Scientia Horticulturae 250 (2019) 223–229

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Scientia Horticulturae
journal homepage: www.elsevier.com/locate/scihorti

Eustressors: Chemical and physical stress factors used to enhance vegetables T

production
M.C. Vázquez-Hernándeza, I. Parola-Contrerasa, L.M. Montoya-Gómeza, I. Torres-Pachecoa,
⁎
D. Schwarzb, R.G. Guevara-Gonzáleza,
a
Biosystems Engineering Group, School of Engineering, Autonomous University of Querétaro, Campus Amazcala, Carr. Chichimequillas-Amazcala Km 1 S/N. Amazcala, C.
P.76265, El Marques, Querétaro, Mexico
b
Leibniz Institute of Vegetable and Ornamental Crops, Theodor Echtermeyer Weg 1, D-14979, Großbeeren, Germany

A R T I C LE I N FO A B S T R A C T

Keywords: Worldwide plants are exposed to different biotic and abiotic stress factors limiting yield, growth, quality and
Plant immunity performance. Agricultural and horticultural practices for food production aim at plant cultivation at minimized
Elicitors stress using different production systems either under protected or open field conditions. However, it is also
Plant quality possible to stress plants to enhance horticultural production. The theory of stress indicates a dose/response
Distress
relationship between the strength and length of the stress factor (stressor) and the plant response. Plant re-
Hormetic dose
sponses to cope stress are triggered after recognition of a range of biological, chemical, and physical stressors.
Slight doses of stressors might cause positive effects on plant performance (“positive stress” or eustress), whereas
on the contrary, high doses provoke negative effects (“negative stress” or distress). Managed as eustress dose and
lenght, an eustressor might stimulates the plant response in such a way that plant production and quality are
improved. A myriad of literature has reported beneficial effects for the applications of biological (biostimulants/
elicitors) and non-biological chemical eustressors in horticulture. However, physical eustressors have not been
exhaustively studied in this sense. The present review aims at presenting the current status of the concepts, case
studies and applications of eustressors in horticulture. Moreover, the review focuses on the necessity of exploring
physical eustressors as stress factors that modulate and increase the quality of horticultural commodities.

1. Introduction (eustress) or a negative (distress) effect on plant metabolism and thus

Lichtenthaler (1996) has defined plant stress as “any unfavourable
conditions or substance that affects or blocks a plant’s metabolism,
growth or development”. Plant stresses can be classified as “internal”
that come from within the plant and “external” that exist outside the
plant. External and internal stresses are usually referred to as “stress
factors” and “stressors”, respectively (Kranner et al., 2010). It is note-
worthy mentioning that the present review focuses on external “stress
factors” and their possibilities to enhance horticultural production. In
horticultural and agricultural practices worldwide, plants are exposed
to different stress factors (stressors) that limit yield, growth, quality and
performance. Based on their origins, they can be separated into biotic,
e.g. pathogens, insects, and abiotic, e.g. drought, extreme temperatures,
salinity, etc. The impact of the stressors is not only controlled by the
dose but also by its duration (Lichtenthaler, 1996). Thus, the balance
between the plant response (yield, growth, quality, defense or toler-
ance) and sensitivity may determine whether a stressor has a positive
growth (Kranner et al., 2010; Hideg et al., 2013; Kaciene et al. 2015).
For example, low temperatures cause distress for vegetative tissues of
vascular plants and is lethal for many plant species below freezing point
temperature (Venema et al., 2005; Schwarz et al., 2010), whereas low
temperature for a short period in the morning (“cool morning pulse”)
induces hardening and tends to improve growth in favour of growers’
targets (Kalberer et al., 2006). Based on this approach, a stress factor
can be called eustressor if plant’s response in terms of yield, growth,
quality, and resistance to diseases/pests or tolerance to abiotic factors is
positive (eustress) or distressor if the response is negative (distress).
