Tomato tolerance to abiotic stress

24 Pages·2017·1.38 MB·English

by  Aneta Gerszberg

Plant Growth Regul (2017) 83:175–198
DOI 10.1007/s10725-017-0251-x
ORIGINAL PAPER
Tomato tolerance to abiotic stress: a review of most often
engineered target sequences
Aneta Gerszberg1 · Katarzyna Hnatuszko‑Konka1 
Received: 6 September 2016 / Accepted: 12 January 2017 / Published online: 27 January 2017
© The Author(s) 2017. This article is published with open access at Springerlink.com
Abstract Tomato is one of the most often cultivated veg- are consecutively presented in this paper rather than the
etable species worldwide. Due to the anti-oxidative and typically reviewed division of stress types.
anti-cancer properties of lycopene, tomato consumption as
well as production is still increasing. However, its produc- Keywords Tomato · Abiotic stress · Tomato
tivity is impaired by a wide range of abiotic stresses, and transformation
the establishment of stress-tolerant crops is a key challenge
for agricultural biotechnology. Until now, a few genetic
approaches have been used to achieve stress tolerance in Introduction
cultivated tomato plants. Such achievements are based on
current knowledge concerning plant adaptation. The pres- Tomato (Solanum lycopersicum L.) is a popular and eco-
ence of adverse environmental factors like extreme temper- nomically important crop plants around the world. It con-
atures, salinity or drought cause definite biochemical and tains a valuable compound, lycopene, which possesses
physiological consequences. Mostly, these are the changes anti-oxidative and anticancer properties. Therefore, tomato
in the metabolic pathways, the expression of stress-induci- production and consumption are permanently increasing
ble genes or the accumulation of low-molecular compounds (Raiola et al. 2014). In 2013 tomato was 7th in global pro-
that play a crucial role in maintaining the plasticity of reac- duction, achieving a world production of approximately
tions. The biotechnological methods used to modify tomato 164,000,000.00 million tonnes on a total area of nearly
to produce “upgraded” plants are based on introgression 4.8 million hectares (FAOSTAT 2013). Being a tropical
of several genes coding enzymes known to mitigate stress plant, tomato is well adapted to almost all climatic regions
or genes contributing to signalling and diverse regulatory of the world; however, environmental stress factors are the
pathways. Here, we present an overview of the most often primary constraints of this crop’s yield potential. Recently,
chosen target sequences/molecules that are genetically the molecular pathways underlying environmental stress
delivered or engineered to obtain tolerance to environmen- tolerance have been studied intensely with much empha-
tal constraints. Since adverse conditions cause interrelated sis on the tolerance mechanisms pertaining to individual
stress responses, it is the tolerance molecular players that stresses. Abiotic stress is a general term, which includes
miscellaneous stresses e.g. chilling, high temperature,
osmotic shock, drought, salinity, water logging, wounding,
* Aneta Gerszberg exposure to ozone, toxic ions, excessive light and UV-B
[email protected] irradiation (Rehem et  al. 2012). Unfortunately, abiotic
stresses are complex in their nature and controlled by net-
Katarzyna Hnatuszko-Konka
[email protected] works of different factors (e.g. genetic and environmental)
that impede crop plant breeding strategies (Da Silva and de
1 Department of Genetics, Plant Molecular Biology
Oliveira 2014).
and Biotechnology, Faculty of Biology and Environmental
While traditional approaches achieve their limit, current
Protection, University of Lodz, Banacha 12/16, 90-237 Lodz,
Poland agriculture must deploy quite novel solutions to meet the
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1 76 Plant Growth Regul (2017) 83:175–198
demands of the world’s population. Genetic engineering is stage appears exclusively when the stress factor is elimi-
one of the many tools available for creating improved, mod- nated before failure becomes too drastic and enables full or
ern crop plants. Recently, technological advances in func- partial recovery of the plant’s physiological function. At the
tional genomics have been made and they have helped to beginning, any abiotic stress response is the perception of
reveal the numerous gene families and processes, that alter stress signals by cell wall receptors, that activate different
adaptation to abiotic stresses and thereby improve yield. signal transduction events involving different intermediate
Since in most cases plants have windows of tolerance to stress genes (Da Silva and de Oliveira 2014). These genes
surrounding environmental factors, genetic engineering can could be members of the mitogen-activated protein kinase
be used to enhance the native adaptation abilities. Genes cascade, or calcium dependent protein kinase cascade
can be placed into various of expression cassettes, and sub- and activate cis-acting elements and transcription factors
sequently introduced to plants in which they do not natu- (TFs) that control expression patterns of stress-response
rally occur. Genetically engineered plants can be employed genes. This leads to plant stress tolerance (Fig. 1). Among
not only as origin of novel cultivars, but can also be help- stress-induced genes three categories can be distinguished:
ful in analysing and describing the activity and interplay the first category includes genes encoding proteins with
of gene networks for abiotic stress tolerance (Kissoudis known functions (structural or enzymatic), the second cat-
et al. 2015). Given the complexity of stress and its genesis, egory contains transcription factors and regulatory proteins
it is rare to meet a single abiotic stress in nature. A great and the third comprises proteins with unknown functions
number of stress-responsive pathways and components is (Yamaguchi-Shinozaki and Shinozaki 2009).
