Plant Physiol. (1991) 96, 675-6790032-0889/91/96/0675/05/$01 .00/0

Received for publication October 1, 1990Accepted March 11, 1991

Review

Secreting Glandular Trichomes: More than Just Hairs

George J. Wagner

Plant Physiology/Biochemistry/Molecular Biology Program, Agronomy Department, University of Kentucky,Lexington, Kentucky 40546-0091

ABSTRACT

Secreting glandular plant trichome types which accumulatelarge quantities of metabolic products in the space between theirgland cell walls and cuticle permit the plant to amass secretionsin a compartment that is virtually outside the plant body. Thesestructures not only accumulate and store what are often phyto-toxic oils but they position these compounds as an apparent firstline of defense at the surface of the plant. Recent advances inmethods for isolation and study of trichome glands have allowedmore precise analysis of gland cell metabolism and enzymology.Isolation of mutants with altered trichome phenotypes providesnew systems for probing the genetic basis of trichome develop-ment. These advances and their continuation can pave the wayfor future attempts at modification of trichome secretion. Thebiochemical capability of glandular secreting trichomes and thepotential for its future manipulation to exploit this external storagecompartment is the focus of this review.

Most surfaces of most plants are said to be pubescent, orbearing of trichomes or hairs. The morphology of these struc-tures can vary greatly with tissue and species. Indeed, thebotanical literature is said to contain more than 300 descrip-tions (uniseriate, capitate-sessile, etc.) to characterize variousmorphological types (see Benhnke, 22). These characteristicshave often been used in plant classification. Functionally,trichomes may be simple hairs which deter herbivores, guidethe path of pollinators or affect photosynthesis, leaf temper-ature, or water loss through increased light reflectance as indesert species (see Kelsey et al., 22). Or, they may be morespecialized tissues (glandular secreting trichomes) whose prin-cipal function(s) may be to produce pest- or pollinator-inter-active chemicals which are stored or volatilized at the plantsurface. It has been suggested that in some desert species theprincipal role of glandular secreting trichomes is to producesuch high levels of exudate that it forms a continuous layeron the plant surface. This layer may increase light reflectanceand thereby reduce leaf temperature (4).

It is the glandular, merocrine, secreting trichome type whichoften produce and accumulate terpenoid oils that will be thefocus of this paper. Other secretary tissues occurring on or inplants including salt glands, salt hairs, nectary and slimeglands, resin ducts, and osmophores (often responsible forfragrances in flowers) will not be included in this discussion.Comprehensive reviews which consider various secretary tis-sues of plants are found in references 4, 6, 19, and 22. We

will argue here that glandular secreting trichomes are anattractive system for study and are now or will soon beamenable to modification using a recombinant DNA ap-proach. Useful modification might be genetic manipulationof an enzyme to alter the chemical nature of exudate for thepurpose ofenhancing disease resistance, enhancing attractive-ness to pollinators, or to expand the metabolism of secretarycells to include synthesis of compounds or intermediates notnormally formed. It is important to point out here that thepotential of secreting trichomes to accumulate exudate ishighly significant in certain plants where, under optimalconditions, secreted products can reach a level of 10 to 30%ofthe dry weight ofleaves (4, and Kelsey et al., 22). Glandulartrichome exudates usually contain terpenes and essential oils(4), lipophilic components not easily stored in large amountswithin the cell. Therefore, if it were desirable to manipulateplants to produce or overproduce a compound in this class ofbiochemicals, the secreting trichome system which amassessecretions outside of gland cells may be more amenable tooverproduction than one requiring intracellular storage.

This minireview will first consider some general aspects oftrichome biology with emphasis on recent work concerningthe molecular basis of trichome and root hair development.This will be followed by sections which consider our presentunderstanding ofwhich tissues form secretions, how structureand ultrastructure relate to the potential to amass secretions,and which metabolic pathways are known to occur in secre-tory cells. A brief"one physiologist's view" of aspects ofplant-insect, plant-microbe interactions will follow and the lastsection will consider some possibilities for future studies andmanipulation of trichome secretion.

