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Vitamins for enhancing plant resistance

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Vitamins for enhancing plant resistance

Hatem Boubakri, Mahmoud Gargouri,

Ahmed Mliki, Faiçal Brini, Julie Chong
& Moez Jbara

Planta
An International Journal of Plant
Biology

ISSN 0032-0935

Planta
DOI 10.1007/s00425-016-2552-0

1 23
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 Author's personal copy
Planta
DOI 10.1007/s00425-016-2552-0

REVIEW

Vitamins for enhancing plant resistance

Hatem Boubakri1 • Mahmoud Gargouri2,3 • Ahmed Mliki3 • Faiçal Brini4 •

Julie Chong5 • Moez Jbara1

Received: 30 January 2016 / Accepted: 29 May 2016

Ó Springer-Verlag Berlin Heidelberg 2016

Abstract facets. However, other vitamins, such as ascorbic acid (AA,

Main conclusion This paper provides an overview on
vitamins with inducing activities in plants, the molecu-
lar and cellular mechanisms implicated, and the hor-
monal signalling-network regulating this process.
Moreover, it reports how vitamins might be part of the
molecular events linked to induced resistance by the
conventional elicitors.
Induced resistance (IR), exploiting the plant innate-defense
system is a sustainable strategy for plant disease control. In
the last decade, vitamins have been proven to act as
inducers of disease resistance, and these findings have
received an important attention owing to their safety and
cost effectiveness. Vitamins, including thiamine (TH,
vitamin B1), riboflavin (RF, vitamin B2), menadione
sodium bisulfite (MSB, vitamin K3), Para-aminobenzoic
acid (PABA, vitamin Bx), and folic acid (FA, vitamin B9)
provided an efficient protection against a wide range of
pathogens through the modulation of specific host-defense
& Hatem Boubakri
hatem.boubakri@cbbc.rnrt.tn
1
Laboratory of Leguminous, Centre of Biotechnology of Borj-
Cédria, 2050 Hammam-Lif, Tunisia
2
Institute of Biological Chemistry, Washington State
University, Pullman, WA 99164, USA
3
Laboratory of Plant Molecular Physiology, Centre of
Biotechnology of Borj-Cédria, 2050 Hammam-Lif, Tunisia
4
Laboratory of Biotechnology and Plant Improvement, Centre
of Biotechnology of Sfax, Route Sidi-Mansour, BP.1177,
3018 Sfax, Tunisia
5 invaders have first to face the preformed physical barriers
Laboratoire Vigne, Biotechnologies et Environnement
(LVBE, EA3991), Université de Haute Alsace, 33 rue de
Herrlisheim, 68000 Colmar, France
vitamin C) and tocopherols (vitamin E), have been shown
to be a part of the molecular mechanisms associated to IR.
The present review is the first to summarize what vitamins
are acting as inducers of disease resistance in plants and
how could they be modulated by the conventional elicitors.
Thus, this report provides an overview on the protective
abilities of vitamins and the molecular and cellular mech-
anisms underlying their activities. Moreover, it describes
the hormonal-signalling network regulating vitamin-signal
transduction during IR. Finally, a biochemical model
describing how vitamins are involved in the establishment
of IR process is discussed.
Keywords Elicitors  Hormones  Induced resistance 
Plants  Pathogens  Vitamins  Signalling pathways
Abbreviations
ET Ethylene
JA Jasmonic acid
IR Induced resistance
PR Pathogenesis-related protein
SA Salicylic acid
NPR1 Non-expressor of PR1
Introduction
Plants are continually exposed to a wide array of pathogen
invaders. To defend themselves, they have developed
sophisticated strategies and complex molecular mecha-
nisms (Eulgem 2005; Jones and Dangl 2006). Therefore,
in the leaf surface formed by the cuticle (Serrano et al.
2014). Apart from these pre-existing defense barriers,

