Braz. J. Bot (2016) 39(2):721–727
DOI 10.1007/s40415-015-0244-9
Seed micromorphology and its taxonomic significance to Xyris
(Xyridaceae, Poales)
Kaire de Oliveira Nardi1 • Aline Oriani1 • Vera Lucia Scatena1
Received: 24 August 2015 / Accepted: 14 December 2015 / Published online: 19 January 2016
Botanical Society of Sao Paulo 2016
Abstract The seed micromorphology was studied in
eight species of Xyris (Xyridaceae) with taxonomic purposes. The results show that the presence of longitudinal
endotegmic ridges in the seed coat is a pattern for the genus
and that the shape of these ridges differentiates among the
species. The following characteristics are also useful to
identify the species: shape and size of the seed, number of
cell rows between the ridges, and the striation pattern of the
seed coat. Based on these characteristics, a standard terminology is proposed to describe the seed coat in species of
the genus. An identification key for the studied species is
also provided.
Keywords Morphology Seed coat ornamentation
Taxonomy Xyridoideae
Introduction
Xyridaceae include ca. 430 species and comprise two
subfamilies: Xyridoideae (Xyris L.) and Abolbodoideae
(Abolboda Humb., Achlyphila Maguire & Wurdack,
Aratitiyopea Steyerm. & P.E.Berry and Orectanthe
Maguire). Xyris is the largest genus, comprising about
90 % of the species of the family, with a pantropical distribution (Wanderley 1992; Campbell et al. 2009).
The anatomy of the seeds was studied for species of
Abolboda, Orectanthe (Carlquist 1960; Oriani and Scatena
& Kaire de Oliveira Nardi
kairenardi@gmail.com
1
Departamento de Botânica, Instituto de Biociências,
Universidade Estadual Paulista (UNESP), Av. 24A, 1515,
C. Postal 199, Rio Claro, SP 13506-900, Brazil
2014) and Xyris (Weinzieher 1914; Rudall and Sajo 1999;
Nardi et al. 2015) and proved to be useful taxonomically.
The importance of seed coat ornamentation for the taxonomy of Xyris has already been demonstrated in the literature (Wanderley 1992; Silva 2010; Mota et al. 2015). Mota
et al. (2015), for example, analyzed the seed coat surface of
17 species of Xyris and used characteristics such as length
and shape of seed, type of striae, and pattern of cross-lines
to distinguish among species. It is worth pointing out that
the knowledge of the ontogeny of the seed is very important for the analysis of micromorphology because it facilitates the understanding of the origin of the tissues
responsible for seed coat ornamentation. Nardi et al. (2015)
studied the ontogeny of seed coat of six species of Xyris
and demonstrated that the mature seeds present exotesta,
endotesta, and endotegmen, and that the endotegmen
undergoes radial elongation, forming ridges in the seed
surface.
In Poales, micromorphological studies of seeds with
taxonomic purposes were also performed for species of
Bromeliaceae (Gross 1988; Melcher et al. 2004), Eriocaulaceae (Giulietti et al. 1986; Nair 1987; Scatena and
Bouman 2001; Melcher et al. 2004; Zona et al. 2012;
Barreto et al. 2013), Poaceae (Melcher et al. 2004), Rapateaceae (Venturelli and Bouman 1988), and Juncaceae
(Brooks and Kuhn 1986; Zech and Wujek 1990; Melcher
et al. 2004; Khalik 2010). These studies have demonstrated
that the micromorphological characteristics of seeds may
be useful for infrageneric classification and may indicate
relationships among taxonomic groups, emphasizing the
importance of seed characteristics for taxonomy and
phylogeny.
