These authors contributed equally to this work.
Over the past decades, average global wheat yields have
increased by about 250 %, mainly due to the cultivation of high-yielding
wheat cultivars. This selection process not only affected aboveground parts
of plants, but in some cases also reduced root biomass, with potentially
large consequences for the amount of organic carbon (OC) transferred to the
soil. To study the effect of wheat breeding for high-yielding cultivars on
subsoil OC dynamics, two old and two new wheat cultivars from the Swiss
wheat breeding program were grown for one growing season in 1.5 m deep
lysimeters and pulse labeled with
Soil management has a large influence on the size of the soil organic carbon
(SOC) stock in managed arable soils. This is evident from the large decrease
in SOC that is generally observed after soils under natural vegetation are
converted to arable land (Don
et al., 2011; Guo and Gifford, 2002; Poeplau et al., 2011). As a
consequence, the mineralization of SOC and the loss of forest caused by land
use change has contributed about 30 % to the increase in atmospheric
The rising awareness that there is potentially an opportunity to increase
subsoil organic carbon (OC) stocks (Chen et al., 2018)
has led to the proposal that agricultural soils can be a sink of atmospheric
In addition, growing crops with deeper roots and/or higher root biomass has been put forward as a strategy to increase OC sequestration in arable soils (Kell, 2011), while deep rooting can also decrease the effect of drought in climates where deep soil water is available during the main cropping season (Wasson et al., 2012). However, a direct or marker-assisted selection for root traits is very rare in conventional breeding programs. Accordingly, we have very limited knowledge on if and how breeders alter the root system and potentially affect belowground carbon cycling. One way to evaluate the effect of breeder's selection on root characteristics and subsoil carbon cycling is to compare old and new varieties of the same breeding program. For the Swiss wheat breeding programs, the selection process reduced the mass and depth of roots under well-watered conditions (Friedli et al., 2019), as has been found for other breeding programs (Aziz et al., 2017), but modern genotypes enhanced root allocation to deep soil layers under drought. However, this pattern has not been observed consistently (Cholick et al., 1977; Feil, 1992; Lupton et al., 1974). To the best of our knowledge, there is no information about the effect of breeding on changes in subsoil OC dynamics and root respiration.
One reason for the lack of quantitative data about the effects of rooting depth on SOC sequestration is related to difficulties in measuring the amount of carbon transferred from roots to the soil (gross rhizodeposition) and the proportion of carbon that is eventually stabilized there (net rhizodeposition), after a portion of gross rhizodeposits are lost from the soil through microbial mineralization or leaching. The fact that rhizodeposition occurs below the soil surface greatly prevents direct observations of this “hidden half of the hidden half” of the SOC cycle (Pausch and Kuzyakov, 2018). First of all, direct measurements of root exudation rates are hampered by the fact that rhizodeposits are used by rhizosphere microorganisms within a couple of hours after they are released, resulting in very low concentrations of root carbon exudates in the soil (Kuzyakov, 2006). Second, the release of carbon exudates by agricultural crops is not equally divided throughout the growing season but mainly occurs in the first 1–2 months of the growing period and decreases sharply thereafter (Gregory and Atwell, 1991; Keith et al., 1986; Kuzyakov and Domanski, 2000; Pausch and Kuzyakov, 2018; Swinnen et al., 1994). Third, measurements of the effects of rhizodeposits on changes in SOC stocks are further complicated by the priming effect, i.e., their positive effect on the mineralization of native SOC (Fontaine et al., 2007; de Graaff et al., 2009).
To overcome these difficulties, rates of C rhizodeposition can be measured
by labeling plants with
In addition, assessing the magnitude of the carbon transfer from roots to the soil is not straightforward, particularly under field conditions. While carbon inputs from crops to the soil are often derived from yield measurements (Keel et al., 2017; Kong et al., 2005; Taghizadeh-Toosi et al., 2016), these quantities are often poorly related to root biomass or the magnitude of root exudates (Hirte et al., 2018; Hu et al., 2018). A better understanding of the factors controlling the rates of carbon rhizodeposition by different agricultural crops is thus necessary to assess how different crops affect SOC cycling and to provide SOC models with reliable rates of carbon inputs to the soil.
