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The International Journal of Plant Reproductive Biology 7(1) pp. 8-31, 2015

Plant embryology, since the 19th century, has come a long way from descriptive and comparative embryology to the developmental biology (Fig. 1), reflecting the ontogeny and evolution of its mechanisms, "EvoDevo" (Dondua 2005).

The prerequisites of plant developmental biology is developed (Batygina, 2011a, b, 2012, 2013, and 2014), one of which: integration and development" ... "interdisciplinary studies" redeploying bridges between traditional disciplines and ... opening the way for the establishment of a universal science, designed to serve as a kind of framework unifying fragmented science in a whole " (Takhtajan 2007).

The creation of a new direction in science requires a certain amount of training the mind (Timofeev-Ressovsky 1980), methodology for studying the human mind and spirit in its higher manifestations, and technology of thinking (Beklemishev 1994). Special attention, "to understand each other", should be given to

DOI 10.14787/ijprb.2015.7.1.8-31

Wonderful orchids-Non-traditional notions on reproduction

T. B. Batygina

Komarov Botanical Institute RAS, Saint Petersburg, Russia

e-mail: [email protected]

Received: 07.06.2014; Accepted & Published online: 01.11.2014

ABSTRACT

From the viewpoint of non-traditional notions, the problem of integrity and reliability system is considered

one of the main problems of biology. The unique plants, the orchids, are of the special interest for studying this

problem. The especial attention must be paid to high totipotency and stemness of cells and diversity of modes

of vegetative propagation. The orchids are the excellent model object for study of various aspects of

developmental biology, particularly of the metamorphosis phenomenon in ontogenesis and its establishing in

evolution. In this regard, some tropical (Cymbidium hybridum) and boreal (Dactylorhiza maculata,

Hammarbia paludosa) orchids are considered. Some aspects of evolutionary processes in orchids are

discussed, which are related with reduction of their vegetative and generative structures leading to change in

behaviour of separate parts of plant. From the viewpoint of system approach and problem of integrity the

attempt is done to discuss some approaches to symbiosis at different hierarchy levels and possible reasons of

presence or absence of morphologically expressed fungus in the seed.

Keywords: Metamorphosis, reproduction systems, integrity and reliability system, apoptosis, protocorm–seedling, generative and vegetative structures.

Fig.1- Principal directions of developmental

biology (Batygina 2000)

the accuracy and clarity of concepts, theories, postulates, The notion of "morphogenesis", as noted by V. the axioms underlying the findings of any direction of all Beklemishev, is used to describe the phenomenon of the branches of science, their evidence, admissibility and body's development since its inception, while usefulness (van der Pĳ l 1969, Batygina 1974, "morfoprocess" is for individual stages.Beklemishev 1994).

Development of problem of integrity should be The basic principle of the creative research scientist carried out taking into account the categories proposed

must be the primacy of an in-depth study of the by us: the center of origin of species, ecology, ethology, genetics (genotype and phenotype), epigenetics, phenomenon in nature. Only in this case, the reserves ("doubling structures), failures, apoptosis, phenomenon can be understood in all its complexity and evolution (co-evolution) and the results of their diversity (Batygina 1974, 1987, 2011, 2014).integration (Batygina 1974, 2012, 2013, 2014).

In the light of the non-traditional views, the author Research of morfoprocesses has particular develops for many years one of the fundamental

perspectives from a position of problem of integrity and problems of biology: problem of integrity (Batygina reliability system (Batygina, 2011, Notov 2010). The 1992, 1994, 2011, 2012, 2013, 2014). The necessary undoubted relevance is the identification of the system

theoretical foundation to broaden and deepen research in of reserves (doubling structures – arhesporial,

this field is the study of morphogenesis and sporogenous cells, hidden reserves – apo- and

morfoprocesses, including the identification of diplosporous embryo sacs, monozygotic twins and

correlative dependencies in the development of various embryoids), failures, apoptosis, which are links in the reproductive and vegetative structures at different same chain and driving flexibility and tolerance hierarchy levels (superorganismic, organismic, organ, (adaptation) not only of the seed, but of the entire plant cellular, molecular) at all stages of ontogenesis, starting [(Fig. 2) (Batygina 1994, 2002, 2010, Batygina et al. from the origin of the organism. 1994, Sheridan et al.1996)].

2015 9Orchids-Non-traditional notions on reproduction—Batygina

Fig. 2— Reproduction of orchids form the angle of reliability of biological systems [Reserves ( “doubling

strucutre”), failures, apoptosis Batygina (1998).

