全 文 ：植 物 分 类 学 报 43(3): 210–224(2005) doi:10.1360/aps040099
Acta Phytotaxonomica Sinica http://www.plantsystematics.com
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Received: 20 August 2004 Accepted: 10 January 2005
Supported by the National Program for R & D Infrastructure and Facility Development (2004DKA30430)), and the Knowledge
Innovation Program of the Chinese Academy of Sciences (Grant No. KSCX2-10106B).
* Author for correspondence. E-mail: .
Comparative morphology of leaf epidermis in Parnassia
(Parnassiaceae) from China
1, 2WU Ding 1WANG Hong 1,2LU Jin-Mei 1LI De-Zhu*
1 (Laboratory of Biodiversity and Plant Biogeography, Kunming Institute of Botany, the Chinese Academy of Sciences,
Kunming 650204, China)
2 (Graduate School of the Chinese Academy of Sciences, Beijing 100039, China)
Abstract Epidermal characters of mature leaves in 30 species representing all the nine
sections of Parnassia (Parnassiaceae) were investigated under both light microscope (LM) and
scanning electron microscope (SEM). The stomata were anomocytic and existed on abaxial
epidermis in all the species examined, and on the adaxial epidermis in some species. The leaf
epidermal cells were usually irregular or polygonal in shape. The patterns of anticlinal walls
were slightly straight, repand or sinuate. Under SEM, the inner margin of the outer stomatal
rim was nearly smooth, sinuolate or sinuous, and the cuticular membrane of the leaf epidermis
was striate, sometimes striate to wrinkled, occasionally granular or foveolate. Stomatal and
other epidermal features in Parnassia appear to be constant within species, and thus can be
used for distinguishing some species. Leaf epidermal features show that Parnassia is a quite
natural genus. The previous reports that the stomata are anomocytic and occur only abaxially
in Parnassia, yet occur both adaxially and abaxially in Lepuropetalon are not confirmed by
this study, which, based on more extensive study, has shown that some species of Parnassia
also exhibited stomata on both adaxial and abaxial sides. Evidence from leaf epidermis,
together with that from floral anatomy and pollen morphology as well as biogeography,
suggests that section Saxifragastrum may be heterogeneous. Parnassia delavayi should be
treated as a section of its own, i.e. section Xiphosandra based on morphological, cytological
and leaf epidermal data.
Key words Parnassia, leaf epidermis, systematic significance.
Parnassia L. is a genus of perennial herbs in wetland, consisting of over 70 species
distributed in the arctic-alpine regions of the northern hemisphere, primarily in southeast and
central Asia (Ku, 1987, 1995; Wu et al., 2003). The mountain ranges of southwest China and
the Himalayas constitute the major centre of species diversity, and possibly also the centre of
origin of this genus (Phillips, 1982; Ku, 1987) with approximately 60 species occurring there,
of which about 50 are endemic to China (Ku, 1995; Gu & Hultgård, 2001; Simmons, 2004).
About 10 species in Parnassia are distributed in North America, the second centre of species
diversity of this genus (Phillips, 1982; Wu et al., 2003). The type species, P. palustris L., is
the most widespread one, occurring in North America, Europe, and Asia, and south to
Morocco (Korta, 1972; Phillips, 1982; Simmons, 2004).
Parnassia is a fairly homogeneous genus with unique external morphological characters,
i.e., solitary, terminal, bisexual and pentamerous flowers with antipetalous staminodes.
However, its systematic position has long been in dispute. Although Parnassia was treated as
a family of its own, Parnassiaceae (Gray, 1821) was not commonly recognized until
No. 3 WU Ding et al.: Leaf epidermis in Parnassia (Parnassiaceae) 211
Hutchinson (1969), Thorne (1983), Dahlgren (1983) and Takhtajan (1969, 1997). It has long
been often treated as a subfamily of Saxifragaceae (Engler, 1930; Thorne, 1976; Dahlgren,
1980; Cronquist, 1981; Ku, 1987, 1995; Gu & Hultgård, 2001). Sometimes Parnassia was
included in Parnassioideae in Droseraceae (Drude, 1875; Pace, 1912; Arber, 1913), and
thought to be closely related to Hypericaceae (Arber, 1913; Jay, 1971), or even
Nymphaeaceae (Hallier, 1901). Recent molecular systematic studies have revealed that
Parnassiaceae, including Parnassia and Lepuropetalon Ell., is a sister group of Celastraceae
(Chase et al., 1993; APG, 1998; Soltis et al., 2000; Savolainen et al., 2000; APG II, 2003).
Drude (1875) recognized four sections within Parnassia based on characteristics of the
staminodes, ovary position, and carpel number, i.e. sect. Nectarodroson, sect. Fimbripetalum,
sect. Nectarotrilobos and sect. Saxifragastrum. Based on the connective elongation of the
fertile anthers, the genus was divided into two sections by Franchet (1897), i.e. sect.
Xiphosandra and sect. Amblysandra.. Mainly following Drude’s classification, Engler (1930)
added a fifth section, i.e. sect. Cladoparnassia, and this was followed by Handel-Mazzetti
(1941). Phillips (1982) studied the species of Parnassia in North America, and established a
new section, sect. Longiloba. In the course of preparing an account for the Flora of China, Ku
(1987) made a revision of the Chinese Parnassia, and divided the Chinese species into nine
sections, i.e. sect. Saxifragastrum, sect. Cladoparnassia, sect. Odontohymen, sect. Nectaro-
trilobos, sect. Nectarobilobos, sect. Allolobos, sect. Fimbripetalum, sect. Nectaroquinquelo-
bos and sect. Parnassia. This was adopted in the Flora of China (Gu & Hultgård, 2001). In
their analysis of biogeographic patterns of families and genera of seed plants of China, Wu et
al. (2003) treated Ku’s section Nectaroquinquelobos as a synonym of section Allolobos, but
recognized Franchet’s section Xiphosandra.
Leaf epidermal characteristics are of potential taxonomical importance (Jones, 1986;
Baronova, 1992). However, the leaf epidermis of the Parnassia species has been little studied
(Gornall & Al-Shammary, 1998). This is no exception for China, a centre of distribution of
Parnassia. This paper, as part of a monographic study of this genus in China, is to report the
leaf epidermal features of 30 species from China, of which 16 are endemic to China, and 28
are investigated for the first time with respect to their leaf epidermis.
1 Material and Methods
For practical reason, the sectional system of classification of Ku (1995) was followed.
Mature leaves of 30 species from China, representing all the nine sections within the genus,
were investigated under light microscope (LM) and scanning electron microscope (SEM).
Most samples were obtained from the field in China’s southwestern part (Yunnan, Sichuan
and Guizhou) and northwestern part (Xinjiang), with a few from the Herbarium of the
Kunming Institute of Botany (KUN). All voucher specimens were deposited in KUN (Table
1).
Samples were taken from mature leaves. The materials for LM study were boiled in
water before being macerated in Jeffrey’s solution (Stace, 1965). Pieces of leaf epidermis
were stained in a solution of 1% safranin (in 50% alcohol) before being mounted in glycerine
jelly. To check the constancy of epidermal structure, at least five slides were made from
different parts of a single leaf or from different leaves of the same species. The stomatal index
was calculated using formula S/(E+S)×100%. The materials for SEM observation were
directly mounted on stubs without any treatment, and sputter coated with gold-palladium.
Observations were made using a KYKY-10000B (Science Instrument Company, Beijing)
electronic microscope at 15 kV. Descriptive terminology of leaf epidermis follows Wilkinson
(1979).
Acta Phytotaxonomica Sinica Vol. 43 212
Table 1 Species, localities and vouchers used for the leaf epidermal studies in Parnassia
Taxon Locality Voucher
sect. Saxifragastrum
P. esquirolii Lévl.
P. longipetala Hand.-Mazz.
P. longipetaloides J. T. Pan
P. tenella Hook. f. & Thoms.
P. yunnanensis Franch.
sect. Cladoparnassia
P. faberi Oliv.
sect. Odontohymen
P. farreri W. E. Evans
sect. Nectarotrilobos
P. cacuminum Hand.-Mazz.
P. chinensis Franch.
P. delavayi Franch.
P. epunctulata J. T. Pan
P. laxmanni Pall.
P. mysorensis Heyne ex Wight & Arn.
P. mysorensis var. aucta Diels
P. pusilla Wall. ex Arn.
P. scaposa Mattf.
P. submysorensis J. T. Pan
P. trinervis Drude
P. venusta Jien
P. viridiflora Batalin
P. yui Jien
sect. Nectarobilobos
P. bifolia Nekrass.
sect. Allolobos
P. wightiana Wall. ex Wight & Arn.
P. monochorifolia Franch.
sect. Fimbripetalum
P. amoena Diels
P. foliosa Hook. f. & Thoms.
P. noemiae Franch.
sect. Nectaroquinquelobos
P. gansuensis T. C. Ku
P. perciliata Diels
sect. Parnassia
P. palustris L.

