Does Shoot Apical Meristem Function as the Germline in Safeguarding Against Excess of Mutations?

Abstract

A genetic continuity of living organisms relies on the germline which is a specialized cell lineage producing gametes. Essential in the germline functioning is the protection of genetic information that is subjected to spontaneous mutations. Due to indeterminate growth, late specification of the germline, and unique longevity, plants are expected to accumulate somatic mutations during their lifetime that leads to decrease in individual and population fitness. However, protective mechanisms, similar to those in animals, exist in plant shoot apical meristem (SAM) allowing plants to reduce the accumulation and transmission of mutations. This review describes cellular- and tissue-level mechanisms related to spatio-temporal distribution of cell divisions, organization of stem cell lineages, and cell fate specification to argue that the SAM functions analogous to animal germline.

Keywords: cell division; germline; shoot apical meristem; somatic mutation; stem cell.

FIGURE 1

Cell lineages minimizing the risk of heritable mutations. Establishment of the germline and somatic lineages in animals (A,B) and plants (C). (A) In most of vertebrates (e.g., mouse and chicken) and ecdysozoans (e.g., Drosophila and Caenorhabditis elegans) the germline (blue) producing gametes (cyan) is specified and separated from somatic lineages (black) during embryogenesis. (B) In other animals (e.g., flatworms, cnidarians, or sponges), the germline is specified during post-embryonic development from multipotent lineages (gray) that produce also somatic lineages. (C) In plants, the germline is specified during post-embryonic development from meristematic cell lineages (gray), that produces also somatic lineages. Empty circle, zygote; black circle, somatic lineage; blue circle, germline; cyan circle, gametes; gray circle, multipotent or meristematic lineage. (D) Hierarchical organization of stem cell lineage. Slowly dividing stem cells (red) produce descendant stem cells and faster dividing transit-amplifying cells (yellow) that eventually enter a differentiation pathway (green). (E–G) The fate of stem cell descendants. (E) Stem cell descendants after the asymmetric division acquire a different fate: the stem cell (red) and the cell that ultimately differentiate (yellow). Stem cell descendants after the symmetric division acquire the same fate: either both become stem cells (F), or both cells ultimately differentiate (G).

FIGURE 2

Stochastic and semi-permanent behavior of plant stem cells. (A) Dynamics of stem cells at the surface of vegetative SAM in Arabidopsis (top view, based on the figure 4, Burian et al., 2016). Stem cells were identified at L1 (the outermost cell layer of tunica) by tracing of cell lineages based on time-lapse imaging with laser confocal microscopy. A stem cell (red) divides asymmetrically producing the descendant cell that maintains its position at SAM center and stem cell fate, and the cell that loses stem cell fate by its displacement to the periphery, and becomes transit-amplifying cell (yellow) undergoing series of cell divisions. Note, that the same set of four stem cells is functioning for at least 9 days. Scale bar, 20 μm. (B) Computer simulation of stochastic stem cell behavior (modified, based on the Video S4, Kucypera et al., 2017). In Kucypera et al. (2017), stem cells were defined by a stable point corresponding to the geometric center of SAM surface. Here, stem cells (red) were defined at t1 by a stable positional information marked by a blue circle. The simulation shows that although these stem cells generally divide asymmetrically, symmetrical divisions can also occur leading to rearrangement of stem cells. Due to cell displacement, both descendants of the stem cell (indicated by an asterisk at t1) lose stem cell fate at t2, and undergo series of cell divisions (yellow). Consequently, the cell clone is displaced from the SAM center at t3. In contrast, both descendants of the other stem cell (indicated by a hash at t1) keep stem cell fate at t2 as they maintain the position at the center. (C) Plausible stem cells below SAM surface. At longitudinal section across the SAM (from A), thicker lines indicate outer cell layers of the tunica (L1 and L2) and inner corpus (L3). Arrows indicate the direction of cell displacement due to oriented cell divisions. Each tunica layer and the corpus contain their own sets of stem cells. Red circle, stem cell of the L1 (identified at A), empty circle, plausible stem cells of L2 and L3. Stem cells of L1 give rise to epidermis, L2 – subepidermal tissues, and gametes, L3 – internal tissues. Scale bar, 20 μm.