Tree Physiology 00, 1–4
doi:10.1093/treephys/tpz005
Commentary
Condensed tannins: arbiters of abiotic stress tolerance?
1,2
Scott A. Harding
1
Warnell School of Forestry and Natural Resources, University of Georgia, Athens, Georgia 30602, USA; 2Corresponding author (sharding@uga.edu)
2370
Received November 19, 2018; accepted January 9, 2019; handling Editor Sanna Sevanto
Gourlay and Constabel (2019) remind us that in temperate for-
ests, condensed tannins (CTs) affect not only trophic interac-
tions such as herbivory and leaf decomposition, but also
processes intrinsic to leaf growth and development. Condensed
tannins, also known as proanthocyanidins (PAs), are non-
structural, polymeric end products of the flavonoid pathway. The
flavonoid biosynthetic pathway is well studied, but there are still
major gaps in our understanding of how CTs are formed and
compartmentalized (Zhao et al. 2010, Brillouet et al. 2013,
Wang et al. 2018). In short, the central phenylpropanoid path-
way gives rise to various hydroxycinnamates and flavonoids,
including flavan-3-ols, which polymerize to form the CT oligo-
mers (Figure 1). It has long been recognized that with their cap-
acity to absorb UV radiation and scavenge damaging radicals,
flavonoids contributed to the survival and early evolution of land
plants (Stafford 1991, Agati and Tattini 2010, Albert et al.
2018). In recent decades, interest has expanded into the
importance of CTs as defensive antifeedants and antimicrobials
with additional ecophysiological roles pertinent to nutrient cyc-
ling (Madritch and Lindroth 2015). The report of Gourlay and
Constabel (2019) now steers the conversation back toward the
intersection of CTs with leaf health and functional resilience
(Figure 1).
Condensed tannins as players in multi-tiered redox
control
The authors present a novel finding that leaf CTs mediate oxida-
tive stress tolerance in vivo with physiologically relevant out-
comes. This is noteworthy in part because flavonoids comprise
only one facet of a plant arsenal based also on ascorbic acid and
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orcid.org/0000-0001-5098-
glutathione as well as various pigments and retrograde signaling
for redox control and the neutralization of harmful radicals
(Kleine and Leister 2016, Smirnoff 2018). The work of Gourlay
and Constabel significantly extends in vitro work using non-plant
systems where the ability of flavan-3-ols and other flavonoid
monomers to oxidize free peroxyl radicals, prevent their chain
propagation and inhibit damaging effects to cellular components
has already been demonstrated (Jovanovic et al. 1996, Arora
et al. 1998). The physiological relevance of such studies has
been challenged in the past due in part to kinetic constraints
which predict that the flavonoid concentrations required for
effective scavenging may be greater than would be achievable
in vivo (Forman et al. 2014). This point was suggested earlier
by Stafford (1991) in tempering the idea that UV-absorbing fla-
vonoids also functioned as radical scavengers in primitive plants.
In addition, direct interactions between dietary flavonoids, gluta-
thione and catalase have been reported (Sudheesh et al. 1999,
Myhrstad et al. 2002, Krych and Gebicka 2013, Majumder et al.
2017). Given the plethora of interacting mechanisms for redox
control, the new findings support an interesting notion that
increased CT abundance can result in a physiologically beneficial
gain in radical scavenging in leaves.
It was perhaps fortuitous that overexpressing CT-regulating
MYB134 or MYB115 (hereafter MYB 134/115) had only a min-
or effect on the levels of other key flavonoids, especially flavo-
nols like quercetin (Mellway et al. 2009, James et al. 2017).
Quercetin glycosides have broad subcellular distribution and
strong radical scavenging abilities (Husain et al. 1987, Jovanovic
et al. 1996, Agati and Tattini 2010). In this respect, Gourlay and
Constabel appear to have threaded a needle. While it seems intui-
tive that reducing flavonol levels might lead to damage, there is
 2 Harding
Figure 1. Suggested impacts of condensed tannin (CT) manipulation.
Sunlight as well as fluctuations in Calvin cycle capacity due to nutrient and
water availability can lead to reactive oxygen species (ROS) excesses in
the chloroplast (green) and photosystem II (PSII) damage, or photoinhibi-
tion. Reactive oxygen species such as H2O2 can also exit in the chloroplast
or be generated in the cytosol. Condensed tannins and monomeric flavo-
nols inhibit ROS accumulation both preventively by absorbing UV radiation,
chelating reactive metals that participate in radical generation, and reac-
tively by scavenging peroxyl radicals. By extension, CT abundance and
compartmentalization should affect ROS-retrograde signaling pathways in
the cytosol. Retrograde signaling can trigger programmed cell death
(PCD) and leaf senescence, itself a radical generating process that affects
leaf area duration. Finally, CT accrual interfaces with that of phenolic glyco-
sides (PGs) via uncharacterized mechanisms to condition trophic interac-
tions important for tree fitness, perennial growth and habitat productivity.
also evidence that a constitutive increase in their cytosolic abun-
dance can be damaging. Flavonols can act as pro-oxidants
(Krych and Gebicka 2013), and in the presence of H2O2, levels
well below those thought to be required for effective intracellular
scavenging have been shown to damage DNA (Sakihama et al.
