Elsevier

Rhizosphere

Volume 9, March 2019, Pages 97-105
Rhizosphere

Light intensity controls rhizosphere respiration rate and rhizosphere priming effect of soybean and sunflower

https://doi.org/10.1016/j.rhisph.2018.12.002Get rights and content

Abstract

Rhizosphere respiration (Rroot) and rhizosphere priming effect (RPE) are crucial for regulating soil carbon dynamics. However, their responses to light intensity are not fully resolved. We investigated Rroot and RPE of soybean and sunflower using a continuous isotope-labeling technique. The two species were subjected to five levels of light intensity in a growth chamber. Plants were maintained at full light from seeding for 45 or 59 days, and switched to shading treatments for four days. Soil respiration was partitioned into root- and soil-derived CO2 during the last five days (day0, full light; day1–4, shading). Both soybean and sunflower Rroot showed significant positive relationships with light intensity, particularly after one day of shading. Moreover, both plants showed positive RPE (44–98%) at full light, but with increasing duration and intensity of shading, the RPE declined and even became negative (up to –20%). Indeed, a positive relationship between light intensity and RPE was observed in both species. Overall, our results showed that shading, by influencing light intensity and presumably photosynthesis rate and belowground carbon allocation, exerts a significant control of rhizosphere respiration rate and priming effect of the two species.

Introduction

Soil respiration plays a vital role in the global carbon cycle (Davidson and Janssens 2006) and it consists of rhizosphere respiration (autotrophic component) and microbial decomposition of soil organic matter (heterotrophic component) (Hanson et al. 2000; Ryan and Law 2005; Kuzyakov 2006). Rhizosphere respiration includes both root respiration and microbial respiration using root-derived substrates (Kuzyakov 2006), and accounts for up to 90% of soil respiration (Hanson et al. 2000). Therefore, rhizosphere processes are an important component of terrestrial carbon cycle, and the rhizosphere has long been recognized as a biogeochemical hotspot (Finzi et al. 2015). However, partitioning of soil respiration into autotrophic and heterotrophic components has been notoriously difficult (Hanson et al., 2000, Trumbore, 2006). Among the available methods, isotope-labeling techniques can provide non-destructive and least-biased measurement of rhizosphere respiration (Hopkins et al. 2013).

Light availability greatly affects plant growth and respiration (Merlo et al., 1994, Xie et al., 2018). Low light not only limits carbon availability for plant growth but also restricts the energy supply for essential metabolic processes (Pons and Poorter 2014). Additionally, substrate supply is one of the major factors regulating rhizosphere processes such as rhizosphere respiration and root exudation (Jones et al., 2004, Hopkins et al., 2013). For example, Craine et al. (1999) showed that variation in environmental factors (e.g. light intensity) that affect carbon availability to roots can be important determinants of soil CO2 efflux in a grassland ecosystem.

Previous studies have shown that soil respiration is not merely a function of soil temperature and moisture, but is also determined by photosynthetic assimilates supply (Bahn et al., 2009, Davidson et al., 2006, Trumbore, 2006). Many studies have explored the effect of aboveground substrate supply on belowground carbon cycle, using methods such as tree girdling, shading, defoliation, grazing and clipping (Bahn et al., 2013, Fu and Cheng, 2004, Hogberg et al., 2001, Subke et al., 2011, Jing et al., 2016, Zhang et al., 2018). Based on these studies, increasing evidence suggested that the supply of photosynthetic assimilates significantly affected both autotrophic and heterotrophic components of soil respiration (Bahn et al., 2009, Subke et al., 2009, Taneva and Gonzalez-Meler, 2011, Xu et al., 2008). Therefore, photosynthetic activity supplying carbohydrates from leaves to roots and rhizosphere microbes is a key driver of soil CO2 efflux (Hogberg and Read 2006). However, the responses of rhizosphere respiration to light intensity and photosynthesis rate are still not fully resolved (Hopkins et al. 2013). Improved understanding of the link between aboveground light intensity and photosynthesis rate and belowground carbon cycle processes will contribute to better understanding ecosystem carbon cycling and its feedback to climate change (Hogberg and Read, 2006, Kuzyakov and Gavrichkova, 2010).

As increasingly recognized, living roots may inhibit or stimulate soil organic matter decomposition, which is termed rhizosphere priming effect (Cheng et al., 2014, Zhu et al., 2014). Recent meta-analysis showed that the rhizosphere priming effect (RPE), on average, stimulated soil organic matter (SOM) decomposition by 59% above the rate of unplanted soil controls (Huo et al. 2017). The RPE can be as important as the effect of temperature and moisture on SOM decomposition (Zhu and Cheng 2011). Thus, it is crucial to understand the factors regulating RPE in order to predict terrestrial carbon cycle feedbacks to future climate change (Schmidt et al., 2011, Finzi et al., 2015). To date, many factors have been found to affect the magnitude and direction of RPE, including plant species and mycorrhizal types, soil types and characteristics, and environmental conditions (Cheng et al., 2014, Huo et al., 2017). However, most of the RPE experiments (Cheng et al., 2014, Huo et al., 2017) were determined under nearly constant-light conditions (Huo et al. 2017). It remains unclear how light intensity and photosynthesis rate control the magnitude and direction of RPE.

