Journal of Plant Physiology 229 (2018) 32–40

Contents lists available at ScienceDirect

Journal of Plant Physiology

journal homepage: www.elsevier.com/locate/jplph

Review article

Phytohormones as targets for improving plant productivity and stress T

tolerance
⁎
Joanna Ciura, Jerzy Kruk
Department of Plant Physiology and Biochemistry, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Gronostajowa 7, 30-387, Kraków,
Poland

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

Keywords: In this review, we summarize the results of experiments that lead to altered levels of phytohormones in trans-
Plant growth regulators genic plants to improve plant productivity. The available data indicate that manipulating the level of phyto-
Phytohormones hormones might also be a promising way to enhance the environmental stress tolerance of crop plants. In the
Stress tolerance regulation of the level of phytohormones, both biosynthesis and their catabolism pathways can be targeted for
Transgenic plants
engineering purposes. Moreover, the signaling pathways of phytohormones should explored in this respect. In
genetic modifications, conditional promoters must be developed to avoid undesired effects on growth. In order
to find a practical application, the effects of genetic modifications should be further verified under field con-
ditions and over a longer time scale.

1. Introduction transduction pathways of phytohormones. In this review, we present

Plant productivity, yield and resistance to environmental stresses
are currently the main points of interest for agriculture and plant bio-
technology. Biotic and abiotic stresses cause huge losses in crop yield.
An increasing human population and food demand necessitate the
creation of plant varieties with improved traits. One of the approaches
for achieving this goal is the metabolic engineering of phytohormones
(Bartwal et al., 2013; Wani et al., 2016).
Phytohormones (plant growth regulators) are compounds that act at
very low concentrations and regulate various cellular processes and
plant responses to changing environmental conditions (Fahad et al.,
2015; Wani et al., 2016). The plant hormones that have been most
investigated include cytokinins (CK), auxins (Aux), gibberellins (GA),
abscisic acid (ABA), ethylene (ET), brassinosteroids (BR) and jasmo-
nates (JA). Representative examples of plant hormone groups are
shown in Fig. 1. It is traditionally assumed that JA and ET are involved
in plant defense, while Aux, CK, GA and BR are associated with plant
development. ABA is the key hormone that regulates plant responses to
abiotic stresses (Kazan, 2015). Therefore, the engineering of phyto-
hormones might be a promising tool for biotechnologists to improve
plant productivity and stress tolerance. The level of phytohormones is
affected both by anabolic (biosynthesis) and catabolic pathways. En-
zymes of both pathways have been used as targets in transgenic ap-
proaches (Fig. 2). Other potential targets are components of the signal
the results of experiments that focus on the engineering of phyto-
hormones that lead to elevated plant productivity and stress resistance,
as well as reports that take advantage of phytohormone mutants when
investigating the stress tolerance of crop plants.
2. Manipulation of the level of phytohormones as a way of
improving plant productivity and resistance to stress
During their lifetimes, plants are exposed to multiple environmental
stresses, both abiotic and biotic, influencing their growth and devel-
opment, which also affects their productivity. Among abiotic factors,
the most important are climatic factors, including water availability,
light intensity, temperature or others (e.g. salinity). Biotic factors, i.e.
interactions of other organisms, could have a beneficial influence on
plant growth, such as symbiosis, but also negative effects, such as
herbivory, pathogen infection or allelopathy. In response to these fac-
tors, plant growth regulators play a crucial function. Phytohormones
regulate the majority of processes associated with growth, development
and response to external stimuli, and thus the targeted control of hor-
mone biosynthesis, metabolism and signaling could significantly affect
plants’ productivity.
Below, we describe examples of experiments that lead to an altered
level of phytohormones, especially in crop plants, and the results of
these manipulations, which are intended to enhance stress tolerance,

⁎
Corresponding author.
E-mail addresses: joanna_ciura@o2.pl (J. Ciura), jerzy.kruk@uj.edu.pl (J. Kruk).

