Two types of germ cells, the sexual reproduction cycle, and the double-ring mode of plant developmental program

ABSTRACT

In this viewpoint, the usages of terms for progenitor cells to meiosis and gametogenesis are discussed. Terms for 2 types of germ cells, i.e. “diploid germ cells” and “haploid germ cells” were suggested to replace “archesporial cells” and “generative cells,” respectively, in plant developmental research. This suggestion was based on 2 newly proposed concepts, the “sexual reproduction cycle” for eukaryotes, and a “double-ring mode” of plant developmental program.

The concept that there are 2 types of germ cells, i.e., diploid germ cells (DGC) and haploid germ cells (HGC) in the plant life cycle was proposed in a recent paper entitled “Phosphorylation of SPOROCYTELESS/NOZZLE by the MPK3/6 is Required for Arabidopsis Anther Development”.¹ In a previous submission of this manuscript to another journal, such a concept was criticized by one reviewer because it was considered inappropriate to use “germ cells” instead of “archesporial cells” to describe the cells committed to meiosis in plants. Although the reviewers of the manuscript by Zhao et al in Plant Physiology accepted the concept,¹ the criticism from the above-mentioned reviewer demonstrated to me a need to further explain why I proposed such a concept and what advantages such a concept offers over traditional terms.

For readers whose mother language is not English, some etymological analysis of the words might be helpful. While “germ” in common parlance can refer to bacteria, it has a Latin root “genmen” meaning “genitor.” “Germ” can be broadly used for cells at an initial stage that will subsequently develop, such as in “germ layers”.² However, “germ cell” specifically denotes a progenitor cell that culminates in a gamete, or the sexual reproductive cell at any stage from the primordial cell to the mature gamete (http://dictionary.com), or even strictly for a gamete (Oxford dictionary). In comparison, “archesporial” comprises “arche” and “sporial,” in which “arche” has the Greek root “archi” meaning “prior, original, and first.” In terms of etymology, it is perfectly fine to term the cell committed into meiosis in plants as the “archesporial cell”.³ The cells in angiosperm pollen that are committed to become sperm are traditionally termed as “generative cells”.³ No terms like “germline” or “germ cell” were used in classic botanical textbooks. In that sense, the criticism of the reviewer was understandable.

However, in recent years, “germ cell” has been used to replace “generative cells” in research in pollen development.⁴ This is probably because these cells are the progenitors of gametes (sperm cells), which are functionally similar to the germ cells in animals. Similarly, Dickinson's group has used “germline” or “germ cells” to refer to the cells committed to meiosis.^5-8 In this case, the usage arises because the sperm cells differentiate from the meiotically produced cells in angiosperms. The former usage meets with problems in plants when bryophytes and pteridophytes are considered because their gametogenesis is more complicated, as the gametophytes are more elaborated. The latter usage poses a problem in terms of how to distinguish the different meanings of same term for cells with different functions and ploidies.

Functionally, regardless of whether we consider animals or plants, every generation of multicellular organisms starts from a single cell, i.e., a diploid zygote, and ends with haploid gametes. After the gametes fuse through fertilization, a new generation starts. Between the diploid zygote and the haploid gametes, there is a conserved event: meiosis.⁹ From this point of view, before I address the questions mentioned above regarding the concept of diploid germ cells and haploid germ cells, it seems necessary to address why people use “germline” or “germ cells” to describe the cells fulfilling the function of generating gametes through meiosis in animals while they use “archesporial cells” and “generative cells” to describe the cells fulfilling the similar function in plants.

Superficially, the answer seems obvious: in most animal species been investigated, there is a unique lineage of cells differentiated during early embryogenesis that are committed to meiosis and gametogenesis. Such a cell lineage is designated as the “germline”.² In plants, however, no such cell lineage committed to meiosis and gametogenesis is observed.¹⁰ All of the cells directly derived from the zygote division differentiate into diploid somatic cells for multicellular structures called sporophytes. The cells committed to meiosis are induced from the somatic cells within particular organs. After meiosis, the resulting haploid cells differentiate into spores first, then the spores produce haploid somatic cells for multicellular structures, called gametophytes. Some of the haploid somatic cells in particular structures are induced to undergo gametogenesis.¹¹ Since the cells committed to meiosis and gametogenesis are separately induced in diploid and haploid somatic cells, in sporophytes and gametophytes respectively, they are designated as archesporial cells and generative cells respectively. Even though the differences described between animals and plants in the process of development from the zygote to the gametes, is there any component in common? If yes, how did such a component originate and how is it maintained?

