Genetic (G) variation in both total stores and partitioning
between sugar and starch
Genetic variation in traits act as the raw material with which
populations can adapt to novel stress. Here, we found heritable genetic
variation in total NSC concentrations (sugar + starch) in the branches
of black cottonwood. Our results reveal that these trees could
potentially evolve greater NSC storage in response to increased stress.
An increase in the concentration of NSC a tree stores may confer
enhanced resilience during times of photosynthetically limiting stress
by serving as a fuel source or osmotic reservoir (Dietze et al., 2014;
Henrik Hartmann et al., 2018; H. Hartmann & Trumbore, 2016; O’Brien et
al., 2017; Wiley & Helliker, 2012). Experimental and observational
studies have demonstrated that trees will draw down NSC stores when
experiencing photosynthetically limiting environmental conditions (Adams
et al., 2013; Adams et al., 2017; Henrik Hartmann, Ziegler, Trumbore, &
Knapp, 2013; Landhäusser & Lieffers, 2011; Sevanto et al., 2014), such
as drought, suggesting that NSCs may be serving a critical metabolic
function. In addition, seedlings with higher NSC stores live longer
through drought, indicating that higher NSC concentrations may enable
trees to live longer under environmental stress (O’Brien et al., 2017).
Given that climate forecasts generally predict more extreme weather
events (IPCC, 2013b), the existence of heritable variation in total NSC
stores may be crucial for tree populations to evolve in response to
climate-driven selection in the future.
In addition to total storage, the proportion of stores individuals put
into starch versus sugar at any given time may be crucial for
withstanding future climate-driven selection. We also found heritable
variation in the proportion of these total stores residing in insoluble
starch for branches, stems, and roots (Table 1, Table S1). Across most
winter deciduous species, the proportion of total stores in starch is at
its lowest in the winter, particularly in January, the month we sampled
in (Furze et al., 2019; Martínez-Vilalta et al., 2016). This is thought
to be because the rate of starch degradation and synthesis is controlled
in part by enzymes with different temperature sensitivities. Starch
degradation enzymes are less sensitive to low temperatures than starch
synthesis enzymes (Pollock & Lloyd, 1987), although below
3-5oC both degradation and synthesis enzymes cease to
function. Thus, at low temperatures (but still above
3-5oC) starch is degraded, leading to a corresponding
increase of sugar in cells (Zwieniecki, Tixier, & Sperling, 2015). This
newly available pool of sugar can be used for maintenance respiration
and may confer an increased cold tolerance to individuals or even signal
when to break dormancy in spring (Aude Tixier, Gambetta, Godfrey,
Orozco, & Zwieniecki, 2019). Thus, being sensitive to changes in
temperature and shifting stores between starch and sugar may be critical
for tree survival under future, more chaotic climate regimes. Our
results indicate that there is genetic variation in if or how trees
shift stores between starch and sugar. This opens the possibility that
trees can adapt their allocation strategy to better fit a changing, more
stressful climate.
Although we found heritable variation in both branch total NSC stores
and proportion of stores in starch, we did not find evidence that this
variation was currently locally adapted. Differentiation across
populations in genetic variation of these traits is minimal. The lack of
adaptive signatures in branch total NSC stores stands in contrast to
adaptive differentiation previously reported for stems and roots. One
reason for this divergence may be that branches are the most proximal of
the three tissues to carbon sources (leaves) and some sinks (buds and
flowers). Over the course of a year, branch NSC stores fluctuate much
more than roots or stems as they are the first storage sink to fill with
new photosynthates and the first to be drawn down in spring (Furze et
al., 2019). This pattern could also be caused by the fact that black
cottonwoods have photosynthetic bark. Branches are exposed to more
sunlight than stems and roots and thus may see a higher degree of
variation in NSC produced via opportunistic bark photosynthesis.
Together, these sources of variation may have a genetic signal, but the
other sources of fluctuations may mask the genetic variation in storage
preventing selection from effectively causing genetic differentiation.