The genus
Haraldiophyllum
comprises seven species worldwide. Six of these are endemics with limited distributions,whereas the type species
H. bonnemaisonii
has been reported from the Atlantic Ocean. In Korea,
H. bonnemaisonii
has been previously recorded from the southern coast. During a red algal collection at Udo, Jeju Island, Korea, we found a potentially undescribed
Haraldiophyllum
species and analyzed its morphology and
rbc
L sequences. Herein we describe a new species,
H. udoensis
sp. nov., and compare our Udo specimen to similar congeners. This new species is characterized by one or several elliptical blades on a short cylindrical stipe with fibrous roots, blades that are monostromatic except at the base and on reproductive structures, a lack of network and microscopic veins, entire margins, lack of proliferations,growth through many marginal initials, and two distinct tetrasporangia layers. A phylogenetic
rbc
L sequence analysis demonstrated
H. udoensis
was distinct from the United Kingdom’s
H. bonnemaisonii
, as well as from other species. Morphological and sequence data indicated a previous misidentification of
H. udoensis
as the type species H.bonnemaisonii. Based on maximum likelihood analysis,
Myriogramme
formed a sister clade with
H. udoensis
, with relatively low bootstrap support.
INTRODUCTION
Zinova (1981) established the genus
Haraldiophyllum
based upon
Myriogramme
bonnemaisonii Kylin(1924), from Atlantic Europe. The
Haraldiophyllum
type species,
H. bonnemaisonii
, is characterized by a broad,erect, foliose thallus with a cylindrical stipe, the absence of a midrib and veins, monostromatic and polystromatic blades, and tetrasporangia sori formed upon both sides of the blade (Maggs and Hommersand 1993). To date,seven species of
Haraldiophyllum
have been recognized worldwide (Guiry and Guiry 2011), as follows:
H. bonnemaisonii
(Kylin) A. D. Zinova (1981);
H. crispatum
(J. D.Hooker & Harvey) Lin, Hommersand & Nelson (2007);
H.erosum
(Harvey) A. J. K. Millar & J. M. Huisman (1996);
H. infossum
A. J. K. Millar (1994);
H. mirabile
(Kylin) Zinova(1981);
H. nottii
(Norris & M. J. Wynne) M. J. Wynne(1983); and
H. sinuosum
(A. H. S. Lucas) A. J. K. Millar(1990).
The type species
H. bonnemaisonii
is typically distributed in the Atlantic Ocean (Maggs and Hommersand 1993, Hardy and Guiry 2003, John et al. 2004, Barbara et al. 2005, Lin et al. 2007). The other six species, however,are endemics with limited distributions.
H. mirabile
and
H. nottii
live only along the western coast of North America(Wynne 1983),
H. sinuosum
and
H. infossum
occur along the eastern coast of Australia and in the southwestern Pacific (Millar 1990, 1994),
H. erosum
inhabits west-ern Australia (Millar and Huisman 1996), and
H. crispatum
occurs in Australia and New Zealand (Lin et al. 2007).
In Asia, Nam and Kim (1996) initially identified
H.bonnemaisonii
based on the specimen collected from Hadong and Kwangyang along the south coast of Korea.They described the Korean specimens as characteristically having monostromatic blades (except for the basal portion), a procarp with one carpogonial branch and two sterile groups, and tetrasporangial sori on both surfaces of the blades (Nam and Kim 1996). They also noted that Korean specimens reached 10-20 cm in height and consisted of flabellate blades on a prominent stipe; however,Korean
H. bonnemaisonii
exhibits some differences when compared to specimens from the British Isles (Maggs and Hommersand 1993), having deeply cleft and non-dichotomously lobed blades.