Recently in various areas of science, scientists main cell lines involved in the genesis of embryos and

focused on the study of stem cells. One of the most shoot apices in Triticum, Cala, Anubias, Dioscorea, etc.).

important is the development of theoretical bases of This gave us the opportunity to give for the first time science on stem cells (origins – Zygote, properties, non-traditional ideas about zigote as a stem cell of the mechanism of niche and pool formation). However, for first order, which is the ancestor of all other plant stem many years a debate continues about who and why first cells. For the first time a complete definition of the used the notion "stem cell". properties of stem cells and their importance in ontogeny

In this regard, remembering the great Russian and evolution is revealed and presented in the literature

scientist V. N. Beklemishev, I would like to say that in (Batygina 2010, 2011, 2013, 2014, Batygina & Rudskiy

order to examine any phenomenon should "understand 2006, Rudskiy et al. 2011), and the notion on stem cell is

each other". extended in the light of the data on the new phenomenon

of embrioidogeny, which is the second type of vegetative The term "stem cell" appeared in the scientific propagation, where the structural unit is an embryoid.literature in the works of the famous German naturalist

and philosopher E. Haeckel (1868). He considered the All these issues were considered from the viewpoint

term "stem cell" (in “German Stammzelle”) in two ways: of genetic regulation of meristems.

single-celled ancestor of all multicellular organisms Discussion about these issues lasted for more than (1868) and fertilized animal egg cell (1877), giving rise 10 years.to all the cells of a multicellular organism.

Albert and Ezhova (2013) in their latest work have However, in the late 19th century, A. Weismann confirmed our theoretical developments with methods

(1883) used this term to describe some of the cells from of molecular biology (Batygina et al. 2004, Batygina & the embryos. Rudskiy 2006, Batygina 2010, 2011, 2013): “... the

In the Russian-language literature the concept notion on stem cells in plants must be significantly

appeared through the works of the prominent histologist expanded, and all cells that can form zygotic and somatic

A. Maksimov, who worked mostly on blood cells embryos should be considered as stem ones, including a

(Maximov 1909, 1916). zygote …”.

Briefly on some aspects of the concept of stem cells The authors confirm the need for the proposed

in plants, their origins and their significance, and briefly expansion of our earlier ideas about the types of stem

on the discoveries, which showed the great importance cells (see Batygina et al. 2004, Batygina & Rudskiy

of various aspects of biology. 2006), their localization and significance in ontogenesis:

zygote, embryoid initials, brood buds, adventitious The “dormant meristem” is identified in the leaf buds, shoot prokambium, méristème d'attente, etc. (see (Sachs 1887, Kerner von Marilaun 1896, 1898, Naylor the picture, presented by the authors, made on the basis 1932, Yarbrough 1932, McVeigh 1938, Batygina et al. of our published data).1996, 2006, 2010), in the ovule (Batygina & Freyberg

1979, Batygina 1991, Batygina & Vinogradova 2007), the Unfortunately, it is impossible to agree with Albert

“quiescent centre” in the apex of the root (Clowes 1954), and Ezhova, that the question on the self-maintenance of

“méristème d'attente” 1 in shoot apex (Buvat 1955). the zygote in plants in vitro culture was never raised

(Genetics, volume 49, no. 2, 2013, p. 157). Suffice it to While studying the properties, structures, ethology say on "identical twins" (twins, triplets, etc.) in plants and the genetics of stem cells, some researchers in the and animals, which are a brilliant example of a self-Laboratory of Embryology began studying and sustaining zygote, it became clear that their claim is not clarifying some issues in developmental biology, related quite fair (Batygina & Osadtchiy 2013).with this notion (see review: Batygina et al. 2004).

Various aspects of these works are ongoing in a number I wish to draw the attention of the reader that,

of model objects (for example, an attempt was unfortunately, the authors use the term “somatic

undertaken to build models of genealogical trees of the embryoidogenesis” in their work, which is in our view

10 Jan, 7 (1)The International Journal of Plant Reproductive Biology 7(1) pp.8-31, 2015

i nappropr i a t e ( t au to logy) . The no t ion o f some mechanisms for switching over developmental “embryoidogenesis” indicates by itself the formation of programs in some taxa, expanding notions on structures of somatic origin (see Batygina 2011). phenomena o f s t emness , embryo idogeny,

polyembryony, genetic heterogeneity of seeds, In the light of the non-traditional ideas the role of viviparity, multiplicity of ontogenesis, considering some stem cells in switching different morphogenetic of the issues of evolutionary biology from the viewpoint developmental programs in various plants is revealed, of stem cells, as well as developing some principles of e.g. from the sexual mode of reproduction to the asexual

formation of systems of reproduction that define one (peony, etc.), as well as implementation of

morphogenetic potentialities of ovule and embryo sac reproductive strategy of species (Batygina 2010, 2011, cells at different types of development (Batygina, 2009- 2013, 2014):2011; Batygina & Vinogradova 2007, Vinogradova üThe principle of self-regulation and self-2013). The universal phenomenon of multistage, and organization of the integrated system, the organism;possibly repeated, transformation of developmental

üThe principle of structural organization, spatial-program in the life cycle is based on two main unique temporal coordination and diversity of embryonic properties of plant cell, the totipotency and stemness. At structure development.that, it should be noted that not every cell possesses

üThe principle of universality of morphogenesis totipotency, not every totipotent cell can become a stem pathways, accompanied by ambiguity, diversity of cell, and not every stem cell is able to form a new matrix processes and heterogeneity of cells.individual (Batygina 2010, 2011). It should be noted that

the totipotency may be accompanied by the ambiguity of üThe principle of continuity of morphogenesis and the matrix processes and cell heterogeneity. These the diversity of modes (sexual, asexual, apomixis), properties condition the continuity of morphogenesis pathways of morphogenesis (embryogenesis, and polyvariancy of modes (sexual, asexual, apomixis) embryo idogenes i s , gemmorh izogenes i s , and forms (viviparity) of reproduction, as well as callusogenesis), forms of reproduction (viviparity, pathways of morphogenesis, leading to the formation of etc.).a new individual (embryogenesis, embryoidogenesis,

üThe principle of integrity and mechanisms of gemmorhizogenesis and kallusogenesis) (Batygina

reliability system: reserves, failures, apoptosis, 1994, 1999; Batygina & Babro 2012, Batygina 2011,

cloning and switching over developmental program.2013).

