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Why are nitrogen concentrations in plant tissues lower under elevated CO2?
A critical examination of the hypotheses.
Daniel R. Taub1, & Xianzhong Wang2
1
Biology Department and Environmental Studies Program, Southwestern University,
1001 East University Avenue, Georgetown TX 78626, USA. 2Department of Biology,
Indiana University-Purdue University Indianapolis, Indianapolis, IN 46202, USA.
Author for correspondence- Daniel R. Taub ([email protected]),
Telephone: 1 512 863-1583 facsimile: 1 512 863-1696
Running title: Elevated CO2 and plant nitrogen concentrations
Abstract
Plants grown under elevated atmospheric [CO2] typically have decreased tissue
concentrations of N compared with plants grown under current ambient [CO2]. The
physiological mechanisms responsible for this phenomenon have not been definitely
established, although a considerable number of hypotheses have been advanced to
account for it. In this review we discuss and critically evaluate these hypotheses. One
contributing factor to the decreases in tissue N concentrations clearly is dilution of N by
increased photosynthetic assimilation of C. In addition, studies on intact plants show
strong evidence for a general decrease in the specific uptake rates (uptake per unit mass
or length of root) of N by roots under elevated CO2, This decreased root uptake appears
likely to be the result both of decreased N demand by shoots and of decreased ability of
the soil-root system to supply N. The best-supported mechanism for decreased N supply
is a decrease in transpiration-driven mass flow of N in soils due to decreased stomatal
conductance at elevated CO2, although some evidence suggests that altered root system
architecture may also play a role. There is also limited evidence suggesting that under
elevated CO2, plants may exhibit increased rates of N loss through volatilization and/or
root exudation, further contributing to lowering tissue N concentrations.
Key Words: carbon dioxide, dilution, elevated CO2, graphical vector analysis, nitrogen,
plants, root uptake, tissue concentrations
Growth of plants at atmospheric concentrations of carbon dioxide (CO2) greater
than the current ambient can greatly affect plant tissue chemistry (Loladze 2002, Poorter
et al. 1997). One of the most commonly seen effects is a decrease in the dry mass
concentration of N (Nm). Cotrufo et al. (1998), synthesizing data from a broad range of
studies, found mean decreases in Nm of 14% in aboveground tissues and 9% in roots.
This compares closely with the findings of other data syntheses, which have found
elevated [CO2] mediated decreases in Nm of 16.4% for leaves of woody plants (Curtis and
Wang 1998), 11% and 14% respectively for leaves of gymnosperms and angiosperms in
open-top chamber experiments (Norby et al. 1999), 12.9% for leaves in free-air carbon
dioxide enrichment (FACE) experiments (Ainsworth and Long 2005), 14% for seeds
(Jablonski et al. 2002) and 9-15% for the edible portions of several major food crops
(although only 1.4% for soybean; Taub et al. 2008). Such decreases in Nm can have
important implications not only for plant physiological processes, but for food chains, as
the performance of insect herbivores often decreases with decreases in Nm (Bezemer and
Jones 1998; Zvereva and Kozlov 2006), and changes in plant tissue quality under
elevated CO2 can affect herbivore population dynamics (Whittaker 1999).
While broad literature surveys have consistently found mean decreases in Nm of
approximately 10 - 15% for plants grown at elevated [CO2], there is considerable
variability in the results of individual studies. Yin (2002) found that, across a wide range
of studies, the elevated [CO2] effect on leaf Nm ranged from a 56% decrease to a 20%
increase, while Norby et al. (1999) found a range from a decrease of 35% to an increase
of 20% for the leaves of trees grown in open-top chambers. A number of factors have
been identified that partially explain this variation among studies. Yin (2002) found that
the effect of elevated [CO2] was greatest for woody deciduous species and that decreases
in Nm under elevated CO2 were most pronounced at high light levels, high temperatures
and large pot sizes. Yin (2002) and Taub et al. (2008) both found that the effect of [CO2]
on Nm was reduced by N fertilization. Several studies have reported that the effect of
elevated [CO2] on Nm is less for nitrogen-fixing species than for other types of plants
(Cotrufo et al. 1998; Jablonski et al. 2002; Taub et al. 2008). Ainsworth and Long (2005)
and Taub et al. (2008) found that the effect of elevated CO2 on Nm increased under ozone
stress (although see Taub et al., 2008 for divergent results for soybean).