Yiliang, Yunnan
Weixi, Yunnan
Lijiang, Yunnan.
Zhongdian, Yunnan
Dêqên, Yunnan

Mt. Emeishan, Sichuan

Gongshan, Yunnan

Dali, Yunnan
Dali, Yunnan
Lijiang, Yunnan
Qiaojia, Yunnan
Mt.Tianshan, Xinjiang
Qiaojia, Yunnan
Dêqên, Yunnan
Zhongdian, Yunnan
Dali, Yunnan
Zhongdian, Yunnan
Nyingchi, Xizang
Qiaojia, Yunnan
Dêqên, Yunnan
Gongshan, Yunnan

Mt. Tianshan, Xinjiang

Gongshan, Yunnan
Qiaojia, Yunnan

Wenchuan, Sichuan
Jinan, Jiangxi
Mt. Jinfoshan, Chongqing

Zhongdian, Yunnan
Mt. Fanjingshan, Guizhou

Hejing, Xinjiang

D. Wu et al. 0313
C. W. Wang 0208834
D. Wu et al. 0305
D. Wu 0366
H. Wang et al. 03066

D. Wu 0217

L. M. Gao et al. 0319

D. Wu et al. 0326
D. Wu et al. 0203
D. Wu 0204
H. Wang et al. 03890
D. Wu et al. 0331
D. Wu 0210
D. Wu 0201
D. Wu et al. 03028
J. P. Yue 030300
H. Wang et al. 0312
H. Y. Ma 03081
D. Wu et al. 0211
H. Wang et al. 03065
L. M. Gao et al. 2327

