African Journal of Biotechnology Vol. 11(21), pp.

4706-4715, 13 March, 2012

Available online at http://www.academicjournals.org/AJB
DOI: 10.5897/AJB11.464
ISSN 1684–5315 © 2012 Academic Journals

Review

Some progress in sexual reproduction and sex

determination of economic algae
Chen Peng1, 4, Chen Qi-Jie2, Chu Li-Ye3 and Shao Hong-Bo1,3*
1
The CAS/Shandong Provincial Key Laboratory of Coastal Environmental Process, Yantai Institute of Coastal Zone
Research, Chinese Academy of Sciences (CAS), Yantai 264003, China.
2
College of Life Science and Technology, Harbin Normal University, Harbin 150025, China.
3
Institute of Life Sciences, Qingdao University of Science and Technology (QUST), Qingdao 266042, China.
4
The Graduate University of Chinese Academy of Sciences, Beijing 100049, China.
Accepted 28 February, 2012

With the rapid development of marine industry, algae as an important economic plant as well as an
extremely promising energy source, is now attracting more and more attention. As a result of this,
elucidating the basic physiological mechanisms of algae becomes even more urgent. Of all the fields,
sexual reproduction and sex determination are basic and essential aspects. In this review, we
summarized the advances of sex in several typical algae which are of great economic importance and
often used as model organism for basic research.

Key words: Sexual reproduction, sex determination, sex-related genes, algae, life cycle.

INTRODUCTION

Algae, with extremely rich diversity, appeared on earth in Studies on these topics may play important roles
the ancient age. Many algae have life cycles involving in understanding algae physiological mechanisms and
quite different stages such as gametophytes, carpos- will provide clues for algal evolution pathways (Zhang et
porophytes and tetrasporophytes (Chen et al., 2009). al., 2005).
Even though the phases and sexes of many algae look
identical before sexual maturation, there are physical
differences between them (Bird and McLanchlan, 1984), EUKARYOTIC MICROALGAE
such as growth rate in phases (Tseng and Xia, 1999), They are unicellular species which exist individually, or in
levels of polyamines in sexes and phases (Santelices chains or groups. Depending on the species, their sizes
and Doty, 1989) and lipid composition among different can range from a few micrometers to a few hundreds of
developmental stages. Owing to their particular life cycle, micrometers. Unlike higher plants, microalgae do not
differentiation of phase and sex in algae has already have roots, stems or leaves. Microalgae, capable of
attracted researchers’ attention. Researchers have been performing photosynthesis, are important for life on earth.
engaged in the study of the mechanisms of phase They produce approximately half of the atmospheric
formation since early time (Fernandez et al., 1989). How- oxygen and use simultaneously the greenhouse gas
ever, no satisfactory results were obtained due to the carbon dioxide to grow photoautotrophically.
limitation of applicable methods in the past. With the
development of molecular biology and other developed
technology, great progress has been made recently. Chlamydomonas

The unicellular green chlorophyte algae Chlamydomonas,

sometimes called the ‘green yeast’, has achieved recog-
*Corresponding author. E-mail: shaohongbochu@126.com nition as a model system for the study of photosynthesis,
(Shao HB); chenqij@yahoo.com.cn (Chen QJ). Tel: +86-0532- organelle biogenesis, transgene and many other aspects
84023984. of cell and genetic biology. It is the first species in which
 Peng et al. 4707

Figure 1. The life cycle of C. reinhardtii (modified from Goodenough et al., 2007).

