University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln eses, Dissertations, and Student Research in Agronomy and Horticulture Agronomy and Horticulture Department 8-2019 Hormonal Signaling Induced in Soybean by Lysobacter enzymogenes Strain C3 Jessica C. Walnut University of Nebraska-Lincoln Follow this and additional works at: hps://digitalcommons.unl.edu/agronhortdiss Part of the Agricultural Science Commons , Agriculture Commons , Agronomy and Crop Sciences Commons , Botany Commons , Horticulture Commons , Other Plant Sciences Commons , and the Plant Biology Commons is Article is brought to you for free and open access by the Agronomy and Horticulture Department at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in eses, Dissertations, and Student Research in Agronomy and Horticulture by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Walnut, Jessica C., "Hormonal Signaling Induced in Soybean by Lysobacter enzymogenes Strain C3" (2019). eses, Dissertations, and Student Research in Agronomy and Horticulture. 173. hps://digitalcommons.unl.edu/agronhortdiss/173
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University of Nebraska - LincolnDigitalCommons@University of Nebraska - LincolnTheses, Dissertations, and Student Research inAgronomy and Horticulture Agronomy and Horticulture Department
8-2019
Hormonal Signaling Induced in Soybean byLysobacter enzymogenes Strain C3Jessica C. WalnutUniversity of Nebraska-Lincoln
Follow this and additional works at: https://digitalcommons.unl.edu/agronhortdiss
Part of the Agricultural Science Commons, Agriculture Commons, Agronomy and CropSciences Commons, Botany Commons, Horticulture Commons, Other Plant Sciences Commons,and the Plant Biology Commons
This Article is brought to you for free and open access by the Agronomy and Horticulture Department at DigitalCommons@University of Nebraska -Lincoln. It has been accepted for inclusion in Theses, Dissertations, and Student Research in Agronomy and Horticulture by an authorizedadministrator of DigitalCommons@University of Nebraska - Lincoln.
Walnut, Jessica C., "Hormonal Signaling Induced in Soybean by Lysobacter enzymogenes Strain C3" (2019). Theses, Dissertations, andStudent Research in Agronomy and Horticulture. 173.https://digitalcommons.unl.edu/agronhortdiss/173
2.3 Results………………………………………………………………………………..78 2.3.1 Localized induction of a defense response upon C3 treatment…………….78 2.3.2 Localized induction of SA pathway upon C3 treatment………………….…78 2.3.3 Localized induction of JA and ET pathways upon C3 treatment ………….80 2.3.4 Systemic induction of defense hormones upon C3 root treatment…….……82
2.4 Discussion………………………………………………………………………........83 2.5 Literature cited……………………………………………………………………….88 2.6 Table………………………………………………………………………………….94
1.0E1 yielded up to 76.92% , but the more stringent the E-value such that; <1.0E180,
there was only1.80% homology between Arabidopsis and soybean (Tian et al., 2004).
Approximately 49.3% (21,299) soybean unigenes could not be corresponded to proteins
from Arabidopsis, likely due from further genome duplication events in Soybean and
other possible mutations since its divergence from Arabidopsis (Tian et al., 2004).
Functional compatibility of some Arabidopsis genes with soybean identified genes that
may be used to engineer resistance to nematodes. AtPAD4 and GmPAD4 (soybean
homolog) share 41.8% amino acid identity, so the sequence is considered moderately
conserved (Youssef et al., 2013).
To determine whether this homology leads to conserved functionality between the
two, Youssef et al, transformed soybean plants to express AtPAD4 gene in soybean roots.
Transformed soybean plants were able to express AtPAD4. In addition, transformed
soybeans that overexpressed AtPAD4 and AtPR1 compared to the empty vector plants
were more resistant to Soybean cyst nematode and root knot nematode (Youssef et al.,
2013). To examine if Arabidopsis genes could confer resistance to Soybean Cyst
Nematode (Heterodera glycines), Matthews et al., (2014) inserted Arabidopsis defense
genes into soybean seedlings via Agrobacterium mediated transformation. Soybean
seedlings overexpressing SA related defense genes (AtNPR1, AtTGA2, and AtPR-5)
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exhibited a 60% decrease in cysts. Another study tested whether the insertion of a
soybean gene GmEREBP1, encoding a transcription factor, into Arabidopsis would be
successful in eliciting downstream signaling. In soybeans GmEREBP1 localizes to the
nucleus to induce expression of PR2, PR3, PR1 an ET regulated gene, a JA and ET
regulated gene, and a SA regulated gene respectively (Mazarei et al., 2007). When
GmEREBP1 was inserted into the Arabidopsis genome, the expression profile of
downstream genes exhibited some conserved signaling (Mazarei et al., 2007). For
example, AtPDF1.2 and AtPR3 were up regulated as well as SA responsive gene AtPR1.
However, PR2 was not upregulated as it was in soybean (Mazarei et al., 2007). This
discrepancy could stem from PR2 being regulated by ethylene in soybeans and salicylic
acid in Arabidopsis. Even though there are some successful examples of soybean and
Arabidopsis genes being able to induce a similar, if not better immune response when
inserted into the other’s genome, it cannot be assumed that all genes with conserved
sequences can be interchangeable and used for improved resistance. For example, even
though salicylic acid pathway genes AtEDS1 and GmEDS1 show considerable conserved
amino acids, overexpression of AtEDS1 in soybean seedlings did not confer the same
level of resistance to soybean cyst nematode as GmEDS1 (Mazarei et al., 2007). As of
now there is a lack of research applying knowledge gained from Arabidopsis to other
agronomic crops. More work is required to study the insertion of Arabidopsis genes into
genomes of agronomic crops to determine their impact on disease
susceptibility/resistance.