Our main objective was to investigate the impact of light intensity on rhizosphere respiration and priming effect. We chose two crop species – a legume soybean (Glycine max) and a non-legume sunflower (Helianthus annuus). These two species were commonly used in previous studies on rhizosphere processes (Table S4), which make the results of this study comparable to those of previous studies. We used shading cloth to create five levels of light intensity and investigated rhizosphere respiration rate and rhizosphere priming effect of these two species using a non-destructive, continuous isotope-labeling technique (Cheng and Dijkstra, 2007, Zhu et al., 2014). We hypothesized that both rhizosphere respiration rate and priming effect show positive relationships with light intensity, because light intensity affects aboveground photosynthesis rate and belowground carbon allocation which control rhizosphere processes. This is the first study of rhizosphere respiration and priming effect under multiple levels of light intensity, which can contribute to our understanding of the linkage between aboveground light intensity and photosynthate supply and belowground carbon cycle processes (i.e. rhizosphere respiration and priming).

Section snippets

Experimental setup

The experiment was conducted in a continuous 13C-labeling growth chamber at University of California, Santa Cruz. When the CO2 concentration inside the growth chamber dropped below 390 ppm, a pulse of 13C-depleted CO2 (−36.5‰) from a gas tank was injected into the growth chamber. During the experimental period, we maintained a constant CO2 concentration (400 ± 10 ppm) and δ13C value (–18.0 ± 0.5‰) inside the growth chamber by automatically adjusting the flow rate of CO2–free air and pure CO2

Plant biomass and δ13C content

Plants appeared healthy with no signs of pests and were flowering during the respiration measurement. Soybean shoot and root biomass were not significantly correlated with light intensity (Table 1, S1). However, sunflower biomass was positively related to light intensity (P < 0.05, Table 1, S1). These results suggest that the four-day shading had a larger impact on sunflower growth than on soybean growth. Moreover, root:shoot ratio showed a weak negative trend with light intensity for both

Discussion

We used shading cloths to create five levels of light intensity in a growth chamber, and measured rhizosphere respiration (Rroot) and priming effect (RPE) of soybean and sunflower in response to shading for five consecutive days (1 day before shading and 4 days after shading). We found that shading showed a significant negative impact on Rroot and RPE of the two species, particularly with extended time of shading (Fig. 5). These results showed that shading, by influencing light intensity and

Acknowledgments

This work was supported by the National Natural Science Foundation of China (31670525, 31622013 and 31621091), and the National Science Foundation (DEB-1354098). We are grateful to the editor (Dr. Sina Adl) and two anonymous reviewers for their insightful comments which improved the manuscript.

References (55)

  • T. Shahzad et al.

    Contribution of exudates, arbuscular mycorrhizal fungi and litter depositions to the rhizosphere priming effect induced by grassland species

    Soil Biol. Biochem.

    (2015)
  • T. Shahzad et al.

    Plant clipping decelerates the mineralization of recalcitrant soil organic matter under multiple grassland species

    Soil Biol. Biochem.

    (2012)
  • E.D. Vance et al.

    An extraction method for measuring soil microbial biomass C

    Soil Biol. Biochem.

    (1987)
  • H. Xie et al.

    Leaf non-structural carbohydrate allocation and C:n:p stoichiometry in response to light acclimation in seedlings of two subtropical shade-tolerant tree species

    Plant Physiol. Biochem.

    (2018)
  • X. Xu et al.

    Root-derived respiration and non-structural carbon of rice seedlings

    Eur. J. Soil Biol.

    (2008)
  • B. Zhang et al.

    Labile soil organic matter in response to long-term cattle grazing on sloped rough fescue grassland in the foothills of the Rocky Mountains, Alberta

    Geoderma

    (2018)
  • B. Zhu et al.

    Nodulated soybean enhances rhizosphere priming effects on soil organic matter decomposition more than non-nodulated soybean

    Soil Biol. Biochem.

    (2012)
  • B. Zhu et al.

    Rhizosphere priming effects on soil carbon and nitrogen mineralization

    Soil Biol. Biochem.

    (2014)
  • M. Bahn et al.

    Responses of belowground carbon allocation dynamics to extended shading in mountain grassland

    New Phytolog.

    (2013)
  • M. Bahn et al.

    Does photosynthesis affect grassland soil-respired CO2 and its carbon isotope composition on a diurnal timescale?

    New Phytolog.

    (2009)
  • G.A. Barron-Gafford et al.

    Quantifying the timescales over which exogenous and endogenous conditions affect soil respiration

    New Phytolog.

    (2014)
  • K.L. Cottingham et al.

    Knowing when to draw the line: designing more informative ecological experiments

    Front. Ecol. Environ.

    (2005)
  • W. Cheng et al.

    Theoretical proof and empirical confirmation of a continuous labeling method using naturally C-13-depleted carbon dioxide

    J. Integr. Plant Biol.

    (2007)
  • W. Cheng et al.

    Synthesis and modeling perspectives of rhizosphere priming

    New Phytolog.

    (2014)
  • W.X. Cheng et al.

    Rhizosphere effects on decomposition: controls of plant species, phenology, and fertilization

    Soil Sci. Soc. Am. J.

    (2003)
  • J.M. Craine et al.

    Predominance of ecophysiological controls on soil CO2 flux in a Minnesota grassland

    Plant Soil

    (1999)
  • E.A. Davidson et al.

    Temperature sensitivity of soil carbon decomposition and feedbacks to climate change

    Nature

    (2006)
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