of sink tissues (e.g., leaves, grains, fruits) to build a large sink to promote C utilization and facilitate C assimilation (Giannopoulos et al., 2019; Wang et al., 2019b). These results indicate that plant hormones can potentially modulate C fluctuations by affecting supply and demand relationships in grazed plants to promote rapid recovery, and understanding these hormones may provide new insights into the regulatory mechanisms involved in stress adaptation.
Inner Mongolia's steppes are typical temperate semi-arid grasslands in northern China, and the dominant Stipa grandis P.A. Smirn. contributes most to the ecosystem's productivity, functions, and C stock (Bai et al., 2004; Yang et al., 2019a). Stipa grandis (abbreviation is S. grandis) is an important perennial bunchgrass species in this area, as it can monopolize the available resources and survive well in a competitive environment, such as under grazing (Liu et al., 2018). To improve our understanding of how this perennial grass recovers under different grazing intensities (light, medium, heavy, and grazing exclusion), we conducted a field experiment to examine the C fixation and allocation by S. grandis by using 13CO2 labeling, and to evaluate the effects of source–sink relationships on NSC metabolism through regulation of sucrose enzymes and plant hormones. We hypothesized that (1) moderate grazing of S. grandis would promote 13C allocation to the aboveground biomass to support regrowth by improving photosynthetic C fixation, but medium and heavy grazing may inhibit C fixation and trigger C storage of roots; (2) increased sink demand by S. grandis (i.e., growing new leaves) during recovery would promote C fixation of the old source leaves and rapid transport of NSCs from old leaves, stems and roots to sink organs; and (3) the regulation by plant hormones and sucrose enzymes would increase NSC storage in the roots of S. grandis with increasing grazing intensity.
Section snippets
Study site and experimental design
The study was conducted at the Grassland Ecosystem Research Station (Chinese Academy of Agricultural Sciences) in a typical grassland (natural grassland) of Xilinhot, Inner Mongolia Autonomous Region, China (43°38′N to 44°49′N, 116°42′E). The mean annual temperature is 0.3 °C, with mean monthly temperatures ranging from 38.5 °C in August to −21 °C in January, and mean annual precipitation is 346 mm, with 60–80% falling from May to August (Bai et al., 2010). We conducted the study in 2017, in a
Leaf gas-exchange parameters
The leaf gas-exchange parameters of S. grandis differed significantly among the three grazing intensities and one control experiment (Fig. 1). Pn increased significantly in LG compared with the control in all seasons (Fig. 1a), and was significantly higher than in the other treatments on all three measurement dates. In addition, it was lower in MG and HG than in the control in all seasons. gs was significantly higher than in the control in June and August in LG and on all three dates in HG,
Response of C fixation and assimilation to grazing intensity
C fixation through photosynthesis is a crucial process and can reflect how plants adapt to external factors, including defoliation by leaf removal (Gomez-Gallego et al., 2020). The Pn of S. grandis increased from July to August, suggesting gradual recovery of growth during the regrowth period. The plants maintained high Pn in LG at all times, which suggested that S. grandis could assimilate more photosynthetic C during the regrowth period under light grazing stress. Defoliation reduces
Conclusions
Our results indicate that the increasing sink demand induced by grazing in a perennial grass growing in a temperate grassland can alter photosynthetic C assimilation, C partitioning, and reallocation of NSC reserves by regulating SPS and SS activity and plant hormones. We confirmed our hypothesis that within the grazing intensity gradient, light grazing represented a threshold that promoted C fixation and assimilation by increasing the photosynthetic capacity of source leaves of S. grandis in a
Authors’ contributions
J. G., X. L., and Y. D. planned and designed the research. Z. Z., B.W., J. S., M.L. and B.Y. performed most of the fieldwork. Z.Z. conducted most of the laboratory experiments. J.G. and Z.Z. analyzed data and wrote the manuscript. All authors contributed critically to the drafts and gave final approval for publication. The authors declare no conflicts of interest.
Credit author statement
Zihe Zhang: Investigation, Data curation, Formal analysis, Writing - original draft; Writing - review & editing. Jirui Gong: Conceptualization, Methodology, Resources, Writing-Review and Editing, Supervision, Project administration, Funding acquisition. Xiaobing Li: Conceptualization, Methodology, Project administration. Yong Ding: Resources, Conceptualization, Methodology. Biao Wang: Investigation. Jiayu Shi: Investigation. Min Liu: Investigation. Bo Yang: Investigation.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
This study was supported by the National Natural Science Foundation of China, China (Grant No. 41571048), the Key National Research & Development program of China, China (Grant No. 2016YFC0500502), and the State Key Research and Development Plan of China (973 Program), China (Grant No. 2014CB138803).
