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First published online July 10, 2003; 10.1104/pp.102.019927 Plant Physiology 132:2098-2107 (2003) © 2003 American Society of Plant Biologists
Salt Stress Activation of Wound-Related Genes in Tomato Plants1U.S. Department of Agriculture-Agricultural Research Service, National Forage Seed Production Research Center, Oregon State University, Corvallis, Oregon 97331–7102
Plants respond to various stresses by expressing distinct sets of genes. The effects of multiple stresses on plants and their interactions are not well understood. We have discovered that salt stress causes the accumulation of proteinase inhibitors and the activation of other wound-related genes in tomato (Lycopersicon esculentum) plants. Salt stress was also found to enhance the plant's response to wounding locally and systemically. The tomato mutant (def-1), which has an impairment in the octadecanoid pathway, displayed a severe reduction in the accumulation of proteinase inhibitors under salt stress, indicating that salt stress-induced accumulation of proteinase inhibitors was jasmonic acid dependent. The analysis of salt stress in another tomato mutant, spr-1, which carries a mutation in a systemin-specific signaling component, and transgenic tomato plants that express an antisense-prosystemin cDNA, showed that prosystemin activity was not required for the salt-induced accumulation of proteinase inhibitors, but was necessary to achieve maximal levels. These results suggest that a prosystemin independent- but jasmonic acid-dependent pathway is utilized for proteinase inhibitor accumulation in response to salt stress.
Plants in the field are exposed to multiple stresses, and their response to these various stresses determines their capacity to survive. Plants can use multiple signaling pathways and signals to mediate their response; for example, at least four different signaling pathways have been identified for water-deficit stress (Shinozaki and Yamaguchi-Shinozaki, 1997  ;
Xiong et al., 2002). Different
forms of stress may activate or utilize the same components, including
proteins and other signaling molecules. Transgenic tobacco (Nicotiana
tabacum) plants expressing constitutively active NPK1, a
mitogen-activated protein kinase kinase kinase (MAPKKK) showed an enhanced
tolerance to cold, heat shock, and salt stress
(Kovtun et al., 2000).
Signaling molecules such as jasmonic acid (JA) are involved in multiple stress
responses and development in plants (Creelman and Mullet,
1995,
1997;
Turner et al., 2002). However,
it is the specific combination of various components of the signaling network
coupled with spatial and temporal factors that allows the plant to mount a
directed response to any given stress factor.
The phenomenon of cross-tolerance where a plant's resistance to one stress
resulted in resistance to another form of stress is a growing area of research
(Genoud and Metraux, 1999
Wounding in tomato (Lycopersicon esculentum) plants is a
well-characterized stress response. Tomato plants respond to mechanical
wounding or herbivorous insect attack by inducing the synthesis of a wide
array of defense-related proteins at the wound site and systemically
throughout the distal portions of the plant
(Bergey et al., 1996
The wound response in tomato plants has been shown to be inhibited as well
as activated by other stresses. The signaling molecule salicylic acid produced
in response to infection with biotrophic pathogens was shown to inhibit the
synthesis of proteinase inhibitors in response to wounding and herbivory
(Doherty et al., 1988 In this report, we have investigated the effects of salt stress on the wound response cascade in tomato plants. Salt stress alone was found to induce wound-related genes and this gene activation was mediated via the octadecanoid pathway. The salt-dependent activation of the octadecanoid pathway was found to be independent of the wound prohormone, prosystemin, but prosystemin (PS) activity was necessary to achieve maximal accumulation of proteinase inhibitors. In addition, salt stress was found to strongly enhance the plant's ability to respond to wounding. This analysis describes how an abiotic stress activates the wound response in tomato, and provides further insight into defense gene signaling and the interaction between stress responses in plants.
Salt Stress Induction of Proteinase Inhibitor II (Inh II) Accumulation We wanted to determine how salt stress would affect the wound response in tomato plants. Salt stress was chosen because it is an abiotic stress that is initially perceived in the roots, in contrast to wounding that is inflicted on the leaves. The roots of 15-d-old soil-grown tomato seedlings were treated with different concentrations of NaCl and were assayed 24 h later for proteinase inhibitor accumulation. Figure 1A shows an NaCl concentration-dependent accumulation of Inh II. Plants exposed for 24 h to 100 mM NaCl produced a weak accumulation of Inh II, nearly 10 µg mL-1 leaf juice. Tomato seedlings treated with 200 mM NaCl produced Inh II levels of 30 µg mL-1 leaf juice, similar to levels that are found in the systemic unwounded leaf in response to wounding (see Fig. 5). Inhibitor levels in plants treated with 300 mM NaCl were about four times higher as in plants treated with 100 mM NaCl. These results demonstrate that salt stress alone induces the accumulation of the Inh II protein. The plants exposed to 100 and 200 mM NaCl stress for 24 h appeared to be a slightly darker green than untreated control plants, but otherwise looked normal. However, plants exposed to 300 mM NaCl displayed signs of necrosis on the leaves.