Because the marine algal flora of Udo, Jeju Island, Korea remains very poorly documented, we have collected extensively there to improve our knowledge of red algal biodiversity. The red algae within the Udo marine forests consist of a turf community growing around and between digitate
Ecklonia cava
holdfasts. While collecting algae from Udo, we found a potentially undescribed species of
Haraldiophyllum
that belonged to the tribe
Myriogramme
ae.A careful examination revealed that this alga represented a new species in the Delesseriaceae. Here, we report on this newly discovered species based on its vegetative morphology and
rbc
L gene sequences, and discuss its taxonomic status among the species of the genus.To elucidate the phylogenetic relationships of the taxa from Udo, Jeju Island, we downloaded the
rbc
L sequence data of four
Haraldiophyllum
species from GenBank.
MATERIALS AND METHODS
- Morphology
For our morphological study, we collected the specimen on a scuba dive, and preserved them in 4% formalin/ seawater, with the exception of a small piece of thallus to be used for molecular study. The voucher specimen was deposited in the herbarium of Jeju National University(JNUB), Jeju, Korea. We sectioned the preserved specimen by hand or using a freezing microtome NK-101-II (Nippon Optical Works Co. Ltd., Tokyo, Japan).The sectioned preparations were stained with 1% aniline blue acidified with 1% HCl and mounted in 25-30% Karo syrup. To photograph the specimen, we used a Digital Sight DS-Fi1 camera (Nikon, Tokyo, Japan) attached to a microscope (ECLIPSE 80i; Nikon) and then imported all images into PhotoShop 7.0.1 (Adobe Systems, San Jose,CA, USA) for plate assembly.
- Molecular study
We air-dried the piece of cleaned thallus and desiccated it using silica gel for the DNA extraction. Using the DNeasy Plant Mini Kit (Qiagen, Hilden, Germany), and following the manufacturer’s instructions, we ground the silica gel-dried thallus in liquid nitrogen and extracted the total genomic DNA. Extracts were dissolved in 200 mL of distilled water. For amplification and sequencing reactions of genes, we employed the specific primer pairs
rbc
LF7-
rbc
LR753 and
rbc
LF645-
rbc
S start (Lin et al. 2001,Gavio and Fredericq 2002). For all polymerase chain reaction(PCR) amplifications, we used Swift MaxPro thermal cyclers (ESCO, Singapore) with an AccuPower PCR PreMix (Bioneer, Daejeon, Korea). The PCR comprised an initial denaturation step, at 94°C for 4 min, 35 cycles 1 min at 94°C, 1 min at 50°C, 2 min at 72°C, and a final 7 min extension cycle, at 72°C. To purify the PCR products,we used an AccuPrep PCR Purification Kit (Bioneer) and then sequenced them commercially (Macrogen, Seoul,Korea). Both electropherogram outputs from each sample were edited using the program Chromas version 1.45.
Using BioEdit (Hall 1999), we collated the total sequences and then aligned them visually. No alignments posed problems, as we observed no gaps. The outgroups we used were
Augophyllum delicatum
(AF257400) and
Nitophyllum punctatum
(AF257402). To confirm the taxonomic position of a potentially undescribed species of
Haraldiophyllum
from Udo, we conducted a maximum likelihood (ML) analysis, using PAUP 4.0 (Swofford 2002). We determined the best model for the individual data sets using Modeltest 3.4 software (Posada and Crandall 1998). The best model was a general time reversible(GTR) evolutionary model with gamma correction for among-site variation (Γ) and proportion of invariable sites (I). To estimate ML trees, we used a heuristic search with 100 random addition sequence replicates and tree bisection and reconnection (TBR) branch swapping. To test the node stability, we performed bootstrap analyses with 1,000 replicated ML searches, using the same program and settings.
RESULTS
- Haraldiophyllum udoensis M. S. Kim et J. C. Kang, sp. nov.
Haraldiophyllum udoensis sp. nov. (A) Holotype (JNU-MSK 30601HU tetrasporophyte) specimen deposited in the Herbarium of Jeju National University (JNUB) Jeju Korea. (B & C) Enlarged photos of Fig. 1A to show tetrasporangial sori (B) and the blade attached to a stone (C). Scale bars represent: A 5 cm; B & C 3 cm.
Description.
