Hormone-induced Alterations in Plant Gene Expression

Biochem. Physiol. Pflanzen 185, 289-314 (1989) VEB Gustav Fischer Verlag Jena

BPP Review

Hormone-induced Alterations in Plant Gene Expression B. PARTHIER Institute of Plant Biochemistry, Academy of Sciences, Halle (Saale), G.D.R. Key Term Index: phytohormones, plant growth regulators, gene expression, inducible mRNA and protein syntheses

Summary Progress in knowledge about the actions of phytohormones in gene expression is reviewed with special reference to phytohormone-induced gene products (mRNA and respective proteins). The topic is focussed to selected developmental processes such as cell enlargement, seed germination, plastid development, leaf senescence, and fruit ripening. Plant growth substances (auxins, cytokinins, gibberellins, abscisic acid, ethylene) and some putative regulatory substances Uasmonates, brassinosteroids, polyamines) are shown to control (modulate) gene expression in these developmental systems in interacting ways; but in general it is unknown whether interactions take place at the level of gene expression or subsequent stages of control. The functions of induced gene products remain to be elucidated in many cases.

Contents 1. 2. 2.1. 2.2. 2.3. 2.4. 2.5. 2.6. 2.7. 3. 4.

Introduction: General Aspects . . . . . . . . . . . Phytohormone-specific Induced Expression of Genes Auxins . . . Cytokinins . Gibberellins. Ethylene . . Abscisic acid Jasmonates . Other putative plant growth regulators Concluding Remarks References . . . . . . . . . . . . .

289 291 291 292 294 296 298 301 303 304 305

1. Introduction: General Aspects

A small number of phytohormones or plant growth substances elicit a sheer multiplicity of responses in the differentiation and development programs of whole plants, organs, or cells (a selection is given in Table 1). Directly or indirectly, most of them are connected with changes in gene expression of the plant tissue. Our knowledge about hormone signal transduction in the Abbreviations: ABA, abscisic acid; ACC, l-aminocyclopropane-l-carboxylic acid; cDNA, complementary DNA; 2-D, two-dimensional; JA, jasmonic acid; JA-Me, methyljasmonate; JIP, jasmonateinduced proteins; kDa, kilo dalton; kb, kilo bases; poly (A), polyadenylated; T-DNA, transferred piece of tumor inducing (T j ) plasmid DNA into plant cells 19

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plant and the signal accessibility to the gene level remains stilI at the "black box" niveau, although progress can be noticed particularly due to the entrance of modem methods coming from genetic engineering . In the presence and in the near future scientists will be able to trace back many physiological processes to the molecular level and eventually learn to understand the way bioactive compounds in general and phytohormones in particular control these processes at the regulatory regions of the genes. We are at the advent of learning the control of gene expression by phytohormones (GOLDBERG 1986; PARTHIER 1986; BAULCOMBE 1987; KEY 1987). Several obstacles in the equally troublesome and exciting progress of acquiring respective knowledge are built up by nature itself: (i) the interdependent structural, functional and regulatory complexity monitoring the developmental processes; (ii) the existence of mystic "sensitivity" and "competence" stages of a given developmental system in order to respond to hormones (TREW Av AS 1982; WAREING 1986); (iii) by the endogenous levels of synergistic (protagonistic) and antagonistic actions of substances representing at least each two different types of plant growth regulators; but also (iv) by the tacit assumption that internal and externally applied plant hormones act in the same manner and result in the same responses. Especially the last point deserves attention, and the legions of physiological and biochemical data obtained with exogenously applied hormones must be car.efully checked for their value in supporting that hormones act as triggers or modulators (enhancers or repressors) in gene expression. The borderline is often narrow between "hormone" and "stress" responses of the plant tissue. A platform for these and related discussions is the increasing number of reports which demonstrate the occurrence of hormone-induced specific gene products. In both qualitative and quantitative aspects such alterations in the gene expression program of hormone-treated plant tissues resemble the genetic reprogramming often described as stress responses, which are caused by extreme temperatures, anaerobiosis, dessication, or salt (reviews: SACHS and Ho 1986; NOVER 1989; and refs. therein). Table 1. Selected plant developmental processes and their control by acting and counteracting phytohormones. System (cell, tissue) and process

1. Cell enlargement 2. Cell division and organogenesis 3. Embryogenesis and seed development 4. Seed germination (cereal aleurone layers) 5. Plastid development 6. Leaf senescence 7. Fruit ripening

Involved hormones protagonistic

antagonistic

auxin cytokinin (auxin) abscisic acid gibberellic' acid cytokinin abscisic acid, jasmonate ethylene

cytokinin, ethylene auxin (cytokinin) cytokinin abscisic acid abscisic acid cytokinin cytokinin

The present review will be restricted to the level of gene expression, i.e . the induction and! or accumulation of specific proteins or mRNAs, respectively , caused by externally applied plant hormones or related compounds in mainly the systems shown in Table 1. The review cannot comprehend the variety of biological responses and the hormone-specific background in terms of physiological and biochemical diversities, in spite of their interrelations with the

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expression of genes. In many cases the functions of the induced proteins are unknown, but others are well-defined as lectins or enzymes. Because of the scarcity of our knowledge about the role of hormone-induced gene products the review will be traditionally divided in chapters following the chemical nature of the various plant growth regulators.

