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Pastos y Forrajes, Vol. 39, No.4, October-December, 219-228, 2016 / Wendy M. Ramírez-Suárez 	219
review paper
Salinity tolerance in turfgrass species
Wendy M. Ramírez-Suárez and Luis A. Hernández-Olivera
Estación Experimental de Pastos y Forrajes Indio Hatuey,
Universidad de Matanzas, Ministerio de Educación Superior
Central España Republicana, CP 44280, Matanzas, Cuba
E-mail: wendy.ramirez@ihatuey.cu
Abstract: Salinity constitutes one of the problems that affect the sustainable development of gardening in
tourism areas, golf courses, public spaces and sports fields; by causing stress in the turfgrass
species and deteriorating the soil structure. Turfgrass production in Cuba takes place at the
Pastures and Forages Research Station Indio Hatuey (Matanzas province), and its starting
point are the results obtained at international level to search for alternatives that allow higher
utilization of salinization-degraded soils and the increase of the production potential of the grass
with the required quality. The objective of this paper is to contribute to the knowledge of salinity
tolerance in turfgrass species. It approaches the stress types in plants, especially the stress
caused by saline soils; the salinity tolerance mechanisms in plants and the studies conducted
in some salinity-tolerant turfgrass species. Understanding the physiological and biochemical
mechanisms and evaluating turfgrass species are essential to provide a practical solution for the
salinity problem and establish a correct management in the turfgrass areas.
Keywords: electrical conductivity, abiotic stress, saline soil
Introduction
The versatility and functionality of turfgrass
species has had a determinant impact on the
accelerated growth of the turfgrass industry in many
countries, whose market value has reached up to 35
billion dollars only in the United States. The increase
of the surface dedicated to the cultivation of turfgrass
species increases in a directly proportional way to the
increase of population nuclei in urban zones, for which
the demand of plants for landscaping and recreational
areas grows exponentially (Huang et al., 2014). In this
sense, Cuba is not an exception. The main tourism
areas of the country are located in the Cuban coasts,
which demand large surfaces covered by turfgrass,
just like the golf courses which have become a
fundamental income source through international
tourism (Marrero, 2006).
However, one of the main challenges faced by
the turfgrass industry is maintaining a high-quality
turfgrass under adverse edaphoclimatic conditions,
with minimum inputs and scarce or no environmen-
tal impact. The most effective way to address this is-
sue is the development, introduction and exploitation
of germplasm that tolerates the main stress factors
which affect turfgrass species (Huang et al., 2014).
These turfgrass species are affected by several
abiotic stress factors that influence especially the
turf aesthetic quality, functionality and yield. In
that sense, it is not strange that most breeding pro-
grams in recent years have been aimed at obtaining
varieties tolerant to abiotic stress factors, such as
salinity (Abogadallah et al., 2010), drought (Barnes
et al., 2014), shade (Trappe et al., 2011) and low
temperatures (Li et al., 2010), among others.
Hydric stress (caused by salinity and/or drought)
is one of the most studied abiotic factors, for two
main reasons: first, because it causes severe damage
on plants; and, second, due to the large land extension
that is affected by these limiting factors (Marcum,
2014). The negative effects of this stress type are
significantly increased in coastal zones because of
the so-called “island effect”, for the high salt content
of the waters (Tang et al., 2013; Manuchehri and
Salehi, 2014).
The current turfgrass production in Cuba is
led by the Pastures and Forages Research Station
Indio Hatuey (Matanzas province), which has a
turfing service that includes the sale, planting,
establishment, fertilization, phytosanitary attention
and rehabilitation of the turf, and in turn aims at
improving the quality of golf courses, sports fields,
gardens and public spaces, without forgetting
the mandatory respect towards the environment.
Likewise, this institution works on the establishment
and evaluation of salinity-tolerant grasses and
220 	 Pastos y Forrajes, Vol. 39, No.4, October-December, 219-228, 2016 / Salinity tolerance in turfgrass species
aims at implementing a technology that prevents
excessive water consumption, to achieve sustainable
development in the new gardening.
Taking such problematic situation into account,
the objective of this paper is to contribute to the
knowledge about salinity tolerance in turfgrass
species.
Distribution, morphology and classification
of turfgrass species
Taxonomically most turfgrass species belong
to the Poaceae family, which is considered highly
important due to its cosmopolitan distribution and
its usefulness (Kellogg, 2001).
The Poaceae family, the largest of flowering
plant families, comprises more than 9 000 species
practically distributed in all the ecotypes of the
planet. However, only fifty of these species have the
adequate agro-morphological characteristics to be
exploited, because of their functional, recreational
and ornamental value, as turf-forming plants. Be-
sides acting as plant cover in public parks, gardens,
landscapes, golf courses and sports fields, they are
able to reduce soil erosion, eliminate dust and dirt
from the air, release oxygen and act as natural filter,
elimination the contaminants of underground wa-
ters (Uddin and Juraimi, 2013).
Turfgrass species are reproduced by seeds, al-
though they can be vegetatively established through
stolons, sods and/or cuttings. They have a dense
and fibrous root system which is extended mainly
within the first 15-30 cm of soil. In turfgrasses there
are three types of stem: crown, flowering culm and
creeping or lateral stems, called stolons or rhizomes
(Uddin and Juraimi, 2013).
Accordingtotheadaptationrangestothedifferent
rainfall and temperature conditions, turfgrass
species can be divided into: megathermal (warm
latitudes) and mesothermal (cold latitudes). The
megathermal ones grow in an optimum temperature
range that varies between 24 and 35 ºC and comprise
perennial species such as Buchloe dactyloides Nutt.
(buffalo grass), Zoysia japonica Steud. (Zoysia
grass), Cynodon dactylon L. Pers. (bermuda),
Eremochloa ophiuroides Munro (centipede grass),
Paspalum vaginatum Sw. (paspalum), Stenotaphrum
secundatum Walt. Kuntze (Saint Augustine grass),
among others. On the other hand, mesothermal
species grow in a temperature range between 10 and
22 ºC and comprise perennial and annual species
such as Festuca arundinacea Schreb. (tall fescue),
Poa pratensis L. (Kentucky bluegrass), Lolium
perenne L. (ryegrass), Festuca rubra var. commutata
and Festuca ovina var. duriuscula (sheep fescue), and
Agrostis stolonifera L. (creeping bentgrass), (Huang
et al., 2014).
The most important morphoagronomic charac-
teristics that the species must have for turf formation
are: fast germination and establishment, fine texture
(leaf width), intense color, strong root system, re-
sistance to trampling, adaptation to low cutting and
creeping and slow growth, besides showing resis-
tance and/or tolerance to biotic and abiotic stresses.
Abiotic stress and climate change
In biology, the concept of stress is hard to define,
taking into consideration that a certain biological
condition can represent stress for an organism and, at
the same time, be optimum for another. In a practical
way, it can be considered as any adverse strength or
condition that inhibits the normal functioning of a
biological system (Mahajan and Tuteja, 2005). The
term stress in the framework of plant physiology
“shows the magnitude of environmental pressure that
forces change in the physiology of a plant” (Nilsen
and Orcutt, 1996). Levitt (1980) defines stress as:
“any environmental factor potentially unfavorable
for living organisms”.
Plants are affected mainly by two types of
stress: biotic and abiotic (physical or chemical). The
biotic ones are originated by living organisms and
comprise allelopathies and susceptibility to pests and
diseases; while the abiotic ones are environmental,
such as salinity, high/low temperatures, drought,
shade, atmospheric contamination and toxins,
among others. Abiotic stresses are one of the main
factors that limit plant distribution and productivity
of agricultural crops, because they affect negatively
plant growth and productivity and trigger a series
of morphological, physiological, biochemical and
molecular disorders (Bhatnagar-Mathur et al., 2008;
Cheng, 2014).
In the last decades, the increase of the CO2
level
in the troposphere has triggered global warming and
the so-called climate change. These conditions have
brought about the increasing appearance of extreme
climate conditions, such as large drought and
floodingperiods,prolongedheatorlowtemperatures;
as well as the increase of soil salinization in many
regions of the world, because of the elevation of sea
level (Feng et al., 2014; Flowers and Colmer, 2015).
