Instituto de Investigación Lightbourn A.C.

Bionanofemtofisiología Vegetal Disruptiva

Fulvalene, Rotaxane and Catenane Compounds: Ultraviolet Radiation Effects on Plants and its

Bioremediation

Lightbourn-Rojas L A1, León-Chan R G1, Heredia J B1, 2

 Instituto de Investigación Lightbourn A.C. Bionanofemtofisiología Vegetal Disruptiva1

Centro de Investigación en Alimentación y Desarrollo A.C. (CIAD) Unidad Culiacán2

Abstract  There are several studies on climate change, which focus on different factors: the

increase in atmospheric CO2, droughts, variable amount of rainfall, sudden

temperature changes and the increase of ultraviolet radiation (UV) due to the

deterioration of the ozone layer by atmospheric contaminants. The increase of UV

radiation causes adverse responses in plants development, particularly in DNA and

in photosynthetic system, especially in photosystem II, therefore the loss of

photosynthetic efficiency and a foods reduction. Plants have developed several

defense systems which are related to the synthesis of anthocyanins. These

compounds can protect plant tissues by absorbing excess of light, UV radiation or

by their antioxidant capacity, scavenging UV produced reactive oxygen species.

However, sometimes these mechanisms are insufficient due to photosynthetic

deficiency; therefore we have developed a new plant nutrition technology, based

on fulvalene, rotaxane and catenane compounds. With this approach, an increase

in the uptake, storage and availability of monochromatic ray at 563 nm can be

achieved. This can induce the photosynthetic optimization and the reduction of

metabolic delays in the photosynthetic system. This would help to maintain the

plant metabolism and therefore the stability of the food production regardless of the

adverse environmental conditions.

 

Introduction    The climate of a planet is determined by its total mass, its distance from the closest

star(s) (in the case of the Earth, the Sun) and the chemical composition of its

atmosphere (González et al., 2003). The latest is the most variable factor, both

naturally and by the activities of the organisms that inhabit it, especially humans. In

recent decades there have been a wide range of environmental changes that are

affecting life on Earth, so there are a variety of studies on climate change, which

focus on different factors such as the increase in atmospheric CO2 concentration,

melting icecap, drought, change in rainfall patterns, wind speed, sudden

temperature change, global warming and increased ultraviolet radiation, among

others (Bellard et al., 2012).

Plants are the organisms more exposed to environmental changes because

they can not migrate from where they develop, so they are essential baseline to

understanding the impact of climate change on Earth. Changes in the environment

to produce a negative impact on growth and development of plants are considered

as stress factors (Bray et al., 2000). This can be classified into primary stress,

when the stress factor directly affects the development of plants, and secondary

stress, when the stress factor provides generation of reactive oxygen species

(ROS) which adversely affect the metabolism of the plant (Ahmad y Prasad 2012).

The effects of climate change on living organisms can be classified into four

categories (Gonzales et al., 2003): 1) geographic distribution (tendency of some

species to move), 2) adaptation (micro-evolutionary changes in situ) 3)

physiological (photosynthesis, respiration, growth) and 4) phenological (changes in

the life cycles such photoperiod effects, cold hours, etc.). Therefore, changes in

radiation and temperature are factors that have more impact on the organisms

present on Earth, especially in plants, which are the basis of life energy on the

Earth, because they can transform solar energy into chemical energy , which is

taken by the rest of the organisms as food.

The plant growth is defined as an increase in dry matter, while development

is the increase in the number and size of their organs by division and/or cell

expansion: leaves, sticks, swords, flowers, roots, etc. The growth rate is

proportional to the product of the rate and efficiency of the catabolic activity to

convert photosynthates to structural biomass, therefore, plant growth is extremely

temperature sensitive (Lightbourn, 2011a; Źróbek-Sokolnik, 2012). On the other

hand, solar radiation (electromagnetic radiation) is one of the most important

factors in the growth and development of plants (Carrasco-Ríos, 2009), and is

involved in many important processes such as photosynthesis, phototropism,

photomorphogenesis, opening stomata, soil and temperature, etc. (Salisbury and

Ross, 1994; Castilla, 2007).

Solar radiation can be divided into three main ranges of wavelength:

infrared, visible and ultraviolet radiation (UV) (Castilla, 2007). UV radiation provides

a higher energy level that can adversely affect the metabolism of any organism.

