2026 Volume 76 Issue 4 Pages 331-340
The transition from mitotic proliferation to meiotic division is a defining developmental event in reproduction. In land plants, meiotic entry occurs within complex multicellular tissues and must be precisely coordinated with developmental cues. Recent studies have revealed that meiotic initiation is not a simple cell-cycle switch but is genetically and mechanistically separable from germ-founder cell specification, leading to the emerging concept that meiotic entry is governed by a hierarchical licensing system operating prior to irreversible commitment to meiosis. This review summarizes current knowledge of the developmental, metabolic, redox, and post-transcriptional mechanisms that establish meiotic competence in plants, and discuss how environmental and metabolic inputs, such as temperature and nitrogen availability, are linked to intracellular permissiveness through these mechanisms, ultimately converging on a meiotic commitment point that marks the transition to meiotic mode. Finally, it is proposed that meiotic entry in multicellular land plants represents a developmentally programmed engagement of intrinsic stress-response pathways evolutionarily originated in unicellular organisms. A deeper understanding of these mechanisms will provide a foundation for future studies improving reproductive stability and crop fertility under global climate change.
Meiosis precedes fertilization and generates new genetic combinations by reshuffling parental chromosomes through homologous pairing and crossover formation, thereby introducing genetic diversity into the next generation. Through these processes, meiosis ensures accurate recognition and segregation of homologous chromosomes, contributing to ploidy maintenance, genome stability and reproductive isolation between divergent genomes (Bomblies et al. 2015). It also underpins plant breeding by facilitating the creation and selection of novel allelic combinations through meiosis.
In unicellular eukaryotes, entry into the sexual program and meiosis is often directly triggered by unfavorable environmental conditions, particularly nutrient limitation, highlighting an intimate link between stress responses and meiotic initiation (Kassir et al. 1988, Sugimoto et al. 1991). Likewise, in the green alga Chlamydomonas reinhardtii, nitrogen deprivation triggers gametogenesis and subsequent sexual development (Goodenough et al. 2007). These systems support a general view that, in unicellular life cycles, environmental stress acts as a direct trigger that switch cells from mitotic growth to the meiotic program.
In flowering plants, germ cells including meiocytes are embedded within multi-layered somatic tissues, which reduces the impact of external environmental fluctuations and allows normal reproductive processes to proceed under intrinsic developmental regulations. However, these processes are still sensitive to environmental stresses, particularly temperature extremes, severely compromising pollen development and fertility in many flowering plants (De Storme and Geelen 2014, Rieu et al. 2017). In Arabidopsis and crop species, heat and cold stress disrupts meiotic processes, including homologous chromosome pairing, synapsis and crossover formation (Draeger and Moore 2017, Hayase et al. 1969, Higgins et al. 2012, Modliszewski et al. 2018, Phillips et al. 2015). Given that environmental stresses often serve as cues to trigger meiosis initiation in unicellular organisms, these observations raise the possibility that flowering plants have evolutionarily internalized some of stress-responsive meiotic programs inherited from unicellular ancestors.
Considering this possibility, this review focuses on developmental and physiological processes establishing meiotic competence prior to meiosis, as the molecular mechanisms governing meiosis progression have been extensively reviewed elsewhere. This review categorizes the process leading to meiosis into three distinct phases (Figs. 1, 2); (1) differentiation of the archesporial cell (AR), the initial cell that establish the reproductive cell lineage and their supporting somatic tissues, (2) specification of the sporogenous cell, which acquires the meiotic competence from the AR, and (3) premeiotic regulation. Within this framework, this review summarizes current understanding of the plant molecular mechanisms underlying each phase, with environmental responsiveness as a unifying theme.