üThe principle of redundancy and competition of In this connection, particular attention should be

units at cellular, organismic and superorganismic paid to the structure and functioning of the somatic and

level as a foundation for sustainable development stem cells. The somatic cell can be considered in this

(stem cells, soil seed bank, etc.).aspect as a “cornerstone” in morphogenesis,

üThe principle of the universality of phenomena in ontogenesis, evolution and reproduction of plants. the development of plants and animals (totipotency, Probably, one should talk about lack of a gap between sexual, somatic and stem cells, metamorphosis, sexual, stem and somatic cells, as well as about the somatic embryogenesis (embryoidogenesis), possibility for homologation of some stem and somatic embryoidogeny, polyembryony, viviparity, etc.).cells with egg cell, “fertilized egg cell” and zygote

(Batygina 2010, 2011). Progress in the study of stem cell üThe principle of the universality of the phenomenon theory will be associated with three major promising of switching over the morphogenetic developmental directions in the study of stem cell in the life cycle of programs, species specificity and possible plants (see Batygina 2011, p. IX). recurrence of their changes.

Complex system analysis of listed problems of üThe principle of determining role of somatic developmental biology using previously developed an evolution in integration of various structures at

innovative approach for the first time allowed revealing different hierarchy levels.


The developed principles of organization of systems At the beginning of the 20th century the concepts of

of reproduction provide flexibility and tolerance and the universal organizational science, the tektology were

determine the reproductive strategy of the species in the developed, the main concern is the search for

ontogeny, life cycle and evolution. organizational principles that underlie all types of

systems (Petrovitch, 1906, Bogdanov 1922). They For a long time, and especially now, scientists served as a source of General systems theory (L. von increasingly consider some general biological Bertalanffy 1950, 1962) and Cybernetics (Wiener 1948)."planetary" problems and issues related to the study of

the biosphere, with the general regularities of living and One of the most important trends in biological

nonliving nature. Researchers have paid particular science is the development of the notion of “biological

attention to the phenomenon of enantiomorphism, i.e. systems” in the aspect of the problem of “systemacity”.

“left-” and “right-handeness” related to the problem of Considering of biological objects as systems allows the

leftishness and rightishness, which has been considered specification of the basic biological laws (Malinowski &

for representatives of the various kingdoms: gastropods, Uyomov 2001).

cereals, etc. In the 20th century it was considered that The system approach and the development of some enantiomorphism is probably related to the influence of models of biosystems, executed on living organisms, the Earth's axis. have made a major contribution to the general theory of

At the same time, from the perspective of the systems and have proved to be promising to solve many

phenomenon of enantiomorphism the brilliant scientists, problems of practical importance in biology (Batygina

S.G. and M.S. Navashin had undertaken a unique work 1983, 2014, Batygina & Vinogradova 2007,

on studying the nuances of the double fertilization, as Vinogradova 2013), allowing to unite scientists around

well as a detailed study of mitosis in somatic cell. the world for the development of science-consumptive

technologies.In the 50's-60's of the 20th century the interesting

works appeared for the first time, continued currently by Development of biological system of plants allows

some scientists, that are focused on the study of the wider and more global considering main statements of

influence of magnetic lines on the ontogeny of different the theory of reproduction, morphogenetic development

plants, taking into account certain influencing factors. programs and mechanisms of their switching over,

All of the above is of great interest both for our planet's where a key role is played by somatic and stem cells, as

fundamental research and applied works related to the well as the integrity and systems of reliability of

study of all the nuances of individual development. organism (reserves, failures, apoptosis) (Batygina 1968,

These works revealed that the phenomenon of 2014).

enantiomorphism defines the difference in grain harvest In biological systems the components at different from cereals: from “right” wheat seedlings compared to levels of organization interact with each other and the the “left” ones. Now one of the most important issues is environment. Hierarchical organization of biosystems the detailed study of the morphogenesis and genetics of illustrates the continuity and discretisation of these grains, and the inheritance of these traits. development. As far as systems merge into larger

It should be noted that currently some scientists functional units, these new systems get unique

consider these excellent experimental works performed properties not available at the previous level.

in 60-ies of 20th century (see Kasinov 1973, Urmantsev Biosystems have properties that cannot be reduced to the

1974). sum of the properties of their constituent subsystems.