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1.7 Induced Resistance Types
1.7.1 Systemic Acquired Resistance (SAR)
Ross (1961) describes SAR as providing resistance to a secondary infection by a
broad spectrum of pathogens in uninfected tissues after primary infection with a pathogen
(Shine et al., 2019). In Arabidopsis, and other dicots, SAR is typically associated with
activation of the salicylic acid pathway. In Arabidopsis there have been reports
implicating JA in SAR (Truman et al., 2007). However, another study found that while
JA is involved in SAR signaling, it is not crucial to SAR establishment (Attaran et al.,
2009). During SAR changes in transcription can be measured in uninfected tissues (Shine
et al., 2019). Upon pathogen infection, four major compounds are synthesized in local
tissues. First local tissues synthesize SA via ICS1, then some SA gets converted to
methyl salicylate (MeSA), an SAR signaling molecule. For some plant species, such as
tobacco, MeSA is the long-distance signaling molecule that travels via phloem A study
performed in tobacco by Park et al., (2007) using Tobacco mosaic virus (TMV)
concluded that both salicylic acid–binding protein 2 (SABP2) and SA methyl transferase
are required for SAR establishment. SA methyl transferase converts SA to MeSA which
is transported to distal tissue. Upon MeSA translocation to un-infected tissues SABP2, a
MeSA esterase, converts MeSa to SA in order for downstream SA signaling to occur
(Park et al., 2007). Another signaling molecule, pipecolic acid (Pip), is synthesized via
ALD1 and is a crucial regulator of SAR and priming (Bernsdorff et al., 2015).
Pseudomonas syringae pv. Maculicola infection leads to Pip and SA accumulation in
inoculated and distal leaves of wild type plants. In sid2 aald1 mutants, unable to produce
Pip or SA ,showed less resistance to Pseudomonas syringae pv. Maculicola, indicating
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both are required for a full resistant response (Bernsdorff et al., 2015). Pip also primes
distal tissues for phenolic compound and SA synthesis (Vogel-Adghough et al., 2013).
Pip acts in a positive loop with MPK3/6, WRKY33, and ALD1. This positive feedback
loop occurs when Pip accumulation triggers MPK3/6 activation, which in turn activates
transcription factor WRKY33. WRKY33 goes on to bind the ALD1 promoter, activating
transcription and in turn activating Pip synthesis (Wang et al., 2018). Flavin-Dependent
Monooxygenase1 (FMO1) is a pipecolate N-hydroxylase that catalyzes Pip to N-
hydroxypipecolic acid (NHP) and is critical in SAR establishment (Hartmann et al., 2018;
Mishina et al., 2006; Návarová et al., 2012). Arabidopsis fmo1 mutants were not able to
establish systemic SA accumulation nor SAR in response to P. syringae pv. maculicola
avrRpm1(avirulent) or virulent P. syringae pv. maculicola (virulent). However, local
gene expression and hormone accumulation was not affected in local tissue infected with
avirulent (Psm avrRpm1) or virulent (Psm) bacteria, indicating that FMO1 is required for
systemic signaling, but not local defenses (Mishina et al., 2006). In addition, the
hydroxylation of Pip to NHP by FMO1 results in the transcription of ALD1 and
FMO1(Chen et al., 2018). Along with NHP, there is an amplification loop with PAD4,
ICS, FMO1, and ALD1, which drives SA and Pip synthesis (Návarová et al., 2012; Shah
and Zeier, 2013). SA synthesis activates NPR1, which is a two-step process. First, SA
promotes the monomerization of NPR1. Then, SNF1-Related Protein Kinase 2.8
(SnRK2.8), activated by signaling independent of SA, phosphorylates NPR1 so that it can
be imported into the nucleus where it activates defense genes (Lee et al., 2015). In
addition to Pip, lipids have also been discovered to play a key role during SAR.
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ROS and nitric oxide (NO) induce the conversion of free C18 unsaturated fatty
acids to azelaic acid (AzA), which in turn stimulates glycerol-3-phosphate (G3P)
synthesis (Wang et al., 2014;Yu et al., 2013). G3P synthesis is vital to distal signaling as,
G3P synthesis mutants, gly1 and gli1, were not able to elicit SAR with exogenous AzA
treatment (Chanda et al., 2011; Yu et al., 2013). Defective in Induced Resistance (DIR1),
an apoplastic lipid transfer protein, is required for transporting lipid derived signaling
molecule to distal tissues to establish SAR (Champigny et al., 2011; Maldonado et al.,
2002). DIR1 is not involved in PTI, just SAR. Dir1-1 mutants are still capable of
inducing local immune responses but are not able to induce defenses in distal tissues
upon infection (Maldonado et al., 2002). DIR1 and AZI1 are required for Aza, and MeSA
induced SAR (Chaturvedi et al., 2012; Jung et al., 2009).
In soybeans, the SAR pathway seems to be similar to Arabidopsis, as SAR is
established in a SA and NPR1 dependent manner. However, in some monocot species,
such as barley, there appears to be a different mechanism involved in SAR. A study
performed by Dey et al., (2014) examined bacteria-induced systemic immunity in barley
and compared it to SAR in dicots (Dey et al., 2014). Unlike in Dicots, HvNPR1 is not
required for systemic resistance as Hvnpr1 mutants were not compromised in their ability
to establish SAR. Bacteria-induced systemic immunity resembles Arabidopsis ISR (Dey
et al., 2014). Furthermore, transcript analysis of systemic tissues after local infection with
Pseudomonas syringae pathovar japonica (avirulent) revealed JA mediated WRKY and
ERF-like transcription factors were induced in local and systemic tissues (Dey et al.,
2014).
