REVI EW

Seed priming for abiotic stress tolerance: an overview

K. C. Jisha

K. Vijayakumari

Jos T. Puthur
Received: 11 July 2012 / Revised: 4 December 2012 / Accepted: 11 December 2012 / Published online: 27 December 2012
Franciszek Gorski Institute of Plant Physiology, Polish Academy of Sciences, Krakow 2012
Abstract Plants are exposed to any number of potentially
adverse environmental conditions such as water decit,
high salinity, extreme temperature, submergence, etc. These
abiotic stresses adversely affect the plant growth and pro-
ductivity. Nowadays various strategies are employed to
generate plants that can withstand these stresses. In recent
years, seed priming has been developed as an indispensable
method to produce tolerant plants against various stresses.
Seed priming is the induction of a particular physiological
state in plants by the treatment of natural and synthetic
compounds to the seeds before germination. In plant
defense, priming is dened as a physiological process by
which a plant prepares to respond to imminent abiotic stress
more quickly or aggressively. Moreover, plants raised from
primed seeds showed sturdy and quick cellular defense
response against abiotic stresses. Priming for enhanced
resistance to abiotic stress obviously is operating via vari-
ous pathways involved in different metabolic processes.
The seedlings emerging from primed seeds showed early
and uniform germination. Moreover, the overall growth of
plants is enhanced due to the seed-priming treatments. The
main objective of this review is to provide an overview of
various crops in which seed priming is practiced and about
various seed-priming methods and its effects.
Keywords Seed priming Abiotic stress Osmopriming
Productivity Hydropriming Chemical priming
Hormonal priming Biopriming Redoxpriming
Matripriming
Introduction
Plants are exposed to various abiotic factors throughout the
course of their growth and development (Zhao et al. 2007).
The major abiotic stresses to which plants are exposed
include extreme temperature, drought or high salinity. These
stresses are the most signicant factors leading to substantial
and unpredictable loss in crop production in agriculture
(Jakab et al. 2005). Modern agriculture strategies aim at
enhancing harvest yields per acreage and reducing pre-har-
vest and postharvest losses caused by detrimental abiotic
cues (Gust et al. 2010). In most plants, drought or salinity
causes a variety of biochemical, physiological and meta-
bolic changes (Xiong and Zhu 2002), which may result in
oxidative stress and affect plant metabolism, performance
and thereby the yield (Sha et al. 2009). Salt and osmotic
stresses are also responsible for both inhibition or delayed
seed germination and seedling establishment (Almansouri
et al. 2001). Soil salinity may affect the germination of seeds
either by creating a lower osmotic potential external to the
seed preventing water uptake, or through the toxic effects of
Na
?
and Cl
-
ions on the germinating seed (Khajeh-Hosseini
et al. 2003). The physiological mechanisms through which
plants respond to salinity and drought show high similarity,
suggesting that both stresses must be perceived by the plant
cell as deprivation of water (Tavili et al. 2011). Other abiotic
stress factors such as heat, cold, irradiation or light stress are
also known to adversely affect the crops (Reyes and Cisn-
eros-Zevallos 2007).
Plant interaction with environmental stress factors is
known to lead to the activation of various defense
Communicated by A. K. Kononowicz.
K. C. Jisha K. Vijayakumari J. T. Puthur (&)
Plant Physiology and Biochemistry Division,
Department of Botany, University of Calicut,
C.U. Campus P.O., Thenjipalam 673635, Kerala, India
e-mail: jtputhur@rediffmail.com; jtputhur@yahoo.com
1 3
Acta Physiol Plant (2013) 35:13811396
DOI 10.1007/s11738-012-1186-5
mechanisms resulting in a qualitative and/or quantitative
change in plant metabolite production, activation of hor-
mone signaling pathways regulated by abscisic acid, sali-
cylic acid, jasmonic acid and ethylene, as well as reactive
oxygen species (ROS) signaling pathways (Fujita et al.
2006). Moreover, both environmental and biotic stresses
can induce emissions of an array of organic compounds in
any plant species, whereas the magnitude of emissions
induced by given stress depends on stress tolerance, timing,
duration and severity (mild vs. strong) of the stress
(Niinemets 2009). Plant produced (biogenic) volatile
organic compounds (BVOCs) function as important pro-
tective and signaling molecules (Vickers et al. 2009).
Various methodologies were adapted from time to time
to achieve tolerance to stresses. These include, conven-
tional breeding methods such as selection and hybridiza-
tion and modern methods such as mutation breeding,
polyploidy breeding, genetic engineering, etc. The con-
ventional breeding techniques have limitations like
requirements of large man power, energy, etc. Attempts to
generate plant varieties with improved salinity and drought
tolerance using selection-based breeding strategies have
proved largely unsuccessful mostly because of the well-
recognized complexity or multigenic nature of salinity and
drought-tolerance traits (Cushman and Bohnert 2000;
Flowers et al. 2000). Attempts were also made to produce
transgenic plants which can withstand various kinds of
stresses. Genetic engineering holds the potential of being
reasonably fast and predictable in its consequences because
of the targeted introduction of individual, heterologous
traits into elite crop lines (Gust et al. 2010). The incorpo-
ration of transgenes into breeding programs is not a simple
process. Due to the effects such as pleiotropy and gene
silencing, it is not possible to continue through the plant
breeding process with the precision with which the selec-
tion of the gene was begun (Flowers et al. 1997). Besides
this major drawback, these methods are also expensive,
cumbersome, and there exist biosafety regulations and
restrictions which hinder the introduction of transgenics
into the eld. Due to the above-mentioned limitations of
the available techniques, it has become imperative to think
of an alternative solution to impart tolerance to plants
against various stresses. The alternative solution would be
more acceptable if it is simple, cost effective and can be
adopted by the farmers without any complication and at the
same time it should be effective in manifesting the
tolerance.