Thalli ellipticus, 22 cm longis et 6 cm latis, consisto singuli aut aliquot laminae affixus per fibrosus hapteron; lamina in brevis cylindricus stipitis, 2-3 cm longis et 1 mm crassus; lamina tenuis, monostromaticis super, tristromaticis in reproductivus area et polystromaticis versus basis, microscopicus vena absens, integer margo et marginalis cellulae divisus oblique; crescens marginalis et diffuses, sine distinctus cullula apicalis; tetrasporangia eferens in ellipticus sori 2 mm longis in medianas factus simultaneous in superficiebus ambabus lamina; tetrasporangia matura factus bistromatica, spherical, tetrahedraliter divisa, ad 80-100 ㎛ diametro.
Thallus elliptical, 22 cm long and 6 cm wide, consisting of one or several blades attached by a fibrous holdfast; blade on a short, cylindrical stipe, 2-3 cm long and 1 mm thick; blade thin, monostromatic above, tristromatic in reproductive areas, and polystromatic toward the base, microscopic veins absent; entire margins and marginal krcells divide obliquely; growth is marginal and diffuse, without distinct apical cells; tetrasporangia occur in elliptical sori 2 mm long on median, formed simultaneously on both surfaces of the blade; mature tetrasporangia forming two layers, spherical, tetrahedrally divided, to 80-100 ㎛ in diameter.
-
Holotype.JNU-MSK30601HU, tetrasporophyte, collected on June 14, 2009 (Fig. 1A).
-
Type locality.Haumokdong, Udo, Jeju Island, Korea (33°30´21˝ N, 126°56´09˝ E)
-
Type locality.Haumokdong, Udo, Jeju Island, Korea (33°30´21˝ N, 126°56´09˝ E)
-
Korean name.우도민엷은잎
Distribution.
Known to occur on the south coast (Nam and Kim 1996) and at Udo, Jeju Island, in this study.
Habitat.
We collected
Haraldiophyllum udoensis
at 12 m in the sublittoral zone of Udo, Jeju Island, Korea. The thallus grew as an epilithic blade on a stone covered with
Lithophyllum
sp. in habitats exposed to strong currents. Among the plants collected along the south coast of Ko-rea by Nam and Kim (1996) and by us for this study, tetrasporophytes were found from March to September. Nam and Kim (1996) collected male and female gametophytes in July and September, respectively, but we collected no gametophytes for this study.
Etymology.
We have chosen the specific epithet to represent the name of the islet collection site-Udo, Jeju Island.
Morphology.
The plant is a greenish red-brown, 22 cm high, 6 cm broad, foliose, and erect on a cylindrical stipe up to 2-3 cm long and 1 mm thick (
Fig. 1
A). The thallus consists of one or several blades, attached by a small fibrous holdfast, that lack midrib and microscopic veins (
Fig. 1
B & C). The blade is thin and monostromatic above, becoming tristromatic in reproductive areas and polystromatic toward the base with evanescent midribs (
Fig. 2
A-D), and increasing in thickness from 35 ㎛ near the apices to 100 ㎛ basally. The blade comprises cells that are elongate-polygonal in surface view (
Fig. 3
A) and 45-70 ㎛ long × 15-45 ㎛ wide, linked by secondary pit connections that increase in abundance in the polystromatic regions. The blade has entire margins, and marginal cells divide anticlinally or obliquely, growing marginal meristems without distinct apical cells (
Fig. 3
A).
Tetrasporangia are produced in small, numerous, circular to elliptical sori, formed randomly on both sides of the blade, and scattered throughout the blade except along the margins and the lowermost parts. Tetrasporangial sori are 2 mm long × 0.6 mm wide, and protrude on either side of the blade, approximately 200 ㎛ thick (
Fig. 3
B). In the transverse section of the sori, the tetrasporangia appear in two layers between both surface cells (
Fig. 3
C). The tetrasporangia are produced from inner cortical cells but occasionally also from primary cells. Mature tetrasporangia are spherical, 80-100 ㎛ in diameter, and divided tetrahedrally (
Fig. 3
D).