common in reactions to multiple stressors. Consequently,
instead of the typically reviewed division of stress types,
we decided to provide a general overview of the molecular Biotechnological strategies
background i.e. genes, proteins and other molecular com-
pounds, that are considered to be significant for plant func- Plant in  vitro tissue culture techniques have become a
tion and response under stress conditions. Its components prerequisite step to further development of plant transfor-
are perceived as targets in “the gene therapy” of plants in mation methods. Furthermore, advances in plant genetic
stress. We present some results of such an approach hop- transformation significantly facilitated progress in the
ing it will allow the readers to get acquainted with the most recognition of individual genes and enzymes involved in
often engineered target sequences. plant tolerance to various abiotic stresses. Additionally,
the advancement of knowledge in the field of genomics of
tomato’s wild relative species can be exploited in a breed-
Physiological basis of abiotic stress tolerance ing programs for the introgression of abiotic stress toler-
in plants ance into common, cultivated tomato cultivars (Foolad
2007; Labate and Robertson 2012).
The concept of stress assumes the occurrence of an exter-
nal factor that disadvantageously influences a plant. It Methodology of tomato transformation
can also be understood as a negative deviation of the liv-
ing conditions that are optimal for a plant. Hence, toler- Over the past two decades, numerous techniques were used
ance must presume certain plasticity in metabolic reactions to introduce foreign genes into both mono- and dicotyle-
that let a plant function in an unfavourable environment donous plants, such as rice, potato, soya bean, tomato or
(to avoid, tolerate or recover from the stress conditions). common bean (Sahoo et al. 2011; Gerszberg et al. 2012;
This ability to limit the damage triggered by a given stress Hnatuszko-Konka et al. 2014). The first protocol for the
may be defined as plant tolerance. Adaptation of plants to genetic transformation of Solanum lycopersicum was
abiotic stresses is a complex process, that is characterized reported in the 1980s and since then a significant pro-
by activation of multifarious responses engaging compos- gress in this field has been made (McCormick et al. 1986).
ite gene interplay and ‘crosstalk’ among many molecular The tested approaches included both direct methods and
pathways (Da Silva and de Oliveira 2014). These com- those using bacterial vectors, differing in transformed
plex cellular responses were explained by advancements target genome (plastid, nuclear) or in the stability of the
made in investigating and comprehension of plant abiotic transformation.
responses at different levels. In general, three stages are Mostly, Agrobacterium-mediated transformation pro-
distinguished during abiotic stress: (1) the stage of alarm; cedures for various tomato cultivars have been expanded
(2) the stage of resistance; and (3) the stage of exhaustion (Gerszberg et al. 2015). The agroinfection process is com-
(Rehem et al. 2012). However, Lichtenthaler (1988) added plex, and its efficiency depends on a broad spectrum of
the fourth stage—the regeneration stage. This particular elements including the presence of a chemoattractant in
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Plant Growth Regul (2017) 83:175–198 177
Fig. 1 The plant response to
abiotic stress. Primary stresses
are interrelated and provoke
cellular damage as well as
secondary stresses. The initial
stress signal cause activation
of signalling process as well as
transcription control. Conse-
quence of this, is initiation of
stress-responsive mechanism to
restoration of cellular homeo-
stasis, accompanied by the
protection and repair dam-
aged proteins and membranes.