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1.7.2 Induced Systemic Resistance (ISR)
ISR is triggered by certain non-pathogenic microbes. Induction of ISR is
dependent on the microbe, the host plant species, and the genotype of the host, meaning
that not all microbes can elicit ISR on all plants within a species (Shine et al., 2019;
Vallad and Goodman, 2004). All forms of ISR have some signaling components in
common such as requiring NPR1for downstream signaling (Jain et al.,2016; Lee et al.,
2015; Shimono et al., 2007; Sugano et al., 2010; Van Wees et al.,2000). However, unlike
in SAR, NPR1 does not act as a regulator of SA synthesis and defense genes. Currently,
the role of NPR1 during ISR is not fully understood. Current work suggests that when JA
and ET accumulate, a signal thought to be methyl jasmonate (MeJA) travels through the
phloem, activating NPR1 signaling in distal cells (MeJA) (Jain et al., 2016). Even though
both ISR and SAR involve NPR1 signaling in distal cells, changes to defense gene
transcription cannot be measured in these tissues prior to pathogen infection in ISR
(Shine et al., 2019; Verhagen et al., 2007).
The lack of an immediate distal response can be due to beneficial microbes
silencing the defense response in order to establish a beneficiary relationship with the
host. In a study by Stringlis et al. (2018), transcripts from Arabidopsis roots elicited by
live cells of the PGPR Pseudomonas fluouresence WCS417, a MAMP from WCS417
(flg22417 peptide) and MAMP from the pathogen Pseudomonas aeruginosa (flg22Pa
peptide) were compared (Stringlis et al.,2018). Both MAMPs induced a similar
immediate transcriptome response, indicating that the plant cannot differentiate
between pathogenic or beneficial bacteria solely on the basis of their MAMPs. WCS417
live cells and MAMP from WCS417 also had a high overlap in induced transcripts, but
38
at later time points, WCS417 live cell induced transcripts were silenced. This led
researchers to the conclusion that while plants will recognize beneficial bacteria and
mount a defense response, beneficial bacteria can silence those responses to facilitate
colonization of the host (Stringlis et al.,2018). The mechanisms involved in this defense
suppression are still unknown.
Another distinction between SAR and ISR is the dependency on SA
accumulation. SAR requires SA accumulation, but ISR does not require SA synthesis
though it can occur (Pieterse et al.,1998). Instead ISR elicitation is dependent on JA
and ET signaling. In a well-studied biocontrol bacteria Pseudomonas fluorescens
WCS417r, ISR is induced without SA involvement, but instead JA and ET (Pieterse et
al.,1998). Arabidopsis mutants compromised in the JA or ET pathways were not able to
elicit an ISR response to WCS417r treatment, indicating that the JA and ET pathways
are required for WCS417r mediated ISR (Pieterse et al.,1998). In a separate study
WCS417r treated Arabidopsis plant inoculated with P. syringae pv. tomato DC3000
induced JA/ET regulated genes but no SA controlled PR proteins were induced
(Verhagen et al., 2007). While SA is not involved in WCS417r- mediated ISR, studies
have confirmed its involvement in ISR in other host-microbe interactions.
ISR has historically been associated with the JA/ET pathways, but recent work
has implicated that depending on the microbe, SA may also be involved. PGPR Bacillus
cereus AR156 induced ISR in Arabidopsis against Pseudomonas syringae DC3000 (Niu
et al., 2011). Upon pathogen inoculation, SA and JA/ET controlled genes , PR1, PR2,
PR5, and PDF1.2, were expressed in the foliage of AR156 treated plants (Niu et al.,
2011). Trichoderma is also an interesting ISR inducer, as it has been shown to induce and
39
prime JA, ET, and SA pathways (Martínez-Medina et al., 2013; Martínez‐Medina et al.,
2017). In Arabidopsis, Trichoderma harzianum Rifai T39 and Trichoderma hamatum
T382 induces resistance to necrotrophic leaf pathogen Botrytis cinerea via the JA/ET
pathway (Korolev et al., 2008). SA impaired Arabidopsis mutants were not affected in
resistance to B. cinerea and were able to express ISR, while ET/JA impaired mutants
were more susceptible and unable to express ISR (Korolev et al., 2008; Mathys et al.,
2012). In tomato plants, Trichoderma is able to prime both SA and JA pathways, which
confers an increased defense response by tomato. The primed SA defenses limited initial
root penetration by the Meloidogyne incognita (root knot nematode). Then a second wave
of primed JA pathway responses inhibited silencing of the JA pathway by nematodes and
thereby minimizing gall formation (Martínez‐Medina et al., 2017). While work in
Trichoderma demonstrates the ability of a beneficial fungi eliciting all three separate
pathways, more work in beneficial bacteria needs to be done.
1.7.3 Implementation of IR for disease control
One paper argues that SAR and ISR reinforce and are an extension of PTI induced
hormone defenses, therefore depending on the hormone pathway normally involved in a
certain pathogen response, SAR or ISR will be more effective (Ton et al., 2005). In
Arabidopsis effectiveness of INA-mediated SAR and WCS417r-mediated ISR was tested
using four different pathogens that activate a different hormone defense pathway upon
infection ,Peronospora parasitica and Turnip crinkle virus (TCV) (SA pathway),
Alternaria brassicicola (JA/ET pathway) and Xanthomonas campestris pv. armoraciae
(JA/ET/SA pathway). SAR but not ISR was effective against P. parasitica and TCV.
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Conversely, ISR was effective at inhibiting A. brassicicola while SAR wasn’t. Both ISR
and SAR were effective in inhibiting X. campestris pv. armoraciae (Ton et al., 2005).
Synthetic inducers are capable of activating the plants immune response, without
detrimental effects on the plant (Alexandersson et al., 2016). Some examples of well-
studied inducers on the market areβ-Aminobutyric acid (BABA) and Benzothiadiazole
(BTH). BABA is a non-protein amino acid inducer and has been effective in controlling
pathogens in the greenhouse and in the field across a variety of monocot and dicot crops
(Beckers and Conrath, 2007). In lettuce, BABA application reduced Bremia
lactucae infection (Cohen et al., 2010). Foliar application of BABA reduced Plasmopara
viticola (Downy Mildew) infection and symptoms in grapes sampled over five field trials
(Reuveni et al., 2001). BTH is an inducer of SAR and is tolerated by most crops and is
the main active ingredient in commercial induced resistance products such as Actigard®
(Beckers and Conrath, 2007). Aside from chemical inducers, beneficial microbes have
been tested in their efficacy at protecting crops in the field through induced resistance.