genetic transformations of all the three genomes (nucleus restoration of nitrogen, moisture and light induce the
genome, chloroplast genome and mitochondria genome) germination process. The dormant zygote initiates
have been successfully carried out (Zhang et al., 2005). meiosis, sometimes followed by a mitotic division, and
In nature, the sexual cycle is a responsive to stress the zygospore wall bursts to release the four progeny.
environment. In the laboratory, gametogenesis is These nuclear genes are inherited in a Mendelian fashion
controlled by nitrogen deprivation and a blue light- and segregate 2:2 among the tetrad products. Chlo-
responsive signal transduction pathway (Gloeckner and roplast genes are inherited uniparentally from the mt+
Beck, 1997; Pan et al., 1997). The sex-determination parent in most zygotes (>95% under the usual laboratory
system of Chlamydomonas is governed by genes in the conditions), whereas mitochondrial DNA in C. reinhardtii
mating-type locus (mt locus, the mt locus is mapped to is transmitted uniparentally from the mt- parent.
the left arm of Linkage Group VI) and entails additional
genes located in autosomes (Ferris et al., 2002; Abe et
al., 2005; Goodenough et al., 2007). Diatom
The life cycle of Chlamydomonas reinhardtii is simple
(Figure 1). Two of the haploid products of each meiosis Diatom, another unicellular alga, is one of the important
inherit a linkage group VI carrying the mt+ locus and two primary producers and acts have an extremely important
inherit a linkage group VI carrying the allelic mt− locus. role in maintaining the ecological balance of water.
Each product divides mitotically to produce clones of Diatoms are autotrophic photosynthesizing algae, which
vegetative cells. Gene expression is initiated by nitrogen mean that they are able to produce their own sugars,
starvation, and cells differentiate into plus or minus lipids and amino acids. They attract researchers’ attention
gametes. When environmental nitrogen levels fall below not only for the large number, but also for their impor-
threshold (Fraser et al., 2004), vegetative cells carrying tance as a wide range biological resource.
+
the mt locus express genes that allow them to mate as A characteristic feature of diatom cells is that they are
plus gametes, and cells carrying the mt− locus express a encased within a unique cell wall made of silica (hydrated
different set of genes that allow them to mate as minus silicon dioxide) called a frustule. These frustules show a
gametes. Gametes express mating type-specific glycol- wide diversity in form, but usually consist of two
proteins (agglutinins) on their flagellar surfaces asymmetrical sides with a split between them, just like a
(Goodenough et al., 1995). Flagellar pairing between a culture dish.
plus and a minus gamete initiates a cascade of process, Reproduction of diatoms is primarily asexual by binary
including lysis of the gametic cell walls by a specific fission (Figure 2). When a cell divides, each new cell
enzyme distinct from the vegetative cell lysine, contact of takes a valve of the parent frustule as its epitheca (or
mating type-specific structures at the cell apices and larger frustule), into which its own hypotheca (or smaller
fusion of the gametic cytoplasms (Ferris et al., 1996; frustule) is constructed within ten to twenty minutes. This
Wilson et al., 1997). All of the above produce a binucleate process may occur one to eight times per day. Availability
zygote. During the next hour, the two nuclei fuse and a of dissolved silica limits the rate of vegetative repro-
novel set of zygote-specific genes is expressed, many of duction (Zhang et al., 2005).
which self-assemble as a zygote-specific cell wall that This form of division results in a progressive size
renders the zygote resistant to freezing, desiccation and reduction of the offspring and therefore the average cell
other environmental insults. When conditions improve, size of a diatom population decreases. It has been
4708 Afr. J. Biotechnol.

Figure 2. The life cycle of diatom for economic algae.

observed, however, that certain taxa has the ability to resting cyst or statospore stage. The siliceous resting
divide without causing a reduction in cell size (Drebes, spore commonly forms after a period of active vegetative
1977). There is a certain threshold of the cell size, which reproduction when nutrient levels have been depleted.
is about one-third of their maximum size (Hasle et al., Statospores may remain entirely within the parent cell,
1997). In order to restore the cell size of a diatom partially within the parent cell or be isolated from it. An
population, sexual reproduction and auxospore formation increase in nutrition levels or length of daylight causes
occur (Hasle et al., 1997). Vegetative cells of diatoms are the statospore to germinate and return to its normal
diploid and so meiosis can take place, producing male vegetative state.
and female gametes which then fuse to form the zygote. The diatom reproduction mode of auxospore is unique.
The zygote sheds its silica theca and grows into a large Besides the requirements of frustule size restoration,
sphere covered by an organic membrane. Auxospores changes of environmental conditions such as light,
are then produced, which are cells that posses a different salinity and temperature may also induce sexual repro-
wall structure lacking the siliceous frustule and swell to duction. Armbust (1999) found a new gene family
the maximum frustule size. The auxospore then forms an expressed during the onset of sexual reproduction in the
initial cell which forms a new frustule of maximum size centric diatom. Researchers speculate that there is a
within itself. Then, a new generation begins. Resting unique secretion signal sequence as well as a cysteine
spores may also be formed as a response to un- rich domain among the amino-terminal peptide of its
favourable environmental conditions with germination members. The polypeptides may be related to the
occurring when conditions improve (Horner, 2002). identified process of sexual reproduction.
In centric diatoms, the small male gametes have one
flagellum, while the female gametes are larger and non-
motile (oogamous). Conversely, in pinnate diatoms, both Chlorophyta
gametes lack flagella (isoogamous) (Hasle et al., 1997).
Certain araphid species have been documented as Chlorophyta (green algae) includes about 7000 species
anisogamous and are, therefore, considered to represent of mostly aquatic photosynthetic eukaryotic organisms.
a transitional stage between centric and pinnate diatoms. Green algae contain chlorophylls a and b, giving them a
Many neritic planktonic diatoms alternate between a bright green color (as well as the accessory pigmentsbeta
vegetative reproductive phase and a thicker walled carotene and xanthophylls). Green algae contain both
 Peng et al. 4709