The eustress approach reminds on the concept of “hormesis” re-
ported for toxins when applied in low doses in medicine (Calabrese,
2004). Anciently, Paracelsus (1493-1541) raised the definition: “All
things are poison and nothing is without poison, only the dose permits
something not to be poisonous” (“Sola dosis facit venenum”). However,
hormesis is currently defined as a biphasic response in which high doses
of a toxic agent could cause inhibition, i.e.distress, while a low dose of

⁎
Corresponding author.
E-mail address: ramon.guevara@uaq.mx (R.G. Guevara-González).

https://doi.org/10.1016/j.scienta.2019.02.053
Received 16 October 2017; Received in revised form 23 January 2019; Accepted 17 February 2019
Available online 22 February 2019
0304-4238/ © 2019 Elsevier B.V. All rights reserved.
M.C. Vázquez-Hernández, et al.
Fig. 1. Classification of biological and non biological origin eustressors based on their nature.
the same toxin can cause stimulation, i.e. eustress; it is this modest
overcompensation response, which is seen as the “hormetic low dose
stimulation” (Vargas-Hernandez et al., 2017).
Plants as sessile organisms have evolved a defense system consisting
in preexisting and inducible responses to cope with different types of
biotic and abiotic environmental stress factors (Mejía-Teniente et al.,
2013; Cardenas-Manríquez et al. 2016). A range of biological stressors
trigger inducible defense responses after being recognized by the plant,
thus providing efficient resistance toward non-adapted pathogens
(Wiesel et al., 2014). Such eustressors are called ‘elicitors’ and can be
derived from either a plant, a microbe, or generated synthetically
(Fig. 1). Interestingly, the use of some elicitors can additionally im-
prove plant growth, development, and produce quality, similar as de-
scribed for plant biostimulants (du Jardin, 2015; Naik and Al-Khayri,
2016; Yakhin et al., 2017).
Several non-biological stressors of chemical or physical origin are
also able to induce a positive plant response resulting in growth or
quality enhancement (Demkura and Ballaré, 2012). A majority of re-
ports evaluating effects of these physical and chemical eustressors on
plant performance confirm their potential and positive role in horti-
culture and agriculture to enhance production (Li and Kubota, 2009;
Trebbi et al., 2007; Telewski, 2006).
Eustressors, especially the chemical ones, as a new type of plant
production activators, should have a national and international legal
framework similar to the legal aspects for biostimulants and agronomic
fertiliser additives in the EU that proposed appropriate data require-
ments and efficient administrative procedures to carry out assessment
of risks and efficacy of plant biostimulants and agronomic fertiliser
additives (PB&AFA; Traon et al., 2014).
This review aimed at presenting the current status of concepts, ex-
amples and applications, as well as the requirement of a legal frame-
work of biological and particularly non-biological, i.e. chemical and
physical eustressors. Moreover, it also attempts to encourage the hor-
ticultural scientific community to discuss the necessity of exploring
especially physical stress factors with the objective to improve horti-
cultural production. Because of the replacement of applications of toxic
chemicals and products with side effects in horticulture we find this
topic even more up to date and currently important. Therefore, an ex-
haustive and detailed description of single physical eustressors, nano-
technology and salinity is summarized in the review papers of the
Special Issue on Abiotic Stress.
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Scientia Horticulturae 250 (2019) 223–229
2. Types of eustressors
So far among the eustressors are different types that are already
defined and applied. These are the groups of biostimulants and elicitors,
both with a clear biological origin (du Jardin, 2015; Mejía-Teniente
et al., 2010). Their definitons overlap, reveal similarities, and need to
be described briefly hereafter. On the one hand, elicitors are com-
pounds of biological origin, which activate chemical defense in plants
(Thakur and Singh Sohal, 2013). Elicitors can be originated from out-
side the plant so called Microbial- and Pathogen-Associated Molecular
Patterns (MAMPs and PAMPs) as well as Herbivore-Associated Mole-
cular Patterns (HAMPs), or from inside the plant named as Damage-
Associated Molecular Patterns (DAMPs) (Vega-Muñoz et al., 2018). On
the other hand, a biostimulant is a “formulated product of biological origin
that improves plant productivity as a consequence of the novel, or emergent
properties of the complex of constituents, and not as a sole consequence of
the presence of known essential plant nutrients, plant growth regulators, or
plant protective compounds “(Yakhin et al., 2017). Thus, biostimulants
have a growth-promoting effect that may, or may not, be accompanied
by a chemical defense-enhancing effect in the plants (Colla and
Rouphael, 2015; du Jardin, 2015). Eustressors with biological activity
on plants share properties recognized in plant biostimulants having or
not elicitor activity. According to the European Biostimulants Industry
Council (EBIC, 2011), biostimulants include diverse formulations of
compounds, substances and other products that are applied to plants or
soils to regulate and enhance crop production. Thus, they improve crop
vigour, yields, quality, post-harvest shelf life, and conservation via in-
creasing the efficiency of different physiological pathways. Their ap-
plications in horticultural crops have widely been tested (Mejía-
Teniente et al., 2010; du Jardin, 2015).
