Timing leaf growth
 

Leaf heteroblasty is the fascinating natural phenomenon by which plants produce different leaves as they grow and mature. This requires a complex interplay between cellular growth and time, and allows a single plant to manifest a diverse range of leaf shapes and sizes over its lifespan. In a recent paper in the journal Current Biology, scientists from the Max Planck Institute for Plant Breeding Research in Cologne have now shed light on how this intricate process occurs during leaf development of the small mustard plant Arabidopsis thaliana. By studying the development of juvenile and adult leaves, they identified key differences in their cellular growth patterns, which they found were controlled by a SPL9-CYCD3 transcriptional module. These findings provide us with a deeper understanding of how the passing of time is encoded into organ growth and morphogenesis, and demonstrate the intricate tempo of plant growth and development.

In many plant species, the size and shape of their leaves change based on how old the plant is at the onset of each leaf’s growth. This process is known as heteroblasty. For example, in the common model species Arabidopsis, early leaves are smaller and rounder than leaves that develop later. An interdisciplinary research team led by Miltos Tsiantis in the Department of Comparative Development and Genetics, aims to understand the cellular and molecular mechanisms behind this phenomenon. As Tsiantis notes, “while we know a lot about spatial control in development, we know far less about how time is incorporated into these complex processes”. In this new study, they have employed advanced techniques including time-lapse imaging, cell fate mapping through live-imaging, computational modelling, and genetic studies. What has emerged from their findings is a nuanced picture of the temporal dynamics of plant growth that challenges common perceptions of plants as static entities. 

Most strikingly, the scientists found that during growth of the juvenile Arabidopsis leaf, there is a “burst” of cell proliferation that then stops abruptly, and is followed by rapid cell expansion. “Arabidopsis development is very well-studied,” explains lead author Xin-Min Li, “so it was incredibly exciting to identify a new feature, and only possible due to the advances we have made in imaging and computational analyses”. This proliferation burst causes juvenile leaves to contain fewer cells, and to be relatively small and round when compared to adult leaves. As the plant matures this growth pattern changes, with cell proliferation in later emerging leaves becoming less pronounced, but being sustained for a longer period. This leads to the production of larger, more elongated leaves in older plants.

Based on this newly-gained knowledge of the distinct growth patterns of juvenile and adult leaves, Xin-Min Li and his colleagues were then able to identify a transcription factor, SPL9, as a key player in orchestrating age-dependent changes in leaf form. Transcription factors such as SPL9 act like switches – they turn other genes on or off to regulate the activity of cells. During leaf development, the scientists found that SPL9 responds to inputs from both the age of the plant shoot and the maturation stage of individual leaves by turning on CyclinD3 family genes (which are important regulators of the cell cycle). In this way, SPL9 causes leaf cells to retain a proliferative status for longer, creating a ripple effect that impacts the overall shape and structure of the leaf. Using a range of intricate genetic experiments, the scientists were then able to demonstrate that CyclinD3 genes are themselves sufficient to control leaf shape and reprogram cellular growth, even in the absence of SPL9. Based on these data, they could then propose a SPL9-CYCD3 genetic regulatory module as a key driver of leaf heteroblasty.

These new insights into the genetic control of heteroblasty not only help us better understand plant growth, they also illuminate how nature can encode time into organ growth and morphogenesis. By connecting events that occur at a cellular level, to their impacts on the whole organism over the course of time, Tsiantis and his team are addressing questions that have captivated scientists for decades. Moving beyond the realm of basic research, understanding the temporal regulation of leaf development also holds great potential for practical applications in agriculture. Looking to the future, Tsiantis reflects, “as juvenile and adult leaves can have very different physiological roles and photosynthetic activities, by deciphering the molecular cues that dictate the growth patterns and shapes of leaves, we gain tools that can be harnessed for crop improvement and sustainable agriculture practices”.

SS & GR