an a cardiac eae evolution toxic phenolic s

The Evolution of Toxic Phenolic Compounds in a Group of Anacardiaceae GeneraAuthor(s): Carlos J. Aguilar-Ortigoza and Victoria SosaSource: Taxon, Vol. 53, No. 2 (May, 2004), pp. 357-364Published by: International Association for Plant Taxonomy (IAPT)Stable URL: http://www.jstor.org/stable/4135614 .

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TAXON 53 (2) * May 2004: 357-364 Aguilar-Ortigoza & Sosa * Compounds in Anacardiaceae

The evolution of toxic phenolic compounds in a group of Anacardiaceae genera

Carlos J. Aguilar-Ortigozal,2 & Victoria Sosal

SInstituto de Ecologia, A.C., Apartado Postal 63, 91000 Xalapa, Veracruz, MWxico. [email protected] (author for correspondence)

2Facultad de Ciencias, Universidad Autdnoma del Estado de MWxico, Toluca, Mixico. aguilarc@ ecologia.edu.mx

Anacardiaceae are largely tropical trees, shrubs and lianas of the order Sapindales, characterized by production of three types of toxic phenols: biflavonoids, alkylcatechols and alkylresorcinols. Anatomical, morphological and rbcL sequence data were used to reconstruct the phylogeny of a group of Anacardiaceae and address questions about the origin and evolution of these toxic phenolic compounds. Their evolutionary patterns are dis- cussed in relation to the group of Hemipteran insects that feed on Anacardiaceae. Our study included 22 taxa of Anacardiaceae and the results support previous phylogenetic studies in that two clades are detected: a basal clade, with Spondias and related genera that do not produce toxic phenolic compounds, and a second clade with the remaining genera, i.e., those that produce biflavonoids, as do species of Burseraceae. The evolution-

ary patterns of alkylcatechols and alkylresorcinols are not straightforward; these substances are produced in unrelated groups of genera. We suggest, however, that Hemipteran insects do not feed on taxa of Anacardiaceae that produce alkylcatechols.

KEYWORDS: alkylcatechol, alkylresorcinol, Anacardiaceae, associated herbivores, biflavonoid, phylogenetics, evolution.

E INTRODUCTION Anacardiaceae are an angiosperm family known to

produce allergenic substances in the resin canals of primary and secondary phloem associated with the veins of leaves and other parenchymatous tissues (Metcalf & Chalk, 1950). Toxic chemicals are phenols of three types: alkylcatechols, alkylresorcinols and biflavonoids. Urushiol, the most allergenic and common of these, is a mixture of saturated and unsaturated pentadecyl- and heptadecylcatechols, found in a number of taxa, such as poison ivy (Toxicodendron radicans; Eggers, 1974; Gross & al., 1975; Baer & al., 1980; Adawadkar & EISohly, 1983; Du & al., 1984; Gambaro & al., 1986; Rivero-Cruz & al., 1997). Cardol, another allergenic phenolic compound that is characteristic of some Anacardiaceae, is a pentadecylresorcinol found in the fruit of the cashew nut (Anacardium occidentale; Tyman & Morris, 1967; Evans & Schmidt, 1980). Heptadecyl- resorcinol is found in the mango fruit (Mangifera indica) (Cojocaru & al., 1986). Biflavonoids are common in most groups of Anacardiaceae but absent from the Spondias group of genera (Young, 1976; Wannan & al., 1985; Young & Aist, 1987; Wannan & Quinn, 1988; Yuh- Meei & al., 1989). Biflavonoids are also common in the gymnosperms (Smith, 1976) and in Burseraceae (Wannan & al., 1985).

In Anacardiaceae toxic phenols are likely a defense against pests, because they are capable of restricting the growth of pathogenic fungi such as Alternaria (Cojocaru & al., 1986; Harbome, 1999). It has also been suggested that toxic phenols are a defense against insects and ver- tebrates (Joel, 1980; Mitchell, 1990; Farrel & al., 1991). Occurrence of toxic phenols in Anacardiaceae and related groups have created interesting plant-insect interactions. For example, Bursera, a group closely related to Anacardiaceae, produces terpenes against Coleoptera such as Blepharida (Furth & Young, 1988; Becerra, 1997). It has also been reported that Blepharida feed on several species of Rhus (Anacardiaceae) in which the toxic phenols that have been detected were flavonoids (Furth & Young, 1988; Becerra, 1997). Calophya, a monophagous genus of Hemiptera, feeds on species of Burseraceae, Anacardiaceae and Rutaceae (Hodkinson, 1989). Coevolutionary hypotheses of the relationship between Calophya and some species of Anacardiaceae have recently been proposed (Burckhardt & Basset, 2000).

Fifty-two species of 27 of the approximately 80 genera of Anacardiaceae contain toxic phenols (Mitchell, 1990; Aguilar-Ortigoza & al., 2003). The majority of these toxic species are members of tribe Rhoeae.

Engler (1883) divided Anacardiaceae into five tribes: Anacardieae, Spondiadeae, Rhoeae, Semecarpeae

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Aguilar-Ortigoza & Sosa * Compounds in Anacardiaceae TAXON 53 (2) * May 2004: 357-364

and Dobineae, based on morphological characters such as carpel and locule number at anthesis and fruit, stylar morphology, insertion of ovule, and leaf morphology. However, studies based on anatomical, morphological, and molecular evidence indicate that there are only two lineages within the family, one formed by the genera of Spondiadeae with a few genera of Rhoeae, and a second with the remaining genera (Wannan & Quinn, 1991; Terrazas, 1994; Terrazas & Chase, 1996; Pell & Urbatsch, 2001).

