The Secret Life of Laticifers

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Review Got milk? The secret life of laticifers

Jillian M. Hagel, Edward C. Yeung and Peter J. Facchini

Department of Biological Sciences, University of Calgary, Calgary, Alberta, T2N 1N4, Canada

Laticifers are specialized cells that occur in over 20 plant 20 000 species in 40 families have been proposed [10].As families in several unrelated angiosperm orders. seen in Figure 1, laticifers are scattered throughout gener- Although laticifers are likely to be of polyphyletic origin, ally unrelated plant orders, suggesting polyphyletic ori- their occurrence is considered a morphological indicator gins. Although distribution occurs mainly in eudicots, of relatedness among species. The classification of lati- laticifers are also found in over half of the genera compris- cifers is based on developmental patterns and overall ing the Arales and Alismatales [11], with sporadic occur- morphology. The cytoplasmic latex exuded in response rences in Liliales (i.e. Allium spp.) and Zingiberales (i.e. the to damage often includes specialized metabolites, such plantain family, Musaceae). Laticifers have also been as cardenolides, alkaloids and natural rubber. Laticifers reported sporadically in conifers (i.e. Gnetum spp.) [12] provide an effective location to store defense metab- and even ferns [9]. olites, although not all latex-bearing plants accumulate Based on their development and overall morphology, bioactive natural products. Ecophysiological studies most laticifers belong to one of two major categories: non- have shown that latex and its associated metabolites articulated and articulated [13]. Non-articulated laticifers are vital for the defense of plants against insects. The are multinucleate, develop from single cells, which anatomy, development and physiology of laticifers are elongate extensively during plant growth, and form either discussed with a focus on evolutionary and ecological unbranched vessels or intricately branched networks perspectives. (Figure 2; Table 1). By contrast, articulated laticifers have a compound origin, in that they develop from multiple cells. Laticifers – more than meets the eye Anastomoses form between the lateral cell walls of adja- Laticifers are highly specialized cells defined by their cent laticifers in some plant species. Catharanthus roseus characteristic anatomy and distinct cytoplasm, known as and Cannabis sativa are examples of plants with non- latex. Despite their unusual nature, the contents of latici- articulated, unbranched laticifers. Non-articulated laticifers have traditional and contemporary importance as fers (branched and unbranched) occur in many Euphorbia- toxins or valuable bioproducts. Aboriginal cultures of ceae and throughout the order Gentianales (Figure 1). Southeast Asia have used exudates of Antiaris spp. con- Well-known examples include spurges (Euphorbia spp.) taining cardiac glycosides as a poison for arrow tips [1,2]. and milkweeds (Asclepias spp.). Articulated laticifers occur Opium poppy (Papaver somniferum) owes both its fame in both monocotyledonous and dicotyledonous plant and notoriety to opiates found in latex [3]. Plants such as orders, especially the Arales, Papaverales, Ebenales, para rubber tree (Hevea brasiliensis) and rubber fig (Ficus Asterales and Campanulales (Figure 1). It should be noted elastica) continue to serve as a commercial source of that the Angiosperm Phylogeny Group [14] has reclassified natural rubber [4]. Laticifers have been found to partici- several taxa according to recent molecular data. In this pate in the biosynthesis of specialized metabolites in cer- context, the Ebenales have been reassigned to the Ericales, tain plants, such as Catharanthus roseus [5]. The latex-bearing members of the Arales have been moved to sequestration of bioactive compounds into laticifers might the Alismatales, most Campanulales belong to the Aster- serve to protect the plant from the cytotoxic effects of its ales, and the Papaverales are grouped with the Ranuncu- own poisons. Moreover, mounting evidence suggests that lales. The occurrence of articulated laticifers has also been latex has a key role in the defense of certain plants against reported in some Euphorbiaceae. Familiar plants posses- herbivores [6–8]. sing such laticifers include poppies (Papaver spp.), sapo- Laticifers are best defined not by what they contain but dilla (Manilkara zapota), lettuce (Lactuca spp.) and para rather by their origins, development and overall anatomy. rubber tree (Hevea brasiliensis). It should be noted that In this review, we examine the distribution and develop- some latex-bearing plants defy the traditional classifi- ment of laticifers in an evolutionary context. We also cation of laticifers. For example, many cacti (Caryophyl- discuss the roles of laticifers in the production and/or lales) possess epithelia-lined, schizolysigenous latex ducts accumulation of specialized metabolites and the involve- [15], whereas latex accumulates in bark parenchymal cells ment of latex and its constituent compounds in plant– in the natural rubber source guayule (Parthenium argen- herbivore interactions. tatum, Asterales) [4]. Several studies have referenced the systematic Classification, occurrence and distribution distribution and morphology of laticifers [13,16–22].A Latex has been reported in 12 500 plant species comparison of diversities in lineages that have either representing 22 families [9], although estimates of up to laticifers or resin canals with their sister groups showed that taxa with secretory structures were consistently more Corresponding author: Facchini, P.J. ([email protected]). species-diverse [20]. The possibility that laticifers promote