GENERAL ASPECTS OF PLANT TRICHOMES

Esau (5) has defined trichomes as "epidermal appendagesof diverse form, structure and functions. ... represented byprotective, supporting, and glandular hairs, by scales, byvarious papillae, and by absorbing hairs of roots." This defi-nition suggests a close relationship between trichomes androot hairs. From this viewpoint, aerial trichomes and subter-ranean "trichomes" could be said to cover or nearly cover thesurfaces of most plants. However, recent results would suggestthat while trichomes and root hairs may resemble each otherin morphology, their genetic determinants may differ (seebelow). Both trichomes and root hairs develop as projectionsfrom protodermal cells. Glandular structures of trichomesarise from a series of anticlinal and periclinal divisions to

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form supporting auxiliary cells and glands as in the case ofCannabis (see Mahlberg et al., 22).Some recent work promises to shed light on the molecular

genetic basis of trichome development. Mutants ofArabidop-sis have been isolated in which phenotypic changes are limitedto trichomes (1 1, 18). The absence of trichomes in mutantsgl 1 and ttgl does not affect overall plant growth and devel-opment to the extent that this has been tested. It is probablethat these loci are the only ones associated with the loss oftrichomes in Arabidopsis because a number of independentlyisolated mutants failed to complement these two loci (18).Thus, these genes appear to be responsible for differentiationofprotodermal cells to form trichomes. Trichomeless mutantsof Arabdopsis form normal root hairs suggesting, as notedabove, that different genes control formation of trichomesand root hairs (C Somerville, personal communication). Note-worthy is the observation that trichomes are often the earliestrecognizable structures to appear during differentiation ofcultured tissue. Perhaps this reflects the linkage of trichome-determining genes and other genes involved in early devel-opment. The study ofthe structure and regulation oftrichomegenes, such as the recent work of Herman and Marks withArabidopsis (12), may serve to better define the genetic mech-anisms of differentiation in plants and perhaps make possiblealteration of trichome density to study the physiological rolesof trichomes in, for example, light reflectance. Trichomestructural and hairless mutants have been characterized at themorphological level in other plants, including tomato (21).Genes affecting the formation of root hairs were also re-

cently identified in Arabidopsis (23). Four classes of mutantsall resulting from single nuclear recessive mutations wereattributed to four different genes. One of these, RHD 1, ap-pears to be responsible for normal initiation of hairs while theothers are involved in normal elongation. Hairy root cultures(24) which often, but not always, proliferate adventitious hairsand Arabidopsis mutants should provide useful systems forstudying gene-level aspects of root hair development.Much of what we know about the tissue and cell level sites

and mechanisms of trichome secretion has come from cyto-chemical and ultrastructural studies (6). The recent develop-ment of a method for preparing protoplasts from root hairs(1) may facilitate characterization of enzymes and organellesof these cells. There is a great need for development ofmethods for preparing organelles from trichome secretarycells or protoplasts which could serve as a source of isolatedorganelles. Such preparations would be useful, for example,in studying the apparent intimate relationship between plas-tids and ER which appears to be so common in terpenesecreting glands (6). We note that we have been unsuccessfulthus far in attempts to prepare protoplasts from tobaccotrichome glands applying protocols used for easily proto-plasted or recalcitrant tissues. The difficulty may be the pres-ence of modified cell walls and wall encrustations which arecommon in secreting glands (see Peterson and Vermer, 22).

