Introduction
Uncertainty in Earth system model projections of our future climate is
largely driven by a lack of understanding and model representation of
ecosystem processes associated with CO2 assimilation and
storage by the terrestrial biosphere
(Friedlingstein et al .,
2014; Lovenduski & Bonan, 2017). Photosynthesis is the largest carbon
flux on the planet and the gatekeeper process for an uncertain
terrestrial carbon sink (Le Quere et al ., 2016). Terrestrial
biosphere models (TBMs) are particularly sensitive to structural and
parametric representation of photosynthesis (Friend, 2010; Bonanet al ., 2011; LeBauer et al ., 2013; Rogers, 2014; Sargsyanet al ., 2014; Rogers et al ., 2017; Ricciuto et al .,
2018). Photosynthetic capacity, specifically the apparent maximum
carboxylation capacity of Rubisco at 25 °C
(Vcmax,25 ), is a key model input that drives
considerable uncertainty in TBM projections
(Friend, 2010; Bonan et
al ., 2011; LeBauer et al ., 2013; Sargsyan et al ., 2014).Vcmax,25 is further used to derive the maximum
rate of electron transport (Jmax ), the triose
phosphate utilization rate (when implemented) and respiration (R )
(e.g. Sitch et al ., 2003; Rogers et al ., 2014; Lombardozziet al ., 2018). If this key parameter shows significant diurnal
variation, the implications for TBM projections of CO2assimilation could be notable.
Terrestrial biosphere models (TBMs) typically representVcmax as a fixed parameter (Rogers, 2014) but
with some consideration of other factors such as day length (Bauerleet al ., 2012), temperature acclimation
(Kattge & Knorr, 2007;
Lombardozzi et al ., 2015; Smith et al ., 2015), and
emerging potential for covariation with environmental drivers (Aliet al ., 2015; Smith et al. 2019). Only a few studies have
investigated diurnal variation in Vcmax (Singsaaset al. , 2000; Kets et al. , 2010; Nascimento & Marenco,
2013). In vitro , Rubisco activation state changes rapidly with
irradiance (Salvucci & Anderson, 1987; Parry et al ., 1997),
shows diurnal variation (Sage et al. , 1993; Pérez et al. ,
2005), and is subject to regulation by Rubisco activase (Portis, 2003;
Sage et al ., 2008), which could contribute substantially to
diurnal variations in Vcmax . However, in
vitro and in vivo data on Rubisco activation state can vary
markedly (Rogers et al ., 2001; Sharwood et al ., 2017), and
without an easy way to assess activation state in vivo , and an
approach to incorporate in vitro measurements into TBM
formulations, a gas exchange approach to measuring Rubisco activity is
desirable.
While there is a paucity of data on whether diurnal changes inVcmax occur (see
Singsaas et al. , 2000;
Kets et al. , 2010; and Nascimento & Marenco, 2013 for examples),
there are many studies investigating diurnal and circadian patterns in
gas exchange parameters. Net CO2 assimilation
(Anet ) is known to vary diurnally
(Leverenz, 1981; Epron et
al. , 1992; Singsaas et al. , 2000; Panek, 2004; Leakey et
al. , 2004; Harrison et al. , 2010; Kets et al. , 2010;
Nascimento & Marenco, 2013; Bader et al. , 2016), which can be
driven by environmental changes. There is a midday depression in net
CO2 assimilation that has been related to vapor pressure
deficit and water relations (Tenhunen et al ., 1984; Rodà, 1999),
whereby stomatal conductance mediates a supply-driven change in carbon
assimilation (Leverenz, 1981; Epron et al. , 1992; Harrisonet al. , 2010; Resco de Dios et al. , 2016a,b) and balances
the need to fix carbon with preventing water loss (Matthews et
al ., 2017), although circadian changes in Anetand gs are decoupled from one another (Doddet al ., 2004; Resco de Dios, 2017). Brodribb & Holbrook (2004)
found that leaf hydraulic conductance declines over the day, which may
mediate declines in mesophyll conductance (gm )
(Bickford et al ., 2009; Flexas et al ., 2013), reducing
chloroplastic CO2 supply (and thereforeAne t) later in the day and may
even mediate changes in stomatal behaviour (Sack et al ., 2016).
Nardini et al . (2005) found that leaf hydraulic conductance
(Kleaf ) was under circadian regulation inHelianthus annuus , which was the cause of diurnal oscillations inKleaf . There may be further changes in realized
quantum yield of photosynthesis that result from delays in recovering
from photoprotection or photodamage throughout the day, limiting energy
available for carbon fixation (Long & Humphries, 1994; Gamon, 2015;
Kromdijk et al ., 2016). As well, there are diurnal shifts in
carbohydrate accumulation, and this can lead to feedback inhibition of
photosynthesis (Sun et al ., 1999). In this way, diurnal changes
in net CO2 assimilation can be driven by both supply and
demand of substrates, and these diurnal changes in gas exchange scale up
to the canopy level (Resco de Dios, 2016a). Many of the diurnal changes
in Anet outlined above are due to diurnal
environmental changes which models can mimic well. However, it is
unclear whether there may be diurnal variation inVcmax , and if there is, diurnal variation inVcmax may present a simple way to account for the
effect of diurnal changes in leaf carbon exchange in models.
Current approaches for measuring Vcmax in vivorequire measurement of the response of photosynthesis (A ) to
internal CO2 concentration (Ci )
which can take over an hour for a single measurement (Bernacchi et
al ., 2003). Recently, Stinziano et al . (2017) developed a method
for the rapid measurement of the A-Ci response
(the RACiR technique). The dramatic shortening of measurement time
enables the collection of high-resolution diurnal patterns in apparentVcmax and apparent Jmax(Stinziano et al ., 2017, 2019ab; Coursolle et al ., 2019;
Lawrence et al ., 2019). In addition, this new technique provides
values for parameters measured in vivo that are directly
applicable to current TBM model formulations and enables measurement of
diurnal dynamics under circumstances where in vitro work cannot
be done, e.g. where sampling constraints in remote locations are
logistically challenging, or when secondary compounds limit the ability
to successfully extract and measure Rubisco activity. Studies assessing
TBM performance on a diurnal scale are limited (in some cases due to
temporal resolution of the models). in the case of ORCHIDEE, carbon
fluxes are consistently over-estimated relative to eddy covariance data
later in the day across plant functional types (Krinner et al .,
2005), while the Community Atmosphere Model (CAM4 and CAM5)
over-estimates latent heat fluxes later in the day at mid-latitude and
boreal regions (Lindvall et al ., 2012) suggesting an
over-estimation of transpiration, which would imply overestimations of
stomatal conductance, Ci , andAnet . These discrepancies may be related to
endogenous rhythms in ecosystem-level gas exchange (Resco de Dioset al ., 2012) that are currently unaccounted for.
Our objective was to determine whether diurnal variation inVcmax occurs, and if so, the extent to which such
variation affects leaf-level gas exchange modeling. Here we show that
the RACiR technique can be used to successfully measure diurnal
variation in Vcmax . We demonstrate that diurnal
variation in Vcmax is variable across 11 species
from several plant functional types, leading to a variable effect on
modelled leaf-level gas exchange, underscoring the need to consider
diurnal dynamics in Vcmax when modeling.