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Abscisic Acid Is Involved in the Wound-Induced Expression of the Proteinase Inhibitor II Gene in Potato and Tomato HUGO PENA-CORTIS*T, Jose J

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Abscisic Acid Is Involved in the Wound-Induced Expression of the Proteinase Inhibitor II Gene in Potato and Tomato HUGO PENA-CORTIS*T, Jose J Proc. Nadl. Acad. Sci. USA Vol. 86, pp. 9851-9855, December 1989 Botany Abscisic acid is involved in the wound-induced expression of the proteinase inhibitor II gene in potato and tomato HUGO PENA-CORTIS*t, Jose J. SANCHEZ-SERRANO*, RUDIGER MERTENSt, LOTHAR WILLMITZER*, AND SALOME' PRAT* *Institut fur Genbiologische Forschung Berlin GmbH, Ihnestrasse 63, D-1000, Berlin 33, Federal Republic of Germany; and tSchering AG, Gollanczstrasse 57-101, D-1000, Berlin 28, Federal Republic of Germany Communicated by J. Schell, August 9, 1989 ABSTRACT Plants respond to wounding or pathogen at- abscisic acid (ABA) have been reported as a result of water tack by a variety of biochemical reactions, involving in some or osmotic stress conditions (8, 9), whereas ethylene biosyn- instances gene activation in tissues far apart from the actual site thesis has been associated with the initial response of the of wounding or pathogen invasion. One of the best analyzed plant tissue to mechanical wounding (10). Indirect evidence examples for such a systemic reaction is the wound-induced for the involvement of ABA in wound responses has also expression of proteinase inhibitor genes in tomato and potato been obtained from two maize proteins, whose synthesis is leaves. Local wounding ofpotato or tomato plants results in the induced by water stress and by ABA and in addition shows accumulation of proteinase inhibitors I and II throughout the low wound inducibility (11, 12). aerial part of the plant. In contrast to wild-type plants, abscisic We, therefore, decided to test whether or not ABA is acid-deficient mutants ofpotato (droopy) and tomato (sit) show involved in the systemic induction of the PI-II gene. More a drastically reduced induction of these genes in response to specifically, we asked the following questions: (i) Does plant wounding. High levels of proteinase inhibitor II gene treatment of nonwounded plants with ABA lead to an induc- expression are obtained in mutant and wild-type plants upon tion of PI-II gene expression? (ii) Do ABA-deficient mutant exogenous application of abscisic acid. Measurements of the plants show a reduced wound-induced expression ofthe PI-Il endogenous abscisic acid levels in wild-type plants show that gene and, if so, can this defect be complemented by applying wounding results in increased levels of this phytohormone in exogenous ABA? (iii) Do known antagonists of ABA reduce wounded and nonwounded systemically induced leaves. Thus or suppress the wound-related induction ofPI-Il gene expres- these results show that the plant hormone abscisic acid is sion? (iv) Does wounding lead to an increased level of ABA involved in the wound-induced activation of the proteinase in wounded and nonwounded parts of the plant? inhibitor II gene. Furthermore,-they are compatible with a In this report we present data based on the analysis of model assuming this hormone to be the actual mediator of the ABA-deficient potato and tomato mutants that strongly sug- systemic wound response. gest that the phytohormone ABA is directly involved in the induction of PI-II genes. Potato and tomato plants accumulate proteinase inhibitors I and II in leaves as a direct consequence of insect damage or mechanical wounding. Both inhibitors are specifically di- MATERIALS AND METHODS rected against insect proteases and are considered to be part Plant Material and Chemicals. Potato line cv. Berolina, of the natural defense mechanism of plants against attacking tomato cv. Money maker, ABA-deficient mutant potato insects (1-3). The accumulation of these proteins is not (droopy, provided by S. Quarrie, Agriculture and Research restricted to the wound site, but it is also observed in Council Institute of Plant Science Research, Cambridge, nonwounded aerial tissues. This indicates that upon wound- U.K.), and tomato (sit, provided by M. Koornneef, Landbouw- ing an inducing factor or wound hormone is released that, universiteit Wageningen, The Netherlands) were grown under probably by way of the vascular system, is rapidly trans- greenhouse conditions (16°C day/10°C night, 50-80% rela- ported to other tissues of the plant, thereby inducing the tive humidity, and normal photoperiod, 14 hr of light). Chito- expression of these proteinase inhibitor genes. Pectic poly- san (from crab shells), gibberellic acid (GA3), (±+-)-ABA, cyclo- saccharides derived from the cell wall have been shown to be heximide, and chloramphenicol were obtained from Sigma. powerful inducers of the proteinase inhibitor genes when Chitosan and GA3 Application. Chitosan was treated before supplied to excised leaves through the cut petiole and have use with nitrous acid according to Hadwiger and Beckman thus been postulated as a