Tree Physiology 35, 581–584
doi:10.1093/treephys/tpv059
Commentary
Where does the carbon go?—Plant carbon allocation under
climate change
Sanna Sevanto1,2 and L. Turin Dickman1
1Earth
and Environmental Sciences Division, Los Alamos National Laboratory, Bikini Atoll Road MS J495, Los Alamos, NM 87545, USA; 2Corresponding author ([email protected])
Received April 6, 2015; accepted May 13, 2015; handling Editor Danielle Way
The ability of terrestrial vegetation to both take up and release carbon and water makes understanding climate change effects on
plant function critical. These effects could alter the impacts and
feedbacks of vegetation on climate and either slow down or accelerate climatic warming (­Bonan 2008). As a result, studies on plant
responses to increased atmospheric CO2 concentration and elevated temperatures have become abundant in the last 20 years (for
reviews, see ­Way and Oren 2010, ­Franks et al. 2013). Predictions
of future increases in the frequency and severity of drought in
many areas of the world (­IPCC 2013) have also led to an emphasis
on plant drought responses and tolerance to climate change
(­McDowell et al. 2008, Adams et al. 2009, ­Breshears et al. 2009,
­Allen et al. 2010). Changes in the environment, however, will not
occur separately, and the combined effects of two or more global
change factors will likely be complex (e.g., ­Norby and Luo 2004).
There is evidence, for example, that increased atmospheric CO2 and
temperature may increase plant productivity, resource-use efficiency
and growth rates (e.g., ­Drake et al. 1997, ­Wullschleger et al. 2002,
­Way and Oren 2010). But these changes could lead to changes in
structure and hydraulics that increase drought vulnerability (­Maherali
and DeLucia 2000, ­Wullschleger et al. 2002, ­Way et al. 2013).
Further, increased atmospheric CO2 concentration may increase
plant water-use efficiency (e.g., ­Franks et al. 2013) while elevated
temperature may reduce it (­Way et al. 2013). To predict future
vegetation changes and the influence of these interactions correctly,
parsing plant responses as independent factors is essential. For
understanding ecosystem-scale responses and verifying models,
combined effects have to be quantified.
Allocation of carbon to different plant organs is central to this
discussion and provides a mechanism by which plants can adapt
to changes in the environment (­Chaves et al. 2002). The term
‘allocation’ has been used to describe everything from fine-scale
carbon dynamics within a plant to coarse-scale carbon dynamics
within an ecosystem (e.g., ­Litton et al. 2007, ­Epron et al. 2012).
Measuring and defining it in a meaningful way has therefore
become one of the greatest challenges in plant science. In a review
of carbon allocation in forests, ­Litton et al. (2007) defined three
constituents of allocation for use in the context of forest ecosystems: biomass (the amount of material present); flux (carbon flow
to a component per unit time); and partitioning (the fraction of
gross primary productivity used by a component). When working
on the individual scale, however, it is important to distinguish
between the mass of all organic components (biomass) and the
carbon quantity in a component (concentration), which is a subset
of the former. When evaluating allocation under stress, it is also
important to distinguish partitioning of recent photosynthates
(none if stomata are closed) from partitioning or redistribution of
carbon stores. The utility of each definition varies depending on
the problem at hand and the measurement techniques available.
For example, to model ecosystem carbon cycling at a seasonal
time scale, measuring carbon allocation using biomass is sufficient
to capture ecosystem response (e.g., ­De Kauwe et al. 2014). But
if the goal is to model climate-induced vegetation mortality mechanistically (for review of theories, see e.g., ­McDowell 2011), partitioning and fluxes during and after environmental stress (e.g.,
drought) become important (­Xu et al. 2013). If, for example, carbon is stored in leaves, as is typical during drought (­Sala et al.