D. Wu et al. 0329

L. M. Gao et al. 2318
H. Wang et al. 031082

D. Wu 0215
J. S. Xiong 97380
D. Wu 0218

D. Wu 0209
L. M. Gao et al. 03353

A. J. Li et al. 0208956

No. 3 WU Ding et al.: Leaf epidermis in Parnassia (Parnassiaceae) 213
2 Results
The characteristics of leaf epidermis in Parnassia under LM and SEM are summarized in
Table 2 and Table 3. Stomatal and other epidermal features appear to be constant within
species and thus may be of systematic significance.
2.1 Characteristics of leaf epidermis under LM
2.1.1 Epidermal cells The form of epidermal cells in Parnassia was usually polygonal or
irregular. The shapes of epidermal cells of the same species were different on the adaxial (Ad)
and abaxial (Ab) sides in most species. Some species have similar epidermal cells between the
Ad and Ab sides, such as P. amoena (Ad and Ab, Figs. 17, 39), P. faberi (Ad and Ab, Figs.
18, 43), P. bifolia (Ad and Ab, Figs. 19, 36), P. yunnanensis (Ad and Ab, Figs. 20, 45), P.
venusta (Fig. 21) and P. laxmanni (Fig, 22). In about 2/3 of the total of species studied, the
shape of the adaxial epidermal cells was usually polygonal. The form of the abaxial epidermal
cells was irregular in all the species except in P. monochorifolia (Fig. 23).
The patterns of anticlinal walls of epidermal cells were slightly straight, repand or
sinuate. The pattern of anticlinal cells may vary in different species or between Ad and Ab
epidermis of the same species, and the undulation of anticlinal walls was usually stronger on
the abaxial side and fell into three types, viz., the straight to arched type, which occurred in P.
submysorensis (Ad, Fig. 1), P. delavayi (Ad, Fig. 2), P. chinensis (Ad, Fig. 3), P. yui (Ad,
Fig. 4), P. tenella (Ad, Fig. 5), P. esquirolii (Ad, Fig. 6), P. noemiae (Ad, Fig. 7), P.
perciliata (Ad, Fig. 8), P. monochorifolia (Ad and Ab, Figs. 9, 23), P. farreri (Ad, Fig. 10), P.
palustris (Ad, Fig. 11) and P. gansuensis (Ad, Fig. 12); the slightly undulate (or repand) type,
which occurred in P. longipetaloides (Ad, Fig. 13), P. cacuminum (Ad and Ab, Figs. 14, 24),
P. epunctulata (Ad, Fig. 15) and P. wightiana (Ad, Fig. 16); and the strongly sinuous type,
which occurred in P. amoena (Ad and Ab, Figs.17, 39), P. faberi (Ad and Ab, Figs. 18, 43),
P. bifolia (Ad and Ab, Figs. 19, 36), P. yunnanensis (Ad and Ab, Figs. 20, 45), P. venusta
(Ad, Fig. 21), P. laxmanni (Ad, Fig. 22), P. mysorensis (Ab, Fig. 25), P. longipetala (Ab, Fig.
26), P. tenella (Ab, Fig. 27), P. yui (Ab, Fig. 28), P. trinervis (Ab, Fig. 29), P. scaposa (Ab,
Fig. 30), P. viridiflora (Ab, Fig. 31), P. pusilla (Ab, Fig. 32), P. mysorensis var. aucta (Ab,
Fig. 33), P. palustris (Ab, Fig. 34), P. perciliata (Ab, Fig. 35), P. foliosa (Ab, Fig. 37), P.
noemiae (Ab, Fig. 38), P. gansuensis (Ab, Fig. 40), P. wightiana (Ab, Fig. 41), P. farreri (Ab,
Fig. 42) and P. esquirolii (Ab, Fig. 44).
2.1.2 Stomatal apparatus Stomata in all species studied were anomocytic. Stomata
existed on the abaxial epidermis in all species, but were absent on the adaxial epidermis in
most species. Of all the materials observed, stomata were found on both adaxial and abaxial
sides in seven species, viz., P. bifolia (Fig. 19), P. esquirolii (Fig. 6), P. faberi (Fig. 18), P.
palustris (Fig. 11), P. tenella (Fig. 5), P. trinervis (Fig. 29) and P. yunnanensis (Fig. 45).
The size of stomata was (32.2-56.8)×(27.5-50.2) µm. The species in sect. Fimbripeta-
lum had larger stomata than those of other sections. For example, the stomata in P. noemiae
were obviously larger than those in P. chinensis and P. cacuminum. The stomatal density was
also different among species. The stomatal index ranged from 37.5% in P. monochorifolia,
with the stomata being densely distributed, to 11.6 % in P. venusta, with the stomata being
sparsely distributed. Furthermore, stomata of the adaxial epidermis were smaller and sparser
than those of the abaxial side.
2.2 Characteristics of leaf epidermis under SEM
2.2.1 Guard cells The outlines of the pair of guard cells were usually suborbiculate to widely
elliptic as seen in surface view, with length/width (L/W) ratio 1.1-1.5:1. Guard cells often
thickened to a certain extent, and were made up of outer stomatal ledges or rims. Three types of the
rim of outer stomatal ledge or rim were observed: nearly smooth, sinuolate to erose, and sinuous.
Acta Phytotaxonomica Sinica Vol. 43 214
Table 2 The characters of leaf epidermis of Parnassia under LM
Taxon Adaxial epidermis Abaxial epidermis Figure
Shape of
cells
Pattern of
anticlinal
walls
Shape of
ordinary
cells
Pattern of
anticlinal
walls
Size of
stomata
(µm2)
Stomatal
index