These atmospheric phenomena drastically affect
plant growth and productivity, and constitute an
increasing threat for sustainability in agriculture,
Pastos y Forrajes, Vol. 39, No.4, October-December, 219-228, 2016 / Wendy M. Ramírez-Suárez 	221
biodiversity and homeostasis of ecosystems (Feng
et al., 2014).
Salinization is one of the most urgent environ-
mental challenges to be solved, because of the dis-
turbances it causes in the microbial communities
and processes, which affects the C cycle in the soil
(Rath and Rousk, 2015); this could limit the role of
the soil as an important carbon sink that contributes
to the mitigation of the climate change.
In this ecological context it is necessary to
identify and study the mechanisms of plants that
are able to survive in such complex environments.
Soil salinization. Causes and origin
At present, soil salinization and sodification
threaten soil fertility and crop productivity (Singh,
2015); this phenomenon has become a worldwide
problem, which affects almost one third of the lands
dedicated to agriculture, and is more serious in the
arid and semiarid regions, where the scarce rainfall
reduces the possibility of washing out the salts that
are being supplied with the irrigation waters. The in-
crease of the water demand in the world, especially
in the arid and semiarid zones, has forced farmers
to use low-quality water in agriculture, mainly from
wells, with a high concentration of salts which often
exceed the salt-tolerance thresholds of many crops
and thus limit their production (Zhang et al., 2013;
Chen et al., 2014; Manuchehri and Salehi, 2014).
Soil salinization precedes the origin of human
civilization and still is the main abiotic stress that
hinders the productivity and quality of harvests
(Lamz and González, 2013). Approximately 20 %
of the cultivated area worldwide and nearly half the
irrigated lands are affected by this factor (Zulkaliph
et al., 2013; Egamberdieva and Lugtenberg, 2014);
recent studies place the increase of the areas affect-
ed by salinity between 1,0 and 1,5 million hectares
per year (Wu et al., 2014; Zhang, 2014). This situa-
tion is daily enhanced, because of the lack of envi-
ronmental awareness and the irrational exploitation
of water resources, besides other edaphoclimatic
factors that influence directly soil salinity (Lamz
and González, 2013). In this sense, Cuba has an
agricultural surface of 6,7 million hectares, from
which approximately 15 % (one million hectares)
is affected by salinity or sodicity, and this limits
the productive potential of Cuban soils (Rodríguez,
2015).
Lamz and González (2013) stated that the term
salinity refers to the presence of a high concentration
of salts which damages the plants due to its toxic
effect and the decrease of the osmotic potential of
the soil.
The salinization phenomenon may have several
causes; primary or natural salinization occurs in soils
which, since their formation, show accumulation
of salts due to rock decomposition or volcanic
activity; and it is found in sites where evaporation
is higher than rainfall, in places close to the sea or
which have saline streams and saline groundwater
(Gómez et al., 2009). However, the most common is
secondary salinization, mainly caused by the effects
of irrigation, the use of low-quality waters, restricted
drainage, low permeability of the soil, and wrong
use of fertilization; which causes the accumulation
of soluble salts, mainly sodium, in the upper
horizons. This situation brings about the loss of
land productivity and their subsequent abandonment
(Egamberdieva and Lugtenberg, 2014).
Álvarez-Menéndez et al. (2008) stated that the
natural salt sources in the salinization process in
Cuba are:
•	 Marine aerosols carried by the atmospheric cir-
culation of prevailing winds (East-Southeast and
Southeast trade winds) and by waves of cold
companion winds from the North.
•	 Old marine sediments north and south of the Cu-
ban archipelago, constituted by saline gypsum
and sandy rocks.
•	 The accumulation of continental sediments ca-
rried by the rivers from the mountains to flat
areas during the quaternary period.
•	 Sea intrusion in calcic groundwater aquifers be-
low the sea level.
•	 The wind from arid regions can also contribu-
te to the salinization process, dragging a large
amount of salts, mainly carbonates, sulfates and
chlorides which are suspended (Fuentes et al.,
2007; Wu et al., 2014).
The main soluble constituents of the soil related
to salinity are cations (Na+
, Ca2+
, Mg2+
and K+
), anions
(Cl-
), sulfate (SO4
2-
), bicarbonate and/or carbonate
(HCO3
/CO3
) and nitrate (NO3
-
) (Nizam, 2011;
Alshammary, 2013; Wu et al., 2014). The high salt
concentrations(particularlyNa+
)whicharedeposited
can alter its basic structure; the Na+
cations displace
Ca2+
from the clayey-humic complex and degrade the
soil structure, which leads to a decrease of porosity
and, consequently, a reduction of aeration. The high
salt concentrations also generate zones of low water
potential, which originates more difficulty in the
plant to take up water as well as nutrients. Thus,
saline stress essentially causes conditions of water
222 	 Pastos y Forrajes, Vol. 39, No.4, October-December, 219-228, 2016 / Salinity tolerance in turfgrass species
deficit in the plant and, subsequently, assumes the
characteristics of physiological drought. The ions of
higher involvement in saline stress are: Na+
, K+
, H+
and Ca+
(Mahajan and Tuteja, 2005).
The most widely used indexes to represent soil
salinity are total dissolved solids (TDS) and electrical
conductivity(EC);thelatterisbasedontherateatwhich
the electrical current passes through a saline solution,
which is proportional to the concentration of salts in
solution. Years ago it was expressed in mmhos/cm, at
present it is expressed in dS.m-1
(dS = deciSiemens)
at 25 ºC (Uddin and Juraimi, 2013); both measures
are equivalent (1 mmhos/cm = 1 dS.m-1
). From the
agricultural point of view a soil is classified as saline
when it has high concentrations of soluble salts, with
an EC of 4 dS.m-1
or higher (Uddin and Juraimi, 2013).
Effect of saline stress on the plant processes
Most cultivated plants (cereals, horticultural
ones, turfgrasses and other industrial crops, etc.) are
susceptible to saline stress (EC > 4 dS.m-1
), with the
subsequent reduction of productivity due to an inade-
quate nutrition (Egamberdieva and Lugtenberg, 2014).
The intensity with which each stress condition
affects plant growth and development depends on
several factors, including: the mophophysiological
characteristics of the species, cultivar, phenologi-
cal state, types of soluble salts, intensity and du-
ration of the stress and edaphoclimatic conditions
(Shahba et al., 2008; Manuchehri and Salehi, 2014).
The consequences of growth in a saline medium
are mainly due, according to Lamz and González
(2013), Bizhani and Salehi (2014) and Manuchehri
and Salehi (2014), to the individual or combined ef-
fect of the following stress factors:
•	 Hydric stress. The presence of solutes causes the
decrease of the osmotic potential of the soil solu-
tion (osmotic stress).
•	 The toxicity associated to the increase of specific
ions, such as sodium and chlorine (saline stress)
•	 The nutritional unbalance due to the high con-
centrations of sodium and chloride which reduce
the capture of K+
, NO3
-
, PO4
3-
, etc.
•	 The accumulation of reactive oxygen species
which destroy the cell membranes and affect vi-
tal molecules, such as proteins and nucleic acids.
Effect of saline stress on turfgrass species
Salinity is the main abiotic stress that influences
the growth and development of turf-forming plants;
affects the normal development of the plant at the
morphological, physiological and biochemical
levels; and, thus, decreases the visual quality and
aesthetic appearance of the turfgrass. Its effects
on the growth of turfgrasses are summarized in:
the reduction of water assimilation due to osmotic
stress, reduction of nutrient assimilation (for
example, the assimilation of potassium is decreased
by the entrance of Na+
) and increase of root biomass,
which increases water absorption and causes
interferences with the photosynthetic process
(Uddin and Juraimi, 2013). Table 1 describes some
studies about the most common effects provoked by
saline stress in turfgrasses.