We used anatomical, morphological and rbcL sequence data to reconstruct the phylogeny of a group of genera belonging to Spondiadeae and others previously considered in Anacardieae and Rhoeae, and to address questions about the origin and evolution of phenolic toxic compounds such as alkylcatechols, alkylresorcinols and biflavonoids. We discuss these compounds in relation to the group of Hemipteran insects that feed on Anacardiaceae.

E MATERIALS AND METHODS Plant material. - Our study includes only repre-

sentatives of 22 out of the 80 genera of the family. However, our sampling strategy for the phylogenetic analysis was to include different species of currently recognized groups in Anacardiaceae as well as species having any of the three toxic phenolic compounds considered in this study. Current molecular phylogenetic evidence indicates that Anacardiaceae are sister to Burseraceae and that Sapindaceae, Rutaceae and Meliaceae are closely related (Savolainen & al., 2000a, b; Soltis & al., 2000). Therefore, as an outgroup, four species belonging to Burseraceae, Sapindaceae, Rutaceae and Meliaceae, were considered. Vouchers and DNA GenBank accession numbers are given in Appendix 1 (see online version of Taxon).

Morphological characters. - The 88 morphological characters used in the present analysis were com- piled from our own observations of herbarium material and supplemented with data in the literature. The characters are essentially those used by Aguilar & al. (2004)

and represent aspects of morphology and anatomy of leaf, inflorescence, flower, fruit, seed and wood (Table 1;. the morphological and anatomical data matrix is pro- vided in Appendix 2 and the examined herbarium specimens in Appendix 3 (both available online).

Chemical characters. - Occurrence of alkylcatechols, alkylresorcinols and biflavonoids in different parts of the plants was taken for most species from the compilation of Aguilar-Ortigoza & al. (2003) (Fig. 1; Appendix 1). For some other species the same methods described in Aguilar-Ortigoza & al. (2003) were carried out to determine occurrence of these chemicals (Appendix 1). In cases where the information was taken from other sources, references are cited.

Molecular methods. - DNA from fresh leaves and herbarium specimens was extracted using the 2X CTAB method of Doyle & Doyle (1987). Total DNA and PCR products were cleaned with QIAquick silica columns (Qiagen, Inc) according to the manufacturer's protocols. The rbcL exon was amplified in two overlap- ping fragments according to the PCR protocol and two pairs of primers described in Savolainen & al. (2000a). PCR products were sequenced in both directions with these PCR primers, using the BigDyeTM Terminator Mix and an ABI 377 automated sequencer following manufacturer's protocols (Applied Biosystems, Inc.).

Phylogenetic analyses and alignments. - Three parsimony analyses were performed, morphology alone, rbcL alone, and a combined analysis. They were performed with PAUP 2.0b2 (Swofford, 2000) and ana- lyzed using Fitch parsimony (Fitch, 1971). The three analyses were heuristic searches performed with 1000 random addition sequence replicates to look for multiple optimal-tree islands (Maddison, 1991). Analyses used TBR (tree bisection reconnection) branch swapping, MULTrees, steepest descent and ACCTRAN optimization. Internal support was evaluated with jackknife analysis (Farris & al., 1996) of 1000 replicates and 30% deletion of characters. In morphological analysis characters were considered unordered. In molecular analysis contiguous sequences were assembled and checked using Sequencher 3.0 (Genecodes, Inc.); rbcL sequences are length conserved and easily aligned by eye.

1o /

OH

H OH OH H 0

OH C15H31

(CHz2)14CH3 (CH2)7CH=CH(CH2)7CH3 H O

(1) A 3-Pentadecylcatechol (2) A 3-Heptadecylcatechol (3) Pentadecyl resorcinol or Cardol (4) Rhusflavanone, a biflavonoid

Fig. 1. Toxic chemicals in Anacardiaceae.

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TAXON 53 (2) * May 2004: 357-364 Aguilar-Ortigoza & Sosa * Compounds in Anacardiaceae

Table 1. Morphological, anatomical and phytochemical character and character-states used in the phylogenetic analyses of genera of Anacardiaceae.

1. Habit of plant: 0 = tree, 1 = shrub. 48. Carpel number: 0 = five, I = three, 2 = two, 3 = one.

2. Leaves: 0 = paripinnate, 1 = imparipinnate, 2 = simple. 49. Locules in ovary at anthesis: 0 = five, 1 = three, 2 = one.

3. Leaf shape: 0 = oblong, 1 = elliptic, 2 = ovate, 3 = obovate. 50. Stylar insertion: 0 = apical, 1 = ventral-lateral.

4. Leaf texture: 0 = chartaceous, 1 = coriaceous. 51. Stigma morphology: 0 = capitate, 1 = spathulate. 5. Leaf duration: 0 = evergreen, 1 = deciduous. 52. Ovule orientation: 0 = epitropous, 1 = apotropous. 6. Leaf grouping in branches: 0 = sparsed, 1 = clustered at apex. 53. Ovules per locule: 0 = two, 1 = one.

7. Leaf margin dissection: 0 = serrate, 1 = entire. 54. Ovule integument: 0 = two, 1 = one.

8. Rachis: 0 = not winged, 1 = winged. 55. Ovule insertion: 0 = apical, 1 = apico-lateral, 2 = latero-basal, 3 = basal.

9. Terminal leaflet shape: 0 = ovate, 1 = elliptic, 2 = obovate. 56. Fruit form: 0 = ovoid, 1 = oblate, 2 = suborbicular.