Finally, plant gained tolerance
or resistance to stress. ABF
ABRE-binding factor, Athk1
Arabidopsis thaliana histidine
kinase-1, bZIP basic leucine
zipper transcription factor, CBF/
DREB C-repeat-binding factor/
dehydratation-responsive bind-
ing protein, CDPK calcium-
dependent protein kinase, COR
cold-responsive protein, Hsp
heat shock protein, LEA late
embryogenesis abundant, MAP
mitogen-activated protein; PLD
phospholipase D – PtdOH,
phosphatidic acid, PX per-
oxidase, ROS reactive oxygen
species, SOD super dismutase,
SP1 stable protein 1
the culture or preculture media, the application of nurse engineering, it was harnessed to produce transgenic plants
cells, bacterial factors (culture density, virulence of the (Hasan et al. 2008; Chetty et al. 2013). Yasmeen et al.
Agrobacterium strain), the type of plasmid vector and the (2009) evaluated fruit maturity, gene construct type and
tissue specific factors (the type of explants and the geno- in planta technique (fruit injection and floral dip) for the
type), the composition of the culture media (concentration establishment of the optimal protocol of transformation. A
of phytohormones), the concentration and kind of selective higher transformation percentage was obtained for mature
agents and the cocultivation time (Guo et al. 2012; Chetty fruits (ca. 15–20 times higher) in comparison to immature
et al. 2013; Shah et al. 2015; Sun et al. 2015). Examples fruits. To reduce the time of obtaining transgenic plants
of optimisation of aforementioned parameters for tomato as well as cases of somaclonal variation, in planta meth-
transformation are presented in Table 1. Despite numerous ods were assessed. Yasmeen et al. (2009) tested the floral
attempts to improve transformation protocols with regards dip procedure for the flower transformation before and
to effectiveness, progress in this area is limited due to geno- after pollination. The results were interesting and clearly
type specificity. Notwithstanding this fact, some efforts to indicated that type of construct and floral stadium are
determine an effective genetic transformation method for important for transformation effectiveness. A higher effi-
such “stubborn” cultivars were made (Fuentes et al. 2008). cacy of transformation was reported in the case of flow-
Agroinfection-mediated modifications utilized both Agro- ers treated with a bacterial suspension before pollination.
bacterium tumefaciens and A. rhizogenes species. Usually, Despite promising transformation efficiency, some adverse
Agrobacterium tumefaciens is the vector of choice for plant changes in the morphology (short and not erected steam,
transformation. Also, in the case of Solanum lycopersicum curled leaves) of the plants were observed in comparison
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1 78 Plant Growth Regul (2017) 83:175–198
a 0)
aci 8) 01
M 0 2
References Moghaieb et al. (2004) Cortina and Culianez-(2004) Orzaez et al. (2006) Wu et al. (2006) Sun et al. (2006) Qiu et al. (2007) Abu-El-Heba et al. (20 Hasan et al. (2008) Fuentes et al. (2008) Briza et al. (2008) Gao et al. (2009) Khoudi et al. (2009) Yasmeen et al. (2009) Sharma et al. (2009) Chaudhry and Rashid ( Islam et al. (2010)
erszberg et al. (2015) Transformation efficiency Regenerated hairy roots at frequency of 54 to 67% Transformation frequency 12.5% NA NA Transformation frequency 40% Max. transformation fre-quency 20.87% Transformation frequency Agrobacterium-30% (mediated), 26.5% (biolistic method) Transformation frequency ranged from 54 to 68.0% Transformation frequency 21.5% transformation frequency ranged from 0.4 to 9.0% Transformation frequency 44.7% Transformation frequency ranged from 14 to 30% Transformation frequency ranged from 12 to 23% (in planta transformation)Transformation frequency AP1LFY17% ( gene),19% ( GUSgene) and 21% ( gene) (agro-infiltration) Transformation frequency 41.4% (for Pusa Ruby), 22% (for Arka Vikas), 41% (for Sioux) Transformation frequency 24% (for Rio Grande), 8% (for Roma) NA
G
1);
1
sed on Pandey et al. (20 Explant type Hypocotyls Cotyledons Fruits Cotyledons, hypocotyls Cotyledons Cotyledons Hypocotyls, and part of cotyledon Mature fruits Cotyledons Cotyledons Cotyledons Cotyledons, leaves Flowers; mature fruits Cotyledons Hypocotyls, leaf disks Cotyledons