https://doi.org/10.1016/j.jplph.2018.06.013
Received 16 February 2018; Received in revised form 15 May 2018; Accepted 11 June 2018
Available online 09 August 2018
0176-1617/ © 2018 Elsevier GmbH. All rights reserved.
J. Ciura, J. Kruk
Fig. 1. Structure of representatives of the main groups of phytohormones.
improved yield and productivity.
2.1. Cytokinins
CK regulate a number of aspects of plant growth and development,
such as cytokinesis, cell differentiation, growth, quiescence, and the
transport of assimilates or senescence. These phytohormones are also
involved in abiotic stress responses. Therefore, they have been long
considered to be connected with plant yield and productivity. The main
biotechnological targets are genes involved in CK synthesis (isopentenyl
transferase IPT) and metabolism (cytokinin oxidase/dehydrogenase
CKX, glucosyltrasferases).
Adenosine phosphate-isopentenyl transferase (IPT) is the key en-
zyme in CK biosynthesis and catalyzes transfer of the isopentenyl
moiety of dimethylallyl pyrophosphate or 1-hydroxy-2-methyl-2-(E)-
butenyl 4-diphosphate to ATP, ADP or AMP. The isopentenyl-ATP,
-ADP and -AMP that form are the precursors of biologically active CK
(Zalabák et al., 2013). Irreversible degradation of CK is catalyzed by
cytokinin oxidase/dehydrogenase CKX, cleaving N6 side chain of CK,
which results in the formation of adenine (or its corresponding deri-
vative of N9 - substituted CK) and the unsaturated aldehyde 3-methyl-2-
33
Journal of Plant Physiology 229 (2018) 32–40
Fig. 2. Target genes of phytohormones anabolism (green) or cat-
abolism (red) whose expression was modified in transgenic ap-
proaches. AAO, aldehyde oxidase; ACC, 1-aminocyclopropane-1-
carboxylic acid; ACD, 1-aminocyclopropane-1-carboxylate dea-
minase; CKX, cytokinin oxidase/dehydrogenase; DWF4/DWARF4,
gene encoding steroid 22α-hydroxylase (CYP90B1); GA20ox, GA
20-oxidase; GA2ox, GA 2-oxidase; GA3ox, GA 3-oxidase; GH3,
proteins responsible for conjugation of Aux to amino acids; iaaM,
bacterial gene encoding tryptophan monoxidase; IPT, isopentenyl
transferase; JMT, jasmonic acid carboxyl methyltransferase; LOS5,
molybdenum cofactor required for AAO activity; 13-LOX, 13-li-
poxygenase; NCED, 9-cis-epoxycarotenoid dioxygenase; NIT, ni-
trilase converting indole-3-acetonitrile to IAA; SDR, short-chain
alcohol dehydrogenase/reductase; tms1, agrobacterial gene en-
coding tryptophan monooxygenase; UGT, UDP-glycosyl-
transferase; YUC, gene encoding enzyme converting tryptamine to
N-hydroxyl-tryptamine; ZEP, zeaxanthin epoxidase.(For inter-
pretation of the references to colour in this figure legend, the
reader is referred to the web version of this article.)
butenal. CKX have been found in many plant species and have a high
level of sequence homology (Frébort et al., 2011). In Arabidopsis, seven
CKX members have been identified. AtCKX1 and AtCKX3 are vacuolar,
while AtCKX2 is an extracellular protein (Werner et al., 2003).
CK activity can also be affected by their conjugation with sugar or
alanine moieties. Glycosylation of CK is catalyzed by UDP-glycosyl-
transferase (UGT). The most common types of CK glycosylate are O- and
N-glycosides at positions 7 and 9 in the purine ring (Zalabák et al.,
2013). Glycosyltransferases are a large group of enzymes which re-
cognize various substrates. In Arabidopsis, only five UGT are able to
glucosylate CK: UGT76C1 and UGT76C2 glucosylate CK at the N7 and
N9 positions, UGT85A1, UGT73C5, and UGT73C1 form the O-gluco-
sides of trans-zeatin and dihydrozeatin (Hou et al., 2004). Less common
is conjugation with alanine at N9 position of adenine moiety, whose
products are characterized by low activity because of the absence of
those enzymes responsible for the hydrolysis of conjugates to the active
form (Bajguz and Piotrowska, 2009).
CK have been found as key factors in the regulation of plant se-
nescence. Controlling the senescence is one of the strategies for im-
proving a plant’s yield and extend vitality. Gan and Amasino (1995)
were the first to use the senescence-specific promoter, SAG12, from
J. Ciura, J. Kruk Journal of Plant Physiology 229 (2018) 32–40

Table 1
Application of transgenic plants with altered phytohormone content to ameliorate plant productivity and stress tolerance. At – Arabidopsis thaliana; bGLU -β-
glucosidase, Ms - Medicago sativa, Gh - Gossypium hirsutum, Pl - Phaseolus lunatus, Pv - Phaseolus vulgaris, Bc - Brassica campestris, OE - overexpression.
Target gene/protein Promoter/gene, regulation Target plant Effect Reference

Cytokinins
IPT SAG12/IPT cassava increased drought tolerance Zhang et al. (2010)
SAG12/IPT creeping bentgrass improved heat and drought tolerance Xu et al. (2010),
Merewitz et al. (2012)
35S/IPT wheat increased tolerant to flooding and higher yield Tereshonok et al. (2011)
SARK/IPT peanut higher yields, improved drought tolerance under field Qin et al. (2011)
conditions
SARK/IPT rice increased grain yield and improved drought tolerance Peleg et al. (2011)
under water deficit
SARK/IPT tobacco increased tolerance to restricted watering regimes Rivero et al. (2009)
SARK/IPT maize higher grain yield, increased tolerance to drought by Bedada et al. (2016)
delayed leaf senescence
AtMYB32xs/IPT canola higher seed yield under rainfed and irrigated conditions Kant et al. (2015)
GhCYSP/IPT cotton improved lint yield and fiber quality, improved salt Liu et al. (2012)
tolerance
CKX CKX1 silencing barley higher plant productivity Zalewski et al. (2010)
bGLU/AtCKX1 barley increased tolerance to drought stress Pospíšilová et al. (2016)
OE
WRKY6/CKX1 OE tobacco improved drought and heat resistance Macková et al. (2013)
WRKY6/CKX1 OE tobacco improved drought tolerance Werner et al. (2010)
35S/GhCKXRNAi cotton increased fruiting branches and bolls, enhanced seed and Zhao et al. (2015)
moderate suppression lint yield
35S/AtCKX2 potato developing larger tubers Raspor et al. (2012)
OE
glycosyl-transferase Ubi/PlZOG1 OE maize shorter stature, increased root mass and branching, Pineda Rodó et al. (2008)
delayed senescence
35S/UGT85A5 OE tobacco increased salt stress tolerance Sun et al. (2013)
Act1/cZOGT1, rice short shoot phenotypes, delay of leaf senescence Kudo et al. (2012)
Act1/cZOGT2
OE