Physiological, biochemical and molecular
mechanisms of salinity tolerance
The knowledge of the mechanisms of the salinity
tolerance phenomenon in plants is essential to face
this world problem.
Plants cannot escape the stress factors as animals
do,buttheymustratherfacetheenvironmentalchanges.
That is why understanding the response mechanisms
of plants to stress constitutes an efficacious tool for
agronomists, breeders and horticulture farmers,
being the basis for the development of strategies and
technologies that improve the resistance of crops to
stresses (Cheng, 2014).
As a result of saline stress, plants (including
turfgrasses) can respond with a wide range of physio-
logical solutions at molecular, cellular and organism
level (Huang et al., 2014). They include, for example,
changes in the development and morphology (inhi-
bition of the apical growth, increase in root growth
and changes in the life cycle), adjustment in the ionic
transport (concentration, expulsion and sequestra-
tion of ions, among which Na+
and K+
stand out), reg-
ulation of the antioxidant defense systems, changes
in the expression of genes and proteins involved in
the response to salinity, as well as other metabolic
mechanisms (carbon metabolism and synthesis of
compatible solutes) (Fuentes et al., 2007; Huang et
al., 2014). Nevertheless, plants do not respond in the
same way to saline stress. For such reason, according
to their capacity of adaptation to high salt concentra-
tions, they are classified into halophytes and glyco-
phytes (Roy and Chakraborty, 2014).
•	 Halophytes: those plants native from saline soils
which are capable of fulfilling their whole ontogenic
cycle in that environment and having mechanisms
for the elimination of salts from the internal tissues.
•	 Glycophytes: those plants which are affected by
salt and incapable of withstanding certain salt
concentrations as halophytes do.
Pastos y Forrajes, Vol. 39, No.4, October-December, 219-228, 2016 / Wendy M. Ramírez-Suárez 	223
The response mechanisms of plants (including
turfgrasses) to saline stress can be summarized in
three fundamental phases: 1) osmotic adjustment, 2)
ionic homeostasis (regulation of the ionic transport),
and 3) elimination of reactive oxygen species. This
is object of discussion in the works related to the
mechanisms of tolerance to abiotic stress factors
(Lamz and González, 2013; Uddin and Juraimi,
2013; Huang et al., 2014; Roy and Chakraborty,
2014; Flowers and Colmer, 2015; Uzilday et al.,
2015).
Flowers and Muscolo (2015) stated that
halophytes are little frequent with regards to the
total number of flowering plants. The order Poales
Table 1. Effect of saline stress in turfgrasses.
Studied species EC
(dS.m-1
)*
Observed effect Source
Cynodon dactylon 6 Loss of ions; decrease of the water and
chlorophyll content, and of the photo-
synthetic rate in the leaves.
Manuchehri and Salehi
(2014)
33 Decrease of the leaf growth and stem
weight, and negative effects on the
aesthetics of turf.
Chen et al. (2014)
5 Reduction of: stem size, dry and fresh
weight of the plant, leaf area, photo-
synthetic rate and chlorophyll content.
Bizhani and Salehi (2014)
Cultivars of Festuca rubra,
F. longifolia and F. ovina
6 Decrease of the germination
percentage and vegetative growth
(stem and root weight, water content).
Zhang et al. (2013)
Festuca spp., Poa pratensis,
Puccinellia distans
6-10
Decrease of the germination percentage
and leaf area.
Zhang et al. (2011)
Cultivars of Festuca spp.,
Agrostis spp., Puccinel-
lia spp. and Deschampsia
cespitosa
14
Decrease of the green color intensity of
the foliage.
Friell et al. (2013)
Lolium perenne
8
Inhibition of the root growth, increase
of the plant mortality; decrease of the
germination rate, root and stem length,
number of leaves, as well as the dry/
fresh weight of the plants.
Nizam (2011)
Poa pratensis
2,5
Reduction of: stem size, dry and fresh
weight of the plant, leaf area, photosyn-
thetic rate and chlorophyll content.
Bizhani and Salehi (2014)
Zoysia japonica 36,0 Reduction of the root and stem growth
and of the turf quality.
Uddin et al. (2010)
Uddin et al. (2011)Stenotaphrum secundatum 31,8
C. dactylon (satiri) 30,9
Zoysia teneuifolia 28,4
Digitaria didactyla 26,4
C. dactylon (Tifdwarf) 25,7
Paspalum notatum 20,8
Axonopus compressus 18,6
Paspalum vaginatum
36,5
49,4
50 % reduction in sprout growth.
50 % reduction in root growth.
Uddin et al. (2010)
*It refers to the electrical conductivity (EC) or the EC range at which the effects were observed.
224 	 Pastos y Forrajes, Vol. 39, No.4, October-December, 219-228, 2016 / Salinity tolerance in turfgrass species
comprises 8,1 % of all the halophyte plant species.
This type of plants has been classified, according
to Roy and Chakraborty (2014), as salt-tolerant
grasses (STGs), and constitutes the most important
source of salinity-tolerant genes. The main survival
mechanism of these plants in saline environments
is the regulation of the ionic transport, and more
specifically their capacity to eliminate the toxic Na+
and replace it by K+
, which is known as selectivity
of K+
over Na+
(Roy and Chakraborty, 2014). In
addition, another salinity tolerance mechanism
which is reported in all the Poaceae subfamilies,
except in Pooideae, is the presence of salt glands;
which play an important role in the regulation of the
ionic balance of the species of this family (Céccoli
et al., 2015).
In several halophyte turfgrass species the presence
of salt-excreting glands in the leaves has been identi-
fied. These glands are generally identified by their
morphology through conventional staining procedures,
along with optical microscopy. Parthasarathy et al.
(2015) used scanning electrochemical microscopy to
identify the glands not only for their morphology, but
also for their performance in the species C. dactylon L.
The study of the mechanisms that influence
significantly the establishment and survival of
halophytes provides basic information on the
functioning of these plants under saline stress
conditions,whichwillcontributetothetransformation
of the current crops, as well as to providing new
tolerant crops (Flowers and Muscolo, 2015).
Breeding and selection for salinity tolerance
in turfgrasses
In recent years the most widely used variables
as selection criteria have been the appearance and
the resistance or tolerance to biotic and abiotic
stress factors (Florkowski and He, 2008). This has
allowed such criteria to be aimed at those aspects
that are close to a more ecological management of
turfgrasses, such as:
•	 Drought tolerance (decrease of irrigation)
•	 Heat tolerance
•	 Salinity tolerance (irrigation with recycled waters)
•	 Shade tolerance (good growth under trees)
There is consensus on the fact that the most
effective method to reduce the effect of these
limiting factors is the attainment of resistant and/
or tolerant varieties, through breeding programs
adapted to the particular conditions of each locality
(Koc et al., 2009; Abogadallah et al., 2010; Li et al.,
2010; Patton, 2010; Trappe et al., 2011).
The study and evaluation of the variability
regarding the salinity tolerance of the species in
their natural environment (Hu et al., 2013; Lamz and
González, 2013), as well as the search for resistance
sources through the characterization and evaluation
of germplasm collections (Friell et al. 2013; Roy and
Chakraborty, 2014), are the key starting points for the
development of programs of breeding and introduction
of tolerant varieties. In this sense, the advances in
biotechnology and genetic engineering have been
successfully used in the attainment of new cultivars.
Thus the tolerance to saline stress has been achieved in
transgenicclonesofC.dactylonandLoliummultiflorum,
compared with the wild varieties (Huang et al., 2014).
On the other hand, Ma et al. (2014) could express genes
of Arabidopsis thaliana in F. arundinacea, with which
salinity tolerance was improved.