10. Apex of the leaf: 0 = acute, 1 = obtuse. 57. Winged fruit: 0 = absent, 1 = present. 11. Lamina type: 0 = dorsiventral, I = isobilateral. 58. Peduncule of fruit: 0 = thin, 1 = thick.

12. Foliar epidermis: 0 = single-layered, 1 = multi-layered. 59. Fruit trichomes: 0 = absent, 1 = present. 13. Foliar hypodermis: 0 = absent, I = present. 60. Epidermis of exocarp: 0 = unlignified, 1 = lignified. 14. Stellate trichomes: 0 = present, 1 = absent. 61. Hypodermis of exocarp: 0 = absent, 1 = present. 15. Capitate trichomes: 0 = present, 1 = absent. 62. Mesocarp sclereids with resin canals: 0 = absent, 1 = present. 16. Cuticular striae: 0 =random, 1 = radial. 63. Mesocarp with inner parts lignified: 0 = absent, I = present. 17. Giant stomata: 0 = absent, 1 = present. 64. Endocarp number of layers: 0 = one, 1 = two, 2 = three, 3 = four.

18. Type of venation: 0 = camptodromous, 1 = craspedodromous. 65. Endocarp discrete fourth layer: 0 = absent, 1 = with parenchyma, 19. Size of primary vein: 0 = massive, 1 = stout. 2 = with sclereids. 20. Angle of secondary vein: 0 = narrow, 1 = moderate. 66. Endocarp crystals in the layer: 0 = absent, 1 = present. 21. Tertiary veins: 0 = percurrent, 1 = reticulate, 2 = ramified. 67. Endocarp discrete third layer: 0 = absent, 1 = with palisade-shaped 22. Marginal venation: 0 = fimbriate, 1 = incomplete. sclereids, 2 = with sclereids.

23. Veinlets: 0 = simple, 1 = branched. 68. Endocarp discrete second layer: 0 = absent, I = with palisade-shaped 24. Inflorescence position: 0 = terminal, 1 = axilar. sclereids, 2 = with osteosclereids, 3 = with brachysclereids. 25. Inflorescence type: 0 = panicle, 1 = thyrsoid. 69. Endocarp discrete first layer: 0 = with sclereids, 26. Cupular involucre: 0 = absent, 1 = present. I = with palisade-shaped sclereids.

27. Flower sex: 0 = unisexual, 1 = bisexual. 70. Endocarp first layer size: 0 =less the twice of rest of layer, 28. Sepal number: 0 = three, 1 = four, 2 = five, 3 = six. 1 = more than twice thickness.

29. Calix aestivation: 0 = valvate, 1 = imbricate. 71. Number of seeds: 0 = five, 1 = three, 2 = two, 3 = one.

30. Sepal indument: 0 = glabrous, 1 = pubescent. 72. Embryo: 0 = straigth, 1 = curved.

31. Margin sepal indument: 0 = glabrous, 1 = pubescent. 73. Testa: 0 = membranous, 1 = crustaceous.

32. Sepal shape: 0 = oblong, 1 = ovate. 74. Endosperm: 0 = present, 1 = absent.

33. Petal number: 0 = five, 1 = four, 2 = zero. 75. Cotyledon margin: 0 = lobed, 1 = entire.

34. Corolla aestivation: 0 = imbricate, 1 = valvate. 76. Wood parenchyma apotracheal: 0 = absent, 1 = present. 35. Petal shape: 0 = oblong, I = elliptic, 2 = ovate. 77. Wood parenchyma paratracheal: 0 = alliform, 1 = banded, 2 = vasicentric.

36. Stamen number: 0 = ten, 1 = five, 2 = eigth. 78. Wood ray width: 0 = 1-5 cells, 1 = 6-10 cells.

37. Filament form: 0 = filiform, 1 = subulate. 79. Wood ray type: 0 = heterogeneous IIB, 1 = heterogeneous IIA, 38. Filament indument: 0 =glabrous, 1 = pubescent. 2 = heterogeneous III. 39. Anther form: 0 = pyriform, 1 = rotund, 2 = botuliform. 80. Septate wood fibers: 0 = present, 1 = absent.

40. Anther: 0 = basifixed, I = dorsifixed. 81. Resin canals in wood rays: 0 = present, 1 = absent.

42. Pollen shape: 0 = prolate, 1 = spheroidal. 82. Resin canals in ploem: 0 = absent, I = present. 42. Pollination: 0 = by insects, 1 = by wind. 83. Vessel clusters: 0 = absent, 1 = present. 43. Nectariferous disk: 0 = intrastaminal, 1 = extrastaminal. 84. Starch in vessels: 0 = absent, 1 = present. 44. Disk form: 0 = patelliform, 1 = cotyliform, 2 = columnar. 85. Growth ring: 0 = absent, 1 = present. 45. Disk margin: 0 = crenate, 1 = lobate. 86. Alkylcatechols: 0 = absent, I = present. 46. Number of disk lobes: 0 = ten, 1 = five. 87. Alkylresorcinols: 0 = absent, 1 = present. 47. Carpellode number: 0 = five, 1 = three, 2 = two, 3 = one. 88. Biflavonoid: 0 = absent, 1 = present.