This type of radiation is partially absorbed by the ozone layer. However, the

increasing of certain gases such as chlorofluorocarbons (CFC's) resulted in the

deterioration of the protective layer, therefore lead to an increase of UV radiation at

the Earth's surface (Hollósy, 2002).

The stress caused by increase of UV radiation triggers a range of

responses, such as alterations in gene expression and changes in cell metabolism,

which has influence on growth, development and production of plants. The length

and severity of stress, as well as the characteristics of the plants, their stage of

development, the affected tissue and genotype would influence on the answers

plants can present (Bray et al., 2000).

One of the most commonly response presented on stressed plants induced

by UV radiation is the synthesis of flavonoids, such as anthocyanins, which may be

due to its ability to absorb UV light or to the antioxidant capacity that these

compounds provide to reverse oxidative damage caused by UV radiation on cells

(Mazid et al., 2011).

However, these mechanisms could be insufficient due to photosynthetic

deficiency induced by UV radiation. Therefore, a new technology in plant nutrition

has been developed which optimizes the photosynthetic efficiency by maintaining

more available the power provided by the monochromatic ray of 563 nm.

   

Temperature    

In recent decades there has been a rise in temperature that is seriously

affecting the biological processes on Earth. This temperature increase is

widespread over the globe, such as in the Arctic, where the average temperature

has increased at almost twice as fast as the global average of the last one hundred

years (IPCC, 2007).

The temperature is not a measure of amount or concentration of a

substance or total energy. The temperature measures the molecular movement,

which means, the kinetic energy of the molecules within the system. Consequently,

the velocity indices of all elemental reactions increase exponentially with the

temperature increments (Lightbourn, 2011a). The thermodynamics first law refers

that the heat added to a system minus the work done by this, it will produce a

change in the internal energy of the system:

ΔE = q - W

where ΔE is the change in internal energy of the system, q is the amount of

heat added and W is the work carried out by the system, in this case we refer to

plants as the system in question. If q < W then the internal energy of the plant

decreases down to death, while if q >>> W then the heat inside the plant will

increase causing denaturation of its components (Lightbourn et al., 2012).

Therefore, a change of a few Celsius degrees leads to a significant change in the

growth rate, and this is because there is not a range in which the temperature

stops changes that affect the growth rates, so it is incorrect to talk about stress

ranges by temperatures, being correct when talking about stress by temperature-

time (Lightbourn, 2011a).

The stress caused in plants by temperature is classified into three types: 1)

cold damage, 2) freezing damage and 3) by high temperatures. This is because

each species or variety has, at any given state of its life cycle, a minimum

temperature below which does not grow, the optimum temperature (or temperature

range) which grows to a maximum rate and temperature above the maximum

which will not grow and may even die (Salisbury y Ross, 1994; Źróbek-Sokolnik,

2012). Therefore, the temperature is defined as an environmental factor that

significantly affects biological processes in all organisms because it will primarily

modify the properties of the membranes, the levels of enzymatic activity, speed up

chemical reactions, as well as affecting the phloem, xylem and cytoplasm solutions

(Taiz y Zeiger 2002; Źróbek-Sokolnik, 2012).

The membranes are in one of three stages depending on the external

environment: 1) as a crystalline liquid phase, which represents the range of fluidity

in which the membrane and its components work naturally, 2) as a solid gel, which

represents a membrane that retains its shape but is rigid and therefore not

functional, 3) and hexagonal and cubic phases, which represents the disruption of

the membrane caused by extreme environments (Nilsen and Orcutt, 1996). In the

first stage we have mentioned a balanced equation of thermodynamics first law,

while cases two and three are derived from an imbalance between the work of the

plant and the added heat (Lightbourn et al 2012).