I would like to refer to one of the most important The problem of integrity and system of reliability, as

questions of biology. I believe that further study and we have pointed out above, is one of the most important

understanding of global issues related to our biosphere is problems of biology. Of particular interest to study of this

impossible without the development and use of systems problem are unique plants – orchids. Because of their

science, and particularly of biological systems. great morphological and taxonomic diversity


(Averyanov 1977, 1979, 1991, Arditti 1992, 1993, 2008, the reduction of the ovule, endosperm and number of

Vakhrameeva et al. 1991, Pridgeon et al. 2001, 2003, stamens, and the formation of pollinaria.

2005) and a number of features of their reproductive According to various authors, there is a wide biology, they are an excellent model object to examine variation in the amount of the smallest seeds in the different aspects of biology. They have an amazing orchid fruit: Listera ovata – 807, Maxillaris sp. – variety of forms and colours of the flowers, and the 17564000, Cattleya sp. – 40000000 (Salisbury 1942, complex, diverse and often unique relationships with Poddubnaya-Arnoldi 1954).pollinators (Nazarov & Batygina 1990, Nazarov 1995).

In the evolution of orchids the selection occurred for Recently for 20 orchid species of the Crimea the 98

the production of a large number of seeds for the expense species of insects-pollinators had been revealed. All of

of reducing the biomass per seed that indicates a trend of this confirms the view of orchids as a phenomenon of the

general reduction in family Orchidaceae and correlates plant kingdom (Ivanov et al. 2009).

with perfecting alleloparasitic lifestyle (Teryokhin Orchids are actively evolving, as evidenced by the 1977). It should also be noted that the evolution of the

configuration of reproductive structures in individuals seed in orchids was designed to increase its sailing of one species and the high frequency of interspecific capacity (Averyanov 1991).and intergeneric hybridization (Averyanov 1991).

As already noted above, seed reproduction depends A number of outstanding features are typical of specific pollinators and symbionts in biocoenoses.

for orchids, among which one of the most important This makes orchid species sensitive to violations of is the high level of totipotency and stemness of their established consort relations (Nazarov 1995).cells. This property allows different pathways of

Duration and pace of the process of fertilization are morphogenesis (embryogenesis, embryoidogenesis,

species-specific and determine the further development gemmorhisogenesis, callusogenesis), modes of

of the sexual embryo and seed. In some species a sexual organism formation (sexual, asexual, apomixis) and

embryo and nuclear endosperm form as a result of forms of reproduction (viviparity), which manifests

double fertilization. In other ones the single fertilization itself in a variety of modes of vegetative propagation: by

is observed, when the embryo forms, but the primary mean of embryoids, buds and brood buds, conditioning

nucleus of endosperm does not form.their rapid distribution and biodiversity (Batygina 1968,

For orchids the phenomenon of polyembryony is 1974, 1998, 2010, 2011, 2012, 2013, Batygina & peculiar (Fig. 3), which is characterized by genetic Vasilyeva 1980, 1983, Batygina & Bragina 2011, heterogeneity of seeds: sexual embryo, somatic embryo Batygina & Babro 2012, Batygina et al. 2003).

We first developed and subsequently

improved classification of different types of

orchid reproduction (Batygina 1998, 2001-

2010, 2012, 2014).

The essential problem of orchid

developmental biology is the study of

evolutionary processes associated with the

reduction of their generative and vegetative

s t r u c t u r e s a n d m o r p h o p r o c e s s e s

(development of the embryo, endosperm),

changing the behavior of individual plant

parts. The major trends are revealed in the

evolution of the gynoecium and androecium

that are increase in placental surface of the

ovary, in the number of embryo sac types,


Fig.3 — Polyembryony formation of embryos of different origin-sexual and somatic in the single seed (sexual and asexual proceed simultaneously). A-Zygopetalum mackayi (Poddubnaya - Arnoldi 1959), B-Hammarbya paludosa (Bragina 2001).


(embryoid) out of the zygote (Eulophia), out of the

nucellar and integumentary stem cell (Nigritella nigra,

Spiranthes cernua), out of the synergids and antipodals

(gametophytic apomixis) (Orchis militaris, Calanthe

veitchii) (Figs. 4, 5) (Batygina 1999, Batygina &

Vinogradova 2007, Batygina & Osadtchiy 2013). One

must again emphasize the fact that orchids are

characterized by the formation of a large number of

embryoids (somatic embryos) a t different

developmental stages of generative and vegetative

structures (e.g. on Hammarbia paludosa leaf) (Batygina

& Bragina 1997).

The development of the fruit, embryo and seed in

orchids is a multistage process, metamorphosis (Fig. 6)

(Batygina & Vasilyeva 1980, 1983, Shevtsova &

Batygina 1987, Rasmussen 1995, Tatarenko 1996, 2007,

Batygina 1998, Batygina & Andronova 2000, Mamaev

et al. 2004, Kolomeytseva 2005, 2006, Shirokov et al.

2005, Yamazaki & Kazumitsu 2006, Vakhrameeva et al.

2008, Cherevchenko et al. 2008, Mayer et al. 2011,

Kolomeytseva et al. 2012, Batygina 2012, Bektas et al.

2013).

Fig.5 Embryoidogenous and embryogenous types of asexual and sexual reproduction (Genetic heterogeneity of seeds). Variants of combinations of embryos at various development character of gametophyte exsist, (Batygina 1989).

