Participation of cytokinin on gas exchange and antioxidant enzymes

Ind J Plant Physiol.
DOI 10.1007/s40502-017-0283-2
REVIEW ARTICLE
Participation of cytokinin on gas exchange and antioxidant
enzymes activities
Fabiana B. de Moura1 • Marcos R. da S. Vieira1 • Adriano do N. Simões1 •
Sergio L. F. da Silva1 • Damiana C. de Medeiros2 • Reinaldo de A. Paes3 •
Arthur A. S. de Oliveira2 • Antônio H. C. do Nascimento1 • Walter S. E. Júnior1
Received: 20 May 2016 / Accepted: 7 January 2017
Indian Society for Plant Physiology 2017
Abstract This review article is aimed to evaluate the
effects of foliar application of cytokinin on enzyme activity
and photosynthetic parameters. The results obtained on gas
exchange and photochemical activity may be related to a
standard mechanism of activation defense under specific
environments. Further on the basis of study of enzyme
activity it can not be stated that cytokinin have effective
role in the delay of oxidative damage as contradictory
results have been observed by various workers.
Keywords Oxidative stress Photosynthesis Plant
hormones Senescence
Introduction
In higher plants, the regulation of metabolism, growth and
morphogenesis often rely on chemical signals from one part
of the plant to another. This idea was proposed by the
German botanist Julius von Sachs in the nineteenth century,
who stated that these chemical messengers are responsible
for the formation and growth of different plant organs, and
external factors can affect the distribution of these
& Marcos R. da S. Vieira
[email protected]
1
Unidade Acadêmica de Serra Talhada, Universidade Federal
Rural de Pernambuco, Serra Talhada, PE CEP: 59909-460,
Brazil
2
Departamento de Agropecuária, UFRN – Unidade
Acadêmica Especializada em Ciências Agrárias, Macaı́ba,
RN, Brazil
3
Centro de Ciências Agrárias-CECA, Universidade Federal de
Alagoas, Maceió, AL, Brazil
substances by the plant (Taiz and Zeiger 2009). The plant
hormones or phytohormones are naturally occurring organic
compounds of low molecular weight, which are produced by
plants at low concentrations (10-4 M), promote, inhibit or
change virtually all morphological and physiological processes thereof (Piotrowska 2009). The mechanism of action
of plant hormones is associated with the direct and specific
molecular interaction, which triggers a series of biochemical
and physiological events that produce measurable responses.
To act, hormones bind to specific protein receptors, forming
a hormone-receptor complex, which releases a secondary
messenger that migrates to the nucleus and causes gene
expression. Consequently, the formation of messenger RNA
(mRNA) from Deoxyribonucleic acid (DNA) induces the
synthesis of enzymes that act on polysaccharide linkages,
triggering cell growth (Castro 2002). Several researchers in
order to to promote, delay or inhibit vegetative growth;
increase effective fructification and fruit size; promote
rooting and break the dormancy of seeds and buds; control
the maturation and slow the process of senescence among
others, have been using synthetic substances that have
properties similar to those of plant hormones, which are
termed as growth regulators, plant regulators, phytoregulators or biostimulators (Biasi 2002). The development of
plant depends on the organization, location and maintenance
of meristems, which involves various regulation mechanisms, including hormone signaling (Courseau 2010). Generally, biostimulators or bioregulators (such as the plant
growt regulators) can be considered as potential chemical
tools, supplementary in the handling of plants (Vieira and
Castro 2004; Castro et al. 2005). The classes of compounds
responsible for these functions are: auxins, gibberellins,
abscisic acid, salicylic acid, jasmonates, brassinosteroids,
ethylene, polyamines and cytokinins (Mahgoub et al. 2011;
Hajizadeh et al. 2012).
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Cytokinin biosynthesis
The adenosine phosphate- isopentenyltransferase (IPT)
used to increase the cytokinin levels in plants was derived
from agrobacteria (Rupp et al. 1999). Adenosine triphosphate/adenosine diphosphate -dependent IPT enzymes
produce iP and trans-zeatin-type cytokinins, whereas
transfer ribonucleic acid(tRNA)-dependent IPT enzymes
are responsible for the production of cis-zeatin-type cytokinins. Two Arabidopsis tRNA-IPT genes, IPT2 and IPT9,
have been identified and analyzed in knockout approaches
(Miyawaki et al. 2006). They showed differential expression domains and levels and can regulate the cytokinin
abundance and spatial distribution (Miyawaki et al. 2006).
Adenosine phosphate-isopentenyltransferase enzymes are
involved in the integration of environmental signals and
development. Expression of adenosine phosphate- isopentenyltransferase3 in Arabidopsis thaliana is regulated by
nitrate availability, while that of IPT5 and IPT7 have been
reported to be upregulated by auxin treatment (Miyawaki
et al. 2004). Adenosine phosphate- isopentenyltransferase
enzymes have been used as a tool to increase the cytokinin
content in a specific spatial and temporal manner by utilizing specific promoters. These experiments linked cytokinin to various functions. A bacterial adenosine
phosphate- isopentenyltransferase driven by the Hsp70
promoter increased the expression of the meristem regulators Knotted-Like from Arabidopsis thaliana (Rupp et al.
1999). Adenosine phosphate-isopentenyltransferase were
used to increase the cytokinin content of plants in a
senescence-specific manner by combining them with the
senescence-associated gene 12 (SAG12) promoter (Merewitz et al. 2011, 2012). In creeping bentgrass senescenceassociated gene 12:: adenosine phosphate-isopentenyltransferase, the photosynthesis, water use efficiency, and
root viability were increased under water stress condition.
Adenosine phosphate-isopentenyltransferase expressed
under the control of a senescence associated receptor protein kinase promoter in rice changed the sink-source-relations in drought-stressed rice towards stronger sinks (Peleg
et al. 2011). Active cytokinins can be released by the
cytokinin hydroxylases CYP735A1 and CYP735A2 (Takei
et al. 2004).
Cytokinin: interconversion, conjugation,
degradation and transport
The most active forms of cytokinins are the free nucleobases (Åstot et al. 2000), but also ribosides seem to be
active (Spichal et al. 2004). In 1977 and 1981 adenosine
nucleosidases were discovered in barley and wheat germ
(Chen and Kristopeit 1981). Free bases can also be directly
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released in a single step reaction by a cytokinin nucleoside
50 -monophosphate phosphoribohydrolase named lonley
guy (Kurakawa et al. 2007). Expression patterns and single
knockouts as well as multiple knockouts were analyzed by
Kuroha and Tokunaga and colleagues (Tokunaga et al.