Gibberellins
GA20ox 35S/GA20ox OE tobacco higher biomass Biemelt et al. (2004)
35S/GA20ox OE hybrid aspen faster growth, elevated biomass Eriksson et al. (2000)
gid1 (gibberellin-insensitive gid1 mutant rice dwarf phenotype, increased cold stress tolerance Tanaka et al. (2006)
dwarf1)
ddf1 (dwarf and delayed-flowering 35S/ddf1 OE Arabidopsis increased tolerance to high-salinity stress Magome et al. (2004)
1)

Brassinosteroids
DWF pAS/DWF4 rice increased grain yield Wu et al. (2008)

Ethylene
ACC synthase ACS, down-regulation maize increased grain yield under stresses Habben et al. (2014)
ACC synthase acs7 mutant Arabidopsis increased tolerance to salt, osmotic, and heat stresses Dong et al. (2011)

Auxins
YUC SWPA2/AtYUCCA6 hybrid poplar increased drought tolerance Ke et al. (2015)
AtYUCCA7 mutant Arabidopsis enhances drought resistance Lee et al. (2012)

Abscisic acid
ZEP 35S/MsZEPOE tobacco drought and salt stress tolerance Zhang et al. (2016)
NDEC DEX/PvNDEC1 OE tobacco drought tolerance Qin and Zeevaart, (2002)
LOS Superpromoter/AtLOS5 OE cotton drought tolerance Yue et al. (2012)
Actin1P/LEA3-1P/ AtLOS5 OE rice improved grain yield under drought stress in the field Xiao et al. (2009)

Jasmonates
JMT 35S/BcNTR1 OE soybean drought tolerance Xue et al. (2007)

Arabidopsis fused with the IPT gene in transgenic tobacco, which re-
sulted in an increased number of flowers, seed yield, biomass, and a
reduction in leaf and floral senescence. Importantly, the plants did not
show developmental anomalies. Since then, SAG12 and other SAG
promoters have been widely used to select constructs for plant trans-
formation. The Senescence Associated Receptor Protein Kinase (SARK)
promoter, a stress- and maturation-induced promoter, is another ex-
ample of a promoter used in transgenic plants to elevate endogenous CK
content. In addition, the expression of IPT under SARK promoter en-
hanced drought tolerance (Rivero et al., 2009; Peleg et al., 2011). To
produce transgenic plants, the native IPT gene of Agrobacterium tume-
faciens is usually introduced for transformation (Table 1).
The use of inducible promoters for the conditional expression of CK
allows one to control hormone levels without negative effects on
growth and development, caused by a high content of the hormone
(Peleg and Blumwald, 2011). The effect of CK on plant productivity
varies and might depend on where and when their content is modified
and how the changes are related to external conditions and other hor-
mones (Wilkinson et al., 2012).
The CK signaling pathway has recently been revealed in Arabidopsis
and the components of the pathway could be potential targets to create
plants with elevated productivity and stress tolerance. The signaling
pathway comprises two-component histidine kinase receptors (AHK)
located in the endoplasmic reticulum, histidine-phosphotransfer pro-
teins (AHPs) and response regulators (ARR) (Cheng and Kieber, 2014).
Type-A ARRs are negative regulators of the CK response, while type-B
ARRs are positive regulators that fulfil the role of transcription factors.
Mutants of type-A ARRs did not cause pronounced morphological

