Plant reproduction requires precisely timed cellular degradation to support developmental remodeling, organelle quality control, nutrient recycling, programmed cell death (PCD), and fertilization. Autophagy and protease-mediated proteolysis are major degradative systems but are often discussed either separately or as functionally linked without sufficient evidence of direct molecular coupling. Autophagy primarily mediates cargo sequestration, vacuolar delivery, metabolic remodeling, and organelle quality control. Proteases, in contrast, execute substrate cleavage, pro-enzyme maturation, nutrient mobilization, and developmentally programmed cell death (dPCD). Evidence increasingly indicates that these pathways contribute to overlapping degradative processes across reproductive development, although the molecular basis of their coordination remains poorly resolved. A key unresolved question is whether and how autophagic cargo delivery is mechanistically connected to vacuolar processing, protease activation, and terminal substrate degradation during reproduction. In this review, rather than revisiting the established functions of autophagy in reproduction, we focus on whether autophagy and protease-mediated proteolysis act independently, converge functionally, or show evidence of direct mechanistic dependence. We specifically evaluate evidence linking autophagic cargo delivery, vacuolar competence, protease activation, and terminal substrate degradation. Finally, we highlight critical knowledge gaps and research priorities needed to determine how these relationships shape fertility and reproductive resilience in angiosperms. This review challenges the common assumption that autophagy and proteases form a unified degradative pathway during plant reproduction, showing instead where they act independently, where they converge, and where true molecular coupling remains to be demonstrated, while defining key degradative checkpoints that shape fertility and reproductive resilience.
In Prunus, self-incompatibility (SI) is controlled by S-RNases and pollen-expressed F-box proteins, whereas the molecular processes governing S-RNase regulation in pollen remain incompletely understood. Here, we characterized PavSDJ, a novel pollen protein from sweet cherry (Prunus avium), as a candidate factor involved in pollen-side S-RNase-associated processes. Sequence and structural analyses identified PavSDJ as a type III J-protein. Phylogenetic analyses placed PavSDJ within a distinct SDJ-like sublineage of the type III J-protein group, separate from a closely related sister lineage. Consistent with this divergence, PavSDJ was strongly expressed in anthers and pollen, whereas its sister gene was broadly expressed across organs. Transient expression assays showed that PavSDJ-GFP exhibited a predominantly cell-peripheral fluorescence pattern consistent with intracellular localization. Biochemical analyses showed that PavSDJ associated with recombinant PavS-RNases in pollen extracts and in reconstituted pull-down assays, without obvious allele preference. Proteomic analysis of PavSDJ co-immunoprecipitants from pollen extracts identified a complex including PavSLFL6 and PavSSK1. Reconstitution assays further showed that PavSDJ promoted the co-precipitation of PavSLFL6 with S-RNase. These findings identify PavSDJ as a candidate pollen-side factor in the Prunus SI pathway and provide evidence that a specialized J-protein may contribute to SI-related protein complex assembly.
The formation of unisexual florets in Poaceae occurs through diverse developmental pathways. However, the morphogenetic mechanisms controlling sex determination in dioecious grasses remain poorly understood. Here, we investigated the developmental basis of floral unisexuality in the dioecious forage species Poa lanigera (section Dioicopoa) to determine whether its developmental trajectory conforms to previously described patterns in grasses or represents a distinct pathway. We also compared stamen arrest in pistillate florets of P. lanigera with suppression of the third stamen in the model grass Brachypodium distachyon to assess potential similarities in organ arrest mechanisms. By using scanning electron microscopy and histological analyses, we reconstructed the sequence of floret organ initiation and differentiation in both species. Florets were initially established as perfect and followed a common sequence of organ initiation, with divergence arising shortly after ovary closure, stylar branch initiation, and the transition of anthers to the tetralobed stage. In pistillate florets of P. lanigera, androecium abortion involved early disorganization of hypodermal anther tissues, which prevented sporogenous differentiation and microsporogenesis, whereas, in staminate florets, gynoecium abortion occurred after sporogenous cell formation through localized tissue degeneration, which disrupted megasporogenesis. These developmental routes differ from previously described patterns in Poaceae, indicating a distinct variant of floral unisexuality. In contrast, suppression of the third stamen in B. distachyon occurred at the primordium stage without tissue degeneration, suggesting a mechanistically different process. Together, these findings provide a developmental framework to investigate the genetic regulation of sex determination in P. lanigera, with potential applications for pasture improvement.
In most angiosperm plants, seeds are produced through a sexual process. Some angiosperms have developed an alternative reproductive strategy termed apomixis which involves producing seeds without the key steps of sexual development (i.e. meiosis, fertilization) and results in progeny genetically identical to the mother plant. Despite significant research advances, the evolutionary origin and molecular nature of apomixis remain unclear. Recent findings suggest that apomixis may have emerged from a sexual pathway deregulated by genetic and epigenetic modifications and stress signals (both endogenous and exogenous) that led to the alteration or omission of selected stages of sexual development. Apomixis, as a natural phenomenon that enables clonal reproduction by seeds, is a desirable trait with great potential in plant breeding, especially in terms of preserving hybrid vigor and gene combinations of elite phenotypes over subsequent generations. Notwithstanding, apomixis does not occur in major crops and therefore research programs focus on how to introgress, induce, or mimic apomixis in agronomically significant sexual species. The present review outlines the history of research on apomixis in flowering plants, its mechanisms, and a summary of the latest and most impactful research advances that may pave the way for the introduction of apomixis to sexually reproducing crops. The reader’s attention is also drawn to the partially explained issue of intercellular communication in ovules during early apomictic processes in the context of the cell wall’s changed chemical composition in cells that enter the apomictic developmental pathway. The review summarizes what we already know about apomixis, starting from early research and ending with the latest reports that present the genetic basis of apomixis and outline future perspectives.
Land plants alternate between multicellular haploid and diploid phases, requiring a tight coordination between vegetative growth and sexual reproduction. We investigated SWI3A/B, an ancient core subunit of the SWI/SNF complex, of the non-vascular liverwort Marchantia polymorpha. A mutation in the promoter of MpSWI3A/B affected gametangiophore development and spermiogenesis in males, revealing its male-specific role in reproductive development. The MpSWIA/B mutant line amplifies vegetative propagation in males under conditions that would normally induce reproductive growth. The phenotype was underpinned by transcriptomic changes, showing that MpSWI3A/B modulates key regulators of gametangiophore initiation (e.g. BONOBO, GLID), sperm development and motility (e.g. DUO1, PKAR), and asexual reproduction (e.g. KAI2). We propose that, as a chromatin-level regulator, MpSWI3A/B may contribute to balancing vegetative and reproductive phases and highlight the protein's potential when exploring ancient epigenetic functions that coordinate developmental phase transitions in land plants.