Figure 1. Distribution of the four major laticifer types and laticiferous cells or cavities in angiosperms. A phylogenetic tree is depicted in cross section with each branch representing a different order in the classification scheme described by Dahlgren [85]. The thickness of the branches is proportional to the number of species in the order, and the relative position of the orders is defined by multiple parameters. The occurrence of various laticifer types in each order is represented as follows: small dots, <1% of genera; medium dots, 1–10% of genera; large dots, 10–50% of genera; entirely filled, >50% of genera. Hatching indicates that a distinction between two laticifer types has not been made. Although some plant taxonomic relationships have been revised [14], the Dahlgren [85] diagram provides a convenient two-dimensional systematic depiction that facilitates the display of relative laticifer distribution among major plant groups. Information regarding laticifer type and occurrence was obtained primarily from Cronquist [86] but also includes several additions and/or updates [11,16–18,87]. species diversification might reflect conferred selective including those found in cassava (Manihot esculenta) and advantages over herbivores through contributions of the para rubber tree, occur in the Euphorbiaceae. This antifeedant phytochemicals and glue-like properties of phenomenon was interpreted as evidence supporting latex [23]. Laticifers are generally considered to be recently either a common origin for non-articulated laticifers evolved cell types, although fossil records suggest that non- [19,26] or the loss of one laticifer type in species that articulated forms were present in arborescent plants of the previously produced both [27]. Molecular phylogenetic Eocene [9]. data has shown that the Euphorbiaceae are not of mono- The occurrence of laticifers has been proposed as an phyletic origin [28]. Current systematics [14] separates important morphological character for phylogenetic plants in the subfamily Euphorbioideae that possess analyses. For example, laticifers have been used as a non-articulated laticifers from those in the subfamily Cro- diagnostic marker for delineating relationships within tonoideae that contain articulated laticifers. the Araceae [21], and the discovery of latex in the Mal- pighiaceae prompted speculation of a shared ancestry with Development and physiology the Euphorbiaceae [17]. Non-articulated laticifers were A distinction between non-articulated and articulated lati- recently described in the Cornales, which supported a close cifers was made as early as the late 19th century [13], with phylogenetic relationship between the Nyssaceae and the former type being more extensively studied in terms of Mastixiaceae families [18,24]. However, despite the gen- development. Figure 2 illustrates the development of each eral taxonomic specificity of laticifer distribution, multiple laticifer class and Table 1 summarizes their main features. laticifer types sometimes occur in single families or even Non-articulated, branched laticifers develop from single single species, demonstrating that caution must be used initials or primordia, which are detectable in immature when drawing phylogenetic conclusions on the basis of embryos at the time of cotyledon initiation [9]. As the individual markers [25]. Both non-articulated laticifers, seedling grows, the laticifer initials elongate and undergo such as those in Euphorbia spp., and articulated laticifers, karyokinesis without the formation of a cell plate. This