—

Fig. 4 — Types of reproductive embryoidogeny in orchids. (1-Swamy 1943, 2-Afzelius 1928, 3-Swamy 1948,

4-Savina 1979, 5- Poddubnaya-Arnoldi 1969).

zones: the apical and basal one (Fig. 7 detail 1). Cells of

apical area are small, actively dividing, with dense

cytoplasm. Parenchyma cells of the basal zone are large,

strongly vacuolated. This stage of the C. hybridum is

critical in the development of the seed, because the

embryo is capable of autonomous development

(Cherevchenko et al. 1982, Batygina & Vasilyeva 1983).

In the later stages of seed development the cells of the basal part of the embryo are usually characterized by disintegration, dedifferentiation and further differentiation (Batygina & Shevtsova 1985, Shevtsova et al. 1986, Shevtsova & Batygina 1987).

The mature embryo in the seed before germination is an organism possessing tissue differentiation. Then it As model objects some tropical (Cymbidium can enter dormancy, which presence and duration are

hybridum) (Figs. 7, 8) and boreal (Dactylorhiza species-specific. A polymorphism of the structure of

maculata, Hammarbia paludosa) orchid species were embryos appears in different species.

used (Figs. 9-12) (Batygina & Shevtsova 1985, The issue on the structure of orchid embryo,

Shevtsova et al. 1986).including the presence or absence of cotyledons was

Upon the formation of the Cymbidium hybridum disputable. For the first time on the basis of comparative seed the differences in the structure and function of embryological studies of different orchid species it was apical and basal zones of the embryo are revealed. The established, that the embryo found in all studied species embryo is multicellular with epidermis, haustorial has no cotyledon neither in seed nor in postseminal

development (Batygina & Vasilieva 1980 1983, suspensor and poor histological differentiation into two


Fig. 7 Morphogenesis of embryo and protocorm (Cymbidium hybridium).1. embryo-globular stage, 2. mature seed at swelling stage, 3. apical part of protocorm, cell division, 4. seedling. (am : apical meristematic zone of embryo; ar : adventitious roots; cs : conductive system; ep : epidermis; su : suspensor; sc : seed coat; sa

: shoot apex). (Batygina & Shevtsova 1985).

—

Fig. 6 — Morphogenesis of seed and embryo (Dendrobium

nobile - Poddubnaya-Arnold 1959).

Batygina & Andronova 1986, 1988). parenchymal cells containing proteins and lipids, and

functions as a “storage organ”, functionally Seedling of C. hybridum initially consists of compensating absence of endosperm in mature seed. In differentiated parenchyma cells, enclosed by single-some cells cytomixis is observed. The procambial strand layer epidermis, and has an obvious suspensor (Fig. 7 arises upon shoot apex formation. For further details of 2 & 3). In the course of its further development development seedling needs a contact with the fungus. the two zones become distinguishable in it. The apical After penetration of the fungal hyphae into the seedling zone (≈ 1/3 of the seedling) consists of small actively body the growth of meristem in apical part of the dividing cells, where the apex of the future shoot embryo, the formation of the shoot apex and the growth initiates endogenously and procambial strand of the seedling for expense of cell extension in its basal differentiates. Cells of the basal zone (≈ 2/3 of the part start. In the course of differentiation of shoot apex seedling) are larger, contain a lot of starch and fulfill the leaf primordia form (Batygina & Vasilyeva 1980, storage function. Further the differentiation of leaf 1983, Batygina & Andronova 2000). primordia and development of the conductive system

occur. Later adventitious root initiates endogenously The leaf primordium at early developmental stage (Fig. 7 detail 4) (Batygina & Shevtsova 1985). appears as a roller. As primordium grows, the hole

limited by the roll edges gradually shifts into the lateral Germination of Dactylorhiza maculata seed is position, likewise it appears on Fig 12 in Bletilla and accompanied by an increase of embryo and its Thunia. Primordium gets the shape of a cone (Figs. 8 & “swelling” (Fig. 9). Seed coat breaks, and the seedling 9). Leaf organs of the protocorm appearing in appears through it. The apical part of the seedling, postseminal development are true leaves (Batygina & consisting of small cells with no starch is the shoot apex. Vasilyeva 1980, 1983, Batygina & Shevtsova 1985, The basal part of the seedling consists of large polyploid


Fig. 8 — Formation of numerous apical meristems on protocorm in vitro (Cymbidium hybridum). Numerous protocorms (1, 1a); development of two apexes on protocorm : appearance (2) and on longitudinal section (2a); formation of five-six protocomrs in different developmental stages; appearance (3) and on longitudinal section (3a) (pr,pr1-pr4 - Protocorm; sa - shoot apex; - - line of possible division into parts). Batygina & Shevtsova 1985


Fig. 10 Development of tuberoid in orchid (Dactylorbiza maculata) (Batygina et al. 2003). (1: Juvenile Plants; 2 : plants of differnet age groups; 3 : generative plants)

—

Fig. 9 — Morphogenesis of embryo and protocorm in natural conditions in Dactylorbiza maculata (Batygina 1997) (l: leaf; pr: protocorm; sa: shoot apex; Bar = 10 micron).

Batygina & Andronova 1988, 1991, 2000). rhizomes, tuberidia and brood buds.