2010 and references therein), but cannot be transported to roots
following drought, lack of resources available to re-establish soil–
root connection may result in plant mortality. At the individual scale,
measuring changes in biomass or concentration is easier than capturing fluxes, so the former are often used as indicators of carbon
movement. Yet changes in fluxes could be the only indicator of a
stress response and therefore critical to measure.
Published by Oxford University Press 2015. This work is written by (a) US Government employee(s) and is in the public domain in the US.
582 Sevanto and Dickman
In this issue, Blessing et al. (2015) present a unique study to
determine the effects of drought and elevated temperature on
allocation. They used 13CO2 pulse labeling to track the recovery
of 13C in different tissues and compounds of beech saplings
during a 9-day chase period. This method offers an elegant way
to measure all three allocation constituents by tracking transport
velocity (flux), distribution (partitioning) and concentration (biomass) of labeled photoassimilates. The authors’ evaluation of
several compounds in which the carbon label could be incorporated and use of this technique in conjunction with both temperature and water manipulation allows for assessment of
allocation priorities under climate change-type stress.
Evaluation of diverse carbon-containing compounds, in addition to the traditionally measured starch and simple sugars
(sucrose, glucose and fructose), is critical for evaluating tree
mortality mechanisms—in particular, the carbon starvation
hypothesis. If these compounds serve as energy reserves or are
essential for cellular metabolism or osmoregulation, they may
play important roles in postponing starvation (­Sala et al. 2010)
or maintaining phloem turgor (see ­Sevanto et al. 2014). Analyzing these compounds could also shed light on how partitioning
between primary growth or storage and stress defense mechanisms is altered by drought and elevated temperatures. Starch
and simple sugars are known to be the primary substances
responsible for growth and storage (­Heldt and Piechulla 2004).
Consistent with the literature, Blessing et al. (2015) found rapid
increases in labeled carbon in leaf sugars and starch, followed
by a rapid decline as recent photoassimilates were transported
from the leaves to the roots in preparation for autumnal root
expansion and long-term storage, as indicated by sustained
residence of the carbon label in root starch. These results highlight the different functions of starch in different tissues, and the
importance of root sampling in order to capture tree carbon
storage. Amino acids and organic acids have been shown to
increase in concentration under stress in many plants (e.g.,
­López-Bucio et al. 2000), suggesting the use for stress defense
such as osmoregulation (­Fougere et al. 1991) or controlling
cell-wall properties (see e.g., ­López-Bucio et al. 2000). Despite
apparently low partitioning of newly assimilated carbon to acidic
compounds in Blessing et al. (2015), this is one of the few
studies addressing possible changes in partitioning to these
compounds. Under changing environment, similar studies are
needed before the consequences of climate change on vegetation can be thoroughly understood and modeled mechanistically.
In combining these comprehensive methods for carbon allocation assessment with drought and temperature manipulation,
Blessing et al. (2015) provided a template for future studies of
plant physiological response to climate change. Based on current
knowledge, the effects of drought and elevated temperature on
allocation are varied (Figure 1) and depend on the impacts of
many factors—including species and habitat (­Way and Oren
2010); life cycle stage (both seasonality and age; see ­Way and
Tree Physiology Volume 35, 2015
Oren 2010); drought severity (­McDowell and Sevanto 2010, ­Sala
et al. 2010); temperature elevation (­Atkin and Tjoelker 2003);
treatment interactions; and duration of the study (­Way and Oren
2010)—on the allocation component in question. Relatively mild
drought is generally thought to increase partitioning to roots to
the detriment of aboveground organs, as shown by Blessing et al.
(2015). But more severe drought could result in reduced flux and
partitioning belowground (Figure 1) if the transport pathway is
disrupted or stress defense mechanisms aboveground require a
larger portion of the limited carbon supply. Though Blessing et al.