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Figure 2. Schematic representation of the development of the four major laticifer types in plants. Initials of unbranched, non-articulated laticifers have not been identified in embryos but are likely to arise in developing leaves or beneath apical meristems and elongate as the plant grows. Branched, non-articulated laticifers arise from relatively few embryonic initials and grow concomitantly with the organ into a highly branched network throughout the plant. The differentiation of articulated laticifers is coordinated with the development of other phloem tissues, with the initials forming longitudinal rows. Perforation of end walls occurs in most species and leads to the formation of continuous, multinucleate cytoplasm. Anastomoses form between adjacent articulated laticifers through cell wall degradation. Laticifers and their initials are shown in red. Abbreviations: s, sieve element; x, xylem vessel. process continues in meristematic regions of the growing The development of unbranched laticifers is less complex plant [25]. The entire non-articulated, branched laticifer than that of branched forms. Branched and unbranched, network is derived from a set number of initials that varies non-articulated laticifers are shown in Figure 3. in different species. For example, 28 initials are typically Initials of articulated laticifers have been observed in found in Nerium oleander embryos [29], whereas only four the embryos of some species but not others [9]. Articulating initials give rise to the laticiferous network of Euphorbia members are recruited initially in the procambium and engelmanni [30]. Initials typically appear in the cotyledon- later in the vascular cambium. As with non-articulating ary node, forming a ring at the periphery of the young types, early differentiation in articulated laticifers is vascular tissue. Primordia of non-articulated, unbranched marked by the formation of numerous small cytoplasmic laticifers have not been recognized in the embryo but have vesicles possibly derived from dilations of the endoplasmic been identiﬁed in developing shoots of Vinca minor and reticulum or dictyosome cisternae [32]. Laticifer differen- Cannabis sativa, and in the shoots and roots of Eucommia tiation occurs simultaneously with surrounding phloem spp. [9,31]. New initials arise repeatedly beneath apical tissues (Figure 2; Table 1) leading to the formation of meristems and elongate into unbranched tubes. In some discrete longitudinal rows. At maturity, articulated latici- species, laticifers are initiated independently in stems and fers are composed of a series of superimposed cells with leaves (Figure 2). However, where and how unbranched perforated end walls that often generate contiguous laticifer development begins remains poorly understood. vessels (Figure 3). Additionally, the perforation of lateral

Table 1. Summary of the main features of different laticifer types Feature Non-articulated, Non-articulated, Articulated, non-anastomosing Articulated, anastomosing unbranched branched Composition Single coenocytic cell Single coenocytic Multicellular columns with intact or Multicellular columns with perforated cell perforated transverse walls transverse and lateral walls Initials Post-embryonic Embryonic Protophloem and/or phloem Protophloem and/or phloem Multinucleate origin Karyokinesis Karyokinesis Protoplast fusion Protoplast fusion Growth Intrusive Intrusive Differentiation of phloem initials Differentiation of phloem initials: some intrusive Appearance at Long, tubular strands Branched networks Long, tubular strands Branched networks maturity