Figure 3. The life cycle of Ulva.

unicellular and multicellular species (Hoek et al., 1995). released into the water, where they settle and grow into
Green algae follow a reproduction cycle called alternation the following generation. This next generation is referred
of generations. Reproduction varies from fusion of to as the gametophyte phase. During the gametophyte
identical cells (isogamy) to fertilization of a large non- phase, after the zoospore develops into sexual
motile cell by a smaller motile one (oogamy). gametophyte, it produces anisogametes (mt+ or mt-) by
mitosis (Zhang et al., 2005). The biflagellate gametes are
produced at the margin of a thallus in a zone 5 to 15 mm
Ulva broad, of different colors from vegetative portion and a
zone in which every cell forms gametes. The gametes are
Ulva is a genus of Chlorophyta living primarily in marine formed by repeated bipartition of the protoplast of a cell.
environments. They can also be found in brackish water, Cleavage continues until 32 to 64 daughter protoplasts
particularly estuaries. They live attached to rocks in the are formed. Each daughter protoplast metamorphoses
middle to low intertidal zone, and as deep as 10 m in into a biflagellate gamete. Just before the cleavage of the
calm, protected harbors. Ulva are usually seen in dense protoplast, each cell develops a beak like outgrowth as its
groups. The shapes of Ulva are quite varied, ranging in outer face and it expends to the thallus surface. Later on,
size from microscopic to tens of centimeters. The delicate a pore is formed at the tip of this beak, through which the
blades of Ulva are usually only 40 microns thick. gametes are liberated. The gametes are smaller than
Green algae such as Ulva have two life phases (Figure zoospores. These anisogametes fuse together in pairs to
3). These two phases are called the sporophyte and create zygotes (Miyamura, 2004). After fusion of the
gametophyte phases. During the sporophyte phase, the gametes, quadriflagellate zygote is formed. It swims for a
algae produce spores by meiosis. During the gameto- short time and then comes to rest, withdraws its flagella
phyte phase, the algae produce gametes by mitosis. and secretes a wall around it. Within a day or two, the
During the sporophyte phase, the membranous thallus, or germination of zygote takes place. The division of the
body of the plant, creates a holdfast attachment to the zygote nucleus is mitotic. The two daughter cells are
rock (Han et al., 2003). The haploid spores (zoospore) formed by means of division of the zygote. One of the two
produced by meiosis during the sporophyte phase are daughter cells develops into a rhizoid and the other
4710 Afr. J. Biotechnol.

Figure 4. The life cycle of Laminaria.

eventually develops into a blade. Then, it grows to enter The differences in life cycle define a number of orders,
the next sporophyte generation. Ulva looks the same in some with a dominant diploid phase (heteromorphic alter-
the gametophyte phase as it does in the sporophyte nation of generations), and some with isomorphic phases
phase. Due to this, it is considered to undergo isomorphic (isomorphic alternation of generations). Some others
alternation of generations, gametophyte and sporophyte have no free-living gametophyte stage at all. The largest
are indistinguishable by external anatomy. kelps are diploid, and release flagellated swimming
In 1996, a research showed that differentiation of Ulva sperm into the water to find egg cells. It has been shown
mutabilis gametangia and gamete release are controlled that chemical signals called pheromones aid the sperm in
by extracellular inhibitors, and maybe glycoprotein their quest in at least some phaeophytes.
(Stratmann et al., 1996).