Salinity-tolerant turfgrass species
The large quantity of studies on salinity-tolerant
turfgrass species shows the preponderance acquired
by this abiotic stress in recent years. Manuchehri and
Salehi (2014) reported that C. dactylon is capable of
adapting moderately to different combined salinity
and drought conditions, with the activation of its os-
motic adjustment mechanisms and the regulation of
the enzymes that control the antioxidant activity. On
the other hand, Zhang et al. (2013) analyzed the per-
formance of nine Festuca cultivars in an EC range of
0-12 dS.m-1
and observed a significant tolerance of
the cultivars Slender and Stonewall to high salinity
concentrations (9-12 dS.m-1
). In a wider study in 74
cultivars of different turfgrass species, F. arundina-
cea showed a better performance and maintained a
medium quality in the green color of the foliage at an
EC of 14 dS.m-1
(Friell et al., 2013).
In a comparative analysis of the tolerance to
salinity in twelve turfgrass varieties, Zhang et al.
(2011) found that P. pratensis had the best perfor-
mance regarding the germination rate and leaf area
in a medium with high NaCl content. However,
Bizhani and Salehi (2014) established very low sa-
linity tolerance ranges for P. pratensis (EC = 2,5
dS.m-1
) compared with other turfgrass species.
Nizam (2011) studied the germination and
growth of L. perenne seedlings under different
stress condition and found a salinity tolerance of up
to EC = 8 dS.m-1
. On the other hand, Chen et al.
(2014) identified the sources of salinity tolerance in
900 accessions of wild germplasm of C. dactylon,
with which they established the bases for future
breeding programs in this species.
Pastos y Forrajes, Vol. 39, No.4, October-December, 219-228, 2016 / Wendy M. Ramírez-Suárez 	225
Uddin et al. (2011) compared salinity tolerance
in several turfgrass species and established a range
from higher to lower degree of tolerance: Z. japonica
> S. secundatum > C. dactylon > Zoysia teneuifolia
> Digitaria didactyla > C. dactylon (Tifdwarf) >
Paspalum notatum.
In a salinity tolerance study in 35 local turf-
grass varieties in Malaysia, Zulkaliph et al. (2013)
found tolerance with a concentration of EC = 24
dS.m-1
in the species P. vaginatum (UPM), local P.
vaginatum, Zoysia matrella, Z. japonica, C. dacty-
lon satiri and C. dactylon (Kuala Muda).
UddinandJuraimi(2013)summarizedthesalinity
tolerance capacity in the main turfgrass species (table
2); P. vaginatum, Z. japonica and S secundatum were
the megathermal species with the best results.
On the other hand, Ruiz et al. (2007) evaluat-
ed the salinity of a cultivated soil with some pas-
ture species, among them C. dactylon, which have
salt-excreting properties, as a physiological mecha-
nism of tolerance to this factor and found a trend to
salt reduction, a decrease of electrical conductivity
and of the concentration of salt-forming cations and
anions. This proved that these species on salinized
soils can constitute a natural ameliorator against this
problem.
In plastic pots prepared with a substratum of sand
and peat (9:1), Uddin et al. (2010) evaluated salinity
Table 2. Salinity tolerance in the main turfgrass species.
Species Tolerance
Mesothermal
Puccinellia spp. (Alkaligrass) T
Poa annua L. (Blue grass) S
Lolium multiflorum (Annual ryegrass) MS
Festuca rubra L. spp. (Chewing fescue) MS
Agrostis tenuis (Colonial bent grass) S
Agrostis palustris (Creeping bent grass) MS
Festuca rubra L. spp. rubra (Creeping red fescue) MT
Agropyron cristatum (Fairway wheat grass) MS
Festuca longifolia Thuill. (Hard fescue) MT
Poa pratensis L. Kentucy (Blue grass) MS
Loium perenne L. (Perennial rye grass) S
Festuca arundinacea Schreb. (Tall fescue) MT
Megathermal
Paspalum notatum Flugge (Bahiagrass) MS
Cynodon dactylon (Bermuda Tifdwarf) MS
Cynodon dactylon (Bermuda Satiri) MT
Bouteloua gracilis (H.B.K) (Blue Grama) MT
Bouteloua dactyloides Nutt. (Buffalo grass) MT
Eremochloa ophiuroides (Centipedegrass) Munro S
Paspalum vaginatum (Seashore paspalum) T
Stenotaphrum secundatum (St. Augustine) T
Zoysia japonica (Japanese lawn grass) T
Zoysia matrella (Manila grass) MT
Zoysia tenuifolia (Korean grass) MS
Digitaria didactylaWild (Serangoongrass) MT
Source: Uddin and Juraimi, 2013; S: sensitive (EC < 3 dS.m-1
), MS: moderately sensitive
(EC = 3-6 dS.m-1
), MT: moderately tolerant (EC = 6-10 dS.m-1
), T: tolerant (EC >10 dS.m-1
).
226 	 Pastos y Forrajes, Vol. 39, No.4, October-December, 219-228, 2016 / Salinity tolerance in turfgrass species
tolerance taking into consideration root and sprout
growth and the leaf burns in species that were sub-
ject to different salinity concentrations (0, 24, 48 and
72 dS.m-1
) through irrigation with seawater. The spe-
cies P. vaginatum and Z. matrella were grouped as
the most tolerant, capable of surviving high salinity
concentrations (between 36,5 and 49,4 dS.m-1
). In the
second group the salinity tolerance of the species was
moderate: local P. vaginatum and C. dactylon were
capable of tolerating EC values between 25,9 and 29,9
dS.m-1
; while in the group with lower tolerance the
species C. dactylon Greenles, E. ophiuroides, Axono-
pus compressus and Axonopus affinis were included;
these varieties were affected in the range of salinity
concentrations between 17,0 and 26,0 dS.m-1
.
Final considerations
Saline stress causes water deficit conditions
in the plant, which is translated into physiological
drought and a toxic effect of the ions as a result of
high solute contents. That is why understanding the
plant response mechanisms to this stress constitutes
an efficacious tool to achieve correct management
in areas affected by this limitation.
Salinity-tolerant plants are capable of growing
and completing their life cycle without significantly
decreasing their yields in substrata with high salt con-
centrations; due to morphological, physiological and
biochemical changes. Salinity influences crop germi-
nation, growth and yield, in general, but a large vari-
ability has been observed in the response to this stress
depending on the species, the cultivar and the pheno-
logical state of the plant.
Several studies have been conducted for the
evaluation of the salinity tolerance mechanisms in
turfgrass species; this knowledge is elementary for
the development of tolerant cultivars that contribute
to the implementation of management strategies in
sites affected by salinity.
For the different saline environments, plants
have developed adaptation mechanisms. The success
or failure of the establishment of turfgrass species
depends on the selection of the species that is best
adapted to the existing salinity conditions, for which
the knowledge of the tolerance mechanisms used by
plants is necessary.