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Figure 3. Anatomy of laticifers (marked with asterisks) in longitudinal sections of stem (or leaf and carpel in the cases of Lactuca sativa and Papaver somniferum, respectively) of eight plant species. Two examples are provided for each of the four major types of laticifer. Red arrows show articulation points between in-file laticifer members, whereas green arrows identify anastomoses in the longitudinal walls between adjacent laticifers. Sections were developed using the periodate Schiff reaction with amido black 10B used as the counter stain. The scale bars represent 60 mm. walls leads to the formation of anastomoses between adja- the plant, laticifers expand along their lateral walls, cent laticifer elements (Figures 2,3). In plants such as elongate intrusively by tip extension between meriste- opium poppy, lettuce and para rubber tree, frequent ana- matic cells and, via branching, expand into newly formed stomoses can lead to large, intricate networks of continu- organs [9,34]. Presumably, intrusive growth should ous cytoplasm. Transverse and lateral perforations require some disassembly of cell wall components and develop on each side of the middle lamella, such that cell the breaking of plasmodesmatal connections. However, wall thinning is a bilateral process [33]. Gradual degener- this does not seem to occur because cell walls in contact ation of the cytoplasm occurs in many species and is often with laticifers do not show damage [32,35]. Laticifer accompanied by the appearance of altered plastids [18] and penetration has been proposed to involve equilibrium be- characteristic starch grains. Both non-articulated and tween cell wall disassembly and cell wall synthesis to articulated laticifers are generally associated with vascu- facilitate penetration of laticifer tips between meristematic lar tissues (Figures 2,3). At maturity, non-articulated and parenchyma, laticifer elongation and the formation of new articulated laticifers often appear to be morphologically bonds between laticifers and neighboring cells [36,37]. similar because cell wall perforations between articulating Alternatively, laticifers could elongate between symplastic members can lead to the appearance of a single cell domains, thereby avoiding damage to nearby cells. (Figure 3). Pectins are major components of the middle lamellae and primary plant cell walls and have a structure that can Cell wall alterations during laticifer growth and be substantially altered by cell wall-associated enzymes maturation [38]. Pectinase has been detected in milkweed latex [39], Considerable research has focused on the identification and transcripts encoding polygalacturonase were abun- and morphological characterization of laticifers in numer- dant in the latex of para rubber tree [40]. Latex-specific ous plant species. However, the mechanism by which transcripts encoding several pectin-modifying enzymes, invading laticifers penetrate meristematic tissues still including pectin methylesterases, have been reported in requires additional investigation. Although intrusive opium poppy [33]. Pectin methyl esterases have major growth is most typical of non-articulated laticifers, the roles in pectin remodeling during cell wall alterations articulated laticifers of plants such as para rubber tree [38] and have been shown to regulate intrusive fiber cell and cassava form elongated intrusive branches in the same growth in developing Populus spp. wood [41] and Arabi- manner as non-articulated types [9]. In growing regions of dopsis thaliana pollen tubes [42]. Similar enzymes might