sect. Saxifragastrum
P. esquirolii Pol Str-arc Irr Sin 47.2×39.0 22.7 6, 44
P. longipetala Pol Str-arc Irr Rep 41.6×34.5 16.9 26
P. longipetaloides Irr Rep Irr Sin 41.5×36.6 23.1 13
P. tenella Pol Str-arc Irr Sin 56.6×49.0 15.6 5, 27
P. yunnanensis Irr Sin Irr Sin 47.9×34.2 28.9 20, 45
sect. Cladoparnassia
P. faberi Irr Sin Irr Sin 47.3×46.9 20.7 18, 43
sect. Odontohymen
P. farreri Pol Str-arc Irr Sin 42.8×35.1 19.4 10, 42
sect. Nectarotrilobos
P. cacuminum Irr Rep Irr Rep 32.8×29.2 14.7 14, 24
P. chinensis Pol Str-arc Irr Rep 32.2×29.1 29.4 3
P. delavayi Pol Str-arc Irr Sin 47.8×41.6 27.8 2
P. epunctulata Irr Rep Irr Sin 35.2×31.9 18.2 15
P. laxmanni Irr Sin Irr Sin 40.1×36.7 17.9 22
P. mysorensis Pol Str-arc Irr Rep 42.9×37.8 23.7 25
P. mysorensis var. aucta Pol Str-arc Irr Sin 41.9×34.8 28.6 33
P. pusilla Pol Str-arc Irr Sin 34.5×28.2 31.1 32
P. scaposa Pol Str-arc Irr Sin 43.5×32.8 31.2 30
P. submysorensis Pol Str-arc Irr Sin 41.1×33.2 24.2 1
P. trinervis Pol Str-arc Irr Sin 38.0×33.3 20.7 29
P. venusta Irr Sin Irr Sin 42.6×33.8 11.6 21
P. viridiflora Pol Str-arc Irr Sin 44.9×37.7 15.4 31
P. yui Pol Str-arc Irr Sin 40.7×34.1 14.3 4, 28
sect. Nectarobilobos
P. bifolia Irr Sin Irr Sin 54.5×47.3 13.3 19, 36
sect. Allolobos
P. wightiana Irr Rep Irr Sin 44.2×36.5 27.3 16, 41
P. monochorifolia Pol Str-arc Pol Str-arc 37.2×34.8 37.5 9, 23
sect. Fimbripetalum
P. amoena Irr Sin Irr Sin 48.5×41.8 22.7 17, 39
P. foliosa Pol Str-arc Pol Str-arc 40.0×33.7 37.2 37
P. noemiae Pol Str-arc Irr Sin 56.8×50.2 21.1 7, 38
sect. Nectaroquinquelobos
P. gansuensis Pol Str-arc Irr Sin 38.7×27.5 34.4 12, 40
P. perciliata Pol Str-arc Irr Sin 48.9×33.2 19.5 8, 35
sect. Parnassia
P. palustris Pol Str-arc Irr Sin 40.3×37.8 19.6 11, 34
Irr=irregular; Pol=polygonal; Str-arc=straight to arched; Rep=repand; Sin=sinuous.



No. 3 WU Ding et al.: Leaf epidermis in Parnassia (Parnassiaceae) 215
Table 3 The characters of leaf abaxial epidermis of Parnassia under SEM
Taxon Cuticular membrane Shape of guard cells
Inner margin of outer
stomatal rim Figure
sect. Saxifragastrum
P. esquirolii
P. longipetala
P. longipetaloides
P. tenella
P. yunnanensis
sect. Cladoparnassia
P. faberi
sect. Odontohymen
P. farreri
sect. Nectarotrilobos
P. cacuminum
P. chinensis
P. delavayi
P. epunctulata
P. laxmanni
P. mysorensis
P. mysorensis var. aucta
P. pusilla
P. scaposa
P. submysorensis
P. trinervis
P. venusta
P. viridiflora
P. yui
sect. Nectarobilobos
P. bifolia
sect. Allolobos
P. wightiana
P. monochorifolia
sect. Fimbripetalum
P. amoena
P. foliosa
P. noemiae
sect. Nectaroquinquelobos
P. gansuensis
P. perciliata
sect. Parnassia
P. palustris

striate and wrinkled
striate
striate and wrinkled
striate
striate and wrinkled

striate and wrinkled

striate

striate
striate
striate
striate
striate and wrinkled
striate and granular
striate
striate
striate and wrinkled
striate
striate
striate and wrinkled
striate and wrinkled
striate

striate and wrinkled

striate
striate and foveolate

striate
striate
striate

striate
striate and wrinkled

striate and wrinkled

widely elliptic
widely elliptic
widely elliptic
widely elliptic
widely elliptic

suborbiculate

widely elliptic

widely elliptic
widely elliptic
widely elliptic
widely elliptic
widely elliptic
widely elliptic
widely elliptic
widely elliptic
widely elliptic
widely elliptic
widely elliptic
widely elliptic
suborbiculate
widely elliptic

widely elliptic

suborbiculate
widely elliptic

widely elliptic
widely elliptic
widely elliptic

widely elliptic
widely elliptic

widely elliptic

sinuous
sinuolate to erose
sinuous
sinuolate to erose
sinuolate to erose

nearly smooth

nearly smooth

sinuolate to erose
sinuolate to erose
nearly smooth
sinuolate to erose
nearly smooth
sinuolate to erose
sinuolate to erose
sinuolate to erose
nearly smooth
sinuous
nearly smooth
sinuolate to erose
sinuolate to erose
nearly smooth