Development of germ-founder cells in the anther and ovule in rice. In the rice anther (top), archesporial cells (ARs, red) give rise to sporogenous cells (SPCs, magenta), and to primary parietal cells (PCs, light green). Primary PCs undergo periclinal divisions and develop the endothecium (yellow), while secondary PCs further develop tapetum (blue) and middle layer (dark green). After the somatic anther wall becomes four-layered including epidermis, SPCs mature into pollen mother cells (PMCs, orange) and undergo male meiosis. In the rice ovule (bottom), ARs are generally thought to directly differentiate to megaspore mother cells (MMCs, orange). However, at the AR initial stage, multiple sub-epidermal cells (red) are marked by MEL1 (Nonomura et al. 2007, Yamaki et al. 2011), which encodes an Argonaute protein required for proper meiosis progression, and these cells gradually converge into a single SPC or MMC. This observation suggests that MMC-neighboring cells initially possess competence toward germ-founder fate, but this potential is restricted by mechanisms that limit the expansion of germ-founder identity, thereby ensuring the specification of a single MMC while surrounding cells differentiate into somatic nucellar cells. In Arabidpsis, nucellar cells adjacent to the MMC become enlarged relative to other nucellar cells (Lora et al. 2017), and their development is genetically regulated by MADS31 (Yang et al. 2025). This figure is reproduced from Mimura et al. (2024) under an open access license.
Hierarchical regulation of mitosis-to-meiosis transition in plants. Schematic overview of the hierarchical regulatory framework governing the transition from mitotic proliferation to meiotic division in plants. Somatic precursor cells (sub-epidermal cells) differentiate into archesporial cells and subsequently into sporogenous cells (SPCs), the germ-founder cells of the male lineage. SPCs are specified as meiocytes via multiple licensing steps—including downregulation of WUS and regulation of hypoxia, hormonal, redox (MSCA1/MIL1), epigenetic (AGO9), metabolic (ETFβ), and post-transcriptional (MEL2) levels—before meiotic commitment, an irreversible cell-cycle switch that establishes spore mother cells as committed meiocytes. All cell types are enclosed with squares, and the germ-founder cells are with bold squares. IAA: auxin, GA: gibberellin, CK: cytokinin.
It should be noted that mechanisms identified in male systems do not necessarily operate in the same manner in female systems, and vice versa. This review therefore attempts to distinguish findings from male and female systems whenever possible, as integrating them into a unified framework remains challenging. In addition, this review adopts the term “germ-founder cells” for cells ranging from ARs to meiocytes (Fig. 2), because in land plants, the germline is conventionally defined as originating in the sexual haploid gametophyte after meiosis, whereas meiocytes are classified as the asexual diploid sporophyte (Borg et al. 2009, Graham and Wilcox 2000, Walbot and Evans 2003).
The initiation of ARs, primordial germ-founder cells in land plants, represents a critical developmental transition at which a subset of sub-epidermal somatic cells within floral meristems acquires germ-founder competence (Goldberg et al. 1993, Scott et al. 2004). Accumulating evidence indicates that this transition is shaped not only by genetic regulators but also by physiological conditions, particularly oxygen availability, as well as by plant hormone signaling. Developing anthers and ovules form intrinsically hypoxic microenvironments (van Dongen and Licausi 2015), which potentially promote AR specification. Consistent with this view, the Walbot group demonstrated that hypoxic conditions promote the specification of ARs in maize anthers (Kelliher and Walbot 2012, Kelliher et al. 2014), although this has so far been demonstrated only in maize.
In maize, MALE STERILE CONVERTED ANTHER1 (MSCA1), a CC-type glutaredoxin (GRX), plays an essential role in AR-fate determination, as loss of MSCA1 results in vasculature-like somatic cells instead of ARs (Kelliher and Walbot 2012). Similarly, loss of MICROSPORELESS1 (MIL1), a rice CC-type GRX, leads to anther locules filled with somatic cells (Hong et al. 2012). In Arabidopsis, the CC-type GRXs, ROXY1 and ROXY2, act redundantly in anther development (Xing and Zachgo 2008). These findings suggest that redox status, in addition to hypoxic conditions, is a critical determinant of AR-fate specification in anthers, although the underlying mechanism remains unclear.
In parallel, auxin maxima established in anther lobes plays a central role in AR specification (Zheng et al. 2021). Importantly, the mutations in both TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS1 (TAA1) and TRYPTOPHAN AMINOTRANSFERASE RELATED2 (TAR2), which act upstream of YUCCA-mediated auxin biosynthesis, compromise auxin maxima formation and cause severe defects in AR initiation, demonstrating that locally produced auxin is essential for AR initiation and specification in Arabidopsis (Cao et al. 2019, Zheng et al. 2021).