Seed priming has proved to be an effective method in
imparting stress tolerance to plants. Seed priming is the
induction of a particular physiological state in plants by the
treatment of natural and synthetic compounds to the seeds
before germination. The physiological state in which plants
are able to faster or better activate defense responses or
both is called the primed state of the plant (Beckers and
Conrath 2007). Over the past few years, priming, particu-
larly seed priming has emerged as a promising strategy in
modern stress (biotic and abiotic) management as it pro-
tects plants against pathogens and abiotic stresses without
heavily affecting tness (Van Hulten et al. 2006). Com-
pounds that are able to reduce damaging effects of various
abiotic stresses should be of great importance from both the
theoretical and application points of view (Uchida et al.
2002). Priming is not exclusive to plants, it has also been
described in animals. A classic example is the enhanced
response of mammalian monocytes and macrophages to
bacterial lipopolysaccharides. Upon recognizing bacterial
lipopolysaccharides, monocytes and macrophages produce
various cytokines with important roles in the defense
against viruses, bacteria, parasites or tumor cells (Raetz
et al. 1991; Chen et al. 1992).
Seed priming is also widely used to synchronize the
germination of individual seeds (Taylor and Harman 1990).
Improved seed invigoration techniques are known to
reduce emergence time, accomplish uniform emergence,
and give better crop stand in many horticultural and eld
crops (Ashraf and Foolad 2005). Seed-priming technology
has twofold benets: enhanced, rapid and uniform emer-
gence, with high vigor and better yields in vegetables and
oriculture (Bruggink et al. 1999) and some eld crops
(Basra et al. 2005; Kaur et al. 2005). According to
McDonald (2000), primed seeds acquire the potential to
rapidly imbibe and revive the seed metabolism thus
enhancing the germination rate.
In many crops, seed germination and early seedling
growth are the most sensitive stages of water limitation and
the water decit may delay the onset and reduce the rate
and uniformity of germination, leading to poor crop per-
formance and yield (Demir et al. 2006). Therefore, the
benecial effects of priming may be more evident under
unfavorable rather than favorable conditions (Parera and
Cantliffe 1994). Primed seeds usually exhibit an increased
germination rate, greater germination uniformity, and at
times, greater total germination percentage (Basra et al.
2005). These attributes have practical agronomic implica-
tions, notably under adverse germination conditions
(McDonald 2000). Therefore, there is a strong interest in
the seed industry to nd suitable priming agent(s) that
might be used to increase the tolerance of plants under
adverse eld conditions (Job et al. 2000).
Although priming at seed stage is the common practice
and most reported, plants are also primed at seedling stage.
For priming the seeds, seeds are partially hydrated until the
germination process begins, but radical emergence does not
occur (Bradford 1986). Information on the application of
priming in the eld is limited (Capanoglu 2010). When
priming is done at seedling stage, the most preferred form
1382 Acta Physiol Plant (2013) 35:13811396
1 3
of application is soil drenching (Cohen et al. 2007) or foliar
spraying (Jeun et al. 2004).
Priming methods/agents
The various approaches include hydropriming, osmopri-
ming, chemical priming, hormonal priming, biological
priming, redox priming, solid matrix priming, etc.
Although priming improves the rate and uniformity of
seedling emergence and growth particularly under stress
conditions (Parera and Cantliffe 1991), the effectiveness of
different priming agents varies under different stresses and
with different crop species (Iqbal and Ashraf 2005).
Hydropriming
Hydropriming has been reported to be a simple, econom-
ical and a safe technique for increasing the capacity of
seeds towards osmotic adjustment, enhancing seedling
establishment and crop production under stressed condi-
tions (Kaur et al. 2002). In this priming method, the seeds
are immersed in sterilized distilled water kept at appro-
priate temperature and the duration of hydropriming is
determined by controlling seed imbibition during germi-
nation (Kaya et al. 2006). It is absolutely necessary to dry
the seeds after soaking as storing of improperly dried seeds
will do more harm than good (Thomas et al. 2000). After
soaking, seeds were re-dried to their original weight with
forced air under shade (Bennett and Waters 1987). In hy-
dropriming, the advantageous fact is the enhancement of
physiological and biochemical events taking place in seeds
even when the germination is suspended by low osmotic
potential and negligible matric potential of the imbibing
medium (Basra et al. 2003). Moreover, the protoplasm of
hydroprimed seeds/plants is found to have a lower viscosity
and exhibit higher permeability to water and nutrients and
also hold water against dehydrating forces (Thomas et al.
2000). Increase in the seedling growth correlated with
higher water uptake by primed seeds is the predominant
feature in the case of hydropriming (Yagmur and Kaydan
2008).
Various works have shown that hydropriming of seeds
have many advantages as compared to non-primed seeds.
Hydropriming has resulted in 3- to 4-fold increases in root
and shoot length in comparison with seedlings obtained
from non-primed seeds in drought condition (Kaur et al.
2002). This phenomenon was explained to be due to faster
emergence of roots and shoots, more vigorous plants, better
drought tolerance under adverse conditions (Amzallag
et al. 1990; Passam and Kakouriotis 1994; Cayuela et al.