possible proteinase-inhibitor- (13). Leaves were harvested and incubated in a solution inducing factor (4-6). In a similar way oligosaccharides such containing chitosan, GA3, or ABA as described by Pefia- as chitosan have been shown to be strong inducers of the Cortes et al. (1). GA3 was dissolved in 5 mM KOH. proteinase inhibitor II (PI-II) gene (1). By using radiolabeled ABA Application. ABA solutions [10 and 100 ,uM (±)-ABA oligosaccharides, however, Baydoun and Fry (7) have shown in sterile water/0.01% ethanol] were applied to plants by that molecules with a degree of polymerization greater than aerial spraying every 6 hr for the entire test period or, 6 do not travel long distances through the plant vascular alternatively, by direct incubation of detached leaves in the system, which argues against them actually mediating the solution. systemic activation of the PI-II gene. Wounding of Potato and Tomato Leaves. Potato and tomato Wounding represents, on the other hand, a special case of leaves were wounded according to Sanchez-Serrano et al. stress for the plant cell. Stress conditions elicit a number of (3). physiological responses, often resulting in changes in the Isolation and Analysis of RNA. Isolation of RNA was internal levels of plant hormones. Thus elevated levels of performed as described by Logemann et al. (14). For gel The publication costs of this article were defrayed in part by page charge Abbreviations:.PI-II, proteinase inhibitor II; ABA, abscisic acid; payment. This article must therefore be hereby marked "advertisement" GA3, gibberellic acid. in accordance with 18 U.S.C. §1734 solely to indicate this fact. tTo whom reprint requests should be addressed. 9851 Downloaded by guest on October 3, 2021 9852 Botany: Pefia-Corte's et al. Proc. Natl. Acad. Sci. USA 86 (1989) electrophoretic analysis, RNA was denatured with formal- wild-type mutant dehyde in the presence offormamide and electrophoresed on cont wound ABA wound ABA cont 1.5% agarose gels. RNA was transferred to nylon membranes and hybridized using PI-1I cDNA-1 (3) as a probe. Hybrid- ization and washing conditions were performed as described (1). The amount of RNA on the membranes was checked by *e hybridizing them to a rRNA probe (data not shown). Protein Analysis. Proteins from seeds of tobacco, tomato, and potato plants were extracted according to Racusen and 1 2 3 4 5 6 7 8 Foote (15), separated by gel electrophoresis (16), and ana- FIG. 2. Accumulation of PI-II mRNA in potato leaves of ABA- lyzed by the Western blot technique as described (17). The deficient mutant and wild-type plants upon wounding and ABA- antibody used for this experiment was raised against the treatment. Total RNA was isolated from leaves of nonwounded (lane potato tuber PI-II protein and purified by affinity chroma- 1, cont), wounded (lane 2), and ABA-sprayed (lanes 3 and 4) tography using an oligopeptide representing the 16 carboxyl- wild-type potato plants (Solanum tuberosum L.) and from non- terminal amino acids ofthe PI-IT protein, as deduced from the wounded (lane 8, cont), wounded (lane 5), and ABA-sprayed (lanes clone cDNA-1 (3). 6 and 7) droopy mutant potato plants (Solanum tuberosum L., group ABA Quantitation. ABA was extracted from potato leaves. phureja), respectively (19). Harvested leaves were immediately frozen in liquid nitrogen levels. More significantly, the systemic induction was limited after weight determination. Tissue was then homogenized in to the aerial parts of the plant with no induction detected in an extraction solution containing 80%o (vol/vol) methanol and and subsequently the root and lower part of the stem. Identical responses were butylated hydroxytoluene (2.5 mg/liter) a ABA Con- mixed for 1 hr at 40C in darkness. The extract was centrifuged obtained with lower concentration of (10 ,uM). at 3000 x g for 7 min at 40C, and the resulting pellet was trol plants sprayed with water did not show any accumulation reextracted twice with the extraction buffer, as described of PI-II mRNA (data not shown). ABA sprayed to the leaves above. The supernatants were pooled, equilibrated in 70% of a plant is thus able to trigger the systemic induction of the methanol, and applied to a 2-ml bed volume Sep-Pak C18 PI-II gene, with a pattern identical to the one described for column (Millipore). Methanol was removed from the frac- wounded plants (1). tions by evaporation in a Rotavapor (Buchi Instruments, Potato and Tomato ABA-Deficient Mutant Plants Fail to Geneva). Samples were dried and resuspended in PBS (10 Accumulate PI-Il mRNA upon Wounding but Show High mM sodium phosphate, pH 7.4/0.15 M NaCl). An aliquot was Levels of PI-Il Expression as a Result of Exogenous ABA used to determine the amount of ABA in the sample by a Application. The induction of PI-TI genes in nonwounded monoclonal antibody-based RIA assay, as described (18). A plants as a direct consequence of ABA application provides minimum of five plants was used for establishing each ABA preliminary evidence that this hormone is involved in the concentration value.
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