Laminaria
Phaeophyta
Laminaria is a genus of 31 species of Phaeophyceae,
The Phaeophyta (brown algae) is a large group of mostly whch is a temperate brown algae belonging to the group
marine multicellular algae, including many seaweeds known as kelps. It is found in the northern Atlantic Ocean
from colder northern hemisphere waters. They play an and the northern Pacific Ocean at depths of 8 to 30 m
important role in marine environments as well as food. (exceptionally to 120 m in the warmer waters of the
For instance, Macrocystis may reach 60 m in length, and Mediterranean Sea and off Brazil). The greater proportion
form prominent underwater forests. Another example is of commercial cultivation is for algin, iodine and mannitol,
Sargassum, which creates unique habitats in the tropical which are used in a wide range of industrial applications.
waters. Worldwide, there are about 1500 to 2000 species The largest producer of kelp products is China.
of brown algae (Hoek et al., 1995). Some species are of Laminaria exhibits a typical heteromorphic alternation
sufficient commercial importance, they have become of generations, which means that the sporophyte
subjects of extensive research (Senn, 1987). generation alternates with the gametophyte generation
Most brown algae have a sexual alternation of (Figure 4). Laminaria exhibits heterothallism. Male and
generations between two different multicellular stages. female gametophytes are morphologically dissimilar, the
 Peng et al. 4711

male gametophyte having smaller cells and being more that sex determination of Laminaria was governed by a
branched than the female gametophyte (Zhang et al., pair of sex chromosomes or sex-determining genes
2007). (Schreiber, 1930). Evans believes that to some extent,
The asexual sporophyte generation produces motile there is a certain universality of XY chromosome sex
zoospores which develop into male and female gameto- determination in Phaeophyta through his researches on
phytes, whereas the sexual gametophyte generation Saccorhiza, Laminaria and Kombu (Evans, 1965).
produces male and female gametes. The male gameto- Parthenogenesis of Laminaria provides evidence to this
phyte produces male gametes called spermatozoids or speculation. In parthenogenesis, spores produced by
antherozoids. The female gametophyte plant produces mature sporophytes all develop into female gameto-
female gametes (eggs). The sperm is released, whereas phytes, which indicates that the sex of Laminaria is
the eggs remain attached to the gametophyte. The sperm determined by X and Y chromosomes. X chromosome
reaches the female gametophyte by a chemical signal determines the female gametophyte, while Y chro-
secreted by the eggs that attract sperm of the same mosome determines male gametophyte. Normal
species (Mizuta et al., 2007). At fertilization, male and chromosome composition of sporophyte is XY, resulting
female gametes fuse to form the zygote which sub- in same number of male and female gametophytes after
sequently develops into a young sporeling at the meiosis. However, the chromosome composition of
beginning of the sporophyte generation. spores in parthenogenesis is XX, so gametophytes are all
Zoospores are produced on the fronds of mature female. Further research also ruled out the possibility that
sporophyte in sporangial sori. Sporangial sori are cup-like the sex determination of Laminaria is governed by a pair
structures where cells divide through meiosis to produce of alleles (Zhang et al., 2005).
haploid male and female zoospores. The pelagic zoo-
spores are motile, having two flagellas. When released
from the sporangial sori, they drift and swim around in the Undaria
water for 5 to 10 min at 15 to 20°C and up to 48 h at 5°C,
then settle and adhere to the substratum where they Studies on another important economic brown algae
develop into male and female gametophytes (Yang et al., Undaria reach similar conclusions with Laminaria. But
2009). specially, it was reported that the male parent affected the
After a number of cell divisions, the microscopic male genetic characters of its filial generation, which is quite
gametophyte plant develops several spermatangia (also different from the general sense of sex-linked inheritance
called antheridia), each spermatangium producing a (Pang and Wu, 1996; Pang et al., 1997). Due to this, for
single motile biflagellate spermatozoid which is released most species, the egg cytoplasm contain a large number
into the seawater. The female gametophyte develops a of cytoplasmic genes while the sperm generally contains
single large oogonium which produces an egg. The egg is little, and the offspring characters are determined by
extruded during ovulation but remains attached to the female parent (Pang, 1998). Until now, the only observed
apical lip of the oogonium. Here, the egg is fertilized by male parental sex-linked inheritance is in drosophila
motile spermatozoids with fusion of male and female (Zhang et al., 2005). However, more evidence is required
gametes producing the fertilized zygote. The zygote to confirm this conclusion.
germinates and develops into a ‘young sporeling’, also
called a ‘young seedling’, which subsequently develops
into a ‘young sporophyte’ (Nimura and Mizuta, 2002). Rhodophyta
In 1896, a research on chromosome number of
Ascophyllum nodudum was carried out by Farmer and The Rhodophyta (red algae) is one of the oldest groups
Willaims, which started the chromosome research on of eukaryotic algae (Lee, 2008) and also one of the
Phaeophyta (Zhang et al., 2005). Until now, more than largest. The red algae form a distinct group and are
200 researches on Phaeophyta chromosome have been characterized by the following attributes: eukaryotic cells
reported (Liu et al., 2009). It is difficult to study the without flagella and centrioles, using floridean starch as
chromosome morphology or caryotype of Phaeophyta for food reserve, with phycobiliproteins as accessory
it is too small in size. That is why researches on Phaeo- pigments (characterized by the accessory photosynthetic
phyta chromosome were mainly focus on comparison of pigments phycoerythrin, phycocyanin and allophyco-
chromosome number and size in the beginning. cyanins arranged in phycobilisomes), and with
Gametophytes of Phaeophyta are also divided into male chloroplasts lacking external endoplasmic reticulum and
and female ones with a ratio of 1:1, which fully indicates containing unstacked thylakoids (Woelkerling, 1990;
the existence of sex determination and sex differentiation Ragan et al., 1994). Most red algae are also multicellular,
in Phaeophyta. In the early 1990s, Schreiber observed macroscopic, marine, and have sexual reproduction
that the ratio of male and female gametophytes produced (Figure 5).
by sporophytes is 1:1, according to which he speculated Within the red algae, a triphasic life history is pretty
4712 Afr. J. Biotechnol.

