Journal of Plant Physiology 169 (2012) 577–585
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Journal of Plant Physiology
jou rn al h o mepage: www.elsevier.de/jplph
Interaction of proline, sugars, and anthocyanins during photosynthetic
acclimation of Arabidopsis thaliana to drought stress
Ilektra Sperdouli, Michael Moustakas
∗
Department of Botany, School of Biology, Aristotle University of Thessaloniki, University Campus, 54124 Thessaloniki, Greece
a r t i c l e i n f o
Article history:
Received 31 August 2011
Received in revised form 28 October 2011
Accepted 1 December 2011
Keywords:
Anthocyanins
Drought stress
Metabolic adjustment
Proline
Soluble sugars
Oxidative stress
Arabidopsis thaliana
a b s t r a c t
The relationships among photosynthetic acclimation, proline (Pro), soluble sugar (SS), and anthocyanin
(An) accumulation in Arabidopsis thaliana leaves to the onset of drought stress (OnDS), mild (MiDS) and
moderate drought stress (MoDS), were evaluated. As leaf water content (LWC) decreased, metabolic
concentrations (Pro, SS, and An) increased and were negatively and significantly correlated with LWC.
Thus, these metabolites may have an important role in the acclimation process to drought stress (DS).
No correlations among Pro, SS and An accumulation with the quantum efficiency of PSII photochemistry
(˚
PSII
) and the excitation pressure (1 - q
P
) were observed under DS. This implies that, while metabolites
increased in a drought-dependent way, PSII activity did not decrease in the same pattern. Our results
indicated that, under MoDS, A. thaliana leaves were able to maintain oxidative compounds such as mal-
ondialdeyde, an end product of lipid peroxidation, within the range of control leaves, and to cope with
oxidative damage, as was evident by the decreased excitation pressure (1 - q
P
) and similar (ns difference)
˚
PSII
to that of control leaves. In addition, a statistically significant increased accumulation of Pro, SS and
An was recorded only under MoDS compared to controls. The better PSII functioning of MoDS Arabidopsis
leaves may reflect the greater capacity of these leaves to undertake key metabolic adjustments, including
increased Pro, SS and An accumulation, to maintain a higher antioxidant protection and a better balance
between light capture and energy use.
© 2012 Elsevier GmbH. All rights reserved.
Introduction
Abiotic stresses, which cause depletion of cellular water
(drought, high soil salinity and temperature extremes) are the pri-
mary causes of crop loss worldwide, reducing average yields for
most major crop plants by more than 50% (Boyer, 1982). Increasing
plant resistance to drought stress (DS) would be the most econom-
ical approach to improving agricultural productivity and reducing
agricultural use of fresh water resources (Xiong et al., 2006).
As the key process of primary metabolism, photosynthesis plays
a central role in plant performance under DS (Chaves et al., 2003,
2009; Flexas et al., 2004, 2009; Lawlor and Tezara, 2009; Pinheiro
and Chaves, 2011). The balance between light capture and energy
use are of great relevance to studies concerning the responsive-
ness of the photosynthetic apparatus to DS (Cornic and Briantais,
1991; Chaves et al., 2009; Lawlor and Tezara, 2009; Aranjuelo
et al., 2011). When photosynthesis decreases, the excess excitation
energy in photosystem II (PSII) leads to an impairment of photo-
synthetic function and to accumulation of reactive oxygen species
∗
Corresponding author. Tel.: +30 2310 998335; fax: +30 2310 998389.
E-mail address: moustak@bio.auth.gr (M. Moustakas).
(ROS), thereby resulting in oxidative stress (Aranjuelo et al., 2011;
Wilhelm and Selmar, 2011).
Although impressive advances have been made in the last
decade with respect to the nature of events occurring in plants
subjected to DS, an integrative picture of the metabolic regulation
that takes place is still lacking (Rolland et al., 2006; Shinozaki and
Yamaguchi-Shinozaki, 2007; Pinheiro and Chaves, 2011). Several
metabolic adjustments occur prior to alteration of the plant water
status, implying that DS is perceived before changes in plant water
status (Pinheiro et al., 2011). Early responses of plants to DS usu-
ally help the plant to survive for some time, while the acclimation
of the plant subjected to drought is indicated by the accumulation
of certain metabolites associated with the structural capabilities to
improve plant functioning under DS (Pinheiro et al., 2001; Reddy
et al., 2004).
General metabolic adaptation, which enables plants to cope
with water or osmotic stress, involves an increased synthesis of
osmoprotectants, such as proline (Pro) (Hare et al., 1998; Dobrá
et al., 2011). This osmolyte is considered to protect plant cells
by osmotic adjustment or by stabilizing membranes (Hare and
Cress, 1997; Kavi Kishor et al., 2005; Verbruggen and Hermans,
2008; Szabados and Savouré, 2010). The level of free Pro is reg-
ulated by the ratio of the rates of its biosynthesis and degradation
(Hare and Cress, 1997; Verbruggen and Hermans, 2008; Szabados
0176-1617/$ – see front matter © 2012 Elsevier GmbH. All rights reserved.
doi:10.1016/j.jplph.2011.12.015