CYCP2;1 integrates genetic and nutritional information to promote meristem cell division in Arabidopsis.

In higher plants, cell cycle activation in the meristems at germination is essential for the initiation of post-embryonic development. We previously identified the signaling pathways of homeobox transcription factor STIMPY and metabolic sugars as two interacting branches of the regulatory network that is responsible for activating meristematic tissue proliferation in Arabidopsis. In this study, we found that CYCP2;1 is both a direct target of STIMPY transcriptional activation and an early responder to sugar signals. Genetic and molecular studies show that CYCP2;1 physically interacts with three of the five mitotic CDKs in Arabidopsis, and is required for the G2 to M transition during meristem activation. Taken together, our results suggest that CYCP2;1 acts as a permissive control of cell cycle progression during seedling establishment by directly linking genetic control and nutritional cues with the activity of the core cell cycle machinery.

ELONGATA3 is required for shoot meristem cell cycle progression in Arabidopsis thaliana seedlings.

A key feature of the development of a higher plant is the continuous formation of new organs from the meristems. Originally patterned during embryogenesis, the meristems must activate cell division de novo at the time of germination, in order to initiate post-embryonic development. In a mutagenesis screen aimed at finding new players in early seedling cell division control, we identified ELONGATA3 (ELO3) as a key regulator of meristem cell cycle activation in Arabidopsis. Our results show that plants carrying a hypomorphic allele of ELO3 fail to activate cell division in the meristems following germination, which leads to seedling growth arrest and lethality. Further analyses suggest that this is due to a failure in DNA replication, followed by cell cycle arrest, in the meristematic tissue. Interestingly, the meristem cell cycle arrest in elo3 mutants, but not the later leaf developmental defects that have been linked to the loss of ELO3 activities, can be relieved by the addition of metabolic sugars in the growth medium. This finding points to a new role by which carbohydrate availability promotes meristem growth. Furthermore, growth arrested elo3 mutants suffer a partial loss of shoot meristem identity, which provides further evidence that cell cycle activities can influence the control of tissue identity.

Regulation of meristem size by cytokinin signaling.

The plant meristems possess unique features that involve maintaining the stem cell populations while providing cells for continued development. Although both the primary shoot apical meristem (SAM) and the root apical meristem (RAM) are specified during embryogenesis, post-embryonic tissue proliferation is required for their full establishment and maintenance throughout a plants' life. The phytohormone cytokinin (CK) interacts with other systemic signals and is a key regulator of meristem size and functions. The SAM and the RAM respond to CK stimulations in different manners: CK promotes tissue proliferation in the SAM through pathways dominated by homeobox transcription factors, including the class I KNOX genes, STIP, and WUS; and curiously, it favors proliferation at low levels and differentiation at a slightly higher concentration in the RAM instead. Here we review the current understanding of the molecular mechanisms underlying CK actions in regulating meristematic tissue proliferation.

Metabolic sugar signal promotes Arabidopsis meristematic proliferation via G2.

Most organs in higher plants are generated postembryonically from the meristems, which harbor continuously dividing stem cells throughout a plant's life cycle. In addition to developmental regulations, mitotic activities in the meristematic tissues are modulated by nutritional cues, including carbon source availability. Here we further analyze the relationship between the sugar signal and seedling meristem establishment, taking advantage of our previous observation that exogenously supplied metabolic sugars can rescue the meristem growth arrest phenotype of the Arabidopsis stip mutant seedlings. Our results show that metabolic sugars reactivate the stip meristems by activating the expression of key cell cycle regulators, and therefore, promoting G2 to M transition in Arabidopsis meristematic tissues. One of the early events in this process is the transcriptional repression of TSS, a genetic suppressor of the stip mutations, by sugar signals, suggesting that TSS may act as an integrator of developmental and nutritional signals in regulating meristematic proliferation. We also present evidence that metabolic sugar signals are required for the activation of mitotic entry during de novo meristem formation from G2 arrested cells. Our observations, together with the recent findings that nutrient deprivation leads to G2 arrest of animal germline stem cells, suggest that carbohydrate availability-regulated G2 to M transition may represent a common mechanism in stem cell division regulation in multicellular organisms.

STIMPY mutants have increased cytokinin sensitivity during dark germination.

The cytokinins regulate a broad range of plant developmental events. We recently reported that the homeodomain transcription factor STIMPY (STIP) positively mediates the cytokinin signals in maintaining proliferative and pluoripotent properties of the shoot apical meristem in Arabidopsis. In line with our proposed model, light-grown stip seedlings are less sensitive to the growth inhibition effect of the exogenously applied cytokinins than wild type. Here we investigate STIP's role in cytokinin signaling in dark-grown seedlings, in which elevated cytokinin levels promote photomorphogenesis. We found that stip mutants show enhanced deetiolation phenotype in response to cytokinin treatment in the dark, suggesting that STIP may be a negative regulator of cytokinin signaling under this condition. We discuss possible explanations for this observed developmental stage-specific function of STIP.

STIMPY mediates cytokinin signaling during shoot meristem establishment in Arabidopsis seedlings.

The establishment of the primary meristems through proliferation after germination is essential for plant post-embryonic development. Cytokinins have long been considered a key regulator of plant cell division. Here we show that cytokinins are essential for early seedling development of Arabidopsis. Loss of cytokinin perception leads to a complete failure of meristem establishment and growth arrest after germination. We also present evidence that cytokinin signaling is involved in activation of the homeobox gene STIMPY (STIP or WOX9) expression in meristematic tissues, which is essential for maintaining the meristematic fate. Cytokinin-independent STIP expression is able to partially compensate for the shoot apical meristem growth defects in mutants that cannot sense cytokinin. These findings identify a new branch of the cytokinin signaling network, linking cytokinin to the process of meristem and seedling establishment.