Other eustressor types of non-biological origin, that cannot be
considered as biostimulants or elicitors, are physical and chemical eu-
stressors. They are within the concept of hormesis and eustress men-
tioned above. Although they may also act on plant defense but outside
the biostimulant definition, they particularly alleviate abiotic and biotic
stresses (Ehsanpour and Razavizadeh, 2005; Demkura and Ballaré,
2012). For instance, low temperatures (cold acclimation) and UV ra-
diation applications on plants induce flavonoids accumulation that
improves freezing and drought tolerance (Samanta et al., 2011;
Nakabayashi et al., 2014). Moreover, chemical eustressors as phosphite,
have been shown to significantly improve crop yield and quality, as
well as to stimulate environmental stress responses in horticultural
crops by increasing biomass, defense responses and uptake of nutrients,
such as phosphorus (Samanta et al., 2011; Nakabayashi et al., 2014;
M.C. Vázquez-Hernández, et al.
Gómez-Merino and Trejo-Téllez, 2015).
In order to facilitate communication, exchange of data, improve and
standardise experimental approaches within the horticultural commu-
nity, we propose a classification for eustressors useful in horticulture
based on their nature as those from biological origin, i.e. biostimulants
and elicitors, and those from non-biological origin, i.e. chemical and
physical eustressors (Fig. 1).
3. Examples and results of eustressor applications to plants
Eustressors are biological, chemical or physical stress factors that
when applied in hormetic doses/duration improve plant performance
by increasing several physiological pathways that may or not include
plant defense. Beside biological eustressors, chemicals from non-bio-
logical origin (Fig. 1) and physical eustressors have also shown to be
useful enhancing horticultural production caused by different me-
chanisms. Thus, brief examples of eustress effects of each type of eu-
stressors in horticulture are mentioned in the following sub-sections.
3.1. Eustressors of biological-origin
All eustressors of biological origin can be classified in biostimulants,
elicitors or both. Because of the recent comprehensive reviews on
biostimulants (du Jardin, 2015; Yakhin et al., 2017) we focus here only
on elicitors. Based on their origin, elicitors can be a) complete cells, b)
microbe-, c) herbivore-, or d) plant-derived cell extracts or e) specific-
single compounds. Meanwhile, several of the aforementioned features
are also displayed by biostimulants as previously discussed (du Jardin,
2015; Yakhin et al., 2017).
a) Complete cells
Plants inoculated with beneficial microorganisms as the Plant
Growth Promoting Rhizobacterias (PGPRs), induce morphological and
biochemical modifications resulting in increased tolerance to abiotic
stresses defined as IST (induced systemic tolerance). PGPRs increase
plant growth and resistance to abiotic stresses through various me-
chanisms such as, production of ACC (1-aminocyclopropane-1-carbox-
ylate) deaminase, reducing production of stress ethylene, modifications
of further phytohormones, induction of synthesis of plant antioxidative
enzymes, improvement in the uptake of essential mineral elements,
extracellular polymeric substance (EPS) production, decrease in the
absorbtion of excess nutrients/heavy metals, and induction of abiotic
stress resistance genes (Etesami and Maheshwari, 2018).
b) Microbial-Associated Molecular Patterns (MAMPs,PAMPs,
NAMPs)
Among the elicitors from microbe-derived extracts are fungi-derived
elicitors coming from cell wall breakdown products, which contain a
mixture of chitin, mannoproteins, and β-glucans, that can elicit a range
of plant responses (Wiesel et al., 2014). Bacterial-derived elicitors are
extracellular polysaccharides (EPS), lipopolysaccharides (LPS), fla-
gellin, and elongation factor Tu (EF-Tu), or mixtures of them and other
molecular compounds of bacterial cells (Deslandes and Rivas, 2012).