Thus, many orchids are characterized by three types Hammarbya paludosa is the only representative of reproduction: sexual (embryogenous) and of the orchids, which is characterised by viviparity, the two types of vegetative (embryoidogenous and brood buds (propagules) development on the leaves. gemmorhizogenous). Propagules form exogenously due to proliferation of

upper epidermis of the leaf. Formed propagule consists The characteristic feature of orchid plant is the

tendency for vegetative reproduction of two types of leaf completely covering the shoot apex and the

overgrown first internodule. Initiation and development (embryoidogenesis and gemmorhizogenesis), which is

cloning, realizing at different stages of ontogenesis (Fig. of the adventitious root occurs after the separation of 11) (Batygina, 2010). In in vitro culture we have propagule from the leaf. In 11.5% of the plants the identified two ways of protocorm cloning: development propagules form on the old pseudobulb as a result of the of a large number of shoot apices with endogenous reactivation of the apical meristem. In rare cases, formation of adventitious roots (gemmorhizogenesis) vegetative reproduction of H. paludosa occurs by means (Figs. 8, 2, 2a); formation of multiple protocorm of the creation of additional axillary shoot. Along with (embryoids) from the cells of the epidermis and vegetative propagation, H. paludosa reproduces also by subepidermis of protocorm (Figs. 8, 3, 3a) (Batygina & seeds (Batygina & Bragina 1997).Shevtsova 1985, Shevtsova et al. 1986, Batygina et al. As a developmental biologist and embryologists I 2003, Batygina 2010, 2011, 2012, 2013).

would like to address briefly some of the general and

particular questions, related to the developmental Vegetative propagation at virginile and generative

stage of ontogeny is realized in many species by mean of biology of orchids, and especially the mechanisms of


Fig. 11 — Morphogenesis of embryo and protocorm in vitro in Dactylobriza maculata (Batygina & Vasilyeva 1983) (am: apical meristematic zone of embryo; amp: apical meristematic zone of protocorm; ar: adventitious root; l: leaf; pr: protocorm; su: suspensor; sa: shoot apex).


Fig. 12 – Polymorphism of protocorms and the first leaf development in orchids in natural conditions and in vitro culture. [1-3 : Dactylorhiza maculata (Batygina et al. 2003) 4-6 : Bletilla striata and 7-9 : Thunia alba, culture in vitro (Batygina & Andronova 1988) fl: first leaf; sa: shoot apex; Bar = 10 micron].

construction has similarities with that of sporophyte of their evolution.clubmosses (Bernard 1909, Andronova et al. 2009).T h e f u n d a m e n t a l e l a b o r a t i o n s o n t h e

morphogenesis and evolutionary establishing of the In the early 20th century, the term "protocorm" was embryo in various monocot species, particularly cereals used for the orchids quite rarely; historically its (Batygina 1968, 1969, 1974, 1977-2013), allowed synonymous terms are “embryonic tubercle” and comparing some of the mechanisms of morphogenesis “seedling” (Bernard 1916, 1932).regularities of the orchid and cereal embryo, and

For many years, the discussion continues on the establishing the parallelism in their development, of

scope of the notions of “seedling” and “protocorm”, course taking into account their specifics (symmetry

their functions and roles in the ontogeny and evolution. I changing during embryo development: radial,

believe that the various authors had received a lot of dorsoventral; the dorsoventral character of shoot apex

interesting data on this subject. However, due to the initiation, the character of initiation of leaf as a “roller”

limitations of this article we have included them just in and root as adventitious, the presence or absence of

the list of the literature.cotyledon).

In this regard, the question on parallelism in In postseminal development of the orchid embryo,

development of protocorm (seedling?) in orchids and like in most flowering plants, as we suppose, a seedling

Lycopodium and on their origin is still unclear.forms with some particular characteristics, e.g. in the

From my point of view, the lack of detailed data on the majority of orchids lack of cotyledons had been revealed structure of the Lycopodium germ, as well as the lack of the (Batygina & Andronova 1991, 2000).nuances of similar data for orchids says that it is not quite

Considering the seedling of the various orchid correct to speak about their similarities. Further elaboration

species, one will have to dwell on the notion of of this issue is necessary using a system approach at

protocorm (Greek protos – primary, first; cormos – stem, different levels of the hierarchy, the comparative study of

shoot, tubercle), which was introduced for the first time morphogenesis and morphoprocesses in these systems, and

in literature by Treub (1884, 1886) upon examining the different methods of research, in particular molecular.

germ of Lycopodium cernuum, and further applied to Using the system innovative approach, I will try to orchids. Treub had referred to as protocorm the structure

approach the complicated issue, which is of the liveliest forming during development of the embryo of interest in biology: the study of the ontogeny and Lycopodium, which functions as the storage organ, has evolution of diverse orchid plants.the shape of a hemisphere covered with hairs and

contains hyphae of the fungus in the cells. I suggest we use the concept of “biosystem” as a

model to consider critical issues related to the Due to the lack of detailed data for different developmental biology of orchid plants at different Lycopodium species on morphostructure and genetics of stages of morphogenesis and hierarchical levels, as well protocorm, which is presumably a “container” of the as some aspects of the symbiosis.fungus, supplying nutrients, I think it would be

premature to talk about the structure and origin of the In view of the foregoing, for most orchidologists the protocorm and entire seedling in the ontogeny and questions would probably represent a keen interest of:evolution of this taxon. I think the most interesting

How do protocorm and seedling correlate in orchid questions are what the developmental stage of the

plants?“container” is when it gets a fungus, what is the critical

Where do the fungus comes from in the protocorm – mass of this fungus and structures related with it.seedling?