The increase in temperature causes a greater fluidity in the membranes,

causing problems in cell functions, mainly in mitochondria and chloroplasts

(Allakhverdiev et al., 2008). Therefore, the deleterious effects that high

temperatures cause on plants mainly occur in photosynthetic functions and

thylakoid membranes. The three more sensitive photosynthetic sites to heat stress

are the carbon assimilation process, the ATP generation and the photosystems,

mainly photosystem II complexes (PSII), which are the most labile part of the

photosynthetic system to the heat effects (Salisbury and Ross, 1994; Allakhverdiev

et al., 2008). Also, the synthesis of various thylakoid membrane proteins is

extremely reduced during elevated temperature exposure (Süss and Yordanov,

1986), i.e. the apoprotein reaction center of photosystem II (P680), the sub-units α

and β of the ATPase synthase, cytochrome ƒ, cytochrome b559 and the apoprotein

from the center of the CP47 antenna complex (Santarius, 1973). This causes a

great disruption of PSII leading the plant inability to produce energy (ATP) from

photosynthesis. In general, the photosynthetic activity is stable until 30 °C but

dramatically decreases above this temperature until a complete inhibition is

reached at 40 °C (Carpentier, 2005).

Moreover, the increase chloroplasts membrane fluidity allows the ATP

molecules to go through more easily from citosol to chloroplasts (Carpentier,

2005). ATP is used in chloroplast to carry out the synthesis of carbohydrates in

mature plants, but in plants in growth phase, the ATP is used predominantly for

proteins and nucleotides synthesis, for which is required greater amount of energy

(Salisbury and Ross, 1994), so that in the photosynthetic system inefficiency

caused by stress is necessary to obtain energy from other sources to continue the

plant development until reserves will allow it. Therefore, the morphological

symptoms presented in heat stressed plants may include sunburn on leaves,

branches and stems, senescence and abscission of leaves, stem growth inhibition

and roots, damage and fruit discoloration, less production, cell size reduction,

stomatal closure and reduction of transpiration to prevent dehydration (Waheed et

al.; 2007 Mitra and Bhatia, 2008).

The observed increase in global average temperatures since the mid-

twentieth century is mainly due to the observed increase in concentrations of

anthropogenic greenhouse gases, which was found at 70% from 1970 to 2004; this

increase is due to the higher emission of these gases in relation of its

decomposition. Human activities result in emissions of four long-lived greenhouse

gases: carbonic anhydride mostly known as carbon dioxide (CO2), methane (CH4),

nitrous oxide (N2O) and chlorofluorocarbons (CFC's, group of gases containing

fluorine, chlorine or bromine). Increased CO2 concentrations are due primarily to

fossil fuel use, the CH4 is predominantly due to agriculture and fossil fuel use and

N2O increased is mainly due to agricultural activities (IPCC, 2007). The increase in

some of these compounds causes the degradation of the ozone layer, allowing a

greater emission of ultraviolet rays at the Earth surface, which also inferred in

plants development (Björn and McEnzie, 2008).

   

Ultraviolet Radiation (UV)    

The UV radiation corresponds to a wavelength range of 200 to 380 nm. This

radiation is low when the sun elevation above the horizon is low and to low altitude.

UV radiation represent about 9% of the solar total radiation energy and can be

divided into UV-A (320 to 280 nm) skin tanning radiation, UV-B (290 to 320 nm)

responsible of skin cancer, and UV-C (200-290 nm) which is potentially hazardous

but almost completely absorbed by the ozone layer (Castilla, 2007, Prado et al.,

2012). The absorption coefficient of ozone decreases rapidly at wavelengths above

280 nm and approaches zero around 330 nm (Hollósy, 2002). Although the

stratospheric ozone determines the amount of UV radiation that reach the Earth

surface, its level is significantly affected by variations in latitude and altitude. The

level of UV radiation over tropical latitude is higher than in temperate regions due

to lesser atmospheric UV absorption determined by the solar angle and the ozone

layer itself, which is thinner in equatorial regions (Jaakola and Hohtola, 2010;

Prado et al., 2012).

In 1987, it was established the Montreal Protocol on "Substances that

deplete the Ozone Layer" to carry out the reduction of these compounds in the

atmosphere, mainly CFCs; however, the deterioration continues increasing to 0.6

% yearly (Prado et al., 2012). In general, every 1 % of reduction in the ozone layer

results in an increase of 1.3 to 1.8 % of UV-B radiation (Hollósy, 2002). Most

studies concerning that the effects of UV radiation increases are focus on UV-B

radiation, however, the presence of UV-C radiation has been show, even within

plastic greenhouses (León-Chan, 2012), so there are some studies that provide

UV-C to study their effects on plants (Mahdavian et al., 2008; Sarghein et al., 2008;

Katerova et al., 2009).

