Wound-Inducible Genes
in Plants
Lan Zhou and Robert Thornburg
Department of Biochemistry and Biophysics, Iowa State INTRODUCTION
All living organisms are involved in a constantly struggle with and against other organisms to exploit their environment. Every organism exploits its ownenvironmental niche to gain nutrients for growth and development. However,when multiple organisms interact, then a direct competition is established be-tween those organisms. The organism that is better able to compete usually hasan evolutionary advantage and is assured of survival. Some organisms movewhen in direct competition, however, because of their sedentary lifestyle, plantsgenerally can not. Instead, plants have developed very potent biochemical re-sponses that serve to protect their integrity and to limit the invasive nature of thecompeting organisms.
Structurally, plants have a polyester coating composed of cutin and suberin (Kolatakuddy, 1980). This coating normally isolates the plant tissues from com-peting organisms and plants are therefore relatively immune from the presenceof these competitors even on their surface. However, if a break or wound occursin this surface coating, then competing organisms gain entrance into the plant’stissues where they can cause injurious damage to those tissues. Consequently,plants have developed a complex response to wounding that dramatically altersthe cellular physiology of plant tissues and results in the production of defenses.
These defenses are particularly potent against microorganisms and are even ef-fective against small herbivores.
The response of plants to wounding has been studied since the early 1970s when Green and Ryan (1972) discovered that an inhibitor of chymotrypsin intomato leaves accumulated in response to wounding. Further, because chymot-rypsin-like proteins do not occur in plants, but are common in insect digestive CAB International 1999. Inducible Gene Expression tracts, they concluded that this inhibitor was part of a wound-responsive plantdefense system. Since that time at least 70 other proteins have been identified asalso being wound-inducible.
Table I provides a list of different genes that have been demonstrated to be wound-inducible. This list is not meant to be all inclusive, but it does give a broadperspective of both the number and classes of plant genes that have been identi-fied to date as being wound-inducible. Many of these genes are discussed in somedetail below. In addition, this table provides additional information about themodes of regulation where known for each particular gene. In some cases, genesencoding a particular protein have been described from multiple species. Thereare sometimes differences in regulation of the genes between species for indi-vidual genes. In addition, many of the genes listed in Table I are members ofmultigene families. In these cases, the several members are often differentiallyregulated, with only one or a few members of the family being wound-inducible.
Because any attempt to adequately discuss the expression of 70 different proteins from at least 38 species across 20 families would result in a morass ofcontradictory information. We will, therefore, limit this article to two areas ofdiscussion. First, because of this large number of proteins that are induced inresponse to a wound, we can identify the classes of proteins produced and begin todraw some conclusions about overall biochemical processes that are important inresponse to a wound. Secondly, there are a few wound-inducible proteins andtheir genes that have been studied in great detail, and the mechanisms of geneactivation of several seemingly unrelated proteins (i.e., proteinase inhibitors ofthe solanaceae and vegetative storage proteins of the fabaceae) share many de-tails of gene activation. Therefore, we will also examine the details of the mecha-nisms of gene activation for these well studied systems.
Wounding results in the activation of many different genes within a plant.
The types of genes and the timing of their activation allows the identification ofdifferent phases following a wound. Each of these phases of the wound-inductionprocess biochemically solves a different problem that wounding causes the plant.
These problems include: placing mechanical barriers to invading organisms, seal-ing the wound tissue, activating defensive compounds against invading organ-isms and recovering from the wound. The sum of these processes results in recov-ery from a wound and return to a normal physiology.
The hydrogen peroxide response
The initial phase of a wound-response is a rapid reaction to close the wound therebyprotecting the plant from loss of cellular components and restricting entry of mi- croorganisms into the plant tissues. This is composed of at least two generalprocesses. Initially there is an almost immediate oxidative burst that results in acrosslinking of plant cell wall proteins (Bradley et al., 1992; Brisson et al., 1994).
This oxidative burst can be detected within 15 seconds. This crosslinking of thecell wall proteins provides a structural barrier that inhibits the invasion of micro-organisms. In addition, H2O2 from this oxidative burst is thought to activate some of the wound-inducible genes (Levine et al., 1994). Because hydrogen per-oxide is itself toxic to plant cells (Lachman, 1986), there are numerous peroxi-dases that are produced in response to a wound to limit peroxide accumulation(Diehn et al., 1993; Mohan et al., 1993).
Up-regulation of phenylpropanoids
In addition to this peroxide response, there is a general up-regulation of genesencoding the phenyl propanoid pathway. The kinetics of this activation are alsoextremely rapid, with new mRNAs for these enzymes appearing within 15 min-utes (Templeton and Lamb, 1988; Lawton et al., 1983). This up-regulation of thephenyl propanoid pathway genes may be regulated by the H2O2 burst because the direct addition of H2O2 to bean suspension cells induced the accumulation of mRNAs encoding phenylalanine ammonia lyase, chalcone synthase and chalconeisomerase (Mehdy, 1994). The function of the up-regulation of these genes is toprovide the cell with lignin precursors which can reseal the wounded surface andto provide cells with precursors of phenolic plant defensive compounds. .
