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Ecotoxicology and Environmental Safety
journal homepage: www.elsevier.com/locate/ecoenv
Simultaneous mitigation of aluminum, salinity and drought stress in Lactuca
sativa growth via formulated plant growth promoting Rhodotorula
mucilaginosa CAM4
Sivagnanam Silambarasan
a
, Peter Logeswari
a
, Pablo Cornejo
a,b,∗
, Jayanthi Abraham
c
,
Alexander Valentine
d
a
Centro de Investigación en Micorrizas y Sustentabilidad Agroambiental, CIMYSA, Facultad de Ingeniería y Ciencias, Universidad de La Frontera, Avenida Francisco
Salazar, 01145, Temuco, Chile
b
Scientific and Technological Bioresource Nucleus, BIOREN-UFRO, Departamento de Ciencias Químicas y Recursos Naturales, Universidad de La Frontera, Avenida
Francisco Salazar, 01145, Temuco, Chile
c
Microbial Biotechnology Laboratory, School of Biosciences and Technology, VIT University, Vellore, 632014, Tamil Nadu, India
d
Botany and Zoology Department, Faculty of Science, University of Stellenbosch, Stellenbosch, South Africa
ARTICLE INFO
Keywords:
Aluminum
Bioaccumulation
Formulation
PGP yeast
Plant growth promotion
ABSTRACT
In the present study, a potent Aluminum (Al) resistant yeast strain CAM4 was isolated from rhizosphere soil of
Rubus geoides, grown in acidic Andisols and identified as Rhodotorula mucilaginosa by 18S rRNA gene sequence
analysis. The strain CAM4 was selected in terms of abiotic stress tolerance to Al, salinity and drought with
multiple plant growth promoting (PGP) traits. Besides, strain CAM4 also exhibited Al removal efficiency
(80–88%) from the culture medium even under combined stresses of salinity and drought. The sawdust-based
formulation of strain CAM4 (sawdust-molasses 5%-PEG 1%-strain CAM4) showed higher cell viability of up to 24
weeks (8.54 log CFU g
-1
). Inoculation of formulated strain CAM4 significantly enhanced the various mor-
phological and biochemical characters of Lactuca sativa grown under abiotic stress conditions. The formulated
strain CAM4 also reduced the accumulation of Al in L. sativa as well that conferring Al tolerance to the plants.
The study concludes that strain CAM4 could be used as a biofertilizer for healthy and safe crop production in
soils, with Al toxicity as well as combined salt and drought stresses.
1. Introduction
Soil acidity is a major constraint for crop cultivation around the
world, as nearly half of the potential arable lands are acidic, which
includes most parts of Chile (acid Andisols) (Aguilera et al., 2017). In
acidic soils, plant growth is highly affected due to the presence of the
third most widespread phytotoxic element in nature, Aluminum (Al)
(Kochian et al., 2004). Al largely exists in the harmless form of gibbsite
and aluminosilicates in soils (Kochian, 1995). However, insoluble Al
can be solubilized at pH < 5 and consequently release Al
3+
, which is
toxic to plants (Seguel et al., 2013). The uptake of Al
3+
may interfere
with a numerous cellular mechanisms, through damaging the roots,
subsequently interrupting absorption and mobilization of essential
elements across the membranes, thereby eventually resulting in poor
plant growth and productivity (Kochian et al., 2015). It has been proven
from the earlier study that Al hinders root cell ion transport proteins
(Rengel and Elliott, 1992). Al either inhibits Ca
2+
transport into the
symplasm of root cells or displaces Ca
2+
from the critical metabolic
sites in the apoplasm (Mossor-Pietraszewska, 2001). Al overexposure
results in oxidative stress as a consequence of the accumulation of re-
active oxygen species (ROS). The damage caused by ROS is often in-
dicated by lipid peroxidation (Riaz et al., 2018). However, plants have
developed a complex antioxidant defence system to cope with the ex-
cess of ROS, which include the activation of antioxidant enzymes such
as catalase (CAT), superoxide dismutase (SOD) and peroxidase (POX).
Moreover, proline also works to signal and regulates metabolic activ-
ities and is considered a non-enzymatic antioxidant against stress con-
dition (Ashraf and Foolad, 2007; Matysik et al., 2002).
In spite of the potential Al toxicity in agricultural soils, the pro-
duction of crops is highly influenced by a variety of other abiotic
stresses imposed by various environmental factors, such as salinity,
drought, heavy metals and temperature. The crop's productivity is
https://doi.org/10.1016/j.ecoenv.2019.05.006
Received 2 January 2019; Received in revised form 27 April 2019; Accepted 1 May 2019
∗
Corresponding author. Centro de Investigación en Micorrizas y Sustentabilidad Agroambiental, CIMYSA, Facultad de Ingeniería y Ciencias, Universidad de La
Frontera, Avenida Francisco Salazar, 01145, Temuco, Chile.
E-mail address: pablo.cornejo@ufrontera.cl (P. Cornejo).
Ecotoxicology and Environmental Safety 180 (2019) 63–72
0147-6513/ © 2019 Elsevier Inc. All rights reserved.
T