While it has been well established that elevated [CO2] typically decreases Nm, the
mechanisms by which this occurs are not certain, although a large number of hypotheses
have been advanced to explain the phenomenon. While there have been a few attempts to
summarize and evaluate several of these hypotheses (Conroy and Hocking 1993; Gifford
et al. 2000; Pang et al. 2006), the current review aims to provide a critical and more
comprehensive evaluation of these hypotheses than has been available previously.
This review focuses on factors at the plant level that may affect Nm. Elevated
[CO2] and other global changes are likely to additionally affect Nm by affecting
ecosystem processes that influence N availability to plants, but this is beyond the scope
of this review; we refer readers to several recent reviews of these topics (Barnard et al.
2005; Luo et al. 2006; Reich et al. 2006).
Dilution Hypotheses
Perhaps the most frequently mentioned hypothesis about the decrease in Nm under
elevated [CO2] is that it results from dilution due to accumulation of non-structural
carbohydrates (NSC; Table 1, Hypothesis 1). Dilution by plant secondary compounds has
also been proposed as a possible mechanism for decreased Nm under elevated CO2 (Table
1, Hypothesis 2). Most authors who have mentioned dilution have not described the
phenomenon in detail; it is therefore uncertain precisely what process is envisioned. Here
we distinguish two different meanings of “dilution”, which we call biomass dilution and
functional dilution.
Biomass dilution occurs whenever the increase in total biomass of a plant or
organ under elevated CO2 relative to growth under ambient CO2 is greater than the
corresponding increase in total N. One tool that may be usefully applied to examining
biomass dilution is graphical vector analysis (GVA; (Haase and Rose 1995; Koricheva
1999). GVA is a technique that allows simultaneous comparison of concentration and
content of a chemical component (e.g., N or NSC) and the biomass of the plant organ that
contains the component (e.g., leaf) in an integrated graph, thus allowing detection of
dilution effects. Our methodology for constructing the vector diagram was modified from
Haase and Rose (1995). We extracted results from publications that contained data on
biomass and on leaf N and NSC contents. We superimposed the vector diagram for N
over the one for NSC to compare their changes in concentration and content relative to
changes in leaf mass under elevated CO2 (Figure 1).
The effect of elevated CO2 on N and NSC is determined by the direction and
magnitude of each vector (the arrows in Figure 1). A vector pointing downward and
toward the right indicates biomass dilution, while one pointing upward and to the right
indicates a concentration effect, in which a constituent increases to a greater extent under
elevated CO2 than does biomass as a whole. A horizontal vector pointing right indicates a
constituent that increases proportionally with increasing biomass. The length of a vector
indicates the magnitude of responsiveness to elevated CO2.
Figure 1 shows four distinct patterns of response to elevated CO2 in N and NSC.
Pattern 1, for Betula pendula, shows a response in which N is diluted and NSC are
concentrated under elevated CO2. Pattern 2, for Pinus plaustris at high soil water
potential, shows a response in which NSC are concentrated under elevated CO2, while N
decreases not only in concentration but in absolute content as well. This suggests that a
mechanism in addition to biomass dilution is contributing to decreasing Nm. Pattern 3, for
Pinus palustris at low soil water potential, shows dilution of N, but there is very little
increase in the concentration of NSC, suggesting that other biomass constituents are
largely responsible for the dilution of N. Pattern 4, for Xanthium strumarium, shows
dilution of both N and NSC by increased biomass.