Inactivation of photosynthetic translation
The second phase of the wound response particularly in monocots, is a turn-off ofphotosynthetic protein translation by arresting the translation of nuclear encodedphotosynthetic genes (Criqui et al., 1992; Reinbothe et al., 1993c). Because main-tenance of the photosynthetic apparatus represent a major expenditure of cellu-lar energy, repressing the synthesis of new proteins would save energy for theplant following the wound. Among these down-regulated proteins are those forthe small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase (SSU, rbcSgene product) and several light harvesting chlorophyll protein complex apoproteins(LHCPs, cab gene products). However, the changes in protein synthesis do notcorrespond to equivalent changes in the rbcS and cab transcript levels. Rather,these mRNAs are shifted to smaller polysomes in methyl jasmonate-exposed leaftissues (Reinbothe et al., 1993a). Control mRNAs encoding leucyl-tRNA synthetase(LRS1, lrs1 gene product) neither changed its abundance nor its association withpolysomes in methyl jasmonate-treated leaves and was translated into the corre-sponding polypeptide.
Several mechanisms are responsible for this altered regulation of the photo- synthetic machinery. First, methyl jasmonate induces a shift in the 5' untranslatedregion of the rbcL transcript (Reinbothe et al., 1993b). The primary transcript isinitiated at -316 from the translation start codon. Under normal conditions, the5' end of the mature rbcL transcript is processed to yield a mRNA with a 59 bp 5'untranslated region. Following jasmonate treatment, the mRNA is alternativelyprocessed to give a 94 bp untranslated region. This alternatively spliced tran-script contains within the 5' untranslated region, a 35-base motif that has highcomplementarity to the 3' terminus of the 16S rRNA. This portion of the 16SrRNA is involved in intramolecular base pairings within the ribosome and canassociate with 30S but not with 70S complexes. Normal transcripts lacking this35-base motif are active in terms of translation initiation. However, those tran-scripts having this sequence interfere with translation initiation by competingfor ribosome binding at the Shine-Delgarno sequence of the rbcL transcript lead-ing to down regulation of the Large subunit which in turn leads to regulation ofthe Small subunit.
A second method that plants use to alter protein synthesis in stressed plant tissues involves the expression of ribosome-inactivating proteins. These havealso been most highly studied in barley. One of these proteins, previously identi-fied as a 60 kDa jasmonate-induced protein (JIP60), has been shown to cleavepolysomes into ribosomal subunits (Chaudhry et la., 1994; Reinbothe et al., 1994).
Finally, chaperonins that interact with ribulose bis phosphate carboxylase/ oxygenase are also strongly repressed following wounding (Zabaleta et al., 1994),thereby further indicating the role of wounding on inhibition of photosynthesis.
Induction of Ethylene Biosynthesis
In addition to being developmentally regulated, ethylene is synthesized followingwounding. SAM synthase catalyzes the formation of S-adenosylmethionine frommethionine and ATP. Ethylene is then formed from S-adenosylmethionine in twosteps (Kende, 1989). The first step is catalyzed by the enzyme ACC Synthase andthe second step by ACC Oxidase.
These genes usually are developmentally expressed in fruit; however, each of the steps in this pathway is also wound-inducible. This wound induction is ap-parently self-propagating because these enzymes are also regulated by ethyleneitself (O’Donnell et al., 1996). Because these genes rely on the synthesis of ethyl-ene to regulate their wound-inducibility, they are often referred to as ethylene-related genes. Varieties of fruit that produce the highest levels of ethylene alsoinduce higher levels of these ethylene-related genes. Some of these ethylene-related genes have unknown functions (Parsons and Mattoo, 1991).
Induction of plant defenses
A major phase of the wound-response is a generalized activation of plant defenses.
Because the majority of microbial infections occur in plants following a wound,plants have developed a variety of biochemical defenses to combat invading patho-gens and even small herbivores. The accumulation of phytoalexins after wound-ing has been a particularly rich area for study. Many different plant species havebeen shown to activate the synthesis of phytoalexins after a wound or after me-thyl jasmonate treatment [Methyl jasmonate has a proposed role in the regula-tion of defense genes. see below]. Phytoalexins are plant synthesized small mo-lecular weight defensive compounds that have biological activity against microor-ganisms or herbivores. These include phenolic, terpenoid, and alkaloid compoundsthat are a major component of plant secondary metabolism.
In the recent literature, some of these induced phytoalexins have been shown to include furanocoumarin biosynthesis in Apium graveolins leaves (Miksch andBoland, 1996); taxol biosynthesis in Taxus cuspidata suspension cultures (Mirjaliniand Linden, 1996); momilactone in suspension cultured rice cells (Nojiri et al.,1996) and alkaloid synthesis in Catharanthus roseus (Aerts et al., 1996). In thesecases, wounding or treatment with jasmonates activates the genes encoding thebiosynthetic pathways for these different biochemicals; however, for many of thesethe individual biochemical steps leading to phytoalexin biosynthesis are not knownor have not been examined.
Some secondary metabolites are even effective against large phytophagous insects. Ramputh and Brown (1996) report on the accumulation of the inhibitoryneurotransmitter, GABA, following mechanical damage of soybean leaves. Theseauthors also demonstrated that increasing levels of GABA decreased the survivalof larvae and increased the length of time that larvae required to pupate.
Leaf damage by herbivores in Nicotiana sylvestris produces a damage signal that dramatically increases de novo nicotine synthesis in the roots. The increasedsynthesis leads to increases in nicotine pools, which in then transported up theplant. This results in increased nicotine pools throughout the plant making plantsmore resistant to further herbivore attack (Baldwin et al., 1994).