Unfortunately, there is a lack of field trials being performed to test the efficacy of
ISR. Seed treatment with, MycoGrow™ Micronized Endo/Ecto Seed Mix, a mixture of
eight species of mycorrhizal fungi, increased disease resistance and growth promotion in
field studies (Beckers and Conrath, 2007). Through various field trials, Bacillus pumilus
INR-7, has proven to be an effective biocontrol agent against foliar pathogens. Cucumber
with seed treatment of Bacillus pumilus INR-7 showed effective control of cucumber
plants against Colletotrichum lagenarium (anthracnose) and Pseudomonas syringae
pv.lachrymans (angular leaf spot) in several field trials (Vallad and Goodman, 2004). In
pepper, a root dip treatment of INR7 prior to field planting decreased disease symptoms
41
of bacterial leaf spot (X. axonopodis pv. vesicatoria) (Yi et al., 2013). A seed treatment of
PGPR strains P. fluorescens strains Pf1 and PB2 was effective in reducing rice sheath
blight symptoms and incidence in the field (Nandakumar, 1998).
While there is field work studying the efficacy of induced resistance in various
crops, there is a lack of work studying the signaling involved in IR in plants aside from
Arabidopsis and other model organisms. More work needs to be done on crop systems, as
the end goal of IR studies is the implementation of these microbes that can induce
systemic induced resistance in the field for crops.
1.8 Critical Questions and Objectives Depending on the phytohormones C3 induces in the plant, JA/ET or SA, it may be
more effective against one pathogen compared to another. Knowing what hormone
pathway(s) C3 induces will allow for more accurate implementation, as it will prevent the
use of C3 ISR against a pathogen that may not be sensitive to the hormone pathway
induced.
While there is work done in monocots such as wheat and grass, there is no work
studying C3-induced resistance in dicots. Dicots make up a large and diverse portion of
important crops, such as soybean, cotton, and tomato. The United States is currently the
leading producer of soybeans, making soybeans an important commercial crop, hence
why it was chosen for this study. According to the USDA, in 2018 the United States
harvested 8.9 million acres of soybeans with a value of $41 billion. While the industry is
profitable, the annual loss of bushels due to fungal pathogens and fungicide resistance
alone was 300 million bushels in 2016 (United Soybean Board, 2018). Currently, there is
not much work studying induced resistance in soybean elicited by bacteria, instead the
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majority of studies focus on IR induced by chemical elicitors or insects (Lin et al., 1990;
Nafie and Mazen, 2008). The aim of this study is to increase the knowledge of ISR in
soybean, and to increase the understanding of ISR elicited by C3.
Prior to analyzing the systemic response of soybeans to C3, the hormone
pathways C3 induced was determined using marker genes for SA, JA, and ET. Then, the
ISR response was characterization in terms of the ability of C3 to induce a measurable
systemic change in hormone marker genes in the foliage post root drench. Implementing
greenhouse trials and molecular techniques, my research will be able to provide a better
understanding of the molecular mechanisms of pathogenesis and disease suppression by
Lysobacter enzymogenes strain C3. Based on that, new strategies can be developed to
improve the efficacy of biological control agents.
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1.10 Tables Table 1: Biocontrol of various pathogens by Lysobacter
Species Pathogen Disease Host References
L.antibioticus HS124 Meloidogyne incognita Root knot Tomato Lee et al., 2013
Phytophthora capsici Phytophthora blight Pepper Ko et al., 2009
L. antibioticus 13-6
Meloidogyne incognita Tomato root-knot Tomato Zhou et al., 2016
Phytophthora infestans Tomato late blight Tomato Puopolo et al., 2015
L. capsici AZ78 Plasmopara viticola Grapevine downy mildew Grape vine Puopolo et al., 2014
L. enzymogenes 3.1 T8
Pythium aphanidermatum Root and crown rot Cucumber Postma et al., 2009
Fusarium graminearum Fusarium Head Blight Wheat Jochum et al., 2006
Heterodera glycines Soybean cyst nematode Soybean Yuen et al., 2018
Heterodera schachtii Sugarbeet cyst nematode Sugar beet Yuen et al.,2018
Magnaporthe poae Summer patch Kentucky bluegrass
Kobayashi & Yuen, 2005
Rhizoctonia solani Brown spot Tall fescue Giesler & Yuen, 1998
Uromyces appendiculatus Bean rust Pinto bean Yuen et al., 2001
L. gummosus L101 Sphaerotheca fuliginea Powdery mildew Pumpkin Furnkranz et al., 2012
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Table 2: PRRs and their corresponding MAMPs and DAMPs *created by Walnut J, adapted from Saijo et al., 2018
Family PRR or PRR complex
Cell surface receptors Ligand Plant References
LRR
FLS2/BAK1 RLK flg22 Arabidopsis Chinchilla et al., 2007; Gómez and Boller, 2000; Roux et al., 2011
FLS3/BAK1 RLK flgII-28 Tomato Hind et al., 2016
EFR/BAK1 RLK elf18 Arabidopsis Kunze et al., 2004; Roux et al., 2011; Zipfel et al., 2006
XA21/SERK2 RLK RarX21-sY Rice Pruitt et al., 2015
CORE/SERK3a RLK CSP22 Tomato Albert et al., 2016
LeEix2 RLP xylanase Tomato Ron et al., 2004
Unknown Unknown GmPep914 soybean Yamaguchi et al., 2011
Unknown Unknown GmPep890 soybean Yamaguchi et al., 2011