2. Phytohormone-specific Induced Expression of Genes 2.1. Auxins (IAA, indole acetic acid; 2,4-D, 2,4-dichlorophenoxyacetic acid) The classic effect of auxins, at concentrations of:S; 10- 6 M, to cause elongation of isolated epicotyls, hypocotyls, and coleoptile sections is accompanied with newly synthesized proteins (reviews: THEOLOGIS 1986; GUILFOYLE 1986; KEY 1987; KEY et al. 1986). Several hypotheses are put forward to explain this auxin response, but only that of gene activation and expression will be taken into consideration in our review. Earlier reports described that auxin treatment rapidly and dramatically increase the synthesis of RNA, which was related to the stimulated activity of RNA polymerase I and ribosome accumulation in the hypocotyl tissue. More detailed studies showed that the kinetics of increase of mRNA for ribosomal proteins was parallel with the increase of rRNA synthesis (GANTT and KEY 1985). On the other hand, the complexity of total poly(A)RNA was not significantly affected by auxins. Nevertheless, several laboratories demonstrated rapid and selective changes of translatable mRNAs both in vivo and in vitro as a consequence of auxin application to sensitive tissues (THEOLOGIS et al. 1985; ZURFLUH and GUILFOYLE 1982). Resolution of the translation products on 2-D gels indicated that several abundant mRNAs changed, about equal numbers showing increase and decrease, respectively (BAULCOMBE and KEY 1980; THEOLOGIS and RAY 1982). Appearance of novel auxin-induced proteins were also observed in cell cultures of tobacco (MEYER et al. 1984; VAN DER ZAAL et al. 1987 a, b) or carrots (O'NEILL and SCOTT 1987)1 and in developing roots (DHINDSA et al. 1987). Several authors discriminated an "early responsive mRNA" versus mRNA which emerged at later stages of cell enlargement. Few polypeptides made in vitro were visualized even within 15 to 30 min after auxin addition to hypocotyls (HAGEN and GUILFOYLE 1985). This response in gene expression is close to the fastest morphological (elongation) response noted after 10 to 15 min (in Avena). Experiments were performed with cDNA clones from poly(A)RNAs that increased in their steady-state levels following auxin treatment of excised elongating soybean hypocotyl tissues. 2 (WALKER and KEY 1982), 3 (THEOLOGIS et al. 1985) and 4 cDNA clones (HAGEN et al. 1984), respectively, were isolated which responded in a manner expected for mRNA involved in the rate-limiting process of cell elongation. The RNAs hybridizing with the 2 cDNA sequences decreased rapidly during incubation of hypocotyl sections in the absence of auxin, and reappeared within 15 min after auxin addition (WALKER and KEY 1982). The observed changes induced by auxins seem to result from increased transcription rates as shown in nuclear run-on transcription experiments (HAGEN and GUILFOYLE 1985). This transcriptional control by auxins was measured after 5 min of hormone addition, and it was auxin-specific. Control of gene expression by auxins was suggested to be directly correlated with the physiological response, e.g. cell enlargement, a view supported by inhibitors of gene 19*

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expression (MCCLURE and GUILFOYLE 1987; THEOLOGIS et al. 1985). The substance specificity for the regulatory efficiency is most striking, since only active auxins such as IAA, 2,4-D, NAA, 2,4,5-T, but neither "unphysiological" indoles (indolealdehyde, tryptophan, cyclohexylacetic acid) nor other plant growth substances such as cytokinin, gibberellin or ethylen were reported to give positive signals (THEOLOGIS et al. 1985; HAGEN and GUILFOYLE 1985; WALKER et al. 1985; WRIGHT et al. 1987). A cascade response oflAA was assumed, in which translation products of the early responsive genes might playa regulatory role for late responsive genes. It was also suggested (KEY 1987) that the auxin-enhanced rate of cell elongation is the result of auxin-stimulated synthesis of specific "rate-limiting" mRNAs and proteins, respectively. Since cytokinins inhibit protein synthesis and auxin-induced cell elongation in excised soybean hypocotyls but do not affect the accumulation of the auxin-specific mRNAs, this phenomenon should be explained that either the auxin-specific proteins are not a part in the rate-limiting steps of cell elongation, or the inhibition of the latter by cytokinin occurs at posttranscriptional steps or even in the function of the auxin-induced proteins. Genomic clones (aux 28 and aux 22) that are homologous to the cDNA clones pJCWl and pJCW2 (WALKER and KEY 1982) have been isolated, and the genes as well as the cDNAs have been sequenced (AINLEY et al. 1988). Aux 28 and aux 22 encode hydrophilic proteins of26.8 and 21.5 kDa, respectively, with very similar hydropathic profiles. The genes are present as 1-2 copies per haploid genome and contain introns. Their coding sequences show high homology at the nucleic acid (77-80%) and protein levels (80-100 %), which together with other indications point to related members of a multigene family. Comparison of aux 28 and 22 sequences and the location of the TATA boxes in 5' flanking regions with that of the b 6 gene of Agrobacterium tumefaciens Ti plasmid shows an interesting identity (AINLEY et al. 1988). Although the collective data cited here provide definitive evidence for a rapid and specific action of auxin on the expression of few genes in tissues undergoing cell enlargement, we do not yet understand the mechanisms involved in the control of steady-state concentrations of auxininduced mRNAs or proteins. The functions of the protein products of auxin-regulated genes must be understood. More insight can be expected from studies of modified gene sequence in transgenic plants, whether either of these genes are directly or indirectly involved in the auxindependent cell- ortissue-specific growth processes. Response kinetics, particularly from run-on transcription studies (HAGEN and GUILFOYLE 1985; VAN DER ZAAL et al. 1987 b) encourage to speculate that these rapid effects may represent primary responses to auxins. 2.2. Cytokinins Together with auxins, the cytokinins belong to the essential hormones necessary for cell division and growth as well as organogenesis in plants. This earlier suggestion is verified by a natural gene transfer phenomenon, the Ti plasmid-induced crown gall tumor. It is the result of phytohormone overproduction due to the expression of two genes for auxin biosynthesis and one gene for cytokinin biosynthesis in the host cells transformed with the T-DNA of the Ti plasmid, which carries these genes (MORRIS 1986, for review). The system opens the possibility to demonstrate the actions of endogenously synthesized cytokinin (and auxin) at a molecular level, especially in gene expression (MEMELINK et al. 1987 a, b; KLEE et al. 1987). Therefore, this chapter will be divided into two parts: (i) effects of endogenous cytokinins in 292

