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Systemic Acquired Resistance (Fifty Years after Discovery): Moving from the
Lab to the Field.
Franco Faoro
Department of Agricultural and Environmental Sciences, University of Milan
Via Celoria, 2 20133 Milano, Italy E-mail: [email protected]
Introduction
Plants possess an innate immune system consisting of an array of either physical and chemical
constitutive and inducible defenses, the latter being activated following pathogen sensing. As a result,
host pattern recognition receptors (PRR), similar to drosophila toll and mammalian toll-like receptors
(TLRs), may recognize pathogen- or microbe-associated molecular patterns (PAMPs or MAMPs) or
pathogen specific effectors (Avr) activating PAMP-triggered immunity (PTI) or effector –triggered
immunity (ETI), respectively. Whatever the recognition type, it may trigger a hypersensitive response
(HR), that is the rapid and programmed cell death at the sites of the attempted pathogen invasion, in
order to impair pathogen spreading. Furthermore, pathogen recognition establishes a state of
immunity in plant tissues nearby the infection site (local acquired resistance, LAR) and very often
also in distal organs, the so called systemic acquired resistance (SAR). The first demonstration of
LAR and SAR phenomena was given by Ros (1961, Virology,14, 340-358) at the beginning of
sixties by inoculating tobacco plants with an HR-inducing tobacco mosaic virus strain. After that
original demonstration, SAR has been comprehensively investigated by a huge number of studies,
covering phytopathological, chemical and biochemical, genetical and genomic, molecular and
agronomic sciences. These studies have contributively assembled and continue to reveal an
impressive volume of facts and information, including a successfully potential way of exploiting
SAR in crop protection.
Induced resistance pathways
The number of facts emerged in the last decades has shown that SAR is just one of the players in a
multifaceted defense system inducible in plants according to distinct pathways, characterized by
different signals, metabolites and genes. SAR is then defined the process depending on the primary
signal salicylic acid (SA) and involving the transduction protein NPR1 to develop a defence
response. A second process, called ISR, is induced by symbionts and orchestrates a pathway
depending on other hormons, such as jasmonate and ethylene (JA/ET). A third mechanism of
defense, the so called beta-aminobutyric acid-induced resistance (BABA-IR) has been emerging in
the last decade by discovering that BABA exogenous application can activate a multiple immune
response by potentiating SA-inducible defenses and priming for pathogen-induced callose deposition,
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independently of SA and JA, but requiring intact biosynthesis and perception of abscisic acid (ABA).
These mechanisms are interconnected and contribute to create a network of defenses controlled by
the plant’s innate immune system that may, more properly, be included in the generic term of
induced resistance (IR), of which SAR represents the best known process involved in response to
pathogen challenges.
SAR long distance signals
Although more than fifty years have already been over since SAR discovery, the long distance
signals responsible for systemization of acquired resistance are far from being fully understood.
Recently, analysis of metabolites isolated from petiole exudates (PEXs) of pathogen-inoculated
leaves have identified several diverse signals. Among them, the most frequently found were: 1)
methyl salicylate (MeSA) which is able to release SA in distal leaves by virtue of a SA-inhibitable
methyl esterase and it is also an aerial signal for resistance priming in the neighboring plants; 2)
dehydroabietinal (DA) an abietane diterpenoid which is active at picograms concentration; 3) azelaic
acid (AZA), a nonandioic acid first isolated from petiole exudates of bacterially infected leaves of
Arabidopsis; 4) the AZA analogous pimelic acid (PIM); 5) pipecolic acid (Pip), a Lysine catabolite
that accumulates in distal, non-inoculated leaves, just preceding that of SA at the onset of SAR. Pip
also modulates BABA-IR resistance against bacterial pathogen infection and orchestrates an
amplification of resistance, with positive regulation of SA biosynthesis and priming for SAR
induction.
SAR exogenous elicitors
One of the most interesting findings of the last two decades is the array of both natural and synthetic
compounds mimicking endogenous molecular signals, or acting as PAMPs, thus able to elicit plant
defense response. These exogenous signals, also known as plant activators, or SAR inducers, deserve
particular interest in agriculture, because of their long lasting ability to protect crops against a broad
spectrum of pathogens at low environmental impact. The action mechanism of these molecules can
be different, because of the diverse signal transduction pathways elicited at the onset of SAR.
Among the several exogenous inducers the most known are: BTH (benzothiadiazole synon.:
acibenzolar-S-methyl, trade name Actigard/Bion), BABA (β-Aminobutyric acid),
Chitosan (a
deacetylated chitin derivative), Laminarin (a linear β-1,3 glucan from the marine brown alga
Laminaria digitata), Saccharin (Ortho-sulphobenzamide, a well-known sweetener), Silicon, Vitamins
(B1, thiamine, B2, riboflavin, and K3, menadione).