Recently, a class of small molecules that is made only by nematodes,
and that functions as pheromones in these organisms, was shown to be
recognized by a wide range of plants. In the presence of these mole-
cules, termed Nematode-Associated Molecular Patterns (NAMPs),
plants activate innate immune responses and display enhanced re-
sistance to a broad spectrum of microbial and nematode pathogens
(Choi and Klessig, 2016).
c) Herbivore-Associated Molecular Patterns (HAMPs)
Herbivores provoking feeding damage on plants deposit abundant
cues as for instance, fatty acid conjugates that plant may perceive and
activate innate immunity. These cues may be present in saliva, oral and
oviposition secretions, and feces in the herbivore and are so called as
herbivore-associated molecular patterns (HAMPs; Acevedo et al.,
2015).
d) Damage-Associated Molecular Patterns (DAMPs)
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Scientia Horticulturae 250 (2019) 223–229
DAMPs are currently considered the most recently discovered ca-
tegory of elicitors as endogenous indicators of injury (Quintana-
Rodríguez et al., 2018). Plant-derived elicitors can be breakdown pro-
ducts of plant cell walls including β-glucans, oligogalacturonides (OGs),
xylose, and phenylpropanoids-containing compounds produced by
herbivores attack to the plants (Ferrari et al., 2013).
e) The group of specific compounds consists of phytohormones,
oligosaccharides, volatile organic compounds, as well as extracellular
ATP and conspecific DNA (Vega-Muñoz et al., 2018). The first are
molecules produced by plants that regulate plant growth and devel-
opment. The main phytohormones, such as auxins, cytokinins, gibber-
ellins, ethylene, abscisic acids, and strigolactones have shown to induce
drought and osmotic stress tolerance in several plant species (Wilkinson
and Davies, 2010; Ruíz-Lozano et al., 2015). Volatile organic com-
pounds from plants as limonene, methyl jasmonates, methyl salicylate,
trans-2-hexenal, carvacrol, nonanal, methanol and nitric oxide from
lettuce, beans, and tobacco, show antimicrobial effects and protect
plants against biotic stress (Tierranegra-Garcia et al., 2011; Dorokhov
et al., 2012; Komarova et al., 2014; Quintana-Rodriguez et al., 2015).
Even microbial volatiles have been shown as plant growth inducers
(Fincheira and Quiroz, 2018).
The successful use of elicitors and biostimulants in horticulture and
agriculture will depend on the understanding of their effects not only
on plant defense/tolerance but also on other aspects related to plant
development and environmental responses to alleviate abiotic stress
(Mejía-Teniente et al., 2010; Yakhin et al., 2017).
3.2. Eustressors of non-biological-origin
3.2.1. Chemical eustressors
Inorganic salts of essential elements required by plants have been
reported with fungicide activity (Deliopoulos et al., 2010). Among the
type of salts with this antimicrobial activity are chlorides, phosphates,
phosphites, silicates and carbonates; these inorganic salts influence pH
and REDOX homeostasis, plant cell osmotic regulation, phytohormone
signaling, and enzymatic activities related to stress response
(Chakraborty et al., 2015).