These results demonstrate that one important reason of lower N under elevated
CO2 is the relatively small increase of its content compared to other components, i.e.
biomass dilution. These results also demonstrate that NSC is in some cases an important
component of the diluting biomass. In no case, however, does NSC increase sufficiently
to entirely account for the dilution of N. This finding seems likely to hold in general.
Poorter et al. (1997) analyzed the chemical composition of the leaves of 27 species grown
under elevated CO2 across a wide range of experimental protocols. They found that Nm
was decreased under elevated CO2 by an average of 17% on a total biomass basis and by
10% under a NSC-free biomass basis. The content of protein (the major nitrogenous
component of leaves) declined not only relative to NSC, but relative to all other classes of
organic compounds, including structural carbohydrates, soluble phenolics, lipids, organic
acids and lignin. Biomass dilution of N under elevated CO2 may therefore be nearubiquitous, but NSC are responsible for only a portion of this effect.
Additional insight into the mechanism of dilution can be obtained through the
concept of functional dilution of N. This concept is based on the functional balance
concept which envisions tissue N concentrations as dependent on the relative activities of
shoots and roots:
Nm ∝
σ r fr
σ s fs
where fr and fs are the fractions of plant mass in roots and shoots, respectively, and σr and
σs are the mass-based specific activities of roots and shoots in acquiring N and
photosynthate, respectively (c.f BassiriRad et al. 2001, Davidson 1969, Hilbert 1990).
Within this model, there are three possible causes of a decrease in Nm: a shift in
allocation of biomass toward shoots, a decrease in specific root activity, or an increase in
shoot specific activity. A decrease in Nm due to increased shoot specific activity can be
regarded as functional dilution; Nm declines because of the accumulation of additional
photosynthate by shoots.
If we can accept photosynthetic rate as the equivalent of shoot specific activity,
functional dilution of N under elevated CO2 appears near-ubiquitous, as enhancement of
photosynthetic rates for plants grown under elevated CO2 is consistently observed on
either a leaf area or leaf mass basis (Ainsworth and Long 2005, Curtis and Wang 1998,
Ellsworth et al. 2004, Norby et al. 1999). The question arises of whether, within the
functional balance concept, dilution is solely responsible for decreased Nm under elevated
CO2, or whether altered allocation and/or decreased specific root activity play a role as
well.
Altered allocation does not appear likely to contribute to decreased Nm; to the
extent that elevated CO2 affects allocation it appears generally to increase root mass
relative to shoot mass (Luo et al. 2006, Norby 1994, Poorter and Nagel 2000). This
should tend to increase, rather than decrease, Nm.
Decreased specific root activity appears more likely than altered allocation to play
a role in decreasing Nm. While a number of experiments have measured the effects of
elevated CO2 on root uptake kinetics in solution (see references in BassiriRad et al.
2001), data on specific root uptake of N (i.e. uptake per unit root mass or length) under
elevated CO2 for intact plants rooted in solid media (i.e. not in hydroponics) are fairly
limited. Table 2 shows the results of all such experiments that we have identified. The
consistent trend toward decreased specific uptake is quite remarkable (although the trends
were often not statistically significant within individual experiments), as is the overall
mean decrease in uptake rate of 16.4%. This result is in striking contrast to the effects of
elevated CO2 on uptake of N from solution. Reviews of the literature on short-term
(minutes to hours) uptake of NH4+ and NO3- from solution have concluded that results
from individual studies are highly variable, with uptake variously increased, decreased or
unchanged under elevated CO2 (BassiriRad et al. 2001, Luo et al. 1998). Studies that
have measured longer-term uptake of N (days to weeks) in plant grown in hydroponics
have also shown variable results, with increases in specific uptake of N under elevated
CO2 appearing more common than decreases (Chu et al. 1992, Gloser et al. 2002, Roumet
et al. 1996). It therefore appears that the factors that lead to decreased specific N uptake
from soils under elevated CO2 are ones not present in hydroponics. This might include
aspects of root system architecture and mycorrhizal status or factors affecting the
movement of N through soils to plant roots (see the following section for an extended
discussion). This suggestion is also consistent with the finding that decreases in Nm under
elevated CO2 are larger in soils than in hydroponics (Poorter et al. 1997). In any case,
decreased rates of root specific uptake of N appear likely to play a role in the decreased
Nm of plants grown in soil.