In addition to the accumulation of the small molecular weight phytoalexins, plants also activate the synthesis of proteins following a wound. Many of thesewound-inducible proteins are directly active against the growth of herbivores andmicroorganisms. Among these are the serine proteinase inhibitors (Ryan, 1981), α-amylase inhibitors (Ishimoto and Chrispeels, 1996), chitinases (Broglie et al., 1991), β-glucanases (Mauch et al., 1988), osmotin (Grosset et al., 1990) lectins (Casalongué and Pont Lezica, 1985) and others. Each of these enzymes or inhibi-tors performs a specific function in combating the invading herbivore or patho-gen.
The serine proteinase inhibitors and the α-amylase inhibitors are particu- larly effective against insects. These proteins block the digestive processes thatliberate free amino acids or glucose in an insect’s digestive tract. By blockingthese processes, the plant limits the nutrition that an insect can glean from thetissue it eats. While these processes may be rather ineffective against singleinsects that may move from plant to plant, they very effectively reduce the fecun-dity of developing larvae that grow and develop on a single plant. It should alsobe pointed out that while plants have many serine proteinase inhibitors, the pres-ence of serine proteinases in plants is rare (Ryan, 1981). Thus, plants apparentlylack the specific target enzymes of these inhibitors. These enzymes are howeververy rich in the digestive tract of insects, and this has led to the conclusion thatthese inhibitors are targeted against insects.
Chitinases and β-1,3-glucanases are other defensive enzymes that have no natural target in plants. Chitin does not exist in plants and β-1,3-glucans are not major components of plant cells. Chitin and β-1,3-glucans are; however, exten- sively found in the cell walls of fungi. Thus, these defensive compounds are ap-parently directed against invading yeast and fungal microorganisms. The ex-pression of these enzymes limits the growth and development of these microor-ganisms, especially during spore germination.
Additional defensive proteins that accumulate in plants following a wound target other specific features of microorganisms or herbivores to limit their growthand development. Note that antibacterial responses and antiviral responses ap-parently require specific interactions with surface or intracellular receptors inplants that activate the hypersensitive responses (Ritter and Dangl, 1996; Reuberand Ausubel, 1996). These responses are mediated by different signal transduc-tion pathways than the classical wound-induction pathways and in general donot cross communicate. Recently, however, studies on the overexpression of smallGTP binding proteins have demonstrated that altered regulation of these G-pro-teins can lead to cross-signaling between these two pathways (Sano et al., 1994;Sano and Ohashi, 1995).
Induction of storage proteins
In plant families, vegetative storage proteins accumulate in leaves prior to anthe-sis, decline during pod filling and then accumulate again after seed maturation(Staswick, 1989). In woody species such as poplar trees, a similar set of proteinstermed bark storage proteins accumulate in the autumn months in the proteinstorage vacuoles of the inner bark parenchyma and xylem ray cells (Coleman etal., 1994). These proteins are remobilized during the spring bud burst when ac-tive growth dictates a need for nitrogen. This pattern of expression is consistentwith the role of these storage proteins as a temporary sink for nitrogen in thegrowing tissues.
In addition to this developmental mode of gene regulation, these proteins are also induced by wounding and by jasmonates (Staswick et al., 1991; Mason et al., 1992). While the teleological reason for induction of these storage proteins fol-lowing a wound is unclear, perhaps, these storage proteins serve to temporarilystore nitrogen and carbon following a wound. This storage would help protectfrom the loss of these metabolites during the wound response. These wound-induced reserves could later serve as a source for new growth after the wound-recovery phase.
Return to normal physiology
The final phase of the wound-response is a recovery phase that returns the plantcell to a normal physiology. This phase is much longer in duration than the ear-lier phases of the wound-response, generally lasting from days to a week or soafter the wound.
Several unique processes occur during this phase. One of these processes includes the uptake of carbohydrates into the wounded tissues. It is known thatboth extracellular invertases (Sturm and Chrispeels, 1990) and sugar transport-ers (Truernit et al., 1996) are induced following wounding. The extracellularinvertases cleave extracellular sucrose into its component sugars. The sugar trans-porters then re-internalize the monosaccharides that may have been spilt by thewound. This process thereby limits the free carbohydrate content of the extracel-lular milieu for any invading microorganisms.
Thus, wounding of plant tissues produces a large scale alteration of plant metabolism that is initiated almost immediately following a wound. Numerousformerly quiescent genes are activated following a wound that mediate this al-tered metabolism. The changes include sealing the wound at the surface of thecell, limiting photosynthetic translation, induction of hormone biosynthesis, pro-ducing secondary metabolites and defense proteins, producing storage proteins,and finally recovery after the wound to return to a normal physiology.
Because of the wide number of genes that are activated and the very differenttime frames during which these genes become activated, it is certain that numer-ous mechanisms are responsible for wound-inducible gene expression in plants.
While some of these mechanisms may involve peroxide-induction of gene expres-sion (Levine et al., 1994), or ethylene (O’Donnel et al., 1996) perhaps the bestcharacterized of the wound-inducible genes are the proteinase inhibitor genes ofsolanaceous plants and the vegetative storage protein genes that are similarlyregulated. The remainder of this article will discuss the mechanism of wound-induction of the proteinase inhibitor and vegetative storage protein genes.
One of the most striking characteristics about the wound-inducibility of the pro-teinase inhibitor genes in solanaceous plants is the fact that local wounding trig-gers expression of these genes at a distal site. Currently there are two mecha-nisms that have been proposed to trigger the wound-induced systemic accumula-tion of these proteinase inhibitor genes. These mechanisms are mediated by ei-ther electrical or chemical signals.