Molecular analysis of rbcL.
To align the five
Haraldiophyllum
species with putative relative genera in the family Delesseriaceae, we used a 1,303 nucleotide (nt) portion of
rbc
L gene and two outgroups. Variable sites occurred at 464 positions (35.6%), and 350 positions (26.9%) were parsimoniously informative. In the ML analysis, we estimated the ?ln likelihood score as 7,899.6647 under the GTR + Г + I model. The sequences differed by up to a 72 bp (5.5%) pairwise distance between
H. udoensis
from Korea and
H. bonnemaisonii
from the United Kingdom. The new species differed from
H. crispatum
from New Zealand,
H. mirabile
from the United States, and
Haraldiophyllum
sp. from Chile by 64, 32, and 39 bp, respectively. The uncorrected sequence divergence (in terspecific p distance) values for the
rbc
L region within
Haraldiophyllum
ranged from 31 bp (2.7%) between
H. mirabile
from the United States and
Haraldiophyllum
sp. from Chile to 87 bp (6.7%) between
H. bonnemaisonii
and
Haraldiophyllum
sp. from Chile. The most-related genus,
Myriogramme
, differed by 109-142 bp (8.3-11%) from
H. udoensis
and by 103-169 bp (8-13%) from the rest of the genera we tested in the present study.
In the phylogenetic tree from
rbc
L, the new species formed an independent clade with strong support (99% for ML) and a sister group with
H. mirabile
from the United States and
Haraldiophyllum
sp. from Chile (
Fig. 4
). The ML analysis of
rbc
L data indicated that
H. udoensis
showed clear separation from
H. bonnemaisonii
and
H. crispatum
from New Zealand. The ML tree showed two groups within
Haraldiophyllum
, and the bootstrap supports were quite strong (100% and 91%). The first clade included
H. udoensis
as the new species,
H. mirabile
and
Haraldiophyllum
sp., and the second clade contained
H. crispatum
and
H. bonnemaisonii.
The genus
Haraldiophyllum
monophyly had definitive bootstrap support (100%). The genus
Myriogramme
formed a sister relationship with the genus
Haraldiophyllum.
DISCUSSION
Haraldiophyllum udoensis
is newly described from Udo, Jeju Island, Korea, based on our detailed morphological observations and molecular analysis. This new species is characterized by the following features: 1) one or several elliptical blades on a short, cylindrical stipe with fibrous roots; 2) monostromatic blades, except at the base and on reproductive structures; 3) a lack of network and microscopic veins; 4) entire margins with a lack of proliferations; 5) growth by means of many marginal initials; and 6) an arrangement of two distinct tetrasporangia layers. Molecular phylogenetic analysis based on
rbc
L sequences demonstrated
H. udoensis
’s distinctness from its congeners, and separated it clearly from the European
H. bonnemaisonii
. The genus
Haraldiophyllum
contains two clusters of species, one from the United Kingdom and New Zealand and the other occurring along the Pacific Coasts of Korea, the United States, and Chile. Our molecular analysis produced similar results to those Lin et al. (2007) reported. The new species is epilithic in the sublittoral zone at depths up to 12 m. It was previously identified in Korea as
H. bonnemaisonii
(Nam and Kim 1996). Although
H. udoensis
closely resembles the type species of
Haraldiophyllum
(
H. bonnemaisonii
from the
Haraldiophyllum udoensis sp. nov. (A-D) Transverse section of the blade which is monostromatic (A & B) tristromatic (C) and polystromatic toward the base (D). Scale bars represent: A 50 μm; B & C 30 μm; D 100 μm.
Haraldiophyllum udoensis sp. nov. (A) Surface view of blade showing elongate-polygonal cells. (B) Small elliptical tetrasporangial sori. (C) Transverse section of sori forming two tetrasporangia layers. (D) Mature tetrasporangia divided tetrahedrally. Scale bars represent: A & D 30 μm; B & C 50 μm.