(2015) found no significant differences in minimum transport
times (maximum transport velocity) among treatments, they did
observe longer mean transfer time of recent photoassimilates to
the roots with elevated temperature. This could have serious
implications for plant vigor or recovery from drought under future
climates, as severe disruptions in carbon transport can lead to
starvation and mortality of tissues downstream (­McDowell and
Sevanto 2010, ­Sala et al. 2010). Given the important function of
roots as carbon storage organs, this decoupling of shoot source
from root sink could impair a plant’s ability to buffer stress under
climate change. Elevated temperatures generally increase aboveground partitioning and growth in temperature-limited (high latitude, high altitude) environments (Way and Oren 2012, see also
­Allen et al. 2010), while, as seen by Blessing et al. (2015), they
have little or no effect on carbon concentrations in roots. But if
heat increases to the limit of plant tolerance, higher partitioning of
resources to these tissues for damage control and repair can be
expected. Elevated temperature may also increase metabolic
rates, increasing soil CO2 efflux (as observed by Blessing et al.
2015) and plant respiration (­Atkin and Tjoelker 2003, ­Smith and
Dukes 2013), potentially shifting plants from carbon sinks to carbon sources. Lack of consistency in treatments and their severity
relative to plant tolerance (Figure 1) makes the synthesis of the
effects of changing climate on plant function almost impossible,
and calls for a metric to allow for comparison. In plant hydraulics,
the concept of safety margins (drought severity relative to plant
hydraulic failure limits; see e.g., ­Meinzer et al. 2009; ­Skelton et al.
2015) is an attempt at such relativization. Blessing et al. (2015)
provided the first steps toward quantifying response thresholds
for carbon allocation by defining an ‘excess carbon’ scale to allow
for comparison of partitioning between individuals of differing tissue biomass. In both cases of hydraulics and carbon dynamics,
however, we are still far from understanding how response thresholds and points of no return should be defined to allow predictions of vegetation changes under changing climate (Figure 1).
In addition to determining tipping points and placing current
conditions relative to tipping points, we need to understand
cause–response relationships to model allocation changes
mechanistically. The various components of carbon allocation
mentioned here are outcomes of many interacting processes
(­Cannell and Dewar 1994, ­Brüggemann et al. 2011), and
detecting whether a shift in biomass, concentration, flux or
Plant carbon allocation under climate change 583
Figure 1. A schematic of potential outcomes for above- (top panel) and belowground (bottom panel) carbon (C) allocation (defined here as partitioning) and carbon transport velocity (flux, middle panel) under changing drought and heat conditions based on current knowledge. Uses of carbon
above- and belowground are indicated on the left. Vertical dashed lines indicate possible tipping points along the stress continuum relative to optimal
conditions for some plant groups or species, with tipping points for transport connected to responses in partitioning. These locations are uncertain,
and the relative locations of heat vs drought conditions and optimal conditions vs tipping points are not fixed. The dashed lines joining the curves
indicate possible variation in responses, and question marks indicate knowledge gaps. Optimal conditions are defined in relation to longevity and resilience to stress rather than maximum productivity. Comments in blue and red highlight current hypotheses for heat and drought responses assuming
that the carbon source is not limited. For drought, higher stress indicates drier conditions and lower stress more moist conditions. For heat, higher stress
can be caused by temperatures that are either too high or too low.
­ artitioning is the cause or response (active or passive) to some
p
other physiological change is a challenge. Although data interpretation for carbon-labeling studies is limited by label-detection
methods and possible label dilution, which can make determination of tissue carbon budgets difficult, studies like that of Blessing et al. (2015) that measure fluxes combined with partitioning
and biomass show a path toward this goal, one that is becoming
increasingly important for improving predictions of climateinduced vegetation changes (­Xu et al. 2013). Reallocation of
stored carbon seems to play a crucial role in plant survival strategies (­Dietze et al. 2014, ­Dickman et al. 2015, see also ­Klein
and Hoch 2015) and studies that can quantify this redistribution
and reuse are critical for the new generation of models to predict
vegetation dynamics of the future.
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