WHICH TRICHOME CELLS FORM SECRETIONS ANDWHAT IS THE EXTENT OF THEIR METABOLIC

INDEPENDENCE?The preceding discussion and much of the literature on

trichomes has assumed that glandular cells of glandular tri-

chomes produce secretions. The appearance of glands atopsupporting cells and the occurrence of exudate around glandcells has suggested to most observers that secretions are pro-duced in gland cells and not by other epidermal or subepider-mal cells. This notion has been supported in a number ofcases by cytochemical evidence showing accumulation oflypophilic materials within secreting gland cells (4, 6). How-ever, proof that gland cells form exudate was only showndirectly when quantities of highly purified glands preparedfrom tobacco (17) were shown to be capable of relativelyefficient, light-dependent diterpene and sucrose ester synthesisfrom as simple a precursor as carbonate (13). Neither epider-mal peels prepared from tissues brushed to remove glands(but not entire trichome stalks) nor pieces of subepidermaltissue synthesized these complex components while peelsbearing glands were biosynthetically competent. Croteau andcoworkers have recently isolated trichome glands from Men-tha. While these glands-which are more difficult to obtainthan glands of tobacco trichomes that have a longer stalk-show only limited potential for biosynthesis, they have beenexpertly exploited for isolation and localization of enzymesspecific to monoterpene synthesis (7, 8). The studies withmint provide strong, indirect evidence that trichome glandsof this plant synthesize and accumulate monoterpenes. Thus,there is now substantial evidence that monoterpenes andditerpenes (also sucrose esters) are produced within gland cellsof secreting trichomes.The finding that isolated secreting glands of tobacco can

convert radiolabel from carbonate to complex diterpenes andto both the sucrose and acyl moieties of sucrose esters suggeststhat in tobacco, photosynthetically competent gland cellsperhaps need only be supplied carbonate (13). Alternatively,sucrose or glucose may be supplied from subepidermis viahighly vacuolated, chloroplast-less stalk cells. In favor of theformer hypothesis is the finding that carbonate was a betterdonor of carbon to principal exudate constituents in glandcells of tobacco than were glucose or sucrose. Gaseous 14C02was incorporated by epidermal peels having intact glands butnot by detached glands. Studies using asymmetrically labeledsucrose ('4C-Glu-Fru) showed that both epidermal peels bear-ing secreting trichomes and isolated gland cell preparationsrandomized label before its incorporation into the sucrosemoiety of sucrose esters (13). Thus, at least the secreting glandcells of tobacco appear to be metabolically independent inthe light in producing principal exudate components if sup-plied carbonate. These cells contain numerous fully developedchloroplasts (20). Despite this compelling evidence for meta-bolic independence, we point out that sustained biosynthesisin isolated glands of tobacco has not been demonstrated.Further study is needed to determine if exudate formation isregulated by the supply of CO2 or sugar in tobacco andother systems. It has been suggested that in mint, availabil-ity of assimilate to cells and cellular compartmentation in-volved in biosynthesis may regulate the rate of monoterpenesynthesis (8).

IS EXUDATE ACCUMULATION CAPACITY RELATEDTO THE STRUCTURE OF SECRETING CELLS?

In the following discussion, potential for amassing highlevels of exudate is emphasized because this aspect may be

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important in selecting plant systems to modify for potentialcommercial exploitation oftrichome exudation or for efficientexperimentation to modify pest-interactive properties of ex-udate. Great diversity exists in the morphology of glandulartrichomes at the organ, cellular, and subcellular levels (6).This diversity occurs in plants which are lower-level accu-mulators (<2% of dry weight of leaves as exudate) and alsoin those which are high level accumulators (-5-30% dryweight of leaves). Many high level accumulators such ascertain species of Beyeria, Eromophilia, Lycopersicon, So-lanum, and Nicotiana appear to contain "bright green" chlo-roplasts (4) in secreting or auxiliary cells suggesting a possiblerelationship between their capacity to amass exudate and theirphotosynthetic capacity to fix carbon and/or to produce ATPand NADPH. However, at least one exception to this rule isfound in Newcastelia. But, glands of this plant contain a typeof plastid and also have exceptional ability to incorporateprecursors into terpenes with unusually high rates as com-pared to most other higher terpene and also monoterpeneproducers (4). Further study comparing high and lower levelsecreting plants is needed to determine ifgland photosyntheticpotential and capacity to secrete are related. Generally, high-level exudate accumulators produce di-, tri-, and sesquiter-penes as major products. Plants which principally form mon-oterpenes commonly amass lower levels of exudate but thegenerally higher volatility of these lower terpenes and theextent of their catabolism and reutilization may factor in theamount of product amassed (8). Volatilized secretions mayescape after damage of the cuticle enclosing the droplet or viapores in this structure (6). The diameter and size of glandsdoes not appear to be correlated with exudate accumulationcapacity (4).