Reconstructing the history of chemical characters. - To investigate the evolutionary history of chemical characters we mapped the presence of each of the three phenolic compounds (alkylcatechols, alkylresorcinols and biflavonoids) on the strict consensus tree

using parsimony optimization and the TRACE option of MacClade version 3.04 (Maddison & Maddison, 1992).

RESULTS Phylogenetic relationships. - Morphological

analysis recovered a single equally most-parsimonious tree (MPT) of 453 steps, with a consistency index (CI) of 0.38 and a retention index (RI) of 0.52, including a total of 88 characters, with 86 parsimony informative charac-

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Aguilar-Ortigoza & Sosa * Compounds in Anacardiaceae TAXON 53 (2) e May 2004: 357-364

ters. Fig. 2 represents one of the MPT selected at random. rbcL analysis recovered 21 MPT of 481 steps, with a CI of 0.73 and a RI of 0.61, including 1414 characters, with 127 parsimony informative characters. Fig. 3 represents one of the MPT selected at random. Matrix of combined analysis included 1502 characters with 213 parsimony informative characters. Eight MPT of 1002 steps were obtained with a CI of 0.57 and a RI of 0.53. Fig. 4

represents one of the MPT, selected at random. Topology of MPT is very similar in the three analyses. The morphological tree is the least supported, with only a few clades receiving jackknife support above 50%. In the tree

analyses the Anacardiaceae clade is always recovered with good jackknife support. In the three analyses, Clade I and Clade II are recovered. Buchanania is always basal in Clade II and Anacardium and Mangifera form a subclade. Position of some of the members of Clade II varies

(Figs. 2-4). For example, Blepharocarya is in a subclade with Anacardium and Mangifera in the rbcL analysis while in the combined analysis it is in a subclade with the rest of the taxa of Clade II. The best supported topology is from combined analysis in which the Anacardiaceae clade is well supported (100% jackknife value). Two clades are found within the family: a well supported basal clade formed by Cyrtocarpa, Spondias and

Tapirira, and a second clade with the rest of the genera

Bursera a-

Ruta 0

Dodonaea

Svetenia 0

Tapirira 62

57 Cyrtocarpa

Spondias

Buchanania

Blepharocarya

Anacardium

Mangifera

Bonetiella

Cotinus

Actinocheita u

Comocladia

Metopiumr

Amphipterygium M c

Pistacia <

Pseudosmodingium

Mosquitoxylum

Schinopsis

Astronium

Schinus

Rhus

Smodingium

Toxicodendron

Fig. 2. MPT tree of the morphological analysis of 453 steps, with CI of 0.38 and a RI of 0.52. Jackknife percen- tages (>50%) are indicated above the branches.

Bursera

Ruta

Dodonaea

Swietenia

Tapirira 62

-E Cyrtocarpa

Spondias

Buchanania

Blepharocarya

Anacardium

83 Mangifera

Bonetiella

Cotinus

Actinocheita

Comocladia

Metopium

Amphipterygium

Pistacia

Pseudosmodingium

Mosquitoxylum

Schinopsis

Astronium

Schinus

Rhus

Smodingium

Toxicodendron

Fig. 3. One of the 21 MPT trees of the rbcL analysis of 481 steps, with a Cl of 0.73 and a RI of 0.61. Jackknife per- centages (>50%) are indicated above the branches.

(strongly supported 90% jackknife value). Buchanania

appears basal in this clade. Well supported groups in these clade are formed by Actinocheita, Bonetiella and Comocladia (jackknife value of 94%), Metopium and Mosquitoxylum (97%) and Astronium and Schinopsis (100%).

Character evolution. - Evolution of the chemical characters show different patterns depending on the

type of toxic phenolic compound. Alkylcatechols evolved in two groups in Anacardiaceae, in a clade (not supported) formed by Actinocheita, Astronium, Bonetiella, Comocladia, Metopium, Mosquitoxylum, Pseudosmodingium and Schinopsis, and in a subclade (well supported) formed by Smodingium and Toxicodendron. The ancestral condition is the lack of

alkylcatechols (Fig. 4). The presence of alkylresorcinols is restricted to the clade of Anacardium and Mangifera and in Schinus (Fig. 4). Biflavonoids arose independently in Burseraceae and in Clade II of Anacardiaceae with the exception of Buchanania (Fig. 4).

DISCUSSION Phylogenetic analysis. - Our results agree with

360



TAXON 53 (2) e May 2004: 357-364 Aguilar-Ortigoza & Sosa * Compounds in Anacardiaceae

Ej 0 Dodonaea

80 O0 Swietenia Outgroup 130 Ruta M0 Bursera

90 Tapirira

S65 0 Cyrtocarpa Clade I E0loo 0O Spondias

=0 Buchanania

90 97 me Anacardium

WM Mangifera

0M 0 Blepharocarya

72 M 0 Cotinus

M10 Amphipterygium

M80

Pistacia

6me Schinus Clade II

8Q O0 Rhus

91 M 0 Smodingium

M0 Toxicodendron

94 Actinocheita

84

M• 0Bonetiella

M( Comocladia

97 • 0 Metopium

6 0 Mosquitoxylum

O Absence of biflavonoids M•1 M Pseudosmodingium m Presence of biflavonoids 100 M 0 Astronium

O Absence of alkylcatechols and alkylresorcinols M @ Schinopsis O Presence of alkylcatechols * Presence of alkylresorcinols

Fig. 4. One of the eight MPT of the combined analysis of 1002 steps with CI = 0.57 and RI = 0.53. Jackknife per- centages (>50%) are indicated above the branches. Evolution of alkylcatechols, alkylresorcinols and biflavonoids are mapped onto the tree.