References (110)
- et al.
Maize roots and shoots show distinct profiles of oxidative stress and antioxidant defense under heavy metal toxicity
Environ. Pollut.
(2020) - et al.
Spectrophotometric total reducing sugars assay based on cupric reduction
Talanta
(2016) - et al.
Grazing intensity modulates carbohydrate storage pattern in five grass species from temperate grasslands
Acta Oecol.
(2019) - et al.
Plant–microbe interactions to probe regulation of plant carbon metabolism
J. Plant Physiol.
(2006) - et al.
Effects of yak and Tibetan sheep trampling on soil properties in the northeastern Qinghai-Tibetan Plateau
Appl. Soil Ecol.
(2019) - et al.
Cadmium induced changes in carbohydrate status and enzymes of carbohydrate metabolism, glycolysis and pentose phosphate pathway in pea
Environ. Exp. Bot.
(2007) - et al.
Enhancing sustainability of grassland ecosystems through ecological restoration and grazing management in an era of climate change on Qinghai-Tibetan Plateau
Agric. Ecosyst. Environ.
(2020) - et al.
Effects of water stress and light intensity on chlorophyll fluorescence parameters and pigments of Aloe vera L
Plant Physiol. Biochem.
(2016) - et al.
Spatial variation in soil available water holding capacity alters carbon mobilization and allocation to chemical defenses along jack pine stems
Environ. Exp. Bot.
(2020) - et al.
Interaction of fertilization and soil water status determine C partitioning in a sedge wetland
Soil Biol. Biochem.
(2019)
Antagonistic shifting from abscisic acid- to salicylic acid-mediated sucrose accumulation contributes to drought tolerance in Brassica napus
Environ. Exp. Bot.
Cultivar variation in hormone- and sugar-response reveals abscisic acid-responsive sucrose phloem loading at the early regenerative stage is a significant determinant of seed yield in Brassica napus
Environ. Exp. Bot.
Seasonal and diurnal patterns of non-structural carbohydrates in source and sink tissues in field maize
BMC Plant Biol.
Interplay between hormones and assimilates during pear development and ripening and its relationship with the fruit postharvest behaviour
Plant Sci.
The flower to fruit transition in citrus is partially sustained by autonomous carbohydrate synthesis in the ovary
Plant Sci.
Spatial distribution and dynamics of sucrose metabolising enzymes in radiation induced mutants of sugarcane
Plant Physiol. Biochem.
Investigating and modelling the morphological plasticity of weeds
Field Crop. Res.
Characterization of high-yielding rice cultivars with different grain-filling properties to clarify limiting factors for improving grain yield
Field Crop. Res.
Herbivory alters plant carbon assimilation, patterns of biomass allocation and nitrogen use efficiency
Acta Oecol.
Resilience in the functional responses of Axonopus affinis Chase (Poaceae) to diurnal light variation in an overgrazed grassland
Agric. For. Meteorol.
Stomatal and non-stomatal limitations are responsible in down-regulation of photosynthesis in melon plants grown under the saline condition: application of carbon isotope discrimination as a reliable proxy
Plant Physiol. Biochem.
Effect of clipping and shading on C allocation and fluxes in soil under ryegrass and alfalfa estimated by 14C labelling
Appl. Soil Ecol.
Grazing enhances plant photosynthetic capacity by altering soil nitrogen in alpine grasslands on the Qinghai-Tibetan plateau
Agric. Ecosyst. Environ.
Physiology of Leymus chinensis under seasonal grazing: implications for the development of sustainable grazing in a temperate grassland of Inner Mongolia
J. Environ. Manag.
Managing grazing intensity linked to forage quantity and quality trade-off in semiarid rangelands
Rangel. Ecol. Manag.
Nitrogen addition alters photosynthetic carbon fixation, allocation of photoassimilates, and carbon partitioning of Leymus chinensis in a temperate grassland of Inner Mongolia
Agric. For. Meteorol.
Glycine betaine reduces chilling injury in peach fruit by enhancing phenolic and sugar metabolisms
Food Chem.
Dynamics and allocation of recently photo-assimilated carbon in an Inner Mongolia temperate steppe
Environ. Exp. Bot.
Source–sink balance and carbon allocation below ground in plants exposed to ozone
New Phytol.
ABA-induced vegetative diaspore formation in Physcomitrella patens
Front. Plant Sci.
Ecosystem stability and compensatory effects in the Inner Mongolia grassland
Nature
Tradeoffs and thresholds in the effects of nitrogen addition on biodiversity and ecosystem functioning: evidence from Inner Mongolia Grasslands
Global Change Biol.