UV radiation can inhibit photosynthesis by altering gene expression and by

damaging the parts of the photosynthetic machinery (Smith et al., 2009). Sites that

are affected by this type of light are the light collector complex II (LHCII), the PSII

reaction center and PSI acceptor. However, most studies have demonstrated that

PSII is more sensitive to UV radiation as compared to PSI; this is due to the

chemical changes which produces the UV radiation on amino acids with double

bonds of the PSII proteins (Carrasco-Ríos, 2009). The aromatic amino acids such

as phenilalanine, tryptophan and tyrosine, as well as cysteine, cystine, and

histidine, would provide to proteins the characteristic of absorbing UV and thereby

the property to be modified (Hollósy, 2002). The amino acid histidine is present in

the PSII D1 protein, which contains chlorophylls linked to it (Taiz and Zeiger,

1998), therefore, the conformational changes causing by UV on these proteins will

liberate chlorophylls, facilitating their photo-oxidation (Mahdavian et al ., 2008).

The UV radiation also induces the loss of enzymes activity involved in the

Calvin cycle, especially on the 1,5 diphosphate carboxylase (Rubisco) which

catalyzes the CO2 incorporation. Another effect of UV radiation is the production of

reactive oxygen species (ROS), which also act on the denaturation of proteins;

moreover, ROS are involved in the lipoperoxidation processes from the plasma

membrane (Björn and McEnzie, 2008, Carrasco-Ríos, 2009). However, ROS can

also initiate signals stress responses to UV, including enzyme activation, gene

expression, programming cell death, etc. (Jaspers and Kangasjärvi, 2010).

The DNA is also sensitive to UV-B and UV-C, because these photons

promote π-π transitions in nitrogenous bases that constitute the nucleotides,

altering the normal establishment of chemical bonds. This mainly causes the

formation of cycle butane pyrimidine dimers (CPD) produced by the dimerization of

adjacent pyrimidines (TT, TC, CT or CC), and produce other compounds known as

(6-4) photo products (Björn and McEnzie, 2008; Carrasco Rivers, 2009). The

biological effects of these lesions are variable, since in some cases replication in

the lesion is stopped, while in other cases the replication continuous, thereby

promoting mutations. Therefore, these products are the leading causes of cancer

(Björn and McEnzie, 2008).

   

Plant Responses to Ultraviolet Radiation     The plants exhibit different responses to environmental stresses like UV

radiation exposure. Under these conditions, plants would show the presence of

wax cuticle deposition and trichomes that function as radiation reflectors; leaf area

reduction and increased of sheet thickness to reduce the damaged area; changes

on stomatal density, reduced of stems elongation, changes in branching pattern,

the synthesis of secondary metabolites with the ability to absorb UV light, as well

as alterations in plant-pathogen plant-predator interactions and gene expression

(Prado et al., 2012).

The synthesis of secondary metabolites of the phenylpropanoid pathway

has been widely studied as a defense mechanism to counteract the deleterious

effects of UV radiation produced in plants. Among these compounds there are

phenolic acids, insoluble polyphenols and flavonoids such as anthocyanins. Today

anthocyanins are the most studied flavonoids usually referred as the compounds

capable of reducing the photo-oxidative damage. These compounds stay mainly in

the epidermis cells, and are also being responsible for a variety of colorations in

plant tissues (Castañeda-Ovando et al., 2009).

Some authors mention that the tissues most exposed to the sun show

higher anthocyanin content, presenting a high variability of the content of these

compounds from leaves or fruits of the same plant (Salisbury and Ross 1994;

Lightbourn et al., 2008; Steyn, 2012). Here, the hypothesis about the anthocyanin

function in plants are showed: 1) protection of chloroplasts from excessive light,

especially in plants in development process or that have developed under shaded

conditions (Oren-Shamir, 2009); 2) protection against UV radiation, by the ability of

these compounds to absorb this type of radiation and, 3) the antioxidant capacity

that these compounds have, several times greater than some of its antioxidant

vitamins analogues. This antioxidant capacity could reduce the damage caused by

ROS generated by UV radiation (Hatier and Gould, 2009).

