The ‘peculiar shade nature’ of cyanic leaves: a perspective in
anthocyanin research
Though cyanic leaves have a suite of morphoanatomical- and
biochemical-related traits that closely resemble those usually displayed
by green leaves growing in low light (true shade leaves), they also
display features that are uncommon in shaded green leaves. First, while
shade leaves typically saturate photosynthesis at much lower PPFD
compared to sunny leaves, photosynthesis in cyanic leaves saturates at
very similar or even higher PPFD than do the green counterparts (Fig.
3). This results simply on the ability of their epidermal anthocyanin
filter in effectively absorbing photons otherwise available to
chlorophylls, especially to Chlb: the actual quantum
yield for CO2 assimilation is lower at moderate or
greater at high light irradiance in red compared to green leaves
(Tattini et al., 2014; 2017, Fig. 3). There is evidence indeed that red
leaves have higher photosynthesis during the central hours of the day
(Tattini et al., 2017), thus adding further support to the effective
photoprotective functions of anthocyanins. Second, stomatal conductance
in red leaves is higher or very similar compared to that of green leaves
(Liakopoulos et al., 2006; Nikoforou et al., 2011; Tattini et al.,
2017). This is unusual for true shade leaves, in which the excess of
green compared to blue (and red) photons opposes the opening and the
development of stomata (Chen, Xiao, Li, & Ni, 2012; Poorter et al.,
2019). However, cyanic leaves sense both higher blue/green and red/green
ratio compared to true shade leaves, and this may promote stomata
opening (Smith et al., 2017). The matter deserves further investigation
aimed at evaluating the relative contribution of blue, green and red
signals (Merzlyak et al., 2008) perceived by cyanic leaves, to the
downstream molecular events regulating the development and the aperture
of stomata (Inoue & Kinoshita, 2017; Hiyama et al., 2017; Kang, Lian,
Wang, Huang, & Yang, 2009).
The profound morpho-anatomical adjustments imposed by the epidermal
anthocyanin shield makes complex the analysis of the ‘photosynthetic
performance’ of cyanic vs acyanic leaves and, hence, of the
photoprotective role of anthocyanins. For instance, Tattini et al.
(2017) have shown that mesophyll conductance to CO2(gm) is substantially lower in purple than in green
basil leaves growing in full sunlight (similar results have been
observed in Acer platanoides , Fini unpublished data). This
conforms to previous observations that gm is usually
lower in shaded than in sun-exposed green leaves (Campany, Tjoelker, von
Cammer, & Duursma, 2016; Peguero-Pina et al., 2016). We hypothesize
that the anatomical adjustments imposed by the shade-avoidance response,
such as the accumulation of chloroplasts toward the periclinal cell
walls (Wada, 2016) may force cyanic leaves to ‘unusually high’ stomatal
conductance (compared to green leaves) to counter large limitations to
CO2 diffusion through the mesophyll (Tattini et al.,
2017). As a result, the drawdown from actual (calculated from response
curves of AN to changes in chloroplast
CO2 concentration, AN/Cccurves) to apparent (calculated from response curves of
AN to changes in intercellular CO2concentration, AN/Ci curves)
carboxylation efficiency (Vc,max) was indeed markedly
higher in red compared to green basil leaves (Tattini et al., 2017). The
lower carboxylation efficiency of red compared to the green counterparts
reported in previous studies (Carpenter, Keidel, Pihl, & Hughes, 2014;
Nikoforou, Nikopoulos, & Manetas, 2011; Ranjan et al., 2014) may merit
extensive re-evaluation. In turn, this poses serious methodological
issues regarding the effective photoprotective potential of cyanic vs
acyanic leaves. We recall that photoprotection, a qualitative parameter
in its nature, closely relates to photoinhibition and, hence, suitably
quantified by high light-induced depression of photosynthesis, rather
than photosynthesis per se . However, in most studies the degree
of photoinhibition in cyanic vs acyanic leaves has been estimated
through light-induced declines in Fv/Fm(∆Fv/Fm) and/or ΦPSII(∆ΦPSII). Nonetheless, when leaves largely differ for
both gs and gm, neither
∆Fv/Fm nor ∆ΦPSII are
good proxies of photoinhibition: gs, and particularly
gm are major constraints to photosynthesis, especially
under high light irradiance. We conclude that quantifying the relative
contribution of diffusional limitations to photosynthesis in cyanic vs
acyanic leaves long-exposed to excessive light (when photoprotection
really makes sense) will significantly improve our understanding on the
actual photoprotective role(s) of anthocyanins.