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the T-DNA influenced gene expression in plants, (ii) changes in gene products caused by exogenously added cytokinins. To start with the latter, the drawback is as with any exogenously applied hormone or other chemical that uncontrolled variables exist in relation with uptake and transport of such compounds. Nevertheless, using this system a number of reports indicated cytokininmediated changes in the synthesis or maintenance of various proteins suggesting a definite role of cytokinins in gene expression. This action may be the background for a cytokininstimulated development of plastids and chloroplasts (review by P ARTHIER 1979). A number of nuclear-encoded mRNAs for chloroplast proteins was suggested to be controlled at the transcript level by cytokinin or by their non-physiological substitutes, furfurylaminopurine = kinetin and benzyl adenine (SEYER and LEscuRE 1984; LERBS et al. 1984; TEYSSENDIER DE LA SERVE et al. 1985 ; FLORES and TOBIN 1986; FUNCKES-SHIPPY and LEVINE 1985 ; LONGO et al. 1986). The cytokinin-mediated effect was specific for chloroplast proteins; other nuclear-encoded proteins were not affected (FUNCKES-SHIPPY and LEVINE 1985). Thus one may suggest that cytokinin-induced changes in the translatable mRNA populations (CHEN and LEISNER 1985; CHEN et al. 1987; LEGOCKA 1987) could be restricted to nuclear-encoded transcripts for chloroplast proteins, since the levels of abundant soluble polypeptides and mRNAs, respectively, do not change significantly (LERBS et al. 1988) . Evidence was provided that the cytokinin stimulation at the transcript level is due to a retardation of mRNA degradation and thus indicative for a post-transcriptional event (TOBIN and TURKALY 1982; FLORES and TOBIN 1986). This action of cytokinin is at least involved in the modulation of the levels for the small subunit of ribulose-l ,5-bisphosphate carboxylase and the light harvesting chlorophyll alb protein , if green Lemna plants were placed from light to darkness (FLORES and TOBIN 1988). Light, especially red light acting through phytochrome, independently of cytokinins stimulate mRNA accumulation markedly above its level in darkness (COLlJN et al. 1982; LERBS et al. 1984, 1988; BRACALE et aI. , 1988; FLORES and TOBIN 1988) suggesting a coaction of light and cytokinin in the photo morphogenesis of plastids (TONG et al. 1983), but the primary modes of actions of the two different effectors in gene expression might be quite diverse ones. Post-transcriptional (translational) control by cytokinins have been likewise described (TEPFER and FOSKET 1978) and suggested to be due to hormone-mediated sti'llulation of polyribosome formation (GWOZDZ and WOZNY 1983; OHYA and SUZUKI 1988), or modification of the secondary structure of poly(A)RNA, which leads to "unmasking" of the message (JACKOWSKI et al. 1987). Kinetin preferentially prevents the protein degradation part in the turnover, thus mimicking cytokinin-stimulated protein levels in comparison to water control (LAMATTINA et al. 1987). The well-known anti-senescence effect of the cytokinin (see also chapter 2.6) might be related with actions of this hormone in posttranslation processes and could well be epigenetic, e.g. supporting the stabilization of cell membranes or counteracting the synthesis of senescence-promoting metabolites (LESHEM 1984). The latter effect is certainly different from the suppression of gene expression (mRNA transcription) for certain proteins in auxin- and cytokinin-supplemented tobacco cell cultures. These proteins in question are ~-1 ,3-glucanase and chitinase (EICHHOLZ et al. 1983; MEINS et al. 1983; FELIX and MEINS 1985; SHINSHI et al. 1987). Using cDNA clones from ~-l ,3-glucanase mRNA, MOHNEN et al. (1985) showed that both auxin and cytokinin, in a BPP 185 (1989) 5/6

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combined action at the level of mRNA formation, block the production of this enzyme which is expressed in tobacco cell cultures in hormone-free medium. As mentioned above, an alternative model system for studies on plant morphogenesis at the molecular level are plant cells transformed by the T; plasmid. At present little is known about alterations in gene expression, i.e. mRNA steady-state levels and populations, in T;-plasmid transformed plant cells. When poly(A)RNA from untransformed potato was compared with that of T-DNA transformed plants, using 2Dseparated cell-free translation products as measure, BURRELL et al. (1986) found that the latter gave more high molecular weight products. However, the results were not clear enough in order to decide whether the observations could be directly referred to as a specific action of the cytokinin gene in the T-DNA (T-cyt gene), resulting in increased endogenous hormone concentration. Four.of five different cDNA clones corresponding to mRNA species which were increased in transgenic T-cyt gene tobacco shoots were found to encode pathogen defense-related proteins. Sequence comparison and cross-hybridization gave rise to identify the isolated clones as cDNA copies of chitinase, extensin, pathogen-related proteins, which are also known to be induced by pathogenic infection or wounding (CHEN and VARNER 1985). The mRNAs for these proteins accumulated in normal shoots in the presence of exogenous cytokinin (MEMELINK et al. 1987 a). This positive (increase) as well as negative control by cytokinin was extented to other more abundant mRNAs in T-DNA transformed tobacco shoots . Clear differences were found in the relative abundance of 18 among 240 translation products between transformed and normal tobacco RNA preparations translated in a wheat germ system, or using Northern blot techniques (MEMELINK et al. 1987b, 1988). According to the authors, the T-cyt directed phenotype is an obvious result of a stress situation, where the transformed cells have to tolerate an elevated concentration of T-cyt encoded cytokinin . Thus the increased stress-related mRNAs were translated to putative stress proteins varying in roots and shoots. These reports, however, do not conclusively prove whether the observed mRNA diversity is an immediate effect of cytokinin on the transcription process or mRNA stability, or whether they are secondary consequences of a cytokinin-induced stress situation. Interestingly, there is good evidence for the induction of chitinase mRNA accumulation by ethylene (BROGLIE et al. 1986). It is open for discussion whether the ethylen production is causally related with a cytokinin stress in a similar respect as C 2 H4 is formed in relation with pathogen infection (MAUCH et al. 1984), which in tum brings about the synthesis of pathogen-related proteins (V AN LOON 1985), cf. Chapter 2.4.