1996; Lee-suskoon et al. 1998). Fujikura et al. (1993)
presented hydropriming as a simple and inexpensive
method of seed priming and according to Abebe and Modi
(2009), it is a very important seed treatment technique for
rapid germination and uniform seedling establishment in
various grain crops.
On-farm seed priming (soaking seeds in water prior
to sowing) has been shown to be effective in producing
early germination, better establishment and increased
yields in a wide range of crops in diverse environments
(Rashid et al. 2006). Hydropriming was found to be the
most effective method for improving seed germination of
onion, especially when the seeds were hydrated for 96 h
compared to 48 h (Caseiro et al. 2004). The benecial
effects of hydropriming on aged or unaged seeds of cau-
liower with respect to germination and percentage of
normal seedlings formed were studied by Fujikura et al.
(1993). In basil (Ocimum basilicum L.) under saline con-
ditions, the seedling vigor, germination percentage and
seedling dry weight was found to increase due to hydro-
priming (Farahani and Marou 2011). Hydropriming was
found to be the most effective in the case of mustard,
amongst the different priming methods tried (Srivastava
et al. 2010a). Moreover, Rashid et al. (2006) have sug-
gested that on-farm priming of barley seeds could be rec-
ommended to farmers in North West Frontier Province
(NWFP) of Pakistan and in similar environments in other
parts of the world. Sung and Chiu (1995) proposed that
emergence force and seedling growth were strengthened by
hydropriming in watermelon seeds. Hydropriming has been
shown to result in the earlier germination of desert cacti
(Dubrovsky 1996), Allium porrum (Ashraf and Bray 1993),
pyrethrum (Tanacetum cinerariifolium) (Li et al. 2011),
and coriander (Rithichai et al. 2009).
On-farm seed priming of maize in the semi-arid tropics
has been shown to improve crop establishment and yield,
but the benets can be variable. Priming decreased the
temperature optimum and ceiling temperature for germi-
nation and also helped in advancing the germination time
and did not decrease the nal percentage emergence
(Finch-Savage et al. 2004). Janmohammadi et al. (2008)
presented hydropriming as suitable, cheap and easy seed
invigoration treatment for inbred lines of maize, espe-
cially when germination is affected by salinity and
drought stress.
In mungbean, primed seeds germinated and emerged
faster and more completely, resulting in the establishment
of 45 % more plants per unit area than non-primed seeds.
Primed crops produced 80 % more above-ground biomass
(3.3 vs. 1.9 t ha
-1
), 264 % more pod yield (1.0 vs.
0.28 t ha
-1
) and 415 % more grain (0.36 vs. 0.07 t ha
-1
)
than did non-primed crops (Rashid et al. 2004). According
to Posmyk and Janas (2007), hydropriming and hydropri-
ming along with proline can be used as a safe priming
Acta Physiol Plant (2013) 35:13811396 1383
1 3
method for improving seed germination and growth of
Vigna radiata seedlings at low temperature and also
allowing fast repair of injuries caused by stress. It was
suggested that exogenously applied proline protects against
lipid peroxidation, by stabilizing membranes during chill-
ing and also functions as a source of nitrogen and carbon,
improving seedling growth and regeneration.
Osmopriming
Osmoconditioning or osmopriming is the soaking of seeds
in aerated, low-water-potential solutions. Osmopriming
essentially exposes seeds to a low external water potential
to restrict the rate and extent of imbibition. The process of
osmopriming is akin to a prolonged early imbibition of
seeds that sets in motion a gradual progression of various
pre-germinative metabolic activities. Thus, it is helpful to
use osmopriming as a model to study the transition of seeds
from a dry and physiologically quiescent to a hydrated and
physiologically active state (Chen and Arora 2011).
A variety of chemicals are used to create low-water-
potential solutions. Polyethylene glycol (PEG) is more
commonly used as water potential lowering agent because
of its nontoxic nature and large molecular size, which
lowers water potential without penetrating into the seeds
during soaking (Thomas et al. 2000). The other chemicals
used to lower water potential are KNO
3
, KCl, K
3
PO
4
,
KH
2
PO
4
, MgSO
4
, CaCl
2
, NaCl, mannitol, etc. (Farooq
et al. 2005). Osmopriming is methodologically, technically
and nancially more exacting than hydropriming (Moradi
and Younesi 2009) because the osmotic seed priming
produces quicker and easier results and is far less expen-
sive than most water conservation techniques, and offers
farmers a highly attractive alternative for improving crop
establishment and yields (Foti et al. 2008). Jett et al. (1996)
explained that, osmopriming in comparison with hydro-
priming can preserve plasma membrane structure and
cause seeds to have better responses to germination traits
because of controlled long hydration in seeds. In rice, the
physiological changes produced by osmohardening
enhanced the starch hydrolysis and made more sugars
available for embryo growth, vigorous seedling production
and later on improved allometric, kernel yield and quality
attributes (Farooq et al. 2006c).
Osmopriming with PEG
Osmo priming with PEG was described as a good
technique for improving seed germination of Bromus
seeds under salt and drought stress (Tavili et al. 2011)
and for increasing the germination percentage and
seedling vigor of bersim (Trifolium alexandrinum) seeds
(Rouhi et al. 2010). In soybean too, seed priming with
PEG was successfully carried out by Khalil et al. (2001).
Osmopriming with PEG results in strengthening the
antioxidant system and increasing the seed germination
potential, nally resulting in an increased stress tolerance
in germinating seeds of spinach (Chen and Arora 2011).