Gibberellin (GA) and cytokinin (CK) signaling, by contrast, primarily regulate cell proliferation and differentiation in surrounding somatic tissues. In Arabidopsis ovules, elevated GA levels in somatic cells result in multiple germ-founder cells and megaspore mother cells (MMCs), a subset of which fails to enter meiosis, suggesting that excessive GA disrupts proper germ-founder cell specification (Cai et al. 2025). GA suppresses CK signaling in surrounding tissues, thereby restricting somatic proliferation and confining germ-founder cell fate to a single MMC (Cai et al. 2025).
In rice, the CK-activating enzyme LONELY GUY (LOG) is transiently expressed during ovule-founder tissue development, and the log-3 mutant exhibits an ovule-less phenotype (Kurakawa et al. 2007, Yamaki et al. 2011). The expression of MEIOSIS ARRESTED AT LEPTOTENE1 (MEL1), encoding a germ cell-specific Argonaute required to ensure faithful meiosis progression (Nonomura et al. 2007), initiates in ARs located beneath transiently LOG-expressing epidermal cells (Yamaki et al. 2011). Given that CK restricts germ cell number (Bencivenga et al. 2012, Cai et al. 2025), transient LOG expression likely organizes a somatic niche rather than directly promoting AR specification. Together, these findings suggest that AR initiation requires transient CK provision and that meiotic fate decisions are established at the onset of germ-founder cell differentiation.
Importantly, hypoxia and hormone signaling are mechanistically interconnected. Hypoxic conditions induce metabolic reprogramming and alter redox status, potentially activating redox-sensitive regulatory modules including CC-type GRXs, which are required for acquisition of germ-founder cell fate (Hong et al. 2012, Kelliher and Walbot 2012). Hypoxia also modulates auxin distribution and downstream transcriptional outputs by altering auxin transport dynamics via ethylene signaling in non-reproductive tissues such as roots (Eysholdt-Derzsó and Sauter 2017, Hartman et al. 2019). In turn, auxin and CK signaling reciprocally regulates cell proliferation and growth through tightly coordinated feedback mechanisms (Moubayidin et al. 2009, Schaller et al. 2015). These interactions suggest that hormonal patterning reinforces hypoxic microenvironments in densely packed reproductive tissues, defining a unique physiological niche for AR initiation (Kelliher and Walbot 2012).
As a key genetic regulator of germ-founder cell and MMC specification, the homeobox gene WUSCHEL (WUS), originally identified as a central regulator of stem cell maintenance, establishes a developmental niche in ovules (Groß-Hardt et al. 2002, Sieber et al. 2004), providing a permissive developmental context for MMC differentiation. Importantly, WUS expression is subsequently repressed upon floral meristem termination through a transcriptional cascade initiated by the C-class MADS-box transcription factor AGAMOUS (AG), which induces the C2H2-type zinc finger protein KNUCLES (KNU) to suppress WUS-dependent meristematic activity (Ito et al. 2004, Payne et al. 2004, Sun et al. 2014). After this process, WUS expression is re-initiated in the epidermis of the ovule primordium (Vijayan et al. 2021). The ovule-specific WUS activity is closely linked to CK signaling and epigenetic pathways operating in surrounding somatic tissues, including RNA-directed DNA methylation, which restrict germ-founder fate and ensure a single MMC (Bencivenga et al. 2012, Mendes et al. 2020, Schmidt et al. 2011).
Together, these findings indicate that hypoxia-defined physiological niches, hormone-mediated positional cues, and WUS-dependent developmental competence represent potential regulatory inputs for germ-founder cell initiation (Fig. 3), although whether and how these mechanisms are integrated in male and female reproductive organs remains unclear.
A model for stepwise restriction of sporogenous cell competence during ovule development. During floral meristem termination, AGOMOUS (AG) epigenetically activates KNUCKLES (KNU), which in turn represses WUSCHEL (WUS) transcription. In parallel, gibberellin and cytokinin levels are locally modulated in epidermal cells, establishing a permissive niche for archesporial cell (AR) initiation in sub-epidermal region. Subsequently, auxin maxima and redox regulation further promote AR specification. During sporogenous cell (SPC) specification, AG directly activates SPOLOCYTELESS/NOZZLE (SPL) transcription, facilitating SPC formation. In parallel, cell-autonomous RETINOBRASTOMA-RELATED1 (RBR1)-mediated repression of WUS and non-cell-autonomous AGO9-dependent pathways cooperatively restricts the number of SPCs and ensure the specification of a single megaspore mother cells.