2.3. Gibberellins (GA3, gibberellic acid) Barley and wheat aleurone layers have provided model systems for the study of the regulation of gene expression by the two plant hormones, gibberellic acid (GA3) and abscisic acid (ABA). These layers playa crucial role in the mobilization of endosperm nutrients to support seedling development after the onset of seed germination. GA3 is synthesized in the germinating embryo and diffuses into the cells of the aleurone layers, where it triggers the synthesis and secretion into the endosperm of several hydrolytic enzymes, which hydrolyze storage macromolecules . Of these enzymes ex-amylase, together with ~-1 ,4-glucanase, proteases (thiol proteases homologous to cathepsins H and B), and nucleases, is the best294

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studied one (CHRISPEELS and VARNER 1967; JACOBSEN and VARNER 1967; BAULCOMBE et al. 1986; Ho et al. 1987). The effects of GA3 on enzyme synthesis are not uniform. For example, the time course of development of protease activity is similar to that for
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in the synthesis, stability and secretion of ex-amylase isoenzymes 1 and 2, but GA3 is required for the transcription of isoenzymes 3 and 4, whereas Ca 2 + may be involved in post-translational processes, e.g. secretion (JONES and JACOBSEN 1983) of these isoenzymes. Similarly, the secretion of the GA 3-induced lysophospholipase is increased in the presence of 50 mM Ca 2 + (LUNDGARD and BAISTED 1984). Nucleotide sequence analysis of GAr induced ex-amylase and thiol protease genes from aleurone layers has provided indications on homologous sequence elements in the 5' region of both genes, which are highly conserved and might be regarded as "enhancer" regions involved in the GA3 response (WHITTIER et al. 1987). The use of cloned cDNA or genomic DNA probes does not only contribute to evolutionary aspects and for the origin of these genes (BAULCOMBE 1987), it likewise provides a sensitive method of measuring gene expression kinetics in a number of isogene families during the development of the biological system. As many genes in higher plants, ex-amylase isozymes are encoded in multiple genes. They are located on chromosomes 1 and 6 in the barley genome (MUTHUKRISHNAN et al. 1984) and on chromosomes 6 and 7 in wheat (LAZARUS et al. 1985). Each locus contains multiple alleles, as shown by analysis of isoenzyme clones of nuclear DNA (HUTTLY and BAULCOMBE 1986), which are not equally expressed in the presence of GA3 (LAZARUS et al. 1985; DEIKMAN and JONES 1985). These findings may illustrate the complexity of the situation. Stimulated expression of multiple, unrelated genes could be mediated through several mechanisms acting variously on different genes (BAULCOMBE 1987). A promising way to prove or disprove this assumption would be the combination of the promoter regions of the respective genes with the same reporter gene, provided the assumed model of a GArcontrolled enhancer action can be verified experimentally. In conclusion, it seems highly probable that GA3 controls the synthesis of aleurone cell enzymes by enhancing the transcription of the respective mRNAs, whereas their steady-state concentrations depend on the action of ABA. As already mentioned for auxins, a better understanding of the role of the two hormones in the gene expression program for seed germination can be expected from progress in receptor research and in the interaction of putative trans-elements with cis-elements in putative cis-regulatory sequences of the GAr activated genes, of which at least two different types are obvious - varying in response to hormone concentration and duration of treatment - not regarded GArsuppressible genes (NOLAN and Ho 1988).

Ethylene, a simple chemical substance, was shown to cause dramatic effects in several plant physiological processes such as leaf and flower abscission, inhibition of stem growth, induction of enzymes in response to pathogenic infection, and stimulation of fruit ripening. Here we will concentrate to the latter phenomenon, since remarkable progress has been made recently in the evaluation of fruit ripening using avocado and tomato fruits as model systems. Tomato ripening is associated with a number of physiological and biochemical changes including degradation of chlorophyll, lycopene synthesis, cell wall solubilization and fruit softening. These processes are accompanied or at least partially triggered by an autocatalytic synthesis of endogenous ethylene, which can be induced by minor amounts of exogenous C 2 H4 gas. Thus it is reasonable to discriminate between ethylene as an inducer and ethylene as a 296

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mediator in the ripening process (MCGLASSON 1985). All the following data favor the view that ethylene induces the expression of genes coding for enzymes which implement fruit ripening; it became manifest by the appearance for ethylene-controlled specific mRNAs . Polygalacturonase (PG) is the major cell waH hydrolase responsible for fruit softening . The levels of this and other " ripening enzymes" are under the strict control of exogenous ethylene (ROBERTS and TUCKER 1985; GRIERSON 1985; LEsHEMet al. 1986, for reviews). Applied C 2H 4 stimulates the accumulation of PG mRNA and other ripening-related mRNAs in tomatoes (DELLA PENNA et al. 1986; GRIERSON et al. 1985; MAUNDERS et al. 1987), or cellulase mRNAs in avocado fruits (CHRISTOFFERSEN et al. 1984) and carrot roots (NICHOLS and LA TIES 1984). Total translatable RNA of ripening avocado does not change very much, since the new message comprise only a small fraction . This shows a sharp rise at 8 h after ethylene addition, together with a three-fold increase of the polysome content (TUCKER and LA TIES 1984). A cDNA library contained ethylene specific clones which were shown to be cellulase, since hybrid-selected in vitro translation products of the hybrid-released mRNA react with antibodies against cellulase. The enzymes were identical with multiple 53 kDa spots synthesized in vitro, and further evidence favored at least two gene families of 3 cellulase genes (LA TIES 1987). The enzymes are synthesized in vivo as membrane-associated precursor proteins of 56.5 kDa, but after processing the deglycosylated mature enzyme corresponds with 52.8 kDa. Other authors working on the ethylene-induced abscission of the petiolar pulvinus of Phaseolus (DEL CAMPILLO et al. 1988) suggested that acid and basic cellulases are derived from two different genes and that the acid enzyme should be converted to the abscission cellulase . Ethylene is required not only to initiate abscission and cellulase gene expression but also to maintain continued accumulation of the mRNA for this enzyme, a 51 kDa protein in Phaseolus vulgaris (TUCKER et al. 1988). The authors came to this conclusion by using the 595 nUfleotides long bean abscission cel1ulase cDNA clone pBACl as a hybridization probe as well as immunological methods . Experiments have shown that the endogenous ethylene concentration in tomatoes rises about 20 h before PG (48 kDa) synthesis can be detected, and this correlates with an increase in ACC synthase level, which is one of the two controlling enzymes in the ethylene biosynthesis pathway. Also the -accumulation of ripening-related PG mRNA seems to occur slowly; it appears highest at the 49th day, when it accounts for 2 .3 % of the total mRNA mass , corresponding with a 2,OOO-fold increase (DELLA PENNA et al. 1987) . It declines within 12 days, but its stability is remarkably high for weeks and can be detected even in the soft red fruits (GRIERSON 1985) . A more rapid turnover was observed with another ripening-related abundant protein of 35 kDa, which disappeared before PG was observed (SMITH et al. 1986). Cloning of ripening genes via poly(A)RNA, especially the PG-specific one, has been successfully done (DELLA PENNA et al. 1986; LINCOLN et al. 1987); and both cDNA and genomic clones encoding the PG gene of tomato has been mapped, sequenced and expressed in transgenic plants (GRIERSON et al. 1986; BIRD et al. 1988). The PG gene covers 7 kb and is interrupted by 8 intervening sequences. The 5' flanking region of 1.4 kb contains putative TAT A and CAAT boxes . In transgenic plants the PG promoter - CAT gene fusion product is expressed in ripe tomato fruits only (BIRD et al. 1988). - Another ethylene-responsive gene, E8, has been also cloned and expressed in transgenic tomato plants' (DEIKMAN and FISCHER BPP 185 (1989) 5/6