Elkoca et al. (2007), recommended hydropriming for
12 h or osmopriming (PEG -0.5 MPa) for 24 h for a
better germination of chickpeas under cold soil condi-
tions. Compared to hydropriming, priming with PEG in a
proper concentration was found to have a better effect on
seed germination and seedling growth under drought
stress (Yuan-Yuan et al. 2010). Rouhi et al. (2011)
suggested that different priming techniques (hydro and
osmopriming) had a varying effects on germination on
each of the four grass species (Bromus inermis, Festuca
arundinacea, Agropyron elongatum and Festuca ovina)
and the result showed that, for most evaluated germi-
nation parameters, osmopriming treatment (with PEG)
was more useful technique to reduce abiotic stress than
hydropriming treatment.
Osmopriming with NaCl
The higher salt tolerance of plants from NaCl-primed seeds
seems to be the result of higher capacity for osmotic
adjustment since plants from primed seeds have more Na
?
and Cl
-
in roots and more sugars and organic acids in
leaves than plants from non-primed seeds (Cayuela et al.
1996). Priming with NaCl solutions may make it possible
to establish a crop by direct sowing in saline conditions
(Cuartero and Fernandez-Munoz 1999). The improved seed
performance could be attributed partially to osmotic
adjustment, metabolic repair processes or a buildup of
germination metabolites during treatments (Haghpanah
et al. 2009). Salt priming with NaCl is an effective pre-
germination practice for overcoming salinity and drought-
induced negative effects in sugarcane (Patade et al. 2009).
Farhoudi and Sharifzadeh (2006) and Sarwar et al.
(2006) while working with canola and chickpea, respec-
tively, reported salt priming-induced improvement in seed
germination, seedling emergence and growth under saline
conditions. Priming led to an increased solubilization of
seed storage proteins like the beta-subunit of the 11-S
globulin in Beta vulgaris L. (Bourgne et al. 2000) and
reduction in lipid peroxidation and enhanced antioxidative
activity in seeds of Momordica charantia L. (Yeh et al.
2005) and Zea mays L. (Randhir and Shetty 2005).
Recently, Afzal et al. (2005) observed that the priming-
induced salt tolerance was associated with improved
seedling vigor, metabolism of reserves as well as enhanced
K
?
and Ca
2?
and decreased Na
?
accumulation in wheat
plants.
1384 Acta Physiol Plant (2013) 35:13811396
1 3
In mungbean, pretreatment of the seeds with sublethal
dose of NaCl ameliorated the injurious effects of NaCl
stress to some extent by increasing growth, photosynthetic
pigments, activities of antioxidant enzymes and accumu-
lation of osmolytes for osmotic adjustments (Saha et al.
2010). Seed priming with NaCl in melon (Cucumis melo)
was also found to be a useful strategy to increase the salt
tolerance of melon plants in the long term and also help in
the establishment of melon crop by direct sowing in a
saline medium and the salt tolerance of seedlings is
obtained by promoting K
?
and Ca
2?
accumulation, besides
inducing osmoregulation by the accumulation of organic
solutes (Sivritepe et al. 2003, 2005). Furthermore, NaCl
priming increased salt tolerance of sunower seeds by
promoting K
?
and Ca
2?
accumulation and inducing
osmoregulation by the accumulation of proline (Bajehbaj
2010). In milk thistle (Silybum marianum) which is a
medicinal plant, seed priming with NaCl and GA
3
had
higher germination rate than control and produced more
dry matter under salinity stress. Moreover, priming with
NaCl was found to be simple and cheap, and therefore
found suitable to be recommended to the farmers, so they
can get better crop stand and synchrony of emergence in
medicinal plants under the environmental stresses (Sedghi
et al. 2010).
Osmopriming with mannitol
It was reported that osmo and hydropriming of chickpea
seeds with mannitol and water alleviated the adverse
effects of water deciency and salt stress on seedling
growth. The treatment of seeds with water, 2 and 4 %
mannitol increased the length and biomass of roots and
shoots of chickpea seedlings as compared to non-primed
controls under salt stressed conditions (Kaur et al. 2002,
2005). Osmo- and hydropriming with water and mannitol
were found to be effective methods to enhance the ability
of salt tolerance and to improve seed germination and
seedling growth of alfalfa under high salt stress condition.
The above priming treatments signicantly enhanced the
activities of catalase (CAT), peroxidase (POD), superoxide
dismutase (SOD) and proline content and reduced the
malondialdehyde (MDA) accumulation and electrolyte
leakage under the salt stress condition. It was suggested
that these priming methods could be applied in alfalfa
production in high saline soils in the future (Amooaghaie
2011).
Osmopriming with other chemicals
Various other chemicals are also reported to act as agents
of osmopriming. Priming with KNO
3
can be used to
increase watermelon germination (Demir and Mavi 2004)
and in tomato, seed priming with KNO
3
increased germi-
nation percentage, germination index, root length, shoot
length and seedling fresh weight (Nawaz et al. 2011). In
rice, seed-priming treatments such as pre-germination,
hydropriming for 48 h, osmohardening with KCl and
CaCl
2
, ascorbate priming and hardening shortened the
emergence time and enhanced the energy and index of
seedling emergence. Seedlings from primed seeds had
greater length, increased number of roots and enhanced
fresh and dry mass than control. Among the treatments,
CaCl
2
, ascorbate and KCl proved better in enhancing
emergence and seedling growth. Seed priming changed the
pattern of nitrogen and calcium homeostasis both of the
seeds and seedlings, which were associated to enhancing
a-amylase activity and reducing sugars content (Farooq
et al. 2006a).