To determine the kinetics for salt-induced activation of the Inh II gene, a gel-blot analysis of Inh II transcript levels was performed in plants exposed to 200 mM NaCl over a 24-h period. As shown in Figure 1B, the analysis of Inh II transcript levels revealed a biphasic activation of the gene. After 4 h of exposure to salt stress, a weak activation of the Inh II gene was observed in the leaves. The transcript levels increased significantly by 6 h and appeared to wane after 8 h of exposure. This was followed by a dramatic increase in the gene activation after 10 h of exposure that was maintained throughout the remainder of the 24-h time course. In the water control plants, we observed only minimal activation of the Inh II gene in the leaves 4 h after watering the roots. This activation increased slightly over the next few hours, but disappeared after 12 h.
Because a limited exposure to salt stress alone induced the accumulation of Inh II in young tomato plants, we wanted to investigate the effects of prolonged exposure to salt stress on the activation of wound-response genes. Fifteen-day-old plants were watered daily with 200 mM NaCl solution over a 5-d period. At 24-h intervals, leaf tissue was collected and assayed for Inh II accumulation and RNA gelblot analysis. As shown in Figure 2A, plants subjected to continual watering with 200 mM NaCl showed a steady increase of nearly 50 µg mL-1 leaf juice per day of Inh II accumulation over the first 4 d of exposure. On the 5th d, we observed a 2-fold increase in total Inh II concentration in the leaf, increasing almost 200 µg mL-1 in a 24-h time period. This dramatic increase in Inh II concentration in 1 d was equal to the combined accumulation of the first 4 d and it was consistently observed during the course of our analysis. It should be noted that after the 5-d treatment period, the salt concentration in the soil might have accumulated to levels higher than 200 mM. Plants exposed to water alone showed limited Inh II accumulation over the 5-d period; this accumulation was most likely due to handling or watering of the plants.
As shown in Figure 2B, the increased accumulation of Inh II mRNA correlated directly with the increase in the levels of Inh II synthesized in the leaf. The steady increase of Inh II accumulation over the first 4 d can be explained by the constant high level of Inh II gene activation due to the continual exposure to salt stress. On d 5, the roughly 2-fold increase of Inh II protein accumulation correlated directly to a similar increase of 1.75-fold in the level of Inh II transcript in the leaves.
To gain further insight into the mechanisms leading to the dramatic
increases in Inh II accumulation in leaves exposed to salt stress, we examined
the patterns of expression of additional wound-related genes. Inh II
and cathepsin D inhibitor (CDI) are defense-related genes
that reflect the magnitude of the plant's wound response. PS and
lipoxygenase (LOX) are signaling-related genes
(Ryan, 2000
Because salt stress resulted in elevated transcript levels of the signaling
genes PS and LOX, we wanted to investigate the roles of PS
and the octadecanoid pathway in mediating this response. To better define the
signal transduction pathway mediating the salt stress activation of the
defense-related genes, we examined the accumulation of Inh II in transgenic
antisense-PS plants and the mutant plants, spr-1 and
def-1. These plants were constantly exposed to 200 mM NaCl
over a 5-d period. The transgenic antisense-PS
(McGurl et al., 1992 As shown in Figure 4, wild-type plants exposed to 200 mM NaCl, displayed a steady increase in the accumulation of Inh II over the first 4 d of exposure. On the 5th d, a nearly 2-fold increase in total Inh II concentration was observed in the leaves, as previously shown in Figure 2A. The antisense-PS and spr-1 plants showed a similar pattern of accumulation, but were approximately 50% of wild-type levels. However, in the spr-1 mutant, the 2-fold increase in Inh II concentration was observed on d 4, rather than d 5 as was seen in wild-type and antisense-PS plants. The def-1 plants showed no Inh II accumulation during the first 2 d of exposure, and on d 3 and 4, Inh II accumulation was less than 10% of levels observed in wild-type plants at the same time points. Similar to wild-type and antisense-PS plants, the def-1 plants also displayed a 2- to 3-fold increase in Inh II accumulation on the 5th d of exposure.