34
J. Ciura, J. Kruk
effects (Cheng and Kieber, 2014). Among the CK signaling components,
the function of CKI1 (Cheng and Kieber, 2014) and HOG1 (Godge et al.,
2008) remains to be clarified.
2.2. Auxins
Aux regulate a wide variety of growth and developmental processes
in plants, including the differentiation of vascular tissues, apical dom-
inance, root formation, embryogenesis, phyllotaxis and tropic re-
sponses. Therefore, the genes involved in Aux biosynthesis, transport
and signal transduction are important biotechnological targets for
modifying plant size and shape, as well as improved yield (Busov et al.,
2008). The indole-3-acetic acid (IAA) was the first hormone of this
group to be identified and it is most frequently found among Aux (Mano
and Nemoto, 2012).
Parthenocarpic fruits and significantly improved tomato pro-
ductivity were obtained when the expression of the iaaM gene under
the control of DefH9 promoter was used (Ficcadenti et al., 1999). The
iaaM gene from Pseudomonas syringae pv savastanoi encodes tryptophan
monoxidase producing indole-acetamide, which is next converted to
IAA. The iaaM transgene also enhanced grape fecundity and yield
(Costantini et al., 2007), as well as fiber yield and quality in cotton
(Zhang et al., 2011). The corresponding gene of auxin synthesis, tms1
from Agrobacterium tumefaciens, under tuber-specific promoter was
manipulated to stimulate tuber formation in potato (Kolachevskaya
et al., 2015).
Many genes are involved in Aux biosynthesis, and this pathway has
not been fully elucidated (Mano and Nemoto, 2012). Transgenic potato
that overexpressed the ArabidopsisAtYUC6 gene exhibited a high-auxin
phenotype such as increased height, erect stature, longevity and en-
hanced drought tolerance because of a reduction in water loss (Kim
et al., 2012). Similarly, transgenic poplar with the overexpression of the
AtYUCCA6 gene displayed increased tolerance to drought stress (Ke
et al., 2015) (Table 1).
The GH3 gene family is involved in Aux homeostasis and their
conjugation to amino acids. OsGH3.1 overexpression in rice caused
dwarfism, inhibited cell growth and cell wall loosening, but enhanced
resistance to a fungal pathogen (Domingo et al., 2009). Overexpression
of OsGH3-2 in rice was related to IAA deficiency, dwarfism, smaller
leaves, and fewer crown roots, although such plants showed increased
cold tolerance due to the combined effects of reduced free IAA content,
attenuated oxidative damage, and decreased membrane penetration
(Du et al., 2012).
Enhanced synthesis of ARGOS, the product of an Aux-inducible gene
(Hu et al., 2003), resulted in increased organ size, while overexpression
of vacuolar H+-pyrophosphatase AVP1, involved in Aux transport,
manifested itself in increased cell division (Li et al., 2005).
The Aux signaling pathway involves three main components, F-box
TIR1/ABF auxin co-receptors, Aux/IAA transcriptional repressors and
ARF transcription factors (Salehin et al., 2015; Lavy and Estelle, 2016;
Leyser, 2018) which could be considered to be potential targets for the
transgenic approach. The function of siRNA and miRNA in Aux sig-
naling should also be taken into account (Si-Ammour et al., 2011).
2.3. Gibberellins
GA comprise a large group of tetracyclic diterpenoid compounds,
which play a crucial role in stem elongation, plant development, seed
germination, leaf expansion and hormonal homeostasis, while a GA
deficit results in plant dwarfism (Golovatskaya, 2008). These hormones
also play important roles in abiotic stress response and adaptation. The
use of semi-dwarf varieties of rice and wheat was a breakthrough in
agriculture because of their higher resistance to damage caused by wind
and rain. GA are promising targets for affecting plant size and biomass
production. Both synthesis, catabolism and the signaling pathway of GA
can be manipulated for this purpose (Fernandez et al., 2009).
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Journal of Plant Physiology 229 (2018) 32–40
So far, the main biotechnological targets have been GA 20-oxidases
and GA 3-oxidases, catalyzing the last two steps of GA biosynthesis, and
GA 2-oxidase that catalyze the conversion of GA to inactive catabolites.
These three types of enzymes are encoded by small families of GA20ox,
GA3ox and GA2ox genes (Bou-Torrent et al., 2011). Transgenic rice,
which constitutively expresses OsGA2ox1, displayed dwarfism, but the
plants were not able to form grains. In turn, overexpression OsGA2ox1
in shoots under the control of the promoter of a GA biosynthesis gene
resulted in a semi-dwarf phenotype and the plants showed normal
flowering and grain development (Sakamoto et al., 2003).
García-Hurtado et al. (2012) reported that GA 20-oxidase controls
the formation and development of tomato fruit. Transgenic tomato with
overexpressed citrus gene GA20ox revealed the induction of parthe-
nocarpic fruit growth, delayed fruit ripening time and a higher yield. In
potato, GA3ox2 which overexpressed lines showed an early tuberiza-
tion response under short-day conditions and a higher mass yield of
tubers per plant (Bou-Torrent et al., 2011). In transgenic tobacco plants,
enhanced stem growth, higher biomass production, lignin content and
rate of photosynthesis was observed in plants that overexpressed the
AtGA20ox gene (Biemelt et al., 2004) (Table 1). Transgenic GA 20-
oxidase hybrid aspen displayed faster growth and elevated biomass
production, as well as xylem fiber length. These traits are desirable in
the production of paper (Eriksson et al., 2000).
In the case of Brassica napus, overexpression of AtGA2ox8 from
Arabidopsis thaliana resulted in an increased number of primary bran-
ches and siliques, which caused a significant increase in the seed yield
(by 9.6–12.4%). The dwarf plants were more resistant to lodging and
had an approximately 8-fold higher anthocyanin content than the wild
