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Heat-shock proteins are induced in unstressed leaves of Nicotiana attenuata (Solanaceae) when distant leaves are stressed¹

²Syracuse University, Biological Research Labs, Syracuse, New York 13244 USA; and ³Desert Research Institute, Reno, Nevada 89512 USA

Received for publication April 18, 2000. Accepted for publication June 27, 2000.

	ABSTRACT

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In Nicotiana attenuata, systemic induction of heat-shock proteins (Hsps) was detected in response to the treatment of single leaves by either heat shock, mechanical damage, or exogenous application of methyl jasmonate (MJ). All treatments increased the abundance of members of the 70-kD Hsp (Hsp70) family and induced synthesis of one or more of the small Hsps (sHsp) (16–23 kD) in both treated and untreated leaves. These results provide the first evidence that Hsps can be systemically induced in plants and suggest that systemic induction of Hsps may be important in pre-adapting leaves to stress.

Key Words: heat-shock • Hsp • mechanical damage • methyl jasmonate • Nicotiana • Solanaceae • systemic induction

	INTRODUCTION

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In higher plants, the systemic induction of defensive compounds by mechanical, insect and pathogen damage is well-characterized (Karban and Baldwin, 1997 ). For example, in some species, the attack of a single leaf by a pathogen or herbivore can elicit a range of induced defensive responses in undamaged leaves. These defensive responses are elicited by a variety of systemic signal molecules such as jasmonic acid and systemin (Karban and Baldwin, 1997 ). However, to our knowledge, systemic induction of heat-shock proteins (Hsp) in response to damage or heat stress has not been reported. This is somewhat surprising, because mechanical damage is known to increase Hsp protein or mRNA levels (Heikkila et al., 1984 ; Henry-Vian et al., 1995 ). In addition, mechanical damage elicits a systemic oxidative burst in species from several plant families (Orozoco-Cardenas and Ryan, 1999 ). This is interesting because it has been demonstrated that small Hsps (sHsp) are induced by oxidative stress (Downs and Heckathorn, 1998 ; Heckathorn et al., 1998 ).

Evidence indicates that Hsps play a role in tolerance to a variety of biotic and abiotic stresses (Vierling, 1991 ; Parsell and Lindquist, 1994 ). Thus, Hsps appear to be general stress proteins that are involved in maintaining cell function and survival during stress or facilitating recovery from stress (Vierling, 1991 ; Parsell and Lindquist, 1994 ; Downs and Heckathorn, 1998 ; Guy and Li, 1998 ; Heckathorn et al., 1998 ). Of particular interest, because of their identified importance in many types of plant stress, are two classes of Hsps, the Hsp 70 class (70 kD) and the small Hsp (sHsp) class (15–30 kD) (Parsell and Lindquist, 1994 ; Guy and Li, 1998 ). The Hsp70 class of proteins are believed to act as molecular chaperones and are found in the cytosol and most organelles (Parsell and Lindquist, 1994 ; Guy and Li, 1998 ). Constitutively expressed Hsp70s assist protein folding and translocation. During heat stress, Hsp70s may be involved in the refolding of denatured proteins or preventing them from stress-induced damage (Parsell and Lindquist, 1994 ; Guy and Li, 1998 ). The sHsp class consists of five major forms, which are localized to the (1) cytosol (two forms), (2) chloroplast, (3) mitochondrion, and (4) endoplasmic reticulum. Recently, potential functions of the chloroplast and mitochondrion-localized proteins have been elucidated. These sHsps appear to protect electron transport when plants are exposed to heat and oxidative stress (and also photoinhibition in chloroplasts) (Downs and Heckathorn, 1998 ; Heckathorn et al., 1998 ; Downs, Ryan, and Heckathorn, 1999 ).

Currently it is thought that Hsp production results solely from the response of individual cells to a stress or stimuli experienced directly by those cells. In nature, plant leaves rarely experience identical environmental or physiological conditions simultaneously. For example, leaves on the east side of the plant are likely to experience their maximal daily temperature several minutes to hours before those on the west. Therefore, heat stress on one leaf may be a strong predictor of forthcoming heat stress on other leaves. It may be advantageous for plants to have a mechanism that allows heat-stressed leaves to signal unstressed leaves. This would enable unstressed leaves to produce protective responses prior to heat stress. This same argument is thought to explain the forces driving the evolution of systemic defense systems for other stresses (Karban and Baldwin, 1997 ). Therefore, we hypothesize that a systemic signal(s) could be sent from a stressed leaf to a nonstressed leaf that would result in increased production of Hsps in unstressed leaves.