2012). Cytokinin ribosides can be converted into inactive
nucleotides by an adenosine kinase (Schoor et al. 2011).
The level of active cytokinin is also regulated by interconversion or conjugation of the free bases. A N-glycosylation can occur in the N3, N7 or N9 position and
inactivate the cytokinin irreversibly, whereas O-glycosylations are reversible and may play a role as storage form
(Munoz et al. 1990). In 1979 Entsch and colleagues identified a N7-glycosyltransferase (Entsch and Letham 1979).
Recently Wang and colleagues analyzed a mutant of
UGT76C2, a N-glycosyltransferase (Wang et al. 2011). In
1999 a zeatin-O-glycosidase was discovered and proved to
be active in Phaseolus (Martin et al. 1999). Degradation of
cytokinins is performed by cytokinin oxidases. They were
first discovered in tobacco and maize crude extracts that
showed cytokinin degrading enzyme activity (Burch and
Horgan 1989). Cytokinin oxidases selectively unsaturated
N6-isoprenoid side chain of the cytokinin to release the
adenine or adenosine (McGaw and Horgan 1983). They
can degrade free cytokinin bases and nucleosides and show
a certain substrate-specificity (Galuszka et al. 2007;
Kowalska et al. 2010). Cyclic or saturated side chains are
mostly resistant towards cytokinin oxidases degradation
(Hare and Van Staden 1994). Aromatic cytokinins are
degraded by cytokinin oxidase enzymes with low efficiency (Kowalska et al. 2010). Phenylurea-type cytokinins
were found to be strong inhibitors of cytokinin oxidase
activity (Laloue and Fox 1989). Overexpression of cytokinin oxidases genes in Arabidopsisas as well as in tobacco
led to a shift in source-sink relations (Werner et al. 2008).
Cytokinin oxidase genes have been studied in several plant
species, maize (Smehilova et al. 2009), tomato (Cueno
et al. 2012), wheat (Mameaux et al. 2012) and barley
(Mameaux et al. 2012). Another possibility to degrade
cytokinins is the deamination. Goble et al. (2011) identified
a cytokinin deaminase that deaminates N6-isopentenyladenine to isopentenylamine and hypoxanthine. Cytokinins are transported short distance via purine permeases
and equilibrative nucleoside transporters. The purine permease transporters were discovered in 2000 by Gillissen
and colleagues and displayed differential cytokinin affinities (Gillissen et al. 2000). Purine permease 1 and purine
permeases 2 were shown to transport energy-dependent
adenine transport with high affinity (Bürkle et al. 2003),
while the purine permeases transporters would cover the
low affinity transport (Cedzich et al. 2008). Intracellular
transporters specific for cytokinin have not been identified
up to now (Hirose et al. 2006). Long distance transport
Ind J Plant Physiol.
seems also to be important as shown by grafting experiments using cytokinin biosynthesis mutants and wild type
plants (Matsumoto-Kitano et al. 2008).
Role of cytokinins on gas exchange phenomenon
The first step of the Calvin cycle is the fixation of carbon
dioxide by rubisco, and plants that use only this ‘‘standard’’
mechanism of carbon fixation are called C3 plants, as the
first compounf of carbon fixation is a three-carbon compound, 3-phosphpglyceric acid (3-PGA). About 85% of the
plant species on the planet are C3 plants, including rice,
wheat, soybeans and all trees (Ueno et al. 2006). In C4
plants, the light-dependent reactions and the Calvin cycle
are physically separated, with the light-dependent reactions
occurring in the mesophyll cells (spongy tissue in the
middle of the leaf) and the Calvin cycle occurring in special cells around the leaf veins. These cells are called
bundle-sheath cells (Sage 2004). In C4 plant atmospheric
CO2 is first fixed in the mesophyll cells to form a simple,
4-carbon organic acid (oxaloacetate). This step is carried
out by a non-rubisco enzyme, PEP carboxylase, that has no
tendency to bind O2. Oxaloacetate is then converted to a
similar molecule, malate, that can be transported into the
bundle-sheath cells. Inside the bundle sheath, malate
breaks down, releasing a molecule of CO2. The CO2 is then
refixed by rubisco and made into sugars via the Calvin
cycle, exactly as in C3 photosynthesis. This process isn’t
without its energetic price, ATP must be expended to
return the three-carbon ‘‘ferry’’ molecule from the bundle
sheath cell and get it ready to pick up another molecule of
atmospheric CO2. However, because the mesophyll cells
constantly pump CO2 into neighboring bundle-sheath cells
in the form of malate, there is always a high concentration
of CO2 relative to O2 right around rubisco (Sage 2004).
The C4 pathway is used in about 3% of all vascular plants;
some examples are crabgrass, sugarcane, sorghum, pearl
millet and corn. C4 plants are common in habitats that are
hot, but are less abundant in areas that are cooler. In hot
conditions, the benefits of reduced photorespiration likely
exceed the ATP cost of moving CO2 from the mesophyll
cell to the bundle-sheath cell. A comparative analysis of
the leaf development in both monocot and dicot C3 and C4
species revealed that the close vein spacing in leaves of C4
plants is due to changes in the initiation frequency and
patterinng of the minor and not the major veins (Ueno et al.
2006; McKown and Dengler 2009). Since the molecular
events causing the initiation of veins are not even completely understood in C3 model plants, it is presently
challenging to predict the changes that led to the C4 typical
leaf anatomy. The activation of bundle sheath cells—the
enlargement of these cells and the increase in the number
of organelles in this tissue might be a secondary effect of
the higher vein density. Typically, the bundle sheath cells
of C3 plants possess only a few chloroplasts, and the
photosynthetic activity is low. With higher vein densities,
the ratio of bundle sheath to mesophyll cells increases.