Another line of evidence that suggests that dilution is not solely responsible for
decreasing Nm under elevated CO2 is the pattern of response of mineral elements other
than N. With either functional dilution or biomass dilution, all elements other than the
elements assimilated through photosynthesis (C, H and O) should be diluted equally
(Loladze 2002). Figure 2 shows that significant decreases are seen in elevated CO2 for
four of five macronutrient elements, but that there are significant differences among the
elements in the effect of CO2. In particular, N is affected by CO2 more than P and K are.
This strongly suggests that the effects of elevated CO2 on mineral element concentrations
are mediated through factors involved in uptake and/or metabolism of these elements, not
simply through dilution.
Hypotheses of decreased nitrogen uptake (source effects)
A variety of hypotheses have been advanced that propose mechanisms by which
growth at elevated [CO2] might decrease acquisition of N. These mechanisms can be
divided into those that affect N uptake by affecting the ability of the soil-root system to
supply N (source effects), and those that affect demand for N by the plant, with
subsequent effects on N uptake (demand effects). In this section we discuss source-driven
effects on N acquisition, with demand-driven mechanisms reserved for the following
section.
One of the most consistent effects of growth at elevated CO2 is a decrease in
stomatal conductance (Ainsworth and Rogers 2007, Wullschleger et al. 2002), leading to
decreased transpiration. Several authors have suggested that this may decrease uptake of
those nutrients for which mass flow through soil plays a major role in uptake, including N
(as nitrate), Ca, Mg and S (Table 1; Line 3; Barber 1984, Marschner 1995).
In support of this hypothesis, several studies have found elevated CO2 to have
similar effects on both transpiration and plant N. Del Pozo et al. (2007), manipulating
both N supply and [CO2] in wheat, found transpiration and leaf N (both on a leaf area
basis) to be positively correlated. Polley et al. (1999) found that elevated CO2 decreased
both whole-plant transpiration and whole-plant N accretion in two C3 perennials.
In either of these studies it is not clear whether transpiration has led to decreased
plant N, or whether decreased photosynthetic capacity (manifested by decreased leaf N)
has led to decreased stomatal conductance and transpiration (Drake et al. 1997). This
caveat does not hold for a study by McDonald et al. (2002), who measured the effect of
elevated CO2 on N uptake rates. They found that over a seven day period, transpiration
per gram of root in Populus deltoides was both decreased by 20.4% under elevated CO2
and positively correlated with N uptake per gram of root.
Additional support for a relationship between elevated CO2-mediated decreases in
transpiration and in Nm can be found by comparing the responses to elevated CO2 of
various soil-derived elements. Figure 2 shows that decreases in concentration under
elevated CO2 are largest for those macronutrients that are supplied to roots by
transpiration-driven mass flow (N, Mg and Ca) and least for those most dependent on
diffusion through soil (P and K). This suggests two possible interpretations. Biomass
dilution may decrease the concentrations of all soil-derived elements, while mobile
elements are additionally decreased due to restricted mass flow. Alternatively, dilution
may decrease the concentration of all soil-derived elements, but this may be partially
ameliorated for diffusion-limited elements by increased soil water content allowing more
rapid diffusion (Van Vuuren et al. 1997).
Several authors have suggested that growth at elevated CO2 may lead to root
system architectures that are less efficient at taking up nutrients, including N (Table 1;
Hypothesis 4). Pritchard and Rogers (2000) presented evidence that under elevated CO2,
root systems often exhibit increased growth of lateral vs. primary roots, leading to
shallower rooting, and suggested that this would lead to decreased efficiency of nutrient
uptake. Berntson (1994), modelling root systems of Senecio vulgaris, found that changes
in root system architecture under elevated CO2 led to decreased efficiency of soil
exploitation. Whether this finding would hold for other species and under different
growth conditions is unknown.