Osmopriming with KNO
3
improved the rate and gen-
erally improved the uniformity of seedling emergence in
leek (Brocklehurst et al. 1984), sorghum (Moradi and
Younesi 2009) and tomato (Heydecker et al. 1973;
Ozbingol et al. 1998). Chiu et al. (2006) reported that
KNO
3
effectively improved germination, seedling growth
and seedling vigor index of the seeds of sunower vari-
eties. Salt priming with KNO
3
, is an effective way to
improve seed and seedling vigor of sunower and
cucumber (Singh and Rao 1993; Ghassemi-Golezani and
Esmaeilpour 2008).
Nutrient priming
Nutrient priming has been proposed as a novel technique
that combines the positive effects of seed priming with an
improved nutrient supply (Al-Mudaris and Jutzi 1999). In
nutrient priming, seeds are pretreated (primed) in solutions
containing the limiting nutrients instead of being soaked
just in water (Arif et al. 2005). Increasing evidence sug-
gests that mineral-nutrient status of plants plays a critical
role in increasing plant resistance to environmental stress
factors (Marschner 1995). Of the mineral nutrients, potas-
sium plays a particular role in contributing to the survival
of crop plants under environmental stress conditions
(Cakmak 2005). Seed priming in Zn
2?
solutions improves
grain yield of chickpea and wheat (Arif et al. 2007).
Ascorbic acid, another important vitamin is also used for
priming due to its antioxidant nature. It has already been
proved that a high level of endogenous ascorbate is
essential to maintain the antioxidant capacity that protects
plants from oxidative stress (Zhou et al. 2009). Ascorbic
acid pretreatment results in improved germination proper-
ties of Agropyron elongatum under salt stress condition
(Tavili et al. 2009).
Acta Physiol Plant (2013) 35:13811396 1385
1 3
Hormonal priming
Seed performance of various crops can be improved by
inclusion of plant growth regulators and hormones during
priming and other pre-sowing treatments (Lee et al. 1998).
Abscisic acid (ABA) is a phytohormone extensively
involved in responses to abiotic stresses such as drought,
low temperature, and osmotic stress (Fujita et al. 2006).
Besides inducing the expression of many salt-responsive
genes (Chandler and Robertson 1994; Ingram and Bartels
1996; Bray 1997; Zhu et al. 1998; Rock 2000), exogenous
ABA application was shown in some experiments to
increase salt tolerance of the treated plants or plant tissues
(Xiong and Zhu 2002). At the molecular level, ABA
induces the expression of numerous plant genes (Rock
2000). Some of these genes encode various signal trans-
duction components such as putative receptors, protein
kinases/phosphatases and transcription factors that may
participate in salt stress signaling; others encode effectors
for stress tolerance (Xiong and Zhu 2002). ABA priming
showed increased rate of germination as compared to non-
primed seeds in Indian mustard (Srivastava et al. 2010a, b).
ABA-primed seeds of Brassica napus exhibited earlier
(27 days) germination and higher nal percent radicle
protrusion than non-primed control seeds, under salt
(100 mM NaCl) or water stress (20 % PEG 8000) and at a
low temperature (8 C) (Gao et al. 2002).
The benecial effects of gibberellic acid (GA
3
) on ger-
mination are well known (Angrish et al. 2001; Radi et al.
2001; Khan et al. 2002). GA
3
(100 mg l
-1
) applied as pre-
sowing treatment resulted in the highest K
?
and Ca
2?
content in the shoots of both faba beans (Vicia faba) and
cotton (Gossypium barbadense) crops (Harb 1992).
Recently, auxin is also used for priming (Akbari et al.
2007). In wheat seed germination, auxin treatments
increased the hypocotyl length, seedling fresh and dry
weight and hypocotyl dry weight (Akbari et al. 2007). The
growth regulators IAA and GA
3
were reported to improve
germination of pyrethrum seeds under non-saline condition
(Bisht et al. 2009).
In wheat, among the different seed-priming agents like
salicylic acid, ascorbic acid, kinetin and GA
3
, ascorbic acid
showed better results (Khan et al. 2011). Salicylic acid
priming in fennel seeds also showed better germination
under low water potential (Farahbakhsh 2012). Moreover,
in Salicornia utahensis, which is a halophyte, priming with
growth regulators like fusicoccin, thiourea, kinetin, and
ethephon alleviated the inhibitory effects of salinity on the
germination, whereas GA
3
, proline, betaine and nitrate had
little effect on germination at all salinities (Gul and Khan
2003). 3 % KNO
3
supplemented with 3 lM methyl jasm-
onate (MeJA) could promote germination and emergence
of dormant Amaranthus cruentus L. seeds (Tiryaki et al.
2005). More recently, seeds of Agropyron elongatum
primed with gibberellin (GA) and abscisic acid (ABA)
exhibited induced CAT and SOD activities under drought
conditions when compared to unprimed seeds (Eisvand
et al. 2010).
Enhanced replication in root tips has been reported by
hormonal and vitamin priming (Shakirova et al. 2003).
Vigor enhancement by the incorporation of growth regu-
lators in priming solution might be due to increased cell
division within the apical meristem of seedling root, which
caused an increase in plant growth. Moreover, hormonal
treatments maintain the IAA and cytokinin levels in the
plant tissues, which enhance the cell division (Sak-
habutdinova et al. 2003).
Redox priming
Cellular redox state is an important factor which regulates
the key process in growth and development as well as
stress tolerance. In response to any external stimuli, plants
modify their redox state and the extent of change is
dependent on the nature of the stimulus itself, the dose and
the time to which the tissue is exposed (Miller et al. 2009).