634 Review Trends in Plant Science Vol.13 No.12 participate in the intrusive growth of laticifers. Invasive and pathogenesis-related polypeptides. Some latex laticifer development has not been reported in opium proteins might be involved in stress-induced signaling poppy, but pectin modification could be involved in cell cascades, such as Ca2+/calmodulin-binding peroxidase in wall degradation between adjoining and adjacent latici- Euphorbia characias [56] and allene oxide synthase from fers. para rubber tree [57]. In cassava, the enzyme linamarase is found mainly in the laticifers of roots and petioles [58]. Phytochemistry and chemical ecology Linamarase catalyzes the hydrolysis of the cyanogenic Latex often contains specialized metabolites such as ter- glycoside linamarin, leading to the production of toxic penoids, cardiac glycosides, alkaloids, lignans, cannabi- hydrogen cyanide (HCN), and is normally compartmenta- noids and tannins [9]. In general, specialized latex lized separate from linamarin. Tissue damage during food metabolites are biochemical end products that do not re- preparation causes mixing of enzymes and substrates. enter primary metabolism. Many of these products are Cyanogenic glycosides are synthesized in the shoot apex cytotoxic, and it has been suggested that laticifers evolved of cassava and are transported to underground organs [59]. as means of sequestering such compounds independent of Linamarase is probably synthesized in aerial organs and vascular tissues [43]. Examples of key latex metabolites possibly transported throughout the plant via the are shown in Table 2. Although many compound classes branched laticifer network in cassava [58]. are characteristic of the taxa in which they occur (e.g. Proteomic analyses on opium poppy [60], greater celan- benzylisoquinoline alkaloids are common in the Papaver- dine (Chelidonium majus) [61] and the poisonous shrub aceae), there is no strict association between compound Calotropis procera [62] have revealed considerable diver- class and laticifer type. Enzymes involved in vindoline sity in the protein composition of latex. Enzymes, chaper- biosynthesis have been localized to laticifers and idioblast ons, nucleases, putative transcription factors and cells in Catharanthus roseus [5], whereas 1,4-dideoxy-1,4- signaling, storage and defense-related proteins were ident- imino-D-arabinitol (D-AB1) and related pyrrolidine alka- ified. Interestingly, only one of the 69 proteins identified in loids are found in mulberry (Morus spp.) latex [44]. The the cytosolic serum of opium poppy latex was a biosyn- narcotic benzylisoquinoline alkaloids morphine, codeine thetic enzyme [60]. This result supported the localization of and thebaine are the predominant alkaloids in opium alkaloid biosynthesis to cell types other than laticifers in poppy latex. Recently, 1H NMR metabolite profiling was opium poppy [63–65]. used to quantify 21 individual metabolites in opium poppy The involvement of laticifers in the biosynthesis, traf- latex [45]. One abundant compound, g-amino butyric acid, ficking and compartmentalization of specialized metab- acts as a neurotransmitter in animals and has been pro- olites is variable and species-specific [5]. Opium poppy posed to have a defensive role in plants [46]. The latex of laticifers only seem to accumulate benzylisoquinoline alka- Persian poppy (Papaver bracteatum) and opium poppy loids, whereas the laticifers of Catharanthus roseus are accumulate the neurotransmitter dopamine [47], a precur- actively involved in monoterpenoid indole alkaloid biosyn- sor to benzylisoquinoline alkaloids [5]. The piperidine thesis. Two key enzymes, desacetoxyvindoline 4-hydroxyl- alkaloid lobeline accumulates in Lobelia spp., such as ase and deacetylvindoline 4-O-acetyltransferase, that Indian tobacco (L. tupa) and cardinal flower (L. cardinalis). catalyze the final steps of vindoline biosynthesis were The application of lobeline to cabbage loopers (Trichoplu- associated with laticifers and specialized idioblast cells sia ni) induces leaf-trenching behavior suggesting its pre- [66,67]. Vindoline is one of two monomeric indole alkaloid sence in the latex [8]. precursors that combine to form the anticancer drug vin- Isoprene-derived specialized metabolites often accumu- blastine. In some plants, cytotoxic metabolites accumulate late in laticifers. Cardenolides are found in milkweed latex in cells other than laticifers. For example, the pentacyclic and accumulate in feeding butterflies, rendering them quinoline alkaloid camptothecin accumulates in the par- toxic or distasteful to predators [48]. Laticifers of the Upas enchyma and/or epidermal cells of the roots, stems and tree (Antiaris toxicara) house the cardenolide toxin anti- leaves of Camptotheca acuminata [68], but not in laticifers arin (Table 2), which is used to poison darts for hunting [2]. [18].InCannabis sativa, cannabinoids accumulate mostly Terpenophenolic compounds have been identified in the in glandular trichomes rather than in the unbranched, latex of mangosteen (Garcinia mangostana) [49]. In can- non-articulated laticifer system [50]. In dedifferentiated nabaceous species, terpenophenolics are largely seques- opium poppy cells, a lack of laticifers does not preclude the tered in peltate glandular trichomes [50], whereas phenolic elicitor-induced biosynthesis and accumulation of the anti- glucosides occur in the shoot laticifers of Cannabis sativa microbial alkaloid sanguinarine [69], although the pro- [51]. Although the presence of sesquiterpene lactones in duction of morphinan alkaloids does not occur. Related latex from Lactuca spp. did not correlate with fungal plants that lack laticifers have evolved different strategies pathogen resistance [52], a chemical basis for the bitter for specialized metabolite formation and storage. Proto- taste of lettuce and chicory was established. Lettuce has berberine alkaloids in yellow meadow rue (Thalictrum also been investigated as a source of natural rubber [53]. flavum) accumulate in the endodermis of roots and the However, natural rubber is predominantly harvested from cortical cells of rhizomes [70]. the laticifers of Hevea brasiliensis [4]. The inconsistent involvement of laticifers in specialized Laticifers not only serve as a repository for natural metabolism raises an important evolutionary question. products but also exhibit unique proteomes. Many latex Were laticifers present before the biosynthetic capacity proteins are thought to have defensive roles in plants, to produce certain metabolites, offering a convenient sto- including cysteine and serine proteases [54,55], chitinases rage site for novel and highly toxic compounds? Plants

