Environmental and Experimental Botany 87 (2013) 69–78
Contents lists available at SciVerse ScienceDirect
Environmental and Experimental Botany
journa l h omepa g e: www.elsevier.com/locate/envexpbot
Differential tolerance to combined salinity and O
2
deficiency in the halophytic
grasses Puccinellia ciliata and Thinopyrum ponticum: The importance of K
+
retention in roots
N.L. Teakle
a,b,1
, N. Bazihizina
a,b
, S. Shabala
c
, T.D. Colmer
b,d,∗
, E.G. Barrett-Lennard
a,b,e
,
A. Rodrigo-Moreno
c,g
, A.E. Läuchli
b,f
a
State Centre of Excellence for Ecohydrology, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia
b
School of Plant Biology, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6019, Australia
c
School of Agricultural Sciences and Tasmanian Institute of Agricultural Research, Private Bag 54, University of Tasmania, Hobart TAS 7001, Australia
d
The UWA Institute of Agriculture, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia
e
Department of Agriculture and Food Western Australia, 3 Baron-Hay Court, South Perth, WA 6151, Australia
f
Department of Land, Air and Water Resources, University of California, 1 Shields Ave, Davis CA 95616-8627, USA
g
Universitat Autònoma de Barcelona, Facultat de Biociències. Edifici C, 08193 Bellaterra, Barcelona, Spain
a r t i c l e i n f o
Article history:
Received 21 June 2012
Received in revised form 21 August 2012
Accepted 19 September 2012
Keywords:
Adventitious roots
Halophytes
Membrane potential
Potassium
Sodium,
Waterlogging
a b s t r a c t
Saline environments of terrestrial halophytes are often prone to waterlogging, yet the effects on halo-
phytes of combined salinity and waterlogging have rarely been studied. Either salinity or hypoxia (low
O
2
) alone can interfere with K
+
homeostasis, therefore the combination of salinity or hypoxia is expected
to impact significantly on K
+
retention in roots. We studied mechanisms of tolerance to the interaction
of salinity with hypoxia in Puccinellia ciliata and Thinopyrum ponticum, halophytic grasses that differ in
waterlogging tolerance. Plants were exposed to aerated and stagnant saline (250 mM NaCl) treatments
with low (0.25 mM) and high (4 mM) K
+
levels; growth, net ion fluxes and tissue ion concentrations were
determined. P. ciliata was more tolerant than T. ponticum to stagnant-saline treatment, producing twice
the biomass of adventitious roots, which accumulated high levels of Na
+
, and had lower shoot Na
+
. After
24 h of saline hypoxic treatment, MIFE measurements revealed a net uptake of K
+
(∼40 nmol m
-2
s
-1
) for
P. ciliata, but a net loss of K
+
(∼20 nmol m
-2
s
-1
) for the more waterlogging sensitive T. ponticum. NaCl
alone induced K
+
efflux from roots of both species, with channel blocker tests implicating GORK-like
channels. P. ciliata had constitutively a more negative root cell membrane potential than T. ponticum
(-150 versus -115 mV). Tolerance to salinity and hypoxia in P. ciliata is related to increased production
of adventitious roots, regulation of shoot K
+
/Na
+
, and a superior ability to maintain negative membrane
potential in root cells, resulting in greater retention of K
+
.
© 2012 Elsevier B.V. All rights reserved.
1. Introduction
Salinity is an environmental constraint that affects plant growth
and development in a range of landscapes, for both irrigated and
non-irrigated agricultural land (Ghassemi et al., 1995). Species
∗
Corresponding author at: School of Plant Biology (M084), The University of
Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.
Tel.: +61 8 6488 1993; fax: +61 8 6488 1108.
E-mail addresses: n.ayers@ecu.edu.au (N.L. Teakle),
nadia.bazihizina@uwa.edu.au (N. Bazihizina), Sergey.Shabala@utas.edu.au
(S. Shabala), timothy.colmer@uwa.edu.au (T.D. Colmer),
ed.barrett-lennard@agric.wa.gov.au (E.G. Barrett-Lennard), Ana.Rodrigo@uab.cat
(A. Rodrigo-Moreno), aelauchli@ucdavis.edu (A.E. Läuchli).
1
Present address: Natasha Ayers, Graduate Research School, Edith Cowan Uni-
versity, 270 Joondalup Dr, Joondalup, WA 6027, Australia.
that thrive in these environments and are adapted to salinity
are called halophytes. The physiology of halophytes has been
studied extensively, and their salinity tolerance is primarily gov-
erned by controlled uptake and compartmentalization of Na
+
,
K
+
, and Cl
-
(Flowers and Colmer, 2008; Shabala and Mackay,
2011). Many of the habitats occupied by terrestrial halophytes
are not only saline, but also prone to waterlogging (Colmer and
Flowers, 2008). Waterlogging causes soils to become hypoxic, due
to biological consumption of O
2
without its effective replacement
(Ponnamperuma, 1984). While the growth effects of combined
salinity and waterlogging have been studied for some halophytes
(see Colmer and Flowers, 2008), the mechanisms of tolerance are
poorly understood. Furthermore, the adverse interactive effects of
these stresses must be considered in the design of revegetation pro-
grammes for salt-affected lands (Barrett-Lennard, 2003; Bennett
et al., 2009).
0098-8472/$ – see front matter © 2012 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.envexpbot.2012.09.006