Since only the mesophyll cells show high photosynthetic
activity, this would imply that the overall photosynthetic
activity of a leaf with a given size decreases. Extant C3-C4
intermediate species possess a photorespiratory glycine
(Gly) shuttle that pumps CO2 into the bundle sheath cells
(Bauwe 2010). This is achieved by restricting the Gly
decarboxylation reaction to the bundle sheath mitochondria, thus all Gly produced by photorespiration in the
mesophyll has to be transferred to the bundle sheath cells
for further processing. The Gly shuttle affects photosynthetic CO2 fixation in two ways. All photorespiratory CO2
is set free inside the leaf far apart from the outer surface.
Therefore it has to diffuse through several cell layers,
before it could escape from the leaf. This enhances the
plant’s chances of refixing the photorespired CO2 and
minimizes the loss of carbon due to photorespiration. In
some C3-C4 intermediate species this refixation capacity is
supported by the spatial distribution of the organelles
within the bundle sheath cell, since the mitochondria
concentrate adjacent to the vascular bundles (Rawsthorne
et al. 1988). Additionally, the Gly shuttle enhances the CO2
concentration within the bundle sheath cells. As a consequence, the carboxylation activity of Rubisco in the bundle
sheath cells increases, while its oxygenase reaction is
outcompeted (Bauwe 2010). It is assumed that the establishment of such a photorespiratory CO2 pump is an
important intermediate step on the way toward C4 photosynthesis. A photorespiratory CO2 pump can easily be
accomplished at the molecular level. The expression of
only one gene, encoding a subunit of the Gly decarboxylase
multienzyme complex, had to be restricted to the bundle
sheath cells. This might have been achieved through relatively subtle changes in the cis-regulatory elements that
control the expression of these genes (Akyildiz et al. 2007).
Some plants that are adapted to dry environments, such as
cacti and pineapples, use the crassulacean acid metabolism
(CAM) pathway to minimize photorespiration. This name
comes from the family of plants, the Crassulaceae, in
which scientists first discovered the pathway. Instead of
separating the light-dependent reactions and the use of CO2
in the Calvin cycle in space, CAM plants separate these
processes in time. At night, CAM plants open their stomata, allowing CO2 to diffuse into the leaves. This CO2 is
fixed into oxaloacetate by PEP carboxylase (the same step
used by C4 plants), then converted to malate or another
type of organic acid. The organic acid is stored inside
vacuoles until the next day. In the daylight, the CAM plants
do not open their stomata, but they can still photosynthesis.
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That’s because the organic acids are transported out of the
vacuole and broken down to release CO2, which enters the
Calvin cycle. This controlled release maintains a high
concentration of CO2 around rubisco.
From the literature it is apparent that cytokinins regulate
the synthesis of pigments and structural proteins necessary
for the formation of the chloroplast thylakoid system and of
the photosynthetic system, and also act as respiration stabilizers (Srivastava 2002; Taiz and Zeiger 2009). One of
the changes that occur during leaf senescence is a rapid
decline in photosynthesis, and can act as a senescence
induction signal, though this theory has not been proven.
Since sugars are primary products of photosynthesis, sugar
concentrations may be part of the signaling system, as high
levels of sugars repress the expression of genes associated
with photosynthesis, through a negative feedback system of
the final product (Quirino et al. 2000). Photosynthesis is a
physiological process essential to the survival of plants.
Increasing the photosynthetic efficiency has been a widely
used resource for improving the production of crops. From
a physiological point of view the agricultural practice aims
to maximize the photosynthetic efficiency of crops and to
canalize its products towards productivity and quality (Ort
et al. 2012). According to Foyer and Galtier (1996), productivity is influenced by morphological and physiological
characteristics of the photosynthetic organs (source) and of
the organs that consume photosynthesized products (sink).
The entire production of biomass depends on the photosynthetic activity of the source, however, the CO2 assimilation is just one of the factors that influence plant
development. In the photosynthetic process, CO2 is converted to 3-phosphoglyceric acid (3-PGA) and glyceraldehyde 3-phosphate (GAP), leading to the production of
terpenes, fatty acids, and particularly to the biosynthesis of
sugars, which represents more than 80% of the photoassimilates (Melis 2013). Regarding the limiting factors of
photosynthesis, this process is limited by the rate of diffusion of CO2 through the stomata and by the ability to
convert light energy into chemical energy and to transform
the CO2 into sugars. The diffusion of CO2 through the
mesophyll (gm) has some physical barriers, like, cell walls,
lipid membranes, cytoplasm, stroma and air, which vary for
each leaf (type and size) (Flexas et al. 2012). It is known
that plants have the ability to modify their growth habit in
response to changing environmental conditions, the light
being one of the most important. However, there may be
acclimatization, which can take days to weeks and aims to
maximize the photosynthetic capacity (Raines et al. 2012).
Plants can move their chloroplasts to places in the cytosol
where the light intensity is more profitable, thus allowing
greater efficiency of photosynthesis. Chloroplasts can also
move away from places where the incidence of light is very
strong, thus preventing excess photo-oxidative damage
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(Wada 2013). Mature chloroplasts of active photosynthetic
cells produce starch in the light period, using fixed carbon
and energy (ATP). A part of the carbon fixed in the day is
remobilized during the dark period (night) to meet the
metabolic demand. The long-term storage occurs in the
amyloplasts of reserve organs (Bahaji et al. 2013).
Photosynthesis is reduced under low cytokinin ratio due
to impaired synthesis of RuBisCo (Buchanan et al. 2001).
It is noteworthy that for higher photosynthesis high stomatal conductance is of dire need to allow an increase in the
fixation of CO2 per unit of leaf area (Blum 1980; Raines
et al. 2012). To maximize carbon gain, the stomata respond
to environmental factors in order to meet the CO2 demand
of photosynthesis. While there is CO2 intake, stomata also
allows water vapor loss to the atmosphere through transpiration. This makes it essential to have a tight control on
the stomatal opening, preventing excessive loss of water by
the plant, or CO2 deprivation, because the water-use efficiency (WUE) is one of the determining factors in the
production of plants (Blum 1980). This control is achieved
by the sensitivity of the guard cells to environmental and
endogenous signals (light, temperature, humidity, CO2,
internal CO2 concentration in the substomatal chamber,
cell solutes, specific ions, pH and abscisc acid). The
increase in transpiration rate (E) or stomatal opening by
cytokinins has been reported in leaves of some plant species (Pospı́šilová and Dodd 2005). Changes in the relationships between source and sink can affect the
productivity of plants, as there may be a reduction in the
number and size of sink organs. The hormonal balance can
influence the regulation of source-sink relationships, and
the plant metabolism (Rui-Ming et al. 2013). The xylem
tracheary elements, together with cytokinins, can replace
leaf primordia in inducing vascular connections in stems,
besides inducing the formation of new vascular components from parenchyma cells, thus influencing the
translocation of photoassimilates (Schmülling et al. 2011).