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1988). The authors were able to identify a DNA-binding protein factor that specifically interact with the 5' -flanking region of the E 8 gene. This factor is low in unripe tomato but increases during fruit ripening . Exposure of unripe tomato fruits to exogenously ethyl en has been shown to increase both in the level of specific mRNAs and in the transcription rate of specific ethylene-inducible genes (E4 , E8, E 17, J 49; they code for respective proteins of unknown functions). They were expressed during ripening only (LINCOLN et al. 1987; LINCOLN and FISCHER 1988 a, b). In a nonripening tomato mutant rin (ripening inhibitor), which is unable to increase the rate of endogenous ethylene formation during fruit development, the mRNA levels and transcription rates of the above-mentioned clonedgenes differ in any case and vary from total suppression to levels and rates unaffected by the mutation (LINCOLN and FISCHER 1988 b). However, if exposed to exogenous ethylene, the mRNAs for all four genes accumulate to similar levels both in wild-type and rin mutant fruits. It shows that the endogenous level of the hormone as well as the sensitivity of the fruit cells play an important role in the regulation of gene expression during the ripening process . Based on the progress in our knowledge on fruit ripening one is tempting to consider this developmental process simply as a result of a redirection of gene expression in response to ethylene. This is certainly only the beginning of the whole story . One intriguing point is e.g . how ethylene initiates the increase in ACC synthase activity , which plays a key role in endogenous ethylene synthesis . Likewise, unripe fruit cells are obviously not yet competent for the ethylene signal or its transduction at the molecular level. This raises the problem of ethylene receptors. Similarities in the responses of plant cells to ethylene and fungal infection or elicitors point to the stress problems in which hormones might be involved (cf. Chapters 2.2, 2.5 and 2.6) . Exogenously applied ethylene caused an increase of chitinase and ~-1 ,3-glucanase in un infected pea pods, similar to the effects fungal elicitors (BOLLER et al. 1983; MAUCH et al. 1984; BROGLIE et al. 1986, FELIX and MEINS 1987) or auxin and cytokinin deficiency in tobacco cell cultures (MOHNEN et al . 1985; FELIX and MEINS 1986). There are indications that different signals (hormones, elicitors) may act independently and separately (BOLLER et al. 1983), but the regulation process is coordinated for the two induced enzymes , chitinase and /3-1 ,3-glucanase (V 6GELI et al. 1988). - The effect of ethylene on two other plant defense response genes, that for phenylalanine ammonium lyase and a hydroxyproline-rich glycoprotein, point in the same direction . Northern blot analysis of RNA from C 2 H4 -treated carrot roots revealed a marked increase in the levels of the mRNA species for the two enzymes. Likewise, chimeric gene constructs with each one of these genes have been expressed in transgenic tobacco plants (ECKER and DAVIS 1987).

2.5. Abscisic acid (ABA, (+ )-abscisic acid = natural compound, (±)-abscisic acid synthetic; both enantiomers are equally active) ABA action is involved in several physiological and developmental processes, e.g . dessication as part of developmental programs such as seed maturation and germination, water and salt stresses, drought and cold tolerance (reviews: WALTON 1980; DAVIES 1987; RHODES 1987; ZEELVAART and CREELMAN 1988), and senescence (THIMANN 1980). Intensively studied systems are those of embryogenesis and seed maturation in different species. 298

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It is generally assumed that dessication as part of the developmental program of the seed