a
B
ansformation of tomato; obacterium strain hizogenes (DCAR-2) umefaciens (LBA4404) umefaciens (NA)umefaciens (LBA4404)umefaciens (C58C1) umefaciens (EHA105) umefaciens (LBA4404) umefaciens (EHA105) umefaciens (LBA4404) umefaciens (LBA4404) umefaciens (LBA4404) umefaciens (LBA4404) umefaciens (EHA105) umefaciens (AGL1) umefaciens (EHA101) umefaciens (LBA4404)
c tr Agr A. r A. t A. t A. t A. t A. t A. t A. t A. t A. t A. t A. t A. t A. t A. t A. t
eti
n
ated to the optimization of ge Transformation method Agrobacterium-mediated Agrobacterium-mediated AgroinjectionAgrobacterium-mediatedAgrobacterium-mediated Agrobacterium-mediated Agrobacterium-mediated/biolistic gun Agro-infiltration Agrobacterium-mediated Agrobacterium-mediated Agrobacterium-mediated Agrobacterium-mediated Agrobacterium-mediated (in planta transformation); Agro-infiltration Agrobacterium-mediated Agrobacterium-mediated Agrobacterium-mediated
el
Examples of studies rTable 1 Cultivar S. lycopersicum Momotaro, UC-97 and EdkawiS. lycopersicum UC82B S. lycopersicum Micro TomS. lycopersicum LichunS. lycopersicum Micro Tom S. lycopersicum Micro Tom S. lycopersicum CastleRock S. lycopersicum (NA) S. lycopersicum Cambell-28 S. lycopersicum Moneymaker S. lycopersicum Zhongshu No.4S. lycopersicum Rio Grande S. lycopersicum Rio Grande S. lycopersicum Pusa Ruby, Sioux, Arka Vikas S. lycopersicum Roma, Rio Grande S. lycopersicum Bina tomato-3, Bina tomato-5, Bahar, PusaRuby
1 3
Plant Growth Regul (2017) 83:175–198 179
1)
1
References Kaur and Bansal (2010) Paramesh et al. (2010) El-Siddig et al. (2011) Cruz-Mendivil et al. (20 Widoretno et al. (2012) Guo et al. (2012) Janani et al. (2013) Chetty et al. (2013) Koul et al. (2014) Shah et al. (2015) Sun et al. (2015)
Transformation efficiency Transformation fre-quency > 37% NA Transformation frequency 7% Transformation frequency 19.1% Regenerated hairy roots at frequency range from 33 to 59% Transformation frequency 5.1% NA Transformation efficiency 65% (GV3101), 40% (EHA105), 35% (AGL1), 15% (MP90) Transformation efficiency ranged from 3.17 to 21.38% for (cotyledon)21.83 to 35.70% for leaf explants in tomato cultivar PED Transformation efficiency 5.49, 7% (Roma) (Mon-eymaker) ; 8.28% (Rio Grande) Transformation efficiency 40%
3
Explant type Cotyledons Cotyledons, hypocotyls Hypocotyls, cotyledons Leaf Hypocotyls Cotyledons Leaf section and shoot tips Cotyledons Cotyledons; leaf Shoot apical meristems of days old seedlings Hypocotyls, cotyledons
4)
Agrobacterium strain A. tumefaciens (GV3101) A. tumefaciens (GV2260)A. tumefaciens (LBA4404)A. tumefaciens (EHA105) A. rhizogenes (ATCC 1583 A. tumefaciens (EHA105) A.tumefaciens (LBA4404)A. umefaciens (AGL1, EHA105, GV3101, and MP90) A. tumefaciens (LBA4404) A. tumefaciens (EHA105) A. tumefaciens (LBA4404)
d d d d d d d d d d d
d e e e e e e e e e e e
metho mediat mediat mediat mediat mediat mediat mediat mediat mediat mediat mediat
on m- m-m-m- m- m- m-m- m- m- m-
mati eriu eriu eriu eriu eriu eriu eriu eriu eriu eriu eriu
nsfor obact obact obact obact obact obact obact obact obact obact obact
Tra Agr Agr Agr Agr Agr Agr Agr Agr Agr Agr Agr
a a
5) us m
(continued)Table 1 Cultivar S. lycopersicum Pusa Ruby,Pusa Uphar, DT-93S. lycopersicum Megha (L1S. lycopersicum SummerS. lycopersicum Micro Tom S. lycopersicum (NA) S. lycopersicum Micro Tom S. lycopersicum ShalimarS. lycopersicum Micro Tom S. lycopersicum Pusa early dwarf (PED), Pusa 120, Phybrid 1, S22, Pusa Ruby and Gaurav S. lycopersicum cv.Rio Grande, Moneymaker, Ro S. lycopersicum Hezuo 908 NA not available
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1 80 Plant Growth Regul (2017) 83:175–198
to wild-type (WT) plants. Although the flowers on these problem, scientists have recruited transient transformation
plants appeared earlier and were normal, unfortunately they methodologies. Such an approach can assure fast imple-
were sterile and did not give fruits (Yasmeen et al. 2009). mentation of the functional analysis of the genes of inter-
So far, this methodology has not been broadly employed in est (GOI) (Wróblewski et al. 2005; Fernandez et al. 2009).