This study was conducted to determine whether Hsps could be systemically induced by heat stress and mechanical damage in Nicotiana attenuata (Torrey ex. Watson). Additionally, the potential role of methyl jasmonate (MJ) in the systemic production of Hsps was investigated. MJ is the methyl ester of the endogenously produced plant hormone, jasmonic acid. Jasmonates act as developmental regulators and signal molecules in plant responses to tissue and membrane damage (Creelman and Mullet, 1997 ). In Nicotiana species, MJ systemically induces the production of nicotine (Baldwin, Schmelz, and Ohnmeiss, 1994 ; Baldwin, 1996 ) and induces a range of other responses in many species throughout the plant kingdom (e.g., tendril coiling, fruit ripening, and increased disease resistance; Creelman and Mullet, 1997 ). Since heat shock disrupts cell membranes (Parsell and Lindquist, 1994 ) and hence may induce the production of jasmonic acid, we predicted that exogenous MJ application might induce Hsp production.

	MATERIALS AND METHODS

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Plant material and growth conditions
Nicotiana attenuata (Torrey ex. Watson) plants were grown from seed in 15-cm pots containing commercial potting soil and were watered daily and fertilized weekly (20:20:20 N:P:K +micronutrients; Peters Professional Plant Food; Scotts-Sierra, Marrysville, Ohio, USA). Plants were raised in growth chambers under 18°/26°C night/day temperatures and at 900 µmol·m^-2·s^-1 PPFD (photosynthetic photon flux density). Twenty mature rosette-stage plants (50 d post germination) were assigned randomly to one of five treatment groups: (1) controls, grown at 18°/26°C night/day growth temperatures, (2) whole plants heat shocked at 42°C for 4 h, (3) plants with single leaves heat shocked at 42°C for 4 h, (4) plants with single leaves mechanically damaged, and (5) plants treated with 50 µg of methyl jasmonate applied in a lanolin mull (Baldwin, 1996 ) to a single leaf. Three plants were also treated with methyl-jasmonate-free lanolin. Treatment with lanolin alone had no significant effects, therefore these data are not presented. Whole-plant heat shock was carried out in growth chambers (as in Downs et al., 1998 ; Heckathorn et al., 1998 ), and the heat stress for both whole plants and single leaves was applied gradually by increasing the temperature over 1.5 h to 42°C. Leaf 6, from the apex of the plant (Fig. 1), was heat shocked by enclosure in a humidified petri-dish chamber (10-cm diameter) flushed with air warmed by a hand-held hair dryer. The hair dryer was attached to a tube with adjustable baffles that enabled regulation of leaf temperature. Temperature of the single heat-stressed leaf and untreated leaves on the same plant was monitored with thermocouples throughout the experiment. The temperature of untreated leaves did not increase relative to control plants (26°C) at any time during the heat shock. Control plants had single leaves placed in a petri-dish chamber flushed with 26°C air by a hand-held hair dryer with the temperature monitored by thermocouples; the temperature did not go above 26°C at any time. After treatment, all temperatures were returned to that of control conditions. Mechanical damage was imposed using a sewing pattern wheel (Prym-Dritz, Spartansburg, South Carolina, USA) to produce four lines of damage on either side of the leaf mid-rib (Ohnmeiss and Baldwin, 1994 ). MJ was applied in a lanolin mull (Baldwin, 1996 ) along the leaf mid-rib (50 µg of MJ per leaf). This level of MJ in is within the physiologically relevant range and is actually lower than the amount required (180 µg·leaf^-1·plant^-1) to elicit a "damage-like" induction of nicotine in wild Nicotiana species (Baldwin, 1996 ; Baldwin et al., 1997 ). Plants from all treatments, with the exception of whole-plant HS, were placed in the same growth chamber during treatments. A fan was placed in the chamber door to provide additional ventilation. The experiment was repeated, and we obtained results that were similar to those reported here.

View larger version (46K): [in this window] [in a new window]   Fig. 1. Drawing of Nicotiana attenuata showing the leaves that were harvested at 8 and 24 h. Leaf 6 was the treated leaf (T) (e.g., heat shocked at 42°C, mechanically damaged with a pattern wheel or treated with 50 µg of methyl jasmonate in lanolin) and was harvested at 8 h along with the untreated (U) leaf 8. Untreated leaves 5 and 7 were harvested at 24 h. For reference leaf 1 is labeled with an arrow