To investigate how salt stress would affect the wound response, the roots of 15-d-old soil-grown tomato seedlings (two-leaf stage) were treated with different concentrations of NaCl. Immediately after salt treatment, the lower leaf was subjected to a single wound across the mid-vein, and leaves were assayed 24 h later for accumulation of proteinase inhibitors. Figure 5, shows a salt concentration-dependent enhancement of wound-induced Inh II accumulation. Wounded plants exposed to 100 mM NaCl produced nearly double the amount of Inh II in the wounded and systemic leaves when compared with water/wound control plants. In plants treated with 200 mM NaCl, the wounded leaves exhibited an increase in Inh II synthesis that was 3-fold higher than was found in leaves that had been wounded without salt treatment. The enhancement of wound-inducible Inh II accumulation was found to be even more pronounced in the systemic unwounded leaves, in which Inh II levels increased 5- to 6-fold in plants treated with 200 mM NaCl when compared with the systemic leaves of wounded nonsalt-treated control plants. Plants subjected to 300 mM NaCl stress had increases in Inh II accumulation that approached 4-fold in wounded leaves and 6-fold in systemic leaves as compared with controls.
To further investigate the salt-enhanced systemic wound response, the transcript levels of wound-related genes were investigated in the upper unwounded leaves over a 24-h time frame. As shown in Figure 6, wounding of the control seedlings resulted in a typical systemic wound response, with Inh II and CDI transcripts beginning to accumulate 2 to 4 h after wounding, reaching a maximum 12 h after wounding, and then declining during the remainder of the time course. Whereas the basal levels of PS and LOX showed a transient increase over the same period. In comparison, plants exposed to both salt stress and wounding exhibited significantly higher levels of mRNA induction. The salt-stressed/wounded plants displayed increased systemic Inh II and CDI transcript levels 4 h after treatment, which continued to increase over the remainder of the time course. Relative transcript levels for the signaling genes LOX and PS were higher in the salt-stressed/wounded plants than in the water/wounded control plants. However, their levels decreased at 24 h in contrast to the defense-related genes.
Because salt stress together with wounding enhanced the systemic expression of the signaling genes, we wanted to further investigate the roles of PS and the octadecanoid pathway in mediating this enhanced response. As shown in Figure 7, antisense-PS and spr-1 plants have a severely reduced systemic response (unwounded leaves) to water/wounding when compared with wild-type plants, but did show a significant accumulation of Inh II in the wounded (local) leaf, approximately 50% of wild-type levels, whereas def-1 plants show no Inh II accumulation in the wounded or unwounded leaves.
When the wild-type, antisense-PS, and spr-1 plants were exposed to 200 mM NaCl and wounding, we observed a 3-fold increase in the levels of Inh II protein in the wounded leaves when compared with the plants wounded without salt treatment. Surprisingly, salt stress and wounding in the antisense-PS and spr-1 mutants resulted in the accumulation of Inh II proteins in the unwounded leaves in contrast to water/wounded plants. Although the systemic accumulation of Inh II was restored, in antisense-PS and spr-1 plants, the overall accumulation of Inh II as a result of salt stress and wounding, both locally and systemically, remained roughly 50% of the levels observed in the wild-type plants. These Inh II levels observed systemically in the unwounded leaves of the antisense-PS and spr-1 plants were higher than what would be expected from just salt stress alone (Fig. 4). No Inh II accumulation was observed in def-1 plants in the wounded or unwounded leaves when subjected to salt treatment and wounding, indicating that an intact octadecanoid pathway is critical for the salt-induced enhancement of the wound response.
The reduced salt stress-induced Inh II accumulation observed in the
antisense-PS and the PS insensitive spr-1 mutant plants
suggested that PS activity is required to obtain maximal accumulation of Inh
II in response to salt stress. To further investigate the role of PS in this
response, we decided to examine the effects of salt stress in transgenic
tomato plants overexpressing the PS cDNA under the control of the 35S
promoter (sense-PS; McGurl et
al., 1994
Wounding in tomato plants is a well-characterized stress response. Tomato plants respond to mechanical wounding and herbivore attack by inducing the local and systemic synthesis of a wide variety of defense-related proteins, including proteinase inhibitors (Bergey et al., 1996 ; Ryan,
2000). The levels of accumulation of wound-inducible proteinase
inhibitors in the leaves reflects the magnitude of the defense response. The
activation and enhancement of the wound response by UV irradiation prompted us
to investigate the effect of another abiotic stress, salt on the wound
response. Our analysis revealed that a 24-h exposure to salt stress alone was
able to induce the accumulation of the wound-inducible Inh II protein in a
dose-dependent manner (Fig.