The application of cytokinins has positive effects on the
growth and yield of plants by inducing the activity of
sources and sinks, as it increases the strength of sinks,
stimulate growth and increases capacity of sucrose utilization by regulating sucrolytic enzymes. In addition to
increasing the photosynthetic activity of the source, it also
delays the senescence of leaves and increases the leaf area
(Rui-Ming et al. 2013). Schippers et al. (2007) reported that
the reduction in the endogenous levels of cytokinin may
signal the beginning of leaf senescence, and exogenous
applications of this hormone can delay this process, since
in addition to the relationship with the gene signaling of the
senescence, this hormone also participates in the regulation
of auxin and sugars, besides the photosynthesis maintenance. Another variable that has been improved in plants
by applying cytokinin is the intracellular CO2 pressure and
Ind J Plant Physiol.
the quantum efficiency of the PS II photochemistry. Photosynthesis allows plants to use sunlight to generate sugars
from CO2 via the Calvin cycle (Wu et al. 2012).
Role of cytokinins in regulating senescence
Cytokinin effects have been shown in many species,
resulting in re-greening of yellowing. Much of the evidence
supporting the role of cytokinin as an endogenous negative
regulator of senescence has come from studies which
examined changes in cytokinin content and the expression
of cytokinin metabolism genes during senescence in leaves
(Zwack et al. 2013). Work in numerous species has indicated a strong correlation between decreased leaf cytokinin
content and the onset and progression of senescence (Singh
et al. 1992; Zwack et al. 2013). Cytokinin synthesized in
roots is transported into leaves through the transpiration
stream. It has been found that the amount of cytokinin in
the xylem of Glycine max rapidly decrease with the onset
of senescence (Noodén et al. 1990). Similarly, a sorghum
cultivar exhibiting delayed leaf senescence had a greater
abundance of cytokinin in its xylem sap as compared with a
normally senescing cultivar (Ambler et al. 1992). Cytokinin in leaves may also be the product of local synthesis.
The process of senescence is highly regulated and dependent upon concurrent increases in both synthesis and
activity of some proteins as well as degradation or inactivation of others. Precise regulation of senescence is crucial
because in preparation for cellular death, the valuable
nutrients and energy released by the breakdown of
macromolecules during this process are reallocated to the
rest of the plant for growth or storage (Hörtensteiner and
Feller 2002). The concentration of citokinin in plants can
vary depending on the organ, the plant development status
and the environmental conditions. According to Coll et al.
(2001), cytokinin in levels can be affected by light and
temperature. In general, the largest concentrations of
cytokinins are found in meristematic regions or in growing
organs with high rate of cell division, such as young leaves,
developing seeds, fruits and roots. The apical root meristem, however, is the primary site of synthesis of cytokinins
in plants and these are translocated via the xylem to the
plant shoot; when they are in the leaves, they are relatively
immobile (Coll et al. 2001; Taiz and Zeiger 2009). Besides
roots, other parts of the plants can synthesize cytokinins,
such as the developing seeds, which have large cytokinin
activity. Another important function of the cytokinins is
inhibiting senescence by acting on protein synthesis,
decreasing the amino acid incorporation rate, slowing the
senescence process (Salisbury and Ross 1991). The role of
cytokins in delaying leaf senescence has been reported for
several plant species (Kim et al. 2006). Much of the
evidence supporting the role of cytokinin as an endogenous
negative regulator of senescence has come from studies
which examined changes in cytokinin content and the
expression of cytokinin metabolism genes during senescence. Work in numerous species has indicated a strong
correlation between decreased leaf cytokinin content and
the onset and progression of senescence (Singh et al. 1992;
Zwack et al. 2013). Cytokinin synthesized in roots is
transported into leaves through the transpiration stream; it
has been found that the amount of cytokinin in the xylem of
Glycine max rapidly decrease at the onset of senescence
(Noodén et al. 1990; Zwack et al. 2013). Transcriptome
analyses of Arabidopsis leaves demonstrated that expression of cytokinin biosynthetic genes greatly decreases
during senescence, while transcripts of cytokinin degrading
enzymes became more abundant (Buchanan-Wollaston
et al. 2005; Breeze et al. 2011). This suggests that cytokinin may delay leaf senescence not only as a result of
exogenous treatment, but also as part of an endogenous
developmental program. Although an antagonistic role of
cytokinin in leaf senescence is strongly supported in these
studies, many of them rely on correlations and do not
clearly demonstrate a causal relationship.
Regulation of genes related to photosynthesis
and senescence by cytokinins
Senescence is a highly regulated degradative process of
plant cellular and tissue structures. Delaying the senescence of source tissues (mainly leaves) would permit
greater capture of sunlight energy for an extended period,
allowing transformation into photosynthates which contribute to improved plant growth and enhanced seed yield.
Additionally, delayed senescence would allow source tissues to degenerate slowly, so that the stored photosynthates, metabolites, proteins and nutrients can be
systematically released and dispatched to corresponding
sink tissues. The benefits of delayed leaf senescence
include better maintenance of photosynthetic rate,
increased plant biomass, higher nitrate influx, increased
post-harvest life in flowers, enhanced drought tolerance
and higher seed yield (Rivero et al. 2007). A new era of
investigations in cytokinin physiology began with
heterologous expression of the Agrobacterium tumfaciens
adenosine phosphate-isopentenyltransferase gene, which
was transferred into plant cells during infection by A.
tumfaciens. The adenosine phosphate- isopentenyltransferase catalyzes the rate-limiting step of cytokinin
biosynthesis in plants; ectopic adenosine phosphateisopentenyltransferase expression in a wide variety of plant
species results in dramatic increases in endogenous cytokinin production (Loven et al. 1993). As constitutive
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expression using the cauliflower mosaic virus 35S promoter (CaMV 35S) severely limited regeneration of plants
due to cytokinin inhibition of root organogenesis, tissuespecific or inducible promoters allowing for targeted overproduction of cytokinin has been employed to varying
levels of success in many species (reviewed by Haberer
and Kieber 2002). Given the senescence delaying effects of
exogenous cytokinin treatment, it was expected that cytokinin overproducing plants would also display increased
leaf longevity (Lin et al. 2015). However, actual findings
were mixed with some plants showing delayed senescence
as expected, but many studies found no change or even
accelerated leaf senescence (Haberer and Kieber 2002;
Merewitz et al. 2011). It has been suggested that these
unexpected results were due to a cytokinin imposed shift in
sink and source identities of organs (Zhang et al. 2010).