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plants can activate structural and chemical defense barriers
after pathogen attack (Jones and Dangl 2006). In incom-
patible interactions, conserved microbial structures
(pathogen-associated molecular patterns, PAMPs) were
recognized by plants via transmembrane receptors (pattern
recognition receptors, PRRs), resulting in triggering intra-
cellular-defense mechanisms (Jones and Dangl 2006; Zip-
fel 2009). This process, known as PAMP-triggered
immunity (PTI), is manifested by extracellular alkaliniza-
tion, protein phosphorylation, defense gene up-regulation,
and the generation of reactive oxygen species (ROS).
These immune-defense facets are responsible for limiting
the growth of invading pathogen (Hann and Rathjen 2010).
However, adapted pathogens might inhibit or deactivate
PTI through the secretion of specific proteins (effectors),
resulting in successful infection, so-called effector-trig-
gered susceptibility (ETS) (Jones and Dangl 2006). In this
case, the control of pathogens is achieved by widespread
applications of chemicals (Komárek et al. 2010; Walters
et al. 2012). However, this practice is refused by wine-
makers and consumers, because of its serious risks on the
environment and on human health (Chen et al. 2007;
Komárek et al. 2010). These limitations have led to a quest
for environmentally safe alternatives to control plant dis-
eases. The use of elicitors of disease resistance is one of the
most recent and safe alternatives in controlling plant dis-
eases. This strategy relies on the manipulation of the nat-
ural host-defense repertoire known as ‘‘induced resistance’’
(IR) (Ryals et al. 1996; Walters et al. 2012; Boubakri et al.
2013a, b, c). IR is characterized by an increased manifes-
tation of plant innate-defense responses against different
pathogens provoked by the application of various external
factors and manifested either before pathogen attack
(elicitation) or after pathogen infection (Priming). The
activation of innate-defense responses during IR led to an
effective resistance against a wide range of intruders, such
as fungi, bacteria, viruses, and even insect herbivores
(Walters et al. 2012; Pieterse et al. 2013; Walters et al.
2013).
IR process is often regulated by a complex signal
transduction network (Garcia-Brugger et al. 2006; Pie-
terse et al. 2013). Two forms of IR have been described
in plants; the first is systemic-acquired resistance (SAR),
induced by chemical compounds and relies mainly on
SA defense-signalling pathway (Pieterse et al. 2013) and
the second form, induced systemic resistance (ISR),
refers to an enhanced state of resistance developed in
plants after colonization by beneficial soil-borne
microorganisms, such as plant growth promoting rhi-
zobacteria and mycorrhizal fungi (Van Wees et al.
2008). Evidence is accumulating that systemic resistance
induced by different beneficial microorganisms relies
on jasmonic acid (JA)-dependent and ethylene
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(ET)-dependent signalling pathways, and is associated
with priming phenomenon for an enhanced defense state
(Van Wees et al. 2008). Although the pathways are
different, both SAR and ISR require a functional NIM1/
NPR1 (Non-expressor of PR1) regulatory gene for
induction of defense gene expression (Delaney et al.
1995; Ryals et al. 1996). SA, JA, and ET are plant-
derived substances that induce unique types of resistance
when topically applied, as well as they could affect the
plant behavior under diverse environmental constraints
(Xie et al. 1998; Kunkel and Brooks 2002).
Although disease resistance inducers have been inten-
sively studied for potential agrochemical development,
several of them, such as DL-3-aminobutyric acid (BABA),
cyclodextrins (CD), methyl-jasmonate (MEJA), benzoth-
iadiazole (BTH), were shown to reduce plant growth (Heil
et al. 2000, 2001; van Hulten et al. 2006; Fürstenberg-Hägg
et al. 2013; Walters et al. 2013; Almagro et al. 2014;
Cipollini and Lieurance 2012; Cipollini and Heil 2010).
This undesirable side-effect has prevented exploitation of
these agents as crop defense activators, despite their
extraordinary effectiveness against a wide range of patho-
gens (Almagro et al. 2014; Walters et al. 2013; Cipollini
and Lieurance 2012; Cipollini and Heil 2010). This phe-
nomenon is known as ‘allocation fitness cost’ or ‘trade-off’
(Heil et al. 2001; Cipollini and Lieurance 2012), and shows
a reduced growth in elicitor-treaded plants, as they need
considerable energy amount for the establishment of IR
process. The molecular mechanisms behind this effect were
suggested to implicate an over-expression of phytotoxic
chemicals mainly phenol-containing compounds (Walters
et al. 2013; Reglinski et al. 2013). Moreover, several genes
known to be implicated in cell-wall modification and
microtubule-driven movement control were down-regu-
lated after treatments with CD and/or MEJ in grapevine-
cultured cells (Almagro et al. 2014). In addition, both CD
and MEJ strongly down-regulated translation-related tran-
scripts like a set of ribosomal proteins which led to the
arrest of the cell cycle. It seems that such behavior in the
elicited plants may contribute to energy saving (Almagro
et al. 2014). To overcome this pitfall, researchers have
attempted to identify compounds that induce resistance
without reducing plant growth in the field (Reglinski et al.
2013; Cipollini and Heil 2010; Boubakri et al. 2015). In
this context, some vitamins were identified to act as
inducers of disease resistance and have received an
important attention owing to their safety and cost effec-
tiveness (Cipollini and Heil 2010; Dong and Beer 2000;
Lyon 2007; Song et al. 2013). In fact, different vitamins
were shown to induce resistance against a wide range of
pathogens (fungus, bacteria and viruses) in arabidopsis,
rice, cucumber, tobacco, grapevine, and tomato (Dong and
Beer 2000; Dong 2001; Ahn et al. 2005; Saikia et al. 2006;
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Taheri and Tarighi 2010, 2011; Azami-Sardooei et al.
2010; Boubakri 2013; Boubakri et al. 2012, 2013a, b, c;
Liu et al. 2010).
The present review reports on the new role of vitamins
in IR in plants. In fact, some vitamins demonstrated
inducing activities when applied exogenously, including
thiamine (TH), riboflavin (RF), menadione sodium bisulfite
(MSB), Para-aminobenzoic acid (PABA), and folic acid
(FA), while others, such as ascorbic acid (AA) and toco-
pherols, were found to be a part of the molecular events
linked to IR process when elicited by the conventional
inducers. We also survey recent progress in deciphering the
immune regulatory role of vitamins with a special focus on
the differential hormonal signalling that govern vitamin-
triggered resistance responses based on recent reports,
mainly from studies using the model plant Arabidopsis
thaliana.
Protective abilities of vitamins
Riboflavin
Dong and Beer (2000) are the first reporting the inducing
activity of riboflavin in plants (Fig. 1). Thereafter, its role
in enhancing disease resistance has been described in other
plant species (Saikia et al. 2006; Taheri and Tarighi
2010, 2011; Boubakri et al. 2013a; Zhang et al. 2009) as
indicated in Table 1. Riboflavin was found to protect
Arabidopsis plants against Pseudomonas syringae pv.
tomato (Pst) and Peronospora parasitica, and tobacco
plants against Tobacco mosaic virus and Alternaria alter-
nata (Dong and Beer 2000; Zhang et al. 2009). Moreover,
Saikia et al. (2006) found that riboflavin is able to induce
resistance against Fusarium wilt and charcoal rot diseases
in Chickpea. Riboflavin treatment also enhanced resistance
to Phytophthora parasitica var. nicotianae and Ralstonia
solanacearum, the respective causal agents of black shank,
and Granville wilt, in tobacco seedlings (Liu et al. 2010).
The exogenous application of riboflavin offered resistance
against sheath blight in rice (Taheri and Hofte 2007). In
bean, riboflavin treatment reduced the number of spreading
lesions caused by Botrytis cinerea by approximately 25 %
compared to control plants (Azami-Sardooei et al. 2010).
Under the field conditions, riboflavin (2.5 mM) treatment
of Soybean seeds significantly reduced the percentage of
damping-off, root rot and/or charcoal rot severity, caused
by Macrophomina phaseolina in two consecutive seasons
compared with the control treatment (Abdel-Monaim
2011). The treatment of rice plants with riboflavin also
offered an efficient protection against Rhizoctonia solani
(Taheri and Tarighi 2010). More recently, Boubakri et al.
(2013a) reported the ability of riboflavin (2 mM) to protect
leaf discs of a susceptible grapevine cultivar (Pinot meu-
nier) against Plasmopara viticola, the causal agent of
downy mildew.
Thiamine
Thiamine (Fig. 1) is a potent antioxidant in vivo. In a
recent study, thiamine application protected paraquat-
treated Arabidopsis plants from oxidative stress (Tunc-
Ozdemir et al. 2009). This same study also showed that
exposure of Arabidopsis plants to various abiotic con-
straints, including paraquat, low temperatures, high light,
osmotic, and salt stress, induced an accumulation of

Fig. 1 Differential induction of

innate-defense facets during
vitamin-IR in plants. Thiamine
is able to activate almost all of
innate-defense mechanisms. RF
activates the majority of defense
facets except of HR. MSB and
PABA activate similar defense
responses (PR, ROS, and HR),
while FA induces mainly PR
proteins. The empty arrows in
triangle form, corresponding to
specific vitamins, mean the
absence of activation or
unavailability of data. TH
thiamine (red), RF riboflavin
(green), FA folic acid (pink),
PABA para-aminobenzoic acid
(dark), MSB menadione sodium
bisulfite (blue)

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Table 1 Induced resistance in plants by vitamins and their differential hormonal signalling
Vitamins Plant Pathogen SAa JAa ETa References

Riboflavin Arabidopsis Peronospora parasitica - - - Dong and Beer (2000, 2002)