tomato transformation. However, Safdar and Mirza (2014) Fundamental progress in rapid reverse genetics was accom-
performed a comparison of transformation through tis- plished by employing RNAi (RNA interference) strategy
sue culture and in planta transformation using an in vitro (Orzaez and Granell 2009; Fernandez-Moreno et al. 2013).
fruit injection method and in vivo fruit and flower injection. In plants, RNAi can be induced in two ways: by a transgene
The results clearly showed superiority of the in vitro fruit (TIGS, transgene induced gene silencing) or a virus (VIGS,
injection method in comparison to conventional methods. virus-induced gene silencing). The first approach was used
Recently, Shah et al. (2015) successfully employed an in for instance to silence gene vis1 (viscosity) in tomato fruit
planta method to obtain cold resistant tomato. Optimization to obtain transgenic lines with delayed ripening under heat
of the transformation parameters allowed to obtain trans- stress (Metwali et al. 2015). Since VIGS represents a use-
formation efficiency of about 8%. ful tool for the identification of gene function, in the other
Tomato engineering via A. rhizogenes was reported approach different types of viruses (e.g. TRV, Tobacco Rat-
by Widoretno et al. (2012) and regeneration of transgenic tle Virus) were successfully used as the VIGS vectors and,
tomato plants from hairy roots by Peres et al. (2001) and among them, the TRV vector gave the most robust results
Moghaieb et al. (2004). As the results showed, regeneration in terms of ease of application, efficiency, and absence of
from hairy roots was possible; however, the considerable disease symptoms (Jaberolansar et al. 2010; Romero et al.
differences in morphogenic responses were revealed. Hairy 2011; Wang et al. 2015). Moreover, Wang et al. (2015)
root-originated plants were characterized by creased leaves, demonstrated that this technology enabled achieving up to
shortened internodes, plentiful root system; they produced 100% VIGS efficiency in different tomato organs (leaves,
flowers (Peres et al. 2001) and fruits with a reduced num- flowers and fruits). Zhou et al. (2012) applied Potato Virus
ber of seeds (Moghaieb et al. 2004). Hairy root culture X in VIGC technology (virus-induced gene complemen-
appeared as an alternative system for producing biop- tation) and determined functions of some TFs involved
harmaceutical compounds in tomato plants. De Guzman in regulation of fruit ripening genes in tomato fruits (rin
et al. (2011) achieved production of the Escherichia coli mutant).
B-subunit heat labile toxin antigen in tomato hairy root cul-
tures (approximately 10 µg/g blotted weight, BW). Unfor-
tunately, numerous attempts to obtain regenerated plants Genetic engineering approaches and achievements
from hairy root cultures were unsuccessful.
In addition to the aforementioned methods, the particle The growing environmental stresses of the modern world
bombardment method was also used for tomato transfor- constitute a serious problem for global productivity of
mation (Cueno et al. 2010). Ruma et al. (2009) performed crop plants. Obviously, abiotic stress factors unfavourably
experiments to equalize crucial factors (e.g. firing distance, impact the whole physiology of plants by changing their
quantity of DNA, concentration of osmoticum, pre-bom- metabolism, growth and development (Mishra et al. 2012).