irreversibly terminates the maturation period and, after a period of metabolic arrest, redirects the developmental program towards expression of genes necessary for germination and seedling growth. Thus embryogenesis and seed maturation on one hand and germination on the other seems to be controlled by at least two interdependent factors: low level of water and high concentrations of ABA (FINKELSTEIN et al. 1985, 1987; FISCHER et al. 1987). ABA accumulates during early embryogenesis and declines again before dessication. It prevents germination but promotes maturation and the expression of storage proteins. - ABA synthesized in the ovule is transported into the embryo, where it turns off the translation of mRNAs specific for germination, i.e. usually hydrolytic enzymes necessary for the substrate supply of the growing embryo. In this connection ABA also prevents precocious germination in many seeds (FINKELSTEIN et al. 1985): If immature embryos of Brassica are excised from the seeds and cultured in vitro in a hormone-free medium precocious germination is observed, but it is prevented after exogenous ABA application. Further evidence for the regulatory role of ABA is provided by the observation of vivipary in ABA-insensitive mutants, by the addition of ABA inhibitors, and by the fact that high concentration of osmotica in the culture medium substitutes the effect of exogenous ABA, because it produces water deficiency (FINKELSTEIN et al. 1987). Changes of major seed storage proteins can be used as a marker of ABA-responsive processes in seeds, e.g. cruciferin and napin in Brassica, (FINKELSTEIN 1985, 1987), vicilin and legumin in Vicia faba (BARRATT 1986), ~-conglycinin in soybean (BRAY and BEACHY 1985; EISENBERG and MASCARENHAS 1985; ROSENBERG and RINNE 1988), late embryogenesis abundant (lea) proteins in cotton (GALAU et al. 1986; HUGHES and GALAU 1987; BAKER et al. 1988), or several storage proteins sedimenting as a 13S complex from mustard seeds (FISCHER et al. 1987). All of them seem to be products of larger gene families. Using storage protein cDNAs as hybridization probes, the steady-state levels of the storage-protein RNAs were found to be variably controlled by external ABA. For instance, the hormone transiently enhances the initially low level of cruciferin mRNA but maintains the already high level of napin mRNA (FINKELSTEIN et al. 1985). In Brassica, ABA responses are antagonized by exogenous cytokinin. As mentioned above, high osmotic potentials ("stress" concentration of 12.5 % sorbitol) can substitute for 10 flM ABA and stimulate storage protein synthesis. However, there is a difference: While ABA is effective in maintaining embryonic gene expression only in the predessication stage (embryos younger than 40 days after anthesis), the sorbitol effect is observed at all developmental stages tested (FINKELSTEIN et al. 1987). The authors' regard the synergistic action of the two different effectors as being consistent with the hypothesis that ABA acts via restricted water uptake, which affects gene expression in some unknown, developmentally related manner. For Sinapis embryos, FISCHER et al. (1987) assume that "both ABA and osmotic stress elicit maturation development independently of each other", i.e. each of them could maintain the water content of the embryo cells below a critical threshold necessary to prevent germination. Novel ABA-induced polypeptides were likewise observed in cereal seeds during embryogeriesis (WILLIAMSON et al. 1985; LIN and Ho 1986; SANCHEZ-MARTINEZ et al. 1986; MUNDY and CHUA 1988; GOMEZ et al. 1988; WILLIAMSON and QUATRANO 1988). In addition to the inhibitory action of the hormone in the synthesis of several abundant GArinduced BPP 185 (1989) 5/6

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enzymes such as
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molecular level. In addition to the results described in the preceding paragraphs, related papers add further data to the implication that reduced cell turgor leads to changes in the population of translatable RNA, i.e. that several poly(A)RNAs are rapidly induced when excised pea shoots are wilted (GUERRERO and MULLET 1988). Increased endogenous ABA levels following experimental desiccation (WALTON 1980; CORNISH and ZEEV AART 1984; HUBICK et al. 1986; LOVEYS and ROBINSON 1987) result in both increased and decreased relative amounts of in vitro translated polypeptides in developing barley embryos (BARTELS et al. 1988) and in soybean hypocotyls (BENSEN et al. 1988). On the other hand, there are results providing evidence by hybridization of wheat-germ cloned cDNA probes that dessication does not affect the synthesis of any ABA-induced gene products (WILLIAMSON and QUA TRANO 1988); but this may be referred as to the mentioned ABA effects dependent on the developmental stage of the embryo or seed. Vsing the ABA-deficient tomato mutant, fiacca, which does not synthesize ABA in response to drought stress, it was possible to distinguish between polypeptides induced directly by altered water contents from those induced in response to elevated ABA levels (BRAY 1988). The findings support the hypothesis that many of drought stress-related mRNAs and polypeptides, respectively, are regulated by altered ABA concentrations. Taken together, most of these data on gene expression modulated by ABA do not further support the earlier assumption of two clear-cut effects of this hormone: control of gene expression in organ development versus role as protectant as stress-metabolite against dessication (drought, salt, chilling or freezing) stresses (MOHAPATRA et al. 1988). Since all of the physiological strains are accompanied by the de novo synthesis of more or less specific proteins, which can be likewise induced by exogenously applied ABA, the central role ABA plays in a genetically controlled general stress response system should be emphasized (NOVER 1989).

2.6. lasmonates (JA, (±) jasmonic acid; JA-Me, (±) jasmonic acid methylester) Jasmonates are cyclopentanone compounds. JA-Me was isolated for the first time from the essential oils of lasminum (DEMOLE et al. 1962) and Tunesian rosemary (CRABALONA 1967) as well of Artemisia (VEDA and KATO 1980). Lateron jasmonates were found to occur ubiquitously in higher plants (YAMANE et al. 1981; MEYER et al. 1984). The occurrence of the physiologically active compounds, (- )-jasmonic acid and (+ )-7-isojasmonic acid, and their methylesters (DATHE et al. 1981; MIERSCH et al. 1986), together with observations on various stimulatory and inhibitory responses in plants (SEMBDNER and KLOSE 1985) were taken as indications for a new class of putative plant growth regulators (VEDA and KATO 1980; MEYER et al. 1984), which most remarkably promote senescence in leaf tissues (VEDA and KATO 1982; VEDA et al. 1981; SATLER and THIMANN 1981; WEIDHASE et al. 1987 a; reviews: PARTHIER 1988, 1989). Typical senescence symptoms such as loss of chlorophylls, increase in respiration, lowering of photosynthesis, and breakdown of ribulose-l ,5-bisphosphate carboxylase/oxygenase were seriously affected by JA-Me (WEIDHASE et al. 1987 a; POPOV A et al. 1988; POPOVA and VAKLINOVA 1988). The effects of jasmonates show similarity to ABA action not only in the promotion of leaf senescence, but also in the induction and accumulation of several abundant protein classes in barley leaf segments (WEIDHASE et al. 1987b). The polypeptides induced by ABA-Me BPP