type. A higher anthocyanin level could improve protection against
oxidation, pathogen infection and cold (Zhou et al., 2012). The next
example of targeting GA 2-oxidase is transgenic switchgrass (Panicum
virgatum) where overexpression of the gene resulted in a modified plant
architecture, such as increased tillering, reduced lignin content and
generally improved plant morphology, as well as reduced biomass re-
calcitrance, beneficial in biofuels production (Wuddineh et al., 2015).
Lodging is a serious problem in crop production. Okuno et al. (2014)
examined rice GA-deficient mutants and high-GA producing lines and
they found that plants with increased production of GA displayed im-
proved lodging resistance and biomass yield. Enhanced breaking-type
resistance was found to be due to an increased lignin content and/or
higher culm diameter.
GA signaling has recently been recognized, including GID1 re-
ceptors, localized both in cytoplasm and nucleus, and DELLA proteins
(transcriptional regulators) as the main repressors of GA response
(Schwechheimer, 2012; Davière and Achard, 2013). GA interacts
through DELLA proteins with the JA pathway, Aux transport compo-
nents and other partners. Thus, multiple components of GA signaling
are potential targets to be investigated using a transgenic approach,
which could result in elevated plant productivity and stress resistance.
2.4. Abscisic acid
ABA regulates several plant physiological processes and develop-
mental stages including seed dormancy and development, embryo
morphogenesis, stomata opening, as well as the synthesis of storage
proteins and lipids. It is also known as a “stress hormone” due to its key
role in the response of plants to abiotic stresses. ABA is involved in the
synthesis of protective proteins (LEA proteins, dehydrins), osmopro-
tectants, antioxidant enzymes and it responsible for turgor main-
tenance. The ABA content increases in response to environmental
stresses, activating signaling pathways that result in gene expression
being activated (Wani et al., 2016). ABA signaling pathway includes the
PYR/PYL/RCAR protein receptor complex, PP2C protein phosphatases
which act as negative regulators, SNRK2 kinases and ABF transcription
factors (Nakashima and Yamaguchi-Shinozaki, 2013; Vishwakarma
et al., 2017).
J. Ciura, J. Kruk
In the early stages of ABA biosynthesis, carotenoid precursors are
involved. Geranylgeranyl pyrophosphate is converted to phytoene and
then via ζ-carotene, lycopene, β-carotene to zeaxanthin. The next step is
the epoxidation of zeaxanthin via antheraxanthin to violaxanthin in
plastids catalyzed by zeaxanthin epoxidase (ZEP). After a series of
structural modifications, violaxanthin is converted to 9-cis-epoxycar-
otenoid by the 9-cis-epoxycarotenoid dioxygenase (NCED). Later steps
take place in cytosol where xanthoxin is converted to ABA. A short-
chain alcohol dehydrogenase/reductase (SDR), encoded by the ABA2
gene, generates ABA aldehyde which is next oxidized to ABA by ABA
aldehyde oxidase (AAO) (Xiong and Zhu, 2003).
It was demonstrated that overexpression of ZEP in Arabidopsis re-
sulted in more vigorous growth of transgenic plants during high salt
and drought treatments than that of the wild-type (Park et al., 2008). In
tobacco, overexpression of ZEP from alfalfa conferred tolerance to
drought and salt stress (Zhang et al., 2016) (Table 1), while that of ZEP
from Eutrema salsugineum (EsABA1) resulted in higher tolerance to salt
stress and enhanced endogenous ABA concentration (Sun et al., 2014).
Significantly more reports concern studies of the NCED gene. Trans-
genic tobacco with overexpressed NCED1 gene from the bean (Phaseolus
vulgaris) showed an increase in ABA content and tolerance to drought
stress (Qin and Zeevaart, 2002). Transgenic petunia plants, that over-
express tomato NCED1 gene, had an elevated ABA content and showed
a significant increase in drought resistance. Moreover, after 14 days
without water, transgenic plants completely recovered when re-wa-
tered (Estrada-Melo et al., 2015). Another example is the transgenic
lines of creeping bentgrass (Agrostis stolonifera), which were highly
tolerant to drought and NaCl stress after overexpression of the NCED1
gene from cowpea (Vigna unguiculata) (Aswath et al., 2005). Likewise,
transgenic tobacco that overexpresses the Citrus reshni NCED1 gene
showed enhanced tolerance to drought, dehydration, salt and oxidative
stresses (Xian et al., 2014).
Among genes of the last steps of ABA biosynthesis, expression of
AtSDR1 does not appear to be regulated by stress (Xiong and Zhu,
2003). ABA aldehyde oxidase requires the sulfurylated form of a mo-
lybdenum cofactor for its activation. LOS5/ABA3 (LOS5) encodes a
molybdenum cofactor and in cotton, overexpression of the AtLOS5 gene
enhanced the ABA level and drought tolerance and its membrane in-
tegrity improved under water stress distinctly (Yue et al., 2012).
Overexpression of the AtLOS5 gene in transgenic rice conferred an in-
creased drought tolerance of transgenic plants under water-deficit in
field (Xiao et al., 2009). Moreover, the plants also showed a sig-
nificantly higher yield. Similarly, enhanced drought tolerance was
found in transgenic tobacco (Yue et al., 2009) and maize (Lu et al.,
2013) that overexpresses the LOS5/ABA3 gene.
Because of the negative regulation of many physiological processes
by ABA, transgenic plants that overexpresses ABA biosynthetic genes
show indirect effects in productivity due to their enhanced resistance to
environmental stresses.
2.5. Ethylene
ET is a gaseous hormone which participates in plant growth and
development, particularly flower senescence, fruit ripening, leaf and
petal abscission and it is a key mediator of biotic and abiotic stress
responses in plants (Wani et al., 2016). ET signaling is still not fully
understood, although it is known that it includes ET receptors (ETR1/2,
ERS1/2, EIN4), the repressor protein CTR1, EIN3/EIL1 proteins and