Ultrastructural features which appear to be common interpene secreting glands (and also secreting resin duct epithe-lial cells [4]) are: extended smooth ER; leucoplasts with poorlydefined internal membranes, or normal or sometimes unusu-ally shaped but otherwise normal appearing chloroplasts; anassociation of ER and plastids; and the relative absence ofgolgi (4). Leucoplast structure appears to vary depending onwhether or not monoterpenes are produced (6). We note thatthe ultrastructure of trichome glands from the mutant, glan-dular, but nonsecreting tobacco T.I. 1406 is similar to that ofsecreting types except for the absence of normal chloroplasts(20). Interestingly, transfer of a single gene via plant breedingrestores secretion and normal chloroplasts in this mutant (20).Most evidence indicates that synthesis ofthe terpene precursorisopentenyl pyrophosphate occurs in the cytosol. This inter-mediate then appears to be utilized by plastids or plastid-ERaggregates to synthesize secreted products (8).

BIOSYNTHETIC PATHWAYS OF GLAND CELLS: WHATDO WE KNOW?

If we are to hope to manipulate trichome gland cells tomodify or extend their metabolic capabilities, we must defineand ascertain the limits of their metabolic potential. Lookingagain to the tobacco and mint systems, we may ask whichmetabolic pathways other than carbon fixation and isoprenoidsynthesis are functional in mature secreting gland cells. Per-haps in developing gland cells undergoing division and prolif-

eration most key metabolic pathways function. But as glandsmature and begin to secrete specific compounds, their metab-olism may be modified and become more specific. This issuggested from recent findings that short branched andstraight chain acyl acids of tobacco-exudate sucrose esters areproducts of modified branched-chain amino acid metabo-lism/catabolism (14). In mature gland cells, pathways forsynthesis of valine, leucine, and isoleucine appear to be di-verted to form CoA-activated acids for esterification in sucroseester formation. We have suggested that normal flow ofcarbon to amino acids is diverted somewhat in mature glandsdue to the lack of a sink for branched-chain amino acid (lackof protein synthesis) or a lack of transaminase to convertketoacid intermediates to amino acids (14, 15). Keto acidsactivated by ketoacid dehydrogenase are usually destined forcatabolism to recover carbon of branched-chain amino acidsas succinyl CoA, acetyl CoA, or acetoacetate. In gland cellsthis pathway may be blocked to allow use of CoA activatedacids for esterification to sucrose (14, 15). Recently, studiesof glucose ester synthesis in tomato tissue bearing trichomessupport the role ofbranched-chain amino acid metabolism inC4 and C5 acyl acid formation (26). In tomato, straight andbranched chain CI0, C1, and C12 acids are also formed andesterified in glucose esters. These are suggested to be derivedfrom fatty acid metabolism by addition of C2 units tobranched-chain, amino-acid-pathway-derived primers. Ka-neda ( 16) had shown earlier that short, branched-chain acidscan serve as primers for >C27 hydrocarbon synthesis in to-bacco (also Bacillus subtilis and Micrococcus lysodeikticus)and concluded that elongation involved either addition of C2units to primer acids or condensation of these with C16 or C18straight chain acids derived from fatty acid synthesis. Thus,mature gland cells of at least tomato may contain active fattyacid metabolism. However, at this time it is not clear if thismetabolism is modified to produce C10 to C12 acids instead ofthe usual >C16 products or if normal fatty acid metabolismcontributes normal long chain acids via condensation reac-tions and the products are subsequently shortened via ,B-oxidation after CoA activation. While it has not been directlydemonstrated that acyl acids or glucose esters of tomatoexudate are produced in trichome gland cells, results obtainedwith the tobacco system (14, 15) suggest that this is probablythe case.

Thus, evidence exists for pathways of carbon fixation, iso-prenoid, branched-chain amino acid, and fatty acid metabo-lism in secreting gland cells. Mitochondrial function to pro-duce ATP and NADH is needed based on the energy demandsof isoprenoid metabolism alone. Gland cells of tobacco andother high-level accumulators appear to have a normal com-plement of mitochondria (4, 20). Clearly, further study isneeded to define the metabolic capability of secreting glandcells but one can already begin to consider modification ofisoprenoid metabolism, reactions which modify terpene skel-etons, and branched-chain amino acid metabolism (in sugarester producers) to alter exudate chemistry.