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and JA- Me are seemingly the same as indicated by immunological cross-reactivity and molecular masses (LEHMANN et al., unpublished). The most abundant jasmonate-induced proteins (HPs) of barley correspond with relative molecular masses (Mr) of 10-12,23,30,37, 66 and 110 kDa), but still more faint bands or spots could be visualized (WEIDHASE et al. 1987b; MUELLER-URI et al. 1988). The three major abundant classes HP23, HP37, HP66, which are immunologically unrelated with each other or with any other soluble barley protein (HERRMANN et al. 1989), consist of multimeric species, probably of isogenic origin. They are synthesized on cytoplasmic polyribosomes (WEIDHASE et al. 1987 b), but location of at least some of them in cell organelles (nuclei) is highly probable (unpublished results). Since JA-Me induces the accumulation of species-specific abundant proteins in many plant species (HERRMANN et al. 1989), this action of the jasmonates could be of general importance in the response of leaf cells. In addition, jasmonate-induced proteins of 39 and 31 kDa were observed also in soybean suspension cultures (ANDERSON 1988). Therefore, a key question concerns whether or notjasmonate induced proteins are directly related with leaf senescence. Cytokinins (benzyl adenine) are able to counteract the abovementioned senescence symptoms but cannot prevent HP occurrence (WEIDHASE et al. 1987 a, b). Labelling experiments show that in vivo, and in vitro using a cell-free wheat germ translation system in order to measure the steady-state level of respective mRNAs, HPs and HP mRNAs were preferentially if not exclusively synthesized in the treated leaf segments (MUELLER-URI et al. 1988). It is concluded that lA-Me action in leaf segments triggers two processes: a rapid induction of HP-specific mRNAs (positive transcription control), and a repression of translation of mRNAs for normally synthesized proteins, suggesting a negative translational control. Kinetic experiments clearly demonstrated HP gene expression prior to the appearance of above-mentioned senescence symptoms, but a causal relationship between HP accumulation and leaf senescence remains to be shown, for HP-like proteins were not detected in senescing barley leaves in situ (HERRMANN et al. 1989). It should be mentioned that "senescence-specific" gene products have been observed by in vitro translation of RNA prepared from isolated and thus senescing plant organs such as wheat leaves (WATANABE and IMASEKI 1982), pea epicotyl (SCHUSTER and DAVIES 1983), soybean cotyledons (SKADSEN and CHERRY 1983), oat leaves (MALIK 1987), Hibiscus petals (WOODSON and HANDA 1987), radish cotyledons (KAWAKAMI and WATANABE 1988). It is difficult to draw a connection between these observations with that of jasmonate-induced abundant proteins. The JA-Me induced reprogramming of gene expression appears similar to that of the heat shock response or responses caused by other stressors. However, HPs are neither related to HSPs nor do heat-shock and jasmonate treatments of barley leaf segments affect the synthesis of the respective proteins (MUELLER-URI et al. 1988), and wounding or salt stress (0.5 M NaCl) is unable to induce proteins which cross-react immunologically with HPs (unpublished results). Thus, in certain aspectsjasmonate action resembles that of ABA, but in other aspects, e.g. ABA mimicking salt stress or osmotic shock response (MUNDY and CHUBA 1988), the two substances differ from each other. The arguments whether jasmonates are to be considered as hormonal regulators or stress factors in leaf senescence have been extensively discussed recently (PARTHIER 1989). At present it is difficult to prefer this or that view because we do neither know the role of jasmonate in the senescence processes nor the primary sites of its action. Some observations point to cell membranes, which very soon after lA-Me treatment lose integrity and show a 302

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disordered ultrastructure. As a hypothesis, cell membrane constituents can be released and, acting as elicitors, induce the above-mentioned alterations in gene expression. Thus exogenous jasmonate must not be directly involved in signal transmission or gene expression chains for the final physiological responses, its trigger function becomes likewise plausible by physico-chemical or chemical interactions with biological membranes. In general terms, one can expect "JIP" formation or leaf senescence not only caused by ABA but also by other chemical substances of proper membrane interactions. Alternatively, if the speculative jasmonate-induced release of cell membrane constituents concerns polyunsaturated fatty acids (THOMAS 1986), a metabolic cascade turns on which uses linoleic or linolenic acids as substrates and finally results in the biosynthesis of endogenous jasmonic acid (VICK and ZIMMERMANN 1984; LESHEM 1987). 2.7. Other putative plant growth regulators a) Brassinosteroids Steroidal lactones of the generalized term brassinosteroids have been regarded as a new class of plant growth regulators, extracted from a great number of plant species (ADAM and MARQU ARDT 1986; MANDA v A 1988 for reviews). The multiplicity of the biological activities reported for exogenously applied compounds spans between stimulation of coleoptile and stem (hypocotyl, epicotyl) elongation (MEUDT 1987; and in this respect comparable with gibberellin and auxin responses), lamina inclination, cell enlargement in suspension cultures (SALA and SALA 1985; BELLINCAMPI and MORPURGO 1988), changes in membrane potentials, H+ extrusion and proton pump activity (DE MICHELIS and LADO 1986), increase in photosynthesis and enzymes of the carbohydrate metabolism, and for practical application: increase in crop yield and biomass produced by treated plants, i.e. increases in fresh and dry weights of leaves, shoots, or tubers (MANDA v A 1988, for refs.) - A synergistic effect of brassinosteroids and auxins are reported for ethylene and ACC production (SCHLAGNHAUFER et al. 1984; ARTEcA et al. 1988), but interactions with other plant growth regulators are less convincing. Little is known as yet about the effects of bras sino steroids in the synthesis or metabolism of nucleic acids and protein that would indicate involvement in gene expression. KALINICH et al. (1985, 1986) found increased levels of nucleic acids in treated bean epicotyls and suggested so far unproved - involvement in the transcription process by enhancement of RNA and DNA polymerase activities. Inhibitors of gene expression steps prevented the brassinosteroidinduced cell elongation and division steps as well as epicotyl growth and H+ extrusion (MANDA VA et al. 1987). An induction of the synthesis of specific proteins by brassinosteroids rather than an indiscriminate increase in overall protein synthesis was suggested (MANDA v A 1988). In this connection the appearance of several novel protein bands and stimulated amino acid incorporation was of interest, observed in heat-shocked (40°C) and control (23 0c) wheat leaves treated with low amounts (l0~8 M) of homobrassinolide (KULAEVA et al. 1989). The authors assume that the steroidal hormone changes gene expression and elevates the thermoresistance of the leaves under temperature stress conditions.