Pseudomonas syringae Zhang et al. (2009)
Tobacco Alternaria alternate - ? - Zhang et al. (2009);
Tobacco mosaic virus Liu et al. (2010)
Phytophthora parasitica
Ralstonia solanacearum
Rice Rhizoctonia solani - ? Nd Taheri and Tarighi (2010)
Chikpea Fusarium wilt Nd Nd Nd Saikia et al. (2006)
Charcoal rot diseases
Bean Botrytis cinerea - ? Nd Azami-Sardooei et al. (2010)
Soybean Macrophomina phaseolina Nd Nd Nd Abdel-Monaim (2011)
Grapevine Plasmopara viticola Nd ? Nd Boubakri et al. (2013a, b, c)
Thiamine Rice Xanthomonas oryzae ? - Nd Ahn et al. (2005);
Sheath blight Bahuguna et al. (2012)
Cucumber Colletotrichum lagenarium Nd Nd Nd Ahn et al. (2005)
Sphaerotheca fuliginea
Arabidposis Pseudomonas syringae ? - - Ahn et al. (2005, 2007)
Tobacco Pepper mild mottle virus Ahn et al. (2005)
Soybean Macrophomina phaseolina Nd Nd Nd Abdel-Monaim (2011)
Barley Aphids - - - Hamada and Jonsson (2013)
Pea Aphids - - - Hamada and Jonsson (2013)
Grapevine Plasmopara viticola Nd ? Nd Boubakri et al. (2013a, b, c)
Menadione sodium Banana Fusarium oxysporum Nd Nd Nd Borges et al. (2003a, 2004)
bisulfite (MSB) Oilseed rape Leptosphaeria maculans Nd Nd Nd Borges et al. (2003b); Liu et al. (2006);
Arabidopsis Pseudomonas syringae ? ? Nd Borges et al. (2009)
Citrus Candidatus Liberibacter Nd Nd Nd Borges-Rodrı́guez and Borges-Pérez (2010)
Pearl millet Downy mildew Nd Nd Nd Pushpalatha et al. (2007)
Para-aminobenzoic Cucumber Cucumber mosaic virus (CMV) Nd Nd Nd Song et al. (2013)
acid (PABA) Xanthomonas axonopodis
Tobcco Pectobacterium carotovorum Nd Nd Nd Yang et al. (2011)
Folic acid Arabidopsis Pseudomonas syringae ? Nd Nd Wittek et al. (2015)
? activates, - does not activate, Nd not determined
a
SA, JA, and ET are figured as dependency (?) of the pathway, or not (-)

thiamine and its derivatives (thiamine pyrophosphate, TPP,
and thiamine monophosphate, TMP) compared with con-
trols (Tunc-Ozdemir et al. 2009).
Ahn et al. (2005) are the first reporting the ability of
thiamine to induce resistance in plants against a wide range
of pathogens (Table 1). In rice plants, thiamine treatment
enhanced resistance to Xanthomonas oryzae pv. oryzae, the
causal agent of leaf blight (Ahn et al. 2005). Moreover, it
provided important resistance levels to Pepper mild mottle
virus (PMMoV) in tobacco plants (Ahn et al. 2005). Ahn
et al. (2005) also reported the ability of thiamine to induce
resistance against anthracnose (Colletotrichum lagenar-
ium) and powdery mildew (Sphaerotheca fuliginea) in
cucumber plants (2005). In addition, thiamine treatment
provided important resistance levels in Arabidopsis against
Pseudomonas syringae pv. tomato (Ahn et al. 2005, 2007).
Under field conditions, thiamine treatment of Soybean
seeds significantly reduced the percentage of damping-off,
root rot and/or charcoal rot severity, caused by
Macrophomina phaseolina (Abdel-Monaim 2011). More
recently, thiamine has been shown to induce resistance
against sheath blight disease in rice (Bahuguna et al. 2012)
and against P. viticola in grapevine (Boubakri 2013;
Boubakri et al. 2012, 2013b). It was also found to alleviate
aphid infestations in barley and pea (Hamada and Jonsson
2013). In contrast to riboflavin, thiamine has been reported
to possess, besides of its inducing effect, a direct antifungal
activity against P. viticola, since the sporangia germination