1).
Prolonged exposure to salt stress over a 5-d period resulted in the
accumulation of high levels of proteinase inhibitors
(Fig. 2). Salt-induced Inh II
levels were as high as 350 to 450 µg mL-1 leaf juice, in
contrast to a typical strong wound response that produces proteinase inhibitor
levels of 100 to 120 µg mL-1 leaf juice. These increased levels
were even more dramatic in sense-PS plants, obtaining levels of almost 600
µg mL-1 in leaf juice. This extremely high level in sense-PS
plants is probably even higher because the concentrations of Inh II are at the
limiting range of the radial immunodiffusion assay. All plants treated with
200 mM NaCl for 5 d grew slowly, with darker green leaves and were
roughly one-half the size of untreated plants. It has been shown that prolong
exposure to salt stress and drought results in lower water content in the
leaves of tomato plants (Cuartero and
Fernandez-Muñoz, 1999
Northern-blot analysis revealed that salt stress elevated the transcript
levels for the wound-signaling gene LOX, suggesting the involvement
of the octadecanoid pathway in mediating the response. This was further
confirmed when the def-1 mutant subjected to salt stress showed a
severe impairment in the accumulation of the Inh II protein as compared with
similarly treated wild-type plants (Fig.
3), and its failure to respond to both wounding and salt stress
(Fig. 7). The def 1
mutant is impaired in the octadecanoid pathway, compromising its ability to
accumulate JA in response to wounding and elicitors
(Howe et al., 1996
In addition to salt stress, we found that wilting alone also induced the
accumulation of proteinase inhibitors, and this response was also mediated via
the octadecanoid pathway (data not shown). These data support the findings
from a microarray analysis in Arabidopsis showing that a subset of
wound-inducible genes was activated in dehydrating leaves
(Reymond et al., 2000 To further investigate the effects of salt stress on activation of wound-related genes, we investigated how salt stress that is initially perceived in the roots would affect the transmission of the wound signal in the leaves. This allowed us to examine the interaction of two distinct stresses that are initially perceived in different tissues and at distant locations. The data in Figure 5 show that tomato plants subjected to wounding and salt stress exhibit an enhanced response to wounding when compared with plants subjected to wounding alone. This salt-induced enhancement of the wound response occurs in the local wounded leaves, but was found to be more pronounced in the systemic unwounded leaves.
The increased accumulation of Inh II due to wounding and salt treatment
cannot be explained solely by the additive effect of salt stress and wounding
alone. We found that the simultaneous exposure to 100 mM NaCl and
wounding increased Inh II levels an average of 60% higher in the wounded
leaves, and 50% higher in the systemic leaves from what we would have expected
if it was merely an additive effect. This enhancement was even more pronounced
in plants subjected to 200 mM NaCl stress, where the increases were
found to be nearly 100% higher in wounded and 180% in systemic leaves above
the expected values for an additive effect. These data indicated that salt
stress not only activates the wound response, but it also strongly enhances
the response. These results are similar to the effects shown by tomato plants
subjected to wounding and UVB/A irradiation
(Stratmann et al., 2000b
PS was another wound-signaling gene that was found to be
up-regulated by salt stress. However, we showed that PS activity was not
required for salt stress-induced accumulation of Inh II protein. This finding
was based on the analysis of the effect of salt stress on the spr-1
mutant and antisense-PS tomato plants. The transgenic
antisense-PS plant has a strongly suppressed PS expression
(McGurl et al., 1992 When we investigated the effects of salt stress on wounding in the spr-1 and antisense-PS backgrounds, we were surprised to discover that salt stress had appeared to restore the systemic accumulation of Inh II, although at 50% the level observed in wild-type plants (Fig. 7). The systemically accumulated Inh II levels cannot be explained by just salt stress induction alone because the Inh II levels were at least two times higher than what is observed in the unwounded salt treated controls (Figs. 1 and 4). However, it is unclear how this restoration of the systemic response occurs.
