Significance: Cell–cell communication is a prerequisite of multicellular development and noncell autonomous stem cell induction has been conserved during evolution. Cytoplasmic bridges, called plasmodesmata, which facilitate the exchange of molecules between neighboring cells, are a striking innovation for cell–cell signaling in plants. Here, we show that plasmodesmata function is required for the activity of shoot apical stem cells in Arabidopsis and provide evidence that the stem cell inducing transcription factor WUSCHEL moves from the niche into the stem cells via this route. WUSCHEL movement is functionally relevant and mediated by multiple protein domains. Because parts of the protein that restrict movement are required for homodimerization, the formation of WUSCHEL dimers might contribute to the regulation of stem cell activity in Arabidopsis .

The regulation of floral organ number is closely associated with floral meristem size. Mutations in the gene FLORAL ORGAN NUMBER1 (FON1) cause enlargement of the floral meristem in Oryza sativa (rice), resulting in an increase in the number of all floral organs. Ectopic floral organs develop in the whorl of each organ and/or in the additional whorls that form. Inner floral organs are more severely affected than outer floral organs. Many carpel primordia develop indeterminately, and undifferentiated meristematic tissues remain in the center in almost-mature flowers. Consistent with this result, OSH1, a molecular marker of meristematic indeterminate cells in rice, continues to be expressed in this region. Although floral meristems are strongly affected by the fon1-2 mutation, vegetative and inflorescence meristems are largely normal, even in this strong allele. We isolated the FON1 gene by positional cloning and found that it encodes a leucine-rich repeat receptor-like kinase most similar to CLAVATA1 (CLV1) in Arabidopsis thaliana. This suggests that a pathway similar to the CLV signaling system that regulates meristem maintenance in Arabidopsis is conserved in the grass family. Unlike CLV1, which is predominantly expressed in the L3 layer of the shoot meristem, FON1 is expressed throughout the whole floral meristem, suggesting that small modifications to the CLV signaling pathway may be required to maintain the floral meristem in rice. In addition, FON1 transcripts are detected in all meristems responsible for development of the aerial part of rice, suggesting that genes sharing functional redundancy with FON1 act in the vegetative and inflorescence meristems to mask the effects of the fon1 mutation.

A major feature of embryogenesis is the specification of stem cell systems, but in contrast to the situation in most animals, plant stem cells remain quiescent until the postembryonic phase of development. Here, we dissect how light and metabolic signals are integrated to overcome stem cell dormancy at the shoot apical meristem. We show on the one hand that light is able to activate expression of the stem cell inducer WUSCHEL independently of photosynthesis and that this likely involves inter-regional cytokinin signaling. Metabolic signals, on the other hand, are transduced to the meristem through activation of the TARGET OF RAPAMYCIN (TOR) kinase. Surprisingly, TOR is also required for light signal dependent stem cell activation. Thus, the TOR kinase acts as a central integrator of light and metabolic signals and a key regulator of stem cell activation at the shoot apex.

Legumes establish symbiotic associations with nitrogen-fixing bacteria (rhizobia) in root nodules to obtain nitrogen. Legumes control nodule number through long-distance communication between roots and shoots, maintaining the proper symbiotic balance. Rhizobial infection triggers the production of mobile CLE-RS1/2 peptides in Lotus japonicus roots; the perception of the signal by receptor kinase HAR1 in shoots presumably induces the production of an unidentified shoot-derived inhibitor (SDI) that translocates to roots and blocks further nodule development. Here we show that, CLE-RS1/2-HAR1 signalling activates the production of shoot-derived cytokinins, which have an SDI-like capacity to systemically suppress nodulation. In addition, we show that LjIPT3 is involved in nodulation-related cytokinin production in shoots. The expression of LjIPT3 is activated in an HAR1-dependent manner. We further demonstrate shoot-to-root long-distance transport of cytokinin in L. japonicus seedlings. These findings add essential components to our understanding of how legumes control nodulation to balance nutritional requirements and energy status.

To elucidate the genetic mechanism that regulates meristem maintenance in monocots, here we have examined the function of the gene FLORAL ORGAN NUMBER2 ( FON2 ) in Oryza sativa (rice). Mutations in FON2 cause enlargement of the floral meristem, resulting in an increase in the number of floral organs, although the vegetative and inflorescence meristems are largely normal. Molecular cloning reveals that FON2 encodes a small secreted protein, containing a CLE domain, that is closely related to CLAVATA3 in Arabidopsis thaliana . FON2 transcripts are localized at the apical region in all meristems in the aerial parts of rice plants, showing an expression pattern similar to that of Arabidopsis CLV3 . Constitutive expression of FON2 causes a reduction in the number of floral organs and flowers, suggesting that both the flower and inflorescence meristems are reduced in size. This action of FON2 requires the function of FON1 , an ortholog of CLV1 . Constitutive expression of FON2 also causes premature termination of the shoot apical meristem in Arabidopsis , a phenotype similar to that caused by constitutive expression of CLV3 . Together with our previous study of FON1 , these results clearly indicate that the FON1–FON2 system in rice corresponds to the CLV signaling system in Arabidopsis and suggest that the negative regulation of stem cell identity by these systems may be principally conserved in a wide range of plants within the Angiosperms. In addition, we propose a model of the genetic regulation of meristem maintenance in rice that includes an alternative pathway independent of FON2–FON1.