bardment and post-bombardment culture periods) which Therefore, the genetic engineering of crop plants aiming
resulted in significant transformation efficiency in different at enhancement of tolerance to different environmental
tomato explants. stresses has recently gained great significance. In contrast
The particle bombardment approach was also used in to the traditional selective breeding, genetic modifica-
the elaboration of stable genetic transformation methodol- tion (GM technology) allows for faster and more effective
ogy of tomato plastids that seemed to be a crucial step in obtaining of plants (including tomato) tolerant to abiotic
the transformation of tomato (Ruf and Bock 2014). This stresses, resulting in increased food supply. To date, there
recently established transformation technology enabled have been many attempts to increase plant tolerance to a
investigation aiming at improvement of the nutrient content wide range of stress factors (e.g. salinity, drought, heavy
in tomato (e.g. vitamin A, β-xanthophylls) (Apel and Bock metals, oxidative stress). These approaches included intro-
2009; D’Ambrosio et al. 2011), as well as biopharmaceuti- duction of various genes involved in regulatory and signal-
cal production (e.g. HIV antigens p24) (Zhou et al. 2008). ling pathways, as well as stress-mitigating enzymes (Vin-
While several protocols for stable transformation of cour and Altman 2005). Modifications of genes encoding
tomato plants have been recently developed (Hasan et al. functional and structural proteins were also made (Table 2).
2008; Sharma et al. 2009; Koul et al. 2014), there is still Here, some examples of genetic modifications of target
lack of reliable and effective procedure to help with sequences encoding molecules involved in stress adaptation
the functional analysis of transgene. To cope with this are presented.
1 3
Plant Growth Regul (2017) 83:175–198 181
5)
0
0
2
13) cia (
0 a
Refernences Khare et al. (2010) Park et al. (2006) Herbette et al. (2005) Álvarez-Viveros et al. (2 Wang et al. (2014) Yu et al. (2009) Dominguez et al. (2010) Liu et al. (2010) Liu et al. (2013) Goel et al. (2010) Patade et al. (2013) Wang et al. (2011) Cheng et al. (2009) Gong et al. (2015) Cortina and Culianez-M
Results Enhanced tolerance to cold, drought and salt Enhanced tolerance to chilling Modification of phohotosynthetic regulation; imparted chilling toler-ance Enhanced tolerance to salt Enhanced tolerance to salinity Enhanced tolerance to chilling Enhanced tolerance to cold; an increase in the 18:3/18:2 ratio in leaves and fruits Enhanced tolerance to high tempera-ture; reductions of trienoic fatty acids Enhanced tolerance to low tempera-ture; enhanced tolerance to cold Enhanced tolerance to salt and drought Enhanced tolerance to cold Enhanced tolerance to dehydratation and drought Enhanced tolerance to high tempera-ture Enhanced tolerance to alkali stress Enhanced tolerance to drought and salt but undesirable changes in plant morphology
y)
a
o pr
abiotic stresses in tomat Expression Overexpression Exogenous aplication (s Overexpression Overexpression Overexpression Overexpression Overexpression Antisense expression Overexpression Overexpression Overexpression Overexpression Overexpression Overexpression Overexpression
ploited to enhance/improve tolerance to Function Mannitol synthesis Metabolite function as stress protect-ant Gluthatione biosynthesis Detoxification system enzymes catalyze the conversion of methyl-glyoxal Regulation of fatty acid unsaturation of membrane lipids (catalyze the conversion of linoleic acid (18:2) to linolenic acid (18:3)) Regulation of fatty acid unsaturation of membrane lipids (catalyze the-conversion of linoleic acid (18:2) to linolenic acid (18:3)) Regulation of fatty acid unsaturation of membrane lipids (catalyze the-conversion of linoleic acid (18:2) to linolenic acid (18:3)) Regulation of fatty acid unsaturation of membrane lipids Regulation of fattyacid unsaturation of membrane lipids Osmotin accumulation (provides osmotolerance) Osmotin accumulation (provides osmotolerance) Involved in PAs biosynthesis Involved in PAs biosynthesis Catalyzes the conversion of ATP and L methionine into S-adenosylme-thionine which is involved in PAs and ethylene biosynthesis Involved in trehalose biosynthesis