Electrical signals
Wildon et al., (1992) have showed that wounding of the cotyledons of a youngtomato plant results in a slow moving action potential that propagates away fromthe site of the wound toward the upper leaves. In all cases, this action potentialcorrelates with the induction of proteinase inhibitor genes. Plants are unique, inthat they have symplastic connections that continue throughout the organism.
These connections are made by plasmodesmota, and are well suited for electricalsignals.
This work has been confirmed (Herde et al., 1995; Stankovic and Davies, 1995) and expanded (Rhodes et al., 1996). Herde et al., (1995) showed that theelectrical induction of the proteinase inhibitor genes correlated with alterationsof the stomatal aperture . Stankovic and Davies (1995) showed that both electri-cally stimulated action potentials and flame-induced hydraulic signals could in-duce high levels proteinase inhibitor mRNA. Rhodes et al., showed that the elec-trical signals traveled from the wounded cotyledon to distant unwounded leavesalong sieve-tubes and companion cells.
While it is clear that such an electrical action potential stimulates the activa- tion of the proteinase inhibitor genes in planta, the mechanisms that translatethis action potential into a chemical form that activates gene transcription havenot been fully elucidated. Recently, Herde et al., (1995) have shown that electri-cal current and localized heating induce the accumulation of ABA and jasmonatein wild type plants to levels that approach that of wounding. They also demon-strate that ABA deficient plants are able to synthesize jasmonate in response toheat, but not in response to wounding. While the mechanism of electrical signaltransduction is unknown, there have been several ion channels identified in plants(Maathuis and Sanders, 1995; Lurin et al., 1996) that could possibly participatein this process. Additionally, one of the inhibitors of wound-inducible gene ex-pression, acetylsalicylic acid, is known to disrupt H+/K+ transporters at theplasma membrane (Glass and Dunlop, 1974). Also an induced oxidative stresshas been shown to be the result of electrical pulses in maize plants (Sabri et al.,1996). It is also not clear whether the electrical stimulation of proteinase inhibi-tor gene induction is capable of inducing the wide a variety of genes that wound-ing induces.
One of the most intriguing recent findings in the area of plant biochemistry is thefinding that polypeptide signals may function in activation of plant defense genessuch as polypeptides activate defenses in animal cells (Bergey et al., 1996). Thesestudies were initiated by the original finding that a polypeptide from tomato leavesat very low concentrations was capable of initiating the signal transduction cas-cade leading to the expression of proteinase inhibitor genes in the absence of awound (Pearce et al., 1991). A synthetic polypeptide identical to the one purifiedfrom plants was also active in proteinase inhibitor gene induction. Further thissynthetic polypeptide was readily mobile in the phloem, as opposed to oligosac-charide signals (Baydoun and Fry, 1985).
The cDNA and gene encoding the signaling molecule, systemin, have been isolated and characterized (McGurl et al., 1992; McGurl and Ryan, 1992). Thesignaling molecule, systemin, is synthesized from a 200 amino acid pro-proteintermed prosystemin that is encoded in 11 exons. The mRNA is found throughoutthe tomato plants with the exception of the roots. Its expression was also wound-inducible in leaves indicating that its expression provides a self-amplification ofthe wound signal.
Systemin must be proteolytically processed to release the active systemin peptide. Recently, Gu et al., (1996) reported on the wound induction of a leucineaminopeptidase that accumulates in tomato leaves. These authors speculate thatthis amino peptidase activity may be important for plant-defense response possi-bly by processing of prosystemin to systemin.
A correlation of the activity of the systemin polypeptide with its structure has been examined (Pearce et al., 1993). Alanine scanning mutations revealedtwo regions required for activity: the first at Pro13 and the other at Thr17 nearthe carboxyl terminus of the peptide. Modifications at or near the carboxyl termi-nus were especially effective in reducing the activity of the polypeptide althoughthese modified systemins could compete with the native systemin interactionswith its receptor.
Alteration of systemin expression has been examined in transgenic tomato plants. Plants transformed with an antisense copy of prosystemin cDNA showeda dramatic suppression of proteinase inhibitor expression in the leaves of thetransgenic plants (McGurl et al., 1992). An over expression of prosystemin cDNAin tomato plants resulted in a constitutive expression of proteinase inhibitor pro-teins in leaves (McGurl et al., 1994). These plants were still wound-inducible,expressing high levels of proteinase inhibitors both locally and systemically fol-lowing wounding. Systemin also is capable of inducing other plant defensiveproteins including polyphenol oxidase (Constabel et al., 1995), indicating thatsystemin has a role in signaling plant defensive genes other than proteinase in-hibitors. In this same study, these authors also grafted non-transformed, wildtype scions onto the transgenic root stock and demonstrated elevated levels ofproteinase inhibitors in the non-transformed scions. These studies demonstrated that a signal could be transmitted from root stock transformed with theprosystemin cDNA through a graft junction to non-transformed leaves in the ab-sence of wounding.
To further investigate this systemic mobility of the systemin polypeptide, Narvaez-Vasquez et al., (1994) have used p-chloromecuribenzene sulfonic acid(PCMBS), an inhibitor of active apoplastic phloem loading. PCMBS was shownto be a powerful inhibitor of wound-induced and systemin-induced activation ofproteinase inhibitor synthesis tomato leaves. When placed on fresh wounds,PCMBS severely inhibited systemic induction of proteinase inhibitors, in boththe presence and absence of exogenous systemin. This process could be reversedby addition of various sulfhydryl compounds.