	RESULTS

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Heat stress
When whole, intact N. attenuata plants were heat stressed (i.e., whole-plant heat stress; = WP-HS in Fig. 2), the content of the Hsp70 and sHsp (16–21 kD) families in leaves increased relative to unstressed controls within 8 h (Fig. 2A; lanes 1 and 2). When single leaves of intact N. attenuata plants were heat stressed (i.e., single-leaf heat stress; = SL-HS), the content of Hsp70 and two sHsps increased in the single leaves that were heat stressed (Fig. 2A: lane 3). When leaves from plants subjected to single-leaf heat stress were analyzed, the abundance of both Hsp70 and sHsp increased in both stressed and unstressed leaves relative to controls (Fig. 2: lanes 3 and 4). Quantification of immunoblots indicated that the Hsp70 content was greatest in SL-HS leaves and lowest in untreated leaves of SL-HS plants (Fig. 3A). In WP-HS leaves, sHsps ranging from 16 to 21 kD accumulated in response to heat shock. However, when a single leaf was heat shocked, there was no apparent accumulation of the Hsp16. In the untreated leaf from SL-HS plants, a single 21-kD band accumulated. In SL-HS plants, the level of the 21-kD sHsp in treated leaves was not different from WP-HS plants. The sHsp content in the untreated leaf of SL-HS plants was 50% lower than WP-HS leaves (Fig. 3C). The appearance of Hsp70 and sHsp family members in untreated leaves from SL-HS plants suggests that there may be a systemic induction of these Hsps.

View larger version (53K): [in this window] [in a new window]   Fig. 2. Immunoblots of whole-leaf extracts from control plants (C), whole plants (WP) subjected to heat stress (HS), or plants on which single leaves (SL) were either heat stressed, mechanically damaged (MD), or treated with methyl jasmonate (MJ). Leaves were harvested either: (A) after an 8-h heat stress; (B) 24 h after heat stress; (C) 8 h following mechanical damage or methyl jasmonate treatment; or (D) 24 h after mechanical damage or methyl jasmonate treatment. Treated (T) or untreated (U) leaves were harvested and assayed for content of Hsp70 or sHsp. Total protein was extracted from leaves and fractionated by SDS-PAGE. Then proteins were electroblotted to membranes and probed with anti-Hsp70 or anti-sHsp. Arrows to the right of blots correspond to molecular mass markers. Each lane contained 50 µg of total protein. Blots are representative of four replicates, each from a different plant

View larger version (30K): [in this window] [in a new window]   Fig. 3. Mean ± 1 SE increase in content of Hsp70 or sHsp above controls in treated (T) or untreated (U) leaves harvested from whole plants (WP) subjected to heat shock (HS), or plants on which single leaves (SL) were subjected to HS, mechanical damage (MD), or methyl jasmonate (MJ) treatments. Results are densitometric values from immunoblots of (A) Hsp70 at 8 h and (B) Hsp70 in leaves above (leaf 5) and below (leaf 7) the treated leaf 24 h following treatment. The sHsp (21-kD) was compared to WP-HS plants at (C) 8 h and (D) in leaves above and below the treated leaf 24 h following treatment. For Hsp70 quantification, a value of 0% corresponds to the amount of Hsp70 in control leaves. For sHsp (21-kD) quantification, a value of 100% corresponds to the amount of sHsp (21-kD) in whole-plant heat shocked leaves. Bars with the same letter are not significantly different at P = 0.05. Bars marked with an asterisk are comparisons of leaves above and below the treated leaf and are not significantly different at P = 0.05

Mechanical damage and methyl jasmonate treatment
Eight hours after mechanical damage to a single leaf (SL-MD) the abundance of Hsp70 and a single sHsp (21 kD) in the treated leaf increased (Fig. 2C: lane 2). There was no increase over the untreated control in Hsp70 and sHsp abundance in undamaged leaves on the SL-MD plants after 8 h (Fig. 2: lane 3). The application of 50 µg of MJ to a single leaf (SL-MJ) increased the content of both Hsp70 and a single sHsp (21 kD) in treated leaves (Fig. 1C: lane 4). In untreated leaves from SL-MJ plants, the abundance of Hsp70 or sHsp did not increase within 8 h (Fig. 2C: lane 5). The relative increase above control levels of Hsp70 and sHsp abundance in SL-MD and SL-MJ plants was 50–60% less than the levels found in WP-HS leaves (Fig. 3A).

After 24 h there was no significant difference between leaves 5 and 7 in Hsp70 or sHsp abundance for any treatment (Fig. 3B, D) and therefore only leaf 7 data are presented in Western blots. In contrast to the results at 8 h, after 24 h untreated leaves from SL-MD plants had increased amounts of Hsp70 and a single sHsp (21 kD) in untreated leaves (Fig. 2D: lane 2). Increased abundances of Hsp70 and a single sHsp (21 kD) were also detected in untreated leaves from SL-MJ plants after 24 h (Fig. 2D: lane 3). The increase above control levels of Hsp70 in SL-MD and SL-MJ plants was 10% less than the levels found in WP-HS leaves, but was not different from SL-HS plants (Fig. 3B). When compared to WP-HS, the abundance of sHsp was lower in SL-MD and SL-MJ plants (Fig. 3D).