RBPG1 RLP endopolygalacturonases Arabidopsis Zhang et al., 2013
PEPR1/2 RLK AtPep1/2 Arabidopsis Huffaker et al., 2006; Krol et al., 2010; Qi et al., 2010; Yamaguchi et al., 2010
LysM
OsCERK1/OsCEBiP RLK/RLP chitin Rice Shimizu et al., 2010
AtCERK1/AtLYK5 RLK chitin Arabidopsis Miya et al., 2007
AtLYM1/AtLYM3 /AtCERK1
RLP/RLP/RLK
Peptidoglycan Arabidopsis Willmann et al., 2011
OsLYP4/OsLYP6/ OsCERK1
RLP/RLP and RLK
Peptidoglycan Rice Liu et al., 2012
OsCERK1 RLK Myc-LCOCO4 Rice Carotenuto et al., 2017
LjNFR5/LfNFR1 RLK Nod factor L. japonicus Maillet et al., 2011
MtNFP/MtLYK3 RLK Nod factor M. truncatula Maillet et al., 2011
GmGEBP/β-glucan-binding protein
RLK β-Glucan elicitors (GEs)
Soybean Daxberger et al., 2007; Takeuchi et al., 1990; Umemoto et al., 2002; Yoshikawa et al., 1981
B-Lec
LORE RLK lipid A Arabidopsis Ranf et al., 2015
Pi‐d2 RLK unknown Rice Chen et al., 2006
DORN1/LecRK‐I.9 RLK ATP Arabidopsis Choi et al., 2014
EGF WAK1 RLK ligogalacturonides Arabidopsis Brutus et al., 2010
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Figures 1.11
Figure 1: PTI induced phosphorylation signaling cascade. MAMP binding leads to the dimerization of PRRs. Membrane-anchored kinases associated and the kinase domain of the PRR transphosphorylate each other inducing a signaling cascade of MAPKKK,MAPKK, and finally MAPK. Ca2+ influx into the cell and ROS production initiate defense responses. Ca2+
binds to CDPKs, activating them. MAPKs and CDPKS go onto phosphorylate transcription factors that will either induces or suppress defense genes. Ca2+ influx The ROS act as self-propagating systemic defense signals.
Figure created by Walnut J
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Figure 2: Synthesis of ET, JA, and SA. Created by Walnut J.
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Figure 3: Simplified interactions between JA (Blue), SA (Orange), and ET (Green) signaling during plant defense responses in Arabidopsis. During necrotrophic pathogen infection, JA and ET signaling is activated. JA and ET signaling activate ET response factors and PR2,PR3, and PDF1.2 Rice PAD4 induces JA accumulation, not SA. During biotrophic pathogen infection, SA and ET signaling is activated. In Arabidopsis ICS is the main gene for SA synthesis, but in Soybean both ICS and PAL genes are required for SA synthesis. Unlike Arabidopsis, cytosolic not nucleic NPR1 monomers inhibit JA signaling in rice. In rice, NPR1 is not the main regulatory node during SA signaling, but acts in parallel with WRK45 to mediate defense responses. In Arabidopsis, EIN3 targets ORA59 for ubiquitination. During, JA signaling EIN3 is prevented from binding to ORA59 .Arrows in purple represent signaling differences in rice, and red indicated differences in soybeans. Arrows indicate positive interactions, blunt-ended lines indicate inhibitory interactions. Created by Walnut J.
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Chapter 2 Hormonal signaling induced in soybean by Lysobacter
enzymogenes strain C3
2.1 Introduction
Lysobacter enzymogenes strain C3 is a biocontrol bacterium that is capable of
inhibiting fungal and nematode pathogens in the greenhouse and field ( Jochum et al.,
2006; Kilic Ekici and Yuen, 2003; Kobayashi et al.,2005; Yuen et al., 2001; Yuen et al.,
2018; Zhang et al., 2000). The biological control activity of C3 has been shown to be due
in part to antagonism via the production of antimicrobial compounds such as proteases,
lipases, chitinases, and β-1,3-glucanases. (Puopolo et al., 2018; Zhang et al., 2000). In
µl cDNA, 3.5 µl nuclease-free water) and 1µl primer mix (0.5 µl forward primer and
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0.5µl reverse primer). qPCR mixture was pipetted into 0.1mL tube strips (Eppendorf,
#951022109) and place in a Mastercycler (Eppendorf Realplex2). The following qPCR
protocol was run: 94 oC 5 min, 40 times (94 oC, 45 sec, 55 oC 30 sec , 72 oC 1.5 min), in
addition a melting curve program (95oC, 15 sec, 60 oC15 sec,, 95 oC, 15 sec,) was run to
check for contamination. Fold changes of relative gene expression were calculated using
the delta-delta Ct method (Livak & Schmittgen, 2001). A fold change greater than 1.0
indicated upregulation, less than1.0 indicated downregulation, a 1.0 fold change indicated
that there was no change in gene regulation compared to the negative SDW control for
that sampling time. Extreme outliers were removed if the fold change seemed
biologically improbable based on other samples within the specific treatment and time.
2.2.7 Statistical Analysis
Results from multiple runs of an experiment were analyzed together. All
statistical analysis was performed using SAS (SAS Institute Inc., Cary, NC) and
Microsoft Excel. Data from each sampling date was analyzed separately by ANOVA to
determine whether there was a significant treatment effect. To determine whether
differences in fold change between pairs treatments were significant, a one tailed T-test
was performed., Differences between treatments and the SDW control at a particular
sampling time were considered significant when P≤0.1 and highly significant when
P<0.05. Differences between sampling times for a given treatment were considered
significant when there was no overlap in standard errors, which represents variation at the
90% confidence level.