In light of the large number of species of Xyris and the
difficulty in identification because of the morphological
similarity (Wanderley 2011), this study aimed to identify
123
Truncate
Acute
Conspicuous
Inconspicuous
Acute
Conspicuous
Acute
Acute
Conspicuous
Inconspicuous
Acute
Truncate
Inconspicuous
Conspicuous
Conspicuous
Conspicuous
Absent
1–2
1–3
Sulcate
0.45 ± 0018 9 0.25 ± 0020
0.46 ± 0022 9 0.21 ± 0018
Ellipsoidal
Ellipsoidal
X. pterygoblephara Steud.
X. subsetigera Malme
Spiral
Conspicuous
1–3
0.72 ± 0031 9 0.23 ± 0019
Fusiform
X. pilosa Kunth.
Smooth
Inconspicuous
Inconspicuous
1–2
2–3
0.53 ± 0032 9 0.19 ± 0023
Fusiform
Smooth
0.42 ± 0026 9 0.21 ± 0016
Ellipsoidal
X. nubigena Kunth.
X. obtusiuscula L.A.Nilsson
Spiral
Inconspicuous
Inconspicuous
1
2–3
Moniliform
1.72 ± 0316 9 0.50 ± 0050
0.40 ± 0020 9 0.21 ± 0018
Ovoid
Ellipsoidal
X. bialata Malme
X. minarum Seub.
Sulcate
Conspicuous
Smooth
Oblong
X. asperula Mart.
1.02 ± 0.040 9 0.54 ± 0048
1–2
Transversal striations
in the zones between
ridges
Longitudinal striations
in the zones between
ridges
Endotegmic
ridges shape
Seed shape
Seed size (mm)
Number of cell
rows between
ridges
Figs. 1–8 Scanning electron micrographs of seeds of Xyris. 1, 2 X. c
asperula. 3, 4 X. bialata. 5, 6 X. minarum. 7, 8 X. nubigena. Scale
bar 100 lm (1, 3, 5, 7); 25 lm (2, 4, 6, 8). 8 hilum, op operculum
seed micromorphological characteristics with taxonomic
importance to identify species in the genus. Based on a
previous study of the seed development in Xyris (Nardi
et al. 2015), a standard terminology is proposed to describe
the seed coat in species of this genus.
Materials and methods
Species
Table 1 Micromorphological characteristics of seeds of Xyris
123
Acute
K. O. Nardi et al.
Hilum
722
Mature seeds of eight species of Xyris were collected in the
Serra do Cipó in Minas Gerais (Brazil) (198–208 S; 438–
44 W) and vouchers were deposited in the Herbarium
Rioclarense (HRCB) at Universidade Estadual Paulista. All
of the species studied belong to section Nematopus: X.
asperula Mart. (Scatena et al. 446), X. bialata Malme
(Nardi et al. 7), X. minarum Seub. (Nardi et al. 9), X.
nubigena Kunth. (Scatena et al. 448, 451; Nardi et al. 8), X.
obtusiuscula L.A.Nilsson (Nardi et al. 13), X. pilosa Kunth.
(Scatena et al. 455; Nardi et al. 4), X. pterygoblephara
Steud. (Scatena et al. 453; Nardi et al. 11, 12, 16), and X.
subsetigera Malme (Scatena et al. 447; Nardi et al. 14, 15,
17). These species were chosen because they have a sympatric distribution, similar morphology and flower
simultaneously.
For the scanning electron microscopy (SEM) study,
mature seeds from at least ten individuals of each species
fixed in FAA 50 were dehydrated in an acetone series,
critical point dried (Balzers, CPD 030) and coated with
gold (Bal-Tec, SCD 050). The results were recorded using
the ‘‘TM 3000 Application Program.’’ Measurements of
length and width of the seeds were analyzed in 30 samples
of each species with an image-capturing device (Leica,
DFC 290) coupled to a microscope (Leica, DMLB) using
the LAS (Leica Application Suite V3.6.0) digital imaging
system.
Results
The micromorphological characteristics of seeds are summarized in Table 1 and Figs. 1–8 and 9–16. The seed shape
varies from oblong in Xyris asperula (Fig. 1), to ovoid in
X. bialata (Fig. 3), ellipsoidal in X. minarum (Fig. 5), X.
nubigena (Fig. 7), X. pterygoblephara (Fig. 13), X. subsetigera (Fig. 15), and fusiform in X. obtusiuscula (Fig. 9)
and X. pilosa (Fig. 11).