In each of the four anther lobes, ARs differentiate into sporogenous cells (SPCs) and parietal cells (Scott et al. 2004) (Fig. 1). SPCs mitotically proliferate several times before developing into meiocytes. Parietal cells undergo periclinal divisions to give rise to sub-epidermal somatic anther-wall layers that surround and support SPCs and subsequent meiocytes. In the ovule, a single SPC derived from the AR develops into a female meiocyte (Fig. 1). A central challenge during premeiotic development is to ensure that meiotic competence is acquired exclusively by SPCs. This requires not only the activation of SPC-specific transcriptional programs but also the active repression of somatic and meristematic identities, thereby preventing inappropriate expansion of germ-founder cell fate.
In Arabidopsis, the SPOROCYTELESS/NOZZLE (SPL/NZZ) pathway constitutes a core genetic module for SPC specification in both male and female reproductive organs. SPL/NZZ encodes a plant-specific transcriptional regulator that acts as a master determinant of SPC identity (Schiefthaler et al. 1999, Yang et al. 1999). SPL/NZZ transcription is directly activated by AG (Ito et al. 2004), and in spl/nzz mutants, primary parietal cells are formed whereas SPC identity fails to be established in anthers (Yang et al. 1999), indicating a specific requirement of the AG-SPL/NZZ pathway for SPC specification. The rice SPL is also required for SPC differentiation and meiotic fate acquisition (Ren et al. 2018). Through this regulatory cascade, developmental trajectories are redirected away from meristematic-states toward reproductive differentiation, thereby stabilizing germ-founder cell identity.
During this stage, WUS continues to be expressed in the ovule epidermis, but the RETINOBLASTOMA-RELATED PROTEIN1 (RBR1) directly suppresses WUS transcription within germ-founder cells (Zhao et al. 2017). Loss of RBR1 leads to ectopic WUS expression and excess cell division, resulting in the formation of multiple MMCs. These observations demonstrate that precise spatial control of WUS activity, rather than its complete silencing, is essential for restricting germ-founder cell fate. Notably, enforced WUS expression in MMCs fails to phenocopy the rbr1 mutant, further indicating that RBR1 acts upstream of, or in parallel with, additional factors beyond WUS to restrict SPC specification. However, given that no WUS upregulation was detected in rbr1 anthers (Arp Schnittger, personal communication) and WUS expression is limited to specific somatic domains such as the stomium (Deyhle et al. 2007), it is likely that additional factors contribute to RBR-mediated SPC specification in the male organ.
In the female organ, an additional regulatory pathway involves ARGONAUTE9 (AGO9) in Arabidopsis, which was reported to limit SPC number via small RNA pathway operating non-cell-autonomously from surrounding somatic tissues (Olmedo-Monfil et al. 2010), although the extent of this effect remains debated. AGO9 predominantly associates with 24-nucleotide (nt) small interfering RNAs (siRNAs) derived from transposable elements, linking epigenetic silencing to germ-founder cell restriction. This pathway may provide an extrinsic layer of control, reinforcing germ-founder fate restriction from the somatic niche.
Together, these findings support a model in which germ-founder cell specification is established through multilayered repression, integrating; (1) transcriptional repression of WUS by KNU in the floral meristem, (2) re-initiation of WUS in the ovule epidermis, coupled with RBR1-dependent repression of WUS within SPCs, (3) AGO9-dependent small RNA pathways acting from surrounding somatic tissues, at least in Arabidopsis ovule.