Figure 5. The life cycle of Porphyra.

common. Red algae lack motile sperm, hence they rely Porphyra umbilicalis (Drew and Kathleen, 1949). It was
on water currents to transport their gametes to the female later shown for species from other regions as well (Brodie
organs, although their sperm are capable of ‘gliding’ to a and Irvine, 2003; Thomas, 2002).
carpogonium’s trichogyne (Lee, 2008). The differentiation of male and female thallus of
Porphyra is complicated. Porphyra yezoensis, Porphyra
suborbiculata are monoecious, while Porphyra dentate is
Porphyra dioecious. Yang et al. (2009) carried out expressed
sequence tags (EST) analysis of P. yezoensis, obtained
Life history of Porphyra has been studied intensely 170 ESTs, of which 73 were new. These new tags may be
throughout time, especially because of its high economic specific genes of P. yezoensis filamentous sporophyte
value. Porphyra displays a heteromorphic alternation of (Chen et al., 2009). Abe et al. (2005) performed com-
generations which is temperature dependent and parative analysis between 10625 ESTs of P. yezoensis
seasonal in nature (Figure 5). The thallus we see is the sporophyte and 10154 ESTs of P. yezoensis gametophyte
haploid generation, it can reproduce asexually by forming and found that 1940 of them were gametophyte-specific,
spores which grow to replicate the original thallus. It can while 1543 of them were sporophyte-specific, still 1013
also reproduce sexually. Both male and female gametes tags were two generations shared. Studies on Porphyra
are formed on one thallus. The female gametes which are purpurea by Mitman et al. (1994) deepen the under-
still on the thallus are fertilized by the released male standing of the sex determination mechanisms, but the
gametes. The fertilized, now diploid, carposporangia after diversity and complexity of Porphyra sex differentiation
mitosis produce spores (carpospores) which settle, then make it extremely complicated mainly in the following
bore into shells, germinate and form a filamentous stage. three aspects: first, time relation between gender mecha-
This stage was originally thought to be a different species nisms and meiosis; second, algae of monoecious type
of algae, and was referred to as Conchocelis rosea. The may have different mechanism of sex determination;
fact that Conchocelis was the diploid stage of Porphyra third, the evolution of Porphyra gender mechanisms
was discovered in 1949 for the European species (Mitman and van der meer, 1994; Liu et al., 1996). Eight
 Peng et al. 4713

Figure 6. The life cycle of Gaillardia (modified from Kain and Destombe, 1995).