Localized interactions
Once the long distance systemic signal reaches its local site of action, that signal(whether electrical or chemical) must be transduced to the nucleus of the cellwhere gene transcription occurs. Electrical signals are known to open ion chan-nels in cells that could lead to a transducing chemical signal; but, the involve-ment of such ion channels have not been demonstrated with any of the chemicalsignals known to induce wound inducible genes. Typically, chemical signals in-teract with a cell surface receptor that then transmits chemical energy across themembrane to the cytoplasm.
Because of the variety and chemical diversity of the signals that are known to activate wound-inducible genes [polyanionic, plant cell wall fragments, (Bishopet al., 1981, 1984); polycationic, fungal cell wall fragments (Walker-Simmons andRyan, 1984); and the polypeptide, systemin (Pearce et al., 1991)] there should benumerous cell surface receptors. However to date, no cell surface receptor hasbeen identified. There are; however, intriguing findings that imply the existenceof such receptors. For example, elicitation of Eschscholtzia cell cultures (Blechertet al., 1995) or tomato cells (Felix et al., 1993) leads to a rapid alkalinization ofthe growth medium, possibly implying the involvement of membrane transportor ion movement. This alkalinization of the medium occurred prior to jasmonateformation and inhibition of this alkalinization process by the protein kinase in-hibitor staurosporine also inhibited jasmonate formation (Blechert et al., 1995).
In addition, the interaction of oligosaccharide elicitors with cells leads to sev- eral alterations in the plasma membrane. It is known that wounded plant cellshave increased membrane fragility (Walker-Simmons et al., 1984) perhaps due tophospholipase action. Further, elicitor treatment of cells lead to the phosphoryla-tion of various plant plasma membrane proteins in both potato and tomato (Farmeret al., 1989; Felix et al., 1993) In tomato both a 34 kDa and 29 kDa proteins werephosphorylated, but in potato only a 34 kDa phosphoprotein was detected. Incontrast to this, the elicitation with systemin resulted in the hyperphosphorylation of a 27 kDa protein. These studies indicate that protein kinases may play animportant role in the mechanism of signal transduction leading to defense geneexpression. Indeed, Bögre et al., (1997) have recently reported that the MMK4MAP kinase is activated within one minute of wounding. This kinase showsmaximal activity by 5 minutes after wounding and then activity dissappears by40 minutes after wounding. The specific role of this or other kinases in wound-induction is unknown, however, protein kinase inhibitors such as staurosporinecan block the synthesis of jasmonates which are intermediates in the signal trans-duction pathway (Blechert et al., 1995).
Recent evidence provided by Damman et al., (1997) demonstrate that an okadiac acid sensitive protein phosphatase is involved in jasmonate induced sig-nal transduction in leaves; however, jasmonate induced gene activation in rootsdoes not require this protein phosphatase to activate gene transcription in roots.
Thus, multiple pathways of signal transduction occur in different tissues.
As mentioned earlier, jasmonic acid and its methyl ester, methyl jasmonate, areactive in inducing the accumulation numerous wound-inducible genes in plants.
Northern analysis of methyl jasmonate-induced inhibitors I and II mRNAs intomato leaves, and of alfalfa trypsin inhibitor mRNA in alfalfa leaves, indicatedthat nascent inhibitor mRNAs were transcriptionally regulated in a manner similarto wounding (Farmer and Ryan, 1990). Further, this induction was systemic(Farmer et al., 1992).
After jasmonates were identified as potential mediators of the wound-response, numerous investigators examined the levels of jasmonates in wounded plants.
Creelman et al., (1992) used isotopically labeled standards to demonstrate thatwounded soybean stems rapidly accumulated jasmonic acid and methyl jasmonate.
Albrect et al., (1993), used an ELISA to show that levels of jasmonic acid roseimmediately and transiently in leaves as a consequence of wounding. The rapid,but transient, synthesis of cis-jasmonic acid was demonstrated after insect attackand by microbial elicitor in plant suspension cultures (Blechert et al., 1995). Leafdamage in Nicotiana sylvestris rapidly causes the level of shoot jasmonic acidpools to rise rapidly (<0.5 hr). Root jasmonic acid pools also rise in response toleaf damage, but more slowly (<2 hrs). The levels of jasmonic acid remain el-evated for 24 hrs in shoots and 10 hrs in roots (Baldwin et al., 1994).
The pathways of jasmonic acid biosynthesis
The synthesis of jasmonic acid requires that starting products be liberated frommembrane phospholipids. Ryu and Wang, (1996) have demonstrated that phos-pholipase D is rapidly activated by wounding in the leaves of castor bean result- ing in an accumulation of phosphatidic acid and free choline throughout the leaf.
New synthesis of phospholipase D mRNA was not observed following a wound,but rather, the wound-activation of the phospholipase resulted from intracellulartranslocation of the protein from the cytosol to membranes. Conconi et al., (1996)have found that the levels of linolenic acid (18:3) and linoleic acid (18:2) increasedwithin 1 hour of a wound. Presumably this is due to phospholipase A1 or A2 activity; although induction of these activities following a wound has not beendemonstrated. After 1 hour, they found a 15-fold excess of 18:3 over that requiredto account for the levels of newly synthesized jasmonic acid.
The intracellular location of jasmonate biosynthesis is thought to be the chlo- roplast envelope membranes (Blée and Joyard, 1996). It is currently unclearwhether the free fatty acids are liberated from chloroplast phospholipids or fromother membranes and are transported to the chloroplast via lipid transfer pro-teins.