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2.3 Results
2.3.1 Local induction of the phenylpropanoid pathway upon C3 treatment
Prior to analyzing hormone responses to C3 treatment, the ability of C3 to induce a
resistance response in soybean needed to be ascertained. To this end, the activation of the
phenylpropanoid pathway was used as a determinant of a resistance response. During
pathogen infection, the phenylpropanoid pathway is involved in numerous defense
responses, including synthesis of lignin and in soybeans, isoflavone (Hahlbrock et al.,
1989; Yu et al., 2000). The gene transcript abundance of Phenylalanine ammonia-lyase
(PAL1) was measured. Relative gene transcript abundance, also referred to as relative gene
expression, was expressed as a fold change compared to SDW. C3 treatment elicited the
highest increase in GmPAL1 transcription as early as 2HrAT, with a 4.8-fold change in
transcription compared to SDW (Figure 2). C3 treatment induction of GmPAL1 continued
at 24HrAT (2.0-fold change) and 48HrAT (3.4-fold change), but gene transcription
upregulation was no longer present at 72HrAT (Figure 2). ASM is capable of inducing
resistance responses in soybeans (Tripathi et al., 2019) and therefore upregulation of
GmPAL1 by ASM treatment indicated that the experiment was successful. ASM induced
GmPAL1 expression at 48HrAT (3.1-fold change) and 72HrAT (1.8-fold change) (Figure
2). Taken together, C3 foliar treatment is capable of inducing a resistance response in
soybean foliage.
2.3.2 Local induction of SA pathway upon C3 treatment
To determine if C3 foliar treatment elicits local induction of the salicylic acid
(SA) pathway, the transcript abundance of 3 genes Phytoalexin Deficient 4 (GmPAD4),
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Nonexpresser of PR genes 1 (GmNPR1), and Pathogenesis Related 1 (GmPR1) were
measured. SA signaling upstream of SA synthesis was assessed using GmPAD4 as a
marker gene because it is one of the first genes induced to begin SA accumulation (Jirage
et al., 1999; Zhou et al., 1998). PAD4 activity leads to SA accumulation, which in turns
leads to further PAD4 gene transcription (Jirage et al., 1999). C3 treatment resulted in an
initial decrease in GmPAD4 transcript abundance compared to SDW at 2HrAT (0.69-fold
change) (Figure 3). C3-treated foliage collected 24HrAT and 48HrAT showed a return in
GmPAD4 transcription to SDW levels. By 72HrAT GmPAD4 transcript abundance in C3
treated leaves were higher compared to the SDW treatment due to C3 treatment (1.54-
fold change) (Figure 3). ASM treated tissues did not show a significant increase in
GmPAD4 transcripts compared to SDW at any sampling time, which was expected as
ASM induces SA regulated genes downstream of SA accumulation.
Downstream of PAD4 activity and SA accumulation, NPR1 is an important
regulatory node of SA signaling. NPR1 activity is controlled through posttranslational
modifications and transcriptional regulation mediated by SA signaling (Cao et al.,1998;
Mukhtar et al., 2009; Yu et al., 2001). GmNPR1 is an oligomer connected by
intermolecular disulfide bonds in the cytoplasm. Upon reactive oxygen production
(ROS), the disulphide bonds are reduced and the NPR1 oligomer becomes a monomer,
allowing SA binding. After target binding is complete, the NPR1 monomer is degraded
and therefore new transcription of NPR1 needs to occur during SA signaling to replenish
NPR1 concentration (Mukhtar et al., 2009; Yu et al., 2001). GmNPR1-1 relative gene
transcription was upregulated by C3 treatment at 2HrAT (2.42-fold change) and 24HrAT
(1.98-fold change). Subsequent sampling times showed no increase in GmNPR1-1
80
transcription in the C3 treatment compared to SDW (Figure 4A). ASM showed similar
transcription levels as C3 treatment (Figure 4B).
NPR1 directly induces GmPR1,a well-established defense gene mediated by SA
signaling (Wu et al., 2011). Due to the interaction between NPR1 and GmPR1, it was
predicted that GmPR1 transcription would be upregulated by C3 treatment as it increased
GmNPR1-1 transcript abundance. GmPR1 transcript abundance was increased in the C3
over SDW at 24HrAT (8.04-fold change). C3 treated soybean tissues collected thereafter
also exhibited increased GmPR1 transcript abundance, with there being no significant
differences between the three sampling times (Figure 4B). The difference between timing
of GmNPR1-1 and GmPR1 transcript accumulation can be attributed to regular gene
activity during the SA signaling response as the positive control exhibited the same
transcript accumulation pattern of GmNPR1 and GmPR1 as in C3 treated tissues (Figure
4A,4B).
2.3.3 Local induction of JA and ET pathways upon C3 treatment
The jasmonic acid and ethylene pathways often act synergistically during
nonpathogenic microbe interactions (Pozo et al., 2004). To determine if this response
occurs during local induced resistance in response to C3 treatment, Allene Oxide
Synthase (GmAOS) and 1-aminocyclopropane-1-carboxylate synthase (GmACS), which
are genes involved in JA and ET synthesis, respectively, were selected. Both GmAOS
and GmACS encode enzymes critical to their respective biosynthetic pathways. AOS
converts (13S)-hydroperoxyoctadecatrienoic acid to allene oxide and ACS converts S-
Adenosyl methionine to 1-aminocyclopropane-1-carboxylic acid (ACC) (Park et
81
al.,2002; Staswick, 2004; Yang and Hoffman, 1984; Yang and Hoffman, 1984).