Ethylene Response Factors (ERFs). These transcription factors in turn
play an essential role in adaptation to stresses caused by pathogens,
wounding, heat and cold stress, UV light, salinity and drought (Müller
and Munné-Bosch, 2015).
As a factor which accelerates fruit ripening and due to its obvious
economic importance, ET was widely used in agriculture, horticulture
and fruit farming. Beyond this use, ET was also used to increase rubber
productivity in Hevea brasiliensis in field experiments (Traore et al.,
36
Journal of Plant Physiology 229 (2018) 32–40
2011) to stimulate latex production in H. brasiliensis (Zhu and Zhang,
2009). ET acts as a positive modulator that accelerates shade-avoidance
responses in tobacco (Pierik et al., 2003). These responses, accom-
panied by enhanced ET production, help to arrange the leaves higher in
the canopy where light conditions are most beneficial (Pierik et al.,
2006).
Biotic and abiotic stress promotes ET production. It was found that
ET negatively regulates plant responses to freezing stress in A. thaliana.
Furthermore, ET-insensitive mutants displayed enhanced freezing tol-
erance (Shi et al., 2012). ET production caused by heat stress induced
kernel abortion and suppression of grain maturation in Triticum aes-
tivum (Hayat et al., 2007).
On the other hand, ET inhibits growth and development, therefore
some studies were aimed to decrease ET production and perception.
The common target of this manipulation is 1-aminocyclopropane-1-
carboxylic acid synthase (ACC synthase), which catalyzes the rate-
limiting step in ethylene biosynthesis. Down-regulation of ACC syn-
thase stabilized female maize reproductive growth and significantly
increased grain yield under abiotic stresses (Habben et al., 2014)
(Table 1). Transgenic apple fruits with ethylene suppression were sig-
nificantly firmer than the controls and had an increased shelf-life
(Dandekar et al., 2004). Also, in melon, which expresses an antisense
ACC oxidase construct, slower ripening connected with the accumula-
tion of larger amounts of soluble solids, softening of the flesh and a
reduction in acidity were observed (Silva et al., 2004). Inoculation of
pea plants cultured in drying soil with the bacteria Variovorax para-
doxus, producing 1-aminocyclopropane-1-carboxylate deaminase
(ACD) that degrades the ethylene precursor ACC, improved the growth,
yield and water-use efficiency of the plants under drought (Belimov
et al., 2009). Similar results were obtained for potato (Belimov et al.,
2015).
ET interacts with other plant regulators such as jasmonates and ABA
through ERFs in abiotic stresses (Müller and Munné-Bosch, 2015) and
influences growth, development and plant defense, which has been
discussed elsewhere (Pierik et al., 2006; Wilkinson et al., 2012; Kazan,
2015).
2.6. Brassinosteroids
BR are polyhormones whose main function is to stimulate cell
elongation and division, differentiation, embryogenesis, senescence and
response to environmental stresses. They also play an important role in
such physiological processes as seed germination, stem and root
growth, rhizogenesis, fertility, flowering, pollen tube growth, photo-
synthesis, ethylene biosynthesis, gene expression or proton pump acti-
vation. Therefore, BR are considered as regulators with pleiotropic ef-
fects (Bartwal et al., 2013; Bharwdaj et al., 2014). Mutants defective in
BR synthesis or signaling show dwarf phenotypes, whereas increased
production of BR can result in higher biomass, plant size and seed yield.
The signaling pathway of BR has been thoroughly investigated and
involves the BRI1-BAK1 receptor complex, substrate proteins BSK1-3
for the receptor complex, BSU1 phosphatase, BIN2 kinase and BES1/
BZR1 transcription factors (Zhu et al., 2013; Clouse, 2014). Moreover,
BR signaling is affected by the negative regulators BKI1, TTL and TRIP.
BR signal transduction components interact with other signaling path-
ways that regulate plant growth and development, like those of GA and
phytochrome (Zhu et al., 2013; Clouse, 2014). The biosynthesis of BR
and genes affected by this phytohormone in different plant species have
been studied in great depth (Fernandez et al., 2009).
BR are polyhydroxy steroids and their structure is similar to that of
animal steroid hormones. Examples of BR are brassinolide, castasterone
(Fig. 1) and 24-epibrassinolide. The concentration of BR in plant tissue
is usually extremely low.
BR were found to be involved in adaptive tolerance to environ-
mental stresses, which translates into better yield. Foliar spray by a
brassinosteroid increased the number of fruits and fruit yield per plant
J. Ciura, J. Kruk
and neutralized the toxic influence of heavy metals in cadmium-
stressed Solanum lycopersicum (Hayat et al., 2012). Exogenous use of 28-
homobrassinolide/24-epibrassinolide also protects the photosynthetic
apparatus and improved the antioxidant defense system in tomato
cultivars (Hasan et al., 2011). A similar effect was observed in the case
of eggplant (Solanum melongena) seedlings exposed to high temperature
stress (Wu et al., 2014). The effects of brassinosteroids on plants sub-
jected to various stresses have been already reviewed (Bajguz and
Hayat, 2009).
Due to the control of several important agronomic traits by BR, such
as flowering time, plant architecture, seed yield and stress tolerance,
these phytohormones have become a biotechnological target for en-
hancing crop yield (Divi and Krishna, 2009). Among the effects of the
wide use of BR one could mention increased vegetative growth, total
yield and the quality of pods in bean (Phaseolus vulgaris) (El-Bassiony
et al., 2012) or the significantly decreased deleterious effects of salinity
on plant productivity in wheat (Talaat and Shawky, 2012). On the other
hand, in Arabidopsis overexpression of the DWF4/DWARF4 gene, which
encodes the steroid 22α-hydroxylase (CYP90B1) – one of the enzymes