In addition, elements as Al, Co, Na, Se, and Si are considered as
beneficial for plant growth (Avila-Juarez et al., 2017). These beneficial
elements have been reported to enhance resistance to biotic stresses
such as pathogens and herbivory, and to abiotic stresses such as
drought, salinity, and nutrient toxicity or deficiency (Pilon-Smits et al.,
2009). Effects as cell wall rigidification, osmoregulation, enzyme reg-
ulation, antitranspiration, thermal regulation, antioxidant protection,
phytohormone synthesis and protection against toxic levels of heavy
metals have been reported for this type of elements promoting plant
growth, quality of plant products and tolerance to biotic and abiotic
stresses (Pilon-Smits et al., 2009; Zengin and Munzuroglu, 2005; Avila-
Juarez et al., 2017).
Furthermore, rare elements are homogeneous elements with similar
chemical properties that include lanthanoides, scandium (Sc) and yt-
trium (Y). The majority of the studies with rare elements has been re-
ported in China, the country with the highest natural deposits of rare
elements in the world. Although not conclusive, some reports display
that rare elements in certain doses in the soil, increase antioxidant
enzymes, total phenols and carotenoids in corn and mungbean, mod-
ifying plant enzymatic activity, and promoting the activation of anti-
oxidant mechanisms such as antioxidant enzymes or secondary meta-
bolites (Gopal and Rizvi, 2008; Challaraj et al., 2010). As other stress
factors, the effect of rare elements on plants varies also depending on
the element, its dosage and residence time. For instance, the lanta-
noides cerium (Ce), lanthanum (La) and neodymium (Nd) can increase
yield and fruit quality in low concentrations in some crops, whereas
they are able to cause toxicity in high concentrations (Wang et al.,
2007).
Salinity is preferentially considered a chemical stressor because,
M.C. Vázquez-Hernández, et al.
although it causes detrimental effects on plant growth by imbalances in
supply and uptake of chemical elements in high concentrations above
4 dS m−1, however, it operates also via an osmotic effect similar to
drought (Bezerra de Lima et al., 2017). Therefore, this topic was in-
cluded in the Special Issue on Abiotic Stress. Salinity affects both,
physical quality and chemical composition of various horticultural
produces (Colla et al., 2013). Moderate salinity can be easily applied by
managing electrical conductivity and concentration of the nutrient so-
lution in order to increase the composition and concentration of phy-
tochemicals (Kyriacou and Rouphael, 2018). Effective application of
eustress, such as moderate salinity, can activate tailored plant responses
involving the activation of physiological and molecular mechanisms
and the strategic accumulation of bioactive compounds necessary for
adaptation to suboptimal environments (Rouphael and Kyriacou,
2018). This salinity eustress treatments on vegetables has been de-
monstrated that increases non-structural carbohydrates and health
promoting phytochemicals such as lycopene, β-carotene, vitamin C,
phenolic contents, and even reduce the concentration of anti-nutrient
compounds such as nitrate due to antagonism between nitrate and
chloride for the same anion channel (Rouphael and Kyriacou, 2018).
Another type of chemical eustressor is the use of nanotechnology in
horticulture and agriculture that is tremendously increasing worldwide,
however, it is generating doubts about the possible environmental and
human risks (Parisi et al., 2012). Nanoparticles have mainly been used
as nanofertilizers or nanoencapsulated nutrients (Milani et al., 2012).
Recent research has shown that improving germination and growth in
tomato and tobacco is promoted by multi-walled carbon nanotubes
(Khodakovskaya et al., 2011, 2012).
3.2.2. Physical eustressors
Traditionally viewed as detrimental to crops, recent evidence shows
that the levels of ultraviolet radiation (UV; 100–400 nm) of sunlight can
actually have a number of beneficial effects on the performance and
nutritional quality of many fruits, vegetables and ornamental crops (Yin
and Wang, 2012). UVA (315–400 nm), UVB (280–315 nm) and UVC
(100–280 nm) were shown to have effects on growth, photosynthesis,
secondary plant metabolites, and pests, such as aphids, whiteflies, and
thrips (Neugart et al., 2012; Bridgen, 2016). UV radiation especially
tested in greenhouses, affected interactions between important crops
and pathogens or pests, interrupting the life cycle of several pathogens
and altering behavior of many insects (Ouhibi et al., 2014). Moreover,
UVeC (100–280 nm) radiation treatments have shown positive effects
in fruit dissinfection and plant protection against pathogens. Visible
radiation as those from the light-emitting diode (LED) technology has
rapidly and tremendously advanced in the past years and is nowadays
linked with controlled environment agriculture. Recent research about
LEDs in the horticulture and floriculture industry, displays achieve-
ments ranging from greenhouse applications to plant factories, vertical
farming and growth chambers. The selection of the appropriate LED
light composition and amount must be carefully taken into account
because it depends on the goal, such as amendment of crop yield,
phytochemical content, nutritional value, flowering control, transplant
success, pre-harvest and postharvest product quality, and production of
regeneration material (Bantis et al., 2016; Snowden and Bugbee, 2016).