The present study addresses the following research question: do wheat cultivars with shallow roots and lower root biomass lead to less net carbon rhizodeposition compared to wheat cultivars with deeper roots and higher root biomass? To address this question, four different bread wheat cultivars from a century of Swiss wheat breeding (Fossati and Brabant, 2003; Friedli et al., 2019) were grown in large mesocosms, which allowed us to study the plant–soil system under controlled conditions that closely resemble a field situation. We hypothesized that wheat cultivars with shallow roots and lower root biomass would result in less net carbon rhizodeposition over the course of a growing season, compared to cultivars with deeper roots and higher root biomass.
To assess the effect of wheat root characteristics on net rhizodeposition in
a realistic soil environment under controlled conditions, an experiment was
set up at the mesocosm platform of the Sustainable Agroecosystems Group at
the Research Station for Plant Sciences Lindau (ETH Zürich,
Switzerland). The platform was located inside a greenhouse and consisted of
12 cylindrical lysimeters with a diameter of 0.5 m and a height of 1.5 m,
constructed using 10 mm wide polyethylene (Fig. S1 in the Supplement). The lysimeters were
equipped with probes installed at five different depths (0.075, 0.30, 0.60,
0.90 and 1.20 m below the surface) to measure the volumetric moisture
content at a temporal resolution of 30 min (
At the top of each lysimeter, pneumatically activated chambers were placed,
which were automatically closed when applying the
Four wheat (
Before the wheat plants were transplanted to the lysimeters, wheat seeds
were germinated in a greenhouse for 2–3 d on perforated antialgae
foil laid over 2 mm moistened fleece at a warm temperature (20
The experimental setup consisted of a randomized complete block design.
Each of the four wheat cultivars was planted in three lysimeters, i.e., three replicates per cultivar, resulting in a total of 12 lysimeters. These were
placed in three blocks of four rows, where each wheat cultivar was planted in one
lysimeter in each block. The plants were grown in the greenhouse for about 5
months, between 24 August 2015 and 1 February 2016. Despite uneven maturing
of plants within and between the lysimeters, all plants had reached
flowering stage at the time of harvest. Fertilizer was applied to the soil
lysimeters a first time on 5 October 2015, at a rate of 84 kg N ha
In order to study carbon allocation within the atmosphere–plant–soil system,
a
Soil gas sampling was performed once per week (Wednesdays) by attaching a
pre-evacuated 110 mL crimp serum vial to a sampling port at each depth,
leaving it equilibrating overnight. For each sample, a 20 mL subsample was
transferred to a pre-evacuated Labco exetainer (12 mL) and used to
determine the
At the end of the experiment, the aboveground biomass of the wheat plants
was harvested separately for each lysimeter and separated into leaves, ears
and stems. Soil from the lysimeters was collected by destructive sampling to
analyze bulk density, root biomass and other soil properties. The sampling
was done layer by layer. After a soil layer had been sampled, it was removed
completely from the lysimeter and the next layer was sampled. From each
depth increment (0–0.15, 0.15–0.45, 0.45–0.75, 0.75–1.05, 1.05–1.35 m depth), five soil cores were collected per lysimeter using a soil
core sampler (5.08 cm diameter, Giddings Machine Company Inc., Windsor, CO,
US). Three of the five cores per lysimeter and depth increment were
used for the determination of root biomass based on a combination of
buoyancy and sieving through a 530
Soil microbial biomass was extracted from soil samples that had been frozen
at
The OC concentration and isotopic composition (
The mass of
To calculate the excess atom fraction (
The absolute amount of carbon rhizodeposition for the different depth
segments in the lysimeters was calculated following Janzen and Bruinsma (1989):
Depth profiles of subsoil
The gas diffusion coefficient in free air was corrected for the individual
lysimeters for variations in temperature and soil moisture throughout the
experiment (Massman, 1998), as
To obtain depth profiles of the total amount of
To account for the three blocks in the randomized complete block design,
statistically significant differences between aboveground characteristics of
different cultivars were checked using a two-way analysis of variance
(ANOVA) without interactions (Dean et al., 2015), followed
