Timing is crucial for plant organ morphogenesis

Abstract

Plants continuously and reproducibly create new organs throughout their lifecycles. Their success in maintaining organ size and shape robustness amazes researchers due to the complexity of plant organ morphogenesis. In this context, robustness is the ability to form organs reproducibly despite intrinsic and extrinsic perturbations. Although there has been some research investigating plant organ robustness, many important questions remain. I started by considering the emergence of plant organs as an engineering task and elucidated the complexity of plant organ morphogenesis. I emphasized the surprising contribution of stochastic variation in gene expression and cellular growth to pattern formation to proper plant organ morphogenesis. I highlighted recent research efforts employing quantitative 4D growth tracking and computational analysis, which also serve as key techniques in my PhD study. I chose Arabidopsis sepals as the model system and identified the variable organ size and shape 2 (vos2) mutant, which has variable sepal sizes throughout the development of the flower. VOS2 encodes a MYB domain transcription factor, which controls the timing of sepal initiation by focusing plant hormone (auxin and cytokinin) signaling in the incipient sepal primordia and by softening cell walls to promote growth of the primordium. Further bioinformatic analysis of RNA-seq and proteomics points to defects in ribosomes and metabolism in vos2 mutants. Sepal initiation is variably delayed in vos2 mutants and the delayed initiation leads to smaller sepal sizes at all later flower stages. Thus, the timing of sepal initiation is crucial for robust sepal size. I also studied the development of Arabidopsis fruit. Previous studies showed that regulatory pathways are conserved among leaves and floral organs, making me curious about whether conserved growth patterns also exist. Surprisingly, my study revealed that unlike the spatial separation of cell division and cell expansion in Arabidopsis leaves and sepals, fruit morphogenesis exhibits a temporal separation of cell division before fertilization and cell expansion after. Through live imaging and computational modeling, I concluded that a signaling cascade initialized at fertilization promotes valve elongation. The extent of fertilization controls the final fruit size and the timing of fertilization controls switch of the growth pattern from cell division to cell expansion.