Controlled water stress during cultivation has shown promising
possibilities to enhance horticultural production, practised in a strategy
called “regulated deficit irrigation (RDI)” (Chai et al., 2016). On one
hand drought is one of the most serious abiotic stresses affecting phy-
siological and biochemical mechanisms in plants and thus restricting
their growth, development and productivity. On the other hand, water
deficiency if well managed may improve fruit quality through higher
concentration of flavor compounds and phytochemicals in different
crops (Veit-Köhler et al., 1999; Cáceres-Mella et al., 2017). Beside fruit
quality further important features in horticultural and agricultural plant
production are compactness, short internodes, balanced growth of
leaves with a similar size and a large number of floral buds (Chai et al.,
226
Scientia Horticulturae 250 (2019) 223–229
2016; Cáceres-Mella et al., 2017). Therefore, regulated deficit irrigation
is another interesting tool as physical eustressor useful in horticulture
that should gain attention. Improved water use efficiency with RDI has
been found mainly due to the following mechanisms, for instance in
wheat and rice: (1) enhanced guard cell signal transduction network
that decreases transpiration water loss, (2) optimized stomatal control
that improves the photosynthesis to transpiration ratio, and (3) de-
creased evaporative surface areas with partial root-zone irrigation that
reduces soil evaporation (García Del Moral et al., 2003; Ashraf et al.,
2012). The mechanisms involved in the plant response to RDI-induced
water stress include the morphological traits, e.g., increased root to
shoot ratio and improved nutrient uptake and recovery; physiological
traits, e.g., stomatal closure, decreased leaf respiration, and maintained
photosynthesis; and biochemical traits, e.g., increased signaling mole-
cules and enhanced antioxidation enzymatic activity (Chai et al., 2016).
As known, each plant species including horticultural crops has an
optimum temperature for growth and development, outside of which
they suffer reduced productivity and quality (Criddle et al., 1997). On
one hand, for some developmental processes, such as bud break in fruit
and nut trees (Chao et al., 2007), vernalization (Michaels, 2009), seed
removal from dormancy (de Castro et al., 2001), low temperature
conditions are demanded. On the other hand, it is possible to improve
plant’s tolerance and thus, growth to non-optimal temperature condi-
tions by applying certain temperature stress conditions. The exposure of
plants to low temperature conditions for a limited and controlled period
of time is one of these strategies (Miao et al., 2009). The result is en-
hanced crop hardiness, i.e. plant tissue is able to resist or tolerate low
temperatures without injury. Some typical annual vegetables, such a
Solanaceae and Cucurbitaceae have a certain amount of hardiness.
Moreover, growing for a better quality under controlled non-optimum
temperature is very common. It is practised particularly under green-
house conditions where temperature control is possible. As a result,
growth is slowed down in some ornamentals at lower temperatures to
reach a better quality (e.g. lilies) or bloom is hastened when needed at
higher temperatures. It also may help to improve quality attributes of
some annual vegetables, such as tomato (Ntatsi et al., 2014). Concepts
in the use of differences in day and night temperature (the DIF tech-
nique; Latimer, 1991) are also common for the purpose of controlling
plant internode length and thus elongation rates, both in ornamentals
and vegetables, particularly for seedlings (Grimstad and Frimanslund,
1993). The thermomorphogenic responses of plants at leaf and stem
elongation in Triticum spp and Lycopersicon esculentum seems to be re-
lated to mechanisms involving changes in the production of gibberellins
(GA3) and tissue sensitivity to these plant growth regulators.
