For centuries, the mechanisms underlying plant growth and morphogenesis have fascinated eminent thinkers who generated intriguing and still timely theories. It suffices to recall the theory on the directionality of cell division within a complex network of cells proposed by Hofmeister over 150 years ago and the theory on the trees’ organ shape proposed by Leonardo DaVinci over 500 years ago. Irrespective of the micro- or macro-dimension level of study, plant growth is ultimately the result of combined phenomena that include cell division, expansion, and differentiation within the constraints of genetic and physical interactions occurring in a growing network of cells. Though the molecular factors responsible for these basic cellular processes have surfaced and are becoming increasingly well characterized, the mechanisms and their precise spatial and temporal control are yet largely unknown. It is also questionable whether all the factors controlling plant growth have been identified. In their work, Skalák et al., 2019 addressed these questions in a study focused on understanding how cell division, expansion, and differentiation processes are coordinated through the action of cytokinines (CK) (Figure 1). It is well established that CKs are plant hormones controlling a plethora of developmental processes, including the determination of the final size and function of plant organs, such as leaves. Although zeatin, the first natural CK was isolated from unripe maize kernels by Letham in 1964, CKs signaling in the course of the transition from cell proliferation to cell expansion in early developing leaves or the differentiation of fully expanded leaf has been enigmatic. Recognizing the complexity of the plants inherent to the broad diversity of tissues, this research led by a collaboration of the Inzé and Brzobohatý groups focused on early leaf development to follow the transition from cell proliferation to cell expansion and differentiation. In their fascinating work, the authors queried the transcriptome and proteome of the leaf 3, being an established developmental model for morphogenesis analyses. Utilizing a suite of biomarkers for CK and inducible genetic tools to modulate CK abundance in situ, the authors were able to follow CK pool and signaling dynamics during the transition from cell proliferation to cell expansion and differentiation in leaf 3, and test their impact in the control of leaf development. The research led to a detailed time-course characterization of cell responses in relation to the CK pool during organ morphogenesis, an unanticipated relationship between CK pool and chloroplast biogenesis during the cell proliferation stage, and the findings supporting that a decrease of CK content at the end of the cell proliferation phase is necessary for the transition to cell expansion stimulation. In particular, a mere decrease in CK content triggered experimentally at the cell proliferation phase was sufficient to down- and up-regulate distinct sets of genes specific for the cell proliferation and cell expansion phase, respectively. Control by CK is novel for most of the genes found regulated during the transition from cell proliferation to cell expansion and differentiation. Intriguingly, genes involved in critical processes, such as cell wall biogenesis, very-long-chain fatty acid production and primary metabolism, were also identified, making several of the findings a springboard for testing the role of novel factors in controlling plant cell expansion. The work could have broader implications, as Brzobohatý states: “Plant biotechnologists might find our data useful when designing strategies to modify leaf size and structure in their efforts to generate novel plant cultivars for needs of sustainable agriculture”. The development of this work required tools and expertise developed in multiple labs. “Dirk's group has made a major contribution towards our understanding of molecular mechanisms governing leaf development. A direct motivation to initiate our collaboration came from re-examination of RNA-seq data sets obtained by transcriptome profiling of leaf 3 transition from cell proliferation to cell expansion phase (Andriankaja et al., 2012) which revealed down-regulation of a cytokinin activating gene (LOG3) during this process. Our transgenic plants enabling us to generate cytokinin excess and deficiency in specific developmental windows and our long-term interest in cytokinin biology together with Ondřej's expertise in hormonomics made it feasible to analyze cytokinin roles in leaf development”, Brzobohatý says. The experience and the tools developed to study leaf 3 development in relation to CK will allow the researchers to move forward to new horizons: “Having determined the multifaceted activity of CK in leaf development under standard conditions, we are now interested in CK roles in leaf development under various suboptimal growth conditions. We believe that by focusing our work on a particular leaf at various developmental windows we will be able to uncover molecular mechanisms, which might remain hidden when a whole rosette is analyzed as has been often the case”. With no doubts, many in the scientific community will be looking forward to the new research developments!
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Open Access
Apr 15, 2022
Gui-Luan Wang + 6