in brassinosteroid biosynthesis – resulted in a 35–47% increase in plant
size and an increase in seed production of up to 59% (Choe et al., 2001).
In the case of transgenic rice with the overexpressed hydroxylase, an
increase in grain yield within a range of 15–44% was observed (Wu
et al., 2008) (Table 1). Under the promoter CaMV35S, overexpression
of EXORDIUM (EXO), which regulates the expression of many BR-re-
sponsive genes, resulted in the formation of larger leaves and stimu-
lated root growth (Coll-Garcia et al., 2004). Genetic manipulation of BR
biosynthesis and signaling could allow a significant increase in crop
yield both by changing the plant metabolism and protecting plants from
environmental stresses in a predictable manner (Divi and Krishna,
2009).
2.7. Jasmonates
JA (jasmonic acid and its derivatives) are lipid-derived compounds
that play a key role in plant stress responses and developmental pro-
cesses, such as callus growth, seed germination, root growth, trichome
and tuber formation, fruiting, flowering and senescence. Their main
function is to respond to wounding, herbivores and pathogen attack,
and also under salinity, drought and cold stresses (Wasternack, 2014).
In JA signaling pathway, the key factors are COI1 receptor, JAZ re-
pressor and MYC2 transcription factors (Kazan and Manners, 2008;
Santino et al., 2013). The active signaling molecule recognized by COI1
is JA-Ile conjugate synthesized by JAR1 (Kazan and Manners, 2008;
Santino et al., 2013).
JA are signaling molecules whose synthesis is induced by various
environmental stresses including salinity, drought and UV irradiation
(Wani et al., 2016). Treatment of JA ameliorated salt-stressed rice
seedlings (Kang et al., 2005) and barley (Walia et al., 2007). Anjum
et al. (2011) suggested the involvement of methyl jasmonate in im-
proving the drought tolerance of soybean by modulating the membrane
lipid peroxidation and antioxidant activities. Applying JA exogenously
to potato resulted in increased tuber production (Pruski et al., 2003)
and a higher tomato yield (Kazemi, 2014).
In addition to the exogenous application of JA, the effect of al-
teration in the endogenous level of jasmonates in transgenic plants has
been analyzed. One of the targets is jasmonic acid carboxyl methyl-
transferase (JMT) which participates in the formation of methyl jas-
monate. Overexpression of the JMT gene increased tuber yield and size
in transgenic potato (Sohn et al., 2011) and promoted the growth of
roots and production of ginsenoside heterogeneity in transgenic roots of
Panax ginseng (Kim et al., 2012). In transgenic soybean, overexpression
of JMT conferred tolerance to water stress (Xue et al., 2007) (Table 1).
13-Lipoxygenase (13-LOX) catalyzes one of the reactions in JA bio-
synthesis and overexpression of its gene tomloxd increased resistance to
Cladosporium fulvum and elevated the temperature in tomato (Hu et al.,
37
Journal of Plant Physiology 229 (2018) 32–40
2013).
3. Plant hormone mutants - their productivity and stress tolerance
CK regulate a broad range of developmental processes and CK-de-
ficient mutants provide excellent models for studying the dependency
between CK and plant adaptation to environmental stresses. Nishiyama
et al. (2011) investigated the influence of CK-deficient Arabidopsis
mutants on salt and drought stress signaling. Their results showed that
ipt1 3 5 7 mutant exhibited improved salt and drought tolerances and
CK-deficient plants that overexpressed CKX displayed an enhanced salt-
and drought-tolerant phenotype. The better tolerance of CK-deficient
plants could be ascribed to their ability to maintain a higher water
content under stress and react faster to ABA and stresses by repressing
CK signaling. Arabidopsis CK receptor mutants also indicate the role of
CK in shoot growth, seed germination and size or root development. For
instance, the triple mutant of CK receptors (AHK2, AHK3 and AHK4)
had seeds more than twice the size of those of the wild-type, and the
double mutant was characterized by increased branching and an en-
hanced root system because the primary root grew faster (Riefler et al.,
2006). Moreover, the ckx3ckx5 double mutants produced larger in-
florescence and floral meristems, leading to a greater number of siliques
and an increased seed yield. These results indicate the vital role of CKs
in reproductive development (Bartrina et al., 2011).
A number of mutants have been shown to have genes involved in
Aux metabolism and signaling. The yuc7-1D mutant of the YUCCA7
gene showed phenotypes similar to those observed in auxin-over-
producing mutants, such as tall, slender stems and curled, narrow
leaves and showed significantly enhanced resistance to drought stress
(Lee et al., 2012). The loss-of-function mutants of the Auxin Response
Factor (ARF) displayed strong and specific phenotypes, including ef-
fects on stature, leaf morphology and root architecture. The arf2 plants
produced longer, thicker inflorescence stems, and larger, darker green
leaves and larger seeds (Okushima et al., 2005). The maize brachytic2
(br2) mutant, characterized by a loss of a P-glycoprotein that modulates
polar auxin transport in the stalk, shows height reduction and compact
lower stalk internodes. This dwarfing mechanism, an important agro-
nomic feature, could be used in agriculture (Multani et al., 2003).
In plant tissue, most IAA occurs in inactive conjugated forms, and
may be hydrolyzed to free IAA by a number of hydrolases (Heden and
Phillips, 2000). TGW6 encodes IAA-glucose hydrolase and the loss of
function of this gene enhanced rice grain weight and significantly in-
creased yield (Ishimaru et al., 2013).
Several studies have been carried out on plant mutants with altered
levels of GA, which resulted in an increase in their resistance to stress. A
GA-insensitive dwarf mutant of rice gid1 (gibberellin-insensitive dwarf1),