Another physical stress tested and able to enhance horticultural
production is the thigmomorphogenesis. The application of mechanical
stimulation has been shown to induce plant responses that yield some of
the commercially relevant phenotypes including increased compact-
ness, higher girth, darker leaves and a delay in flowering (Chehab et al.,
2009). Mechanical stimulation in nature occurs e.g. through wind, rain,
neighboring plants or predatory animals and induces a range of mor-
phogenic responses that have been summarized under the term thig-
momorphogenesis. Thus, a number of examples suggest that mechan-
ical stimulation applied in a greenhouse setting can be used to alter
plant growth in order to produce marketable plants (Braam, 2005).
Electricity is a further physical stress that deserves to be explored
for improvements in horticultural production. The impact of electricity
on plant development and accumulation of metabolites is not well
understood. Studies in plants including effects of strong and weak
electric fields, magnetic fields and electric currents on growth and de-
velopment, as well as on plant metabolites, have been shown for hor-
ticultural/agricultural applications resulting in higher yields in terms of
fruit yield and fruit number at least for strawberries (Dannehl et al.,
2012). Moreover positive effects on germination rates, fresh weight of
leaves and roots in sunflower, pea and Vicia faba have been reported for
electricity treatments (Maffei, 2014).
M.C. Vázquez-Hernández, et al. Scientia Horticulturae 250 (2019) 223–229

Table 1
Effects of some chemical and physical eustressors on plant performance.
Eustress Factor Plants species Results Reference

Chemical
Salinity (NaCl)
Inorganic salts (Phosphite)
Beneficial elements (Se)
Rare elements (Ce+3)
Nanostructures (Carbon
nanotubes)
Physical
UV radiation (UV-A)
RDI
Acoustic waves (25 kHz at 75 dB
during 180 minutes)
DIF
Tomato, pepper, melón, Increase in levels of sugars, aminoacids and organic acids Rouphael and Kyriacou,
watermelon, eggplant, lettuce and 2018
cauliflower
Celery, lettuce, potato, sweet Improvement in yield, chlorophyll content, fruit size, phosphorus Gomez-Merino and trejo-
pepper, tomato content in the whole plants Tellez, 2015
Soybean Increase antioxidant capacity of tissues and promotes resistance to Avila-Juarez et al., 2017
abiotic stress factors
Horseradish Increase levels of K, Mg, Ca, Cu, Fe and Mn contents Wang et al., 2008
Tomato Increase in numebr of flowers and fruits Khodakovskaya et al., 2012
Tomato, radish, kale Increasing fresh and dry weights, chlorophyll contents, Tezuka et al., 1993
photosynthetic activity, dark respiration and delay in senescence of Neugart et al., 2012
tomato leaves. Flavonoids contents increased
Tomato Increase in fruit yield and quality Chai et al., 2016
Cucumber and zucchini Increase in poliamines, vitamin C and respiration rate Shigeoka et al., 2002
Tomato Slow internode growth regulation depending on the +/- DIF value

Beside these five physical eustressors several more are able to affect
and even enhance vegetables production, such as acoustic waves, other
ligth spectra than UV-light and magnetic fields (Fig. 1; see also the
reviews of the Special Issue on Abiotic Stress). A brief summary of some
significant case studies using chemical and physical eustressors in
plants is shown in Table 1.
4. Product formulation, regulation and legal framework of
eustressors
Most manufacturers do not reveal the technology of elicitors, bios-
timulants and chemical eustressor products due to their commercial
secrets (Traon et al., 2014). Some chemical eustressors produce similar
responses among a wide range of plants, but others are unique to a
specific plant species (Schmelz et al., 2009; Avila-Juarez et al., 2017).
The product formulation depends on the chemical nature of an eu-
stressor including adjuvants, tensioactives and other co-formulants, as
well as on the way of application (spray, liquid, powder) (Reglinski
et al., 1994).