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Table 2. Examples of specialized metabolites that occur in the latex of various plants Laticifer type Taxa Compound class Example Structure Non-articulated, unbranched Catharanthus roseus Monoterpenoid indole Vindoline (Madagascar periwinkle) alkaloid Apocyanaceae

Non-articulated, unbranched Cannabis sativa Phenolic glucoside Phloroglucinol-b-D- (Hemp, marijuana) glucoside Cannabaceae

Non-articulated, unbranched or Asclepias eriocarpa Cardenolide Labriformin branched (California milkweed) Asclepiadaceae

Non-articulated, branched Morus spp. Pyrrolidine alkaloid D-AB1 (Mulberry) Moraceae

Non articulated, branched Antiaris toxicara Cardenolide Antiarin (Upas tree) Moraceae

Articulated, anastomosing Hevea brasiliensis Isoprenoid Natural rubber (Para rubber tree) Euphorbiaceae

Articulated, anastomosing Papaver somniferum Benzylisoquinoline alkaloid Morphine (Opium poppy) Papaveraceae

Articulated, anastomosing Lactuca sativa Sesquiterpene lactone Lactucin (Lettuce) Asteraceae

Articulated, anastomosing Papaver bracteatum Catecholamine Dopamine (Persian poppy) Papaveraceae

Articulated, anastomosing Lobelia spp. Piperdine alkaloid Lobeline (Cardinal ﬂower, Indian tobacco) Campanulaceae