previous phylogenetic studies (e.g., Gadek & al., 1996), in that Anacardiaceae are a monophyletic group. The two lineages in Anacardiaceae mentioned in our results are also detected in molecular phylogenetic studies (Miller & al., 2001; Pell & Urbatsch, 2001) and in studies that combined character sets (DNA sequences and morphology, Terrazas & Chase, 1996). Furthermore, endocarp and wood characters also indicate two groups in the family, comprised of the same genera (Wannan & Quinn, 1990, 1991). Two types of endocarp are found in Anacardia- ceae, the Anacardium-type (with discrete and regularly arranged layers), three or fewer carpels and a unilocular ovary, and group B with the Spondias-type of endocarp (a thick mass of usually lignified and irregularly oriented sclerenchyma), more than three carpels and a multilocular ovary. Group B corresponds to tribe Spondiadeae from Engler's (1883) classification or to Clade I, including Antrocaryon, Cyrtocarpa, Dracontomelon, Haema- tostaphis, Harpephyllum, Lannea, Sclerocarya, Spondias and Tapirira, among others. The Spondias clade retained plesiomorphic characters such as a gynoecium with five carpels, fruit often multilocular with a thick endocarp, lignified, and with irregularly oriented sclereids (Wannan & Quinn, 1990). The Spondias-type of endocarp is also present in some Burseraceae (Wannan & Quinn, 1990).

The genera of Clade II share morphological characters such as a tricarpelar gynoecium, unilocular fruit with

Burseraceae .--- C. nigridorsalis

Sapindaceae C.

rhois Meliaceae

Rutaceae C. duvauae

Tapirira C. evodiae

Cyrtocarpa C. nigrilineata

Spondias C. monticola Buchanania

Anacardium -C. longispiculafa Anacardium

Mangifera C. spondiasiae

Blepharocarya C. verrucosa

Cotinus C andina

Amphipterygium C. clausa

Pistacia

Schinus C. mammifex

Rhus C. patagonica

Smodingium C rubra

Toxicodendron C. orbicola Actinocheitaorbicola

Bonetiella C. gallifex

Comocladia C. schini

Metopium C. scrobiocola Mosquitoxylum

C. catillicola Pseudosmodingium

Astronium C. hermicitae

Schinopsis L C. terebinthifolii

Fig. 5. Feeding preferences of Calophya species (right) on Anacardiaceae, Burseraceae and Rutaceae hosts (left). Calophya phylogeny based on Burckhardt & Basset (2000).

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Aguilar-Ortigoza & Sosa * Compounds in Anacardiaceae TAXON 53 (2) e May 2004: 357-364

an endocarp composed of discrete and regularly arranged layers of cells (Wannan & Quinn, 1990). One of the well supported subclades in Clade II is formed by Schinus, Rhus, Smodingium and Toxicodendron. They all share characters such as imparipinnate leaves sparsely distrib- uted along branches, ovate and chartaceous leaflets; moreover, they have the same calyx indument, thyrsoid inflorescence and wood having the heterogeneous IIB type of ray. Rhus and Toxicodendron are cosmopolitan, while Schinus is from South America and Smodingium is endemic to South Africa. The other subclade, also well supported, is formed by Actinocheita, Bonetiella and Comocladia. These three neotropical genera share characters such as coriaceous leaves, panicle type of inflorescence with axillar insertion and imbricate calyx aestivation. Actinocheita and Bonetiella are endemic to Mexico, and Comocladia to Mexico and the West Indies. Metopium and Mosquitoxylum are a sister group distrib- uted in Mexico and the West Indies. The closely related group formed by Pseudosmodingium, Astronium and Schinopsis is also neotropical.

Character evolution. - One of the most interesting patterns of evolution of the toxic phenolic compounds in Anacardiaceae is that shown by the biflavonoids. Burseraceae, included as an outgroup in our analyses and recognized as sister to Anacardiaceae (Gadek & al., 1996; Terrazas & Chase, 1996; Pell & Urbatsch, 2001), synthesizes biflavonoids. These biflavonoids are not produced by the genera of Clade I of Anacardiaceae, the Spondiadeae of Engler (1883), but they are produced in the taxa of Clade II, arising only once in the history of the group. Wannan & al. (1985) and Young & Aist (1987) previously pointed out this pattern. Furthermore, the genera of Clade I did not produce the phenolic compounds we considered. The members of Clade II, with the exception of Buchanania, synthesize biflavonoids. The presence of this compound strongly supports the inclusion of Amphipterygium and Blepharocarya in Anacardiaceae, although these genera have been considered in Julianiaceae and Blepharocary- aceae, respectively (Airy Shaw, 1965; Hemsley, 1908). Amphipterygium's flowers lack a corolla and Blepharocarya possesses small globose inflorescences and their leaves are opposite and pinnate, characters not common among Anacardiaceae.

The evolutionary patterns of alkylcatechols and alkylresorcinols in the members of Clade II are not straightforward. Alkylcatechols evolved in two groups: in a clade formed by Actinocheita, Astronium, Bonetiella, Comocladia, Metopium, Mosquitoxylum, Pseudosmodingium and Schinopsis, and in a subclade formed by Smodingium and Toxicodendron.