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Accepted: May 19, 2016

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Salinity tolerance in turfgrass species

  • 1. Pastos y Forrajes, Vol. 39, No.4, October-December, 219-228, 2016 / Wendy M. Ramírez-Suárez 219 review paper Salinity tolerance in turfgrass species Wendy M. Ramírez-Suárez and Luis A. Hernández-Olivera Estación Experimental de Pastos y Forrajes Indio Hatuey, Universidad de Matanzas, Ministerio de Educación Superior Central España Republicana, CP 44280, Matanzas, Cuba E-mail: wendy.ramirez@ihatuey.cu Abstract: Salinity constitutes one of the problems that affect the sustainable development of gardening in tourism areas, golf courses, public spaces and sports fields; by causing stress in the turfgrass species and deteriorating the soil structure. Turfgrass production in Cuba takes place at the Pastures and Forages Research Station Indio Hatuey (Matanzas province), and its starting point are the results obtained at international level to search for alternatives that allow higher utilization of salinization-degraded soils and the increase of the production potential of the grass with the required quality. The objective of this paper is to contribute to the knowledge of salinity tolerance in turfgrass species. It approaches the stress types in plants, especially the stress caused by saline soils; the salinity tolerance mechanisms in plants and the studies conducted in some salinity-tolerant turfgrass species. Understanding the physiological and biochemical mechanisms and evaluating turfgrass species are essential to provide a practical solution for the salinity problem and establish a correct management in the turfgrass areas. Keywords: electrical conductivity, abiotic stress, saline soil Introduction The versatility and functionality of turfgrass species has had a determinant impact on the accelerated growth of the turfgrass industry in many countries, whose market value has reached up to 35 billion dollars only in the United States. The increase of the surface dedicated to the cultivation of turfgrass species increases in a directly proportional way to the increase of population nuclei in urban zones, for which the demand of plants for landscaping and recreational areas grows exponentially (Huang et al., 2014). In this sense, Cuba is not an exception. The main tourism areas of the country are located in the Cuban coasts, which demand large surfaces covered by turfgrass, just like the golf courses which have become a fundamental income source through international tourism (Marrero, 2006). However, one of the main challenges faced by the turfgrass industry is maintaining a high-quality turfgrass under adverse edaphoclimatic conditions, with minimum inputs and scarce or no environmen- tal impact. The most effective way to address this is- sue is the development, introduction and exploitation of germplasm that tolerates the main stress factors which affect turfgrass species (Huang et al., 2014). These turfgrass species are affected by several abiotic stress factors that influence especially the turf aesthetic quality, functionality and yield. In that sense, it is not strange that most breeding pro- grams in recent years have been aimed at obtaining varieties tolerant to abiotic stress factors, such as salinity (Abogadallah et al., 2010), drought (Barnes et al., 2014), shade (Trappe et al., 2011) and low temperatures (Li et al., 2010), among others. Hydric stress (caused by salinity and/or drought) is one of the most studied abiotic factors, for two main reasons: first, because it causes severe damage on plants; and, second, due to the large land extension that is affected by these limiting factors (Marcum, 2014). The negative effects of this stress type are significantly increased in coastal zones because of the so-called “island effect”, for the high salt content of the waters (Tang et al., 2013; Manuchehri and Salehi, 2014). The current turfgrass production in Cuba is led by the Pastures and Forages Research Station Indio Hatuey (Matanzas province), which has a turfing service that includes the sale, planting, establishment, fertilization, phytosanitary attention and rehabilitation of the turf, and in turn aims at improving the quality of golf courses, sports fields, gardens and public spaces, without forgetting the mandatory respect towards the environment. Likewise, this institution works on the establishment and evaluation of salinity-tolerant grasses and
  • 2. 220 Pastos y Forrajes, Vol. 39, No.4, October-December, 219-228, 2016 / Salinity tolerance in turfgrass species aims at implementing a technology that prevents excessive water consumption, to achieve sustainable development in the new gardening. Taking such problematic situation into account, the objective of this paper is to contribute to the knowledge about salinity tolerance in turfgrass species. Distribution, morphology and classification of turfgrass species Taxonomically most turfgrass species belong to the Poaceae family, which is considered highly important due to its cosmopolitan distribution and its usefulness (Kellogg, 2001). The Poaceae family, the largest of flowering plant families, comprises more than 9 000 species practically distributed in all the ecotypes of the planet. However, only fifty of these species have the adequate agro-morphological characteristics to be exploited, because of their functional, recreational and ornamental value, as turf-forming plants. Be- sides acting as plant cover in public parks, gardens, landscapes, golf courses and sports fields, they are able to reduce soil erosion, eliminate dust and dirt from the air, release oxygen and act as natural filter, elimination the contaminants of underground wa- ters (Uddin and Juraimi, 2013). Turfgrass species are reproduced by seeds, al- though they can be vegetatively established through stolons, sods and/or cuttings. They have a dense and fibrous root system which is extended mainly within the first 15-30 cm of soil. In turfgrasses there are three types of stem: crown, flowering culm and creeping or lateral stems, called stolons or rhizomes (Uddin and Juraimi, 2013). Accordingtotheadaptationrangestothedifferent rainfall and temperature conditions, turfgrass species can be divided into: megathermal (warm latitudes) and mesothermal (cold latitudes). The megathermal ones grow in an optimum temperature range that varies between 24 and 35 ºC and comprise perennial species such as Buchloe dactyloides Nutt. (buffalo grass), Zoysia japonica Steud. (Zoysia grass), Cynodon dactylon L. Pers. (bermuda), Eremochloa ophiuroides Munro (centipede grass), Paspalum vaginatum Sw. (paspalum), Stenotaphrum secundatum Walt. Kuntze (Saint Augustine grass), among others. On the other hand, mesothermal species grow in a temperature range between 10 and 22 ºC and comprise perennial and annual species such as Festuca arundinacea Schreb. (tall fescue), Poa pratensis L. (Kentucky bluegrass), Lolium perenne L. (ryegrass), Festuca rubra var. commutata and Festuca ovina var. duriuscula (sheep fescue), and Agrostis stolonifera L. (creeping bentgrass), (Huang et al., 2014). The most important morphoagronomic charac- teristics that the species must have for turf formation are: fast germination and establishment, fine texture (leaf width), intense color, strong root system, re- sistance to trampling, adaptation to low cutting and creeping and slow growth, besides showing resis- tance and/or tolerance to biotic and abiotic stresses. Abiotic stress and climate change In biology, the concept of stress is hard to define, taking into consideration that a certain biological condition can represent stress for an organism and, at the same time, be optimum for another. In a practical way, it can be considered as any adverse strength or condition that inhibits the normal functioning of a biological system (Mahajan and Tuteja, 2005). The term stress in the framework of plant physiology “shows the magnitude of environmental pressure that forces change in the physiology of a plant” (Nilsen and Orcutt, 1996). Levitt (1980) defines stress as: “any environmental factor potentially unfavorable for living organisms”. Plants are affected mainly by two types of stress: biotic and abiotic (physical or chemical). The biotic ones are originated by living organisms and comprise allelopathies and susceptibility to pests and diseases; while the abiotic ones are environmental, such as salinity, high/low temperatures, drought, shade, atmospheric contamination and toxins, among others. Abiotic stresses are one of the main factors that limit plant distribution and productivity of agricultural crops, because they affect negatively plant growth and productivity and trigger a series of morphological, physiological, biochemical and molecular disorders (Bhatnagar-Mathur et al., 2008; Cheng, 2014). In the last decades, the increase of the CO2 level in the troposphere has triggered global warming and the so-called climate change. These conditions have brought about the increasing appearance of extreme climate conditions, such as large drought and floodingperiods,prolongedheatorlowtemperatures; as well as the increase of soil salinization in many regions of the world, because of the elevation of sea level (Feng et al., 2014; Flowers and Colmer, 2015). These atmospheric phenomena drastically affect plant growth and productivity, and constitute an increasing threat for sustainability in agriculture,