Recent studies from Croteau's laboratory on localization ofenzymes involved in monoterpene biosynthesis have usedgland isolation and histochemical techniques to show that(-)-limonene cyclase and (-)-limonene hydroxylase, key en-zymes in the synthesis of (-)-carvone in spearmint, are local-

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ized exclusively in gland cells (8). A number of other mono-terpene biosynthetic enzymes have been shown to be enrichedin isolated gland preparations including several highly sub-strate-specific terpene cyclases (7).The best evidence for metabolic turnover of glandular

secretions comes from the work of Croteau and colleaguesusing the mint system (2). Two types ofmonoterpene turnoverhave been distinguished. In immature tissue diurnal fluctua-tion thought to be synchronized with photosynthesis is ob-served, but synthesis exceeds loss resulting in accumulation.Late in development a net decrease in monoterpenes is ob-served. In Mentha piperita a major secreted component, 1-menthone, is converted to 1-menthol and the water solubleneomenthol-glucoside which is transported out of the gland.The extent ofhigher terpene turnover in glands which producethese compounds has not been studied.Low incorporation of radiolabeled carbon donors has long

plagued attempts to study metabolism of trichome exudatecomponents. This has been attributed to poor access of ex-ogenously supplied precursors to glands and compartmenta-tion within the gland itself (see Croteau and Johnson, 22).Slow turnover numbers for enzymes of the terpenoid pathwaymight also be a factor. It is also possible that new synthesis isinhibited by existing accumulated exudate. In this regard, aninteresting observation was made in recent studies of glucoseester metabolism in tomato. Young leaves were briefly washedwith 100% ethanol prior to labeling to remove all but 10 to20% of exudate (26). While comparison of incorporation ofdonors in washed versus unwashed leaves was not reported,washing presumably did not inhibit biosynthetic capacity ofgland cells. Levels of incorporation of '4C-valine were notreported but incorporation of stable isotopes used was said tobe substantially improved by the washing procedure. Perhapspartial removal of preexisting exudate can increase incorpo-ration in tracer experiments in other systems and therebyfacilitate further characterization of gland metabolism.

TRICHOME EXUDATE AND PLANT-INSECT, -MICROBEINTERACTIONS

My purpose here is not to attempt to survey the vastliterature on plant-insect, plant-microbe interactions relatedto trichome secretions. I only attempt to provide a very briefdescription of "one plant physiologist's view" of this veryimportant aspect of trichome biology. (Some detailed reviewson the subject are found in references 3, 22, 25 and referencestherein.)

Interactions between terpenoids and insects are complex.Growth and development of many insects is regulated byterpene-containing substances and terpenoids can attract, re-pel, cause alarm, or initiate defense reactions in differentinsects (see Kelsey et al, 22). Many insects are dependent onplants as a source of sterols since they are incapable ofsynthesizing the sterol nucleus (4). While the effects of expo-sure to terpene compounds on insects can range from attrac-tant to toxin, specific responses can depend on insect species,concentration, other chemicals present, and on the mode ofcontact. Extensive studies have been made in a number ofsystems to evaluate the influence ofspecific exudate chemicalson specific insects. These have involved comparisons of insect

behavior and exudate composition in natural and experimen-tal populations of plants, studies comparing insect responsewith intact tissue versus tissue with exudate removed or tissuewith exudate removed and specific purified componentsadded back. Injection, topical application, or inclusion ofexudate components in artificial diets have been used asapproaches to study effects of exudate components on rearedinsects. Despite complexities involved in studying systemscontaining more than one organism, many tissues, etc., cleareffects of exudate components have been established fromstudies of potato (25), tobacco (3), tomato (9), and severalother species. For example, Goffreda et al. (9) recently com-pared potato aphid behavior on the wild tomato Lycopersiconpennellii, domesticated Lycopersicon esculentum, and an F.hybrid of these. Aphid feeding behavior on L. pennelli andthe hybrid (possessed type IV, sugar ester-producingtrichomesof L. pennellii) was characterized by a delay in initiation offeeding and in reduced feeding time. Removal of exudatefrom L. pennellii resulted in increased feeding and its appli-cation to L. esculentum decreased feeding. In this example,behavior of this insect appears to be primarily dependent onchemistry of exudate of one trichome type. In contrast, insectavoidance/deterence in potato appears to result from differentphysiochemical and chemical properties oftwo different typesof trichomes (25). Exudate terpenes, essential oils, and sugaresters are often sticky in nature and have long been known toentrap insect pests. For this reason, exudates having bothsticky properties and insect-interactive chemicals are said tocomprise a physiochemical defense mechanism (25). It is notsurprising that insect resistance mechanisms involving tri-chomes are complex and highly variable.