Another mechanism that might potentially affect N uptake rates is altered uptake
capacity of individual roots (Table 1; hypothesis 5). The expectation of most authors has
been that elevated CO2 would increase rather than decrease uptake capacity, by providing
additional photosynthate to roots for the energy demanding processes of N uptake
(BassiriRad et al. 1996, 2001). Studies of root uptake of NH4+ and NO3- from solution
have, however, yielded highly variable results (Luo et al. 1998), with a majority of the
experimental observations summarized by BassiriRad et al. (2001) showing decreases in
NH4 and NO3 uptake rates under elevated CO2. The mechanisms by which elevated CO2
might lead to such decreases are not known. The large variability seen for the effects of
elevated CO2 on root uptake capacity suggest that this factor is not primarily responsible
for the decrease in Nm typically seen under elevated CO2, but may contribute to the
variation seen in magnitude of the Nm response.
Altered mycorrhizal status under elevated CO2 has also frequently been
mentioned as a mechanism that might affect plant nutrient status (Table 1; Hypothesis 6).
Growth at elevated CO2 often increases the proportion of roots colonized by mycorrhizal
fungi (Treseder 2004). It may also have greater positive effects on the mass of
mycorrhizal fungi than of their associated plants (BassiriRad et al. 2001; though see
Staddon et al. 2002), and increase the growth of extraradical mycelium more than it
increases the growth of fungal hyphae in direct association with plant roots (Alberton et
al. 2005). These changes collectively could potentially increase nutrient uptake efficiency
under elevated CO2 by the fungal-plant system, as fungal hyphae have greater uptake
capacity on a mass basis than plant roots (BassiriRad et al. 2001). Alternatively, the
greater fungal mass under elevated CO2 might provide a larger sink for minerals, so that
less is translocated to plants (Alberton et al. 2005, BassiriRad et al. 2001). BassiriRad et
al. (2001) found that, under elevated CO2, mycorrhizal plants typically had higher Nm
than non-mycorrhizal plants. This suggests that effects on mycorrhizae are unlikely to be
responsible for the decrease in Nm typically found under elevated CO2. Differences in the
extent of mycorrhizal development may, however, explain some of the variability found
in the effect of elevated CO2 on Nm, with colonization by mycorrhizal fungi partially
ameliorating the decreases in Nm that are typically seen.
Hypotheses of decreased nitrogen demand
Plants can sustain growth at a lower Nm under elevated than under ambient CO2,
as reflected in a lower critical foliar N concentration (the concentration at which biomass
production is 90% of maximum; Conroy 1992) and increased plant nitrogen use
efficiency (Stitt and Krapp 1999). Assuming that N uptake is at least partially regulated
by demand (BassiriRad et al. 2001), this decreased N requirement can lead to decreased
whole-plant Nm (Table 1, Hypothesis 7).
Increased plant N efficiency for biomass production under elevated CO2 is almost
certainly the product of an increased photosynthetic N use efficiency (PNUE). This
increased PNUE appears to be a result both of the effect of [CO2] on the efficiency of
carboxylation of RUBP and of decreased investment in photosynthetic and
photorespiratory enzymes (Davey et al. 1999, Gifford et al. 2000, Stitt and Krapp 1999).
While there have been suggestions that decreased accumulation of photosynthetic
enzymes under elevated CO2 result from a general decline in leaf N status (Stitt and
Krapp 1999), there is also evidence for a specific downregulation of photosynthetic
enzymes mediated by a sugar-sensing mechanism (Moore et al. 1999).