nearly smooth

nearly smooth
sinuolate to erose

nearly smooth
sinuolate to erose
nearly smooth

nearly smooth
nearly smooth

sinuolate to erose

68

67
64
66

49

50, 51


60
58

57
62



69
54




52, 53

48
61


63
55, 56

46, 47
59

65



Acta Phytotaxonomica Sinica Vol. 43 216

Figs. 1-15. Characteristics of adaxial epidermal cells (LM). 1-12. Polygonal cells with straight anticlinal walls. 1.
Parnassia submysorensis. 2. P. delavayi. 3. P. chinensis. 4. P. yui. 5. P. tenella. 6. P. esquirolii. 7. P. noemiae. 8. P.
perciliata. 9. P. monochorifolia. 10. P. farreri. 11. P. palustris. 12. P. gansuensis. 13-15. Irregular cells with repand
anticlinal walls. 13. P. longipetaloides. 14. P. cacuminum. 15. P. epunctulata. Scale bar=50 µm.
No. 3 WU Ding et al.: Leaf epidermis in Parnassia (Parnassiaceae) 217

Figs. 16-30. Characteristics of epidermal cells (LM). 16. Irregular cells with repand anticlinal walls, Parnassia
wightiana (Ad). 17-22. Irregular cells with sinuous anticlinal walls, all Ad. 17. P. amoena. 18. P. faberi. 19. P. bifolia. 20.
P. yunnanensis. 21. P. venusta. 22. P. laxmanni. 23. Polygonal cells with straight anticlinal walls, P. monochorifolia (Ab).
24-26. Irregular cells with repand anticlinal walls, all Ab. 24. P. cacuminum. 25. P. mysorensis. 26. P. longipetala. 27-30.
Irregular cells with sinuous anticlinal walls, all Ab. 27. P. tenella. 28. P. yui. 29. P. trinervis. 30. P. scaposa. Scale bar=50
µm.
Acta Phytotaxonomica Sinica Vol. 43 218

Figs. 31-45. Characteristics of epidermal cells (LM). Irregular cells with sinuous anticlinal walls, all Ab. 31. Parnassia
viridiflora. 32. P. pusilla. 33. P. mysorensis var. aucta. 34. P. palustris. 35. P. perciliata. 36. P. bifolia. 37. P. foliosa. 38. P.
noemiae. 39. P. amoena. 40. P. gansuensis. 41. P. wightiana. 42. P. farreri. 43. P. faberi. 44. P. esquirolii. 45. P.
yunnanensis. Scale bar=50 µm.
No. 3 WU Ding et al.: Leaf epidermis in Parnassia (Parnassiaceae) 219

Figs. 46-57. Characteristics of epidermal surface under scanning electron microscopy (SEM), all Ab. Nearly smooth of
the inner margin of the outer stomatal rim. 46, 47. Parnassia gansuensis. 48. P. wightiana. 49. P. faberi. 50, 51. P. farreri.
52, 53. P. bifolia. 54. P. trinervis. 55, 56. P. noemiae. 57. P. laxmanni. Scale bar=10 µm.
Acta Phytotaxonomica Sinica Vol. 43 220