In parallel with SPC specification, the differentiation of parietal cells into somatic nursery layers is also actively regulated in anthers. SPCs are thought to secrete the peptidic ligands, including TAPETUM DETERMINANT1 (TPD1) in Arabidopsis (Yang et al. 2003), TPD1-LIKE1A (TDL1A)/MICROSPOROCYTELESS2 (MIL2) in rice (Yang et al. 2016, Zhao et al. 2008), and MULTIPLE ARCHESPORIAL CELLS1 (MAC1) in maize (Sheridan et al. 1999). These ligands are perceived by leucine-rich repeat receptor-like kinases, such as EXCESS MICROSPOROCYTES1 (EMS1)/EXTRA SPOROGENOUS CELLS (EXS) (Canales et al. 2002, Zhao et al. 2002) and MULTIPLE SPOROCYTES1 (MSP1) (Nonomura et al. 2003), thereby promoting specification and differentiation of somatic nursery cell layers, in addition to the inhibition of supernumerary pollen mother cells (PMCs) that undergoes male meiosis (Fig. 2).
Through both cell-autonomous and cell-non-autonomous networks integrally ensure precise control of germ-founder cell number and specification, reinforcing the partitioning of meiotic and somatic fates in developing reproductive organs (Fig. 3).
Genetic analyses in plants have identified numerous mutants in which SPC-like cells are formed but fail to initiate or complete meiosis. Such mutants imply the existence of a meiotic commitment step, an irreversible switch from mitotic to meiotic cell-cycle programs (Rimal and Winter 2022, Tsuchiya et al. 2014), although it has recently been proposed in the Arabidopsis female that, even after the meiotic commitment, meiocytes can allow one or more mitotic divisions without overwriting the programming to become a meiocyte (Hu et al. 2026).
Here, we adopt a phenotype-based definition of meiotic commitment. Under this framework, mutants in which all SPCs uniformly acquire meiotic fates but arrest during meiotic progression are classified as acting downstream of commitment, whereas mutants in which SPCs completely or partially fail to enter meiosis are positioned upstream. Accordingly, in this review, the relevant mutants are categorized based on SPC behavior: (1) retention of a somatic state, (2) partially or heterogeneous meiocyte identity, or (3) uniform meiotic entry.
In maize, AMEIOTIC1 (AM1) defines an early regulatory step in the mitotic to meiotic transition. Strong am1 alleles cause all SPCs to continue mitotic proliferation, resulting in complete failure of meiocyte formation (Golubovskaya et al. 1993), indicating that AM1 functions upstream of meiotic commitment, while weaker am1 alleles permit partial meiotic entry but disrupt early meiotic progression (Pawlowski et al. 2009), suggesting additional post-commitment roles. Consistently, rice AM1 is dispensable for SPC specification but essential for the leptotene-zygotene transition (Che et al. 2011). SWITCH1/DYAD (SWI1/DYD), the Arabidopsis ortholog of AM1, plays a crucial role in establishing sister chromatid cohesion during early meiosis (Mercier et al. 2001). Together, these studies indicate that AM1-family proteins play critical roles in the regulation of early meiotic development, although their precise timing and functional contribution vary among plant species.
In rice, loss of ELECTRON TRANSFER FLAVOPROTEIN SUBUNIT β (ETFβ) prevents meiotic initiation under nitrogen starvation (Yang et al. 2022). ETFβ functions in branched-chain amino acid catabolism and nitrogen reutilization, and the meiotic defects in etfβ mutants are rescued by inorganic nitrogen supplementation, indicating that meiotic entry remains reversible and metabolically gated. Thus, ETFβ represents an upstream environmental licensing step rather than a commitment mechanism, ensuring that SPCs initiate meiosis only when sufficient metabolic resources are available.
Generally, proper progression of meiosis requires a tightly regulated meiotic arrest/resumption system (Clift and Schuh 2013, Sagata 1996). In rice, MEIOSIS ARRESTED AT LEPTOTENE2 (MEL2) plays a central role in this framework. In wildtype anthers, male meiosis proceeds synchronously within each lobe despite asynchronous SPC proliferation, whereas mel2 mutants exhibit heterogeneous outcome, with some cells entering meiosis while others continue mitosis in each anther lobe (Nonomura et al. 2011). This phenotype indicates defective coordination of meiotic entry across SPCs, rather than a simple block before or after the commitment. MEL2 therefore defines a licensing step closely associated with commitment, coordinating premeiotic arrest/resumption. In ovules, which contain a single SPC, MEL2 is likely to regulate the timing of meiotic entry rather than synchrony. MEL2 is an RNA-binding protein that potentially forms cytoplasmic RNA granules (Mimura et al. 2024) (Fig. 4), implicating post-transcriptional regulation in this licensing process toward meiosis.