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ability of the pathogen was partially reduced (43 % of
germinated sporangia) in vitro after incubation with a
30-mM thiamine solution (Boubakri et al. 2012).
Menadione sodium bisulfite
Recently, MSB (Fig. 1) has been reported to function as a
plant-defense activator against several pathogens
(Table 1). This vitamin was reported to protect banana
against Fusarium oxysporum f.sp. cubense (Borges et al.
2003b, 2004). MSB enhanced resistance, both locally and
systemically, to phoma stem canker disease caused by
Leptosphaeria maculans (West et al. 2001) in oilseed rape
plants (Borges et al. 2003a; Liu et al. 2006). In addition,
MSB treatment induced resistance against downy mildew
in pearl millet (Pushpalatha et al. 2007), and against the
virulent P. syringae pv. tomato DC3000 (Pst) in Ara-
bidopsis (Borges et al. 2009). Another notable effect of
MSB is its ability to induce a reduction in insect growth
(Borges et al. 2014). More recently, this vitamin has been
shown to protect citrus plants against both Triozaerytreae
and Diaphorinacitri (Borges et al. 2014).
Para-aminobenzoic acid
Para-aminobenzoic acid belongs to the vitamin B group
(Fig. 1). This vitamin is synthesized by plants, yeast, and
bacteria (Maki and Takeda 2000). The biosynthesis of folic
acid which also belongs to vitamin B group requires
PABA. In human, PABA is known for its role in activating
the synthesis of interferon that possesses an antiviral effect
(Akberova 2002).
PABA is known to control fungal pathogens in China
(Table 1), but the implicated mechanisms, such as a pos-
sible induction of host-defense responses, was not studied
(Kelman and Cook 1977). Recently, PABA was identified
to be capable of inducing SAR against bacterial and viral
diseases in pepper plants (Yang et al. 2011; Song et al.
2013). PABA is the only vitamin that was found to be able
to induce resistance against a viral disease caused by Cu-
cumber mosaic virus (CMV). Besides of its role in induc-
ing resistance to both Cucumber mosaic virus and
Xanthomonas axonopodis, PABA was found to enhance
pepper plant yield under field conditions in a simultaneous
manner (Song et al. 2013). In the same study, BTH which,
reduced disease progress, provoked a shortening of plant
shoots and also a reduction in fruit weight when compared
to both the PABA-treated samples and controls.
Folic acid
Recently, Wittek et al. (2015) were able to identify the
folate precursors 7,8-dihydropteroate (DHP) and 4-amino-
4-deoxychorismate (ADC) in A. thaliana. These authors
reported for the first time that both folic acid and the DHP
precursor 7,8-dihydroneopterin (DHN) were able to induce
resistance in Arabidopsis against P. syringae. Similar to
SA, folic acid application locally increased Arabidopsis
susceptibility to the necrotrophic fungus Alternaria
brassicicola.
Host-defenses and hormonal signalling
during vitamin-IR
Riboflavin
Riboflavin treatment was found to up-regulate multiple
facets of host-defense responses in several plant species, as
shown in Fig. 1 (Taheri and Hofte 2007; Taheri and Tar-
ighi 2011; Dong and Beer 2000; Boubakri et al. 2013a).
H2O2 induction has been reported to be necessary for
riboflavin-IR establishment in different plant-pathosystems
(Asai et al. 2010; Azami-Sardooei et al. 2010; Taheri and
Tarighi 2010, 2011). Riboflavin-IR to P. syringae pv.
tomato DC3000 (Pst) in Arabidopsis plants implicated a
rapid H2O2 accumulation as a key element in riboflavin
signal transduction (Zhang et al. 2009; Azami-Sardooei
et al. 2010). Moreover, riboflavin-IR in bean against
B. cinerea rely on H2O2-fueled defense responses (Azami-
Sardooei et al. 2010). More recently, Boubakri et al.
(2013a) reported that riboflavin-IR to P. viticola in
grapevine involved H2O2 accumulation.
On the other hand, an up-regulation of PR genes was
observed during riboflavin-IR in different pathosystems.
Riboflavin has been reported to induce PR gene expression
either through direct elicitation or through priming phe-
nomenon, where the pathogen infection is required for the
manifestation of amplified defense responses. Dong and
Beer (2000) have reported that riboflavin treatment of
Arabidopsis plants elicited the expression of defense-re-
lated genes, including the NPR1 gene, that is known to
regulate PR gene expression. Moreover, Liu et al. (2010)
reported that riboflavin addition to tobacco suspension
cultured cells elicited the expression of PR-1a, PR-1b, and
LPO (lipoxygenase) genes. However, this vitamin was also
found to induce resistance through priming phenomenon,
for example, in beans; it induced defense-related genes
only after B. cinerea invasion (Azami-Sardooei et al.
2010). More recently, Boubakri et al. (2013a) have repor-
ted that riboflavin application on grapevine leaf discs eli-
cited the expression of a battery of PR genes. Among them,
Glu, encodes for b-1,3-glucanase, known for its antifungal
effect through degradation of b-1,3-glucan that constitutes
fungal cell walls (Van Loon and Van Strien 1999) and
Chit1b, encodes chitinase Class I-b enzyme which is an
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antifungal protein responsible for the degradation of chitin
that constitute fungal cell walls (Van Loon and Van Strien
1999). In addition, riboflavin induced the expression of
PIN- and GST-encoding inhibitors of serine proteases and
Glutatione-S-transferase, respectively. PIN belongs to a
class of antifungal PR-6 proteins known for their strong
activity against a wide range of pathogens and GST
belongs to a phase II detoxification enzymes that have
peroxidase and isomerase activities, thereby, protecting
cells from elevated ROS content (Van Loon and Van Strien
1999).
Riboflavin-IR in plants also implicated callose deposi-
tion in stomata cells. The essential role of callose in plant
defense mechanisms is to act as a physical barrier against
intruders, but it can also hinder pathogen toxins enter into
plant cells (Zhou et al. 2013). Zhang et al. (2009) reported
that riboflavin-IR to P. syringae in Arabidopsis manifested
by a marked callose deposition. In addition, Boubakri et al.
(2013a) checked whether callose synthesis could be a part
of riboflavin-IR process to P. viticola in grapevine using a
pharmacological approach and found that a pre-treatment
with DDG (an inhibitor of callose synthase) reduced the
effectiveness of riboflavin to induce resistance by 64 %.
Collectively, these reports confirm the importance of cal-
lose formation in riboflavin-IR process.
Another cellular defense reaction that was reported to be
tightly linked to IR process is the cell death or hypersen-
sitive response (HR). Cell death is a highly regulated
process manifested by stereotypical morphological changes
of the cellular architecture involving cell shrinkage, cell
detachment, nuclear condensation, and DNA fragmentation
(Brauchle et al. 2014). Contrarily to several conventional
inducers, such as harpin (Dong et al. 1999), that induce cell
death as a main event for the establishment of IR process,
riboflavin-IR in all plant species did not involve cell-death
manifestation (Dong and Beer 2000; Zhang et al. 2009;
Azami-Sardooei et al. 2010; Taheri and Tarighi
2010, 2011; Boubakri et al. 2013a). This indicates that
riboflavin acts differentially compared to the conventional
inducers which might be due to a distinct signalling
network.
Several studies were achieved to decipher the hormonal-
signalling pathways regulating riboflavin-IR in plants.
Dong and Beer (2000) described that riboflavin-IR was not
influenced in the Arabidopsis mutant line NahG, which is
incapable to accumulate SA. This indicates that riboflavin-
IR does not rely on SA-signalling pathway (Fig. 2).
Moreover, riboflavin-IR to P. syringae was not affected in
the Arabidopsis mutant line jar1 (JA-insensitive), indicat-
ing that riboflavin signalling does not involve JA pathway
(Zhang et al. 2009). In addition, riboflavin-IR in Ara-
bidopsis was independent of ET- and ABA-signalling
pathways (Zhang et al. 2009). Collectively, these findings
confirm that riboflavin induces a non-specific disease
resistance by triggering a novel (non-hormonal) defense-
signalling pathway in Arabidopsis. However, contradictory
findings have been reported in rice plants, riboflavin lost
the ability to induce disease resistance when LOX (a

Fig. 2 Schematic
representation of defense-
signalling pathways regulating
vitamin-IR in the model plant A.
thaliana. TH and FA rely only
on SA-signalling pathway to
induce resistance. MSB-IR
seems to be regulated
simultaneously by SA- and JA-
signalling pathways, while
PABA-IR appears to be
regulated by both SA- and ET-
signalling pathways. Contrarily
to the other vitamins, a distinct
(non-hormonal) signalling
pathway is responsible for RF-
IR establishment, potentially
involving H2O2 which can
directly activate NPR1 leading
to defense response induction.
TH thiamine, FA folic acid,
PABA para-aminobenzoic acid,
MSB menadione sodium
bisulfite, RF riboflavin

