Annals of the Missouri Botanical Garden [electronic resource] - CSIC

POME ANATOMY OF Juan Jost Aldasoro, 2 Carlos Aedo 1 and 

Carmen Navarr° 3 

ROSACEAE SUBFAM. 

MALOIDEAE, WITH SPECIAL 

REFERENCE TO PYRUS 1 

Abstract 

Two anatomical features of the pome in Kosaceae subfam. Maloideae are investigated: sclereid type and epidermal 

structure. The large and irregular groups of sclereids in Pyrus are different from those in Sorbin subgenera Aria, 

Chamaemespilus, and Cormus, and similar to those in Cydonia. In addition, multilavered epidermis, hitherto unreported 

from Pyrus, is documented in Pyrus sect. Pashia. Consequently, both the monophyly of Pyrus and its current sectional 

classification are supported. 

The taxonomy of Rosaceae subfam. Maloideae is styles (free in Pyrus). This feature is consistent, but 

problematic in terms of generic- delimitation. The may be difficult to evaluate in practice. Thus, Bai- 

inconsistency of the main generic characters has ley (1949) reported the structure of the flower clus- 

generated a great deal of disagreement in the tax- ter as the most obvious distinction between Pyrus 

onomic treatment of the group. A representative of and Malus: the Pyrus inflorescence has a rachis 

the more synthetic view was de Candolle (1825), from which the pedicels emerge, while that of Malwho 

included in Pyrus species now usually referred us has an umbellate structure. Nevertheless, Rob- 

to Malus, Photinia, Eriolobus, and Sorbus. This ertson et al. (1991) showed that both Pyrus and 

classification was followed by Sax (1931) and Rob- Malus could have corymbs, panicles, or umbels, 

ertson (1974). Conversely, Decaisne (1874) and Finally, the supposed scarcity or absence of sc-ler- 

Koehne (1890) used smaller generic concepts. They eids in the pomes of Malus was contested by sev- 

treated Pyrus in a more restricted sense, and split eral authors, including Rehder (1940), Browicz 

off Photinia, Malus, and Sorbus. A comprehensive (1969), Terpo (1968), and Iketani and Ohashi 

review of taxonomic treatments applied to these (1991). Robertson et al. (1991) reported that Malus 

genera was provided by Robertson et al. (1991). may have abundant sclereids under the skin and 

Malus, Cydonia, Sorbus subg. Aria Pers., and around the core of the pomes. Hybridization and 

Sorbus subg. Chamaemespilus (Medik.) K. Koch grafting experiments provide additional data about 

have all been advanced as close relatives of Pyrus Pyrus relationships. According to Taylor (1983) Py- 

(Weber, 1964; Iketani & Ohashi, 1991; Campbell rus and Malus do not hybridize and cannot be graft- 

et al., 1995). According to Decaisne (1874), pomes ed one to the other. They also differ in flavonoid 

ol both Sorbus subg. Aria and S. subg. Chamae- composition (Williams, 1982). However, Weber 

mespilus are characterized by their heterogeneous (1964) and Robertson (1974) reported that Pyrus, 

flesh. Flesh heterogeneity of pomes in subfamily Malus, and Cydonia can and do hybridize among 

Maloideae was studied by Kovanda (1961) and Ike- themselves. 

tani and Ohashi (1991), who showed that it was According to Rohrer et al. (1991: 78), the skin 

caused by groups of parenchyma cells filled with of the pomes of subfamily Maloideae "consists of a 

tannic- substances. Cydonia, formerly included in single epidermal layer of tightly packed, anticlin- 

Pyrus by Linnaeus (1753), and closely related to it ally flattened, rectangular cells covered with a cu- 

according to Robertson et al. (1991), is easily dis- tide." Such an epidermal structure has been detinguishable 

by its solitary flowers and numerous scribed for Crataegus (Akhunova, 1986), Malus 

ovules per locule. Malus is separated by its connate (Clements, 1935), and Amelanchier (Olson & 

' The authors thank M. Jerez for aiding with photographic and microscopic preparations. Gines Lopez, N. Taylor, S. 

Spongberg. and the editors are thanked lor helpful criticisms of the manuscript. We are also indebted to the curators 

of the Royal Botanic Gardens, Kew. University of Liverpool Botanic Gardens (NSS), Sir Harold Hillier Gardens and 

Arboretum. U.K., and Wakehurst Garden for their kind permission to collect living materials. 

- Real Jardfn Botanico, Consejo Superior de Investigaciones Cientfficas, Pla/.a de Murillo 2. 28014 Madrid, Spain 

(e-mail address: aedo(o'ma-rjb. csic.es). 

1 

Departamento de Biologfa Vegetal II. Facultad de Karmacia. Universidad Complutense. 2H040 Madrid. Spain. 

Ann. Missouri Bot. Card. 85: 518-527. 1998.