x
e
s
e
n
e
g
e d
Examples of diversTable 2 Gene/origin mt1DE. coli/ Glycine betaine GPXMus musculus/ GlyIGlyIIB. juncea and - anP.glaucum LeFAD3/tomato LeFAD3/tomato FAD3rape FAD7potato// LeFAD7/tomato LeFAD7/tomato Osmotin/tobacco Osmotin/tobacco PtADCP.trifoliata/ SAMDC/yeast SlSAM1/tomato ScTPS/yeast
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1 82 Plant Growth Regul (2017) 83:175–198
1)
1
0
2
Refernences Lyu et al. (2013) Grichko and Glick (2001) Gisbert et al. (2000) Garcia-Abellan et al. (2014) Olias et al. (2009) Leidi et al. (2010) Huertas et al. (2013) Bhaskaran and Savithramma Yarra et al. (2012) Hu et al. (2012) Sade et al. (2009) Sade et al. (2010) Kadyrzhanova et al. (1998) Nautiyal et al. (2005) Mahesh et al. (2013) Zhao et al. (2007) Wang et al. (2006) Duan et al. (2012) Mohamed et al. (2003)
Results Enhanced tolerance to drought and salt without any growth aberrations Enhanced tolerance to salt and water logging (degradation of ethylene by ACC deaminase) Enhanced tolerance to salinity Enhanced tolerance o salinity Enhanced tolerance salinity Enhanced tolerance to salinity Enhanced tolerance to salinity Enhanced tolerance to salinity Enhanced tolerance to salinity Enhanced tolerance drought Enhanced tolerance to drought Enhanced tolerance to salinity (improving WUE, hydraulic con-ductivity, and yield production) Enhanced tolerance to chilling Enhanced tolerance to high tempera-ture Enhanced tolerance to high tempera-ture Improved tolerance to tunicamycin-ER Enhanced tolerance to heat and UV-B enhanced tolerance to cold Improved tolerance to photo-oxida-tive stress caused by drought
n n n n n n n n n n n n n
o o o o o o n o o o o o o o
ession expressi expressi expressi expressi ession expressi expressi xpressio expressi expressi expressi expressi ession ession ession ession expressi expressi expressi
xpr ver ver ver ver xpr ver ver o-e ver ver ver ver xpr xpr xpr xpr ver ver ver
E O O O O E O O C O O O O E E E E O O O
Function Involved in trehalose biosynthesis Non-plant enzyme that metabolizes ACC +Changed ions homeostasis both Na +and K Maintained ions homeostasis both ++ Na and K Maintained ions homeostasis both ++ Na and K Ion transport. Compartmentalization **of NA and K in vacuoles Ion transport; compartmentalization of ions+ in Compartmentalization of Navacuoles Ion transport; compartmentalization of ions Maintenance of ion homeostasis Involved in plant water balance Involved in plant water balance Involved in temperature-responsive stress mechanism (accumulation of heat shock proteins) Involved in temperature-responsive stress mechanism (accumulation of heat shock proteins) Involved in temperature-responsive stress mechanism (accumulation of heat shock proteins) Accumulation of heat shock proteins during antibiotic treatment Detoxification—removed HO22 Detoxification—stimulating the conversion of HO into HO222 Oxidative stress (catalase)
oli
c
(continued)Table 2 Gene/origin TPSP (TPSTPPE. / fusion gene)/ ACC deaminaseEnterobacter /cloacae HAL1/yeast HAL5/yeast SISOS1/tomato AtNHX1A.thaliana/ LeNHX2/tomato AVP1 and PgNHX1P.glaucum/ TaNHX2/wheat MdVHA-B/appleSlTIP2;2/tomatoNtAQP1/tobacco LeHSP 17.6/tomato MT-sHSP/tomato MasHSP24.4Musa acuminata/ LeHSP21.5/tomato cAPX/pea LetAPX/tomato katEE. coli/
1 3
Plant Growth Regul (2017) 83:175–198 183
4)
Refernences Wang et al. (2007) Baranova et al. (2010) Hu et al. (2015a) Thipyapong et al. (200 Orellana et al. (2010) Huang et al. (2004) Pan et al. (2010) Seong et al. (2007) Vannini et al. (2007) Meng et al. (2015) Mishra et al. (2012) Hsieh et al. (2002) Singh et al. (2011) Rai et al. (2013a) Shah et al. (2015) Miura et al. (2012)
