Clemson University Clemson University TigerPrints TigerPrints All Theses Theses August 2021 Constitutive Expression of the Inositol Polyphosphate 5- Constitutive Expression of the Inositol Polyphosphate 5- Phosphatase Gene Alters Plant Development and Enhances Phosphatase Gene Alters Plant Development and Enhances Abiotic Stress Tolerance in Creeping Bentgrass Abiotic Stress Tolerance in Creeping Bentgrass Chen Chang Clemson University, [email protected]Follow this and additional works at: https://tigerprints.clemson.edu/all_theses Recommended Citation Recommended Citation Chang, Chen, "Constitutive Expression of the Inositol Polyphosphate 5- Phosphatase Gene Alters Plant Development and Enhances Abiotic Stress Tolerance in Creeping Bentgrass" (2021). All Theses. 3587. https://tigerprints.clemson.edu/all_theses/3587 This Thesis is brought to you for free and open access by the Theses at TigerPrints. It has been accepted for inclusion in All Theses by an authorized administrator of TigerPrints. For more information, please contact [email protected].
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Clemson University Clemson University
TigerPrints TigerPrints
All Theses Theses
August 2021
Constitutive Expression of the Inositol Polyphosphate 5- Constitutive Expression of the Inositol Polyphosphate 5-
Phosphatase Gene Alters Plant Development and Enhances Phosphatase Gene Alters Plant Development and Enhances
Abiotic Stress Tolerance in Creeping Bentgrass Abiotic Stress Tolerance in Creeping Bentgrass
Follow this and additional works at: https://tigerprints.clemson.edu/all_theses
Recommended Citation Recommended Citation Chang, Chen, "Constitutive Expression of the Inositol Polyphosphate 5- Phosphatase Gene Alters Plant Development and Enhances Abiotic Stress Tolerance in Creeping Bentgrass" (2021). All Theses. 3587. https://tigerprints.clemson.edu/all_theses/3587
This Thesis is brought to you for free and open access by the Theses at TigerPrints. It has been accepted for inclusion in All Theses by an authorized administrator of TigerPrints. For more information, please contact [email protected].
1. Molecular analysis of TG lines overexpressing InsP 5-ptase gene........................24 2. Development of wild-type (WT) and transgenic (TG) plants ................................27 3. Response of wild-type (WT) and transgenic (TG) plants to drought stress ..........34 4. Response of wild-type (WT) and transgenic (TG) plants to heat stress ................38 5. Response of wild-type (WT) and transgenic (TG) plants to salt stress .................41 6. A model of the IP3-mediated signaling pathway and the
1. Primer sequences were used in this study ..............................................................48 2. The mediums were used in this study ....................................................................48
1
CHAPTER ONE
LITERATURE REVIEW
Abiotic Stress
Although it is difficult to accurately estimate the impacts of abiotic stress on crop
production, it has become evident that the number of publications on the effects of abiotic
stress on plants has increased dramatically in recent years. In early 1982, Boyer foreboded
that the environmental factors may limit crop production by as much as 70% (Boyer et al.,
1982, Cramer et al., 2011). According to the 2007 FAO report, the global land area not
affected by environmental constraints only occupies 3-5%. With the reduction of arable
land, the decline of water resources, increased global warming due to the climate changes,
it is expected that the outputs of crops will dramatically decline in many areas in the future
(Colville et al., 2011; Cramer et al., 2011).
Abiotic stress is considered the negative effect of non-living factors on living things
in a specific environment (Ben-Ari et al., 2012). Most of the abiotic stresses for plants are
caused by the soil factors, such as the high concentration of salt; air pollution, such as acid
2
rain; and climate changes, which is considered the most critical factor, incurring various
stresses, such as drought and heat (Phil Riddel et al., 2003). Abiotic stresses, especially
salinity and drought, are considered the leading causes of global crop yield loss. Contrary
to the resistance of plants to biotic stresses (mainly depending on monogenic traits), the
genetically complex response to abiotic stresses is multigenic and more challenging to
identify and manipulate (Ben-Ari et al., 2012).
Plants need a lot of water and nutrients throughout their life cycle, and all aspects of
plant development will be affected by the reduction of water content in the soil (Sarker et
al., 2005). Drought can lead to nutrient deficiencies (even in the fertilized soil) due to the
decreased mobility and absorption of individual nutrients, leading to the reduced diffusion
rate of minerals from the soil matrix to the roots (Silva et al., 2001). Therefore, drought is
undoubtedly the most important stress factor that limits plant life. Drought can trigger a
variety of plant responses (Anjum et al., 2011). Plant growth changes, which are translated
into reduced leaf size, reduced leaves, less fruit yield, and changes in reproductive stages.