Auto-regulatory loop specifically targeted cytokinin
increases in senescing cells, yet prevented over-accumulation. The senescence-associated gene 12:: adenosine
phosphate- isopentenyl transferasesystem has since been
incorporated in a number of important crop species
including: lettuce, rice, ryegrass, tomato, alfalfa, cauliflower, wheat, cassava, broccoli and cotton; all of which
demonstrated delayed leaf senescence (Wang et al. 2007).
The two-component cytokinin signal (TCS) pathway is
fairly well understood as a result of work done over the
past 15 years. It functions as a multi-step phospho-relay
involving hybrid histidine kinase receptors (HKs) and
downstream transcription factors (Gupta and Rashotte
2012). The first direct link between the TCS pathway and
senescence regulation came about with the characterization
of an Arabidopsis mutant with a delayed senescence phenotype, ore12, which turned out to be a gain of function
allele of the cytokinin receptor AHK3. Further investigation indicated that AHK3 specifically mediates the senescence-delaying response in leaves in a manner partially
dependent upon the phosphorylation/activation of the typeBRR Arabidopsis (ARR2) (Kim et al. 2006). It has since
been shown that plants expressing a proteolytic-resistant
version of ARR2 exhibit delayed dark-induced leaf
senescence (Kim et al. 2012). A similar phenotype was
observed in plants overexpressing the cytokinin inducible
transcription factor CRF6. CRF6 mutants were found to
have reduced sensitivity to the senescence delaying effects
of cytokinin (Zwack et al. 2013). While cytokinin response
factors (CRFs) have been shown to function as a side
branch of the TCS, this is one of the first functional roles in
a cytokinin regulated process directly linked to a CRF
protein—the first involving senescence (Rashotte et al.
2006). However, a further examination is required to
demonstrate that CRF6 and ARR2 could potentially function in complex to regulate transcriptional response to
cytokinin during senescence (Zwack et al. 2012). Another
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gene encoding an acyltransferase of unknown function
(At5g47980) has also been found in numerous microarray
studies, which is also regulated by cytokinin (Heyl et al.
2011). Interestingly, plants with a higher thalianol content
show a stunted shoot growth but have longer roots (Field
and Osbourn 2008), both phenotypic features reminiscent
of cytokinin-deficient plants (Werner et al. 2010). However, the exact role of thalianol in regulating root and shoot
growth and its possible interplay with cytokinin is
unknown. A function of cytokinin in regulating uptake and
metabolism of different nutrients–nitrogen, sulfate, phosphate, and iron—has been known for some time (Rubio
et al. 2009). The sulfate transporter (SULTR1:2) is
responsible for sulfate uptake into the roots, while the exact
role of the other two sulfate transporters, (SULTR3:1) and
(SULTR3:4), is not yet clear. The sulfate transporter 1:2
and sulfate transporter 1:1 were shown to be negatively
regulated by cytokinin in a partially CRE1/AHK4-dependent manner, associated with decrease in sulfate uptake
(Maruyama-Nakashita et al. 2004). The functions of the
phosphate transporters (PHT1:2 and PHT1:4) are not
restricted to phosphate uptake from the soil into the root,
but extend to broader roles in phosphate remobilization and
distribution throughout the whole plant.
Ten of the 19 genes assigned to the category primary
metabolism are involved in trehalose-6-phosphate metabolism. It has been shown that trehalose synthesis genes are
regulated by cytokinin in an opposite fashion than genes
encoding trehalose-degrading enzymes, supporting the idea
that trehalose-6-phosphate levels are regulated, at least
partly, by cytokinin (Brenner et al. 2005).
Role of cytokinins in modulating, enzymatic
and non-enzymatic antioxidants
Photosynthesis produces reactive oxygen species such as
superoxide (O-•
2 ), hydrogen peroxide (H2O2), hydroxyl
radicals (OH-) and singlet oxygen (1O2) (Asada and
Takahashi 1987). Singlet oxygen and hydroxyl radical can
cause major damage to the membranes and form lipid
peroxides derived from polyunsaturated fatty acids.
Hydrogen peroxide is the most potent inhibitor of the
assimilation of photosynthetic CO2 (Kiehl 2006). To minimize the deleterious effects of reactive oxygen species
(ROS) and modulate their quantity, aerobic organisms have
developed an antioxidant defense system, also known as
scavengers, being enzymatic and non-enzymatic. Non-enzymatic antioxidants includes a-tocopherol (vitamins E),
ascorbic acid (vitamins C), glutathione (GSH), b-carotene,
phenolics, and polyamines. The enzymatic antioxidants
involves superoxide dismutases, catalases, peroxidases,
glutathione peroxidase, ascorbate peroxidase, glutathione
Ind J Plant Physiol.
reductase and glutathione S transferase (Blokhina et al.
2003; Scandalios 2005). Along with other physiological
mechanisms, the antioxidant system efficiency increases
the plant’s tolerance capacity due to the generation of ROS.
Several studies claim that the apoplast, chloroplast, cytoplasm, mitochondria and peroxisome contain ROS scavenging mechanisms (Pignocchi and Foyer 2003). The
cycles involved in the ROS eliminating pathways of plants
are as follows: water-water cycle in chloroplasts including
superoxide dismutase; ascorbate–glutathione cycle in
chloroplasts, cytosol, mitochondria, apoplast and peroxisomes; glutathione reductase (GR) and catalase in peroxisomes (Delite 2007). During the photosynthetic light
reaction, there is photoreduction of dioxygen to water in
photosystem I (PS I) by the electrons generated in photosystem II (PS II), referred to as water-water cycle in
chloroplasts (Gratão et al. 2005). The functional significance of this cycle is the elimination of O-•
2 and H2O2 from
their generating sites, minimizing the possibility of production of OH and its interaction with molecules present in
the chloroplasts (Asada 2000). Under abiotic and biotic
stresses, mitochondria may be damaged by oxidative stress,
for being susceptible to the oxidative inhibition of its
functions (Taylor et al. 2003). To prevent the inhibition of
enzymes in the Calvin cycle, it is essential to remove the
H2O2 that is produced in the chloroplast (Willekens et al.