Volume 85, Number 3 

1998 

Steeves, 1982). On the other hand, Miller (1984) 

reported a multilayered epidermis in Mespilus ger- 

manica L. Our survey of anatomical characteristics 

of pomes of subfamily Maloideae has documented 

the occurrence of a multilayered epidermis in both 

Pyrus and Sorbus torminalis (Aldasoro et al., 1998). 

The supraspecific taxonomy of Pyrus is also con- 

troversial. Decaisne (1871—1872) recognized 23 

species arranged in six informal groups. Koehne 

(1890) described two sections: Pashia and Achras. 

Fedorov (1954) recognized four sections: Pashia, 

Pynis (— sect. Achras Koehne), Xeropyrenia Fed., 

and Argyromalon Fed. Tuz (1972) reduced these to 

two, Pashia and Pyrus, each with several subsec- 

tions. Terpo (1985) added his section Pontica, but 

the classification of Tuz (1972) was accepted by 

Browicz (1993), who pointed out that the two sec- 

tions could be distinguished by certain obscure 

characters. According to Browicz (1993) the more 

operative ones are: the sepal persistence on the 

pome, the presence or absence of whitish lenticels, 

and the thickness and flexibility of the pedicels in 

fruit. The character states of section Pyrus are: se- 

pals persistent, white lenticels absent, and thick, 

stiff pedicels; and of section Pashia: sepals decid- 

uous, white lenticels present, and thin, flexible 

pedicels. Nevertheless, these characters showed 

some inconsistency; for example, several species of 

section Pashia may have thick pedicels. 

The aim of the present work is to investigate 

some anatomical features of subfamily Maloideae 

pomes with special reference to Pyrus, and to dis- 

cuss their bearing on the taxonomic issues detailed 

above. The currently accepted concept of Pyrus is 

that of Decaisne (1874), and the sectional division 

of the genus that proposed by Tuz (1972), because 

they are better supported by morphological and an- 

atomical data (Robertson et al., 1991; Browicz, 

1993; Aldasoro et al., 1996). 

Material and Methods 

Pomes were collected (see Table 1) and pre- 

served in Kew mixture (Forman & Bridson, 1989). 

They were cut with a razor blade both longitudi- 

nally and transversely in order to examine the in- 

ternal structure. Thin hand-cuts were taken in the 

proximal third of the pome and photographed by 

light microscopy. Other cuts were made with a 

SLEE-MAINZ-MTC microtome and stained with 

Fasga mixture (Tolivia & Tolivia, 1987). In some 

cuts, malachite green was used to stain the scler- 

eids. For scanning microscopy, dried pomes were 

cut, glued to aluminum stubs, coated with 40—50 

Aldasoro et al. 

Pome Anatomy of Rosaceae 

519 

nm gold and examined in a JEOL-TSM T330A 

scanning electron microscope at 20 kV. 

Results 

Usually, sclereids are present in the flesh of 

pomes of subfamily Maloideae. They may occur un- 

der the skin, in the core or spread throughout the 

flesh, isolated or in groups, and vary considerably 

in shape and size. 

Four main sclereid types could be distinguished 

in the flesh (Table 1): isolated sclereids, as in Rhaphiolepis; 

small groups (less than 10), as in Ame- 

lanchier, Chaenomeles, Cotoneaster, Crataegus, Er- 

iobotrya, Malus, Photinia, and Sorbus subgenera 

Sorbus and Torminaria; large but irregular groups, 

as in Pyrus (Fig. 1A, B) and Cydonia; and large 

and rounded groups, as in Sorbus subgenera Aria, 

Chamaemespilus, and Cormus (Fig. 1C, D). 

The groups of sclereids in Pyrus and Cydonia 

are remarkably dense (over 50 sclereids can be 

counted in an equatorial section) and have an ir- 

regular outline, while in Sorbus subgenera Aria, 

Chamaemespilus, and Cormus they comprise less 

than 40 sclereids and have an elliptic outline (Fig. 

1C, D). Some consistent differences in the size and 

shape of these sclereids were observed (Table 1). 

Pyrus and Cydonia sclereids are smaller and have 

a smaller lumen (40—80 fixa long; lumen diameter 

10—51 fxm; wall thickness 10-20 p,m) than those 

of Sorbus subgenera Aria, Chamaemespilus, and 

Cormus (110—240 fua long; lumen diameter 76— 

180 pan; wall thickness 6-32 ju.ni) (Fig. 1). Scler- 

eids in pomes of Malus were isolated or in small 

groups, and were larger and with a greater lumen 

diameter (75—360 pun long; lumen diameter 12— 

310 /i.m; wall thickness 15—80 /u,m) than those of 

Pyrus pomes. 