Phylogenetic tree for Haraldiophyllum and relatives derived from maximum likelihood using plastid-encoded rbcL sequence data. The bootstrap values shown above branches are from bootstrap analyses employing 1000 replicated maximum likelihood searches.
British Isles),
H. bonnemaisonii
has a distinct thallus that divides regularly and dichotomously into overlapping lobes, frequently proliferating on the blade and forming a single tetrasporangia layer in a zigzag manner (Maggs and Hommersand 1993, Lin et al. 2007). In addition, the reproductive structure in
H. udoensis
is larger; the cystocarp diameter of > 700 ㎛ contrasts with the < 600 ㎛ in
H. bonnemaisonii
, and tetrasporangia in
H. udoensis
are > 80 ㎛ in diameter, as opposed to < 70 ㎛ in
H. bonnemaisonii
(
Table 1
).
In recognizing the species of
Haraldiophyllum
, which currently contains seven species, the vegetative characteristics are viewed as important diagnostic features, such as whether thallus size is diminutive, whether shape of the base and margins are dentate or entire, whether the branching pattern is dichotomous, whether the lobed blade is deeply cleft, and the presence or absence of stipes (
Table 1
). Thallus size is useful for identifying species of
Haraldiophyllum
;
H. bonnemaisonii
and H. crispatum reach 20-25 cm, whereas
H. infossum
and
H. nottii
are 2-7 cm smaller than other species (Millar 1994, Womersley 2003, Lin et al. 2007). In particular,
H. infossum
from Australia differs from all other species in the genus due to its diminutive size (up to 1.9 cm).
Haraldiophyllum
sinuosum is by far the largest of the genus with plants reaching lengths of 20-35 cm.
Haraldiophyllum
erosum and
H. mirabile
are of medium size at around 10 cm (Millar and Huisman 1996), but the new species
H. udoensis
is approximately 20 cm in length. The shapes of the base and margins have been demonstrated as valid characteristics for delineating some species of
Haraldiophyllum
, as for example Millar and Huisman (1996) showed changes of the
Haraldiophyllum
species’ margins display a continuum from species with entire margins to those with fringed margins. Most of
Haraldiophyllum
species including the new species
H. udoensis
have entire or dentate margins, except for two:
H. erosum
and
H. infossum
(Millar 1994). According to Millar and Huisman (1996), H. erosum from western Australia has an unusual marginal fringe with numerous multicellular
Morphological comparisons of species in the genus Haraldiophyllum
Morphological comparisons of species in the genus Haraldiophyllum
processes. They report these marginal processes are often polysiphonous and divaricately branched, and they always terminate single apical cell in a transversely-dividing (Millar and Huisman 1996).
H. infossum
often has a stoloniferous base and prominently dentate blade margins (Millar 1994).
The branching pattern in relation to the presence or absence of lobed blades and stipes can also be an important distinguishing feature.
H. bonnemaisonii
comprises one to several fan-shaped blades, borne on cartilaginous stipes and dividing dichotomously into overlapping lobes with rounded apices (Maggs and Hommersand 1993, Lin et al. 2007).
H. crispatum
has an exceedingly variable shape, dividing partially into broad lobes with rounded margins or cleaving into irregular, dichotomously-branched segments with proliferations (Lin et al. 2007).
H. erosum’s
blades have dichotomous or irregular lobes and often have irregularly-shaped holes in the surfaces (Millar and Huisman 1996).
H. infossum
has ovated to elongated individual blades that often overlap in an imbricate arrangement with the creeping stoloniferous parts compressed (Millar 1994).
H. mirabile
from Alaska has less prominent stipes, and the blades are roundish to deeply lobed or cleft (Kylin 1925). The blades of
H. nottii
are complicated and subdichotomously branched with lobed, narrow stipes (Norris and Wynne 1968). The blades of
H. sinuosum
are generally entire and not deeply cleft but have short, blunt lobes, and the plants have short stipes that do not persist into the lower blades (Lucas 1913). The new species
H. udoensis
appears to differ from other species mostly by its one to several elliptical, non-lobed blades.