Temperature-responsive properties of MEL2 and stress granules. Rice protoplasts co-expressing MEL2-GFP (green) and UBP1b (magenta), a core component of stress granules. Upon temperature shift from 26˚C (top) to 45˚C (bottom), cytoplasmic granules containing MEL2 and UBP1b become enlarged (arrow heads). Scale bars, 5 μm. N, nucleus; V, vacuole. Images are reproduced from Mimura et al. (2024) under an open access license.
One downstream effector of MEL2 is GLUCAN SYNTHASE-LIKE5 (OsGSL5), which mediates transient robust β-1,3-glucan deposition between PMCs and surrounding tapetal cells during premeiosis (Somashekar et al. 2023). In Osgsl5 mutants, PMCs uniformly enter meiosis but display precocious DNA replication and aberrant chromosome behavior, indicating a role after commitment. OsGSL5-dependent callose prevents premature plasmodesmata (PDs) closure, and ensures timely symplastic isolation of PMCs, a prerequisite for faithful meiosis (Somashekar et al. 2024). Conservation of MEL2-like proteins across land plants and streptophyte algae (Mimura et al. 2024), together with widespread premeiotic callose accumulation in angiosperm anthers (De Storme and Geelen 2014, Scott et al. 2004), supports a conserved module acting at the meiotic commitment-execution interface.
Following meiotic commitment, additional mechanisms ensure faithful execution of meiotic machineries. In rice, the germ cell-specific Argonaute MEL1 exemplifies this downstream layer. Although MEL1 transcription initiates in ARs, mel1 mutants form meiocytes but fail to progress through prophase I (Nonomura et al. 2007), placing the MEL1 function downstream of commitment. MEL1 binds reproductive 21-nt phased secondary siRNAs (phasiRNAs) (Komiya et al. 2014, Ono et al. 2018), and promotes meiotic competence by cell-autonomous elimination of SPC-expressed mRNAs (Jiang et al. 2020, Zhang et al. 2020). Notably, these phasiRNAs are produced predominantly in the anther epidermis of grasses (Pokhrel et al. 2021, Zhai et al. 2015). Thus, unlike AGO9, which restricts germ-founder cell fate non-cell-autonomously, MEL1 acts SPC-autonomously to execute the meiotic program using non-cell-autonomously supplied phasiRNAs.
Together, these genetic analyses delineate multiple regulatory layers that license SPCs for meiotic entry across premeiotic stages before, at and after meiotic commitment in plants (Fig. 2).
As discussed in the preceding section, a key conceptual distinction has emerged in plant meiosis between SPC specification and meiotic commitment. Building on this distinction, accumulating evidence supports a hierarchical model in which meiotic entry is governed by multi-layered metabolic and environmental licensing mechanisms (Figs. 2, 3). In rice, identification of ETFβ as a nitrogen-dependent regulator of meiotic initiation provides a direct genetic link between nutrient availability and meiotic entry. An additional licensing layer is provided by MEL2-dependent post-transcriptional regulation, in which cytoplasmic RNA granule-associated pathways remodel transcript populations required for the mitotic-to-meiotic transition. Together, AM1-, ETFβ- and MEL2-mediated pathways converge upstream of a bona fide meiotic commitment point (Fig. 2).
Consistent with this model, re-analysis of transcriptomic data from wildtype and mel2 mutant anthers (Mimura et al. 2024) revealed that transcriptional level of the early licensing factors AM1 and ETFβ remained largely unchanged in premeiotic mel2 anthers, whereas those of meiosis-executing factors, including RAD21-4 (REC8), DMC1A, ZYGO1, were significantly reduced (Fig. 5). These results indicate that MEL2-mediated regulation acts in parallel with, or downstream of AM1- and ETFβ-mediated licensing prior to commitment. Together, this framework redefines meiotic entry as a developmental decision shaped by layered extrinsic and intrinsic inputs, providing a basis for interpreting diversity in meiotic control across plant lineages, including AM1 and SWI1/DYD. Variation in how these licensing modules operate relative to SPC specification likely reflects differences in how environmental and metabolic signals are integrated into meiotic regulatory networks.