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b) Polyamines The plant growth regulator functions, particularly the antisenescence effect of diamines (putrescine, cadaverine) and still more the triamine spermidine and the tetraamine spermine have been a matter of discussion since more than 10 years (for reviews cf. ALTMAN et al. 1982; SLOCUM et al. 1984; SMITH 1985). Polyamines were found in all plants studied (but likewise in microorganisms), and their concentrations usually rise when growth rates are increased. Likewise, exogenously applied polyamines cause growth-stimulating effects combined with a higher nucleic acid and protein content in the treated tissues. Although stimulation of in vitro protein synthesis by polyamines is often noted, the inhibition of protein degradation may well contribute to a high protein level by inactivation of proteases via polyamine binding to the enzymes (KAUR-SAWHNEY et al. 1982). Senescence retardation was suggested to be related with an inhibition of ethylene biosynthesis by polyamines (APELBAUM et al. 1981; SUTTLE 1981), another aspect than that of repression of RN ase (KA UR-SA WHNEY and GALSTON 1979), which resembles, but is stronger than the anti senescence actions of cytokinin and cycloheximide. The role of polyamines in reproductive differentiation is also discussed, e.g. in the induction of floral buds in tobacco tissue culture, where labelled spermidine is specifically bound to a 18 kDa protein (APELBAUM et al. 1988). One should keep in mind that polyamines have been generally found to stabilize the intramolecular structure of nucleic acids and negatively charged plasma membranes by surface phospholipid binding. This mode of action cannot be excluded for an explanation in the anti senescence function of polyamines (ALTMAN et al. 1982). The latter effect points to a more general view of polyamine action in plant tissues under stress conditions. FLORES and GALSTON (1984) observed a rapid polyamine accumulation via activation of arginine decarboxylase in osmotically stressed cereal leaves. Salinity stress and ion imbalance, protoplast stabilization, wound effects and ethylene formation seem to be related with the metabolic involvement of polyamines (ALTMAN et al. 1982; SMITH 1985). However, polyamines, if at all deserve of being called plant growth substances, would not interact with gene expression in the direct way described for the above-mentioned phytohormones.

3. Concluding Remarks "Developmental control" is a very general term, which harbors the ignorance we feel in a complex field of interactions between structural, metabolic and genetic processes by a number of low-molecular weight chemical substances (signals). Phytohormones constitute only one group of such modulators, although a very potent one. This group is as little uniform in respect to the action spectrum at the molecular levels as it shows uniformity at the higher levels of plant cell or organ organization. The observed variability of effects seems to prevent an unifying concept, in addition to the lack of correlation between endogenous phytohormone contents and developmental events (W AREING 1986). On the one hand, the classic plant growth regulators such as auxins, gibberellins or ethylene are able to induce - or being more precisely, promote or stimulate - a set of specific proteins (enzymes). These are probably synthesized at low basal levels; its hormonemediated enhancement is a prerequisite for continuing the physiological (developmental) process. Other hormones (abscisic acid, cytokinins) counteract the effects of the hormones just mentioned in respective processes, but we do not really know whether they exert their

~

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antagonistic function at the same site in the gene expression chain, where the protagonistic hormone is supposed to act. In addition, these substances could be involved in the processes by a second mode of action beyond the genetic level. Indeed many results encourage us to question that the observed antagonistic effects take place in gene expression sensu stricto but rather belong to post-translational effects, e.g. protecting membrane structures as by polyamines. The question reflects, of course, the present status of unsufficient knowledge. On the other hand, certain plant growth regulators elicit "unspecific" gene products (proteins) similar to abundant polypeptides known as stress proteins. Substances such as ABA or jasmonates, if exogenously applied to plant tissues, provoke the synthesis of novel abundant proteins resembling the well-known stress proteins (NOVER 1989; SACHS and Ho 1986). Both compounds may be considered as stress factors or stress modulators (LANKS 1986) capable of enhancing or suppressing plant responses against unconvenient changes in the environment, e.g. extreme temperature, drought, pathogen invasion, etc. Under this view-point also cytokinins and ethylen as well as polyamines ,can be included in this type of plant growth regulators, independent of their actions in gene expression steps or elsewhere. Extrapolation of the results on stress modulating agents could abandon the terms "classic" and "putative" plant growth substances and would end up in a diffuse collection of bioactive chemicals. If we focus phytohormone actions at the molecular genetic level, several examples cited in this review (e.g. auxins, gibberellins, abscisins, ethylene) suggest direct implication in the transcription control of specific genes. It is vastly assumed, and in several cases experimentally confirmed that hormones, via binding to still unknown trans-acting elements (proteins), interact with cis-acting elements (consensus sequences, enhancers, silencers) in the regulatory regions of the gene(s) as a prerequisite for expression (GOLDBERG 1986; BAULCOMBE 1987). This assumption does not only fit in the general picture of regulated gene expression, it was manifold verified for the action of animal hormones (RoY and CLARK 1987). Thus the gate seems open for future understanding of the modes of phytohormone action and probably also for their mutual interactions in developmental processes. However, the present paucity of knowledge about phytohormone binding proteins, both membrane-bound receptors (KLAMBT 1987) and soluble trans-acting elements should reduce too euphoric expectations. JOE KEY'S statement (1987) "that 'elegant' molecular genetics will give way to 'trivial' biochemistry in order to make further progress" pinpoints the very problem. Nevertheless, the vision of V AN OVERBECK (1966) that the "site of action of phytohormones ... is close to the gene" comes close to the truth.

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Received March 20, 1989; accepted May 3, 1989 Author's address: Prof. Dr. B. PARTHIER, Institut flir Biochemie der Pflanzen, Akademie der Wissenschaften der DDR, Weinberg 3, Halle (Saale), DDR - 4050.

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