The seed length ranges from 0.40 to 0.72 mm, and the
seed width ranges from 0.19 to 0.25 mm, except in X.
asperula and X. bialata, which have larger seeds with mean
Seed micromorphology and its taxonomic significance to Xyris (Xyridaceae, Poales)
723
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724
K. O. Nardi et al.
dimensions
of
1.02 mm 9 0.54 mm
and
1.72 mm 9 0.50 mm, respectively.
All of the studied species have longitudinal endotegmic
ridges in their seed coat surfaces, which can be smooth
(Figs. 1, 2, 7, 8 and 11, 12), moniliform (Figs. 3, 4), sulcate
(Figs. 5, 6, 13, 14), or spiral (Figs. 9, 10, 15, 16).
The number of cell rows between the ridges also exhibits interspecific variation and occur as 1 row (Figs. 5, 6),
1–2 rows (Figs. 1, 2, 7, 8, 15, 16), 1–3 rows (Figs. 11, 14),
or 2–3 rows (Figs. 3, 4, 9, 10). Longitudinal and/or
transversal striations are observed in the zones between
ridges and may be conspicuous or inconspicuous (Figs. 2,
4, 6, 8, 10, 12, 14, 16).
The hilum (h) and micropyle appear at opposite ends of
the seed (Fig. 1). The micropyle is protected by the operculum (op) (Fig. 1). The hilar region can be acute (Figs. 1,
5, 7, 9, 11, 13) or truncate (Figs. 3, 15).
Based on these characteristics, an identification key for
the studied species is provided.
Key to Xyris species based on seed characteristics
1.
Smooth endotegmic ridges
2.
20 .
Cell rows between ridges, 1–3………X. pilosa
Cell rows between ridges, 1–2
3.
30 .
10 .
Conspicuous longitudinal striations between
ridges………X. asperula
Inconspicuous
longitudinal
striations
between ridges………X. nubigena
Moniliform, sulcate, or spiral endotegmic ridges
4.
40 .
Moniliform ridges………X. bialata
Sulcate or spiral ridges
5.
Sulcate ridges
6.
60 .
50 .
Spiral ridges
7.
70 .
123
Cell row between ridges, 1; inconspicuous longitudinal striations between
ridges………X. minarum
Cell rows between ridges, 1–3; conspicuous longitudinal striations between
ridge…X. pterygoblephara
Cell rows between ridges, 2–3; inconspicuous longitudinal striations between
ridges….X. obtusiuscula
Cell rows between ridges, 1–2; absent
longitudinal striations between ridges…..…..…..X. subsetigera
Figs. 9–16 Scanning electron micrographs of seeds of Xyris. 9, 10 X. c
obtusiuscula. 11, 12 X. pilosa. 13, 14 X. pterygoblephara. 15, 16 X.
subsetigera. Scale bar 100 lm (9, 11, 13, 15); 25 lm (10, 12, 14, 16)
Discussion
Based on the obtained results, the following seed coat
characteristics have taxonomic importance to identify
species of Xyris: the shape and the size of the seed, the
shape of the endotegmic ridges, the number of cell rows
between the ridges, and the striation pattern of the seed
coat. These characteristics vary among the species studied,
allowing their identification, and are therefore of great
importance to the genus considering that numerous species
of Xyris occur sympatrically and are difficult to identify
because of their high morphological similarity. Although
we have not observed any intraspecific variation in relation
to these characteristics, there are reports in the literature
that seed shape may vary within the species, for example,
in Xyris asperula, whose seed shape may be fusiform or
ellipsoidal according to Wanderley (2011). Considering
this variation, we used only the most consistent characteristics in the species identification key such as shape of
the endotegmic ridges, the number of cell rows between the
ridges, and the striation pattern of the seed coat. The
importance of seed micromorphology for taxonomy has
been previously reported for the closely related family
Eriocaulaceae, whose species have also seed coat characteristics with interspecific variation (Giulietti et al. 1986;
Nair 1987; Zona et al. 2012).
