The Casparian strip in the root endodermis forms an apoplastic barrier between vascular tissues and outer ground tissues to enforce selective absorption of water and nutrients. Because of its cell-type specificity, the presence of a Casparian strip is used as a marker for a functional endodermis. Here, we examine the minimal regulators required for reprograming non-endodermal cells to build a functional Casparian strip. We demonstrate that the transcription factor SHORT-ROOT (SHR) serves as a master regulator and promotes Casparian strip formation through two independent activities: inducing the expression of essential Casparian strip enzymes via MYB36 and directing the subcellular localization of Casparian strip formation via SCARECROW (SCR). However, this hierarchical signaling cascade still needs SHR-independent small peptides, derived from the stele, to eventually build a functional Casparian strip in non-endodermal cells. Our study provides a synthetic approach to induce Casparian-strip-containing endodermis using a minimal network of regulators and reveals the deployment of both apoplastic and symplastic communication in the promotion of a specific cell fate.

Suberin lamellae, which provide a hydrophobic protective barrier against biotic and abiotic stresses, are widely deposited in various cell types during plant development and in response to stress. However, it remains unclear how developmental programs interact with stress responses to direct the precise spatiotemporal pattern of suberin deposition. In this study, we found that SHORT-ROOT (SHR), together with its downstream factor MYB36, guided suberization specifically in the root endodermis. Despite a partial dependence on abscisic acid (ABA), the suberization mediated by SHR and MYB36 appeared to derive from a slow readout of developmental programs, which was in contrast to the rapid but transient suberization induced by ABA. Furthermore, we found the MYB39 transcription factor functioned as a common downstream hub of the SHR/MYB36 pathway and the ABA-triggered response. MYB39 could directly bind to the FAR5 (alcohol-forming fatty acyl-coenzyme A reductase) promoter to activate its expression. In addition, overexpression of MYB39 dramatically increased the amount of suberization in Arabidopsis roots. Our results provide important insights into the interaction between developmental programs and environmental stimuli in root suberization in Arabidopsis.

Flooding tolerance is an important trait for tomato breeding. In this study, we obtained a recessive mutant exhibiting highly enhanced submergence resistance. Phenotypical analyses showed that this resistant to flooding (rf) mutant displays slightly chlorotic leaves and spontaneous initiation of adventitious roots (ARs) on stems. The mutation was mapped to the phytochromobilin synthase gene AUREA (AU), in which a single amino acid substitution from asparagine to tyrosine occurred. In addition to the classic function of AU in phytochrome and chlorophyll biogenesis in leaves, we uncovered its novel role in mediating AR formation on stems. We further observed temporal coincidence of the two phenotypes in the rf mutant: chlorosis and spontaneous AR formation and revealed that AU functions by maintaining heme homeostasis. Interestingly, our grafting results suggest that heme might play roles in AR initiation via long-distance transport from leaves to stems. Our results present genetic evidence for the involvement of the AU–heme oxygenase-1–heme pathway in AR initiation in tomato. As fruit production and yield in the rf mutant are minimally impacted, the mutation identified in this study may provide a target for biotechnological renovation of tomato germplasm in future breeding.

Summary Fruit malformation is a major constrain in fruit production worldwide resulting in substantial economic losses. The farmers for decades noticed that the chilling temperature before blooming often caused malformed fruits. However, the molecular mechanism underlying this phenomenon is unclear. Here we examined the fruit development in response to cold stress in tomato, and demonstrated that short‐term cold stress increased the callose accumulation in both shoot apical and floral meristems, resulting in the symplastic isolation and altered intercellular movement of WUS. In contrast to the rapidly restored SlWUS transcription during the recovery from cold stress, the callose removal was delayed due to obstructed plasmodesmata. The delayed reinstatement of cell‐to‐cell transport of SlWUS prevented the activation of SlCLV3 and TAG1, causing the interrupted feedback inhibition of SlWUS expression, leading to the expanded stem cell population and malformed fruits. We further showed that the callose dynamics in response to short‐term cold stress presumably exploits the mechanism of bud dormancy during the seasonal growth, involving two antagonistic hormones, abscisic acid and gibberellin. Our results provide a novel insight into the cold stress regulated malformation of fruit.