Figs. 58-69. Characteristics of epidermal surface (SEM), all Ab. 58, 59. Nearly smooth of the inner margin of the outer
stomatal rim. 58. Parnassia delavayi. 59. P. perciliata. 60-66. Sinuolate to erose of the inner margin of the outer stomatal
rim. 60. P. chinensis. 61. P. monochorifolia. 62. P. mysorensis. 63. P. foliosa. 64. P. tenella. 65. P. palustris. 66. P.
yunnanensis. 67-69. Sinuous of the inner margin of the outer stomatal rim. 67. P. longipetaloides. 68. P. esquirolii. 69. P.
submysorensis. Scale bar=10 µm.
No. 3 WU Ding et al.: Leaf epidermis in Parnassia (Parnassiaceae) 221
The first type with nearly smooth inner margin of the outer stomatal rim was found to
occur in 13 species, such as P. gansuensis (Figs. 46, 47), P. wightiana (Fig. 48), P. faberi
(Fig. 49), P. farreri (Figs. 50, 51), P. bifolia (Figs. 52, 53), P. trinervis (Fig. 54), P. noemiae
(Figs. 55, 56), P. laxmanni (Fig. 57), P. delavayi (Fig. 58) and P. perciliata (Fig. 59). The
type with sinuolate to erose inner margin of the outer stomatal rim may represent an interme-
diate one, which was found to occur in 14 species, such as P. chinensis (Fig. 60), P. mono-
chorifolia (Fig. 61), P. mysorensis (Fig. 62), P. foliosa (Fig. 63), P. tenella (Fig. 64), P.
palustris (Fig. 65) and P. yunnanensis (Fig. 66). The sinuous type existed in three species, i.e.
P. longipetaloides (Fig. 67), P. esquirolii (Fig. 68) and P. submysorensis (Fig. 69).
Strikingly tall, upright outer stomatal rims occurred in all species, except in P. delavayi,
in which the stomatal rims were almost at the same level with or slightly lower than the
epidermis. Furthermore, the cuticular thickening of the common wall between the guard cells
was found in some species, such as P. viridiflora (Fig. 31), P. bifolia (Ab, Fig. 36), P.
gansuensis (Ab, Fig. 40), P. esquirolii (Ab, Fig. 44) and P. yunnanensis (Ab, Fig. 45).
2.2.2 Cuticular membrane Hairs were absent on both Ad and Ab of the species
investigated. The cuticular membrane of the leaf epidermis was striate, sometimes striate to
wrinkled, occasionally granular or foveolate. Based on the characters observed on the abaxial
epidermis, three types of the cuticular membrane were found, viz., Type I, smooth to weakly
undulate type,which occurred in P. gansuensis (Fig. 46), P. wightiana (Fig. 48), P. trinervis
(Fig. 54), P. delavayi (Fig. 58) and P. submysorensis (Fig. 69); Type II, striate to wrinkled
type, which occurred in P. faberi (Fig. 49), P. bifolia (Fig. 52), P. laxmanni (Fig. 57), P.
palustris (Fig. 65), P. yunnanensis (Fig. 66), P. longipetaloides (Fig. 67) and P. esquirolii
(Fig. 68); and Type III, striations with granular or foveolate type, which occurred in P.
mysorensis (Fig. 62) and P. monochorifolia (Fig. 61).
3 Discussion
The species observed covered all sections and subsections of Parnassia in Ku’s (1987,
1995) system of classification of the genus. It was shown that the stomata were anomocytic
and existed on abaxial epidermis of all species. This was in consensus with the previous
reports (Gornall & Al-Shammary, 1998). With the exception of P. monochorifolia, the form
of epidermal cells was irregular on the abaxial side. The cuticular membrane of the leaf
epidermis was generally striate. The leaf epidermal features among species were fairly similar
to each other. The features of leaf epidermal showed that Parnassia was a quite natural genus.
Stomata have been previously reported to be anomocytic and only abaxial in Parnassia,
yet both adaxial and abaxial in Lepuropetalon (Gornall & Al-Shammary, 1998). This study,
which is based on more extensive sampling, has shown that many taxa in the genus Parnassia
did have stomata only on the abaxial side, but some species had stomata on both Ad and Ab
sides. The species with adaxial stomata were P. bifolia, P. esquirolii, P. faberi, P. palustris, P.
tenella, P. trinervis and P. yunnanensis, although the stomata were smaller and inconspicu-
ous. The character of the presence of stomata on both sides occurred in different groups not
very closely related, indicating that this character might not have a single origin. P. bifolia, a
very distinct species with 2-lobed flat staminodes and two cauline leaves, was treated as a
section of its own, sect. Nectarobilobos (Ku, 1987, 1995; Wu et al., 2003). Leaf epidermal
features of this species were also distinctive. The stomata occurred on both sides. The form of
the leaf epidermal cells was considerably similar on the Ad and Ab sides, and belonged to the
irregular type. The cuticular thickening of the common wall between the guard cells was also
present in P. bifolia. These features support the segreation of the monotypic section Nectaro-
bilobos.
Acta Phytotaxonomica Sinica Vol. 43 222
In Parnassia, the leaf epidermal cells varied in shape, and diversified in the patterns of
anticlinal walls, especially so on the abaxial side. These variations correlated to a certain
extent with the gross morphology, palynology and biogeography in the genus. There are eight
species in sect. Saxifragastrum, four of which, i.e. P. tenella, P. longipetala, P. longipeta-
loides and P. yunnanensis, were studied here. This section is characterized by having terete,
apically entire, rounded or discoid staminodes. On the abaxial side, the shape of epidermal
cells in P. tenella was polygonal, while irregular in P. yunnanensis. The patterns of anticlinal