2002, Labieniec et al. 2003, Azam et al. 2004). Current animal
system models suggest that cytosolic flavonoids provided in the
diet operate at very low concentrations, less by radical scaven-
ging and more as receptor ligands for the prevention of oxidative
imbalances via the nuclear factor erythroid 2-related (NRF2) sig-
naling pathway (Forman et al. 2014, Loboda et al. 2016). Plants
lack orthologs for the NRF2 signaling pathway, perhaps not sur-
prisingly since flavonols are light-regulated UV filters and prob-
ably too abundant to serve as signaling molecules. Flavonol
levels in the cytosol are partly controlled by mitochondrial and
chloroplast sensing, as well as by various transporters and ves-
icular trafficking (Giraud et al. 2008, Morishita et al. 2009, De
Clercq et al. 2013, Zhao 2015). Subcellular compartmentaliza-
tion, though as yet poorly understood, therefore deserves further
Tree Physiology Volume 00, 2019
consideration for the enhanced constitutive scavenging observed
in the high-CT transgenic poplars.
Compartmentalization and localization as
facilitators of CT function
One distinguishing feature of plant compared with animal cells is of
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course the large central vacuole where flavonoids can concentrate.
Not only does the vacuole act as a flavonoid reservoir, but polymer-
ization of CTs is thought to increase in the vacuole (Figure 1), albeit
by mechanisms that remain unknown (Jiang et al. 2015, Wang et al.
2018). Additionally, at least on the basis of in vitro studies, the
enzymatic polymerization of catechin monomers increases their anti-
oxidative capacity on a per carbon basis (Kurisawa et al. 2003).
Given these contexts, demonstration of the ameliorative effects on
photoinhibition by Gourlay and Constabel provides new impetus for
exploring the partnership between compartmentalization and flavon-
oid pathway fluxes in abiotic stress tolerance. One of several ques-
tions raised by the current findings concerns the mechanism of
photosystem II (PSII) protection. Preemptive UV filtering through the
vacuole and enhanced radical scavenging in the cytosol both remain
as mechanisms (Figure 1). However, the effect of MYB134/115-
regulated CT increases on their subcellular distribution and oligomer-
ization prior to vacuolar import is unclear. The so-called ‘tannosome’
transport model is based on evidence that suggests a chloroplastic
origin for CTs followed by their delivery to the vacuole in tannosome
vesicles derived from chloroplasts (Brillouet et al. 2013). Other
models support the biosynthesis of CTs and their oligomerization at
the endoplasmic reticulum (Liu et al. 2016). Ultimately, greater certi-
tude about the topology and capacity of CT trafficking will lend clarity
as to how increased CT accrual leads to decreased PSII damage.
In addition to the matter of compartmentalization, future stud-
ies will need to determine whether CT localization within the leaf
is a factor in its remedial effects. Most UV filtering occurs in the
leaf epidermis (Stapleton and Walbot 1994), but in quaking
aspen (Populus tremuloides Michx.) at least, CTs are normally
less abundant in the upper epidermis than in other cell layers
(Kao et al. 2002), including the palisade mesophyll where most
photosynthetic reactive oxygen species (ROS) occur. Altered
localization of CT accrual including the possibility of ectopic
accrual in the upper epidermis needs to be considered as a pos-
sible contributor to effects such as those reported by Gourlay
and Constabel.
Condensed tannins: important contributors to tree
fitness?
Room for varied cell-specific and subcellular localization of CTs
suggests potential for dynamic interactions and tradeoffs involv-
ing CTs, abiotic stress tolerance and defense (Figure 1). One
defining feature among the Salicaceae (poplars and willows) is
wide genetic diversity when it comes to foliar CT and salicinoid
phenolic glycoside (PG) levels (Orians et al. 2000, Harding et al.

2005). Such variation probably serves an important purpose
since CTs and PGs function differently in chemical defense of
aspens (Hemming and Lindroth 1995). In fact, a clear allocation
tradeoff between CTs and PGs with trophic implications has
been reported for the MYB134 poplar lines (Mellway et al.
2009, Kosonen et al. 2012). Recent work has shown a positive
correlation between CT concentration and poplar resistance to
rust (Melampsora larici-populina) (Ullah et al. 2018). Little is
known about the genetic mechanisms that underlie the partition-
ing of metabolic carbon between CTs and PGs in these species.
However, low-nitrogen-induced CT enhancements costly to PG
accrual, and to the availability of primary metabolites for growth
(Harding et al. 2005, 2014), can now be viewed in the added
context of shifts in the demand for antioxidants in response to
adverse conditions.
Finally, leaf senescence is an inherently oxidative process
during which nutrients derived from the turnover of cellular con-
tents are resorbed by the stem and roots (Zimmermann and
Zentgraf 2005) (Figure 1). Whether the filtering and antioxi-
dant properties of CTs conditionally modulate programmed turn-
over of cellular contents during senescence has not been
evaluated. Condensed tannin polymers are more persistent than
flavonoid monomers or small CT oligomers as leaves senesce
(Kandil et al. 2004). However, measurement of CT levels in
senescing leaves has not been without challenge since their
extractability may decrease due to extensive polymerization and
binding prior to leaf abscission (Lindroth et al. 2002). One pos-
sible outcome of elevated CT level is the possible delaying
effect that it could have on the initiation of seasonal or prema-
ture leaf senescence. As recently reviewed by Petrov et al.
(2015), leaf senescence is triggered in part by retrograde sig-
naling pathways in response to specific ROS signals from the
chloroplast and mitochondria (Figure 1). Delayed onset of sea-
sonal senescence would therefore conceivably lead to reduced
resorption of leaf resources by the plant before killing conditions
terminate the process. How scenarios like these might play out
in nature will depend on the regulation of CT biosynthesis as
well as on the processes that control CT trafficking and the loca-
tions of CT accrual in the cell. Much also remains to be learned
about CT accrual in the contexts of changing temperatures, pre-
cipitation and atmospheric CO2 levels, work that has begun
(Kosonen et al. 2012) and presumably will continue with the
current findings of Gourlay and Constabel in mind.
Conflict of interest
None declared.
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