by a Tukey test, based on the values obtained for the individual
replicates (
The aboveground biomass produced at the end of the experiment was
significantly different between Zinal and Probus, while the aboveground
biomass of CH Claro and Mont-Calme 268 was not significantly different from
any other cultivar (Fig. 1, Table 1). The biomass of the ears was
significantly higher for Zinal, compared to CH Claro, Probus and Mont-Calme
(Fig. 1, Table S1 in the Supplement). It is noted that these data should be interpreted with
care, since not all plants reached maturity at the time of harvest and are potentially not representative for the biomass of the ears of full-grown
plants. No significant differences were found between the
Aboveground
Characteristics (
The average root biomass was highest in the topsoil and significantly lower
in the subsoil layers of all four wheat cultivars (Fig. 1b). Root biomass of
Zinal was significantly lower compared to the root biomass of Probus and
Mont-Calme 268, while the root biomass of CH Claro was not significantly
different from any of the other cultivars (Fig. 1b). These differences were
mostly present in the two uppermost soil layers, while root biomass was not
significantly different between different cultivars at any depth, except for
Zinal and Mont-Calme 268 between 0.45 and 0.75 m depth (Fig. 1). The
root : shoot ratio varied between
The depth profiles of the
The SOC concentration in the lysimeters was similar to the OC concentration of the initial soil (Fig. 3a). A direct comparison between the SOC concentration before and after the experiment could not be made, as no measurements of the OC concentration of the soil in the lysimeters before the start of the experiment could be made. However, the SOC concentration measured at the different depths in the lysimeters was similar to the OC concentration measured on the soil that was used to fill the lysimeters (Fig. 3a). No statistically significant differences in SOC concentration were found between the different cultivars at any depth.
Depth profiles of organic carbon concentration
The SOC in the two uppermost soil layers (0–45 cm) of all wheat cultivars
was enriched in
There was no significant effect of cultivar on the bulk density of the soil
at the end of the experiment (
The total amount of
Absolute
The total amount of net carbon rhizodeposition measured at the end of the
experiment down to 0.45 m decreased with depth for all wheat cultivars (Fig. 4c), with this difference only being statistically significant for CH Claro.
The highest amount of net carbon rhizodeposition was observed for Probus
(
Throughout the experiment, the change in the
Changes in the
Despite these high
Depth profiles of calculated cumulative
The aim of the present study was to assess differences in belowground carbon transfer and net rhizodeposition by wheat cultivars with different root biomass and rooting depth. Our results show that although there are marked differences in both the amount of carbon transferred belowground and the timing of belowground carbon transfer, there is no clear relationship between root characteristics and the amount of net rhizodeposition. Therefore, the fate of root biomass might determine the total amount of subsoil carbon stabilization in the long term.
No consistent differences in total aboveground biomass between old and new wheat cultivars were observed. The aboveground biomass values were at the high end of reported values for wheat plants in the field (Mathew et al., 2017), while the lack of consistent differences in the biomass of wheat cultivars released over a time span of multiple decades has generally been observed (Brancourt-Hulmel et al., 2003; Feil, 1992; Lupton et al., 1974; Wacker et al., 2002).
The fraction of biomass in the grain-bearing ears was, however, much larger for the modern wheat cultivars (on average 9 % and 47 % of total aboveground biomass for CH Claro and Zinal respectively) compared to the old wheat cultivars (on average 1 % and 2 % for Mont-Calme 268 and Probus respectively). While an increase in the fraction of biomass allocated to grains is generally observed in old versus modern wheat cultivars (Brancourt-Hulmel et al., 2003; Feil, 1992; Shearman et al., 2005), mostly as a consequence of the introduction of reduced height genes (Tester and Langridge, 2010), the harvest index reported here for the old cultivars might have been underestimated because older cultivars were not yet fully mature at plant harvest.