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lipoxygenase responsible for JA biosynthesis) activity was
altered in mutant lines (Taheri and Tarighi 2010). Similar
results were also obtained in bean plants when studying
riboflavin-IR against B. cinerea, ETYA (an inhibitor of JA
biosynthesis) pre-treatment abolished the protective effect
of riboflavin (Azami-Sardooei et al. 2010). More recently,
Boubakri et al. (2013a), using a pharmacological approach,
deduced the implication of JA signalling in riboflavin-IR to
P. viticola in grapevine leaf discs. Therefore, it is clear that
riboflavin signal transduction might differ depending on
the plant species.
On the other hand, some reports suggested that ribo-
flavin can also play a role of mediator of plant defense
reactions during basal resistance. As known, the COR-
ONATINE INSENSITIVE1 (COI1) gene of A. thaliana
encodes an F-box protein implicated in assembling
SCFCOI1 complexes that are necessary for jasmonates (JAs)
perception and signalling. When investigating the molec-
ular basis of JA action, Xiao et al. (2004) identified a
coronatine insensitive 1 suppressor1 (cos1) mutant which
re-establish the coi1-related phenotypes, including alter-
ations in JA perception and defense reactions. Interest-
ingly, the COS1 gene was found to encode a lumazine
synthase, an enzyme implicated in riboflavin biosynthesis
(Xiao et al. 2004). Thus, these findings suggest a new role
for riboflavin that acts downstream of COI1 in the JA
defense-signalling pathway and is required for inhibiting
COI1-mediated plant defense responses (Xiao et al. 2004).
There are additional reports that support a mediator role for
riboflavin in plant basal resistance. For example, the find-
ings reported by Asai et al. (2010) describing that H2O2
and NO (nitric oxide) generation during plant responses to
invading pathogens required the biosynthesis of riboflavin
and its derivatives flavin mononucleotide (FMN) and flavin
adenine dinucleotide (FAD). Moreover, it was reported that
glycosylated forms of riboflavin, which are considered
unimportant in plant, may serve as a signal-storage com-
pound (Sierra and Vidal-Valverde 1999). This role
resembles that of glycosylated SA and calmodulins, which
function in the SA and Ca2? signalling, respectively.
Altogether, these findings suggest that riboflavin-IR relies
on a distinct hormonal-signalling network during IR pro-
cess compared with the conventional elicitors and, in
addition, this vitamin might be implicated in mediating
plant defense responses during basal resistance.
Thiamine
In a first report, Ahn et al. (2005) described that thiamine-
IR in Arabidopsis plants relies on the elicitation of the
innate-defense repertoire, but in a subsequent report, these
authors showed that thiamine activity relies on priming
phenomenon (Ahn et al. 2007). Thereafter, several reports
have described that thiamine can induce resistance in dif-
ferent pathosystems via direct elicitation of host-defenses
in the absence of any pathogen infection (Boubakri et al.
2012, 2013b). Thus, thiamine might act through elicitation
or priming of defense responses depending on the plant
species.
Several defense facets were shown to be associated to
thiamine-IR in plants (Fig. 1). In Arabidopsis, Ahn et al.
(2005) reported that thiamine primed H2O2 generation after
pathogen infection. Catalase pretreatment (a hydrogen
peroxide scavenger) entirely nullified host-defense reac-
tions induced by thiamine as well as the offered-resistance
to the virulent P. syringae (Ahn et al. 2005). Moreover, the
exogenous application of thiamine to a suspension cultured
cells of grapevine elicited the production of H2O2 in the
extracellular medium 1-h post-treatment (Boubakri et al.
2012). These findings suggest the involvement of H2O2 in
the regulation of the succeeding defense facets induced by
thiamine in plants.
On the other hand, thiamine application induced the
expression of several genes known to be implicated in
defense mechanisms. Boubakri et al. (2012) reported that
thiamine treatment of grapevine plants elicited the
expression of several PR genes, including, Glu, Chit4-C,
Chit-1b, PIN, and GST. Thiamine treatment also elicited
the expression of several PR genes in rice plants, such as
PR-1, PBZ1, and POX22.3 genes encoding PR protein 1,
PR-10, and peroxidase (PR-11), respectively (Ahn et al.
2005). These same genes were also up-regulated in
cucumber plants pre-treated with thiamine and inoculated
with anthracnose pathogen (Ahn et al. 2005). Moreover, in
Arabidopsis plants, thiamine application potentiated the
expression of PR-1 (Ahn et al. 2007). As mentioned above,
the products of these PR genes were shown to have
important antifungal activities (Sheehan et al. 2001).
Thiamine derivatives, TMP and TPP, were also found to
prime defense-related genes, such as PR1 gene, in rice
plants leading to an enhanced resistance to the causal
agents of rice blast and bacterial leaf blight diseases in a
similar way as thiamine but at a more lower dose (Ahn
et al. 2007). In contrast to riboflavin, thiamine was found to
induce HR-like cell death during IR process. Ahn et al.
(2005) described that thiamine-IR in Arabidopsis plants
against P. syringae was accompanied by the formation of
necrotic zones that correspond to HR-like cell death.
Boubakri et al. (2012) also reported that thiamine-IR to P.
viticola in grapevine plants involved cell-death establish-
ment. In addition, using epifluorescence microscopy, the
authors did not observe any mycelia structure growth in
and around these necrotic zones in inoculated and thi-
amine-treated leaves, providing evidence that cell death is
an important event during thiamine-triggered resistance in
plants.
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The induction of the plant secondary metabolites is
another facet of defense responses which found to be dif-
ferentially activated by riboflavin and thiamine treatments
in the same plant species. In fact, thiamine-IR to P. viticola
in grapevine implicated the biosynthesis of diverse sec-
ondary metabolites (Boubakri 2013; Boubakri et al.
2013b), while these compounds were not induced during
riboflavin-IR using the same pathosystem (Boubakri et al.
2013a). Therefore, thiamine treatment of grapevine plants
up-regulated phenylpropanoid pathway gene expression,
including PAL, encodes phenylalanine ammonialyase;
C4H, encodes cinnamate 4-hydroxylase; 4CL, encodes
4-coumarate CoA ligase; CHS, encodes chalcone synthase;
STS, encodes stilbene synthase; and finally, CCR, encodes
cinnamoyl-CoA reductase. The up-regulation of these
genes led to accumulation of flavonoids, lignin, phenolic
acids and stilbenes, such as both e- and d-viniferins and
pterostilbene, that never produced by plants under normal
conditions (Boubakri et al. 2013b). These authors observed
a concomitant presence of stilbenic compounds and
degraded-P. viticola mycelial structures in the intercellular
space of the leaf mesophyll of thiamine-treated samples,
indicating a possible involvement of these secondary
metabolites in thiamine-IR in grapevine.
Important research work was carried out to determine the
hormonal-signalling network, regulating the multiple facets
of innate-defense responses induced by thiamine. Using
different Arabidopsis mutant lines, Ahn et al. (2005) mon-
itored the expression of PR1 gene (a marker of SAR) after
thiamine treatment and found that PR-1 mRNA transcripts
were up-regulated in the wild-type Col-0; etr1 (defected in
ET perception); and jar1 (insensitive to JA). Contrastingly,
PR-1 mRNA transcripts were not up-regulated in nahG, an
Arabidopsis mutant line where SA levels are down-regu-
lated, or npr1, and a mutant that does not accumulate PR-1
in response to SA (Ahn et al. 2005). Moreover, thiamine
fails to protect nahG and npr1 Arabidopsis mutant lines