1997). Another result of the oxidative stress is the proliferation of peroxisomes, containing an effective system for
the removal of ROS, especially H2O2 (Igamberdiev and
Lea 2002). Like the chloroplasts and mitochondria, the
plant peroxisomes have two sites of generation of O-•
2
anion (one in the organelle matrix and another in the
NADPH-dependent peroxisome membranes) (del Rı́o et al.
2002). The primary enzyme against damage caused by
ROS in cells is known as superoxide dismutase (SOD; EC:
1.15.1.1) (Alscher et al. 1998). This enzyme catalyzes the
dismutation reaction of the superoxide anion into oxygen
and hydrogen peroxide. Superoxide dismutase is a group of
metalloenzymes, viz., Cu–Zn–SOD, Fe–SOD and Mn–
SOD, which catalysis the formation of H2O2 from O-•
2 ,
thus freeing cells from the risk of oxidation by these radicals (Scandalios 2005). These enzymes are the only ones
whose activities interfere with the concentrations of O-•
2
and H2O2, which in the Haber–Weiss reaction produce
hydroxyl radical (Alscher et al. 1998). Catalase (CAT; EC:
1.11.1.6) is the only H2O2 scavenging enzyme that does not
consume equivalent cell reductants, having an efficient
mechanism for the removal of the H2O2 formed in cells
under conditions of stress (Scandalios 2005), and found in
the mitochondria, peroxisomes and glyoxysomes of plants,
active in the decomposition of H2O2 (Mallick and Mohn
2000). Catalase can be found in all living organisms,
depending on the concentration of hydrogen peroxide it can
perform peroxidative and catalytic actions. The most
important enzyme for the detoxification of H2O2 in plant
cells is the ascorbate peroxidase (APX; EC: 1.11.1.1)
(Mehlhorn et al. 1996). The ascorbate peroxidase is an
enzyme that catalyzes the substrate oxidation concomitantly to the reduction of H2O2 to H2O (Mehlhorn et al.
1996; Noctor and Foyer 1998). It is a reaction in which two
molecules of ascorbate are oxidized to reduce the H2O2
molecule to water, and is involved in the detoxification of
H2O2 both within the cell and in the apoplast (Zheng and
Van huystee 1992). It is a constituent of the ascorbate–
glutathione cycle or Foyer-Halliwel-Asada cycle, being an
efficient way for plant cells to eliminate H2O2 in cellular
compartments (Halliwell and Gutteridge 2001). Maintenance of protective activity of these scavenging enzymes
by regulating the genes controlling their activities, especially in chloroplasts, may delay senescence (Peñarrubia
and Moreno 1995). The intimate relationship between the
antioxidant activity and the stress tolerance has also been
identified in crops such as corn (Zeamays L.) (Song et al.
2016) and tobacco (Nicotiana tabacum) (Perl et al. 1993).
Cytokinins can also participate in the removal of ROS from
the cell and delay senescence by slowing down decomposition of macromolecules, principally those that are components of photosynthetic apparatus (Koeslin-Findeklee
et al. 2015; Chang et al. 2016). The opposite effects of
ROS and cytokinins on the integrity of cell biomolecules
and senescence imposes the question how cytokinins affect
the concentration of ROS. There is less information on
differential responses of wheat cultivars to leaf senescence
influenced by water stress during grain filling (Mohammadi
and Moradi 2016). As a possible direct effect of cytokinins
could be their effect on the activity of antioxidant enzymes,
including SOD (Stopariã1 and Maksimoviã 2008). While
studying the effects of cytokinins, such as zeatin and
benzyl adenine on senescence, these were found to increase
the activity of some antioxidative enzymes (SOD, CAT),
and therefore delay senescence of the plant tissue (Liu and
Huang 2002). Leshem et al. (1981) showed that cytokinin
inhibit the activity of xanthine oxidase, an enzyme that is
one of the generators of ROS in the cell. The senescence
was also delayed by reduction in lipoxygenase activity
induced by cytokinins, thus contributing to preserve the
integrity of cell membranes. As the biosynthesis of cytokinin is stimulated when environmental conditions are
favorable for plant growth and development, it is highly
probable that binding of cytokinin to specific receptors in
the cell membranes induces the production of a signal that
triggers the synthesis of enzymes that allow plants to utilize
as much as possible favorable environmental conditions
(Stopariã1 and Maksimoviã 2008). In addition, under
favorable environmental conditions, accompanied by
higher cytokinin content, the need for antioxidant enzymes
123
Ind J Plant Physiol.
is reduced. On the contrary, He et al. (2005) observed that
inhybrid corn exhibiting delayed senescence, an increase in
cytokinin content is accompanied with an increase in SOD
activity. Liu and Huang (2002) observed an increase in
SOD activity following addition of zeatin-riboside to the
rhizosphere of the grass Agrostis palustris, which was
exposed to combined stress provoked by high temperatures
of the soil and the air. Durmus and Kadioglu (2005) treated
maize leaves with 2.5 and 25 mg benzyl amino purine
(BA) dm-3 and recorded an increase in the activity of SOD
in plants treated with paraquat 8 h after the BA treatment,
but if paraquat was applied 12 or 24 h after BA there was
no increase in the activity of SOD. The variable effects of
different cytokinin on the activity of SOD can be explained
by the fact that the activity depends, among the other
factors, on the plant and tissue age, complexity of environmental factors, partitioning between enzymatic and
non-enzymatic antioxidants in the plant, and on the nature
and intensity of the eventual stress factor(s) (Stopariã1 and
Maksimoviã 2008).
Role of cytokinin on regualion of cell-wall
invertase
The downstream mechanism of cytokinin induced delay in
leaf senescence is not fully understood, though it is widely
thought to involve the regulation of sink/source relation
(Thomas 2013). The influence of cytokinin on sink/source
relations is exerted in part by regulation of cell-wall
invertase (CWINV) activity. The cell-wall invertase
enzyme is secreted and ionically bound to cell walls, where
it catalyzes the cleavage of sucrose into hexose monomers
(Zwack et al. 2013). Because sucrose diffuses passively
through the phloem, the rate of its metabolism at the site of
unloading is a major determinant of sink strength (Jin et al.