	DISCUSSION

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The results of these experiments demonstrate that three localized stresses—heat shock, mechanical damage, and MJ treatment—can increase Hsp accumulation in tissues that did not directly experience the stress. This suggests that the induction of Hsps is not strictly a cellular response to stressful conditions, but may be a part of a whole-plant response to stress. The most significant finding is the accumulation of Hsp in adjacent unstressed leaves at 8 h when a single leaf was subjected to heat stress. It is unlikely that this is due to differences in leaf development because no increased Hsp accumulation was observed in different-aged leaves from control plants. By removing the heat-stressed leaf at 8 h and testing leaves from the same plant at 24 h for Hsp accumulation, we have data suggesting that systemic induction of Hsps occurred. Zhang and Baldwin (1997) showed that leaf-applied ¹⁴C-jasmonic acid was transported out of a treated leaf to other leaves and roots within 3 h of application. It is possible that the observed response is elicited by a stress "signal" that exits the treated leaf within 8 h. Data from the mechanical damage and MJ application treatments further support this idea, because Hsp induction occurred locally in these treatments within 8 h, whereas systemic induction in untreated leaves did not occur until 16 h after removal of the treated leaf.

It is possible that the volatilization of MJ from treated leaves is the cause of the observed response in control leaves that were not directly treated with MJ. It is known that volatile MJ can cause the induction of "stress" responses in plants that are kept in small sealed chambers without the circulation of fresh air (Farmer and Ryan, 1990 ; Avdiushko et al., 1995 ). There are two pieces of evidence that suggest that volatile MJ was not the cause of the observed responses. First, after treating plants with MJ, both control and treated plants were present in the same growth chamber. The induction of Hsps in only treated plants and not the controls suggests that volatile MJ concentrations in the growth chamber were not high enough to elicit the response. Second, to ensure that high volatile MJ concentrations were not localized near the leaves of treated plants relative to controls, fresh air was circulated in the growth chambers in order to homogenize MJ concentrations. Although we did not quantify local concentrations of MJ in the chamber, it is likely that they were low in the proximity of untreated leaves. Even if volatile MJ, and not a systemic signal, caused the induction of Hsps in leaves that did not receive the MJ treatment, the major point of this paper would still be valid. Both heat shock and mechanical damage unambiguously induced the production of Hsps in leaves that did not receive either stress. This suggests that heat shock protein production can occur in cells that do not directly experience the environmental signal.

The systemic induction of Hsps may serve a protective function in unstressed leaves. For example, leaf temperatures can vary significantly within a single plant, throughout the day (Larcher, 1995 ), which may stress only certain leaves at any given time. The potential ability of stressed leaves to signal other leaves and induce the production of Hsps suggests that a systemic nature of the heat-shock response might be adaptive for stress tolerance. It may prepare unstressed leaves for a stress that might occur in the near future. Additionally, induced responses are believed to reduce the resource costs associated with the production of a given response (reviewed in Karban and Baldwin, 1997 ). With respect to Hsps, nitrogen availability has been demonstrated to influence their accumulation (Heckathorn et al., 1996a ) as well as their potential protective ability (Heckathorn et al., 1996b ). This suggests that induction of Hsps may also act as a cost-saving measure, particularly since they play such a vital role in the survival and fitness of organisms (Feder and Hofmann, 1999 ).

	FOOTNOTES

 
¹ The authors thank I Baldwin for providing seeds and S. A. Heckathorn, D. S. Luthe, S. J. McNaughton, J. L. Zimmerman, and an anonymous reviewer for comments on this manuscript. This research was supported by the NSF and the Andrew W. Mellon Foundation.

⁴ Author for reprint requests (ewhamilt{at}syr.edu ).

⁵ Current address: Washington and Lee University, Biology Department, Lexington, VA 24450.

	LITERATURE CITED

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———, ———, ———, and ———. 1996b Nitrogen availability and vegetative development influence the response of ribulose 1,5-bisphosphate carboxylase/oxygenase, phosphoenolpyruvate carboxylase, and heat-shock protein content to heat stress in Zea mays L. International Journal of Plant Sciences. 157: 546–553

———, C. A. Downs, T. D Sharkey, J. S. Coleman 1998 The small, methionine-rich heat-shock protein protects photosystem II electron transport during heat stress. Plant Physiology 116: 439–444[Abstract/Free Full Text]

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This Article Abstract Full Text (PDF) Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via ISI Web of Science (6) Citing Articles via Google Scholar Google Scholar Articles by Hamilton III, E. W. Articles by Coleman, J. S. Search for Related Content PubMed PubMed Citation Articles by Hamilton III, E. W. Articles by Coleman, J. S. Agricola Articles by Hamilton III, E. W. Articles by Coleman, J. S.