Interplay between miRNA regulation and mechanical stress forCUCgene expression at the shoot apical meristem

Abstract

The shoot apical meristem is the central organizer of plant aerial organogenesis. The molecular bases of its functions involve several cross-talks between transcription factors, hormones and microRNAs. We recently showed that the expression of the homeobox transcription factor STM is induced by mechanical perturbations, adding another layer of complexity to this regulation. Here we provide additional evidence that mechanical perturbations impact the promoter activity of CUC3, an important regulator of boundary formation at the shoot meristem. Interestingly, we did not detect such an effect for CUC1. This suggests that the robustness of expression patterns and developmental programs is controlled via a combined action of molecular factors as well as mechanical cues in the shoot apical meristem. KEYWORDSCUC genes; mechanical stress; Meristem; micro-RNAs Throughout their lifetime, plants are exposed to a number of external mechanical perturbations, such as wind or touch. This leads to changes in mRNA level of many genes, and long-term developmental responses such as stem thickening and flowering delay 5 In addition to these external factors, plants are also constantly affected by intrinsic tensile stresses, notably because plant cells are under high turgor pressure. There is now accumulating evidence that these internal stresses are affecting many aspects of the cells, thus channeling growth in the long term.14 The shoot apical meristem (SAM) is the central organizer of plant aerial organogenesis. Initiation of new organs and maintenance of SAM is achieved through the concomitant action of multiple regulatory pathways. Genetic screens have identified many key players, including transcription factors, hormones, and microRNAs. 38,48,53,55 In addition to these biochemical factors, mechanical forces are also present within the meristem. In particular, the boundary domain that separates newly emerging organ from the meristem is under highly anisotropic tensile stresses. 4,15,32 A key question for the future is the analysis of the interplay between mechanical forces and the molecular regulators of meristem function (Fig. 1A).In a recent article, 26 we showed that a master regulator of meristem maintenance, the homeodomain protein SHOOT MERISTEMLESS (STM) is expressed at a higher level in the boundary domain, and that this local increase in promoter activity can be related to mechanical stress: mechanical perturbations are sufficient to induce STM expression in the meristem. Interestingly, mechanical perturbations do not affect all boundary-expressed genes in the same way. For instance, the promoter activity of the PINOID gene, which is also increased in the boundary domain, is not affected by mechanical perturbations. 26Here we focus on the most canonical genetic markers of boundary identity, the CUP SHAPED COTYLEDON (CUC) genes. CUC1, CUC2 and CUC3, belong to a group of NAC domain transcription factors and show a high level of functional redundancy. They play an essential role in shoot meristem initiation throug...

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