2009). A cytokinin-induced increase in invertase activity
was first demonstrated in calli from Cichorium intybus
(Lefebvre et al. 1992). It was later shown that a similar
increase specifically of CWINV in the cultured cells of
Chenopodium rubrum and leaves of tomato (Solanum
lycopersicum) was due to induced gene expression (Ehness
and Roitsch 1997). Importantly, a coordinated increase was
also observed in hexose transporter expression, which is
required for uptake of the products of the invertase reaction
into cells (Ehness and Roitsch 1997). A link between
cytokinin induced CWINV and delayed leaf senescence
was first observed in an analysis of tobacco senescenceassociated gene 12:: adenosine phosphate- isopentenyltransferase lines, where it was found that the long-lived
leaves of these plants had unusually high levels of CWINV
activity. It was further demonstrated that plants expressing
a proSAG12::CWINV transgene exhibited delayed leaf
123
senescence, as did specific tissue regions in which an
inducible CWINV construct was expressed in a localized
manner. Moreover when a CWINV inhibitor protein was
expressed under a cytokinin inducible promoter, treatment
with the hormone no longer resulted in delayed senescence
(Balibrea Lara et al. 2004). Similar results were obtained in
a later study where activity of CWINV in tomato leaves
was increased by the silencing of its inhibitor (Jin et al.
2009). Together these works demonstrate that the induced
expression/activity of CWINV which occurs naturally in
response to cytokinin is both necessary and sufficient to
cause a delay in leaf senescence. This is a highly significant
point as it provides both a physiological link between
senescence regulation and primary metabolism as well as at
least a partial mechanism by which senescence is delayed
by cytokinin.
Molecular mechanism of cytokinin actions
in relation to photosynthesis
Role of the plant hormone cytokinin in regulating the
development and activity of chloroplasts was described
soon after its discovery as a plant growth regulator more
than 50 years ago. Its promoting action on chloroplast
ultrastructure and chlorophyll synthesis has been reported
by various workers, especially during etioplast-to-chloroplast transition. Recently a protective role of the hormone
on the photosynthetic apparatus during high light stress has
been shown. Details about the molecular mechanisms of
cytokinin action on plastids have emerged from genetic and
transcriptomic studies (Sugiyama 2014). The cytokinin
receptors AHK2 and AHK3 are mainly responsible for the
transduction of the cytokinin signal to B-type response
regulators, in particular ARR1, ARR10, and ARR12, which
are transcription factors of the two-component system
mediating cytokinin functions. Additional transcription
factors linking cytokinin and chloroplast development
include CGA1, GNC, HY5, GLK2, and CRF2. One of the
challenges of research is to identify biochemical
site(s) regulating the N-responsible accumulation of cytokinin in roots and to understand the molecular mechanism
underlying. Presently it is not possible to explain as to what
is the real molecular species of cytokinin for transcription
of C4 genes. It has been widely assumed that cytokinin are
transported by transpiration stream toward the leaf in the
form of cytokinin-nucleoside. The transport process may
be complicated as is predicated by the evidence that suggest that cytokinin are metabolized and compartmentalized
in such a way that they are unavailable (Sugiyama 2014).
With regard to its compartmentalization, for example,
cytokinin nucleotides are the predominant form in the
xylem. This suggests that the nucleotides may be the form
Ind J Plant Physiol.
Fig. 1 Scheme of inorganic
N-mediated gene regulation for
C4 photosynthesis. Compounds
in hatcted boxes and enzyme
underlined represent internal
signals of inorganic N and genes
of enzymes, which are upregulated by nitrate,
respectively
of cytokinins transported in the xylem. Little is known
about the role of cytokininis in root to leaf signal. This
would allow the C4 plants to coordinate the photosynthesis
capacity with the availability of external inorganic
N-sources. It is interesting to speculate that the leaves
transport some signal toward the roots where cytokinin are
produced. In this context it has been demonstrated using
grafiting technique with pea mutant rms4 that shoots may
transmit a signal to roots and thereby may control process
involved in the regulation of cytokinin biosynthesis in roots
(Satoh and Murata 2012). Novel plant protein CIPI has
been assigned as a signaling component between cytokinin
and transcription of C4PEPC gene (C4Ppcl), carbonic
anhydrase (CA) and pyruvate orthophosphate dikinase
(PPDK) and a phosphorylation and dephosphorylation
system of protein between glucose insensitive (Gin) and
transcription and/or posttranscription of the genes. Important questions on the novel plant protein, CIPl, remain to be
answered with regard to the cellular and sub-cellular
location and the function in transcription of the genes. In
the scheme illustrated in Fig. 1, we assign phosphorylation/
dephosphorylation of protein as a signaling, component in
the Gin-mediated posttranscriptional regulation of the
C4Ppcl mRNA. This idea is supported by evidence that the
accumation of C4Ppcl-mRNA was totally blocked by
okadaic acid, an inhibitor of 2A type protein-phosphatase,
while the cytokinin-mediated transcription of C4Ppcl was
not inhibited by the inhibitor (Satoh and Murata 2012). Gin
and/or its metabolite have been shown to act as a signal in
exactly opposite manner to NR (nitrate reductase) expression in tobacco and squash. In maize leaves, NR levels
increase preceding an increase in the accumation of C4Ppcl
when nitrate is supplied to N-starved plants (Sugiyama
2014). This predicated that the level of NR mRNA would
accumulate earlier than a rise in Gin levels, which, in turn,
would cause the inhibition of NR gene expression after
supplying nitrate to N-starved plants. Such a reciprocal
function of Gin as signal may allow plants to regulate N
partition into C and N assimilation systems in response to
the availabity of inorganic N-sources.
Occurrence of phosphoenolpyruvate carboxylase (PEPC)
is ubiquitous, distributed widely in photosynthetic and
nonphotosynthetic tissues of higher plants, green algae,
bacteria, protozoa and legume root nodules and apparently
absent in animal tissues, yeast or fungi (Izumi et al. 2004).
The activities of PEPC in leaves of C3 plants are about
2–5% of that found in C4 plants (Latzko and Kelly 1983).