636 Review Trends in Plant Science Vol.13 No.12 seem to store many natural products in laticifers, gland- cals act as behavioral stimulants [8,23]. The consistency of ular trichomes and other specialized cell types to position latex itself also seems to have a defensive role because the defensive metabolites in appropriate locations. The glue-like exudate coats the mouthparts of foraging herbi- capacity to synthesize many types of specialized metab- vores and seals wounds in the plant from pathogen attack olites, such as benzylisoquinoline alkaloids, is of ancient [23,79]. and monophyletic origin [71,72]. The occurrence of highly conserved benzylisoquinoline alkaloid biosynthetic Applications and future directions enzymes in plants with and without latex suggests that Due to their secretory nature, laticifers have been proposed laticifers arose in the Papaveraceae after the emergence of as potential sinks for the storage of excess atmospheric the metabolic pathways. The accumulation of the mono- carbon [9]. Moreover, the ability of plants to synthesize and terpenoid indole alkaloid camptothecin in glandular tri- store copious amounts of latex has been suggested to chomes in Camptotheca acuminata [18,68] might reflect a contribute to the regulation of levels of atmospheric iso- storage solution that occurred before the appearance of prene gas, which is expelled into the atmosphere in laticifers in this species. The sequestration of camptothecin quantities comparable to methane [80]. The ability to to glandular trichomes, rather than laticifers, would also accumulate high concentrations of toxic chemicals renders advantageously place this putative defense compound at laticifers relevant in a phytoremediation context. Nickel the plant surface. The polyphyletic origin of laticifers concentrations of up to 26% dry mass have been found in explains in part the myriad roles observed for these cell the latex of the rare rainforest tree Sebertia acuminata types within the context of specialized metabolism [9].A [81,82]. Determining the mechanism of nickel sequestra- parallel and as yet unaddressed question concerns the tion to S. acuminata laticifers could provide interesting extent to which laticifers of monophyletic origin display options in the development of metal hyperaccumulators. similar physiological functions. The developmental biology of laticifers also has industrial implications. In para rubber tree, the number of Adaptive mechanisms of feeding insects laticifers is a key factor influencing rubber yield, which Many studies have linked the unique biochemistry of lati- has prompted efforts to increase laticifer biogenesis and cifers with the defense of plants against herbivores [25]. induce differentiation [57,83]. Solutions to problems Both proteins and metabolites within latex have been shown associated with reduced latex flow will require a better to protect plants against feeding insects. However, certain understanding of the interaction between plant defense insect specialists have evolved adaptive mechanisms to responses and laticifer biology [84]. Studies on laticifer overcome the toxic properties of some compounds. The physiology might also contribute to the reduction of illicit cysteine protease papain was identified as a crucial factor opium poppy cultivation. Whereas licit poppy agriculture in protecting papaya trees (Carica papaya) against Eri employs modern, mechanized farming methods, black- silkworm, cabbage moth and tobacco cutworm [7]. Moreover, market opium for heroin production is collected using the application of C. procera latex proteins to various crop traditional lancing techniques. Opium (i.e. dried opium pests reduced their growth and survival [73]. The complex poppy latex) is harvested via the incision of immature seed relationship between mulberry and the silkworm Bombyx capsules, which releases a milky exudate owing to turgor mori has also been investigated. Mulberry trees have long pressure within the articulated, anastomosing laticifer been used to rear the economically valuable worm as a network. Interestingly, biotechnological intervention source of silk proteins. Mulberry latex rich in sugar-mimic aimed at precluding the formation of perforations among alkaloids such as D-AB1 (Table 2) reduces the feeding of laticifer initials has been suggested as a means of reducing generalist caterpillars but not the silkworm, indicating that latex flow and hampering the illicit collection of opium [33]. this specialist can circumvent the toxicity of D-AB1 [7].The Laticifers have undoubtedly contributed to the overall recent discovery of b-fructofuranosidase genes in mulberry ability of plants to synthesize and store toxins, medicines silkworm has provided a molecular basis for pyrrolidine and other bioproducts important for human use and in the alkaloid tolerance [74]. Unlike the more common a-gluco- defense against herbivores. Due, in part, to the wide and sidases used for digesting sugars, b-fructofuranosidases are variable taxonomic distribution of laticifers within vascu- not inhibited by high concentrations of pyrrolidine alka- lar plants, it has generally been assumed that articulated loids, thus permitting the silkworm to feed. and non-articulated laticifers evolved independently [9]. Numerous studies have revealed a similarly complex However, comparative systematic studies are scarce and relationship between cardenolide-rich milkweeds and more evidence is needed to draw better evolutionary con- monarch butterflies [75,76]. Milkweed cardenolides are clusions. Despite the biological and industrial importance toxic to generalist caterpillars [77], and insect feeding of laticifers, research focusing on the development and can increase the cardenolide content of latex [78]. Monarch biosynthetic role of laticifers has been lacking. Renewed larvae circumvent this plant defense mechanism by chew- interest in laticifer biology should arise through efforts ing a furrow in the leaf midrib or petiole (i.e. ‘trenching’ aimed at the metabolic engineering of valuable specialized behavior), which releases the laticifer contents. The larvae metabolites and studies on phytoremediation and plant– then proceed to feed beyond the cut site where latex flow is insect interactions. minimal. Many insects exhibit trenching behavior, which reduces their exposure to latex or resinous exudates. The Acknowledgements Research program support was provided by Natural Sciences and application of common latex compounds to cabbage loopers Engineering Research Council of Canada Discovery (E.C.Y. and P.J.F.) induced trenching behavior, suggesting that certain chemi- and Strategic Project (P.J.F.) Grants. J.M.H. is the recipient of an Alberta

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