GmAOS2 transcripts accumulated to higher levels in the C3 treatment than SDW at
2HrAT (3.08-fold change), 24HrAT (1.87-fold change), and 72HrAT (1.92-fold change)
(Figure 5). C3 treatment did not result in an increase in GmAOS2 transcript abundance at
48HrAT compared to the SDW control. As with C3 treatment, MeJA treatment
upregulated transcription of GmAOS2 at 2HrAT and 24HrAT, but not at 48HrAT,
confirming that the regulation corresponds to jasmonic acid induced expression. C3
treatment caused increased GmACS abundance compared to SDW at 2HrAT (4.34-fold
change) (Figure 6).Then there was a significant reduction in GmACS transcription in the
C3 treatment such that GmACS transcription at 24HrAT and subsequent sampling times
were lower than or the same as in SDW. MeJA treatment led to a different expression
pattern. The initial upregulation of GmACS at 2HrAT was followed by a decrease in
transcription to SDW levels, similar to what was observed with C3 treatment. However,
MeJA treatment increased transcription at 48HrAT and 72HrAT, while C3 treatment did
not (Figure 6). These results suggest that C3 treatment leads to early activation of the JA
and ET pathways upstream of hormone synthesis.
Upstream transcription of genes involved in hormone synthesis does not
necessarily mean that JA and ET downstream signaling is occurring as JA signaling is
inhibited downstream of synthesis, through SA inhibition of JA mediated defense gene
transcription (Leon-Reyes et al., 2010; Van der Does et al., 2013). Therefore, a
downstream PR gene that is upregulated by JA and ET signaling was selected to assess
whether C3 treatment induces JA and ET mediated defense response. GmPR3, encoding a
chitinase, is activated by JA and ET, but not SA, therefore any upregulation of this gene
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cannot be attributed to the SA pathway (Mazarei et al., 2007). C3 treatment led to an
accumulation of GmPR3 transcripts when applied to the foliage. GmPR3 induction
occurred 24HrAT (3.80-fold change), with a reduction in transcription 48HrAT (1.56-
fold change). , There was once again an upregulation of transcription (5.42-fold change)
in the C3 treatment at 72HrAT (Figure 7). MeJA treatment induced the same expression
pattern as C3 treatment from 2HrAT to 48HrAT. However, unlike C3 treatment, there
was no MeJA induced transcription of GmPR3 at 72HrAT (Figure 7). It is unclear if the
72HrAT expression difference is due to the difference in defense gene induction between
a bacterium and a hormone application. Nonetheless, the gene expression analyses
indicate that ET and JA pathways are activated upon C3 foliar treatment.
2.3.4 Systemic induction of defense hormones upon C3 root treatment
To assess if C3 root drench treatments applied to soybean could lead to systemic
induction of defense genes, GmPR1 and GmPR3 expression was analyzed in soybean
foliage after root treatment (Figure 8). Systemic resistance can lead to either measurable
transcription changes in distal tissues upon an induced resistance response, or a priming
response in which case no change in known defense related gene transcription will be
measured in distal tissues prior to pathogen inoculation. To assess if C3 root drench
treatments applied to soybean could lead to systemic induction of defense genes, GmPR1
and GmPR3 expression was analyzed in soybean foliage after root treatment (Figure 8).
ASM and MeJA were used as positive controls for systemic induction of GmPR1 and
GmPR3, respectively, as both treatments are known to induce systemic signaling in
soybeans. C3 treatment led to higher accumulation of GmPR1 transcripts 3DAT and
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GmPR3 transcripts at 7DAT compared to SDW at those sampling dates (Figure 8A, 8B).
These responses to C3 treatment were relatively weak compared to the response to ASM
and MeJA, as both of these chemicals caused significantly higher transcription of their
response defense genes compared to SDW at most sampling dates. Unlike chemical
treatments, bacterial treatments may take more time to elicit a signal in the roots due to
time required to colonize the roots. This delayed induction of defense responses in
soybean foliage following root application compared to a foliage drench was also
reported by Kilic-Ekici and Yuen (2003) in tall fescue experiments. C3 foliar applications
increased peroxidase activity as early as 2HrAT, while a root drench activated peroxidase
activity 2DAT in the foliage (Kilic-Ekici and Yuen, 2003). As in root treatments in tall
fescue, C3 root treatment of soybean roots was able to induce a systemic resistance
response in the foliage.
2.4 Discussion
In this study, I investigated the nature of the response of soybean to treatment
with C3. The first objective was determining if soybeans can recognize and respond to
C3 treatment. To that end the phenylpropanoid pathway was selected, specifically the
gene that encode the first enzyme in said pathway, GmPAL1. Phenylpropanoids are
involved in plant defense through cell wall fortification (lignin) and antioxidant agents.
Phenolic compounds prevent ROS from diffusing across the membrane and in turn
preventing the oxidation of membrane lipids that can damage the cell membrane (Kulbat,
2016; Sharma et al., 2012). Transcript analysis indicated that C3 treatment does in fact
lead to a resistance response in soybeans. This response can be due to a defense response
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requiring phenylpropanoid pathway products, the production of ROS when it induced
PTI, or both. After determining that there is a resistance response in soybean foliage,
hormone pathway responses were analyzed.
C3 application to soybean leaves increased gene transcripts in those leaves that
are associated with hormone responses involving JA and ET, and SA. C3 led to increases
in transcripts for all three pathways. Taken together this indicates that C3 treatment
activates SA, JA, and ET signaling pathways locally in soybean. This makes this study
with C3 the first report of a biocontrol bacterium inducing three hormone pathways in
soybean upon foliar application.
To examine the induction of these hormone signaling pathways, genes upstream
and downstream of hormone synthesis were selected. GmPAD4 transcripts were not
significantly different in C3 treated leaves compared to SDW until 72HrAT. This delay in
induction of gene transcription was only observed in GmPAD4, not in GmNPR1 and
GmPR1. This may be attributed to the SA amplification loop that occurs during SA
signaling. GmPAD4 is activated during SA signaling, which positively regulates SA
accumulation, and GmPAD4 transcription (Jirage et al., 1999). As mentioned previously,
C3 treatment increased the transcript level of GmNPR1. NPR1 is involved in signaling
occurring during both ISR and SAR (Cao et al., 1994; Pieterse et al., 1998). Unlike in
SAR, NPR1 does not act as a regulator of SA synthesis and defense genes during ISR.