Some researches have shown an anthocyanins increase by effect of UV

radiation on different plant sources and in different development stages

(Mahadavian et al., 2008; Saghein et al., 2008, Guo and Wang 2010; Leon Chan,

2012). Therefore, there are investigations about the induction of some enzymes

involved in anthocyanin synthesis by radiation effect, finding an increase in the

activity of some of them, among which are the phenylalanyl ammonia lyase (PAL),

chalcone synthase (CHS), chalcone isomerase (CHI), dyhydroflavonol 4-reductase

(DFR), anthocyanin synthase (ANS), flavonone-3-hydroxylase (F3H), etc. (Tsukasa

et al. 2000; Hao et al., 2009; Guo and Wang 2010). With these facts, it has been

proven the involvement of these compounds on UV protection effects; besides

obtaining more information about the expressing routes and thereby creating new

alternatives that will promote the survival of plants against UV radiation stress (Guo

et al., 2008).

   

Other Environmental Impacts by Ultraviolet Radiation    

The changes in plants metabolism due to the increase of UV radiation not

only reduce the life of plants affected, because the reduction of food production

would cause great problems in the life of other organisms, particularly in humans;

as well as other issues like the balance of certain cycles, such as the carbon cycle

that can be severely affected by the changes in damaged plants and their capture

mechanism, as well as photosynthesis, carbon storage and respiration, among

others (Zepp et al., 2007). The classification of the UV radiation impact on the

Earth's surface is related to direct effects such as photosynthesis inhibition and the

carbon cycle balance; and indirect effects such as the alteration of the chemical

composition of plant foods which will also affect the decomposition of organic plant

matter in the soil by other organisms (Smith et al., 2009).

The increase of anthocyanins in plant tissues can cause changes in plants

interactions with other organisms. These interactions include attracting pollinators

and frugivores as well as herbivores and parasites repellents (Lev-Yadum and

Gould, 2009). It has also been observed some reduction of pathogenic attack,

therefore the increase of these compounds in certain case could be beneficial

(Paul et al., 2012). However, the production of these compounds may result in a

high energy cost to the plants, and it can become even greater considering the

deficiencies in energy production of plants whose have been damaged by UV

radiation; so there is a difficulty to the plant in order to sustain this defense

systems, as well as to reduce the production of plants with this stress (Wargent

and Jordan, 2013). This reduction in food production may become even a greater

problem, considering the increase in world population that is estimated at 9 billion

of people by 2050 (The Royal Society, 2009).

The leaves commonly that contain anthocyanins absorb more light in the

visible green and yellow region spectrum regarding those leaves which do not

contain it; however, is unknown this energy function (Hatier and Gould, 2009). This

energy could be used in repair mechanisms or photosynthesis optimization,

whereby the plant can continue to perform its metabolic activities with the least

possible deficiency; nevertheless, this mechanism may occur deficient with

nutritional techniques that have to now, since the increase in certain nutrients

appears not to be improved in plants that are damaged by UV light, because it only

considers some basic elements and excluding that plants would use many more

elements to carry out their functions (Lightbourn et al., 2011; Singh et al., 2012).

On the other hand, there is an increase in the use of plastic greenhouses in

order to reduce the risk of pathogen attack, and also to reduce high UV radiation

levels, therefore preventing from reaching and damaging the plants. However,

when the light passes from one medium to another, it suffers inverted cycloid

deviations namely tautocrony producing dicroism and birefringence that affects the

polarity and intensity of the light beam incident and refracted which consequently

alters the photosynthetic phenomenon. This can be quantified as a function of light

energy, starting from the basic conceptions and traditional until the logic formality

given by the mathematical complex of variations calculation in cycloid curves of

mathematical analysis (Lightbourn, 2010).

   

Reducing Plant Damage It has been demonstrated that with the application of a high dose of

photosynthetically active radiation (PAR) in conjunction with low levels of UV-B

radiation, Rubisco levels are unaffected; therefore, a sufficient amount of PAR

radiation diminishes the UV radiation adverse effects (Hollósy, 2002). Furthermore

inhibition of PSII activity in intact leaves during heat stress at 40 °C is mitigated if

performed during a low-intensity illumination. This is because light is responsible to

activate the adaptation mechanisms of the photosynthetic apparatus in the

presence of stress temperature, especially photosystems repair, which require a

low light intensity to carry out the protein phosphorylation and stimulation of diverse

enzymes activity. In contrast, a strong light accelerates the PSII deterioration

(Carpentier, 2005; Allakhverdiev et al., 2008).

