Global socioeconomic developments create strong incentives for farmers to shift from transplanted to direct-seeded rice (DSR) as a means of intensification and economization(1). Rice production must increase to ensure food security(2) and the bulk of this increase will have to be achieved through intensification of cultivation, because expansion of cultivated areas is reaching sustainable limits(3). Anaerobic germination tolerance, which enables uniform germination and seedling establishment under submergence(4), is a key trait for the development of tropical DSR varieties(5,6). Here, we identify a trehalose-6-phosphate phosphatase gene, OsTPP7, as the genetic determinant in qAG-9-2, a major quantitative trait locus (QTL) for anaerobic germination tolerance(7). OsTPP7 is involved in trehalose-6-phosphate (T6P) metabolism, central to an energy sensor that determines anabolism or catabolism depending on local sucrose availability(8,9). OsTPP7 activity may increase sink strength in proliferating heterotrophic tissues by indicating low sugar availability through increased T6P turnover, thus enhancing starch mobilization to drive growth kinetics of the germinating embryo and elongating coleoptile, which consequently enhances anaerobic germination tolerance.

No abstract

In angiosperms, transition from floral organ maintenance to abscission determines plant reproductive success and seed dispersion. For petal abscission, local cell fate decision at petal cell base is more important than general senescence or cell death of petals at organ levels. However, how this decision is regulated in a spatiotemporal manner remains unclear. Here, we describe a jasmonic acid (JA)–regulated chromatin state change that directs the local cell fate determination via autophagy at the base of petals. During petal maintenance phase, transcriptional co-repressors of JA signaling accumulate at the base of petals to block MYC activity, leading to lower reactive oxygen species (ROS) levels. JA acts as an airborne signaling molecule transmitted from stamens to petals and accumulates primarily in petal bases to trigger epigenetic reprograming, allowing MYC transcription factors to interact with MEDIATOR25 and to increase chromatin accessibility for key downstream targets, such as Arabidopsis NAC DOMAIN-CONTAINING PROTEIN102 (ANAC102). ANAC102 specifically accumulates at the base of petals just prior to petal abscission and triggers local ROS accumulation and cell death via AUTOPHAGY-RELATED GENES induction. Notably, this ANAC102-triggered autophagy at the petal base causes maturation, vacuolar delivery, and breakdown of autophagosome for terminal cell differentiation. Because dynamic changes in the number of vesicles and cytoplasmic components in the vacuole are often seen in many plants, the local cell fate determination by autophagy may be conserved for petal abscission across angiosperms and may have been recruited under the JA/NAC module to pattern plant organ detachment systems.

The MADS domain transcription factor AGAMOUS (AG) regulates floral meristem termination by preventing maintenance of the histone modification H3K27me3 along the KNUCKLES (KNU) coding sequence. At two days after AG binding, cell division has diluted the repressive mark H3K27me3, allowing activation of KNU transcription prior to floral meristem termination. However, how many other downstream genes are temporally regulated by this intrinsic epigenetic timer and what their functions are remain unknown. Here, we identify direct AG targets regulated through cell cycle–coupled H3K27me3 dilution in Arabidopsis thaliana. Expression of the targets KNU, AT HOOK MOTIF NUCLEAR LOCALIZED PROTEIN18 (AHL18), and PLATZ10 occurred later in plants with longer H3K27me3-marked regions. We established a mathematical model to predict timing of gene expression and manipulated temporal gene expression using the H3K27me3-marked del region from the KNU coding sequence. Increasing the number of del copies delayed and reduced KNU expression in a Polycomb Repressive Complex 2– and cell cycle–dependent manner. Furthermore, AHL18 was specifically expressed in stamens and caused developmental defects when mis-expressed. Finally, AHL18 bound to genes important for stamen growth. Our results suggest that AG controls the timing of expression of various target genes via cell cycle–coupled dilution of H3K27me3 for proper floral meristem termination and stamen development.

The termination of floral meristems is regulated by the MADS domain transcription factor AGAMOUS (AG) by passively diluting the H3K27me3 mark along the KNUCKLES (KNU) coding sequence. How many other downstream genes are similarly regulated by this intrinsic epigenetic timer and whether it can be harnessed for engineering synthetic circuits are unknown. Here, we describe a biotimer gene regulatory network downstream of AG and manipulate the timing of KNU expression through a synthetic system. We manipulated temporal gene expression using the del region from the KNU coding sequence, which is decorated by H3K27me3-marked nucleosomes. Increasing the number of del copies delayed and reduced KNU expression in a PRC2- and cell cycle-dependent manner. We propose that PRC2 deposits H3K27me3, while cell divisions dilute H3K27me3 accumulation on the extended KNU coding sequence. Our results shed light on temporal transitions governing flower development and provide a novel tool for tunable gene expression.