For the orchids term “protocorm” was introduced Most researchers believe that the fungus is already later, and today it is impossible to say who used it first present in the seedling.(Batygina & Andronova 2000). A number of authors Therefore, I suggest considering complex biosystem considering the seedling of orchids believe that its


rdconsider the 3 biosystem “fruit – seed – embryo – “the ovary-fruit-seed-embryo” taking into account the

spatiotemporal correlations (see Batygina 2011). At fungus – protocorm (?) – seedling” and examine in different developmental stages of the biosystem the details the following questions using the various following structures develop in it: the maternal methods of research:sporophyte – fruit wall, seed coat; gametophyte – embryo ·What is the origin of the initial cells of the seedling?sac, the egg apparatus, antipodals, endosperm; daughter

·Where the development of the orchid seedling sporophyte – embryo (taking into account the reduction).begins: in seed or postseminal development?

I think one should consider this biosystem from ·What is the cause of arising of the initial cells giving viewpoint of a morphologist, embryologist, anatomist,

physiologist, geneticist, cytogeneticist, epigeneticist, rise to the seedling shoot apex: their naturally

determined formation in post seminal development etc., and use their methods to understand the following

out of apical seedling cells independently of the two questions:

fungal influence, or penetrating of the fungus into üAt what stage the fungus “penetrates” the biosystem the fruit-seed-embryo?“ovary-fruit-seed-embryo”?

·What are the genetics (uniparental, biparental) and üWhich way the fungus appears inside the seedling, the origin (sexual or asexual) of the embryo in the which of the abovementioned structures are seed?influenced as a result of this event, and what

methods (embryological, cytogenetic, etc.) one can ·Is there any difference in interaction of a fungus with reveal these facts? sexual and somatic embryo (embryoid) and with I think that it is very likely to agree with researchers their initial cells?

claiming that the penetration of the fungus into seed ·How will the embryo or seedling development

conditions the all subsequent morphoprocesses, taking proceed in species that do not have contacts with the

place upon the development of the orchid embryo and fungus due to their developmental biology?

seedling.

Special attention should be given to the role of the In accordance with my new views on reproduction fungus in the ontogeny and evolution of various plant in plants from a position of the problem of integrity, taxa. Mycorrhizal symbioses are very well represented reliability system of the organism and morphogenetic in the world of plants: more than 80% of the species of developmental programs one should consider the terrestrial flowering plants and the gymnosperms form biosystem “ovary – fruit – seed – embryo” forming in the the mycorrhizae of some type, the fungal symbioses are process of orchids development (Batygina 1994, 2010, known also in sporous plants (Voronina 2010).2011, 2013).

Typically, the phenomenon of symbiosis was Probably, the integrity of this biosystem gets considered relating to the organismic level, and just disturbed by presence of the fungus. This induces some scientists have tried to interpret the objects of other specific switching over the morphogenetic

nddevelopmental program and creating a new 2 biological structural levels (populational, coenotic) with

symbiotic perspective (Savinov 2006, Pozdnyakova biosystem “ovary – fruit – seed – embryo – fungus”.

2013). This confirms my view that any biological Thus, the fungus acts as a trigger of this process.

phenomenon should be considered at different hierarchy From the perspective of system approach, problem levels (cellular, tissual, organismic, populational) of integrity and reliability the fungus as an organism can (Batygna 1987, 2010, 2013).be considered in different guises. In the course of

evolution it is mainly determined for the relationship Importance of symbiosis as evolutionary factor in with the plant, in which it “performs” its fundamental plants, particularly in orchids, remains quite unrevealed role in evolution by providing trophic function of “host”. and debatable, as it was emphasized earlier (Danilov

1921). Orchid plants probably were “born” at the moment In view of all of the above, one should probably


of the symbiosis formation and are the product of an early systems, which in its early stages of ontogenesis is the integration of the fungus and somatic (stem?) cell. interconnection of the fungal and the plant cells.

Biosystem "fungus-plant" developed firstly, as I From the viewpoint of non-traditional views, the believe that, namely as a result of a somatic co-evolution assumption can be made that at the dawn of the universe (Batygina 2010, 2011, 2013). Further, the system involved when the “fungi” and “plants” in the modern sense did not such phenomena as sexual process, double fertilization, exist, the interaction began between their seed and fruit, which have made substantial changes not “undifferentiated” (?) biosystems (biosystem of “fungus” only in inheriting, but on the first stages of uniting the and biosystem of “plants”), which had established a fungus with the plant. These phenomena already fall specific trophic relationships with each other. This early within the scope of the interests of embryology and contact of fungus with plant was probably a factor of cytogenetics. One can expect several trends in the evolution providing homeostasis (stable balance): the formation out of two biosystems “fungus” and “plant” of a plant becomes for the fungus a supplier of organic matter, new biosystem “fruit – seed – fungus – plant”:derived from photosynthesis, while the fungus, existing ·In some species the fungus periodically due to decomposition of complex substances supplied by

“penetrated” into the seed and integrated with its the plant provides a mineral food for the latter. Therefore, structures.the birth of the relationship between the fungus and the

plant was mutually profitable from the earliest stages of ·In other representatives of orchids genes of the their evolution. Symbiosis, which is considered fungus were probably “built in” the genome of nowadays, probably is the result of many hundreds of possible ancestors of orchids and most other plant

millions of years of the evolution. groups upon the formation of complex biosystem.