BTH and chitosan are possibly the most widely used and we have been studying their action
mechanisms for many years. Both compounds activate LAR and SAR, via an oxidative burst due to
H2O2 accumulation. However in BTH-treated leaves, H2O2 is uniformly localized on epidermal cell
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wall at a sub-lethal level, without stimulating a cell death program, while in chitosan sprayed plants
it accumulates in a few mesophyll cells, causing them to die and generating a network of microlesions mimicking an HR-inducing pathogen infection.
It must be mentioned that, besides the above resistance activators, also some conventional
agrochemicals are able to elicit defense mechanisms. In particular, the fungicides Probenazole
(Oryzemate), Pyraclostrobin and Phosphonates (Phosphites) and the insecticide Imidacloprid are
possibly the most active and represent a valid integration to the use of resistance activators for a
better control of pests and diseases at a lower environmental impact.
Fitness cost of SAR and priming for defense
One of the main criticisms regarding induced resistance is the fitness cost associated with SAR, as it
requires significant consumption of resources by the plant in terms of new expressed genes, proteins
and metabolic pathways also in absence of pathogens. All results so far reported show that fitness
costs may depend by several, not always evident, factors, including nature of the chemical inducer,
dose applied, species and variety of plant, pathosystem, crop conditions, and so on. This problem can
be often overcome by using elicitor type/concentration that does not directly activated defense
mechanisms but only primes them for a rapid and strong activation only upon pathogen challenge.
Priming can be often obtained by seed treatments instead of spraying plants.
The mechanism o priming is still far from being fully understood, certainly is a sort of pretranscriptional state of genes codifying defense metabolites, such as those involved in ROS
production, PR proteins and phytoalexins synthesis, depending on chromatin chemical modifications
for more robust activation. Covalent modifications of histones are known to occur by acetylation and
methylation of their basic groups (mainly Lysine and Arginine) and have been assumed to serve as
docking sites for transcriptional co-activator proteins or anyhow have a role in gene activation. Thus,
priming would be an epigenetic process, involving DNA acetylation/methylation through RNAdirected DNA Methylation (RdDM) which is a form of gene silencing directed by small interfering
RNAs (siRNAs). More important, recent studies have also brought evidence in favor of a
transgenerational SAR transmitted by DNA hypomethylation that would provide epigenetic
inheritance of disease resistance, at least at the next generation.
Factors affecting efficacy of induced resistance in open field
Fitness costs are not the only problem to consider when dealing with the practical use of SAR
inducers under field conditions. Induced resistance is a host response and as such is greatly
influenced by genotype and environment that lead sometimes to a relatively poor disease control
compared with fungicides. Furthermore, the timing of inducer application and its concentration is of
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crucial relevance, i.e. resistance inducers should be applied early to reduce pathogen/insect infection
and colonization, thereby allowing less fungicide/insecticide to be used and prolonging their life pan.
The limited number of field trials carried out under totally natural conditions shows usually a better
performance on dicots than on monocots. The latter, however, appear to preserve longer the induction
without requiring repeated applications as often needed by dicots. In any case, the main factors that
can limit the effectiveness of inducers in open field are: genotype dependence, nutrient soil
properties, environment and prior induced state of plant. While the first two of these factors may be
manageable to a great extent by farmers, the last two appear, at the moment, to be largely outside the
human control and require more knowledge and information on the ambient. As far as more field
trials will be expanded and novel inducers tested, the practice derived from such experience will help
to solve many problems and questions.
Concluding remarks
The chemical approach to induce and activate SAR represents a sustainable way to control plant
diseases by exploiting a natural phenomenon. As such, it may be considered as an alternative, or
complementary, strategy to the use of pesticides. With respect to the latter, it appears to be less likely
to select resistant strains of pathogens and offers an environmentally safe and friendly technology.
Unfortunately, so far it has not yet met enthusiastic favor by the farmers, at least in Europe. In few
words, no farmer will ever adopt a whatever innovative and friendly strategy, alternative to the
standard one, until he will not be reasonably convinced that it is successful. The mandatory of
introducing Integrated Pest management by all Member States of European Union since January
2014 hopefully will help to overcome this attitude. Certainly, to gain more widespread acceptance for
induced resistance in crop protection, there will need to be a lowering of expectation in terms of
levels of disease.
For further information and comprehensive literature see: F. Gozzo and F. Faoro, 2013. Systemic
acquired resistance (50 years after discovery): Moving from the lab to the field.
Agricultural and Food Chemistry 61:12473-12491.
Journal of