The total root biomass of the older wheat cultivars was substantially larger
compared to the more recent cultivars, although these differences were not
consistently significant between all modern and old varieties (Table 1).
These differences were mostly apparent in the top 0.45 m of the lysimeters
(Fig. 1). It is not clear if the lack of statistically significant
differences in the root biomass within the deeper soil layers was due to (i) inability to collect all fine roots from the soil or (ii) actual differences
in root biomass. These results are in line with a recent study on the
biomass of roots of different wheat cultivars of the Swiss wheat breeding
program, including the cultivars used in our experiment (Friedli et al., 2019). This study showed
that, under well-watered conditions, older wheat cultivars had a substantially higher root biomass compared to the more recently released
wheat cultivars. Similar results have been obtained for wheat cultivars
released in, e.g., Australia (Aziz et al., 2017) and other
countries around the world (Waines and
Ehdaie, 2007). The root : shoot ratios of the wheat cultivars in our study
(
The maximum rooting depth was similar between the old and recent wheat
cultivars (Fig. 1b). This is in contrast with the results from
Friedli et al. (2019), who found that the
older wheat cultivars had deeper roots (the depth above which 95 % of
roots were found (
The
The partitioning of the
The total amount of carbon assimilated by the wheat cultivars that was
transferred to roots and soil in the top 0.45 m at the end of the experiment
ranged between
Average belowground carbon allocation (net rhizodeposition and root
biomass combined) and net carbon rhizodeposition by the different wheat
cultivars, calculated down to a depth of 0.45 m (variation is reported as
the standard error,
In contrast to the total amount of carbon translocated belowground, the
amount of net carbon rhizodeposition was not consistently different between
the old and more recent wheat cultivars (
A large uncertainty associated with calculated values of subsoil carbon
sequestration using isotopic labeling approaches is related to the
assumption that the isotopic enrichment of roots and rhizodeposits is
similar (Eq. 4). This simplification is made because of the difficulties in
measuring quantitative characteristics of rhizodeposits in a soil medium
(Oburger and Jones, 2018) but leads
to erroneous calculations of the amount of carbon rhizodeposition when this
assumption is violated (Stevenel et al., 2019). To
assess the uncertainty of calculated values of subsoil carbon sequestration,
we calculated how these values differ when the value of root
Our results indicate that the old wheat cultivars, with deeper active roots throughout the experiment and larger root biomass, allocated more assimilated carbon belowground, although the differences were not statistically significant (Fig. 4c, Table 2). However, we found no evidence that wheat cultivars with larger root biomass lead to higher net carbon rhizodeposition (Table 2). Our hypothesis, which stated that wheat cultivars with larger root biomass and deeper roots would lead to larger amounts of net carbon rhizodeposition, could therefore not be confirmed.
The total amount of OC that will be stabilized in the soil by the studied wheat cultivars will therefore depend on the long-term fate of the root biomass. The root biomass was higher for the old wheat cultivars, although these differences were mainly limited to the upper 0.45 m of the soil. Due to the destructive sampling of vegetation and soil at the end of the experiment, the fate of root biomass after harvest could not be assessed. Based on the results, one could therefore hypothesize that the higher root biomass of old wheat cultivars would lead to larger rates of carbon sequestration in the long term. Similarly, Mathew et al. (2017) suggested that growing grasses and maize plants would lead to larger SOC stocks because these plants have the highest total and root biomass compared to growing crops with a lower biomass. However, it is not straightforward to make predictions about the amount of root biomass that will be stabilized in the soil in the long term, as this depends on the efficiency with which plant-derived biomass is incorporated in microbial biomass (Cotrufo et al., 2013) and interactions between soil depth, the microbial community composition and its substrate preference (e.g., Kramer and Gleixner, 2008), among other factors. During the past century, there has been a continuing increase in the importance of wheat cultivars with smaller root biomass (Fossati and Brabant, 2003; Friedli et al., 2019; Waines and Ehdaie, 2007). This can have profound implications for OC stocks of soils under wheat cultivation, as rhizodeposition and root-derived carbon are the most important inputs of OC to the soil (Kong and Six, 2010). Testing the long-term effect of the gradual change in wheat cultivars on OC inputs to the soil would thus require experiments that run over multiple growing seasons and allow the quantification of the amount of root carbon that is eventually stabilized in the soil.