It should be emphasized that the longitudinal ridges
observed in the seeds of the studied species were also
reported for all species of Xyris analyzed in previous
studies (Rudall and Sajo 1999; Silva 2010) and are thus a
pattern for the genus. An anatomical study of the ovule and
seed development of Xyris asperula Mart., X. cipoensis
L.B.Sm and Downs, X. nubigena Kunth, X. pterygoblephara Steud., X. pilosa Kunth., and X. subsetigera Malme
(Nardi et al. 2015) has demonstrated that the cells of the
exotegmen degenerate, while some cells of the inner layer
of inner integument (endotegmen) elongate radially,
forming ridges in the seeds, termed here as endotegmic
ridges. In Abolboda, the seed coat ornamentation is given
by the cells of the exotegmen, which do not degenerate,
forming exotegmic ridges (Carlquist 1960; Oriani and
Scatena 2014).
In Eriocaulaceae, the sister-group of Xyridaceae (Bouchenak-Khelladi et al. 2014), the development of the seed
coat is similar in all the genera studied, including the
Seed micromorphology and its taxonomic significance to Xyris (Xyridaceae, Poales)
725
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726
degeneration of the exostesta cells and of the outer periclinal walls of the endotesta cells (Scatena and Bouman
2001; Coan et al. 2010). In this family, the anticlinal walls
of the endotesta cells thicken during the seed coat development and are responsible for the ornamentation of the
seed surface, forming endotestal ribs (Scatena and Bouman
2001; Coan et al. 2010). Silva (2010) also used the term
‘‘ribs’’ to describe the seed coat ornamentation of seeds of
Xyris, whereas Mota et al. (2015) used the term ‘‘striae.’’
However, since the cell layer responsible for the seed coat
ornamentation in Eriocaulaceae and Xyridaceae is not
homologous, we believe that the term ‘‘endotegmic ridges’’
is more appropriate to describe the seed coat ornamentation
of Xyris.
The term ‘‘reticules’’ used by Silva (2010) and ‘‘crosslines’’ used by Mota et al. (2015) correspond to the ‘‘longitudinal and transversal striations’’ reported in the present
study and the ‘‘reduced or evident intercostal spaces’’
(Silva 2010) are herein described by the number of cell
rows between the ridges. According to our results, the
terminology proposed here is the most suitable since it is
based on the ontogeny of the seed structures (Nardi et al.
2015) and refers to characteristics that are easily observed.
In contrast to the ontogeny and anatomical structure of
the seed, which are uniform across the genus (Nardi et al.
2015), the micromorphological characteristics of the seeds
vary among the species of Xyris and, beyond their taxonomic significance, have ecological importance because
these characteristics may be related to different dispersal
strategies. To date there is no study on seed dispersal of
Xyridaceae; however, based on our results we can suggest
the following hypotheses: (I) Air bubbles may be retained
between the ridges and striations favoring wind dispersal,
as suggested for species of Syngonanthus Ruhland and
Paepalanthus Kunth (Eriocaulaceae) (Melcher et al. 2004);
(II) Ridges and striations can increase air resistance and air
buoyancy, decreasing the sink velocity of the seed (Johri
1984) and facilitating dispersal for long distances from the
mother-plant (Niklas 1994); (III) Ridges and striations can
be hygroscopic, similar to the ribs of Eriocaulaceae seeds,
and are most likely adaptations for the dispersal and the
germination of species that mainly inhabit regions with dry
periods (Giulietti et al. 1986); (IV) Water drops can be
stored between the ridges and striations, facilitating their
imbibition and promoting germination. Because the species
of Xyris usually occur in regions with low water availability, the hypothesis III and IV are more plausible.
However, further studies on seed dispersal are necessary to
adequately test these hypotheses. We suggest that the
micromorphological variations observed in the seeds of
Xyris have arisen to provide effective seed dispersal,
allowing seeds to reach areas suitable for germination and
seedling establishment.
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K. O. Nardi et al.
Acknowledgments We thank CAPES—Coordenação de Aperfeiçoamento de Pessoal de Nı́vel Superior (MSc fellowship to K.O.N.)
and FAPESP—Fundação de Amparo à Pesquisa do Estado de São
Paulo (grant 2011/11536-3 to A.O.) for financial support and the
Laboratório de Microscopia Eletrônica da Universidade Estadual
Paulista/Rio Claro for the use of the scanning electron microscope.
We also thank Dr Maria das Graças Lapa Wanderley for identifying
the species, and the anonymous reviewers for their valuable comments to improved the paper.
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