‘Last In–First Out’: seasonal variations of non-structural
carbohydrates, glucose-6-phosphate and ATP in tubers of two
E. Petrussa , F. Boscutti , A. Vianello & V. Casolo
Laboratory of Plant Biology, Department of Agricultural, Food, Animal and Environmental Sciences, University of Udine, Udine, Italy
Arum italicum; Arum maculatum; ATP; non-
structural carbohydrates; phenology; starch;
V. Casolo, Laboratory of Plant Biology,
Department of Agricultural, Food, Animal and
Environmental Sciences, University of Udine,
Via delle Scienze 91, 33100 Udine, Italy.
Received: 15 September 2017; Accepted: 13
Knowledge on the metabolism of polysaccharide reserves in wild species is still scarce.
In natural sites we collected tubers of Arum italicum Mill. and A. maculatum L. – two
geophytes with different apparent phenological timing, ecology and chorology – dur-
ing ﬁve stages of the annual cycle in order to understand patterns of reserve accumula-
tion and degradation.
Both the entire tuber and its proximal and distal to shoot portion were utilised. Pools
of non-structural carbohydrates (glucose, sucrose and starch), glucose-6-phosphate
and ATP were analysed as important markers of carbohydrate metabolism.
In both species, starch and glucose content of the whole tuber signiﬁcantly increased
from sprouting to the maturation/senescence stages, whereas sucrose showed an oppo-
site trend; ATP and glucose-6-phosphate were almost stable and dropped only at the
end of the annual cycle. Considering the two different portions of the tuber, both ATP
and glucose-6-phosphate concentrations were higher in proximity to the shoot in all
seasonal stages, except the ﬂowering stage.
Our ﬁndings suggest that seasonal carbon partitioning in the underground organ is
driven by phenology and occurs independently of seasonal climate conditions. More-
over, our results show that starch degradation, sustained by elevated ATP and glucose-
6-phosphate pools, starts in the peripheral, proximal-to-shoot portion of the tuber,
consuming starch accumulated in the previous season, as a ‘Last In–First Out’ mecha-
nism of carbohydrate storage.
Studies of global climate change now include wider effects on
plant phenology and distribution (Bertin 2008). In trees, it is
well documented that carbon metabolism plays a pivotal role
in plant response to climate variability (McDowell & Sevanto
2010), but little information is available for herbaceous species
(Ball & Morell 2003; Keeling & Myers 2010). Among these,
geophytes, which have a dormant bud on an underground
storage organ (Raunkiaer 1934), can be considered an interest-
ing model for understanding plant acclimation (Eppich et al.
2009). In fact, they completely depend on non-structural car-
bohydrate (NSC) reserves that also reﬂect the climate condi-
tions and phenological life cycle (Chapin et al. 1990).
Geophytes preferentially store NSC in their underground
organs in order to mitigate climate variations and so satisfy
their energy requirements during the annual life cycle (Chapin
et al. 1990). This kind of reserve also represents an essential
trait to promote vegetative propagation in all clonal plants
sharing ramet growth (Meyer & Hellwig 1997; Pan & Price,
2001). The storage declines during epigeous growth, where the
underground organ is the source system, but recovers when
aerial growth stops, switching to a sink pool (Chapin et al.
1990). Stored carbohydrates are utilised both as energy and
carbon supply during sprouting (Orthen & Wehrmeyer 2004).
The seasonal trend of reserve accumulation and degradation
must be described by considering the underground organ
(sink) in the context of the whole plant. However, growth of
the whole plant in natural systems is also dependent on the
development of its perennial organ, and this process is strictly
linked to carbohydrate accumulation and allocation (Lapointe
Studies on storage carbohydrates in different geophytes
reveal that the major forms of such reserves are starch and
fructans (Ranwala & Miller 2008), sometimes stored in the
same underground organ (Brocklebank & Hendry 1989;
Orthen 2001). Variations in these pools are observed during
speciﬁc phenological stages, suggesting their involvement in
different metabolic pathways (Meyer & Hellwig 1997; Orthen
& Wehrmeyer 2004). Moreover, soluble sugars (mostly sucrose
and glucose) are also present in storage organs of various geo-
phytes and, generally, the concentration of sucrose is always
higher than that of glucose or fructose (Ranwala & Miller
The conversion of sucrose into starch is dependent on
adenylates (ATP, UDP, ADP-glucose and UDP-glucose) and
on phosphorylated intermediates, as well as oxygen availability
(Geigenberger 2003; Hajirezaei et al. 2003). In particular, the
seasonal changes in adenylate pools have been studied in
autumn-sown sugar beet roots (Garcia-Maurino et al. 2005)
Plant Biology 20 (2018) 346–356 © 2017 German Society for Plant Sciences and The Royal Botanical Society of the Netherlands
Plant Biology ISSN 1435-8603