In a different approach to understanding the basis of insectresistance, Goffreda et al. (10) recently used graft chimeras todetermine the contribution of various leaf surface tissues toinsect resistance. They prepared periclinal chimeras of aphid-susceptible L. esculentum and aphid-resistant L. pennelli todetermine if resistance required interaction of trichome-bear-ing epidermal with subepidermal tissues or was solely depend-ent on the presence of epidermal glucose ester secreting tri-chomes as had been concluded earlier. Though aphids feedby inserting their proboscis into subepidermal tissue, it wasfound that epidermal features alone accounted for aphidresistance and resistance was correlated with the occurrenceof trichome-secreted glucose esters.The antibiotic and antimicrobial potential of essential oils

was recognized early and plant extracts are thought to havebeen the first preservatives used by man. Mono-, sesqui-, di-,and triterpenes, sesquiterpene lactones, flavones, and isofla-vones have been shown to have antibiotic or antimicrobialactivity toward certain organisms. It is probable that most ofthese compounds are products of glands but some may beproduced by epidermal cells and then secreted through thecuticle as with surface waxes. In several cases studied, theresponse ofmicroorganisms to exudate compounds have beencompared in vivo and on plant tissue as in the case of thesesquiterpene lactone parthenolide from Chrysanthemumparthenium (see Kelsey et al., 22). The possibility that tri-chome exudate components may function as plant growthregulators and alleochemicals has also been discussed (3, andKelsey et al., 22). Finally, nicotine-related alkaloids are sig-

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nificant pest-interactive components ofNicotiana and Petuniatrichome exudates. Alkaloids, phenolics, and lignans arethought to be important insect-interactive components se-creted or accumulated by trichomes of certain plants (seeKelsey et al., 22).

FUTURE STUDIES

As we become more familiar with the metabolic potentialof trichome gland cells, we may be in a position to transferfrom one genus or species to another genes encoding enzymeswhich can provide modified metabolites having superior pestor pollinator interactive properties. Or, we may be able tointroduce novel modifications to endogenous components,thereby producing new compounds. To reiterate, certainplants can amass high levels of trichome exudate. With to-bacco, for example, using standard cultural practices and avariety yielding 10% of leaf dry weight as exudate, it istheoretically possible to obtain about 225 kg of exudate perhectare. A number of tobacco varieties possess both highbiomass and high exudate accumulation potential. Exudatecan simply and cleanly be recovered by submersion of theplant in noninvasive solvent, again, because this material isessentially accumulated outside the plant.

Plant breeding has been used successfully to manipulatetrichome numbers and exudate composition in a number ofcultivated plant species. Often these efforts have involvedattempts to retrieve from wild species trichome related, pest-resistance-conferring traits which were lost as a result ofselective breeding. An alternative to this approach is to at-tempt direct single gene changes using recombinant DNAmethods. Such attempts at modification may require the useof trichome-specific promoter elements which will probablybe available in the near future. Alternatively, changes whichimpact only on metabolic steps restricted to exudation (i.e.an enzyme specific to exudate compound synthesis) may notrequire such promoters. To this author, the real challenge tothose wishing to cause substantial modification of trichomesecretion using the recombinant DNA approach is not indevising or applying molecular techniques. Rather, it is inidentifying those simple changes ofexisting metabolism whichmay have substantial and desirable impact. Clearly, morestudy is needed to better define existing metabolism of glandcells to expand the possibilities. Finally, experiments to intro-duce novel genes into gland cells will undoubtedly provide agreater understanding of processes governing exudate forma-tion and secretion.