The conversion of free 18:3 fatty acids into jasmonic acid occurs in five steps through an oxidative pathway. The intermediates are termed oxylipins. Initially,lipoxygenase catalyzes the incorporation of molecular O2 into certain polyunsatu- rated fatty acids having a cis, cis 1,4-pentadiene system to form a fatty acid hy-droperoxide. Typically in plants, there are numerous lipoxygenases and only someisoforms of these enzymes are themselves wound-inducible (Royo et al., 1996).
Thus, like many of the wound-inducible target genes, those genes which partici-pate in the activation process are also wound-inducible. In addition, many ofthese lipoxygenases are induced by a variety of biochemical components such asfungal elicitor, plant and fungal cell wall oligosaccharides, and methyl jasmonate(Bohland et al., 1997). In Arabidopsis, the lipoxygenase involved in jasmonatebiosynthesis is LOX2 (Bell et al., 1995). Cosuppression of LOX2 in transgenicplants leads to reduced levels of jasmonate biosynthesis as well as reduced levelsof wound-inducible gene expression. The Arabidopsis lipoxygenase LOX2 that isinvolved in jasmonate biosynthesis is chloroplastic (Bell et al., 1995).
Following the formation of 13-hydroperoxylinolenic acid, the enzyme allene oxide synthase forms an epoxide intermediate termed allene oxide. The flax alleneoxide synthase contains a 58 amino acid chloroplast transit peptide (Harms et al.,1995). These same authors constitutively overexpressed the flax allene oxidesynthase cDNA in transgenic potato plants. This expression led to an increase inthe endogenous level of jasmonic acid within the plants. However, despite the factthat the transgenic plants had levels of jasmonates similar to those found innontransgenic wounded plants, the wound-inducible pin2 genes were not consti-tutively expressed in the leaves of these plants (Harms et al., 1995). The reasonfor this lack of expression is not clear, but perhaps compartmentalization of thesignaling factors is involved.
Following the formation of allene oxide, a cyclooxygenase acts to form 12-oxo- phosphodienoic acid (12-oxo-PDA). Originally the substrate for this enzymaticstep was thought to be the 13-hydroperoxylinolenic acid (Vick et al., 1980); but,Harms et al., (1995) indicate that allene oxide may be the substrate for the cy-clization. The ring double bond of the 12-oxo-PDA is then reduced by a NADP+utilizing enzyme to form 12-oxo-PMA. This is the rate limiting step of jasmonatebiosynthesis (Vick and Zimmerman, 1986). Utilization of NADP+ is consistentwith the localization of these enzymes in the chloroplast. Finally jasmonic acid issynthesized from the 12-oxo-PMA by three rounds of β-oxidation. It is not clear whether a novel fatty acid oxidase functions in the synthesis of jasmonic acid oreven whether Coenzyme A derivatives or acyl carrier proteins are involved.
It has also been proposed that a second oxylipin cascade exists in plants start- ing from linoleic acid via 15,16-dihydro-12-oxo-phytodienoic acid to 9,10-dihydrojasmonate (Blechert et al., 1995). Recently, the cDNA encoding alleneoxide synthase has also been isolated from Arabidopsis thaliana (Laudert et al.,1996). After expression of this enzyme in E. coli, the protein was enzymaticallyactive with substrates derived from either linolenic acid or linoleic acid, verifyingthat there are indeed duplicate pathways to the synthesis of jasmonic acid anddihydrojasmonic acid.
In addition, to the synthesis of jasmonates, a wide variety of other oxylipin products from n-hexenal to ketols to traumatic acid are also derived from thesesame intermediates (Avudiushko et al., 1995; Blée and Joyard, 1996). Whetherthese intermediates also have gene regulatory activity will require further ex-amination. It is known; however, that n-hexenal accumulates in the volatile head-gas of wounded plants and there has been speculation that this may be involvedin rejection of plants by insects (Röse et al., 1996).
Inhibitors of oxylipin metabolism
Numerous inhibitors of the expression of wound-inducible genes have been re-ported. By far the majority of these inhibitors support occur in the oxylipin path-way. Inhibitors of lipoxygenases that inhibit wound inducible gene expressioninclude phenidone (Farmer et al., 1994), SHAM and ZK139817 (Peña-Cortés etal., 1993). Propyl gallate and piroxicam (Peña-Cortés et al., 1993) and salicylicacid (Doherty et al., 1988; Peña-Cortez et al., 1993; Doares et al., 1995) are inhibi-tors of hydroperoxide dehydrase (cyclooxygenase). Numerous studies involvingsalicylic acid have demonstrated that this compound blocks activation of protein-ase inhibitor genes by electrical signals (Doherty et al., 1988), oligouronide induc-tion, systemin induction, and linolenate induction (Doares et al., 1995) as well astranscription of the genes encoding proteinase inhibitor II, cathepsin D inhibitor,and threonine deaminase (Peña-Cortés et al., 1993).
Metabolism of jasmonates
The synthesis of jasmonates is a relatively transient response. Usually, jasmonatelevels decline rapidly following the burst of synthesis (Albrect et al., 1993; Blechertet al., 1995; Conconi et al., 1996); yet many plant responses remain activated formany hours. In an attempt to explain this phenomenon, Krumm et al., (1995)have investigated the role of amino acid conjugation of jasmonates. These au-thors have prepared many jasmonate-amino acid conjugates. They have shownthat many of these amino acid conjugates are inactive, however conjugates ofleucine and isoleucine retain their activity. These authors speculate that theseactive conjugates may function in the long-term maintenance of jasmonate-medi-ated signaling in plants.