from bacterial infection, while it offered protective levels
similar to the wild-type Col-0 in the case of etr1 and jar1
mutant lines (Ahn et al. 2005). Altogether, these findings
indicate that the induction of defense reactions by thiamine
is independent of JA and ET signalling, but relies on SA
defense-signalling pathway (Fig. 2).
Several signal transduction modules known to be
involved in plant-defense mechanisms, including flux of
Ca2? and up-regulation of protein kinase C-like activity,
were modulated by thiamine. These modules known to be
key regulators of NADPH oxidase (NOX) during plant
response to various constraints (Jiang et al. 2011). Simi-
larly, Zhou et al. (2013) reported that thiamine could
reverse the initial reducing status through up-regulation of
NADPH oxidase-mediated ROS signalling to perturb the
disease progress of Sclerotinia. Collectively, these findings
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might highlight a mediator role for ROS during thiamine-
IR process in plants. Thus, further experiments are needed
to confirm this possible mediator role for ROS, determine
what ROS forms are implicated and decipher the mecha-
nisms by which ROS can be operative in thiamine-trig-
gered plant immune responses.
Menadione sodium bisulfite
The redox properties of MSB insured by the presence of a
double quinone functional group provided it important
physiological roles in plants (Lehmann et al. 2012). More-
over, given its hydrophobic nature, MSB can easily enter
into organelles through biological membranes of plant cells,
and catalyze ROS generation (Lehmann 2009).
Liu et al. (2006) have reported that MSB treatment of
Brassica napus plants caused the formation of necrotic
zones in mesophyll cells at 24 h after inoculation with L.
maculans. In contrast, no visible host reaction was
detectable in water pre-treated control plants. However,
staining assays of MSB-treated Arabidopsis plants did not
reveal ROS accumulation in plants, despite the fact data
generated from a microarray transcriptomic analysis
showed a positive regulation of genes implicated in the
ROS detoxification mechanisms (Borges et al. 2014). Such
findings could be explained by the fact that MSB-IR in
Arabidopsis relies on priming phenomenon (Beckers and
Conrath 2007). Expression change analysis revealed a
unique molecular mark triggered by 0.2-mM MSB treat-
ment in Arabidopsis plants, manifested by up-regulating
differentially 158 genes implicated in ‘‘response to stress’’
categories (Borges et al. 2009). Among the represented
roles of the induced genes, there are cytochrome P450s,
transcription factors (putative regulators of the G-box), and
glutathione S-transferases (Borges et al. 2009). Further-
more, studies using the western blot technique demon-
strated that MSB does not itself activate PR1 protein
expression in Arabidopsis (Dong 2001). Contrastingly,
3 days after inoculation with P. syringae, MSB-pretreated
plants exhibited an enhanced expression of PR1 protein
compared to mock plants (Borges et al. 2009). Collectively,
these findings suggest that MSB acts through priming of
specific sets of the plant innate-defense repertoire (Fig. 1),
and induces a unique molecular footprint. This behavior
might be due to specific-signalling events that took place
during MSB-IR.
MSB is the most recent inducer of disease resistance
discovered among the vitamins showing inducing activities
in plants. Thus, the hormonal-signalling network regulating
MSB-IR process is still largely unknown (Fig. 2). How-
ever, recent data based on transcriptomic analysis gave
some ideas on the different signalling pathways implicated
in this process. Microarray analysis revealed that MSB
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treatment up-regulates the expression of a gene encoding a
GRX480 protein, a member of the glutaredoxin family that
regulates protein redox state (Ndamukong et al. 2007).
GRX480 is known to interact with TGA factors, sup-
pressing JA-responsive PDF1.2 transcription. Moreover,
GRX480 transcription could be induced by SA- and
requires NPR1 and may be involved in SA/JA cross-talk
(Ndamukong et al. 2007). MSB also induced the expression
of several transcription factors (TF) that moderate plant
defense responses, mainly genes encoding C2H2 and
C3HC4-type zinc finger proteins. C2H2-type TF is known to
be implicated in osmotic stress tolerance similar to the
DREB2A transcriptional activator and a JA-inducible
transcription factor (Wang et al. 2008). The other set of
defense-related TF up-regulated by MSB involved ethylene
responsive element-binding proteins. On the other hand,
McGrath et al. (2005) reported that members of this TF
family, such as TDR1 and ATERF-1 genes, were inducible
by MEJA treatment as well as A. brassicicola inoculation.
Altogether, it seems that MSB signal transduction might
involve both JA- and SA-signalling pathways. As MSB
also induced genes coding for calcium-transport ATPase
and calmodulin which are calcium ion-binding proteins
(Reddy 2001), Ca2? might play a role of second messenger
at the earlier signalling events associated to MSB-IR.
Future work is needed to decipher the whole hormonal-
signalling network regulating MSB-IR in plants and con-
firm whether calcium is implicated in the diverse signalling
events linked to this process.
Para-aminobenzoic acid
Song et al. (2013) reported that PABA acts mainly through
priming of host-defense responses (Fig. 1). In pepper, the
exogenous application of PABA was found to prime the
expression of the SA marker genes, CaPR9 and CaPR4
(Yang et al. 2011). After 6-h post-inoculation, the expres-
sion of other defense genes, such as CaPIN2 (protease
inhibitor 2) at 20 day post-treatment and CaTIN1 (TMV-
induced Clone 1) at 30 dpt, was down-regulated by PABA
treatment, indicating the occurrence of cross-talking
between defense signalling (Yang et al. 2011). It seems that
systemic defense signalling induced by PABA mainly
involves SA pathway (Fig. 2). However, future work is
needed to explore more protective abilities of PABA,
determine the molecular and cellular defense mechanisms
implicated, and decipher the signalling network regulating
PABA-IR in plants.
Folic acid
Recently, Wittek et al. (2015) reported that folic acid
application activated the expression of the SA marker
gene PR1 in Arabidopsis leaves (Fig. 1). However, folic
acid has also been reported to be modulated by the con-
ventional elicitors. For example, the supplementation of
plant growth regulators (6-benzylaminopurine, kinetin, and
ABA) to a Coriandrum sativum callus cultures induced an
increase in folate content (Puthusseri et al. 2012). The same
authors also reported that the addition of MEJA or SA-
increased folate content in C. sativum cell cultures. When
elicitor treatments were done on whole plants, SA induced
an increase in the folate content by two-folds, although the
amount varied with diurnal rhythms (Puthusseri et al.
2012).
The findings of Wittek et al. (2015) described that 7,8-
dihydroneopterin- and folic acid-induced systemic resis-
tance depend on SA-signalling pathway. The same authors
also reported that FA treatment of Arabidopsis plants
simultaneously induced local and systemic resistance
to P. syringae and increased susceptibility to A. brassici-
cola, suggesting the occurrence of a crosstalk between the
different signalling pathways regulating plant innate-im-
munity (Wittek et al. 2015). Regarding the very few reports
on the role of folate in inducing disease resistance in plants,
it is difficult to say whether folic acid could act as an
inducer of disease resistance in plants and/or might be a
part of the molecular mechanisms linked to IR elicited by
the conventional inducers. Clearly, there are still important
ambiguities which require clarification on the role of folic