Photosynthetic enzymes, particularly RUBISCO, make up a large fraction of total
leaf N in C3 species (Evans and Seemann 1989). A number of authors have therefore
suggested that downregulation of photosynthesis may be partially or largely responsible
for the effects of elevated CO2 on Nm in leaves and other photosynthetic tissues (Table 1,
Hypothesis 8). Fangmeier et al. (1999, 2000, 2002) have pointed out that downregulation
of photosynthetic enzymes in leaves may also decrease N availability to organs such as
seeds and tubers that obtain N translocated from catabolised proteins in leaves. Increased
PNUE and decreased demand for photosynthesis may therefore explain, at least in part,
decreased Nm in a variety of plant tissues.
Elevated CO2-mediated nitrogen loss hypothesis
While many authors have considered possible CO2 effects on N acquisition, only
one study that we are aware of has considered the possibility that elevated CO2 decreases
Nm by affecting the rate of plant loss of N (Table 1; Hypothesis 9). Pang et al. (2006)
examined N relations in rice grown in pots of nutrient solution under free-air carbon
dioxide enrichment. They documented that N loss per pot was greater under elevated than
ambient CO2 at both high and low N supply. They attributed this N loss to volatilization
of NH3 from senescing plant tissues, and possibly to root exudation of organic N, and
suggested that these increases in N loss were responsible for the observed decreases in
Nm.
Closer examination of their data suggests that other mechanisms must have also
been operating. In their experiment, whole-plant Nm (recalculated from their data) was
decreased under elevated CO2 by 26.4% and 26.5% at low and high N, respectively. Had
all of the N lost from pots been retained in the plant tissues, Nm would still have been
decreased under elevated CO2 by 21.4 and 19.1% at low N and high N, respectively.
Effects of elevated CO2 on N loss therefore may have played a role in the observed
decrease in Nm under elevated CO2, but other mechanisms were probably more
important. Whether the effect of elevated CO2 on N loss is particular to this system also
appears to be unknown. Loss of N from senescing leaves does not appear likely to
explain the decreases in Nm seem in many experiments in young, non-senescent tissues.
Hypothesis of ontogenetic drift in N concentration
Coleman et al. (1993) proposed that the observed effects of elevated CO2 on Nm
may be ontogenetic rather than functional. Plants grow more quickly under elevated than
ambient CO2. Comparisons between elevated and ambient CO2-grown plants of the same
age are therefore comparisons between plants of different sizes. For seedlings, Nm often
decreases during early ontogeny. Differences in Nm between elevated and ambient-CO2
grown plants may therefore simply reflect the fact that the plants are of different sizes
rather than any specific effect of CO2 on plant physiology.
Coleman et al. (1993) presented data showing that for two annual species,
seedlings grown under elevated CO2 had lower Nm than ambient-grown seedlings when
compared at identical ages. When the comparison was made between elevated and
ambient-grown plants at the same size, the difference disappeared.
Subsequent studies have in general not fully replicated this finding. The effect of
elevated CO2 in some studies is less when compared at the same size rather than the same
age, but allometric analyses typically show differences in Nm between elevated and
ambient grown plants that are independent of plant size (Bernacchi et al. 2007, Harmens
et al. 2001, Lutze and Gifford 1998, Marriott et al. 2001). Some studies also show an
effect of CO2 on Nm, with little or no evidence for ontogenetic drift in Nm (den Hertog et
al. 1996, Lutze and Gifford 1998, Marriott et al. 2001).
Ontogenetic drift also appears unlikely to explain elevated CO2-mediated
differences in Nm seen in perennial plants after more than one season of growth (e.g.
Curtis and Wang 1998, Ellsworth et al. 2004) or between seeds compared at full maturity
(e.g. Jablonski et al. 2002, Taub et al. 2008). Overall, ontogenetic drift in Nm appears
likely to play only a minor role in creating the general pattern of decreased Nm under
elevated CO2.
Conclusions
A variety of physiological effects of elevated CO2 on plants have been proposed
that could potentially influence plant tissue concentrations of N. It is possible that many
or even all of these mechanisms genuinely operate in plants, at least for particular species
or under particular environmental conditions. Some mechanisms, such as increases in
mycorrhizae or increased capacity for N uptake at root surfaces, appear likely to affect
Nm in a positive direction. Other mechanisms, such as biomass dilution, decreased
transpiration, decreased efficiency of root architecture and increased N loss are likely to
lead to decreased Nm.