It is believed that if the reduced redox state is maintained,
the extent of stress-induced damage can be minimized
(Mittler 2002). It was earlier reported that pretreatment of
seeds and foliar spray of the seedlings at later stages in
mustard and wheat with different thiol compounds and
particularly with thiourea could increase the stress toler-
ance and, more importantly, crop productivity (Sahu and
Singh 1995; Sahu et al. 2005). Thiourea treatment to the
seeds of Brassica juncea was found to be helpful in
maintaining the integrity and functioning of mitochondria
in seeds as well as seedlings exposed to salinity, which was
otherwise found to be negatively affected under salinity
stress (Srivastava et al. 2009). Thiourea treatment to the
seeds of B. juncea was also found to regulate different
signalling and effector mechanisms in a synchronized
manner, at an early stage to alleviate stress even under a
high degree of salinity (Srivastava et al. 2010b).
Both ROS such as hydrogen peroxide and reactive
nitrogen species such as NO are involved in a wide range
of stress responses. These include cold, heat, pathogen
challenge and drought responses (Hancock et al. 2011).
Seed priming with H
2
O
2
was found to enhance the chilling
tolerance of capsicum (Yadav et al. 2011) and is known to
induce chilling tolerance in B. juncea L. and which was
further ameliorated in combination of H
2
O
2
with 24-epi-
brassinolide (24-EBL). 24-EBL treatment at seed and
seedling stage helped in alleviating the toxic effects of
H
2
O
2
through antioxidant defense system by increasing the
activities of various enzymes involved in the antioxidant
1386 Acta Physiol Plant (2013) 35:13811396
1 3
defense system such as catalase, ascorbate peroxidase and
superoxide dismutase (Manish et al. 2010). Seed priming
with H
2
O
2
was also reported in wheat (Wahid et al. 2007).
Signicant enhancement of seed germination and seedling
vigor due to exogenous application of NO donors through
seed treatment was reported in pearl millet (Manjunatha
et al. 2008). Recently, Barba-Esp n et al. (2012) reported
that H
2
O
2
could act as signaling molecule in the beginning
of seed germination involving specic changes at proteo-
mic, trancriptomic and hormonal levels.
Glutathione is one of the most important compound in
the antioxidant pathway of plants and animals, where it
participates in the cellular redox signaling networks that
inuence growth, development and defense (Foyer and
Noctor 2005; Maughan and Foyer 2006). According to
Draganic and Lekic (2012), priming with solutions of
antioxidant substances like ascorbic acid, glutathione and
tocopherol increased the vigor of sunower seeds exposed
to low temperatures. The role of cysteine is not direct in
redox priming, but positively inuences GSH synthesis
(Barba-Esp n et al. 2012). In sorghum, seed priming with
cystiene reduced the injury caused by gamma radiation and
the effects of cysteine were most pronounced in primary
root elongation (Reddy and Smith 1978). In contrast,
L-cysteine did not protect the barley seeds against methyl
methanesulfonate (MMS) damage except for a slight pro-
tection at high doses (0.5, 0.7 %) (Rubluo 1982).
Chemical priming
Several chemicals were employed to bring about priming
in various crops. Plants can acquire resistance to abiotic
stress after treatment with several natural or synthetic
compounds such as butenolide, selenium, CuSO
4
, ZnSO
4
,
KH
2
PO
4
, ethanol, putrescine, paclobutrazol, choline, and
chitosan (Shao et al. 2005; Su et al. 2006; Foti et al. 2008;
Hasanuzzaman et al. 2010; Demir et al. 2012).
Butenolide
Butenolide, 3-methyl-2H-furo [2,3-c]pyran-2-one, has been
shown to improve seedling vigor of various crop species
and improves seedling emergence and growth in Capsicum
annum L. and Salvia L. (Demir et al. 2012). The butenolide
compound was isolated from plant-derived smoke and
burnt cellulose. The enhanced and more rapid seedling
emergence, as result of butenolide treatment, reduces the
possibility of pathogenic attack. It was also made clear that
treatment of seeds with smoke extract plays a role in pro-
tecting seed and seedlings against pathogens in the seed
bed (Kulkarni et al. 2006). Jain et al. (2006) reported the
advantages of butenolide treatment at lower temperatures
such as 10 and 15 C compared to optimum and high
temperatures in tomato seeds.
Selenium, CuSO
4
, ZnSO
4
, KH
2
PO
4
Selenium has been shown to exert a positive effect on crop
growth and stress tolerance at low concentrations (Hasa-
nuzzaman et al. 2010). Chen and Sung (2001) reported that
priming bitter gourd seeds with Se solution may partially
protect them against suboptimal temperature-induced oxi-
dative injury by coupling the changes in the reduced and
oxidized forms of antioxidants.
In Z. mays, seed priming with copper sulphate and zinc
sulphate signicantly increased the nal caryopses germi-
nation and increased seed emergence by 43 and 29 %,
respectively (Foti et al. 2008). Seed priming with KH
2
PO
4
had shown good potential to enhance germination, emer-
gence and plant growth of wheat (Das and Choudhury
1996; Ghana and Schillinger 2003; Korkmaz and Pill
2003). Priming treatment with 0.5 % K
2
HPO
4
and 0.5 %
KNO
3
gave better results as compared to higher concen-
trations of these chemicals (Sarwar et al. 2006). KH
2
PO
4
priming in Triticale cultivars increased germination per-
centage and seedling growth (Yagmur and Kaydan 2008).