  • 3. Pastos y Forrajes, Vol. 39, No.4, October-December, 219-228, 2016 / Wendy M. Ramírez-Suárez 221 biodiversity and homeostasis of ecosystems (Feng et al., 2014). Salinization is one of the most urgent environ- mental challenges to be solved, because of the dis- turbances it causes in the microbial communities and processes, which affects the C cycle in the soil (Rath and Rousk, 2015); this could limit the role of the soil as an important carbon sink that contributes to the mitigation of the climate change. In this ecological context it is necessary to identify and study the mechanisms of plants that are able to survive in such complex environments. Soil salinization. Causes and origin At present, soil salinization and sodification threaten soil fertility and crop productivity (Singh, 2015); this phenomenon has become a worldwide problem, which affects almost one third of the lands dedicated to agriculture, and is more serious in the arid and semiarid regions, where the scarce rainfall reduces the possibility of washing out the salts that are being supplied with the irrigation waters. The in- crease of the water demand in the world, especially in the arid and semiarid zones, has forced farmers to use low-quality water in agriculture, mainly from wells, with a high concentration of salts which often exceed the salt-tolerance thresholds of many crops and thus limit their production (Zhang et al., 2013; Chen et al., 2014; Manuchehri and Salehi, 2014). Soil salinization precedes the origin of human civilization and still is the main abiotic stress that hinders the productivity and quality of harvests (Lamz and González, 2013). Approximately 20 % of the cultivated area worldwide and nearly half the irrigated lands are affected by this factor (Zulkaliph et al., 2013; Egamberdieva and Lugtenberg, 2014); recent studies place the increase of the areas affect- ed by salinity between 1,0 and 1,5 million hectares per year (Wu et al., 2014; Zhang, 2014). This situa- tion is daily enhanced, because of the lack of envi- ronmental awareness and the irrational exploitation of water resources, besides other edaphoclimatic factors that influence directly soil salinity (Lamz and González, 2013). In this sense, Cuba has an agricultural surface of 6,7 million hectares, from which approximately 15 % (one million hectares) is affected by salinity or sodicity, and this limits the productive potential of Cuban soils (Rodríguez, 2015). Lamz and González (2013) stated that the term salinity refers to the presence of a high concentration of salts which damages the plants due to its toxic effect and the decrease of the osmotic potential of the soil. The salinization phenomenon may have several causes; primary or natural salinization occurs in soils which, since their formation, show accumulation of salts due to rock decomposition or volcanic activity; and it is found in sites where evaporation is higher than rainfall, in places close to the sea or which have saline streams and saline groundwater (Gómez et al., 2009). However, the most common is secondary salinization, mainly caused by the effects of irrigation, the use of low-quality waters, restricted drainage, low permeability of the soil, and wrong use of fertilization; which causes the accumulation of soluble salts, mainly sodium, in the upper horizons. This situation brings about the loss of land productivity and their subsequent abandonment (Egamberdieva and Lugtenberg, 2014). Álvarez-Menéndez et al. (2008) stated that the natural salt sources in the salinization process in Cuba are: • Marine aerosols carried by the atmospheric cir- culation of prevailing winds (East-Southeast and Southeast trade winds) and by waves of cold companion winds from the North. • Old marine sediments north and south of the Cu- ban archipelago, constituted by saline gypsum and sandy rocks. • The accumulation of continental sediments ca- rried by the rivers from the mountains to flat areas during the quaternary period. • Sea intrusion in calcic groundwater aquifers be- low the sea level. • The wind from arid regions can also contribu- te to the salinization process, dragging a large amount of salts, mainly carbonates, sulfates and chlorides which are suspended (Fuentes et al., 2007; Wu et al., 2014). The main soluble constituents of the soil related to salinity are cations (Na+ , Ca2+ , Mg2+ and K+ ), anions (Cl- ), sulfate (SO4 2- ), bicarbonate and/or carbonate (HCO3 /CO3 ) and nitrate (NO3 - ) (Nizam, 2011; Alshammary, 2013; Wu et al., 2014). The high salt concentrations(particularlyNa+ )whicharedeposited can alter its basic structure; the Na+ cations displace Ca2+ from the clayey-humic complex and degrade the soil structure, which leads to a decrease of porosity and, consequently, a reduction of aeration. The high salt concentrations also generate zones of low water potential, which originates more difficulty in the plant to take up water as well as nutrients. Thus, saline stress essentially causes conditions of water
  • 4. 222 Pastos y Forrajes, Vol. 39, No.4, October-December, 219-228, 2016 / Salinity tolerance in turfgrass species deficit in the plant and, subsequently, assumes the characteristics of physiological drought. The ions of higher involvement in saline stress are: Na+ , K+ , H+ and Ca+ (Mahajan and Tuteja, 2005). The most widely used indexes to represent soil salinity are total dissolved solids (TDS) and electrical conductivity(EC);thelatterisbasedontherateatwhich the electrical current passes through a saline solution, which is proportional to the concentration of salts in solution. Years ago it was expressed in mmhos/cm, at present it is expressed in dS.m-1 (dS = deciSiemens) at 25 ºC (Uddin and Juraimi, 2013); both measures are equivalent (1 mmhos/cm = 1 dS.m-1 ). From the agricultural point of view a soil is classified as saline when it has high concentrations of soluble salts, with an EC of 4 dS.m-1 or higher (Uddin and Juraimi, 2013). Effect of saline stress on the plant processes Most cultivated plants (cereals, horticultural ones, turfgrasses and other industrial crops, etc.) are susceptible to saline stress (EC > 4 dS.m-1 ), with the subsequent reduction of productivity due to an inade- quate nutrition (Egamberdieva and Lugtenberg, 2014). The intensity with which each stress condition affects plant growth and development depends on several factors, including: the mophophysiological characteristics of the species, cultivar, phenologi- cal state, types of soluble salts, intensity and du- ration of the stress and edaphoclimatic conditions (Shahba et al., 2008; Manuchehri and Salehi, 2014). The consequences of growth in a saline medium are mainly due, according to Lamz and González (2013), Bizhani and Salehi (2014) and Manuchehri and Salehi (2014), to the individual or combined ef- fect of the following stress factors: • Hydric stress. The presence of solutes causes the decrease of the osmotic potential of the soil solu- tion (osmotic stress). • The toxicity associated to the increase of specific ions, such as sodium and chlorine (saline stress) • The nutritional unbalance due to the high con- centrations of sodium and chloride which reduce the capture of K+ , NO3 - , PO4 3- , etc. • The accumulation of reactive oxygen species which destroy the cell membranes and affect vi- tal molecules, such as proteins and nucleic acids. Effect of saline stress on turfgrass species Salinity is the main abiotic stress that influences the growth and development of turf-forming plants; affects the normal development of the plant at the morphological, physiological and biochemical levels; and, thus, decreases the visual quality and aesthetic appearance of the turfgrass. Its effects on the growth of turfgrasses are summarized in: the reduction of water assimilation due to osmotic stress, reduction of nutrient assimilation (for example, the assimilation of potassium is decreased by the entrance of Na+ ) and increase of root biomass, which increases water absorption and causes interferences with the photosynthetic process (Uddin and Juraimi, 2013). Table 1 describes some studies about the most common effects provoked by saline stress in turfgrasses. Physiological, biochemical and molecular mechanisms of salinity tolerance The knowledge of the mechanisms of the salinity tolerance phenomenon in plants is essential to face this world problem. Plants cannot escape the stress factors as animals do,buttheymustratherfacetheenvironmentalchanges. That is why understanding the response mechanisms of plants to stress constitutes an efficacious tool for agronomists, breeders and horticulture farmers, being the basis for the development of strategies and technologies that improve the resistance of crops to stresses (Cheng, 2014). As a result of saline stress, plants (including turfgrasses) can respond with a wide range of physio- logical solutions at molecular, cellular and organism level (Huang et al., 2014). They include, for example, changes in the development and morphology (inhi- bition of the apical growth, increase in root growth and changes in the life cycle), adjustment in the ionic transport (concentration, expulsion and sequestra- tion of ions, among which Na+ and K+ stand out), reg- ulation of the antioxidant defense systems, changes in the expression of genes and proteins involved in the response to salinity, as well as other metabolic mechanisms (carbon metabolism and synthesis of compatible solutes) (Fuentes et al., 2007; Huang et al., 2014). Nevertheless, plants do not respond in the same way to saline stress. For such reason, according to their capacity of adaptation to high salt concentra- tions, they are classified into halophytes and glyco- phytes (Roy and Chakraborty, 2014). • Halophytes: those plants native from saline soils which are capable of fulfilling their whole ontogenic cycle in that environment and having mechanisms for the elimination of salts from the internal tissues. • Glycophytes: those plants which are affected by salt and incapable of withstanding certain salt concentrations as halophytes do.
