Discussion
We investigated the assumption that heat tolerances promote carbon
assimilation at higher temperatures. We did not find support for our
first hypothesis (H1) that PSII heat tolerance is coordinated with
Tmax. One reason that Tmax may not be
directly correlated with PSII heat tolerance is because it and the
Tmin parameter used to fit Eq. 2 are purported to have
no physiological significance (Cunningham S. C. & Read J. 2003), and
in many cases Tmin is unrealistically low (Slot &
Winter 2017a). It is also likely that stomatal closure ceases carbon
assimilation before the actual thermal limits of plant biochemistry
(i.e. electron transport or NADPH and ATP generation) are reached (Slot
& Winter 2017a b). While PSII heat tolerance and Tmaxwere not correlated we did find limited support for our hypothesis H1
that PSII heat tolerance provides a conservative high-temperature limit
for Tmax. Our estimates of Tmaxcorresponded to the temperatures that caused between 0 and 45% damage
to FV/FM, indicating that
T50 may provide a reasonable upper bound for estimates
of Tmax. On the other hand, our estimates of
Tcrit, which corresponded to temperatures causing
~2% damage to FV/FM,
were still higher than Tmax for one third of our study
species.
The positive correlations we observed between T50,
T95 and Ω support our second hypothesis (H2) that PSII
heat tolerance is characteristic of thermal generalists. This is a
notable result given that it is one of the only examples in plants
providing an explicit physiological mechanism for the macroecological
hypothesis that greater thermal variability should select for broader
physiological tolerance (Janzen 1967; Perez et al. 2016).
Specifically, our results showed that species with the greatest thermal
ranges for photosynthesis also tend to have the highest PSII heat
tolerances. These results are generally consistent with the predictions
of leaf thermoregulatory theory. Deviations from this expectation may occur if there are acclimatory shifts of the PSII heat tolerance or
photosynthetic traits away from their optimal values for which the leaf
thermoregulatory theory was developed. However, these these deviations from theoretical trait
relationships are unlikely given our resuls.
The negative correlations that we observed between
T50, T95 and Popt does
not support our hypothesis H3 as proposed in accordance with leaf
thermoregulatory theory. Instead these results are consistent with the
prediction that species with low carbon assimilation rates are likely to
exhibit greater stress tolerance (Wright et al. 2004; Reich
2014). Indeed, maintenance of PSII heat tolerance imposes a large
metabolic cost that ‘fast’ species may not be able to incur (see below).
Our final hypothesis (H4) posited that if PSII heat tolerance promoted
greater carbon assimilation at higher temperatures, it should correspond
to higher Topt. However, our results suggest that high
PSII heat tolerance may actually reduce Topt. This
counterintuitive relationship may be explained by the metabolic cost of
maintaining high PSII heat tolerance. PSII heat tolerance is linked to
increased production of heat shock proteins (Wahid, Gelani, Ashraf &
Foolad 2007), isoprenoids (Logan & Monson 1999), photoprotective
pigments (Krause et al. 2015), membrane-fortifying solutes (Hüve,
Bichele, Tobias & Niinemets 2006), and the saturation of lipid bilayers
(Zhu et al. 2018). The production of some of these metabolites
may deplete the pools of NADPH and ATP that are available for carbon
fixation as they are redirected to PSII thermoprotection (Süss &
Yordanov 1986; Gershenzon, 1994; Wahid et al. 2007; Taylor,
Smith, Slot & Feeley 2019; Voon & Lim 2019), explaining why both
Topt and Popt decrease as PSII heat
tolerance increases.
An important assumption we made was that our data were phylogenetically
non-independent before we tested our hypotheses. Given that we measured
species from a diverse set of families and clades (i.e., 21 species in
20 families), the topology and branch lengths of our phylogenetic tree
are likely to provide a reasonable hypothesis of species relatedness.
However, our assumption of phylogenetic non-independence could be
violated if plasticity in PSII heat tolerance and carbon assimilation
actually caused our trait estimates to be unrepresentative of each
species (Way & Yamori 2014; Sastry, Guha & Barua 2018). That said, our
results currently suggest that there is strong covariation between some
PSII heat tolerances and carbon assimilation parameters within
phylogenies. Regardless of any phylogenetic correction, we confirmed
that at the species-level Tmax occurs at lower
temperatures than T50 but not Tcrit, and
that a community’s mean Tcrit may provide a reasonable
approximation for Tmax; however we found little evidence
to support the assumption that heat tolerance promotes carbon
assimilation at high temperatures.
According to our phylogenetically corrected results, the only way that
PSII heat tolerance may promote carbon assimilation at higher
temperatures is by expanding Ω, but this benefit may be offset by
concomitant decreases in Topt and Popt.
This is potentially explained by high PSII heat tolerance promoting
electron transport or the production of NADPH and ATP at high
temperatures (Genty et al. 1989; Baker 2008). We noted that the
heat tolerances that signify greater PSII impairment (i.e., greater
Fv/Fm damage) tended to have stronger correlations with carbon
assimilation parameters. This is consistent with the hypothesis that
larger reductions in the quantum yield have a greater effect on plant
carbon economics, and may explain why Tcrit heat
tolerance was not correlated with any metric of carbon assimilation
(Perez & Feeley 2020). Consequently, T95 may
characterize plant thermal ecological strategies more effectively than
T50, but provide overestimates of Tmax.
Our results suggest that the heat tolerances of PSII measured with
dark-adapted quantum yield (FV/FM) are
not ideal proxies for carbon assimilation. Heat tolerances estimated
with light-adapted quantum yield
(Fq’/Fm’) may be better proxies for
assimilation (although these heat tolerances estimates are also subject
to biases; Baker 2008). Importantly, we show that T50 provides an upper bound for Tmax. We also show that high
PSII heat tolerance is characteristic of thermal generalist plant
species with ‘slow’ carbon acquisition strategies. These results
increase our understanding of the high temperature limits of
photosynthesis and can potentially be used to explain macroecological
patterns in plant responses to climate change. More specifically, since
PSII heat tolerance can characterize thermal specialization, it may
prove as a useful tool for predicting the thermal specialists and
generalists that are hypothesized to be most and least vulnerable to
climate change, respectively (Perez & Feeley 2020).
Acknowledgements: The authors would like to thank Fairchild
Tropical Botanic Garden for providing access to their collections.