Plant stem cells are typically found in meristems, and their defining characteristics include being cells specialized in producing new cells and organs, self-maintenance, slow proliferation with an extended G1 (or G0) cell state, pluripotency (ability to differentiate into multiple cell types), and regenerative potential or the ability to repopulate after damage [6,7,8]. The study of apical meristems (AMs) is particularly intriguing due to their stem cell pool, also known as promeristems, located at the central part of the shoot and the root apex. A continuous differentiating cell flux occurs throughout plant development from stem cells to proliferating cells, finishing with differentiating cell states [9]. Two types of plant cell differentiation exist: terminal and non-terminal. Terminal differentiation implies that a cell can no longer change its fate, while non-terminal differentiation allows a cell to change its fate when exposed to the correct signals, such as normal ontogeny, wounding, or other physiological changes [10]. Cells undergoing non-terminal differentiation appear to retain a stem cell potential [3]. However, the specific conditions activating their differentiation into various cell types remain largely unknown [11]. Standard models for studying plant cell differentiation include embryos, protoplasts, callus, and meristems [11,12,13,14]. These models are valuable as they contain pluripotent or totipotent cells that ultimately give rise to different plant tissues and even regenerate whole plants. Hence, an interesting perspective to understand this phenomenon is to focus on the evolution of pluripotency by comparing the meristems of early and modern diverged land plants, pointing out the common factors of pluripotency through evolution.

Extensive research has been conducted to understand RAM evolution, but little is known about the SAM evolutionary process. Since both AMs are structures with similar characteristics, studying the RAM can be a starting point for understanding the SAM. Some common attributes are that both are reservoirs of stem cells, both are promeristems that give rise to five primary meristems (protoderm, ground meristem, procambium, pericycle, and calyptrogen in the root [10]), and they are first determined during embryogenesis [15]. Stem cells in the root apical meristem (RAM) are present and maintained in the quiescent center (QC). In contrast, in the shoot apical meristem (SAM), stem cells are contained in the central zone (CZ) and maintained by the organizing center (OC) [16]. The QC and OC are the signaling centers responsible for stem cell maintenance in both meristems [16] and have been proposed to be functionally equivalent [17,18].

Studies conducted on the model plant Arabidopsis thaliana suggest that the organization of the signaling components required for stem cell initiation and maintenance in the RAM and SAM are relatively conserved. Consequently, similar classes of genes have been co-opted as central regulators in both types of meristems [18,19]. However, despite these shared mechanisms, the hormonal function is inverse [20,21]. In the SAM, auxins trigger differentiation, whereas in the RAM, they maintain the stem cell niche and support cell proliferation [22]. On the other hand, in the SAM, cytokinin promotes tissue proliferation of differentiating cells, whereas it promotes cell differentiation in the RAM [23,24]. The OC of the SAM is the site of maximal cytokinin activity, whereas the auxin maximum is in the QC of the RAM [24] (Figure 1).

Fossil evidence suggests that the RAM evolved at least twice independently rather than having a single origin [25,26]. The first appearance occurred in the lycophytes clade, followed by a second evolutionary event, likely in the ancestor of euphyllophytes (vascular plant non-lycophytes) [27]. It has even been proposed that RAM independently evolved multiple times in lycophytes [28]. Moreover, the similarities between lycophyte and euphyllophyte roots, including indeterminate growth, apical meristem protected by a root cap, root hairs, and a stele covered by a specialized endodermal cell layer, are clear examples of convergent evolution [29,30]. Genomic analyses revealed that limited gene expansion occurred at the divergence between the lycophyte and euphyllophyte clades [31]. Consequently, all the similarities produced by convergent evolution did not require extra gene families, suggesting that the rewiring of existing genetic programs was sufficient to generate multiple independent emergences of the RAM [32].

The plant life cycle comprises two alternating phases: the haploid or gametophyte phase and the diploid or sporophyte phase. The diploid phase concludes with meiosis, while the haploid phase ends with the generation and union of gametes [35]. It is remarkable that, as land plants diversified, life cycle generation dominance twisted, and the sporophyte generation became dominant and increasingly specialized, whereas the gametophyte generation became reduced [36,37]. This trend is reflected in SAMs. Non-seed plants have simple meristems, sometimes with a single apical cell, to sustain their growth. In contrast, seed plants’ sporophytes develop complex multicellular meristems to support their growth and specialization, while their gametophytes lack meristems [38,39] (Figure 2). As both phases have meristems, it is reasonable to discuss the origin of meristems in terms of the plant life cycle. 

Two hypotheses have been proposed that explain the appearance of the alternation cycle [41]. First, the homologous hypothesis describes the ancestor of land plants with an originally haplontic life cycle that gives rise to a sporophyte through delay in meiosis, resulting in the intercalation of a new diploid organism [37,42]. This assumption outlines the gametophytic SAM as the ancestor of the sporophytic SAM. The second hypothesis is the antithetic hypothesis, which proposes that sporophytic SAM is independent of gametophytic SAM. According to this hypothesis, the sporophytic SAM evolved de novo by intercalating a system between embryonic and reproductive growth [37,43]. Current evidence based on embryophytes and fossil records is more compatible with the antithetic hypothesis than the homologous hypothesis [44,45]. Hypotheses derived from the antithetic hypothesis include (1) the embryophyte SAM originated from the transient seta meristem (sporophyte) of a bryophyte, (2) the hornwort sporophyte meristem is the possible ancestor of the SAM, and (3) the SAM in vascular plants arose de novo from a bryophyte ancestor [46].

Overall, evidence suggests that gametophyte and sporophyte SAM have an independent origin. However, because plants have retained a common set of genetic components since they diverged from algae, they are likely to share homologous regulatory loops and mechanisms in regulating their SAM. In fact, moss and fern gametophyte SAMs share key transcription factors (TFs) with angiosperm sporophyte SAMs [47,48], which suggests the existence of fundamental mechanisms involved in stem cell regulation across land plants.

3. Shoot Apical Meristem Regulation and Maintenance

3.1. The Regulatory Model: Angiosperms

3.2. SAM TFs Conserved throughout Evolution

3.2.1. KNOX TFs

3.2.2. MADS TFs

3.2.3. AP2/ERF TFs