Ethanol, putrescine, paclobutrazol
Priming rice seeds with 1 or 5 % ethanol solution resulted
in earlier and more uniform germination and higher leaf
score (Farooq et al. 2006b). Seed priming with putrescine
can improve the chilling tolerance in tobacco during seed
germination and seedling growth by the activation of
antioxidant system in the plant cells (Xu et al. 2011).
Another important chemical paclobutrazol has signicant
role in contributing salt stress tolerance of Catharanthus
roseus by improving the components of antioxidant
defense system (Jaleel et al. 2007). According to Shahrokhi
et al. (2011), paclobutrazol seed priming in F. arundinacea
L. (turf grass) affected growth and physiological traits of
plants during drought stress, but it related to concentration
of paclobutrazol and the nature of the cultivar.
Choline
Exogenous application of choline to seeds confers salt
tolerance in plants via accumulation of glycinebetaine
(Cha-um et al. 2006; Su et al. 2006). Glycinebetaine is
synthesized from choline in various plants via two-step
oxidation (Chen and Murata 2002; Sakamoto and Murata
2002). Moreover, choline has a vital role as the precursor
for phosphatidylcholine, a dominant constituent of mem-
brane phospholipids in eukaryotes (Rathinasabapathi
2000). Choline chloride priming of caryopses (in particular
Acta Physiol Plant (2013) 35:13811396 1387
1 3
5 mM) was found to enhance wheat salt tolerance (Salama
et al. 2011).
Chitosan
Chitosan is a large cationic polysaccharide mainly obtained
from waste materials from seafood processing. Chitosan
priming-induced resistance to certain diseases, increased
the energy of germination, germination percentage, lipase
activity, GA
3
and IAA levels and also improved the seed
quality of crops (Reddy et al. 1999; Zhou et al. 2002; Shao
et al. 2005). Chitosan treatment of wheat seeds induced
resistance to certain diseases and improved seed quality
(Reddy et al. 1999). Seed coated with chitosan was found
to accelerate seed germination and improve the tolerance to
stress condition of hybrid rice seedlings (Ruan and Xue
2002). Seed priming with two different acidic chitosan
solutions improved the vigor of maize seedlings (Shao
et al. 2005). Seed priming with chitosan also improved the
speed of germination of maize seed and thus benets the
seedling growth under low-temperature stress (Guan et al.
2009).
Priming with fungicides
Various fungicides are used in enhancing the biotic stress
tolerance of plants. But some fungicides are reported to
bring about a positive effect on germination and early
seedling vigor. Strobilurin formulations (strioxystrobin,
kresoxim-methyl, and azoxystrobin) when tested, exhibited
strong in vitro inhibition of the pathogen as well as an
increase of sunower seed germination and vigor and
moderate translaminar activity. These strobilurin fungi-
cides, apart from their action against sunower downy
mildew pathogen, are good plant growth promoters, which
is an added advantage for any practical agricultural system
(Sudisha et al. 2010). These strobilurins also proved to be
excellent in yield increase and quality of agricultural pro-
duce (Margot et al. 1998; Bartlett et al. 2002). The miti-
gative effects of triadimefon (5 mg l
-1
) through seed
priming on the germination, early seedling growth, pho-
tosynthetic pigments, non-enzymatic antioxidant contents
and activities of antioxidant enzymes were studied in salt
stressed (40 mM NaCl) Withania somnifera Dunal plants
by Jaleel et al. (2008).
In most studies fungicides are applied either by seed
dressing or seed soaking along with methylcellulose in
powder form (Ali et al. 2001). During pelleting the seeds
are tumbled with an adhesive material such as gum arabic
and carboxy methylcellulose (CMC) and fungicide powder
is mixed throughout the coating material or can be added in
discrete layers or in the outermost part of the pellet
(Agarwal and Sinclair 1997; Mohanan and Sharma 1991).
Solid matrix priming
In solid matrix priming (SMP) or matric conditioning, solid
or semi-solid medium is used as an alternative to liquid
medium (Copeland and McDonald 1995). This technique is
accomplished by mixing seeds with a solid or semi-solid
material and specied amount of water. SMP utilizes the
chemical and physical characteristics of a solid material to
restrict the water uptake of seeds. Unlike hydropriming,
SMP makes use of a small amount of liquid per unit of seed
and solid particles. During SMP, water is slowly provided
to the seeds and thus, slow or controlled imbibition occurs,
allowing repair mechanisms to operate. Commonly used
solid matrices include exfoliated vermiculite, expanded
calcined clay, Agro-lig, bituminous soft coal, sodium
polypropionate gel or synthetic calcium silicate (Kubik
et al. 1988). Locally available materials that are commonly
utilized as solid matrices are sawdust, charcoal and vol-
canic cinder (Lorenzo 1991).
Many studies on seed invigoration using liquid as
medium have been conducted, but only a few were done
using solid matrices. In the study of Lorenzo (1991) on
SMP using sawdust, ground charcoal and volcanic cinder,
soybean seeds responded favorably to shorter incubation
periods. The longer incubation periods and higher water
levels were harmful to the seeds because they encouraged
fungal growth. SMP was effective in invigorating seeds of
soybean through improvement in seed germination per-
centage (Mercado and Fernandez 2002). It was also found
that SMP treatment signicantly reduced the negative
effect of high temperature on celery seed germination
(Parera et al. 1993). According to Pandita et al. (2010),
SMP in combination with Trichoderma viride can be suc-
cessfully used to improve seedling emergence and pro-
ductivity of okra under low temperatures.