Correct knowledge on the amount of OC that is transferred belowground by plants is necessary to reliably model SOC dynamics. However, this knowledge is currently limited and changes in belowground carbon allocation due to the cultivation of different cultivars are generally not considered in SOC models. Moreover, it has recently been shown that accounting for changes in belowground carbon allocation by relating this to changes in aboveground biomass does not improve model results (Taghizadeh-Toosi et al., 2016). Rather, it has been suggested that more reliable model results are obtained when crop-specific amounts of belowground carbon allocation are used, independent of aboveground biomass production (Taghizadeh-Toosi et al., 2016). Since model results are very sensitive to the amount of carbon inputs (Keel et al., 2017), and cereal crops are grown on ca. 20 % of croplands globally (Leff et al., 2004) (covering ca. 12 % of global land mass and storing ca. 10 % of global SOC in the upper meter of soil; Govers et al., 2013), a correct assessment of a potential decrease in belowground carbon inputs by wheat plants over the past century through the cultivation of different cultivars will have important implications for the simulation of changes in SOC on the global scale.
Assessing the overall impact of the past evolution of wheat cultivars on SOC stocks also requires taking into account the amount of land needed to produce sufficient food. For example, if future research would show that more recent wheat cultivars lead to less SOC stabilization compared to older cultivars, this does not necessarily imply a net loss of SOC as a consequence of the historical shift to planting recently developed wheat cultivars. If the aim is to increase overall SOC stocks, it might be more favorable to grow high-yield wheat cultivars that sequester less OC per unit area compared to a low-yielding cultivar, if this results in a larger area of arable land that can be taken out of cultivation. This land can be put under native vegetation, such as forest or grassland, which stores substantially more SOC compared to arable land (Jobbágy and Jackson, 2000).
In this study, four different wheat cultivars were grown in lysimeters and
labeled with
Additional figures and tables can be found in the Supplement.
The data associated with this paper are available in the Supplement and at
The supplement related to this article is available online at:
CD, SA, AH, CF and JS conceived the idea for the study. CD set up the lysimeter and labeling experiments and collected the data. SG, CD, SA and RAW performed lab analyses. MVdB, SG, CD and JS analyzed and interpreted the data and performed the statistics. MVdB and SG wrote the paper, with contributions from CD, AH, SA, JS, CF and RAW. MVdB and SG contributed equally to this paper.
The authors declare that they have no conflict of interest.
The authors are very grateful to Matti Barthel, Benjamin Wild and Christopher Mikita for their help with setting up the lysimeters, data collection and interpretation. The authors also appreciate the Grassland Sciences Group of ETH Zürich for providing the laboratory facility to perform part of the analyses performed in this study. We thank Brigitta Herzog and Hansueli Zellweger for their help with greenhouse management and plant protection at the ETH Research Station for Plant Sciences in Lindau. Stefan Karlowsky and one anonymous reviewer are thanked for their comprehensive feedback, which improved the quality of this paper.
This research has been supported by Plant Fellows, a postdoctoral fellowship administered by the Zurich Basel Plant Science Center and funded under the European Union's Seventh Framework Programme for research, technological development and demonstration (grant no. GA-2010-267243 – Plant Fellows); the Swiss National Science Foundation (project numbers 205321_153545 “CarIN” and 200021_160232); and ETH core start-up funds provided to Johan Six.
This paper was edited by Sara Vicca and reviewed by Stefan Karlowsky and one anonymous referee.