Differentially expressed genes between wildtype and mel2 anthers at the premeiotic stage in rice. A volcano plot highlighting sixteen differentially expressed genes (black circles), based on a re-analysis of transcriptomic data reported by Mimura et al. (2024). Genes that functions predominantly after meiotic commitment, including RAD21-4 (REC8), DMC1A and ZYGO1, are significantly downregulated in mel2 premeiotic anthers. In contrast, genes implicated in meiotic licensing and commitment proximal processes, such as MIL1, ETF1b, RBR1 and AM1 show little or no change in expression. These results support a model in which MEL2 acts near the meiotic commitment point, primarily affecting downstream meiotic executing machineries rather than upstream licensing steps.
Several fundamental questions remain: how do diverse licensing signals converge on meiotic commitment, to what extent are metabolic, redox, and RNA-based mechanisms are conserved, and how do these pathways interact with chromatin-based epigenetic regulation? Addressing these issues will be essential for understanding plant reproductive biology and for manipulating meiotic control in crop breeding and environmental resilience.
This review proposes that land plants have evolutionarily internalized ancestral stress-responsive programs by generating endogenous stress signals. Specifically, land plants rewired the starvation-activated meiotic induction pathway of unicellular eukaryotes by embedding nutrient sensing systems, as exemplified by rice ETFβ (Yang et al. 2022), into a developmental licensing framework. Furthermore, regulated reactive oxygen species (ROS) production appears to have been internalized within reproductive tissues and/or germ founder cells (Guo et al. 2022, Shi et al. 2022, Zhao et al. 2018). This idea is supported by the fact that callose deposition as observed in premeiotic anthers is frequently accompanied by localized ROS accumulation (Daudi et al. 2012, Ellinger and Voigt 2014). In this framework, this premeiotic micro-environment is characterized by a “programmed stress state”, where MEL2/OsGSL5-mediated callose deposition, ROS-generating systems, and redox-mediated regulatory modules involving CC-type GRXs such as MSCA1 and MIL1, may cooperate to promote meiosis transition.
This system allows land plants to execute meiosis more stably than unicellular ancestors, whose meiotic initiation depends on fluctuating and unpredictable environmental cues. However, this same responsiveness makes the system inherently fragile: extreme external stresses can override the internal signals, leading to a temporal dysregulation of meiotic entry.
Consistently, MEL2 granules frequently colocalize with stress granules (SGs), which mediate mRNA triage under adverse environmental conditions such as heat, oxidative stress, hypoxia and nutrient deprivation (Anderson and Kedersha 2008, Protter and Parker 2016), and heat stress induces enlargement of MEL2 granules together with SGs in rice protoplasts co-overexpressing MEL2 and a core SG component OLIGOURIDYLATE BINDING PROTEIN1b (UBP1b) (Mimura et al. 2024) (Fig. 5). Consistent with this view, SGs have also been implicated in meiotic regulation in Arabidopsis, where localization of the meiotic cyclin TARDY ASYNCHRONOUS MEIOSIS (TAM) to SGs is required to maintain proper meiotic progression, particularly under heat stress (De Jaeger-Braet et al. 2022, 2025).
In conclusion, meiotic entry in plants is not merely a cell-cycle transition but a tightly regulated stress-adaptive state, in which environmental responsiveness has been evolutionarily co-opted to ensure robust execution of sexual reproduction. Understanding how ROS-generating enzymes, RNA-based regulatory modules and callose-mediated cell wall dynamics are integrated will be essential for elucidating the molecular basis of meiotic resilience and fragility under changing environments.
The author solely contributed to all aspects of this review.
In presenting a simplified conceptual framework for meiotic entry, I necessarily omit many relevant genes and studies, and acknowledge all researchers whose work has contributed to the field of plant reproduction, as well as all past and current members of the Nonomura laboratory. I am grateful to Profs. Arp Schnittger (Univ. Hamburg, Germany) and Toshiro Ito (Nara Inst. Sci. Tech., Japan) for reading the manuscript and providing critical comments. This work was supported by JSPS KAKENHI Grants 21H04729, 24K21874 and 26K02054.