Biological priming/biopriming
Applying benecial microorganisms to the seed during
priming may further improve establishment of the crop,
particularly if seed-applied microorganisms subsequently
become established in the root zone of the plant and con-
tribute to longer-term plant health or plant growth pro-
motion (Bennett and Whipps 2008). Biopriming involves
coating seed with a bacterial biocontrol agent such as
Pseudomonas aureofaciens Kluyver AB254 and hydrating
for 20 h under warm conditions (23 C) in moist vermic-
ulite or on moist germination blotters in a self-sealing
1388 Acta Physiol Plant (2013) 35:13811396
1 3
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Acta Physiol Plant (2013) 35:13811396 1389
1 3
plastic bag and the seeds are removed before radicle
emergence (Callan et al. 1990). Dual application of bene-
cial microorganisms to carrot and onion seed during drum
priming was demonstrated by Bennett and Whipps (2008).
Rhizobacteria are used as inoculants to enhance crop yield
and for biological control of fungal pathogens. Certain
strains of rhizosphere bacteria stimulate plant growth and
are, therefore, called plant growth-promoting rhizobacteria
(PGPR) (Tonelli et al. 2011). In the roots of rice and
tomato plants, mycorrhizal fungi were shown to induce the
accumulation of a number of transcripts and proteins,
respectively, many of which with a predicted function in
plant defense (Sharmila et al. 2000; Guimil et al. 2005;
Pozo and Azcon-Aguilar 2007). In Cicer arietinum L.,
application of PGPR improves the percentage of seed
germination under saline conditions and also increased the
shoot length, root length and dry matter (Mishra et al.
2010). In wheat, seed biopriming with different salinity-
tolerant isolates of Trichoderma were effective in
improving germination percentage and reducing reduction
percentage of germination during salinity stress (Rawat
et al. 2011). Biopriming of sunower seeds with Pseudo-
monas uorescens UTPf76 and UTPf86 enhanced the
ability of seeds to invigorate and seedlings to grow uni-
formly (Moeinzadeh et al. 2010).
Merits and demerits of priming
According to Bradford (1986), priming treatment of seeds
has been shown to improve the germination and emergence
of many species and the seed-priming techniques have
been found effective for better germination and seedling
establishment under controlled conditions (Basra et al.
2005). On-farm seed priming with water is used in the
semi-arid agricultural land of India to grow maize, rice and
chickpeas. Direct benets to all three crops included faster
emergence, better stands and lower incidence of re-sowing,
more vigorous plants, better drought tolerance, earlier
owering, earlier harvest and higher grain yield (Harris
et al. 1999). Interestingly, priming repairs damage of aged
seeds (Bailly et al. 1998; Butler et al. 2009) or seeds
exposed to abiotic stresses such as salinity (Ehsanfar et al.
2006) and also improves the germination performance.
Among various strategies, pre-sowing treatment and
priming of seeds are easy, low-cost, with low-risk and
effective approaches to overcome the environmental stress
problems (Ashraf and Foolad 2005).
Altogether, disadvantages of seed priming should be
lower than advantages in comparison. There are very few
reports about the demerits of seed priming. Induced resis-
tance by priming was found to be benecial against dif-
ferent abiotic stresses, but a precautious state developing in
T
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1390 Acta Physiol Plant (2013) 35:13811396
1 3
the seed right before the germination may adversely affect
the seedling emergence vigor.
Summary
Over the past few years, seed priming has emerged as a
promising strategy in modern stress management because it
protects plants against various abiotic stresses without
heavily affecting tness. Moreover, seed priming offers a
smart, effective and realistic option for effective plant
protection. Drought, salinity, extreme temperatures and
oxidative stress are often interconnected, and may induce
similar damage. As a consequence, these diverse environ-
mental stresses often activate similar cell signaling path-
ways and cellular responses. It is known that seed priming
can activate these signaling pathways in the early stages of
growth and result in faster plant defense responses. The
exact molecular mechanism behind priming is not com-
pletely known, it is speculated that sensitization was
associated with accumulation of inactive signaling proteins
in primed cells. Upon subsequent exposure to abiotic
stresses, a second signaling event could hyperactive the
signaling proteins thereby amplifying signal transduction,
and thus leading to more rapid and/or more intense acti-
vation of defense responses (Conrath et al. 2006).
Besides the above, there are various other views put
forward by other authors on the mechanism behind prim-
ing. According to Nascimento and West (1998), the
increase in germination percentage/seed vigor of primed
seeds is due to reserve mobilization of food materials,
activation and resynthesis of some enzymes and also due to
the increased DNA and RNA synthesis. Priming is also
capable of repairing some of the damages due to seed
erosion which in turn results in increased vigor of primed
seeds (Arif et al. 2008). Seed priming affects the lag phase
of seed germination and thus causes early DNA replication
(Bray et al. 1989). It is desirable to design suitable seed-
priming methods for different crop plants to meet the
challenges of the environment. The current knowledge of
different seed-priming methods practiced in various crops
is summarized in the Table 1.
Author contribution The idea on the writing of this
review and its common structure and organization came
from Jos T. Puthur, who wrote the draft. K.C. Jisha wrote
the main text of the manuscript and collected the necessary
references. K. Vijayakumari supported with supplementary
data and in preparing the table. All authors have read and
approved the nal manuscript.
Acknowledgments J.T.P. would like to acknowledge the funding
received fromUniversity Grants Commission (India) (39-367/2010(SR)
and KSCSTE, Govt. of Kerala (India) (011/SRSLS/2010/CSTE).
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