Of the four possible stereoisomers of jasmonic acid growth inhibitory activity was associated with both of the 1R stereoisomers, however there was no observeddifference between the inhibition of straight growth of oat coleoptiles indicatingthat there may be multiple receptors mediating jasmonate activities (Koda et al.,1992). Further, stereochemically-locked cis- and trans-7-methyl derivatives ofmethyl jasmonate have low biological activity suggesting that the introduction ofthe locking methyl group at position 7 considerably lowers affinity for thejasmonate receptor, presumably owing to a steric effect (Koda et al., 1995).
Mutant in jasmonic acid synthesis and action
An ethylmethanesulfonate mutant (jar1) of Arabidopsis thaliana has been iso-lated that showed decreased sensitivity to methyl jasmonate inhibition of rootelongation (Staswick et al., 1992). The jasmonate-inducibility of leaf proteinswas 4-fold less in the jar1 mutants than in the wild type Arabidopsis plants.
Signaling mutants have also been prepared in tomato (Lightner et al., 1993).
These mutants, JL1 and JL5, were blocked in the induction of proteinase inhibi-tor genes. These mutants were deficient in the systemic-induction of both Pro-teinase Inhibitor I and II; however, these mutants showed some localized induc-tion of proteinase inhibitors. These results were interpreted as suggesting thatmultiple signaling pathways (one systemic and another local existed in responseto wounding. Further, these mutants were fully responsive to the addition ofmethyl jasmonate, indicating that the lesion in these mutants was located some-where upstream of the final step in jasmonate biosynthesis. Recently, Howe etal., (1996) demonstrated that the JL5 mutant are affected in octadecanoid me-tabolism between the synthesis of hydroperoxylinolenic acid and 12-oxo-phytodienoic acid.
Other mutants have been selected using coronatine. Coronatine is a chloro- sis-inducing phytotoxin produced by several pathovars of Pseudomonas syringae.
In tomato, coronatine induces the accumulation of proteinase inhibitors (Palmerand Bender, 1995), but they are not protective against the Pseudomonas patho- gen. Treatment of Arabidopsis plants with coronatine leads to inhibited rootgrowth, anthocyanin accumulation and the induction of two proteins of 31 and 29kDa (Feys et al., 1994). Similar responses are induced in response to jasmonates.
Arabidopsis mutants have been isolated that are resistant to this phytotoxin (Feyset al., 1994) and these mutants are also insensitive to methyl jasmonate inhibi-tion of root growth. These coi1 mutants were all male sterile, producing abnor-mal pollen and had reduced levels of the 31 kDa protein. These authors concludethat the coi1 protein controls jasmonate perception or response and also partici-pates in flower development.
Jasmonates affect transcription
After jasmonates are synthesized, it is unclear how the biological activity of thesecompounds are transmitted to the promoters of the various genes that they acti-vate. However, there is a recent report of a jasmonate binding protein that medi-ates the wound inducible regulation of transcription of the potato proteinase in-hibitor 2 gene (Gurevich et al., 1996). In this work, a fragment of the pin2 genewas isolated by PCR and used as an affinity sorbent. Nuclear proteins were boundand the sorbent was eluted with physiological concentrations of jasmonate. Fourproteins were isolated by this procedure. The characterization of these proteinswill require further studies.
Another factor that affects proteinase inhibitor expression downstream of jasmonates was discovered by Schaller et al., (1995). These authors found thatan inhibitor of some aminopeptidases, bestatin, was able to induce proteinaseinhibitor genes without affecting systemin, octadecanoids, or jasmonate. Fur-thermore, defense genes were induced by bestatin in the JL5 mutant tomato linethat has a defect in the octadecanoid pathway. Thus, bestatin appears to functionclose to the level of transcription of wound-inducible genes. These authors specu-late that a regulatory protease may be involved.
There is significant evidence that the initial stages of wound induction requirethe initial biosynthesis of abscisic acid prior to transcription of wound-induciblegenes (Peña-Cortés et al., 1989, 1991; Hildmann et al., 1992). These studies dem-onstrate that exogenous application of abscisic acid induces a systemic pattern ofProteinase Inhibitor II mRNA accumulation that is identical to mechanical wound-ing. Numerous other wound-inducible genes are known to also be induced byABA (see Table 1). These same authors also demonstrated that ABA-deficientplants do not respond to wounding unless ABA is supplied exogenously. There isalso an increase in ABA in the leaves of tomato, potato and tobacco plants follow- ing a wound (Sanchez-Serrano et al., 1991). In contrast to this, no increase inABA was observed in leaves incubated with jasmonic acid, suggesting thatjasmonates act after abscisic acid (Hildmann et al., 1992). Recently, Peña-Cortéset al., (1995) have shown that either electrical signals or systemin leads to anincrease in ABA which in turn leads to an increase in jasmonic acid which thenregulates gene transcription. According to this hypothesis, all jasmonate regu-lated genes should also be ABA regulated. Lee et al., (1996); however, have iden-tified four genes by differential display which are regulated by jasmonate but arenot regulated by ABA indicating that the signaling pathways for ABA andjasmonates function independently and not sequentially.