acid in both basal resistance and induced resistance in
plants.
Vitamins as part of the molecular events linked to IR
Besides their role as inducers of disease resistance in
plants, some vitamins [ascorbic acid (vitamin C) and
tocopherols (vitamin E)] are modulated by the conven-
tional elicitors of disease resistance (Wolucka et al. 2005;
Khan et al. 2012).
Ascorbic acid
AA is the most abundant and ubiquitous cellular antioxi-
dant (Khan et al. 2012; Turner et al. 2002). It is present in
plants, animals, and single-cell organisms. Some fungi can
synthesize erythroascorbic acid, a vitamin-C analogue with
similar biological functions (Khan et al. 2012). In addition,
blue green algae have been reported to have a small content
of AA (Arrigoni and De Tullio 2002). Given its ability to
neutralize ROS in plant cells, AA is considered as a major
antioxidant compound among the plant antioxidant-defense
system. To control the amount of H2O2 within the cell, it
acts in coordination with glutathione (GSH) and enzymatic
antioxidants in the ascorbate–glutathione cycle (Asensi-
Fabado and Munne-Bosch 2010). As an antioxidant,
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ascorbate (ASC) acts either as a direct scavenger of ROS,
or indirectly, as a substrate for a highly specific ascorbate
peroxidase (APX) in the neutralization of H2O2 as follows:
2 ascorbate þ H2 O2 ! 2 monodehydroascorbate
þ 2H2 O
APX is an important H2O2-scavenging enzyme and its
isoforms are present in several compartments of the plant
cell (Jimenez et al. 1997). Several environmental con-
straints that result in the accumulation of ROS induced the
APX expression. As indicated in Fig. 3, monodehy-
droascorbate (MDHA) derived from ASC oxidation might
either reacts spontaneously with itself to undergo dispro-
portionation into dehydroascorbate (DHA) and ASC, or
pursues a direct reduction to ASC by the dehydroascorbate
reductase (DHAR) (Maksymiec and Krupa 2002).
The role of AA in the IR process has been investigated
using elicitors known for their inducing activities in vari-
ous plant species, such as JA and its methyl ester (methyl-
jasmonate, MEJA). Both JA and MEJA are known to be
Fig. 3 Proposed model of the vitamin modulation during IR process.
JA, MEJA, and BABA provoked AA biosynthesis by enhancing the
transcription of VTC1 gene. Catabolism of AA led to OA synthesis
and released ASC. OA can be transformed into H2O2 by OX. H2O2
generation induced redox balance change of in the GSH pool which
can easily shift to its oxidized form, GSSG. Such change activated
NPR1, the regulatory protein of PR. The released ASC is transformed
to MDHA by APX, which either reacts spontaneously with itself to
undergo disproportionation into ASC and DHA, or pursues a direct
reduction to ASC by the DHAR, thereby affecting the cellular thiol-
disulfide redox balance, including the GSH/GSSG couple, which is
implicated in regulating PR synthesis through NPR1 activation.
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potent elicitors of innate-defense responses in several plant
species (Turner et al. 2002; Belhadj et al. 2006; Almagro
et al. 2014). In addition, jasmonate-signalling results in a
transcriptional reprogramming leading to an enhanced
resistance against pathogens (Almagro et al. 2014; Turner
et al. 2002). It was reported that treatment of N. tabacum
and A. thaliana suspension cells with MEJA stimulated the
de novo biosynthesis of AA (Wolucka et al. 2005). On the
basis of transcript profiling data, it was found that this AA
accumulation in tobacco cells was accompanied with an
important induction of VTC1 gene encoding a GDP-man-
nose pyrophosphorylase, a key enzyme in AA biosynthesis
pathway (Wolucka et al. 2005). In addition, upon infection
with Plectosphaerella cucumerina, BABA primes VTC1
expression in Arabidopsis, while APX1 transcription was
inhibited (Pastor et al. 2013). This might engender a more
oxidized environment in the cell and allow increased ROS
accumulation (Pastor et al. 2013). In BABA-treated plants,
the level of mRNA transcripts of VTC1 gene was enhanced,
but not that of GSH1 gene. This transcriptomic regulation
Dashed pathway consists on the elicitation of tocopherol biosynthesis
by JA and MEJA through enhanced transcription of HPPD and HPT
genes and the importance of these tocopherols in mediating cellular
responses by interacting with a specific transcription factor. Circles
respresent genes and rectangles are used for metabolites. JA jasmonic
acid, MEJ methyl-jasmonate, BABA b-aminobutyric acid, AA ascorbic
acid, VTC1 GDP-mannose pyrophosphorylase 1, OA oxalic acid, OX
oxidase, ASC ascorbate, GSH reduced glutathione, GSSG oxidized
glutathione, MDHA monodehydroascorbate, APX ascorbate peroxi-
dase, DHA dehydroascorbate, DHAR dehydroascorbate reductase,
HPPD p-hydroxyphenyl pyruvate dioxygenase, HPT homogentisate
phytyltransferase, Tocopheryl-P tocopheryl-phosaphate
 Author's personal copy
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would allow for an oxidized state of the cytoplasm insured
by the augmented H2O2 accumulation which is confirmed
by the lower levels of GSH/GSSG in BABA-treated plants
following P. cucumerina inoculation (Pastor et al. 2013).
On the other hand, AA is known to be a main precursor
of oxalic acid (OA) which contributes in the synthesis of
H2O2 in plant-pathogen interaction and plays an important
role in reducing pathogen growth (Dias et al. 2011; Khan
et al. 2012; Bala and Thukral 2011). Increased amount of
H2O2 might influence the redox status in the GSH pool and
can easily shift to its oxidized form, GSSG (Pavet et al.
2005). GSH/GSSG couple is well suited to the role of
redox sensor seen that it is an indicator of the general
cellular thiol-disulfide redox balance (Pavet et al. 2005).
Cytosolic thiol-disulfide status has been shown to be
important in regulating PR gene expression through NPR1
pathway (Mou et al. 2003). Given the sensitivity of the
NPR1 regulatory gene to changes in cellular redox status,
abiotic or biotic stresses that disturb cellular redox balance
might induce PR gene expression via the NPR1 pathway
(Mou et al. 2003). This process might explain, for example,
the activation of PR genes in plants after exposure to UV-B
(Green and Fluhr 1995) or in mutants that showed defects
in catalase activity (Chamnongpol et al. 1996). The NPR1
regulatory gene was found to convert from an inactive
oligomer to an active monomer due to changes in the redox
status of the cell environment triggered by SA treatment,
an inducer of SAR in plants (Mou et al. 2003). It was
reported that the active form of NPR1 crosses the nuclear
membrane and activates the expression of PR genes (De-
spres et al. 2003). Collectively, it seems that the increase of
AA amounts provoked by the activators of disease resis-
tance might induce changes in the redox balance of the cell
environment, thereby, stimulating PR gene expression via
NPR1 gene activation, as shown in our proposed model
(Fig. 3).
The efficiency of SAR establishment and pathogen
resistance was studied in two AA-deficient Arabidopsis
mutants, vtc1 and vtc2 (Pavet et al. 2005). The vtc1-1
mutant contains a point mutation in VTC1, resulting in a
70 % lower AA amount as compared to that of the wild-
type (Conklin et al. 1999). A point mutation in the vtc2-1
mutant leading to 70–80 % lower AA levels in comparison
with the wild-type (Conklin et al. 2000). These changes are
accompanied by an enhanced resistance to P. syringae pv.
maculicola ES4326 and to the oomycete Hyaloper-
onospora parasictica pv. Noco. in both vtc1-1 and vtc2-1
mutant lines (Pavet et al. 2005; Barth et al. 2004). The
enhanced state of resistance was correlated with an up-
regulation of PR genes, including PR1 and PR5, increased
levels of SA, and premature senescence (Barth et al. 2004).