What insights can we derive from our analysis of salt stress activation of
the wound response with respect to signaling? We found that the initial
activation of Inh II gene occurs 4 h after wounding or salt treatment
alone. This suggests that the initial salt-induced signal from the root
travels (Fig. 1) at the same
velocity to the leaf as the wound signal from wounded to systemic leaf
(Fig. 6). However, these
signals were generated differently. In leaves, a single transient wound across
the mid-vein was made, whereas intact roots where exposed to a continual salt
stimulus. Another possibility could be that the salt-induced signal travels
faster but the concentrations are very low, requiring 4 h to reach levels that
can induce the gene. This salt-induced gene activation appears to occur in two
phases. One can speculate that the initial signal leading to gene activation
originates from the roots (Jackson,
1997
There is evidence suggesting that JA acts as the long-distance wound signal
(Zhang and Baldwin, 1997
Based on these recent findings, we can propose a mechanism for accumulation
of Inh II in response to salt stress. Salt stress leads to the synthesis and
release of JA. JA induces the synthesis of the PS and Inh II proteins. The
newly synthesized PS can activate the wound-response pathway
(Dombrowski et al., 1999
Whether the strong induction of the wound response by salt stress is
relevant to the success of the plant in the field is not known. In addition,
it is unclear if this activation provides the plant any increased tolerance to
water-deficit stress. Sense-PS plants were found to survive higher
initial concentrations of salt than wild-type plants (J.E. Dombrowski and C.A.
Ryan, unpublished data). One possible explanation for their increased survival
rate could be that in addition to accumulating wound-related proteins, there
is a concurrent activation of water deficit-tolerance genes. In support of
this hypothesis, microarray analysis revealed that mechanical wounding
activated osmotic stress-related genes in Arabidopsis
(Reymond et al., 2000
JA has been implicated in a wide range of stress responses, as well as
development in plants (Creelman and Mullet,
1995 Why would a plant redirect energy and resources to activate a defense pathway and accumulate such high levels of proteinase inhibitors during a period of water deficit? One possible rationale could be that plants under water stress display reduced growth, which results in decreases in the overall biomass for herbivorous insects to feed on. The activation of the wound response by water-deficit stress would protect the plant against defoliating chewing insects during periods of low growth and would preserve limited foliage until water resources are no longer limiting, thereby improving their survivability. Alternatively, the water deficit-mediated activation of the wound response could simply be a serendipitous event due to functional redundancy in stress signaling networks. We are beginning to discover that responses to stress are not linear pathways, but are complicated integrated circuits involving multiple pathways and specific cellular compartments, tissues, and the interaction of additional cofactors and/or signaling molecules to coordinate a specified response to a given stimulus. The work described here provides another important step toward unraveling the interactions of stress-activated pathways in plants.
Plant Material Wild-type tomato (Lycopersicon esculentum cv Castlemart and cv Better Boy), mutants def-1 and spr-1 (cv Castlemart), transgenic tomato plants overexpressing the sense orientation of PS cDNA (cv Castlemart), and the antisense orientation of PS cDNA (cv Better Boy) were grown in peat pots for 17 h at 28°C under >300 µE m-2 s-1light followed by a 7-h, 17°C dark period. Plants at this stage of development displayed two expanded leaves and a small apical leaf.
Seven-day-old seedlings in peat pots were transferred to plastic trays and
were watered at their base to avoid background due to touch response
(Stratmann et al., 2000b
Leaves were harvested at the times indicated in the "Results"
and were immediately frozen in liquid nitrogen for RNA extraction. A minimum
of three plants per time point was used. Total RNA extractions were performed
using Trizol reagent (Life Technologies, Gaithersburg, MD) following
manufacturer instructions. Twenty micrograms of total RNA was loaded in 1.4%
(w/v) agarose gels for separation, and gel-blot analyses were performed as
described in Moura et al.
(2001
All molecular biology procedures and solutions used here were as described
by Sambrook et al. (1989
I thank the following: Dr. Clarence A. Ryan (Washington State University, Pullman, WA) for his generous support that enabled me to conduct this research in his laboratory; Dr. Daniel Moura (Washington State University, Pullman, WA) for his invaluable help on the northern-blot analyses and generation of figures; Sue Vogtman (Washington State University, Pullman, WA) for growing and maintaining the plants used in this research; and Dr. Gregg A. Howe (Michigan State University, East Lansing, MI) for his generous gift of the spr-1 mutant. Received December 31, 2002; returned for revision February 25, 2003; accepted April 29, 2003.
1 This research was supported in part by Washington State University College of Agriculture and Home Economics (Project no. 1791), by the National Science Foundation (grant no. IBN 9601099), and by the U.S. Department of Agriculture/Competitive Grants Research Office (grant no. WNP03153).  * E-mail dombrowj{at}onid.orst.edu; fax 541–738–4160.
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TOP
ABSTRACT
RESULTS
-3 fatty acid desaturases in defense response of higher plants.
J Plant Res 111:
481-486
-glucan elicitor in suspension-cultured Lycopersicon peruvianum
cells. Proc Natl Acad Sci USA 97:
8862-8867