Specific roles for ABA have been proposed. ABA might lead to the activation of a lipoxygenase that generates hydroperoxides from free fatty acids within thecell (Peña-Cortés et al., 1995). Further evidence to support this hypothesis isprovided by Abián et al., (1991), who demonstrated alterations in oxylipin me-tabolism in maize embryos in response to ABA. It is also known that water-stressalso causes accumulation of ABA and activates a set of water-stress genes; how-ever it does not induce wound-inducible genes (Hildmann et al., 1992). Thusdifferent signal transduction mechanisms must regulate the ABA induction ofthese different sets of genes.
Mutants affecting ABA inductionBecause ABA has been identified as a factor involved in the activation of protein-ase inhibitor gene activation following wounding, there have been several inves-tigations examining wounding in ABA deficient plants (Peña-Cortés et al., 1989,1991). Several different ABA deficient plant lines have been used to evaluate theinvolvement of ABA in wound-inducible gene expression. The tomato mutantsused for these studies are flaca and sitiens and the potato mutant is droopy. Inall of these plants, proteinase inhibitor genes are not expressed unless abscisicacid is added. However, care should be taken in interpretations of the data de-rived from these hormone deficient plants, because they are often pleiotrophicmutations. For example the tomato mutant, flaca, is known to have elevatedlevels of IAA in addition to reduced levels of ABA (Tal and Imber, 1970). Further,there are numerous examples in the literature that exogenous application of ABAto plant tissues can cause alterations in endogenous levels of IAA within thosetissues (Chang and Jacobs, 1973; Anker, 1975; Wodzicki and Wodzicki, 1981; Terek,1982; Pilet and Rebeaud, 1983; Dunlap and Robacker, 1990).
As mentioned above, ethylene is synthesized following a wound and many wound-inducible genes are also responsive to ethylene. Recently, O’Donnell et al., (1996)have demonstrated that ethylene is absolutely required for wound-induction of the proteinase inhibitor genes of tomato. These authors use norbornadiene, whichis an inhibitor of ethylene synthesis (Sisler et al., 1990), and silver thiosulphate,which disrupts binding of ethylene to its receptor (Veen, 1987), to demonstratethat both jasmonic acid as well as ethylene are required for proteinase inhibitorgene expression. They propose that both ethylene and jasmonates are co-stimu-latory for the other hormone, that is, after wounding the synthesis of ethyleneinduces higher jasmonate levels, and endogenous jasmonates induce higher eth-ylene levels. In this way, a sufficient amount of these hormones accumulate toregulate the wound-process (O’Donnell et al., 1996).
Additional studies in support of this hypothesis come from the study of a tomato ethylene mutant, termed Never-ripe (NR), which have a partial loss ofethylene sensitivity (Yen et al., 1995). In these plants, the wound-induced accu-mulation of proteinase inhibitor transcripts is significantly delayed. Also,transgenic tomato plants expressing an antisense ACC oxidase do not accumu-late proteinase inhibitor transcripts in response to wounding. Thus, these stud-ies also suggest that ethylene is required for wound-inducible gene expression ofthe proteinase inhibitor genes.
Auxin has also been demonstrated to prevent expression of wound-inducible pro-teinase inhibitors (Kernan and Thornburg, 1989). This inhibition of expressionoccurs both in tissue cultured cells as well as in whole plants. It was specific forbiologically active auxins and occurred at near physiological IAA concentrations.
Auxin inhibition of gene expression has been demonstrated for a number of wound-inducible genes (see Table 1). Auxin also inhibits other chemical inducers. Auxinhas also been shown to strongly inhibited methyl jasmonate-induced wound-in-ducible gene expression in soybean suspension-cultured cells (DeWald et al., 1994)and the expression of β-glucanase in response to fungal elicitor in tobacco and soybean cells (Jouanneau et al., 1991).
Thornburg and Li (1991) have also demonstrated that IAA in bulk leaf tis- sues declines by two to three fold following a wound and that the kinetics ofIAA decline inversely correlate with the induction of wound-inducible gene ex-pression.
Other cellular machinery required for induction of wound-inducible genes has not been fully elucidated, however, recent work indicates that this is a richfield for study. It is known that small GTP-binding proteins can mediate cross-signaling between the wound- and pathogen-induced signal transduction path-ways (Sano et al., 1994; Sano and Ohashi, 1995). More recently, these authorsdemonstrated that these transgenic plants overexpressing this small GTP bind- ing protein can synthesize jasmonates more rapidly than control plants. Theyalso provide evidence based upon competition with 2-chloro-4-cyclohexylamino-6-ethylamino-s-triazine (a potent cytokinin antagonist) that cytokinins may be es-sential for accumulation of wound-inducible proteinase inhibitor transcripts (Sanoet al., 1996). Indeed it has been previously suggested that wounding enhancesendogenous cytokinin activity in cucumber (Crane and Ross, 1986).
From all of these studies, we can see the involvement of multiple long range signals, both chemical and electrical, multiple short range signals of plant andfungal origin, several signal transduction cascades involving GTP binding pro-teins, kinases, and phosphatases along with variations in multiple plant hormones,ethylene, cytokinins, auxin, and abscisic acid in addition to the biosynthesis ofjasmonates. All of these factors clearly do play a role in the transcriptional acti-vation of wound-inducible genes. It cannot be argued that these factors are coor-dinated in a vastly complex, well regulated network of responses leading to geneactivation. In spite of all that is currently known about the expression of thesegenes, there is a long way to go before we fully understand wound-inducible geneexpression in plants.
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