This supports previous findings describing that AA defi-
ciency led to the expression of PR genes in an SA-
dependant manner and the premature senescence positively
contributed to this offered-resistance (Kus et al. 2002).
Moreover, the findings by Pavet et al. (2005) led to the
conclusion that AA-deficiency-induced PR gene expression
through an enhanced glutathione accumulation and higher
redox levels (more glutathione reduced than oxidized). The
authors, however, suggested that H2O2-signalling pathway
and SA-signalling pathway are not implicated in this pro-
cess. In contrast, the findings of Mukherjee et al. (2010)
described that the enhanced resistance to P. syringae in the
AA-deficient A. thaliana vtc1-1 mutant correlates with
elevated levels of SA, which induced PR proteins. The
authors suggested that AA deficiency causes constitutive
priming via a buildup of H2O2 that stimulates SA accu-
mulation, leading to an increased disease resistance. On the
other hand, Botanga et al. (2012) have reported that the
Arabidopsis vtc1 and vtc2 mutants were revealed more
sensitive to the pathogenic ascomycete A. brassicicola.
These authors also described that ASC levels declined after
A. brassicicola inoculation, whereas DHA levels increased,
which led to a shift of the redox balance between these
compounds towards oxidation.
As known, plant responses to stress are governed by a
complex-signalling network, involving ET, JA, SA, ABA,
and gibberellic acid (GA3). Molecular and genetic studies
suggest the concept that the cross talk between AA and
plant hormones implicates alteration in the expression of
hormone biosynthetic genes (Fujita et al. 2006; Khan et al.
2012). Clearly, the role of AA in the context of plant–
microbe interaction remains unclear and sometimes con-
troversial; therefore, future work is needed for a better
understanding of the role of this vitamin in both basal
resistance and induced resistance against microbial patho-
gens in plants.
Tocopherols
Tocopherols, collectively known as vitamin E, are lipo-
philic antioxidants, exclusively synthesized by photosyn-
thetic organisms. Of the four forms (a, b, c, and d), a-
tocopherol is the most produced form of vitamin E in plant
tissues, and has the highest vitamin E activity (Caretto
et al. 2010). Functionally, tocopherols and tocotrienols
have the ability to directly quench ROS or indirectly ter-
minate lipid peroxidation chain reaction by eliminating
polyunsaturated fatty acid radical species (Caretto et al.
2010). More recently, they were shown to participate in
intracellular signalling mechanisms in mammals and, in
plants (Azzi et al. 2004; Caretto et al. 2010; Asensi-Fabado
and Munne-Bosch 2010; Munne-Bosch et al. 2007).
Two inducers of disease resistance in plants (JA and
MEJA) were found to modulate the endogenous level of
tocopherol in plants (Gala et al. 2005; Antognoni et al.
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2009). In fact, a marked accumulation of a-tocopherol was
observed, in sunflower and Arabidopsis cell cultures, after
a treatment with 5-mM JA (Gala et al. 2005). The authors
reported that such enhancement of tocopherol production
was due to the ability of JA to up-regulate genes implicated
in the tocopherol-biosynthetic pathway (Fig. 3), including,
p-hydroxyphenyl pyruvate dioxygenase (HPPD) and
homogentisate phytyltransferase (HPT) genes (Caretto
et al. 2010). Moreover, in Amaranthus caudatus cultures,
treatment with MEJA enhanced the production of a-toco-
pherol up to five-fold, and the inductive effect was affected
by the hormonal composition of the medium (Antognoni
et al. 2009). Using A. thaliana mutant lines showing
defects in tocopherol biosynthesis (vte1), it was found that
tocopherol deficiency may affect endogenous phytohor-
mone levels in plants (Munne-Bosch et al. 2007). In fact,
these authors described that the limited growth of toco-
pherol-deficient lines correlated with increases in JA con-
tents. Other studies revealed the relationship of tocopherol
content with other antioxidants, like AA and GSH. In fact,
it was reported that the amount of tocopherol is negatively
correlated with the amount of AA and GSH. However, in
some cases, such as sunflower cell lines, the lines with high
level of tocopherols had higher content of AA and GSH
(Caretto et al. 2010).
A number of lines of evidence, molecular, biochemical,
and functional suggested that the natural function of a-
tocopherol is cell signalling. Recent experiments revealed
that a-tocopherol, but not other antioxidants, is the pre-
cursor of a-tocopheryl phosphate which is a more active
form of vitamin E. In fact, a-tocopheryl phosphate was
found to specifically interact with a receptor or transcrip-
tion factor and modulates cell functions (Negis et al. 2006).
As suggested in our proposed model (Fig. 3), tocopherol
accumulation provoked by inducers of disease resistance
might be implicated in specific-signalling mechanisms that
contribute in the modulation of cell functions. These
findings would open the door to future work that aims for a
better understand of role of tocopherols during both basal
resistance and induced resistance in plants.
Conclusion
IR is an attractive strategy for plant disease control, as it
appears to be safer for the environment than the use of
chemical pesticides. The main objective of research on IR
is its use to manage plant diseases under field conditions
without affecting plant growth. However, several conven-
tional elicitors, despite of their extraordinary effectiveness,
reduced plant growth when exogenously applied by a
mechanism referred to as ‘allocation fitness cost’. Vitamins
with inducing activities did not show any toxic effects on
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the plant (Song et al. 2013). Several reports have shown
that vitamin can improve plant growth when applied
exogenously (Pushpalatha et al. 2007). For example, the
fruit yield was increased in PABA-treated pepper plants
under field conditions (Song et al. 2013). Moreover,
Pushpalatha et al. (2007) have reported a positive impact of
some vitamins, such as thiamine, riboflavin, and MSB, on
pearl millet plant grown under the greenhouse conditions.
This behavior might be due to a distinct transduction-sig-
nalling network regulating vitamin-IR. Nevertheless, vita-
mins like other elicitors exert their effect by the induction
of a complex metabolic network of cross-talk and feedback
mechanisms. Therefore, vitamin-IR might be influenced by
diverse environmental factors. Thus, for successful use of
vitamins in agriculture, it is important to understand their
effects not only on plant defense, but also on other aspects
of plant development and environmental responses.
Apart from their biological role in vivo, vitamins with
inducing activities could be used as model system for the
study of important events linked to perception and trans-
duction of external signals to activate host-defense
responses. The findings provided by such studies may lead
to very practical means for developing new environmen-
tally safe formulations for plant disease management.
Moreover, the fact that some vitamins, such as tocopherols
and AA, are important components of IR by the conven-
tional elicitors; this would open the door for future work on
developing metabolic-engineered crops over-expressing
specific vitamin biosynthetic genes. Finally, we believe
that it is very interesting to investigate the efficiency of the
integration of vitamin-IR in a disease management pro-
gram in conjunction with other control strategies.
Author contribution statement All authors jointly wrote
the manuscript.
Acknowledgments The author thanks the Ministry of Higher Edu-
cation and Scientific Research of Tunisia for the support.
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