High temperatures change the perspective: integrating hormonal responses in citrus plants under co-occurring abiotic stress conditions
Physiol. Plantarum
Jasmonic acid regulation of the anti-herbivory mechanism conferred by fungal endophytes in grasses
J. Ecol.
TOR dynamically regulates plant cell-cell transport
Proc. Natl. Acad. Sci. U.S.A.
Sucrose metabolism at three leaf development stages in bean plants
Photosynthetica
Effect of vapor pressure deficit on gas exchange in wild-type and abscisic acid-insensitive plants
Plant Physiol.
Pyrophosphate-fructose 6-phosphate 1-phosphotransferase (PFP1) regulates starch biosynthesis and seed development via heterotetramer formation in rice (Oryza sativa L.)
Plant Biotechnology Journal
Drying times: plant traits to improve crop water use efficiency and yield
J. Exp. Bot.
Winter's bite: beech trees survive complete defoliation due to spring late-frost damage by mobilizing old C reserves
New Phytol.
Enzymes of sucrose and hexose metabolism in developing kernels of two inbreds of maize
Plant Physiol.
Molecular interactions between plants and insect herbivores
Annu. Rev. Plant Biol.
Ecosystem carbon stocks and their changes in China's grassland
Sci. China Life Sci.
Enzyme-mediated metabolism in nutritive tissues of galls induced by Ditylenchus gallaeformans (Nematoda: anguinidae)
Plant Biol.
Abscisic acid signaling in seeds and seedlings
Plant Cell
Soluble sugars mediate sink feedback down-regulation of leaf photosynthesis in field-grown Coffea arabica
Tree Physiol.
The fate of recently fixed carbon after drought release: towards unravelling C storage regulation in Tilia platyphyllos and Pinus sylvestris
Plant Cell Environ.
Hormone distribution and transcriptome profiles in bamboo shoots provide insights on bamboo stem emergence and growth
Plant Cell Physiol.
Exogenous classic phytohormones have limited regulatory effects on fructan and primary carbohydrate metabolism in perennial ryegrass (Lolium perenne L.)
Front. Plant Sci.
Cystoliths of Parietaria judaica can serve as an internal source of CO2 for photosynthetic assimilation when stomata are closed
J. Exp. Bot.
Cited by (7)
Correlations between root phosphorus acquisition and foliar phosphorus allocation reveal how grazing promotes plant phosphorus utilization
2024, Plant Physiology and BiochemistryPartitioning evapotranspiration and carbon flux in ungrazed and grazed tallgrass prairie
2023, Agriculture, Ecosystems and EnvironmentCitation Excerpt :Despite the reduction in AGB and GLAI caused by grazing (Fig. 2), similar cumulative GPP values at both paddocks suggest that there are compensatory mechanisms maintained similar CO2 assimilation at UG and GR. The regrowth of new leaves, which have greater stomatal conductance and photosynthetic capacity, associated with the higher penetration of solar radiation inside the canopy are the probable reasons for the higher carbon assimilation efficiency in grazed systems (Owensby et al., 2006; Zhang et al., 2021; Wang et al., 2011; Otieno et al., 2011). In addition, leaf regrowth probably contributed to maintaining similar T/ET at GR as the one at UG in the end of the growing season (Fig. 4d-f).
N addition rebalances the carbon and nitrogen metabolisms of Leymus chinensis through leaf N investment
2022, Plant Physiology and BiochemistryCitation Excerpt :The supernatant was collected after centrifugation as crude enzyme extract. The SPS and SS contents were then determined by means of the HCl–resorcinol method (as described in Section 2.5), and the absorbance was measured at 480 nm (Zhang et al., 2021a). We assayed the NR content using the sulfanilamide method of (Kim et al., 2021) and measured the absorption at 540 nm.
Multiple herbivory pressures lead to different carbon assimilation and allocation strategies: Evidence from a perennial grass in a typical steppe in northern China
2022, Agriculture, Ecosystems and EnvironmentCitation Excerpt :The δ13C value of leaves reached a peak on the first day after labeling and then sharply decreased (by 75.8%) within the first 7 days after labeling in all treatments. This sharp decrease resulted from transfer of new photoassimilates to the stems and roots (which showed subsequent increases in δ13C values, with a time delay of 1–2 days), respiration loss, and a dilution effect of CO2 assimilation or a mixing of recent photoassimilates with older carbon reserves in the leaves (Furze et al., 2019; Zhang et al., 2021). The δ13C value of the leaves was higher in LG than in the control, which was consistent with the high photosynthetic rate and carbon assimilation of L. chinensis under light grazing.
Nitrogen uptake and reallocation from roots drive the regrowth of a dominant plant in temperate grassland after low defoliation
2023, Biology and Fertility of Soils