Results Improved tolerance to salt and oxida-tive stress (caused by herbicide methyl viologen) Enhanced tolerance to oxidative stress (caused by UV irradiation); enhanced the stability of the photo-synthetic apparatus Conferred tolerance to chilling Improved tolerance to water Improved tolerance to water and salt Improved tolerance to osmotic stress caused by salt Enhanced tolerance to salt (changed agronomic features: higher produc-tion of flowers, fruits, seeds) Enhanced tolerance to salt and oxida-tive stress Enhanced tolerance to drought but no tolerance to cold Improved tolerance to heat Enhanced tolerance to drought with reduction in the plant growth rate Improved tolerance to cold with undesirable changes such as stunned growth, a reduced fruit size, reduced seeds number per fruit Improved tolerance without any growth aberrations Improved tolerance to drought Improved tolerance to cold Enhanced tolerance to cold
A
9
D2 of
n n n n n n n n n n der control of R n under control moter n of under Lip9 n
xpression verexpressio verexpressio xpression verexpressio verexpressio verexpressio verexpressio verexpressio verexpressio verexpressio verexpressio xpression xpression unpromoter verexpressioRD29A pro verexpressiopromoter verexpressio
E O O E O O O O O O O O E E O O O
Function Alleviates oxidative stress (conver-−sion O to HO and O)2222 Alleviates oxidative stress (conver-−sion O to HO and O)2222 Maintain cellular redox homeostasis Photoreduction of O by PSI2 TF, regulation stress-related genes (abiotic and biotic stress) Ethylene responsive TF, integrates ethylene and osmotic stress path-ways Ethylene responsive TF; transcrip-tional regulation Influence antioxidant system Transcription of stress-related gene Induced the up-regulation of several structural genes in the anthocyanin biosynthetic pathway and anthocya-nin accumulation Transcriptional regulation; a TF viainduced during drought stress a mechanism that requires production of ABA TF, transcriptional regulation TF, transcriptional regulation TF, transcriptional regulation; influ-ence on enzymatic antioxidant system TF, transcriptional regulation stress-related genes TF, transcriptional regulation
a
sis an
(continued)Table 2 Gene/origin Mn-Hevea brasilienSOD/ FeSODA.thaliana/ AtGRXA.thaliana/ PPO/potatoSlAREB1/tomato TERF1 SlERF3DRD/tomato CaKR1/pepper Osmyb4/rice LeAN2/tomato ATHB-7A.thaliana/ CBF1A.thaliana/ AT-CBF1A.thaliana/ AtDREB1ACBF3A.thali// AtDREB1AA.thaliana/ SlICE1/tomato
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1 84 Plant Growth Regul (2017) 83:175–198
2)
1
0
Refernences Rai et al. (2013b) Shah et al. (2013) Li et al. (2015) Rochange et al. (2001) Muñoz-Mayor et al. (2 Liu et al. (2015) Li et al. (2016) Hu et al. (2015b) Yang et al. (2015)
Results Enhanced tolerance to drought Enhanced tolerance to heat Enhanced tolerance Impairment under salt and ABA stress with growth aberrations (dwarfish plants, seedlings with altered hypocotyl) Enhanced tolerance to drought and salinity without any growth aber-rations Improved tolerance to cold, drought and salinity Enhanced tolerance to chilling Enhanced tolerance to salt Increased sensitivity to osmotic stress
n n n n n n n n n
o o o o o o o o o
si si si si si si si si si
ession expres expres expres expres expres expres expres expres expres
pr er er er er er er er er er
x v v v v v v v v v
E O O O O O O O O O
Function TF, encodes a C2H2 zinc finger pro-tein, transcriptional regulation TF, encodes a C2H2 zinc finger pro-tein, transcriptional regulation TF, transcriptional regulation stress-related genes Accumulation expansin- protein with ability to stimulate wall loosening during cell expansion Accumulation of protein with chaper-one-like and detergent properties Accumulation of protein with chaper-one-like and detergent properties Regulation ROS homeostasis through activation of cellular antioxidant systems; modulating the transcrip-tion of stress associated genes Signal transduction proteins; influ-ence on ion-driving transport mechanisms Involved in regulation abscisic acid signaling, involved in osmotic stress signal transduction
o
at
m
o
2/t
2.
s K
e R
d) ait Sn
(continueTable 2 Gene/origin ZAT12B. carinata/ ZAT12B.carinata/ SpWRKY1/tomato CsExp1/cucumber tas14/tomato ShDHNS. habroch/ SlMPK7/tomato MdSOS2L1/apple SlSnRK22.1Sl and
1 3