ABSTRACT
Plant morphogenesis is achieved by an interplay among the processes of cell differentiation, elongation, and specialization. During leaf development cells proceed through these processes at different rates depending on position along the medio-lateral and proximal-distal axes of the organ. The gene expression changes controlling cell fate along these axes remained elusive due to the difficulties in precise tissue isolation. This study combines rigorous early leaf characterization, laser capture microdissection, and transcriptomic sequencing to ask how patterns of gene expression regulate early leaf morphogenesis along the medio-lateral and proximal-distal axes in wild type Solanum lycopersium (tomato) and a leaf morphogenetic mutant trifoliate (tf-2). This work reveals transcriptional regulation of cell differentiation patterning along the proximal distal axis, and also identifies molecular signatures that delineate the classically defined marginal meristem / blastozone region early in leaf development. We describe and verify the importance of endoreduplication during leaf development, when and where photosynthetic competency is first achieved in the organ, regulation of auxin transport and signaling processes occurring along both the proximal-distal and medio-lateral axes, and narrow in on BLADE-ON-PETIOLE2 (BOP2) as a key regulator of margin tissue identity . CRISPR knockout mutants of BOP2 helped identify a unique phenotype of ectopic SAM formation on the complex leaf in tomato. Precise sampling practices allowed us to map gene expression signatures in specific domains of the leaf across multiple axes and evaluate the role of each domain in conferring indeterminacy and permitting blade outgrowth. This work also provides a global gene expression atlas of the early developing compound leaf.
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