A substantial number of literature surveys are in agreement that the mean effect of
elevated CO2 on Nm is a 10-15% decrease (Ainsworth and Long 2005, Cotrufo et al.
1998, Curtis and Wang 1998, Jablonski et al. 2002, Norby et al. 1999, Taub et al. 2008).
This suggests that physiological changes leading to decreased Nm under elevated CO2
predominate in their effects over factors that would tend to increase Nm.
We suggest that the predominant mechanisms by which elevated CO2 affects Nm
are dilution of N in plant tissues by increased concentrations of compounds derived from
photosynthate, and decreases in root specific N uptake. Decreased specific uptake is
likely due both to decreased demand by the plant (due to increased photosynthetic
nitrogen use efficiency and to downregulation of photosynthetic enzymes) and to
decreased ability of the soil-root system to supply N. While a number of mechanisms
have been proposed that might account for this decreased N supply, we suggest that
decreased transpiration-driven mass flow of N is the mechanism that is best supported by
the available evidence.
Two additional mechanisms appear particularly worthy of additional
investigation. Both decreased efficiency of root system architecture (Berntson 1994) and
increased loss of N by plants under elevated CO2 (Pang et al. 2006) have received
experimental support as possible mechanisms contributing to decreased Nm. However, in
each case this is based (to the best of our knowledge) on a single study, and additional
studies are clearly needed if these mechanisms are to be substantiated.
Acknowledgments
We thank the Cullen Fund of Southwestern University for financial support (to DRT).
Lisa Anderson helped in obtaining literature. Jim Coleman and Kelly McConnaughay
provided helpful discussion of their research, and the reviewers and editor provided
helpful suggestions on the manuscript.
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Table 1: Hypotheses to account for the decrease in tissue N concentrations under elevated
[CO2]. Papers cited discuss, but do not necessarily endorse, the hypotheses under
question.
Hypothesis
Selected references
1
Dilution by carbohydrates
1, 2, 3
2
Dilution by secondary compounds
1
3
Decreased N uptake due to decreased transpiration
4, 5, 6, 7
4
Less efficient root architecture
8, 9, 10
5
Altered root uptake capacity
9, 11
6
Altered mycorrhizal status
11, 12
7
Increased N efficiency
13, 14
8
Downregulation of photosynthesis
1, 15, 16
9
Increased N loss
17
10
Ontogenetic drift of N concentration
18, 19
1
(Gifford et al. 2000) 2(Kuehny et al. 1991) 3(Wong 1990) 4(Van Vuuren et al. 1997) 5(Del Pozo et al. 2007)
6
(McDonald et al. 2002) 7(Conroy and Hocking 1993) 8(Pritchard and Rogers 2000)
9
(Berntson and Bazzaz 1996) 10(Lynch and St.Clair 2004) 11(BassiriRad et al. 2001)
12
(Alberton et al. 2005) 13(Stitt and Krapp 1999) 14(Conroy 1992) 15(Fangmeier et al. 1999)
16
(Fangmeier et al. 2000) 17(Pang et al. 2006) 18(Coleman et al. 1993) 19(Bernacchi et al. 2007)
Paper
Coleman and Bazzaz (1992)
Coleman and Bazzaz (1992)
Coleman and Bazzaz (1992)
Coleman and Bazzaz (1992)
Israel et al. (1990)
Israel et al. (1990)
Israel et al. (1990)
Rogers et al. (1992) *
Zerihun et al. (2000)
Zerihun et al. (2000)
Zerihun et al. (2000)
Larigauderie et al. (1994)
Larigauderie et al. (1994)
BassiriRad et al. (1996)
BassiriRad et al. (1996)
McDonald et al. (2002)
Vivin et al. (1996)
Species
Abutilon theophrasti
Abutilon theophrasti
Amaranthus retroflexus
Amaranthus retroflexus
Glycine max (nonnodulated)