Alkylresorcinols are less common than alkylcatechols or biflavonoids among Anacardiaceae. They arose

independently at least twice, in the clade of Anacardium + Mangifera and in Schinus. These phenolic compounds are synthesized in the pericarps of three economically important species: the cashew nut (Anacardium occidentale), the mango (Mangifera indica) and the less widely known Brazilian pepper (Schinus terebinthifolius). Their fruits have been reported to cause dermatitis in certain individuals (Morton, 1978, 1981).

Spondias which does not produce alkylcatechols, alkylresorcinols or biflavonoids has the capacity to synthesize phenolic compounds (Corthout & al., 1989). Spondias mombin L. has been reported to possess the metabolic route to synthesize these substances, since the precursors of the formation of a related phenol, hep- tadecadienyl-phenol, have been detected (Corthout & al., 1989).

Biosynthetic routes of alkylcatechols and biflavonoids are involved in the shikimate pathway (Van Sumere, 1989). Accumulation of alkylcatechols, alkylresorcinols and biflavonoids is in some cases restricted to certain organs of the plant. Alkylcatechols and biflavonoids are usually present in leaves and bark. But in some species such as Metopium brownei alkylcatechols also found in wood (Young, 1976). A few Semecarpus species (not included in our analysis) also produce alkylcatechols in fruits (Carpenter & al., 1980). Occurrence of these chemicals in only certain organs of the plant can be explained in terms of enzyme specificity and substrates. Schwab (2003), in a review of metabolome diversity, concluded that diversity of metabolites is caused by low enzyme specificity but availability of suitable substrates due to compartmentation has also been taken into account.

It has been documented that in Anacardiaceae, alkylcatechols are toxic and repellent, and hence an effective defense system against herbivory by insects (Farrell & al., 1991). The diversification of certain groups of insects as a result of a feeding relationship with certain groups of plants has been reported for a number of groups, e.g., Phyllobrotica (Chrysomelidae) and Lamiales (Farrel & Mitter, 1990; Mitter & al., 1991); Blepharida (Chrysomelidae) and Bursera (Becerra, 1997). Among Lamiaceae, species of genera such as Stachys, Physostegia and Scutellaria produce toxic iridoid (ter- penoids) compounds that restrain several herbivores (Farrel & Mitter, 1990). However, species of Phyllobrotica feed on species of these Lamiaceae (Mitter & al., 1991). Phyllobrotica is a genus strictly monophagous (Farrel & Mitter, 1990; Mitter & al., 1991). Bursera species produce pinene, camphene, phelandrene and limonene (terpenes) in resin canals. These terpenes are toxic to most herbivores. However, species of the monophagous genus Blepharida feed on certain Bursera species depending on a specific terpene (Becerra, 1997).

Burckhardt & Basset (2000) indicated that the diver-

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TAXON 53 (2) e May 2004: 357-364 Aguilar-Ortigoza & Sosa * Compounds in Anacardiaceae

sification of the hemipteran genus of insects, Calophya, is closely related to the plants they feed on. Their phylogenetic study of Calophya corroborates such relationships, suggesting that these hemipteran insects are monophagous and only feed on species of the related groups of plants such as Anacardiaceae, Rutaceae and Burseraceae (Burckhardt & Basset, 2000). According to their results, Calophya evodiae feeds on Rutaceae, C. nigrilineata feeds on Burseraceae, C. spondiasiae on Spondias pinnata, C. longispiculata on Buchanania lan- zan, C. rhois on Cotinus coggygria, C. nigridorsalis on Rhus trichocarpa; and more than ten species of Calophya feed on species of Schinus. When the two phy- logenies of Calophya and Anacardiaceae with their closely related groups are compared (Fig. 5), it can be shown that species of Calophya feed mainly on taxa of Rutaceae and Anacardiaceae that are not capable of pro- ducing toxic phenolic compounds such as alkylcatechols. However, Calophya species are capable of feeding on taxa of Burseraceae, Rutaceae and Anacardiaceae that produce biflavonoid and resorcinol phenolic compounds. Most species of Calophya are found to feed on species of Schinus that do not produce alkylcatechols but can synthesize alkylresorcinols and biflavonoids (Fig. 5). Further information is needed to test whether other groups of insects are capable of feeding on Anacardia- ceae that produce alkylcatechols. Bioessays are also needed to confirm feeding preferences of Calophya species.

ACKNOWLEDGEMENTS The project was made possible by a grant from CONACYT

Mexico (225260-5-29378N to VS) and from PROMEP (to CJA-

O). We thank Francisco Lorea for his help in obtaining herbarium

specimens, and Rauil Acevedo, Sergio Avendailo and Santiago Barrios for their help with field work. We are grateful to Bianca Delfosse for editing the English version of this manuscript.

E LITERATURE CITED Adawadkar, P. D. & EISohly, M. A. 1983. An urushiol deriv-

ative from poison sumac. Phytochemistry 22: 1280-1281. Aguilar-Ortigoza, C., Sosa, V. & Aguilar-Ortigoza, M. 2003.

Toxic phenols in various Anacardiaceae species. Econ. Bot. 57: 354-364

Aguilar-Ortigoza, C., Sosa, V. & Angeles, G. 2004. Phylogenetic relationships of three genera in Anacardiaceae: Bonetiella, Pseudosmodingium, and Smodingium. Brittonia 56: 169-184.

Airy Shaw, H. K. 1965. Diagnoses of new families, new names, etc., for the seventh edition of Willis's Dictionary. Kew Bull. 18: 249-273.

Albert, V. A., Williams, S. E. & Chase, M. W. 1992. Carnivorous plants: phylogeny and structural evolution. Science 257: 1491-1495.