unique cDNAs for the sporophyte and seven specific for product of a single fusion of gametes, are numerous and
the gametophyte, including elongation factor alpha and genetically identical. Each spore can develop into a
lipoxygenase encoding genes have been isolated from P. diploid tetrasporophyte in which reproduction involves
purpurea. meiosis, resulting in haploid genetically variable
tetraspores (Chen et al., 2009).
Gracilaria has a life history involving three distinct
Gracilaria stages: gametophytes, carposporophytes and tetra-
sporophytes. Researchers have been engaged in the
Gracilaria lemaneiformis is a commercially important study of the mechanisms of phase formation since 1976
agarophyte that can be used to produce agar, a major (Ren and Zhang, 2008). With the development of
ingredient of dairy products, surgical jellies, ointments, molecular biology, great progress has been made
cosmetics and healthcare products (Chen et al., 2009). recently (Ye et al., 2006). Six inter simple sequence
Gracilaria, along with Porphyra, Laminaria and Undaria repeat (ISSR) primers, which had proved previously to be
has a bulk production by farming in China. It is not only able to yield clear bands in Gracilaria, were used to
an economically important algae species, but also a good distinguish the phases and sexes of G. lemaneiformis
material for genetical studies (Bird and Mc Lanchlan, (Sun et al., 2003). Until now, several phase-specific and
1982). Thus, it is important to pursue basic studies on sex-specific genes have been identified. A heat-shock
Gracilaria. protein encoding gene, which might be involved in the
In most populations of Gracilaria, the life history is like differentiation of female gametophyte, has been identified
that of the Polysiphonia type, that is, having in Griffithsia japonica (Lee et al., 1998). An ubiquitin gene
morphologically identical diploid tetrasporophyte and of G. lemaneiformis during phase formation is identified
haploid gametophyte phases, the latter consisting of and characterized (Ren et al., 2009). GlRab11, the first
equal numbers of male and female plants (Figure 6). The functional Rab-like protein identified in G. lemaneiformis
female gamete is fertilized in situ and the zygote was isolated and the cDNA full-length of GlRab11 was
develops as a third phase, the diploid carposporophyte, a obtained (Ren et al., 2008). Sun (2002) reported an
spore-producing structure entirely dependent on the analysis of 180 ESTs of the G. lemaneiformis
female gametophyte. The resulting carpospores, the tetrasporophyte cDNA library. Suppression subtractive
4714 Afr. J. Biotechnol.