Glycine max (nonnodulated)
Glycine max (nonnodulated)
Glycine max (nonnodulated)
Helianthus annuus
Helianthus annuus
Helianthus annuus
Pinus taeda
Pinus taeda
Pinus taeda
Pinus ponderosa
Populus deltoides
Quercus robur
Conditions
28 degrees
38 degrees
28 degrees
38 degrees
Method and duration of N-uptake
measurements
Sequential harvests (20 days)
Sequential harvests (20 days)
Sequential harvests (20 days)
Sequential harvests (20 days)
Single harvest (27 days)
High N, High P
Root specific uptake rate
under elevated CO2 as %
of that under ambient CO2
59.6%
60.6%
56.6%
76.7%
89.2%
Single harvest (27 days)
High N, low P
103.1%
Single harvest (27 days)
Low N, High P
87.2%
Single harvest (18 days)
Low N
Medium N
High N
Low N
High N
Sequential harvests (20 days)
Sequential harvests (20 days)
Sequential harvests (20 days)
Sequential harvests (117 days)
Sequential harvests (117 days)
+
Uptake of 15NH4 (48 hours)
15
Uptake of NH4+(48 hours)
Uptake of 15NO3- (7 days)
Uptake of 15NO3- (12 hours)
mean (across all studies)
median (across all studies)
90.7%
71.4%
100.0%
76.9%
79.2%
122.9%
82.6%
79.3%
86.4%
100.0%
83.6%
82.6%
Table 2: Effect of growth under elevated CO2 on root specific uptake rates (i.e. uptake per gram root) in studies performed on intact
plants rooted in solid media. When a time-series was reported, measurements are those from the period of greatest uptake rate.
Sequential harvest techniques estimate uptake by integrating root mass (or area) and plant N content over the interval between two
harvests at which these are measured. The single harvest technique uses a single harvest to obtain the root mass (or area) and N
measurements at the end of the experiment. As Israel et al. (1990) point out, this is better thought of as an index of relative N uptake
rather than a true estimate of specific uptake. * uptake per root surface area rather than weight.
Figure Legends
Figure 1. Graphical vector analysis of the effect of elevated CO2 on leaf concentrations of
N and non-structural carbohydrates (NSC) in four experiments. All data values are
percents relative to the value at ambient CO2, with the large diamond at (100,100)
representing the value of all measurements under ambient CO2. All other data points are
for plants under elevated CO2. Diagonal lines indicate relative leaf mass (i.e. leaf mass
under elevated CO2 as a percentage of that under ambient CO2). See text for further
explanation. Data is taken from: 1- Pettersson and McDonald (1992) 2,3- Runion et al.
(1999), -0.5 Mpa, -1.5Mpa water potential, respectively 4- Lewis et al. (2002).
Figure 2. Effect of elevated CO2 on macronutrient concentrations in the edible portions of
food crops of studies that measured all elements in the same tissues (n=42). Results are
from an unpublished meta-analysis of the relevant research literature (D. Taub and X.
Wang). Geometric means and bootstrapped 95% confidence limits (Adams et al. 1997).
Vertical dashed line indicates no effect of elevated CO2.
Figure 1:
40
Relative Leaf Mass
80
100
60
Relative N% (open symbols), Relative NSC% (closed symbols)
200
180
120
160
140
140
160
120
180
100
80
60
60
80
100
120
140
160
180
200
Relative N content (open symbols), Relative NSC content (closed symbols)
1 - Betula pendula
2 - Pinus palustris (-0.5 Mpa)
3 - Pinus palustris (-1.5 Mpa)
4 - Xanthium strumarium
1 - Betula pendula
2 - Pinus palustris (-0.5 Mpa)
3 - Pinus palustris (-1.5 Mpa)
4 - Xanthium strumarium
Figure 2:
N
P
K
Ca
Mg
-25
-20
-15
-10
-5
0
Percent decrease in concentration under elevated CO2
5