PerspectivePlant Reproduction

Linking stem cells to germ cells

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Science  28 Apr 2017:
Vol. 356, Issue 6336, pp. 378-379
DOI: 10.1126/science.aan2734

In response to their sessile nature and a need for flexibility in adapting to the environment, plants can often propagate through organ regeneration, develop functional gametes without a need to eliminate half of their chromosomes, generate embryos from somatic cells in almost any tissue, or produce viable seeds in the absence of fertilization. In many cases, this intriguing flexibility relies on developmental alternatives to classic sexual reproduction. Like many multicellular organisms, most plant species harbor gametes poised to give rise to progeny after fusion of a sperm and egg. However, plants generate gamete precursors from adult somatic tissue, rather than during embryogenesis. On page 396 of this issue, Zhao et al. (1) report the role of a signaling circuit that, by controlling cell proliferation and differentiation in young reproductive organs, is essential for initiating meiosis and generating gametes in the sexual model species Arabidopsis thaliana. The finding opens new opportunities for establishing an integrative view of how reiterative developmental mechanisms contribute to the acquisition and maintenance of reproductive versatility in plants.

Animal development is characterized by a progressive restriction of embryonic competence. This allows the proliferation of stem cells, which progressively differentiate into diverse cell types. By contrast, flowering plants produce organs throughout their life cycle by maintaining “stemness” in meristem tissue, tightly associated cells located at the root and shoot apices. Consequently, the male and female germ lines are not established in the embryo but in the adult plant during floral organ differentiation.

Gamete specification

Flowering plants display continuous postembryonic development and differentiation of the germ line during adulthood.

GRAPHIC: G. GRULLÓN/SCIENCE

In many flowering plant species, including Arabidopsis, a single somatic cell initiates the female reproductive lineage (see the figure). The somatic cell first differentiates into a female meiotic gamete precursor (a meiocyte) during early ovule formation in the adult plant. A meiocyte subsequently gives rise to a single viable haploid cell (its three companion sister cells immediately degenerate after meiosis). The coordination of ovule growth with meiocyte specification requires a subtle spatiotemporal synchrony of cell proliferation and differentiation. During the eukaryotic cell division cycle, a gap (G1) phase ensures a molecular checkpoint before launching the synthesis (S) phase that triggers DNA replication. The overall topology of the G1-to-S-phase control mechanism in animals is conserved in plants, particularly during female gametogenesis (2). In mammals, a key regulator of this mechanism is the tumor suppressor retinoblastoma (Rb) protein. Rb is a multifunctional transcriptional repressor that controls cell proliferation, differentiation, and survival. It inhibits the expression of genes required for S-phase entry, but also interacts with transcription factors and chromatin remodeling enzymes that are important for the development of specific cell lineages, such as those of progenitor and stem cells (3). During the Arabidopsis cell cycle, inhibitory action of the Rb homolog RETINOBLASTOMA-RELATED 1 (RBR1) is repressed when it is phosphorylated by cyclin-dependent kinase A;1 (CDKA;1). CDKA;1 is, in turn, repressed by the redundant activity of several CDK inhibitors of the KIP-RELATED PROTEIN (KRP) family. Because RBR1 inhibits KRP degradation, the circuit controls cell proliferation through the antagonistic interaction between CDKA;1 and KRPs.

Zhao et al. determined that a similar signaling module coordinates proliferation and differentiation of the plant germ line, mainly through the action of RBR1. The authors discovered that simultaneous mutations in three Arabidopsis CDK inhibitors (KRP4, KRP6, and KRP7) result in the differentiation of supernumerary female meiocytes that often give rise to ectopic nonfunctional gametes. This rare phenotype was previously reported in rice and maize plants that were defective in a leucine-rich receptor membrane protein or its ligand (4, 5), suggesting that signaling pathways could link meiocyte differentiation and survival to the action of specific signaling proteins (6). Dosage-sensitive genetic complementation in Arabidopsis showed that the defect in meiocyte production is caused by a failure of KRPs to inhibit CDKA;1. As expected, plants defective in RBR1 also showed supernumerary female meiocytes, a phenotype that was not previously reported (7). A decrease of CDKA;1 activity in the rbr1 mutant did not reduce the number of abnormal meiocytes, demonstrating that the defect does not depend on cell proliferation. Rather, the defect is caused by failure of a mechanism that restricts cell differentiation before meiosis. Strikingly, this mechanism is driven by the action of RBR1 as a direct repressor of the gene WUSCHEL (WUS). WUS encodes a homeobox transcription factor that is crucial for specifying stem cells in the shoot apical meristem (8). WUS plays a role in ovule development, but its role in promoting meiocyte differentiation has not been clear (9, 10). WUS protein localization is restricted to epidermal cells of the ovule by the action of RBR1 and CDK inhibitors, confirming that its regulation is also important for the specification of the female germ line.

RBR1 controls context-dependent signaling pathways by interacting with diverse binding partners, giving rise to a large collection of cell lineages and cell identities that are crucial for the plant life cycle. Does the RBR1-WUS circuit interact with RNA-dependent DNA methylation and chromatin to avoid gametogenesis in somatic cells (11, 12)? Although RBR1 is required for regulating chromatin remodeling late during gametogenesis (13), it is not clear how plant Rb proteins could epigenetically connect environmental response, cell cycle progression, and internal differentiation signals.

The findings of Zhao et al. provide a previously unknown link between stem cell and germ cell differentiation through the extended aura that surrounds Rb and homeobox proteins. These proteins are indeed among the most versatile regulators for controlling animal and plant development.

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