with an inactive GA receptor, showed a severe dwarf phenotype and
contains high concentrations of endogenous GA (Table 1). It showed
increased tolerance to cold stress and resistance to blast fungus infec-
tion (Tanaka et al., 2006). The study conducted on the dwarf and de-
layed-flowering 1 (ddf1) mutant confirmed that DDF1 is involved in
stress tolerance and transgenic plants that overexpress DDF1 showed
increased tolerance to high-salinity stress (Magome et al., 2004)
(Table 1). Similarly, a GA biosynthetic mutant, ga1-3, showed improved
tolerance to salt stress (Magome et al., 2004). In the Arabidopsisga4-1
mutant, which is deficient in GA4/1, the growth of vegetative and re-
productive organs and development was delayed, and plant seed pro-
ductivity was decreased (Golovatskaya, 2008).
The examples of ABA hormone mutants include the aba1 mutant of
ZEP in rice which displayed a low ABA content and upon drought in-
duction the ABA level was not up-regulated (Agrawal et al., 2001).
AREB1, AREB2 and ABF3 belong to ABA-responsive element-binding
proteins/transcription factors. The areb1 areb2 abf3 triple mutant dis-
plays increased ABA resistance and reduced drought tolerance, which
indicates that these three factors coordinately govern ABRE-dependent
gene expression under water stress conditions (Yoshida et al., 2010).
J. Ciura, J. Kruk
An example of BR mutants of practical application is the new cul-
tivar of rice with erect leaves. In rice, two different cytochromes
CYP90B2/OsDWARF4 and CYP724B1/D11 catalyze C-22 hydroxyla-
tion, while CYP90D2/D2 catalyze C-3 oxidation in brassinosteroids
biosynthesis. Hong et al. (2003) reported that a rice dwarf mutant, ebisu
dwarf (d2), which is defective in the CYP90D2/D2 protein, has erect
leaves but a lower height and decrease in grain yield. Erect leaves allow
better penetration of light to the lower leaves, hence favoring photo-
synthetic rates, but a decrease in grain yield is unfavorable for crop
breeding. However, the recently identified mutant, Osdwarf4-1, dis-
played erect leaves, increased biomass production and grain yield
without abnormal flower or grain morphology (Sakamoto et al., 2006).
This semi-dwarf mutant is of special interest for agriculture.
ET is a vital signaling molecule in plant stress response. Therefore,
inhibiting ET signal transduction may contribute to enhanced tolerance
to stress and an amelioration in productivity. A series of ethylene re-
sponse mutants was identified in Arabidopsis and tested in several crop
plants. The ethylene resistant1-1 (etr1-1) mutant, under an inducible
promoter, showed elongation of hypocotyl and roots in dark-grown
tomato seedlings in the presence of ET (Gallie, 2010). This experiment
demonstrated that ethylene responses could be manipulated to achieve
better control over developmental processes such as fruit ripening or
stress responses that affect crop yield. In Arabidopsis, the etr1-1 mutant
showed an increased sensitivity to osmotic and salt stress during ger-
mination and seedling development, which provides physiological and
genetic evidence that the ethylene receptor ETR1 modulates plant re-
sponse to abiotic stress (Wang et al., 2008). In turn, the acs7 mutant of
ACC synthase 7 showed increased tolerance to salt, osmotic, and heat
stresses by modulating ABA sensitivity and accumulation (Dong et al.,
2011). These examples show that manipulating various target of ethy-
lene biosynthesis and signaling could provide an efficient control
system for developmental processes, an appropriate response to en-
vironmental stresses and crop improvement.
4. Future perspectives
These data show clearly that manipulating phytohormones in
transgenic plants is a promising way to improve plant productivity and
could also result in enhanced tolerance to biotic and abiotic stresses.
Nevertheless, phytohormones (e.g. BR and GA) certainly cannot be
regarded as the only factors responsible for plant height and biomass
production (Fernandez et al., 2009), as the main driving force for
growth and biomass production in plants is photosynthesis, which
supplies the required energy and carbon for the biosynthesis of organic
compounds necessary for development. When regulating the phyto-
hormones level both synthesis and their catabolism pathways are im-
portant and can be targets for phytohormone engineering. Moreover,
components of signaling pathways of phytohormones, including tran-
scription factors, should be explored in this respect. Several potential
targets include those of GA catabolism (EUI1, GAMT) (Fernandez et al.,
2009) and signaling pathways of GA (DELLA, GID, SLR1) (Fernandez
et al., 2009), Aux (ARGOS, AVP1, ARF2) (Hu et al., 2003; Li et al.,
2005), CK (HOG1) (Godge et al., 2008), BR (e.g., EXORDIUM, BRI1,
TTL, BES1/BZR1) (Coll-Garcia et al., 2004) or those of ET (e.g., ERF,
ETR, ARGOS) (Shi et al., 2015).
Modifications to the genes responsible for the phytohormone level
should be controlled adequately as their constitutive expression may
result in undesired, negative effects on plants’ growth. There is a need
to use conditional, stress-induced or senescence-induced promoters.
Moreover, the signaling pathways of phytohormones are known to in-
teract with each other (crosstalk) (Wani et al., 2016; Fernandez et al.,
2009), which should be taken into account in future genetic mod-
ifications. In addition to laboratory scale conditions, the effects of
phytohormone engineering should be tested under field conditions in a
natural, changing environment and over a longer time scale.
38
Journal of Plant Physiology 229 (2018) 32–40
Acknowledgments
JK acknowledges financial support from the grant 2015/19/B/NZ9/
00422 obtained from the National Centre of Science of Poland. The
Jagiellonian University is a partner of the Leading National Research
Center (KNOW) supported by the Ministry of Science and Higher
Education.
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