Currently, the role of NPR1 in ISR is not fully understood. In soybeans, as with
Arabidopsis, NPR1 is constitutively expressed but is in its inactive form as an oligomer
(Sandhu et al., 2009). Soybean has two copies of the genes encoding GmNPR1,
GmNPR1-1 and GmNPR1-2, both of which are induced upon treatment with a SA inducer
85
2,6-dichloroisonicotinic acid (INA) (Sandhu et al., 2009). As with AtNPR1, GmNPR1
becomes a monomer after treatment with SA or with a SA inducer and activates the
transcription of PR1 (Sandhu et al., 2009). The basal level at which it is expressed is
often enough to induce an effective amount of defense gene transcription to inhibit
pathogen growth (van Wees et al., 2000). However, to prevent an accumulation of NPR1
monomers, NPR1 is degraded through a ubiquitin dependent proteasome pathway
(Mukhtar et al., 2009). Therefore, as a result, new NPR1 is required for further signaling,
in which case more NPR1 transcription may be necessary (Mukhtar et al., 2009). This
may explain why C3 treatment lead to an increased expression of NPR1 in soybeans.
Regardless, the increase in transcription of NPR1 can be beneficial, as just a two-fold
change has been shown to provide resistance in Arabidopsis to P. syringae pv.
maculicola ES4326 and Peronospora parasitica (Cao et al., 1998).
PR1 class of proteins are thought to be antifungal compounds (Mitsuhara et al.,
2008; Sarowar et al. 2005). The induction of SA pathway gene, GmPR1, by C3 treatment
correlates with experiments done in tall fescue plants (Kilic-Ekici & Yuen, 2003). C3
root and leaf treatment increased peroxidase activity, indicating that ROS production was
occurring systemically in the leaves and locally in the roots (Kilic-Ekici & Yuen, 2003).
ROS signaling occurs upstream and downstream of SA synthesis (Chen et al., 1993). The
initial ROS burst during early PTI responses induces SA synthesis, and consequently
activates NPR1 and induces PR1 transcription. Both genes were upregulated as a result of
C3 treatment in this study. SA in turn induces ROS production by regulating transcription
of redox genes (Herrera-Vásquez et al., 2015).
86
The JA and ET pathways were also activated locally when soybean foliage was
treated with C3. Tissues accumulated JA and ET marker genes, GmAOS, GmACS, and
GmPR3, transcripts. GmAOS and GmACS are both upstream of JA and ET synthesis,
respectively. As there weren’t any hormone synthesis studies carried out, it cannot
definitely be said that C3 treatment led to JA or ET accumulation. However, as GmPR3
transcription was upregulated post C3 treatment it can be stated that downstream
signaling for those two pathways occurred (Mazarei et al., 2007). Interestingly, GmPR3,
like GmPR1, encodes an antifungal defense related protein, specifically a chitinase (Ali et
al., 2018). It would be worthwhile to determine if C3 treatment can induce other defense
related genes, such as genes that encode other classes of PR proteins involved in
antibacterial activity.
One possible implication of signaling via three hormone pathways, JA/ET and
SA, versus only one hormone pathway is a higher level of induced resistance and towards
a broad range of pathogens with different modes of nutrient acquisition. Arabidopsis
plants treated with Trichoderma atroviride were less susceptible to infection by
hemibiotrophic pathogen Pseudomonas syringae pv. tomato and necrotrophic pathogen
Botrytis cinerea (Salas-Marina et al., 2011). This enhanced resistance was attributed to T.
atroviride inducing SA, JE, and ET pathways locally in the roots and systemically in the
foliage prior to pathogen inoculation (Salas-Marina et al., 2011). Penicillium
simplicissimum GP17-2 treated Arabidopsis seedlings had enhanced disease resistance to
Pseudomonas syringae pv. tomato due to induced resistance. Induced resistance by
GP17-2 was determined to act through the JA, ET, and SA pathways, upregulating
expression of PR-2 and PR-5 (Hossain et al., 2007). Further work in Arabidopsis has
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demonstrated that the co-activation of SA and JA, by inducing ISR and SAR, leads to
increased resistance against pathogens. Arabidopsis plants treated a combination of both
SAR and ISR inducers, SA and Pseudomonas fluorescence WCS417r, resulted in higher
protection against Pseudomonas syringae pv. tomato infection (Van Wees et al., 2000).
With root treatments, C3 was able to induce expression of SA or JA/ET
downstream genes GmPR1 and GmPR3, respectively, in soybean. There was a previous
report in which a biocontrol bacterium, Bacillus amyloliquefaciens strain KPS46, could
prime JA and SA in soybeans (Buensanteai et al., 2009). However, this is the first study
to report the ability of a biocontrol bacteria to induce a measurable change in defense
responses in systemic tissues prior to pathogen inoculation.
This project has laid the foundation for understanding the interaction between C3
and soybeans. C3’s ability to induce the SA pathway in systemic tissues and JA, ET, and
SA in local tissues can be further examined in terms of C3’s ability to inhibit different
pathogens that induce different hormonal pathways. To be able to utilize C3 induced
resistance in soybeans, more work needs to be done in understanding ISR responses. As
previously mentioned, ISR is dependent on the microbe and genotype of the host,
therefore the ability for C3 to induce resistance in other cultivars of soybean should be
determined. Furthermore, as a biocontrol agent, it is pertinent to assess the effectiveness
of C3 induced resistance on disease inhibition using various pathogens of economic
importance.
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2.6 Tables
Table 1: Soybean primers for genes used during qPCR analysis.