  • 5. Pastos y Forrajes, Vol. 39, No.4, October-December, 219-228, 2016 / Wendy M. Ramírez-Suárez 223 The response mechanisms of plants (including turfgrasses) to saline stress can be summarized in three fundamental phases: 1) osmotic adjustment, 2) ionic homeostasis (regulation of the ionic transport), and 3) elimination of reactive oxygen species. This is object of discussion in the works related to the mechanisms of tolerance to abiotic stress factors (Lamz and González, 2013; Uddin and Juraimi, 2013; Huang et al., 2014; Roy and Chakraborty, 2014; Flowers and Colmer, 2015; Uzilday et al., 2015). Flowers and Muscolo (2015) stated that halophytes are little frequent with regards to the total number of flowering plants. The order Poales Table 1. Effect of saline stress in turfgrasses. Studied species EC (dS.m-1 )* Observed effect Source Cynodon dactylon 6 Loss of ions; decrease of the water and chlorophyll content, and of the photo- synthetic rate in the leaves. Manuchehri and Salehi (2014) 33 Decrease of the leaf growth and stem weight, and negative effects on the aesthetics of turf. Chen et al. (2014) 5 Reduction of: stem size, dry and fresh weight of the plant, leaf area, photo- synthetic rate and chlorophyll content. Bizhani and Salehi (2014) Cultivars of Festuca rubra, F. longifolia and F. ovina 6 Decrease of the germination percentage and vegetative growth (stem and root weight, water content). Zhang et al. (2013) Festuca spp., Poa pratensis, Puccinellia distans 6-10 Decrease of the germination percentage and leaf area. Zhang et al. (2011) Cultivars of Festuca spp., Agrostis spp., Puccinel- lia spp. and Deschampsia cespitosa 14 Decrease of the green color intensity of the foliage. Friell et al. (2013) Lolium perenne 8 Inhibition of the root growth, increase of the plant mortality; decrease of the germination rate, root and stem length, number of leaves, as well as the dry/ fresh weight of the plants. Nizam (2011) Poa pratensis 2,5 Reduction of: stem size, dry and fresh weight of the plant, leaf area, photosyn- thetic rate and chlorophyll content. Bizhani and Salehi (2014) Zoysia japonica 36,0 Reduction of the root and stem growth and of the turf quality. Uddin et al. (2010) Uddin et al. (2011)Stenotaphrum secundatum 31,8 C. dactylon (satiri) 30,9 Zoysia teneuifolia 28,4 Digitaria didactyla 26,4 C. dactylon (Tifdwarf) 25,7 Paspalum notatum 20,8 Axonopus compressus 18,6 Paspalum vaginatum 36,5 49,4 50 % reduction in sprout growth. 50 % reduction in root growth. Uddin et al. (2010) *It refers to the electrical conductivity (EC) or the EC range at which the effects were observed.
  • 6. 224 Pastos y Forrajes, Vol. 39, No.4, October-December, 219-228, 2016 / Salinity tolerance in turfgrass species comprises 8,1 % of all the halophyte plant species. This type of plants has been classified, according to Roy and Chakraborty (2014), as salt-tolerant grasses (STGs), and constitutes the most important source of salinity-tolerant genes. The main survival mechanism of these plants in saline environments is the regulation of the ionic transport, and more specifically their capacity to eliminate the toxic Na+ and replace it by K+ , which is known as selectivity of K+ over Na+ (Roy and Chakraborty, 2014). In addition, another salinity tolerance mechanism which is reported in all the Poaceae subfamilies, except in Pooideae, is the presence of salt glands; which play an important role in the regulation of the ionic balance of the species of this family (Céccoli et al., 2015). In several halophyte turfgrass species the presence of salt-excreting glands in the leaves has been identi- fied. These glands are generally identified by their morphology through conventional staining procedures, along with optical microscopy. Parthasarathy et al. (2015) used scanning electrochemical microscopy to identify the glands not only for their morphology, but also for their performance in the species C. dactylon L. The study of the mechanisms that influence significantly the establishment and survival of halophytes provides basic information on the functioning of these plants under saline stress conditions,whichwillcontributetothetransformation of the current crops, as well as to providing new tolerant crops (Flowers and Muscolo, 2015). Breeding and selection for salinity tolerance in turfgrasses In recent years the most widely used variables as selection criteria have been the appearance and the resistance or tolerance to biotic and abiotic stress factors (Florkowski and He, 2008). This has allowed such criteria to be aimed at those aspects that are close to a more ecological management of turfgrasses, such as: • Drought tolerance (decrease of irrigation) • Heat tolerance • Salinity tolerance (irrigation with recycled waters) • Shade tolerance (good growth under trees) There is consensus on the fact that the most effective method to reduce the effect of these limiting factors is the attainment of resistant and/ or tolerant varieties, through breeding programs adapted to the particular conditions of each locality (Koc et al., 2009; Abogadallah et al., 2010; Li et al., 2010; Patton, 2010; Trappe et al., 2011). The study and evaluation of the variability regarding the salinity tolerance of the species in their natural environment (Hu et al., 2013; Lamz and González, 2013), as well as the search for resistance sources through the characterization and evaluation of germplasm collections (Friell et al. 2013; Roy and Chakraborty, 2014), are the key starting points for the development of programs of breeding and introduction of tolerant varieties. In this sense, the advances in biotechnology and genetic engineering have been successfully used in the attainment of new cultivars. Thus the tolerance to saline stress has been achieved in transgenicclonesofC.dactylonandLoliummultiflorum, compared with the wild varieties (Huang et al., 2014). On the other hand, Ma et al. (2014) could express genes of Arabidopsis thaliana in F. arundinacea, with which salinity tolerance was improved. Salinity-tolerant turfgrass species The large quantity of studies on salinity-tolerant turfgrass species shows the preponderance acquired by this abiotic stress in recent years. Manuchehri and Salehi (2014) reported that C. dactylon is capable of adapting moderately to different combined salinity and drought conditions, with the activation of its os- motic adjustment mechanisms and the regulation of the enzymes that control the antioxidant activity. On the other hand, Zhang et al. (2013) analyzed the per- formance of nine Festuca cultivars in an EC range of 0-12 dS.m-1 and observed a significant tolerance of the cultivars Slender and Stonewall to high salinity concentrations (9-12 dS.m-1 ). In a wider study in 74 cultivars of different turfgrass species, F. arundina- cea showed a better performance and maintained a medium quality in the green color of the foliage at an EC of 14 dS.m-1 (Friell et al., 2013). In a comparative analysis of the tolerance to salinity in twelve turfgrass varieties, Zhang et al. (2011) found that P. pratensis had the best perfor- mance regarding the germination rate and leaf area in a medium with high NaCl content. However, Bizhani and Salehi (2014) established very low sa- linity tolerance ranges for P. pratensis (EC = 2,5 dS.m-1 ) compared with other turfgrass species. Nizam (2011) studied the germination and growth of L. perenne seedlings under different stress condition and found a salinity tolerance of up to EC = 8 dS.m-1 . On the other hand, Chen et al. (2014) identified the sources of salinity tolerance in 900 accessions of wild germplasm of C. dactylon, with which they established the bases for future breeding programs in this species.
  • 7. Pastos y Forrajes, Vol. 39, No.4, October-December, 219-228, 2016 / Wendy M. Ramírez-Suárez 225 Uddin et al. (2011) compared salinity tolerance in several turfgrass species and established a range from higher to lower degree of tolerance: Z. japonica > S. secundatum > C. dactylon > Zoysia teneuifolia > Digitaria didactyla > C. dactylon (Tifdwarf) > Paspalum notatum. In a salinity tolerance study in 35 local turf- grass varieties in Malaysia, Zulkaliph et al. (2013) found tolerance with a concentration of EC = 24 dS.m-1 in the species P. vaginatum (UPM), local P. vaginatum, Zoysia matrella, Z. japonica, C. dacty- lon satiri and C. dactylon (Kuala Muda). UddinandJuraimi(2013)summarizedthesalinity tolerance capacity in the main turfgrass species (table 2); P. vaginatum, Z. japonica and S secundatum were the megathermal species with the best results. On the other hand, Ruiz et al. (2007) evaluat- ed the salinity of a cultivated soil with some pas- ture species, among them C. dactylon, which have salt-excreting properties, as a physiological mecha- nism of tolerance to this factor and found a trend to salt reduction, a decrease of electrical conductivity and of the concentration of salt-forming cations and anions. This proved that these species on salinized soils can constitute a natural ameliorator against this problem. In plastic pots prepared with a substratum of sand and peat (9:1), Uddin et al. (2010) evaluated salinity Table 2. Salinity tolerance in the main turfgrass species. Species Tolerance Mesothermal Puccinellia spp. (Alkaligrass) T Poa annua L. (Blue grass) S Lolium multiflorum (Annual ryegrass) MS Festuca rubra L. spp. (Chewing fescue) MS Agrostis tenuis (Colonial bent grass) S Agrostis palustris (Creeping bent grass) MS Festuca rubra L. spp. rubra (Creeping red fescue) MT Agropyron cristatum (Fairway wheat grass) MS Festuca longifolia Thuill. (Hard fescue) MT Poa pratensis L. Kentucy (Blue grass) MS Loium perenne L. (Perennial rye grass) S Festuca arundinacea Schreb. (Tall fescue) MT Megathermal Paspalum notatum Flugge (Bahiagrass) MS Cynodon dactylon (Bermuda Tifdwarf) MS Cynodon dactylon (Bermuda Satiri) MT Bouteloua gracilis (H.B.K) (Blue Grama) MT Bouteloua dactyloides Nutt. (Buffalo grass) MT Eremochloa ophiuroides (Centipedegrass) Munro S Paspalum vaginatum (Seashore paspalum) T Stenotaphrum secundatum (St. Augustine) T Zoysia japonica (Japanese lawn grass) T Zoysia matrella (Manila grass) MT Zoysia tenuifolia (Korean grass) MS Digitaria didactylaWild (Serangoongrass) MT Source: Uddin and Juraimi, 2013; S: sensitive (EC < 3 dS.m-1 ), MS: moderately sensitive (EC = 3-6 dS.m-1 ), MT: moderately tolerant (EC = 6-10 dS.m-1 ), T: tolerant (EC >10 dS.m-1 ).