Previously, we proposed the concept of the “sexual reproduction cycle (SRC)”.^12,13 Based on analysis of the life cycles of unicellular eukaryotes, we proposed that 3 independently-originated unicellular events, i.e., fusion of particular cells (fertilization), meiosis, and heterogametogenesis, were integrated in unicellular eukaryotes to form a novel process we termed the SRC. In terms of change in cell number, the net outcome of the SRC is that one diploid cell becomes 2 (one diploid zygote becomes 4 haploid meiotically-produced cells, and 4 of those cells fuse into 2 diploid zygotes of the next generation through fertilization), equivalent to a regular mitotic cell cycle. However, an essential difference from the mitotic cell cycle is that through the SRC, a diploid eukaryote cell can autonomously increase genetic variation with higher efficiency. As meiosis and/or heterogametogenesis can be induced upon environmental stresses, the SRC, as a modified cell cycle, functions as the ultimate mechanism that enables diploid eukaryotic cells to effectively adapt to unpredictable environmental changes. Probably because of its unparalleled efficiency, this process was selected for and maintained in all eukaryotes including both unicellular and multicellular organisms. This schema therefore explains why all investigated eukaryotes have meiosis, fertilization, and heterogametogenesis in their life cycles. The key difference between unicellular and multicellular eukaryotes is the cell status interpolating into the interval between the zygote and the meiotic cell, and that between the meiotically-produced cells and the cells committed to gametogenesis.^12,13 In unicellular eukaryotes, the cells interpolated into these 2 intervals exist mainly in a free-living status (as in yeast, although some species lack multiple free-living cells interpolated into one of the 2 intervals, e.g. as in Chlamydomonas). In multicellular eukaryotes, the cells interpolated into the 2 intervals mainly exist in organized multicellular structures.^13,14

Using the concept of the SRC, it is clear that plants and animals are derived from unicellular eukaryotes via different organization strategies for the multicellular structures that interpolated into the 2 intervals of the SRC. In most animals, the multicellular structures derived from the zygote division rapidly diverged into 2 lineages, the soma and the germline.^2,14-16 The germline functions as a carrier of the SRC, and soma functions to interact with the environment, sensing and transmitting environmental changes into the germline to complete the SRC. I have referred to such a morphogenetic strategy a “dichotomous mode”.^14-16 In plants, as described above, 2 multicellular structures, respectively diploid and haploid, were interpolated into the 2 intervals of the SRC. This morphogenetic strategy was designated as “double-ring mode”(Fig. 1).^14-16 From this perspective, regardless of the tremendous differences in morphological and molecular characteristics between animals and plants, there must be regulatory processes for induction of meiosis and of heterogametogenesis. Considering the conservation of meiosis on the cellular and molecular basis, it will be interesting to explore how somatic cells are induced to commit in meiosis, no matter the length of the causal chains. Similar questions exist for the inductive mechanisms of heterogametogenesis.

Figure 1.

Schematic elaboration of a SRC-derived “double-ring mode” of plalnt morphogenetic strategy and its application to the 3 major plant groups. (A) A diagram of the modified cell cycle called “sexual reproduction cycle, SRC.” The 3 rounded rectangules containing yellow ovals represent diploid cells. The red dashed line and arrows represent one diploid cells become 2 (a cell cycle). Dark red dashed curve represnets a process, in which 3 biologic events, i.e., meiosis, fertilization and heterogametogenesis, integrated, and inserted into the cell cycle represented by the rounded recutangules. Through the SRC, a diploid eukaryote can automously generate genetic variations and increase fitness to the unpredictablly changed environment. (B) A diagrame of the SRC-derived double-ring mode of plant morphogenetic strategy. Into the 2 intervals in the SRC, 2 multicellular strcutures are interpolated, i.e., sphorophytes (green dashed circle) and gametophytes (light green dashed circle). In the either ring, the multicellular structures increase the size from a single cell (such as a zygote or a spore) driven by photoautotroph, and reduce the size compelled by internal and external stress, ultimately back to the unicellular SRC through induction of germ cells. (C) A transformation of the double rings by stretch the circle into a linear version, thus to position the diploid ring above the core process of SRC and the haploid ring below. In such a transformation, the major morphological structures, the lateral organs derived from growth tips, of all 3 groups of land plants, i.e., bryophyta, pteridophyta and spermatophyta, can be aligned for comparison (All diagrams were adopted from reference 16).

Now we can go back to the questions why I would suggest to use diploid and haploid germ cells to replace the archesporial cells and generative cells: if we use morphologically-derived terms, there is no reason to compare the induction of meiosis in animals and plants as in animals, it is an event during germline differentiation, which is accessory to individuals; while in plants, it is an event of sporangium differentiation. However, if we instead consider a common evolutionary origin from the SRC, there must be an evolutionarily diverged process for the induction of meiosis from a simple stress response into a set of diversified mechanisms in the different contexts of the multicellular structures in animals and plants. From this point of view, the concept of diploid and haploid germ cells would cover both functionally equivalent cells found in animals and plants, respectively, for meiosis induction and gametogenesis. This view thus provides a basis for investigation of the similarities and differences of induction of meiosis and gametogenesis; as well as the mechanisms integrating multicellular structures with the SRC from an evolutionary perspective, and therefore confers advantages over using traditional morphologically-derived terms.

Disclosure of potential conflicts of interest

No potential conflicts of interest were disclosed.