Maybe organisms “used” different epigenetic Of great interest is the hypothetical possibility of

mechanisms.early “association” of two ancestral biosystems

Perhaps, at present, many researchers working with “fungus” and “plant” in natural conditions into a single orchids are unable to see fungus in cells at some stages, biosystem by a mechanism, similar to the parasexual

th such as the fruit and the seed, but in fact it is present in the hybridization in vitro discovered in 50-60-ies of 20 cells, and can only be found with methods of century. Due to the possible lack of evident cell walls (?) cytogenetics and molecular biology.at any stage in their life cycle their protoplasts could

merge that resulted in “embedding” of the fungal In different orchids fungi penetrate the different genome into the genome of archaic plant at the early parts of the seed and organs of the new sporophyte stages of the symbiosis formation. This enables during its further development. Probably, the fungus

located in the plant can be inherited and influence the hypothetical figure that in some orchid species there will

course of morphogenesis of the new daughter organism not be the fungus in the seed, and hence the seedling also

will lack the fungus. In the course of evolution some from the earliest stages of its development.

orchids arose that have no fungus and propagation As noted above, the penetration of the fungus into occurs asymbiotically, with possible transition to the the embryo is the obligatory precondition for further symbiotic way during further development. seedling development in most orchids, and therefore

raises the question on the possible fungal induction of So, probably, the boundary between symbiotic and initial cells giving rise to the shoot apex of the seedling. asymbiotic reproduction of the orchids can sometimes In connection with the possible homologizing plant be conventional. Probably, this issue is a big problem somatic cells with a zygote, it is interesting to draw a taking into account their peculiar species diversity, and it parallel between the inducing role of the fungus is unclear whether it can be said that, as noted by some penetrating the somatic cell before initials formation authors, Orchidaceae are an extremely complex during germination, and similar role of a sperm cell, phenomenon that is the symbiosis of two cellular


Didymoplexis the mycorrhizal fungi are other than in entering the ovule during fertilization, that causes the most chlorophyll-bearing ones (Shmucker 1959).start of zygotic embryogenesis. This similarity might

suggest that the penetration of the fungal hyphae into the Probably, the fungus in its different forms can be somatic cells of the embryo initiates the process of inherited and influence the morphogenesis of seed and a embryoidogenesis, i.e. causes the formation of initial new organism from the early stages of its development.cell of the bipolar structure, the embryoid, and thus the Most plants interact with fungi and many of them protocorm formation in orchids can be attributed to the form a symbiosis (Famintsyn 1907, Kozo-Polyansky second type of vegetative propagation, i.e. the 1924, Purves & Hadley 1975, Selivanov 1981, Dĳ k embryoidogeny. If this assumption is correct, than the 1988, Smith & Read 2008, Provorov & Vorobyov 2012, embryoidogeny plays a much more important role in the Pozdnyakova 2013). life cycle of orchids than traditionally accepted, along

In our understanding the fungus is a factor, without with the sexual process and the first type of vegetative

which plants as such could not arise and develop up to propagation, the gemmorhizogeny. In this case, the present time.obviously it makes sense to offer up a new biosystem

The question remains only to Nature, how the “fruit – seed – embryo – fungus – embryoid process of switching over the morphogenetic (protocorm) – seedling”. This feature is of great interest developmental programs proceeded in course of the long

for the study, as if assuming the induction of co-evolution, that identified various biosystems, and

embryoidogeny phenomenon by fungus entering the how were the mechanisms and approaches “worked out”

somatic cell is true for orchids, then it may prove to be to “create” for orchids the biological system “fruit – seed

much more universal phenomenon involved from the – fungus – plant” (Various variants of biosystems are

earliest stages of evolution of the organic world, when possible).

the first interaction of primitive “undifferentiated” Acknowledgements — Author expresses cordial biosystems “plants” and “fungi” began, which was gratitude to colleagues and research workers or the considered above.Laboratory of Embryology and Reproductive Biology

Symbiotic germination under natural conditions is BIN RAS E. V. Andronova, E. A. Bragina, V. E.

much more common for orchids. Asymbiotic Vasilyeva, G. Yu. Vinogradova, E. E. Evdokimova, V. V.

development is known also in some of the more Nazarov, J. V. Osadtchiy and G. E. Titova, who have

specialized orchids, such as Laelia, Cattleya, some granted some materials and participated in discussion of

Cymbidium species (Burgeff 1936, 1954, Teryokhin this work.

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