Compared with chemical compounds physical eustressors are en-
vironmental factors and therefore, it is obvious that they cannot be
formulated for horticultural applications. However, because they are
also eustressors they need to be applied considering dose and time of
application during plant production.
Currently, no laws are in use for the application of eustress-causing
products of physical or chemical (different to elicitors) nature in
greenhouses and in open fields. Moreover, it is important to know their
harmful side effects generated when a plant is subjected to them and
whether or not they affect consumer health. The problem of estab-
lishing legislation for the broad group of eustressors and their use in the
agronomic industry lies in the precise description of their definition. On
one hand, some chemical eustressors of non-biological origin might be
subjected to the legal framework established for biostimulants (du
Jardin, 2015), following the national/local rules according to EBIC
(European Biostimulant Industry Council), AAPFCO (American Asso-
ciation of Plant Food Control Officials), USDA (United States Depart-
ment of Agriculture), or EPA (Environmental Protection Agency). On
the other hand, other chemical (those of non-biological origin) and
physical eustressors must be clearly considered in future legislation for
horticultural and agricultural applications. The more eustressors will be
applied under praxis conditions, the more a real demand for legislation
is created in regulating their application worldwide. This is necessary to
avoid misconceptions, to establish guidelines for their commercializa-
tion, and thereby to generate greater sustainability and more
environmentally friendly agronomic activities (Malusá and Vassilev,
2014). In the report of the European Commission for Management of
Enterprises and Industries (Traon et al., 2014), some considerations are
explained in detail regarding regulation of fertilizers (EC No. 2003/
2003; 2004/2007), which establishes guidelines of legislation only of
inorganic fertilizers (mineral salts) (Torre et al., 2013; La Torre et al.,
2016; du Jardin, 2012, 2015; The EU Nitrates Directive, 2010). The
legislation for physical eustressors should likely be prepared following
existing legislations in other areas as for example, in medicine. Agree-
ments and regulations are available for their use in humans, such as: UV
radiation, electromagnetism, sound, microwave, etc. Entities such as
the World Health Organization (WHO), and National board or appro-
priate organizations for safety and healthcare responsible for regulating
properly their use to avoid side effects when they are applied through
therapies in hospitals or when there is a exposure either prolonged or
not in a work environment. In Latin America only 10 countries regulate
the doses of exposure to non-ionizing radiation among them Mexico
(Habash, 2001).
These laws currently applied to humans can be a starting point for
the development of the regulation of physical eustressors used in plant
production. Such legislation must consider a serious characterization
and evaluation of their effects on plant metabolism and performance, as
well as an assessment of possible danger for consumers’ health.
5. Concluding remarks
Eustressor is a term rarely used so far. It summarizes a diverse group
of biological, chemical and physical factors with a positive effect on
plant performance, i.e. promoting plant growth and/or quality. Their
use must help vegetables production by improving nutrient and water
uptake, increasing plant tolerance to abiotic stress as well as defense
against pathogens and pests, thus diminishing the use of conventional
agrochemicals during cultivation. Moreover, eustressors might be an
adequate tool to be used in current and future sustainable plant pro-
duction systems worldwide. Efforts on the design of proper strategies
about using eustressors during vegetables production systems (“con-
trolled elicitation”) should include aspects related to adequate doses in
terms of concentration (for chemicals) or intensity (physicals), as well
as the periodicity of applications during cultivation. Studying the
former aspects of applications of eustressors should define if acute or
chronic treatments will be the best ones depending on the effects on
plant performance (biomass, fruit and seeds production, phytotoxicity
and tolerance to stresses) and quality (phytochemicals). Finally, In
order to commercialize eustressors, a clear legislation must be carried

227
M.C. Vázquez-Hernández, et al.
out. A legal framework will help in the registration of eustressor-based
products as a crucial element to ensure their practical, safe and legit-
imate application in vegetables production.
Acknowledgements
M.C.V-H, I.P-C and L.M.M-G thank Ciencia Básica 2016 (SEP-
CONACYT) 283259 for grant support during the elaboration of this
manuscript.
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