Actually a new technology has developed in plant nutrition that consists on

clusters of selenium, nickel, titanium and polioxomolibdato. This is in fulvalenic

rotaxane-catenananica base, generating orthogonal sequence dendrimers that are

intra-tilacoidic nanosomes, which enables to optimize the photosynthetic efficiency

by capturing, storing and maintaining more available power provided by the

monochromatic beam of 563 nm. Therefore, induces the photosynthesis

optimization, serving as a light reserve at chloroplasts level. This helps to maintain

the plant metabolism, which results in phytotaxic stability, and therefore, stability of

production, irrespective of any adverse conditions such as UV radiation stress

(Lightbourn 2011b).

Furthermore this technology contains zinc as the principal element, which is

required for growth hormones synthesis (cytokinins and auxins), besides

participate in chlorophyll production and possibly prevent its destruction (Salisbury

and Ross, 1994), thereby further reduce the damage caused by high temperatures

and UV radiation.

This compound is applied by foliar absorption and involves an innovation in

signaling and synchronization cell, because provide continuity in photosynthetic

energy uptake and transfer, due to that clusters absorb and store energy.

Furthermore, owing of these clusters not interrupt the metabolism on account of

darkness, there are no delays in the formation and maintenance of plant tissue

which means the total dejection of metabolic delays and consequences translated

into structural failures, metabolic, energetic and homeostatic that directly affect the

quantity and quality of biomass (Lightbourn, 2011b).

Besides the damage due to overheating and/or UV radiation, may be

metabolic delays, which are because when the active photosynthetic cycle has

been initiated in diurnal phase and this is interrupted by reasons such lack of light

or decreased of light intensity, results in a total restart of metabolic energy

mechanism. These interruptions or decrease of PAR radiation may be due to

changes in weather, such as air pollution or sudden cloud, as well as the use of

greenhouses that being a barrier which causes changes in the light beam and can

also accumulate substances that block the arrive of PAR radiation to the foliage

plants. i.e., in crops which begin its photosynthetic processes and are interrupted

by blockage or decreased of solar radiation due to cloudy, the plants must wait for

a recurrence of the initial conditions of radiation to restart the total process

because the plants do not continue its metabolism in the point where is stopped.

Therefore, this involves a long metabolic delay of many hours or even days, this

depend of the event length, which is reflected in a reduction of the creation and

repair of maintenance and production tissues.

The implementation of this technological innovation made by Lightbourn Metabolic

Engineering and Lightbourn Biochemical Model, diametrically change the situation

because when the clusters of selenium, titanium, nickel and polioxomolibdate are

applied with an amphiphilic colloids nutrition, they are directly positioned on the

chloroplast tilacoidic structures and this acting as absortors, storers and

interconverters in a intermolecular triple switch, that able to realize consecutive and

reversible monoelectrics reductions, schematized as shown in the following figures:

Photosynthetic Phenomena

Optimizing of 563 nm Monochromatic Beam to Optimized Induced

Photosynthesis

I1 = Ultraviolet radiation

I2 = Visible light

I3 = H+ induce the interconversion among the states 5, 6 and 7, the 5 state do not

absorbs in the visible region, the 6 state (yellow-green) absorbs in 401 nm (01), the

7 state absorbs in 563 nm (02) purple.

The (H+) controls the reversible interconversion between 8 and 9, in

response to ultraviolet (I1) and visible (I2) stimuli. The intramolecular triple switch

modulates the ratio between the two forms and the absorbance (O) of ⑨ through

of photoinduced protonic transfer, the truth table and the logical sequence of the

circuit shows as performed intramolecular communication.

ó 1

TETRAHIAFULVALENE (TTF) BIPINIDINIUM (BIPY) ABSORBANCE

Low Low High

Low High Low

High Low Low

High High High

The fluorescence of Pyrazolina interval is high when the (H+) is low and

viceversa. The fluorescence of the derived antrcinic is high when (Se+) or (K+) is

high, the emission is low when the concentration of both is low. (Low = 0) (High =

1)

Rotaxane (2)

Nanoscaled incorporating a Ni (II) Tris-Bipyridine stopper and two Bipyridium

electroactive units. This unit is able to perform two consecutive monoelectric

reductions and reversible in the presence of Triethylenediamine solution.

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