Baer, H., Hooton, M., Fales, H., Wu, A. & Schaub, F. 1980. Catecholic and other constituents of the leaves of Toxicodendron radicans and variation of urushiol concen- trations within one plant. Phytochemistry 19: 799-802.

Becerra, J. X. 1997. Insects on plants: macroevolutionary chemical trends in host use. Science 276: 253-256.

Burckhardt, D. & Basset, Y. 2000. The jumping plant-lice (Hemiptera, Psylloidea) associated with Schinus (Anacardiaceae): systematics, biogeography and host plant relationships. J. Nat. Hist. 34: 57-155.

Carpenter, R. C., Sotheeswaran, S., Sultanbawa, M. U. & Balasubramaniam, S. 1980. (-)-5-methylmellein and catechol derivatives from four Semecarpus species. Phytochemistry 19: 445-447.

Cojocaru, M., Droby, S., Glotter, E., Goldman, A., Gottlieb, H. E., Jacoby, B. & Prusky, D. 1986. 5-(12- Heptadecenyl) - resorcinol, the major component of the antifungal activity in the peel of mango fruit. Phytochemistry 25: 1093-1095.

Corthout, J., Janssens, J., Pieters, L., Vanden Berghe, D. & Vlietninck, A. J. 1989. The isolation of a long chain phenol from Spondias mombin. Planta Med. 55: 112-113.

Di Lullo, 0. 1934. El paaji une nouvelle dermatite veneneuse. Revue Sud-American Mkdicine 5: 513.

Doyle, J. J. & Doyle, J. L. 1987. A rapid DNA isolation pro- cedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19: 11-15.

Du, Y., Oshima, R. & Kumanotani, J. 1984. Reversed-phase liquid chromatographic separation and identification of constituents of urushiol in the sap of the lac tree, Rhus ver- nicifera. J. Chromatogr. 284: 463-467.

Eggers, S. H. 1974. Vesicant principles of Smodingium argutum (Anacardiaceae). J. South African Chem. Inst. 27: 99-104.

Engler, A. 1883. Anacardiaceae. Pp. 171-546 in: Candolle, A. P. de & Candolle, A. C. de (eds.), Monographia Phanero- gamarum, vol. 4. G. Masson. Paris.

Evans, F. J. & Schmidt, R. J. 1980. Plants and plant products that induce contact dermatitis. Pl. Med. 38: 289-316.

Farrel, B. D., Dussourd, D. E. & Mitter, C. 1991. Escalation of plant defense: Do latex and resin canals spur plant diversification? Amer Naturalist 138: 881-900.

Farrel, B. D. & Mitter, C. 1990. Phylogenesis of insect/plant interactions: Have Phyllobrotica leaf beetles (Chrysomelidae) and the lamiales diversified in parallel? Evolution 44: 1389-1403.

Farris, J. S., Albert, V. A., Kallersjd, M., Lipscomb, D. & Kluge, A. G. 1996. Parsimony jackknifing outperforms neighbor-joining. Cladistics 12: 99-124.

Fernando, E. S., Gadek, P. A. & Quinn, C. J. 1995. Simaroubaceae, an artificial construct: evidence from rbcL sequence variation. Amer J. Bot. 82: 92-103.

Fitch, W. M. 1971. Toward defining the course of evolution: minimum change for a specific tree topology. Syst. Zool. 20: 406-416.

Furth, D. G. & Young, D. A. 1988. Relationships of herbivore feeding and plant flavonoids (Coleoptera: Chrysomelidae and Anacardiaceae: Rhus). Oecologia (Berlin) 74: 496-500.

363



Aguilar-Ortigoza & Sosa * Compounds in Anacardiaceae TAXON 53 (2) o May 2004: 357-364

Gadek, P. A., Fernando, E. S., Quinn, C. J., Hoot, S., Terrazas, T., Sheahan, M. & Chase, M. W. 1996.

Sapindales: molecular delimitation and infraordinal

groups. Amer J. Bot. 83: 802-811. Gambaro, V., Chamy, M. C., Von Brand, E. & Gambarino,

J. A. 1986. 3-(pentadec-10-enyl)-catechol, a new aller-

genic compound from Lithraea caustica (Anacardiaceae). Pl. Med 44: 20-22.

Gross, M., Baer, H. & Fales, H. M. 1975. Urushiols of poisonous Anacardiaceae. Phytochemistry 14: 2263-2266.

Gunter, L. E., Kochert, G. & Giannasi, D. E. 1994.

Phylogenetic relationship of the Juglandaceae. Pl. Syst. Evol. 192: 11-29.

Harborne, J. B. 1999. Classes and function of secondary products from plants. Pp. 17-19 in: Walton, N. J. & Brown, D. E. (eds.), Chemicals from Plants. Imperial College Press, London.

Hemsley, W. B. 1908. On the Julianiaceae: a new natural order of plants. Philos. Trans. Ser. B 199: 167-197.

Hodkinson, J. D. 1989. The biogeography of the Neotropical jumping plant-lice (Insecta: Homoptera: Psylloidea). J. Biogeography 16: 203-217.

Joel, D. M. 1980. Resin ducts in the mango fruit: a defense system. J. Exp. Bot. 31: 1707-1718.

Maddison, D. R. 1991. The discovery and importance of mul-

tiple islands of most-parsimonious trees. Syst. Zool. 40: 315-328.

Maddison, W. P. & Maddison, D. R. 1992. MacClade:.