hybridization (SSH) was employed between RNA reinhardtii, as analyzed by mutants for gametogenesis. Plant Cell.
Physiol. 46:312-316.
extracted from female gametophyte and tetrasporophyte.
Armbust EV (1999).. Identification of a new gene family expressed
Fourteen cDNAs are identified, among which SSH466 is during the onset of sexual reproduction in the centric diatom
a putative tetrasporophyte-specific gene (Ren et al., Thalassionsira weissflogii. Appl. Environ. Micrbiol. 65: 3121-3128.
2006). Gracilaria is dioecious, it is shown that the sex of Bird CJ, Lanchlan JMc (1982). Some underutilized taxonomic criteria in
f m Gracilaria (Rhodophyceae, Gigrtinales). Bot. Ma. 25: 557-562.
Gracilaria is determined by a pair of alleles, mt and mt .
f Bird CJ, Lanchlan JMc (1984). Taxonomy of Gracilaria: evaluation of
In gametophyte generation, mt determines female some aspects of reproductive structure. Hydrobiologia, 116/117: 41-
m
gametophyte and mt determines male gametophyte. In 46.
sporophyte generation, this pair of alleles is in mtf / mtm Brodie JA, Irvine LM (2003). Seaweeds of the British Isles. Volume 1
Part 3b. London: The Natural History Museum.
heterozygous state (Zhang et al., 2005). Chen P, Shao HB, Xu D, Qin S (2009). Progress in Gracilaria biology
and developmental utilization: main issues and prospective. Rev. Fish
Sci. 17: 494-504.
FUTURE PROSPECT Drebes G (1977). Sexuality. Botanical Monographs, 13: 250-283.
Drew KG, Kathleen M (1949). Conchocelis-phase in the life-history of
Porphyra umbilicalis (L.) Kütz. Nature, 164:748-74.
Algae are of great economical, ecological and social Evans LV (1965). Cytological studies on the Laminariales. Ann. Bot.
significance. They are also good research materials in Nbew. Series, 29: 541-562.
biology and molecule researches. At present, however, Fernandez LE, Valiente OG, Mainardi V, Bello JL, Velez H, Rosado A
(1989). Isolation and characterization of an antitumor active agar-type
there are still many shortages in this field, such as polysaccharide of Gracilaria dominguensis. Carbohydr. Res. 190: 77-
cloning and analysis of genes which are crucial in growth, 83.
development and sex differentiation. Biological growth, Ferris PJ, Armrests EV, Goodenough UW (2002).Genetic structure of
differentiation, cell cycle regulation and also response to the mating-type locus of Chlamydomonas reinhardtii. Genetics, 160:
181-200.
stimulation, are all regulated by gene expression. Gene Ferris PJ, Woessner JP, Goodenough UW (1996). A sex recognition
expression depends on the differentiation stage of glycoprotein is encoded by the plus mating-type gene fus1 of
organism, characteristics of genes and environmental Chlamydomonas reinhardtii. Mol. Biol. Cell. 7: 1235-1248.
factors. Whether in lower or higher organisms, gene Fraser JA, Diezmann S, Subaran RL, Allen A, Lengeler KB, Dietrich FS
expressions at different developmental stages and parts (2004). Convergent evolution of chromosomal sex-determining
regions in the animal and fungal kingdoms. Plos. Biol. 2: p. 384.
show significant diversity, which is a prominent feature of Gloeckner G, Beck CF (1997). Cloning and characterization of LRG5, a
gene. With the explosive development of molecular gene involved in blue light signaling in Chlamydomonas
biology and information technology, more and more gametogenesis. Plant J. 12: 677-683.
Goodenough UW, Armbrust EV, Campbell AM, Ferris PJ (1995).
researchers are devoted to explore the molecular mecha- Molecular genetics of sexuality in Chlamydomonas. Annu. Rev.Plant.
nism of biological development, including sex deter- Physiol. Plant. Mol. Biol. 46: 21-44
mination and differentiation. It can be easily predicted Goodenough UW, Lin H, Lee JH (2007). Sex determination in
that human understanding of biological evolution and Chlamydomonas. Semin. Cell. Dev. Biol. 18:350-361.
Han T, Han YS, Kain JM, Häder DP (2003). Thallus differentiation of
development will continue to progress. In the past few photosynthesis, growth, reproduction, and uv-b sensitivity in the
years, a series of genes involved in algae sex deter- green alga Ulva Pertusa (Chlorophyceae). J. Phycol. 39: 712-721.
mination have been identified and analyzed which are Hasle GR, Syvertsen EE, Steidinger KA, Tangen K, Tomas CR (1997).
really helpful in elucidating sex determination mecha- Identifying Marine Diatoms and Dinoflagellates Marine Diatoms.
nism. Progresses in this field will greatly promote the Massachusetts: Academic Press
Hoek C, van den Mann DG, Jahns HM (1995). Algae: An Introduction to
understanding of biological evolution and enable us to Phycol. Cambridge: Cambridge Univ. Press.
carry out beneficial biological modification. Horner RAA (2002). Taxonomic Guide to Some Common Marine
Phytoplankton. Bristol. Bio. press. Ltd.
Lee YK, Kim SH, Hong CB, Chah OK, Kim GH (1998). Heat-shock
ACKNOWLEDGEMENTS protein 90 may be involved in differentiation of the female
gametophytes in Griffithsia japonica (Ceramiales, Rhodophyta). J.
This work was jointly supported by The Science and Phycol. 34: 1017-1023.
Lee RE (2008). Phycology, 4th edition. Cambridge: Cambridge Univ.
Technology Development Plan of Shandong Province Press.
(2010GSF10208), One Hundred-Talent Plan of Chinese Liu QY, Baldauf SL, Reith ME (1996). Elongation factor 1 alpha genes of
Academy of Sciences (CAS), the CAS/SAFEA red alga Porphyra purpurea include a novel, developmentally
International Partnership Program for Creative Research specialized variant. Plant Mol. Biol. 31: 77-85.
Liu YS, Li LH, Wu WK, Zhou ZG (2009). A scar molecular marker
Teams, the Important Direction Project of CAS (KZCX2- specifically related to the female gametophytes of Saccharina
YW-JC203) and the Strategic Priority Research Program (Laminaria) Japonica (Phaeophyta). J. Phycol. 45: 894-897.
of the Chinese Academy of Sciences (XDA01020304). Mitman GG, van der meer JP (1994). Meiosis, blade development, and
sex deremination in Porphyra prupruea (Rhodophyra). J. Phycol. 30:
147-159.
REFERENCES Miyamura S (2004). Sex specific arrangement of cell fusion site in
marine green alga, Ulva Arasakii. J. Plant. Res. 117: p. 40.
Abe J, Kubo T, Saito T, Matsuda Y (2005). The regulatory networks of Mizuta H, Kai T, Tabuchi K, Yasui H (2007). Effects of light quality on the
gene expression during the sexual differentiation of Chlamydomonas reproduction and morphology of sporophytes of Laminaria japonica
 Peng et al. 4715