The enzyme is confined to the cytoplasm of mesophyll cells
in C4 and CAM plants. In C3 plants, PEPC may be localized
in both cytosol and chloroplasts of the leaves. Thus, PEPC is
considered as a typical marker enzyme for cytosol and for
C4 mesophyll cells. PEPC has many faceted physiological
roles in plants (Latzko and Kelly 1983), which are distributed among several isoforms with different catalytic and
regulatory properties including, important roles in the photosynthesis of C4 and CAM plants, supplying carbon to N2
fixing legume root nodules, and maintaining cellular pH.
The biosynthesis of PEPC in leaves of C3 and C4 plants is
highly regulated by the availability and source of nitrogen
(Murchie et al. 2000). The studies cited above mostly
focused on the cytokinin effect on pigment and protein
levels and enzyme activities. Recent studies have revealed
that cytokinin alters transcript levels of specific genes of the
tetrapyrrole biosynthesis pathway during de-etiolation.
Cytokinin increases the steady state mRNA levels of the
HEMA1, CHLH, and CHL27 genes in etiolated Arabidopsis
seedlings (Tanaka et al. 2011). The regulation of these and
additional chlorophyll synthesis genes (GSA1, GUN4,
CHLM) by cytokinin was shown to be reduced in AHK2
AHK3 cytokinin receptor mutants. This coincided with a
decreased greening rate and lack of increased GluTR protein
levels in response to cytokinin treatment, which indicated
the stimulating effect of cytokinin on chlorophyll biosynthesis during de-etiolation is mediated by the AHK2 and
123
Ind J Plant Physiol.
AHK3 receptors. Similarly to AHK2 AHK3 mutants, the
cytokinin-dependent induction of some chlorophyll biosynthesis genes was lowered in the ARR1 ARR12 mutants,
suggesting participation of ARR1 and ARR12 in regulating
these genes (Cortleven et al. unpublished). Several studies
reporting the transcriptomic response to cytokinin have been
published, including three meta-analyses analysing and
summarizing the outcome of these studies (Bhargava et al.
2013). A number of the cytokinin-regulated genes linking
the hormonal activity to chloroplast function have been
identified in this way. However, among all the genes regulated by cytokinin, there are only a few that appear to have a
role in regulating chloroplast function. It has been suggested
that cytokinin metabolism and signalling genes have been
delivered through the endosymbiont pathway via horizontal
gene transfer from cyanobacteria, the plastids’ ancestors
(Gruhn and Heyl 2013). Interestingly, this scenario would
imply that after transfer of the cytokinin genes from the
plastid genome to the nuclear genome, they would have
been adapted to regulate development and function of their
place of origin, the plastids. Currently, however, the evolutionary path of the cytokinin genes has not been traced
back unequivocally to a cyanobacterial origin (Gruhn and
Heyl 2013). The earliest traces appear before the landfall of
plants and the complexity of the cytokinin system has
increased during the development of modern land plants
(Gruhn and Heyl 2013). A large number of studies documenting the influence of cytokinin on plastid-related nuclear
genes have been cited in an earlier review describing cytokinin-regulated gene expression. For example, CAB,
encoding chlorophyll a binding proteins of photosystem II,
and genes encoding both the small and large subunit of
RubisCO (RBCS/RBCL) were identified in several species
(tobacco, cucumber, Arabidopsis) to be strongly upregulated
by cytokinin (Chory et al. 1994). Genome-wide transcript
analyses documenting the influence of cytokinin on gene
expression, which has been performed primarily in Arabidopsis, but also in Oryza sativa and other species such as
Medicago trunculata, Brassica oleracea, and Populus (Liu
et al. 2013), identified additional cytokinin-regulated
chloroplast-related genes. One other example is the induction of a gene encoding oligogalactosyldiacylglycerol synthase, an enzyme involved in the synthesis of galactolipids,
more specifically of monogalactosyldiacylglycerol and
digalactosyldiacylglycerol, key components of the thylakoid
membranes. A connection between cytokinin and the formation of these galactolipids had been reported by Yamaryo
et al. (2003) in cucumber. To date, few studies have
investigated the effect of cytokinin on the plants’ proteome.
Lochmanová et al. (2008) studied the proteomic changes
during cytokinin-induced photomorphogenesis in darkgrown Arabidopsis. They reported that even a modest
increase in the endogenous cytokinin content (\2-fold)
123
resulted in the upregulation of 37 proteins identified by
MALDI-TOF MS and/or LC–MS/MS. Chloroplast proteins
involved in photosynthetic processes or chloroplast biogenesis represented a major fraction (26%) of the cytokinininduced proteins. These proteins included the gamma-subunit of ATP synthase, glyceraldehyde-3-phosphate dehydrogenase, ATP-dependent Clp proteolytic subunit, and
ribosomal protein L21. There was only a small overlap with
those proteins identified previously to be induced during
photomorphogenesis. Černý et al. (2011) described a rapid
cytokinin impact on the proteome and the phosphoproteome
in 7-day-old Arabidopsis seedlings. Only 15 min after
cytokinin treatment, significant changes were seen in 53
spots of the proteome and 31 spots of the phosphoproteome.
These changes were mainly in the range of 1.3- to 2-fold,
which is much smaller than those seen on the transcript
level, but they were consistently obtained with different
cytokinins and a large part was absent or reduced in cytokinin receptor mutants. A relevant role of cytokinin with
respect to photosynthesis that is only rarely considered is its
protective role of the photosynthetic apparatus under light
stress. It is known, for example, that cytokinin prolongs
antioxidant-based protection in chloroplasts resulting in an
extension of their life span (Procházková et al. 2008). A
detailed study on the protective function of cytokinin during
high light stress reported that plants with a lower cytokinin
status show increased photoinhibition (Cortleven et al.
2014). This was caused by a higher degree of photodamage
and reduced efficiency of the photoprotective scavenging
system. The protective function of cytokinin during light
stress was dependent on the AHK2 and AHK3 receptors and
the transcription factors ARR1 and ARR12.
Acknowledgements The authors acknowledge NationalCouncil for
Scientific and Technological Development (CNPq) and Fundação de
Amparo a Ciência e Tecnologia de Pernambuco (FACEPE/APQ0053-5.01/14, DCR-0093-5.01/13) for the financial support to this
work.
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