Analysis of Phylogeny and Character Evolution, version 3.0. Sinauer, Sunderland, Massachusetts.

Metcalf, C. R. & Chalk, L. 1950. Anatomy of the

Dicotyledons. Clarendon Press, London. Miller, A. J., Young, D. A. & Wen, J. 2001. Phylogeny and

biogeography of Rhus (Anacardiaceae) based on ITS

sequence data. Int. J. PI. Sci. 162: 1401-1407. Mitchell, J. D. 1990. The poisonous Anacardiaceae genera of

the world. Advances Econ. Bot. 8: 103-129. Mitter, C., Farrel, B. & Futuyma, D. J. 1991. Phylogenetic

studies of insect-plant interactions: insights into the gene- sis of diversity. Trends Ecol. & Evol. 6: 290-293.

Morton, J. F. 1978. Brazilian pepper-its impact on people, animals and the environment. Econ. Bot. 32: 353-359.

Morton, J. F. 1981. Anacardiaceae. Pp. 469-479 in: Morton, J.F. (ed.) Atlas of Medicinal Plants of Middle America. Bahamas to Yucatan. Charles C. Thomas, Illinois.

Pell, S. K. & Urbatsch, L. 2001. Evaluation of evolutionary relationships in Anacardiaceae using matK sequence data.

Botany 2001. Plants and People. August 12-16, Albuquerque New Mexico. Abstract 142.

Rivero-Cruz, J. F., Chaivez, D., Hernindez, B., Anaya, A. L. & Mata, R. 1997. Separation and characterization of Metopium brownei urushiol components. Phytochemistry 45: 1003-1008.

Savolainen, V., Chase, M. W, Hoot, S. B., Morton, C. M., Soltis, D. E., Bayer, C., Fay, M. F., De Brulin, A. Y., Sullivan, S. & Qui, Y. L. 2000b. Phylogenetics of flower- ing plants based on combined analysis of plastid atpB and rbcL gene sequences. Syst. Biol. 49: 306-362.

Savolainen, V., Fay, M. F., Albach, D. C., Backlund, A., Van der Bank, M., Cameron, K. M., Johnson, S. A., Lledo, M. D., Pintaud, J. C., Powell, M., Sheahan, M. C., Soltis, D. E., Soltis, P. S., Weston, P., Whitten, W. M.,

Wurdack, K. J. & Chase, M. W. 2000a. Phylogeny of the eudicots: a nearly complete familial analysis based on rbcL gene sequences. Kew Bull. 55: 257-309.

Schwab, W. 2003. Metabolome diversity: too few genes, too

many metabolites. Phytochemistry 62: 837-849. Smith, P. M. 1976. The Chemotaxonomy of Plants. Edward

Arnold, London. Soltis, D. E., Soltis, P. S., Chase, M. W., Mort, M. E.,

Albach, D. C., Zanis, M., Savolainen, V., Hahn, W. H., Hoot, S. B., Fay, M. F., Axtell, M., Swensen, S. M., Prince, L. M., Kress, W. J., Nixon, K. C. & Farris, J. S. 2000. Angiosperm phylogeny inferred from 18S rDNA, rbcL, and atpB sequences. Bot. J. Linn. Soc. 133: 381-461.

Swofford, D. L. 2000. PA UP*: Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4.0b2. Sinauer, Sunderland, Massachusetts.

Terrazas, T. 1994. Wood Anatomy of the Anacardiaceae: Ecological and Phylogenetic interpretations. Ph.D. Thesis, Univ. North Carolina, Chapel Hill.

Terrazas, T. & Chase, M. W. 1996. A phylogenetic analysis of Anacardiaceae based on morphology, anatomy and rbcL

sequence data. Amer J. Bot. 83, (suppl.): 197-198. [Abstr.]

Tyman, J. H. & Morris, L. J. 1967. The composition of cashew nut-shell liquid (CNSL) and the detection of a novel phenolic ingredient. J. Chromatogr 27: 287-288.

Van Sumere, C. F. 1989. Phenols and phenolic acids. Pp. 29-73 in: Dey, P. M. & Harborne, J. B. (eds.), Methods in Plant Biochemistry (Plant Phenolics), vol. 1. Academic Press, London.

Wannan, B. S. & Quinn, C. J. 1988. Biflavonoids in the Julianaceae. Phytochemistry 27: 31-62.

Wannan, B. S. & Quinn, C. J. 1990. Pericarp structure and

generic affinities in the Anacardiaceae. Bot. J. Linn. Soc. 102: 225-252.

Wannan, B. S. & Quinn, C. J. 1991. Floral structure and evolution in Anacardiaceae. Bot. J. Linn. Soc. 107: 349-385.

Wannan, B. S., Waterhouse, J. T., Gadek, P. A. & Quinn, C. J. 1985. Biflavonyls and the affinities of Blepharocarya. Biochem. Syst. Ecol. 13: 105-108.

Young, D. A. 1976. Heartwood flavonoids and the infragener- ic relationships of Rhus (Anacardiaceae). Amer J. Bot. 66: 502-510.

Young, D. A. & Aist, S. J. 1987. Biflavonoids and the taxonomy of the Anacardiaceae. Amer J. Bot. 74: 705. [Abstr.]

Yuh-Meei, L., Fa-Ching, C. & Kuo-Hsiung, L. 1989. Hinokiflavone a cytotoxic principle from Rhus suc- cedanea and the cytotoxicity of the related biflavonoids. Pl. Med. 55: 166-168

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