walls varied in different species. The anticlinal walls were straight to arched in P. tenella,
slightly undulate (or repand) in P. longipetaloides, and strongly sinuous in P. yunnanensis.
The pollen morphology is inconstant within sect. Saxifragastrum. P. tenella is of foveolate
reticulate exine sculpture of pollen while P. longipetala and P. yunnanensis are of coarsely
reticulate exine sculpture of pollen (Wu et al., 2005). In addition, the section is restricted in
southwest China in distribution, and each species is highly restricted in distributional range
(Phillips, 1982). All species in the section are distributed in higher altitudinal zones of the
Himalayan-Hengduan Mountains region (Wu et al., 2003), which is considered as one of the
world’s “hot spots” of biodiversity (Myers, 1988; Myers et al., 2000). Evidence from leaf
epidermis, just as that from floral anatomy and pollen morphology as well as geographical
distribution, suggests that this section may still be in active differentiation, and may be a
heterogeneous group.
The results of our study show that the characteristics of the leaf epidermis can provide
some anatomical evidence for the classification of Parnassia. Parnassia wightiana is the most
widespread species of the genus in Asia, occurring from northeast India to the Himalayan-
Hengduan Mountains region, and to south-central mountains of China (Wu et al., 2003).
Morphologically, it is also a highly variable species, and the intermediate forms occur in
various regions (Ku, 1987; Gu & Hultgård, 2001; Wu et al., 2003). Ku (1987) described the
populations from southern Gansu as a new species, P. gansuensis. The characteristics of leaf
epidermis support this treatment. The shape of the leaf epidermal cells in P. wightiana was
repand while in P. gansuensis it was straight to arched on the Ad side. The stomatal density
was also different between the two species, with the stomatal index in P. gansuensis being
34.4%, while 27.3% in P. wightiana. In addition, the cuticular thickening of the common wall
between the guard cells was present in P. gansuensis, but absent in P. wightiana. Both mor-
phological and leaf epidermal features indicate that P. gansuensis should be a good species.
The cuticular membrane of the leaf epidermis in all the species studied was striate,
sometimes striate to wrinkled, occasionally granular or foveolate. The characters of the cuticular
membrane of the leaf epidermis could serve as a criterion of distinguishing some species in the
genus, for example P. mysorensis and P. monochorifolia. The former had striate, granular
cuticular membrane while the latter had striate, foveolate cuticular membrane.
Parnassia delavayi has 3-lobed staminodes, and has been placed in sect. Nectarotrilobos
(Drude, 1875; Engler, 1930; Handel-Mazzetti, 1941; Ku, 1987, 1995). Cytological studies
have revealed some variation in the basic chromosome numbers of the genus Parnassia
(Funamoto et al., 1998, 2001). The chromosome number is 2n=14 with x=7 in P. delavayi,
rather than 2n=18 with x=9 and 2n=16 with x=8 as in other species. The epidermal features as
revealed in this study have shown that P. delavayi is quite unique in the genus by having
stomatal rims which were almost at some level with or slightly lower than the epidermis. On
the contrary, all the other species had conspicuously tall and upright outer stomatal rims.
Geographically, P. delavayi is restricted to China and the Himalayas. Morphologically, its
anther connectives elongate beyond the anther sacs. Based on the connective elongation of the
fertile anthers, the genus Parnassia was divided into two sections by Franchet (1897). Therefore,
evidence from morphology, leaf epidermis and cytology strongly suggested that P. delavayi
No. 3 WU Ding et al.: Leaf epidermis in Parnassia (Parnassiaceae) 223
should be treated as a section of its own, i.e. sect. Xiphosandra (Franchet, 1897). This treatment
has also been supported by the biogeographic analysis performed by Wu et al. (2003).
Acknowledgements The authors would like to thank the curator of the Herbarium,
Kunming Institute of Botany, the Chinese Academy of Sciences (KUN), for providing
specimen materials. We are indebted to GAO Lian-Ming, YANG Han-Qi, FAN Xi-Kai and
LIU Jian-Hong for their kind assistances.
References
Angiosperm Phylogeny Group (APG). 1998. An ordinal classification for the families of flowering plants.
Annals of the Missouri Botanical Garden 85: 531-553.
APG II. 2003. An update of the Angiosperm Phylogeny Group classification for the orders and families of
flowering plants. Botanical Journal of the Linnean Society 141: 399-436.
Arber A. 1913. On the structure of the androeceum in Parnassia and its bearing on the affinities of the genus.
Annals of Botany 27: 491-510.
Baranova M A. 1992. Principles of comparative stomatographic studies of flowering plants. The Botanical
Review 58: 49-99.
Chase M W, Soltis D E, Olmstead R G, Morgan D, Les D H, Mishler B D, Duvall M R, Price R A, Hills H G,
Qiu Y L, Kron K A, Rettig J H, Conti E, Palmer J D, Manhart J R, Sytsma K J, Michaels H J, Kress W J,
Karol K A, Clark W D, Hedrén M, Gaut B S, Jansen R K, Kim K J, Wimpee C F, Smith J F, Furnier G R,
Strauss S H, Xiang Q Y, Plunkett G M, Soltis P S, Swensen S M, Williams S E, Gadek P A, Quinn C J,
Eguiarte L E, Golenberg E, Learn G H, Graham S W Jr, Barrett S C H, Dayanandan S, Albert V A. 1993.
Phylogenetics of seed plants: an analysis of nucleotide sequences from the plastid gene rbcL. Annals of
