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In a groundbreaking study published in PLOS Genetics, researchers from Cold Spring Harbor Laboratory have unveiled a fascinating evolutionary puzzle that has shaped the genetic regulation of plant growth and development. The study, led by Danielle Ciren, Sophia Zebell, and Zachary B. Lippman, focuses on the extreme restructuring of cis-regulatory regions controlling CLAVATA3 (CLV3), a gene crucial for maintaining the balance between stem cell proliferation and differentiation in plants.
CLV3, a signaling peptide, acts as a negative regulator of meristem proliferation in flowering plants. It is responsible for ensuring that the plant’s growing tips maintain a pool of undifferentiated stem cells, which are essential for the continuous formation of new organs. Despite its conserved function and expression pattern over approximately 125 million years, the cis-regulatory sequences upstream and downstream of CLV3 in Arabidopsis thaliana (Arabidopsis) and Solanum lycopersicum (tomato) have diverged significantly.
Using CRISPR-Cas9 genome editing, the researchers generated over 70 deletion alleles in the regulatory regions of CLV3 in both Arabidopsis and tomato. Their analysis revealed striking differences in the sensitivity of these regions to mutations. In tomato, the sequences upstream of CLV3 were highly sensitive to even small perturbations, whereas its downstream region was more tolerant. Conversely, in Arabidopsis, CLV3 function was resilient to severe disruptions both upstream and downstream of the coding sequence.
The study also uncovered distinct regulatory strategies between the two species. In tomato, CLV3 function primarily relies on interactions among cis-regulatory elements (CREs) in the 5′ non-coding region. In contrast, Arabidopsis CLV3 depends on a more balanced distribution of functional CREs between the 5′ and 3′ regions. This divergence in regulatory mechanisms highlights the remarkable malleability in the cis-regulatory structural organization of a deeply conserved plant stem cell regulator.
The researchers’ findings suggest that major reconfigurations of cis-regulatory sequence space are a common yet cryptic evolutionary force altering genotype-to-phenotype relationships in conserved genes. This study underscores the importance of lineage-specific dissection of the spatial architecture of cis-regulation to effectively engineer trait variation from conserved productivity genes in crops.
The implications of this research extend beyond understanding the evolutionary dynamics of plant stem cell regulation. It provides valuable insights into the mechanisms by which plants have adapted to diverse environments and offers potential avenues for crop improvement. By unraveling the complexities of cis-regulatory evolution, scientists can develop strategies to enhance crop yield, resilience, and adaptability to changing climate conditions.
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h ttps://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1011174