At the same time, excessive salt concentrations have a significant impact on plants. It can
cause osmotic stress and ion imbalance due to the accumulation of toxic ions (such as Cl-
and Na+). Salt stress also hurts mineral homeostasis, especially Ca2+ and K+ (Isayenkov et
al., 2012). In addition, high temperatures can cause significant damage to plants. At very
high temperatures, plants may suffer from severe cellular damage and even cell death
3
within minutes (Schöffl et al., 1999). Injuries or death occur in plants after long-term
exposure to moderately high temperatures. Direct damages caused by high temperatures to
plants include protein denaturation and increased membrane lipids fluidity. Indirect
thermal damages include inhibition of protein synthesis, protein degradation, inactivation
of enzymes in chloroplasts and mitochondria, and damage of membrane integrity (Howarth,
2005). These damages ultimately lead to growth inhibition, reduced ion flux, and
production of toxic compounds (Schöffl et al., 1999, Howarth, 2005). Therefore, tackling
the impact of drought, salinity, and high temperatures in agriculture is essential for
achieving food security worldwide (Rizwan et al., 2015). In the long-term evolution, plants
have formed many molecular, cellular, and physiological mechanisms to deal with these
abiotic stresses.
The Response of Plants to Stresses
The first step in plant response to abiotic stress is the perception of stress. Once plant
cells sense stresses, the signal is transmitted by second messengers, such as calcium ions,
nitric oxide (NO), reactive oxygen species (ROS), and different protein kinases (Kudla et
al., 2018; Testerink et al., 2011). Stress-induced increase in cytosolic Ca2+ concentration
4
can be detected in Arabidopsis guard cells within 15 seconds after osmotic stress treatment
(Yuan et al., 2014). The Ca2+ can then be detected by calcium-binding proteins, which
usually transfer the signal to interacting protein kinases, such as calcium-dependent protein
kinases (CPKs). ROS in plants can be accumulated by various organelles, such as
chloroplasts, mitochondria, and peroxisomes (Zhang et al., 2020). The accumulated ROS
can stimulate specific calcium and electrical signals, and also mediate transductions of
systemic signals in response to stress immediately (Choi et al., 2016). Various abiotic
stresses also promote phosphatidic acid (PA) production, which plays a positive or negative
role under different stress conditions (Hong et al., 2016; Testerink et al., 2011). In addition,
plants accumulate many organic and inorganic compounds such as amino acids (proline),
normal sugars (sucrose), and organic acids (oxalic acid) to protect cellular proteins under
stress conditions (Valliyodan et al., 2006). These osmoprotectants protect plant cells under
stress without affecting the biochemistry of the cellular environment (Kaur et al., 2020).
Stress signals in plants also involve different kinase families, including kinase families in
the mitogen-activated protein kinase (MAPK) module (Zelicourt et al., 2016)). For
example, MPK3, MPK4, and MPK6 can be activated within 2 minutes after exposure to
drought and salt stresses (Zhang et al., 2020). It is obvious that signaling transductions are
crucial during the entire regulation process of plants response to stress.
5
There are many types of signaling pathways in plant response to stresses, and the ABA
signaling pathway is one of them. The stress-induced biosynthesis of ABA mainly occurs
in vascular tissues, but ABA exerts its impact in various cells (Kuromori et al., 2010).
Therefore, the ABA response needs to be transferred from ABA-producing cells via cell-
to-cell transport to allow distribution into adjacent tissues rapidly (Danquah et al., 2014).
Under osmotic stress conditions, ABA can regulate expression of many genes. The ABA
response element (ABRE) is the main cis-element for ABA response to many gene
altered plant development with reduced leaf clippings and less chlorophyll production (Fig.
2s, j). This is different from previous studies in transgenic Arabidopsis (Perera et al., 2008).
Overexpression of InsP 5-ptase did not adversely affect plant growth. TG Arabidopsis had
less ABA accumulation than WT controls (Perera et al., 2008). ABA is an important plant
hormone that can inhibit plant growth (Nambara et al., 2017). Interestingly, the reduced
ABA accumulation in TG Arabidopsis did not show impaired plant growth. On the contrary,
InsP 5-ptase TG creeping bentgrass had reduced leaf clippings and decreased internode
length, especially in the group 2 TG plants (Fig. 2s, m). Most likely, the overexpression of
the InsP 5-ptase gene may have led to modified IP3 level in TG plants, altering ABA
biosynthesis, which negatively impacts plant growth. The fact that group 2 TG creeping
bentgrass exhibited more severely impacted internode growth than group 1 TG plants
indirectly supports this hypothesis. Further analysis of ABA level in TG plants compared
43
to WT controls would provide information to better understand impacted plant growth by
IP3-ABA module.
