Introduction
The heat tolerance of plants’ photosystem II (PSII) photochemistry may
provide a useful estimate of the upper thermal limit of photosynthesis,
and has the potential to explain the physiological mechanisms underlying
some of the ecological responses of plants to climate change (Clark,
Piper, Keeling & Clark 2003; Doughty & Goulden 2009; Mau, Reed, Wood
& Cavaleri 2018; Pau, Detto, Kim & Still 2018; Feeley, Fadrique, Perez
& Zuleta 2020). Higher heat tolerance of PSII photochemistry is
generally assumed to allow for improved growth, reproduction, and/or
survival in hot environments, presumably by allowing for photosynthesis
at higher temperatures (Krause, Winter, Krause & Virgo 2015; Feeley,
Martinez-villa, Perez & Duque 2020a; Perez & Feeley 2020; Tiwariet al. 2020). However, these assumptions have not been widely
tested and it is unclear how PSII heat tolerance integrates with
different thermal strategies that may be important for determining the
impacts of climate change.
Heat tolerance of PSII is commonly measured using chlorophyll a fluorescence. Early studies to adopt the use of chlorophyll fluorescence
quantified PSII heat tolerance using the F0 fluorometric
parameter - indicating the number of maximally open reaction centers -
and found it was correlated with the temperature that caused carbon
assimilation to approach zero (Tmax; Downton, Berry &
Seemann 1984; Seemann, Berry & Downton 1984). However,
F0 can provide biased estimates of PSII function during
heat treatments that change leaf optical properties (Baker 2008), which
has led many researchers to adopt the maximum quantum yield
(FV/FM) fluorometric as a more robust
metric for estimating PSII heat tolerance where FV =
FM - F0, and FM indicates closed reaction centers in saturating light (Maxwell &
Johnson 2000; Baker 2008)
Although FV/FM can reliably measure PSII
function under stress treatments and is commonly used to measure PSII
heat tolerance, FV/FM may not be a
reliable proxy for carbon assimilation under field conditions.
FV/FM is only proportional to carbon
assimilation under low light conditions and when photorespiration is
minimized (Brooks & Farquhar 1985; Baker 2008). These conditions are
not met in the field when leaves experience high light and temperatures.
Few studies have tested if FV/FM heat
tolerance promotes carbon assimilation in hotter environments, but
empirical evidence and ecological theory generally support this
assumption.
As was shown with heat tolerance estimates that used F0(Downton et al. 1984; Seemann et al. 1984), one way the
PSII heat tolerance could promote photosynthesis at higher temperatures
is if it is correlated with Tmax. Reported values for
Tmax range from 40.1 to 41.8˚C and
are comparable to the temperatures that cause the first signs of damage
in FV/FM (Tcrit) for
tropical species (Fig. 1a ; Slot et al. 2018; Tiwariet al. 2020; Perez and Feeley 2020). Coordination between
Tcrit and Tmax would provide support for
the hypothesis that PSII heat tolerance fixes the upper limit of carbon
assimilation by limiting electron transport (Slot & Winter 2017a).
Another way that PSII heat tolerance could promote carbon assimilation
at higher temperatures is by increasing the breadth of temperatures over
which carbon assimilation can occur (Ω; Fig. 1a ; Cunningham S.
C. & Read J. 2003; Slot & Winter 2017a). The Ω metric can be used to
characterize plants as physiological thermal generalists vs.
specialists, similar to what is done with animal species (Huey & Hertz
1984; Ghalambor, Huey, Martin, Tewksbury & Wang 2006; Huey 2012). A
positive correlation between PSII heat tolerance and Ω would be
consistent with a thermal generalist strategy of carbon assimilation and
would provide a physiological explanation for why thermal specialist
plant species are more susceptible to climate change than generalist
plants (Janzen 1967; Ghalambor et al. 2006; Perez, Stroud &
Feeley 2016). Indeed, Ω is a key trait linking leaf
thermoregulation to the “fast-slow” leaf economic spectrum (Michaletzet al. 2015, 2016). Since variation in PSII heat tolerance is
driven by high leaf temperature (Perez & Feeley 2020) and ‘fast’
species are expected to have high leaf temperatures and large Ω
(Michaletz et al. 2015, 2016), PSII heat tolerance is expected to be
proportional to Ω.
Plants with ‘fast’ resource acquisition strategies are characterized in
part by their high rates of carbon assimilation (Wright et al.2004; Reich 2014). The plant economic spectrum typically proposes that
‘fast’ strategies are characterized by poor physiological tolerances
(Reich 2014), such that the optimum rates of photosynthesis
(Popt, Fig. 1a ) and PSII heat tolerances may be
inversely proportional. Conversely, since ‘fast’ species are also
characterized by high leaf temperature (Michaletz et al. 2015,
2016), PSII heat tolerance may be positively correlated to
Popt. This expectation is consistent with the idea that
high PSII heat tolerance is beneficial for plants growing in hot
environments.
The optimum temperature for carbon assimilation (Topt, Fig. 1a ) is another important parameter that describes carbon
assimilation as a function of temperature and is potentially coordinated
with PSII heat tolerance. For example, species tend to increase in both
their PSII heat tolerance and Topt when grown in hotter
environments (Valladares & Pearcy 1998; Way & Yamori 2014; Zhuet al. 2018). High PSII heat tolerance may promote increases in
Topt by improving electron transport or the availability
of ATP and NADH at high temperatures (Genty, Briantais & Baker 1989;
Maxwell & Johnson 2000; Baker 2008), in support of the assumption that
PSII heat tolerance will facilitate carbon assimilation in hot
environments.
In this study we measured three common metrics of PSII heat tolerance
that indicate the temperatures that cause an initial, 50%, and 95%
decrease in FV/FM(Tcrit, T50 and T95,
respectively; Fig. 1b ). We compared these metrics of heat
tolerance to Tmax, Popt,
Topt, and Ω for 21 plant species grown in a quasi-common
garden environment (Fairchild Tropical Botanic Garden, Coral gables FL
USA; Perez et al. 2019). We tested four hypotheses consistent
with the assumption that high PSII heat tolerance promotes carbon
assimilation in hotter environments. Specifically, we looked at the
correlations among the different metrics of heat tolerance and carbon
assimilation, after controlling for any potential effect of phylogenetic
non-independence, to test the hypotheses that H1) Tmaxis constrained by PSII heat tolerance; H2) high PSII heat tolerance is
indicative of a thermal generalist strategy of carbon assimilation; H3)
high PSII heat tolerance is characteristic of species with “fast”
carbon acquisition strategies; and H4) high PSII heat tolerance promotes
higher Topt (Fig. 2 ).