Response of root nutrient resorption strategies to rhizosphere soil microbial nutrient utilization along Robinia pseudoacacia plantation chronosequence
Graphical abstract
Introduction
Nutrient resorption is the process whereby plant tissues or organs transfer a portion of their nutrients (such as nitrogen and phosphorus) to other living tissues before abscission (Freschet et al., 2010). This strategy is regarded as a key nutrient conservation mechanism that extends the retention time of nutrients within plants, increases nutrient utilization efficiency, and reduces plant dependence on soil nutrients (Brant and Chen, 2015, Peng et al., 2019). The translocation of nutrients between plants and soil is strongly dependent on the nutrient utilization efficiency of plant systems (Ehrenfeld et al., 2005). Furthermore, the nutrient loss rate of senesced organs is considered feedback to soil nutrient dynamics at the population level, whereas the concentration of nutrients in the remaining organs in turn affects the rate of decomposition and soil nutrient availability (Aerts, 1996, Freschet et al., 2010). The roots also play an essential role in plant–soil nutrient cycles (McCormack et al., 2015). Compared with leaves, however, considerably less is known regarding the variation in soil nutrient dynamics and resorption in fine roots. Therefore, it is important to examine the role of root resorption strategies in the utilization of nutrients by plants.
Plant succession typically has the effect of improving soil conditions and promoting ecosystem restoration (Chang and Turner, 2019). Root growth may drive further changes in the diversity and composition of microbial communities at different stages of restoration (Bonkowski et al., 2000, Blagodatskaya et al., 2010). For example, previous studies have clarified that the biomass of root exudates and the decomposition of senesced roots contribute to promoting the nutrient contents of rhizosphere soil and the growth and activity of microbes (Singh et al., 2007), whereas changes in rhizosphere soil nutrients such as C, N, and P have significant effects on soil microbial communities and the restoration of vegetation (Bell et al., 2014, Li et al., 2020). Furthermore, the ratios of microbial biomass to rhizosphere soil nutrients are considered indices of microbial nutrient utilization efficiencies (Zhang et al., 2018, Chen et al., 2020). Some studies found that the growth and metabolism of soil microorganisms regulate the efficiency of nutrient conversion between plants and soil (Guyonnet et al., 2018), which may affect the nutrient resorption properties of fine roots. Therefore, gaining an understanding of the coupling relationships between rhizosphere microbial nutrient utilization and root nutrient resorption strategies during the different stages of restoration can provide indirect insights into mechanisms underlying the response of root nutrient resorption to soil properties.
Robinia pseudoacacia is a perennial leguminous plant, the strong biological N2-fixing capacities of which are assumed to lead to a significant increase in the growth and nutrient metabolism of the plant rhizosphere N2-fixing flora with forest growth (He et al., 2016). Indeed, the planting and growth of R. pseudoacacia has been shown to alter the soil characteristics in hilly and gully areas, and indirectly affect the nutrient levels in senesced roots (Liu et al., 2018a). Furthermore, Ren et al. (2017) have clarified that changes in microbial biomass and community composition were sensitive to the variation in soil nutrients following afforestation. And numerous studies have clarified that changes in rhizosphere soil microbial communities can determine the efficiency with which plants utilize soil nutrients (Vale et al., 2005, Toberman et al., 2011). Some studies have also established that the nutrient utilization strategy of plants is closely associated with the nutrient resorption of senesced organs (Reed et al., 2012, Vourlitis et al., 2014). However, how the root nutrient resorption strategies of plants respond to the nutrient utilization of the rhizosphere soil microbial population remains unclear.
To illustrate how changes in the nutrient utilization efficiency of rhizosphere soil microorganisms can affect nutrient resorption by the roots of R. pseudoacacia in the Loess Plateau, China, we examined root nitrogen and phosphorus resorption efficiencies (NRE and PRE, respectively), soil nutrient contents, the diversity and composition of bacterial and fungal communities, and microbial biomass. Firstly, it is shown that plant tissues or organs maintain a relative balance of nutrient absorption and transfer during growth (Guyonnet et al., 2018). This helped us to test a hypothesis that the responses of root NRE and PRE would be strongly dependent on vegetation stages, which can be attributed to the strategies of nutrient resorption. Secondly, it is also reported that the increase of rhizosphere soil microbial nutrient use efficiency enhanced the uptake of available nutrients by plant fine roots (Ren et al., 2017, Liu et al., 2018a), which may weaken the resorption efficiency of nutrients by plant senesced roots. Based on this, we also hypothesized that the nutrient-use efficiency of rhizosphere soil microbes negatively drives root nutrient resorption. The objectives of the study were to (i) quantify the changes in root NRE and PRE with increasing stand age; (ii) examine the response of nutrient resorption efficiencies to rhizosphere soil nutrients; and (iii) clarify the response of root nutrient resorption strategies to rhizosphere soil microbial nutrient utilization at different stages of restoration.
Section snippets
Study area and sampling
The experimental sites were located at the Wuliwan watershed in the central region of the Loess Plateau, China (36°5113″–36°5218″N, 109°2053″–109°2127″E). The average annual precipitation of this area is 510 mm, with over 60% falling from July to September. The annual average temperature, number of hours of sunshine, and frost-free period are 8.8 °C, 2415 h, and 157 days, respectively. The soil is mainly of a typical loess texture characterized by overall looseness (as judged by the FAO).
Changes in root nutrient resorption efficiency
The results showed that the nutrient resorption of R. pseudoacacia roots underwent significant changes with increasing stand age (Fig. 1). The contents of total nitrogen and phosphorus in live roots were significantly higher than those in dead roots. The ranges of total nitrogen (RTN) and phosphorus (RTP) contents in live roots were 22.89–25.91 and 2.17–2.38 g kg−1, respectively, compared with 9.80–12.55 and 1.08–1.23 g kg−1, respectively, in dead roots. Furthermore, the results showed that the
Changes in root nutrient resorption at different stages of restoration
In this study, we established that both root NRE and PRE initially underwent a significant decline but then subsequently increased during the progression of vegetation restoration (Fig. 1), which is consistent with our hypothesis. We can observe from our results that for root NRE and PRE, R. pseudoacacia showed similar strategies in response to changing stand age. Notably, both NRE and PRE had increased sharply at 45-year-old sites compared with the 30-year-old sites, thereby indicating that
Conclusions
In summary, we found that the restoration of R. pseudoacacia forest improved the nutrient contents of rhizosphere soil and the growth and nutrient metabolism of microbial communities. The rhizosphere soil microbial community was shown to respond positively to nutrient-use efficiency and soil nutrient availability. Moreover, the efficiency of root nutrient resorption showed a strong response to rhizosphere soil nutrient contents and microbial communities. Notably, our results showed that the
CRediT authorship contribution statement
Miaoping Xu: Data curation, Writing - original draft. Junnan Jian: Visualization, Investigation. Jiayi Wang: Writing - review & editing. Zhenjiao Zhang: Software, Validation. Gaihe Yang: Writing - review & editing. Xinhui Han: Conceptualization, Methodology, Software. Chengjie Ren: Supervision.
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
National Natural Science Foundation of China (No. 41877543), Natural Science Basic Research Project of Shaanxi Province (2019JM-211), Forest and Grass Technology Innovation Development and Research Project of the State Forestry and Grassland Administration (2020132111), Key project of Shaanxi Provincial Natural Science Foundation (2018JZ4002) and Shaanxi Engineering Research Center of Circular Agriculture (2019HBGC-13) financially supported this work. The authors especially thank Ansai field
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