Researchers have documented the diagnostic characteristics of the genus
Haraldiophyllum
’s reproductive structures for the female reproductive organs, such as the procarp, carposporangia, and cystocarp. The procarps contain two groups of sterile cells, one group of cover cells and two periaxial cells parallel to the frond’s longitudinal axis (Millar 1994). The carposporangia are borne singly and terminally on gonimoblast filaments. The cystocarp has a fusion cell incorporating gametophytic cells at the floor of the cystocarpic cavity. Kylin (1925) noted this feature of the cystocarp fusion cell is probably useful for generic recognition of the genus
Haraldiophyllum
. Maggs and Hommersand (1993) and Millar (1994) also included this characteristics in their generic circumscription of
Haraldiophyllum
, while Millar and Huisman (1996) recognized two different sequences of cell formation leading to the procarp’s final structure in
Haraldiophyllum
. They observed
H. bonne
maisonii has only one sterile cell group cutting off from the supporting cell prior to the initial carpogonial branch. The production of the second sterile cell group delays until after carpogonial branch formation. The same sequence occurs in
H. crispatum, H. erosum
, and
H. nottii
, but that of
H. infossum
differs in forming the two sterile cell groups before initiating the carpogonial branch (Millar 1994). Millar and Huisman (1996), therefore, concluded these differences appear to be stable within the
Haraldiophyllum
species. In the new species,
H. udoensis
, procarp formation and cystocarp development follow a pattern similar to those previous studies describe (Millar 1994, Millar and Huisman 1996, Nam and Kim 1996, Lin et al. 2007).
While researchers often use the female reproductive organ’s structure to distinguish species within the genus and genera in the family, they have not considered the number of layers in the tetrasporangia arrangement to be of any significance in this genus. The type species
H. bonnemaisonii
has only a single layer of tetrasporangia arranged in a zigzag manner, and the same feature occurs in
H. crispatum, H. infossum,
and
H. nottii
. However, two species,
H. udoensis
sp. nov. and
H. erosum
, form two layers of tetrasporangia. To verify the importance of the number of layers in the tetrasporangia arrangement from a phylogenetic perspective, further observation and molecular analysis for all seven species are necessary.
The genus
Haraldiophyllum
superficially resembles two genera,
Myriogramme
and
Nitophyllum
, although
Haraldiophyllum
clearly belongs to the tribe
Myriogramme
ae based on vegetative and reproductive developmental characteristics (Hommersand and Fredericq 1997). The genus
Haraldiophyllum
is readily separated from the genus
Myriogramme
by carposporangia organization, which is terminal solitary in
Haraldiophyllum
but terminal chains in
Myriogramme
(Wynne 1983, Lin et al. 2007). The new species
H. udoensis
forms a separate clade from
Myriogramme
based on molecular analysis of
rbc
L sequence data. However, the new species is linked to
Myriogramme
as a sister clade with low bootstrap support in the ML analysis.
Haraldiophyllum
is distinguished from the genus
Nitophyllum
by the number of sterile cell groups in the procarps, with two for
Haraldiophyllum
and only one for
Nitophyllum
, as well as by the two periaxial cells’ alignment with respect to the frond’s longitudinal axis, showing a parallel manner in
Haraldiophyllum
and a perpendicular manner in
Nitophyllum
(Zinova 1981, Wynne 1983). In the molecular phylogenetic tree, the
Haraldiophyllum
clade is distantly separate from the
Nitophyllum
clade including its type species,
N. punctatum
from Spain.
Our ongoing studies of the Delesseriaceae from Jeju Island, Korea have thus far clarified the generic placement of
Haraldiophyllum
and led to the recognition of a new species,
H. udoensis
. On Jeju Island, many delesseriaceous taxa remain that require critical reexamination in light of recent taxonomic developments within the family.
Acknowledgements
This work was supported by a National Research Foundation of Korea grant, funded by the Korean Government (2011-0003792), and as part of the Survey of Indigenous Biology of Korea by the National Institute of Biological Resources (NIBR).
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