Phaeophyceae). Aquact. Res. 38: 1323-1329. Sun X, Zhang XC, Mao YX, Liu JJ, Sui ZH (2003). ISSR analysis of
Nimura K, Mizuta H (2002). Inducible effects of abscisic acid on marine red algae Gracilaria (Rhodophyceae). High Technol. Let. 13:
sporophyte discs from Laminaria japonica Areschoug (Laminariales, 89-93.
Phaeophyceae). J. Appl. Phycol. 14: 159-163. Thomas D (2002). Seaweeds. London: The Natural History Museu.
Pan JM, Having MA, Beck CF (1997). Characterization of blue light Tseng CK, Xia BM (1999). On the Gracilaria in the western Pacific and
signal transduction chains that control development and maintenance the Southeastern Asia region. Botanica. Marina, 42: 209-217.
of sexual competence in Chlamydomonas reinhardtii. Plant Physiol. Wilson NF, Foglesong MJ, Snell WJ (1997). The Chlamydomonas
115: 1241-1249. mating type plus fertilization tubule, a prototypic cell fusion organelle:
Pang SJ, Hu XY, Wu CY (1997). Intraspecific crossing of Undaria Isolation, characterization, and in vitro adhesion to mating type minus
pinnatifida (Harv.) Sur-A possible time-saving way of strain selection. gametes. J. Cell, Biol. 137: 1537-1553. Woelkerling WJ (1990). An
Chin. J. Oceanol. Linmol. 15: 227-235. introduction: Biology of the red algae. Cambridge: Cambridge Univ.
Pang SJ, Wu CY (1996). Study on gametiphyte vegetative growth of Press.
Undaria pinnatifida and its applications. Chin. J. Oceanol. Limnol. 14: Yang GP, Sun Y, Shi YY, Zhang L, Guo SS, Li BJ, Li XJ, Li ZL, Cong YZ,
205-210. Zhao YS, Wang WQ (2009). Construction and characterization of a
Pang SJ (1998). Intraspecific crossings of Undaria pinnatifida (Harv.) tentative amplified fragment length polymorphism-simple sequence
Sur-on morphological and growth variability of Juvenile sporophytes. repeat linkage map of Laminaria (Laminariales, Phaeophyta). J.
Oceanologia. Et. Limnologia. Sinica, 29: 577-581. Phycol. 45: 873-878.
Ragan MA, Bird CJ, Rice EL, Gutell RR, Murphy CA, Singh RK (1994). Ye NH, Wang HX, Wang QC (2006). Formation and early development
A molecular phylogeny of the marine red algae (Rhodophyta) based of tetraspores of Gracilaria lemaneiformis (Gracilaria, Gracilariaceae)
on the nuclear small-subunit rRNA gene. Proc. Natl. Acad. Sci. 91: under laboratory conditions. Aquaculture, 254: 219-226.
7276-7280. Zhang QS, Tang XX, Cong YZ, Qu SC, Luo SJ, Yang GP (2007).
Re XY, Sui ZH, Mao YX, Zang XN, Xu D, Zhang XC (2009). Cloning and Breeding of an elite Laminaria variety 90-1 through inter-specific
characterization of two types of ubiquitin genes from Gracilariopsis gametophyte crossing. J. Appl. Phycol. 19: 303-311.
lemaneiformis (Gracilariales, Rhodophyta). J. Appl. Phycol. 21: 273- Zhang XC, Qin S, Ma JH, Xu P (2005). The genetics of marine algae.
278. Beijing: Agric. Press.
Ren XY, Sui ZH, Zhang XC (2006). Cloning and characterization of
glyceraldehyde-3-phosphate dehydrogenase encoding gene in
Gracilaria/Gracilariopsis lemaneiformis. J. Ocean. Univ. Chin. 2: 146-
150.
Ren XY, Zhang XC, Mao YX, Sui ZH, Xu D, Zang XN (2008). Cloning
and characterization of a Rab11 homologue in Gracilariopsis
lemaneiformis. J. Appl. Phycol. 20: 1103-1109.
Ren XY, Zhang XC (2008). Identification of a putative tetrasporophyte-
specific gene in Gracilaria lemaneiformis (Gracilariales, Rhodophyte).
J. Ocean, Univ. Chin. 3: 299-303.
Santelices B, Doty MS (1989). A review of Gracilaria farming.
Aquaculture, 78: 59-133.
Schreiber E (1930). Untersuchungen uder parthenogenesis,
geschlechbestimmung and bastardierungsvermogen bei Laminaria.
Planta, 12: 331-353.
Stratmann J, Paputsoglu G, Oertel W (1996). Differentiation of Ulva
mutabilis (Chlorophyta) gametangia and gamete release are
controlled by extracellular inhibitors. J. Phycol. 32: 1009-1021.
Sun X, Yang GP, Mao YX, Zhang XC, Sui ZH, Qin S (2002). Analysis of
expressed sequence tags of a marine algae, Gracilaria/Gracilariopsis
lemaneiformis. Progr. Nat. Sci. 12: 518-523.