  • 8. 226 Pastos y Forrajes, Vol. 39, No.4, October-December, 219-228, 2016 / Salinity tolerance in turfgrass species tolerance taking into consideration root and sprout growth and the leaf burns in species that were sub- ject to different salinity concentrations (0, 24, 48 and 72 dS.m-1 ) through irrigation with seawater. The spe- cies P. vaginatum and Z. matrella were grouped as the most tolerant, capable of surviving high salinity concentrations (between 36,5 and 49,4 dS.m-1 ). In the second group the salinity tolerance of the species was moderate: local P. vaginatum and C. dactylon were capable of tolerating EC values between 25,9 and 29,9 dS.m-1 ; while in the group with lower tolerance the species C. dactylon Greenles, E. ophiuroides, Axono- pus compressus and Axonopus affinis were included; these varieties were affected in the range of salinity concentrations between 17,0 and 26,0 dS.m-1 . Final considerations Saline stress causes water deficit conditions in the plant, which is translated into physiological drought and a toxic effect of the ions as a result of high solute contents. That is why understanding the plant response mechanisms to this stress constitutes an efficacious tool to achieve correct management in areas affected by this limitation. Salinity-tolerant plants are capable of growing and completing their life cycle without significantly decreasing their yields in substrata with high salt con- centrations; due to morphological, physiological and biochemical changes. Salinity influences crop germi- nation, growth and yield, in general, but a large vari- ability has been observed in the response to this stress depending on the species, the cultivar and the pheno- logical state of the plant. Several studies have been conducted for the evaluation of the salinity tolerance mechanisms in turfgrass species; this knowledge is elementary for the development of tolerant cultivars that contribute to the implementation of management strategies in sites affected by salinity. For the different saline environments, plants have developed adaptation mechanisms. The success or failure of the establishment of turfgrass species depends on the selection of the species that is best adapted to the existing salinity conditions, for which the knowledge of the tolerance mechanisms used by plants is necessary. Bibliographic references Abogadallah, G. M.; Serag, M. M.; El-Katouny, T. M. & Quick, W. P. Salt tolerance at germination and vegetative growth involves different mechanisms in barnyard grass (Echinochloa crusgalli L.) mu- tants. Plant Growth Regul. 60 (1):1-12, 2010. Alshammary, S. F. Effect of salinty on ion relations of four turfgrasses. J. Food Agric. Environ. 11 (2):1321- 1326, 2013. Álvarez-Menéndez, A.; Baños, R. & Otero, Lázara. Salinidad y uso de aguas salinas para la irriga- ción de cultivos y forrajes en Cuba. Ciencia y tecnología ganadera. 2 (1):1-12, 2008. Barnes, B. D.; Kopecký, D.; Lukaszewski, A. J. & Baird, J. H. Evaluation of turf-type interspecific hybrids of meadow fescue with perennial ryegrass for impro- ved stress tolerance. Crop. Sci. 54 (1):355-365, 2014. Bhatnagar-Mathur, P.; Vadez, V. & Sharma, K. K. Transgenic approaches for abiotic stress toleran- ce in plants: retrospect and prospects. Plant Cell Rep. 27 (3):411-424, 2008. Bizhani, S. & Salehi, H. Physio-morphological and structural changes in common bermudagrass and Kentucky bluegrass during salt stress. Acta Physiol. Plant. 36 (3):777-786, 2014. Céccoli, G.; Ramos, J. C.; Pilatti, Vanesa; Dellaferre- ra, I. M.; Tivano, J. C.; Taleisnik, Edith et al. Salt glands in the Poaceae family and their relation-ship to salinity tolerance. The Botanical Review. 81 (2):162-178, 2015. Chen, J.; Zong, J.; Gao, Y.; Chen, Y.; Jiang, Q.; Zheng, Y. et al. Genetic variation of salinity tolerance in Chinese natural bermudagrass (Cynodon dac- tylon (L.) Pers.) germplasm resources. Acta Agr. Scand. B-S P. 64 (5):416-424, 2014. Cheng, Z-M. Introduction to the Special Issue: Stress biology of specialty crops. Crit. Rev. Plant Sci. 33 (2-3):90-91, 2014. Egamberdieva, Dilfuza & Lugtenberg, B. Use of plant growth-promoting rhizobacteria to alleviate sali- nity stress in plants. In: M. Miransari, ed. Use of microbes for the alleviation of soil stresses. New York: Springer. p. 73-96, 2014. Feng, G-Q.; Li, Y. & Cheng, Z-M. Plant molecular and genomic responses to stresses in projected future CO2 environment. Crit. Rev. Plant Sci. 33 (2-3):238-249, 2014. Florkowski, W. J. & He, S. Preference of golf-course ope- rators for various turf varieties and their perceived importance of selected problems in turf maintenan- ce. In: M. Pessarakli, ed. Handbook of turfgrass ma- nagement and physiology. Boca Ratón, USA: CRC Press, Taylor & Francis Group. p. 3-26, 2008. Flowers, T. & Colmer, T. Plant salt tolerance: adaptations in halophytes. Ann. Bot.-London. 115 (3):327-331, 2015. Flowers, T. J. & Muscolo, Adele. Introduction to the Special Issue: Halophytes in a changing world. A o B Plants. 7:1-5, 2015. Friell, J.; Watkins, E. & Horgan, B. Salt tolerance of 74 turfgrass cultivars in nutrient solution culture. Crop Sci. 53 (4):1743-1749, 2013.
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Physiology of plants un- der stress. vol. I Abiotic factors. New York: John Wiley & Sons, Inc., 1996. Nizam, I. Effect of salinity stress on water uptake, germi- nation and early seedling growth of perennial rye- grass. Afr. J. Biotechnol. 10 (51):10418-10424, 2011. Parthasarathy, M.; Pemaiah, B.; Natesan, R.; Padma- vathy, S. R. & Pachiappan, J. Real-time mapping of salt glands on the leaf surface of Cynodon dactylon L. using scanning electrochemical mi- croscopy. Bioelectroch. 101:159-164, 2015. Patton, A. Turf quality and stress tolerance: Improve turf performance and environmental stress to- lerance through proper cultivar selection. Golf Course Management. 78 (5):90-95, 2010. Rath, K. & Rousk, J. Salt effects on the soil microbial decomposer community and their role in orga- nic carbon cycling: A review. Soil Biol. Biochem. 81:108-123, 2015. Rodríguez, D. La conservación y el mejoramiento de los suelos en Cuba, medidas para su manejo sostenible. 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