In this study, we also observed that TG plants exhibited a reduced chlorophyll content,
especially in group 2 TG plants, displaying a pale green leaf color (Fig. 2). It has previously
been shown that TG tomato plants with increased InsP3 hydrolysis in the cytosol exhibited
increased net CO2-fixation in source leaves (Khodakovskaya et al., 2010). Interestingly,
the rate of CO2-fixation in soybean was found to be four times faster in pale green plants
than in dark green plants (Koller et al., 1974). We speculate that a higher InsP 5-ptase
expression level in group 2 TG creeping bentgrass may cause more IP3 hydrolysis, leading
to impaired chlorophyll biosynthesis and therefore pale-green leaf color. It might also result
in more and faster net CO2-fixation. Further analysis of TG plant IP3 level and CO2-fixation
rate would provide evidence validating this hypothesis.
Enhanced Drought and Heat Resistance in TG Creeping Bentgrass Overexpressing InsP
5-ptase Is Likely Associated with Up-regulated DREB2A Expression
In the present study, TG creeping bentgrass overexpressing InsP 5-ptase exhibited
significantly enhanced drought (Fig. 3) and heat tolerance (Fig. 4). This is consistent with
44
a previous observation in TG Arabidopsis overexpressing InsP 5-ptase, which also
exhibited enhanced drought resistance (Perera et al., 2008). The enhanced drought
resistance was found to be associated with an up-regulated expression of DREB2A, a
dehydration-responsive element-binding protein 2A transcription factor gene (DREB2A)
(Perera et al., 2008). DREB2A was found to be highly expressed in drought and salt
treatment in an ABA-independent pathway (Liu et al., 1998). The intact DREB2A protein
cannot activate downstream genes under normal conditions. It needs posttranslational
modification to remove the negative regulatory region (NRD) for activation (Sakuma et al.,
2006). Similarly, we speculate that the enhanced drought and heat resistance in TG
creeping bentgrass overexpressing InsP 5-ptase was likely caused by IP3-mediated up-
regulation of the DREB2A gene, triggering downstream drought and heat resistance gene
expression.
In addition, InsP 5-ptase TG creeping bentgrass showed an enhanced drought
tolerance associated with a lower proline accumulation and a non-suppressed stomatal
conductance. This was probably because the three-day water withholding was perceived as
normal condition to TG plants, so the mechanisms regulating proline accumulation and
stomatal conductance change did not need to be activated to protect themselves from
drought stress. In fact, the increased IP3 hydrolysis in TG plants would cause a decreased
Ca2+ signaling and lead to non-suppression of H+-ATPases and inward-rectifying K+
45
channels, and therefore causing the suppression of stomatal closure (Fig. 6) (Blatt et al.,
1990; Lemtiri-Chlieh et al., 1994; Kim et al., 2010).
Figure 6. A model of the IP3-mediated signaling pathway and the InsP 5-ptase-regulated
stomatal closure. The stress-stimulated ABA signals, the first messenger, are received by
G protein, which then activates phospholipase C (PLC) to hydrolyze PIP2 into IP3 and DAG
(secondary messengers), triggering the transfer of more Ca2+ ions into the cytoplasm to
cause plant cell response to stresses. Meanwhile, the Ca2+ signal will inhibit the inward-
46
rectifying K+ channel to induce stomatal closure, while the InsP 5-ptase induces the
inhibition of stomatal closure by reduced IP3. The blue arrows are the regular regulations
of WT under drought stress, while the red arrows are the plants overexpressing InsP 5-
ptase.
Enhanced Salt Tolerance in the TG Creeping Bentgrass Overexpressing InsP 5-ptase May
be Associated with Altered ROS Production and Salt-responsive Gene Expression
Our results also showed that TG creeping bentgrass overexpressing InsP 5-ptase
exhibited enhanced salt tolerance (Fig. 5). It has previously been reported that the T-DNA
insertion mutant of Arabidopsis thaliana Inositol Polyphosphate 5-Phosphatase7
(At5PTase7) gene increased salt sensitivity, whereas overexpression of At5PTase7 in TG
plants increased salt tolerance (Kaye et al., 2011). Ten to fifteen minutes after salt treatment,
the At5PTase7 mutant Arabidopsis plants exhibited reduced production of ROS in roots.
In addition, the expression of salt-responsive genes (such as RD29A and RD22) was not as
highly induced in the mutants as in the wild type under salt stress (Golani et al., 2013).
This suggests the important role InsP 5-ptase gene play in regulating ROS accumulation in
plants and the expression of stress-related genes, such as RD29A and RD22. Most likely,
47
Overexpression of InsP 5-ptase gene in TG creeping bentgrass impacted plant ROS balance
and the expression of RD29A and RD22 or other stress-related gene, leading to improved
salt tolerance. Further analysis of ROS accumulation and different stress-related gene
expression in TG creeping bentgrass compared with WT controls would provide
information to better understand the molecular mechanisms underlying IP3-mediated plant
salt tolerance.
48
Table 1. Primer sequences were used in this study.
Table 2. The mediums were used in this study.
49
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