LITERATURE CITED

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2. Croteau R (1986) Catabolism of monoterpenes in essential oilplants. In BM Lawrence, BD Mookherjee, BJ Willis, eds,Proceedings of the 10th International Congress of EssentialOils, Fragrances and Flavors. Elsevier Science Publishers, BVAmsterdam, pp 65-84

3. Cutler HG, Severson RF, Cole PD, Jackson DM, Johnson AW(1986) Secondary metabolites from higher plants. Their possi-ble role as biological control agents. ACS Symp Ser 29C: 178-196

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5. Esau K (1953) Plant Anatomy. John Wiley & Sons, New York6. Fahn A (1988) Secretory tissues in plants. New Phytol 108: 229-

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8. Gershenzon J, Croteau R (1990) Regulation of monoterpenebiosynthesis in higher plants. Rec Adv Phytochem 24: 99-160

9. Goffreda JC, Mutschler MA, Tingey WM (1988) Feeding be-havior of potato aphid affected by glandular trichomes of wildtomato. Entomol Exp Appl 48: 10 1-107

10. Goffreda JC, Szymkowiak EJ, Sussex IM, Mutschler MA (1990)Chimeric tomato plants show that aphid resistance and tria-cylglucose production are epidermal autonomous characters.Plant Cell 2: 643-649

11. Haughn GW, Somerville CR (1988) Genetic control of morpho-genesis in Arabidopsis. Dev Genet 9: 73-89

12. Herman PL, Marks MD (1989) Trichome development in Ara-bidopsis thaliana. II. Isolation and complementation of theGLABROUS 1 gene. Plant Cell 1: 1051-1055

13. Kandra L, Wagner GJ (1988) Studies of the site and mode ofbiosynthesis of tobacco trichome exudate components. ArchBiochem Biophys 265: 425-432

14. Kandra L, Severson R, Wagner GJ (1990) Modified branched-chain amino acid pathways give rise to acyl acids of sucroseesters exuded from tobacco leaf trichomes. Eur J Biochem 188:385-391

15. Kandra L, Wagner GJ (1990) Chlorsulfuron modifies biosyn-thesis of acyl acid substituents of sucrose esters secreted bytobacco trichomes. Plant Physiol 94: 906-912

16. Kaneda T (1967) Biosynthesis of long-chain hydrocarbons. I.Incorporation of /-valine, /-threonine, l-isoleucine and l-leucineinto specific branched-chain hydrocarbons in tobacco. Bio-chemistry 6: 2023-2031

17. Keene CK, Wagner GJ (1985) Direct demonstration of duvatri-enediol biosynthesis in glandular heads of tobacco trichomes.Plant Physiol 79: 1026-1032

18. Koornneef M, Dellaert LMW, van der Veen JH (1982) EMS andradiation-induced mutation frequencies at individual loci inArabdopsis thaliana. Mutat Res 99: 109-123

19. Luttge U, Schnepf E (1976) Organic substances. Eliminationprocesses by glands. In U Luttge, MG Pitman, eds, Transportin Plants II, Part B, Tissues and Organs. Academic Press, NewYork, pp 244-277

20. Nielsen MT, Akers CP, Jarlford VE, Wagner GJ, Berger S(1991) Comparative ultrastructural features of secreting andnon-secreting glandular trichomes of two genotypes of N.tabacum. Bot Gaz (in press)

21. Reeves AF (1977) Tomato trichomes and mutations affectingtheir development. Am J Bot 64: 186-189

22. Rodriguez E, Healy PL, Mehta I (1984) Biology and Chemistryof Plant Trichomes. Plenum Press, New York

23. Schiefelbein JW, Somerville C (1990) Genetic control of roothair development in Arabidopsis thaliana. Plant Cell 2: 235-243

24. Tepfer D (1984) Transformation of several species of higherplants by Agrobacterium rhizogenes: sexual transmission of thetransformed genotype and phenotype. Cell 37: 959-967

25. Tingey WM (1991) Potato glandular trichomes: defense activityagainst insect attack. ACS Symp Ser (in press)

26. Walters DS, Steffens JC (1990) Branched-chain amino acidmetabolism in the biosynthesis of Lycopersicon pennelli glu-cose esters. Plant Physiol 93: 1544-1551

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