the Missouri Botanical Garden 80: 528-580.
Cronquist A. 1981. The Integrated System of Classification of Flowering Plants. New York: Columbia
University Press.
Dahlgren R M T. 1980. A revised system of classification of the angiosperms. Botanical Journal of the Linnean
Society 80: 91-124.
Dahlgren R M T. 1983. General aspects of angiosperm evolution and macrosystematics. Nordic Journal of
Botany 3: 119-149.
Drude O. 1875. Über die Blüthengestaltung and die Verwandtschaftsverhältnisse der Gattung Parnassia, nebst
einer systematischen Revision seiner Arten. Linnaea 39: 239-324.
Engler A. 1930. Saxifragaceae. In: Engler A, Prantl K eds. Die Natürlichen Pflanzenfamilien. Leipzig:
Wilhelm Engelmann. 18a: 74-225.
Franchet M A. 1897. Les Parnassia de I’Asie orientale. Bulletin de la Société Botanique de France 44:
244-263.
Funamoto T, Kondo K, Hong D-Y, Zhou S-L, Deguchi H. 1998. A chromosome study of three Parnassia
species collected in the Qin-Ling Mountains, Shaanxi Province, China. Chromosome Science 2: 111-115.
Funamoto T, Kondo K, Hong D-Y, Zhou S-L, Ogura H. 2001. Chromosomes in four species of Parnassia
(Saxifragaceae) in the northern part of Sichuan Province, China. Chromosome Science 5: 19-25.
Gornall R J, Al-Shammary K I A. 1998. Parnassiaceae. In: Cutler D F, Gregory M eds. Anatomy of the
Dicotyledons: Saxifragales. Oxford: Clarendon Press. 4: 245-247.
Gray S F. 1821. Parnassieae. A Natural Arrangement of British Plants. New York: Academic Press. 2: 623.
Gu C, Hultgård U M. 2001. Parnassia. In: Wu Z-Y,Raven P H eds. Flora of China. Beijing: Science Press; St.
Louis: Missouri Botanical Garden Press. 8: 358-379.
Hallier H. 1901. Über die Verwandtschaftsverhältnisse der Tubifloren und Ebenalen den polyphyletischen
Ursprung der Sympetalen und Apetalen und die Anordnung der Angiospermen überhaupt. Abhandlungen
Naturwissenschaftlicher Verein zu Bremen 16: 1-112.
Handel-Mazzetti H. 1941. Die Chinesischen Parnassia-Arten. Österreichische Botanische Zeitschrift 90:
127-136.
Hutchinson J. 1969. Evolution and Phylogeny of Flowering Plants. New York: Academic Press.
Jay M. 1971. Quelques problèmes taxinomiques et phylogénétiques des Saxifragacées vus à la lumière de la
biochemie foavonique. Bulletin du Muséum National D`histoire Naturelle 42: 754-775.
Acta Phytotaxonomica Sinica Vol. 43 224
Jones J H. 1986. Evolution of the Fagaceae: the implications of foliar features. Annals of the Missouri
Botanical Garden 73: 228-275.
Korta J. 1972. Anatomical analysis of Parnassia palustris L. Acta Biologica Cracoviensia 15: 31-37.
Ku T C (谷粹芝). 1987. A revision of the genus Parnassia (Saxifragaceae) in China. Bulletin of Botanical
Research (植物研究) 7: 1-59.
Ku T C (谷粹芝). 1995. Parnassioideae. In: Flora Reipublicae Popularis Sinicae (中国植物志). Beijing:
Science Press. 35 (1): 1-66.
Myers N. 1988. Threatened biotas: “hot spots” in tropical forests. Environmentalist 8: 187-208.
Myers R A, Mittermeier C G, Da Fonseca G A B, Kent J. 2000. Biodiversity hotspots for conservation
priorities. Nature 403: 853-858.
Pace L. 1912. Parnassia and some allied genera. The Botanical Gazette 54: 306-328.
Phillips R B. 1982. Systematics of Parnassia (Parnassiaceae): Generic Overview and Revision of North
American Taxa. PhD Dissertation, Berkerley: University of California.
Savolainen V, Chase M W, Hoot S B, Morton C M, Soltis D E, Bayer C, Fay M F, de Bruiji A Y, Sullivan S,
Qiu Y-L. 2000. Phylogenetics of flowering plants based on combined analysis of plastid atpB and rbcL
gene sequences. Systematic Biology 49: 306-362.
Simmons M P. 2004. Parnassiaceae. In: Kubitzki K ed. The Families and Genera of Vascular Plants. Berlin:
Springer. 6: 291-296.
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, Nixon K C, Farris J S. 2000. Angiosperm phylogeny inferred from a
combined data set of 18S rDNA, rbcL, and atpB sequences. Botanical Journal of the Linnean Society
133: 381-461.
Stace C A. 1965. Cuticular studies as an aid to plant taxonomy. Bulletin of the British Museum (Natural
History) Botany 4: 1-78.
Takhtajan A. 1969. Flowering Plants: Origin and Dispersal. Washington: Smithsonian Institution Press.
Takhtajan A. 1997. Diversity and Classification of Flowering Plants. New York: Columbia University Press.
Thorne R F. 1976. A phylogenetic classification of the Angiospermae. Evolutionary Biology 9: 35-106.
Thorne R F. 1983. Proposed new realignments in the angiosperms. Nordic Journal of Botany 3: 225-348.
Wilkinson H P. 1979. Anatomy of the Dicotyledons. 2nd ed. Oxford: Clarendon Press. 97-165.
Wu D, Wang H, Li D-Z, Blackmore S. 2005. Pollen morphology of Parnassia (Parnassiaceae) and its
systematic implications. Journal of Integrative Plant Biology 47: 2-12.
Wu Z-Y(吴征镒), Lu A-M (路安民), Tang Y-C (汤彦承), Cheng Z-D (陈之端), Li D-Z (李德铢). 2003. The
Family and Genera of Angiosperms in China: A Comprehensive Analysis (中国被子植物科属综论).
Beijing: Science Press.
中国梅花草属植物的叶表皮特征及其系统学意义
1, 2吴 丁 1王 红 1卢金梅 1李德铢*
1(中国科学院昆明植物研究所 昆明 650204)
2(中国科学院研究生院 北京 100039)
摘要 利用光学显微镜和扫描电镜对梅花草属Parnassia 30种植物的叶表皮进行了观察。结果表明:气孔
器普遍存在于叶的下表皮,少数种的上表皮也有分布,均为无规则型。叶表皮细胞形状为多边形或不规则
形;垂周壁式样可区分为近平直、浅波状和波状。在扫描电镜下,叶表皮气孔器外拱盖内缘为近平滑、浅波
状或波状;一些种的保卫细胞两端有加厚;角质膜条纹状,有的条纹隆起,有的条纹上附有颗粒或小孔穴。
气孔器类型及下表皮细胞形状的一致性表明梅花草属是一个自然分类群;sect. Saxifragastrum叶表皮特
征具有多样性显示该组可能是一个复合群;突隔梅花草P. delavayi属于subsect. Xiphosandra,其气孔下陷,
与其细胞学特征相似,支持独立为一组;此外,气孔器的分布、保卫细胞两端加厚、气孔器外拱盖内缘形态
以及角质膜等特征对该属部分种的区分有一定的参考价值。
关键词 梅花草属; 叶表皮; 系统学意义