We were able to study the pomes of 16 of the 38 

species of Pyrus accepted by Browicz (1993): 9 be- 

longing to section Pyrus, and 7 to section Pashia 

(Table 1). A multilayered epidermis was found only 

in Pyrus sect. Pashia, while species of section Py- 

rus had only a single layer of epidermal cells that 

produced a thick cuticle (Fig. 2C, D). The remain- 

ing species of subfamily Maloideae showed a sin- 

gle-layered epidermis, except for Mespilus german- 

ica and Sorbus torminalis (Table 1; Miller, 1984; 

Aldasoro et al., 1998). 

In Pyrus, the multilayered epidermis has 3—6 

layers of cells, each layer with a cuticular membrane. 

These cells are tangentially compressed and 

filled with tannic substances (Fig. 2A, B). They de- 

velop from a tangential meristem layer that is some- 

what similar to the phellogen, a meristem that ap-

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Figure 2. SEM and optical photomicrographs of the epidermis in Pyrus pomes. —A. SEM photomicrograph of Pyrus 

pashia (Aldasoro 641) showing the multilayered epidermis (me) and the hypodermis (h). —B. Optical photomicrograph 

of P. pashia (Aldasoro 641) showing the multilayered epidermis (me) and the hypodermis (h). —C. SEM photomicrograph 

of P. spinosa (Navarro et al. 1405) showing the one-layered epidermis (e). the cuticle (c) and the hypodermis (h). —I). 

Optical photomicrograph of P. spinosa (Navarro et al. 1405) showing the one-layered epidermis (e), the cuticle (c) and 

the hypodermis (h). Scale bars: A = 10 p,m\ B: 25 pm; C: 5 jxm; I): 20 pm. 

525



pears in the subepidermal region of the incipient 

lentieel. Like the phellogen, the tangential meri- 

stem of the multilayered epidermis divides peri- 

clinally, producing layers of cells that undergo a 

progressive exfoliation. In some cases, it was ob- 

served that lentieel concrescence occurred prior to 

the development of a multilayered cuticle. 

Discussion 

The hypothesis that Pyrus and Cydonia are sister 

taxa was advanced by Rohrer et al. (1994) on the 

basis of a single presumed synapomorphy: a pit in 

the floral cup surrounding the style group. The data 

contributed by Campbell et al. (1995) on ITS DNA 

sequences also support this view. Our studies show 

that these genera have sclereids similar in size, 

structure, and arrangement, which strengthens this 

idea. However, several other characters uphold the 

continued recognition of Cydonia and Pyrus as sep- 

arate genera: Cydonia has pluriovulate carpels, 

leaves with no adaxial glands, and solitary, pink 

flowers. In contrast, Pyrus has biovulate carpels, 

adaxial leal glands, and corymbose, white flowers. 

Iketani and Ohashi (1991), Sterling (1966a, b), and 

Kalkman (1988) proposed that Pyrus may have 

branched from the ancestor of Cydonia before the 

latter acquired the pluriovulate condition. Thus, the 

previously mentioned characters would support the 

monophyly of Pyrus sensu Decaisne (1874). This 

would be of remarkable interest in subfamily Ma- 

loideae, the genera of which have rather few apo- 

morphic character states. However, our data do not 

support a close relationship between Pyrus and 

Malus, since they have different types of sclereid 

groups. 

The distribution of the multilayered pome epi- 

dermis in Pyrus seems to support the infrageneric 

classification proposed by Tuz (1972) and Browicz 

(1993), at least in terms of the sectional division. 

This is interesting because, as mentioned previous- 

ly, some of Browicz's sectional characters, such as 

pedicel thickness, are variable: the pedicels of P. 

pyrifolia and P. pashia (sect. Pashia) are thicker 

than those of some species in section Pyrus. 

Some other taxa of subfamily Maloideae {Mespi- 

lus, Sorbus) may also have a multilayered pome epi- 

dermis. According to Phipps et al. (1991) and 

Campbell et al. (1995), Mespilus, Pyrus, and Sorbus 

(subg. Torminaria) are not closely related. More- 

over, pomes with a multilayered epidermis were not 

present in any of the primitive genera of Maloideae 

studied (i.e., Cotoneaster, Eriobotrya, Heteromeles, 

Photinia, and Rhaphiolepis; primitive according to 

Phipps et al., 1991; Campbell et al., 1995). Con- 

sequently, a multilayered epidermis is most parsi- 

moniously viewed as derived, and it seems an in- 

dependently acquired character state in these 

genera. The adaptative role of the multilayered epi- 

dermis is unknown, but it may be related to seed 

dispersal by mammals. All pomes of subfamily Ma- 

loideae studied with a multilayered epidermis pre- 

sent traits associated with mammalian zoochory 

syndromes: green or brown skin inconspicuous to 

birds, copious lenticels permitting scent to ema- 

nate, seeds protected against mammal-stomach gas- 

tric juices by many sclereids, tannins inhibiting 

bacterial or fungal damage in the ground, and high 

fiber content (Herrera, 1989). 

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1998 

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