Role of BLADE-ON-PETIOLE1 and 2 in patterning the Arabidopsis thaliana leaf and inflorescence

The architectural design of plants is selected by nature for optimal survival and reproductive fitness. A major goal of plant developmental biologists is to identify genes that control plant shape and form and to understand how these genes interact to create structural diversity. BLADE-ON-PETIOLE1 (BOP1) and BOP2 are an ancient and conserved set of plant-specific transcriptional co-regulators that play a key role in determining the architecture of leaves, inflorescences, and fruits in the model plant species, Arabidopsis thaliana. Phenotypes in bop1 bop2 loss-of-function mutants include leafy petioles, asymmetric flowers subtended by a bract, lack of floral-organ abscission, and the partial conversion of flowers to shoots. Conversely, BOP1/2 gain-of-function mutants have severe defects in internode elongation resulting in short, compacted inflorescences. However, the mechanisms behind these architectural variations have yet to be determined. In my thesis, I show that BOP1/2 are expressed in initiating lateral organ primordia during both the vegetative and reproductive phases of Arabidopsis development. As these primordia separate from the meristem, BOP expression stably shifts to the proximal boundary region that separates these primordia from the meristem or from adjacent structures. In floral meristems, I show that BOP1 and BOP2 function redundantly with LEAFY, a master regulator of floral-meristem identity, to promote the expression of APETALA1, a key marker of commitment to floral fate. All three activities then converge in the floral meristem during stages 2-3 to down-regulate the expression of inflorescence identity genes including AGAMOUS-LIKE24 to promote the formation of a determinate floral shoot. In leaves, I show that BOP1 and BOP2 in the petiole function redundantly with leaf patterning factors ASYMMETRIC LEAVES1 (AS1) and AS2 to maintain the stable repression of Class I KNOTTED1-LIKE HOMEOBOX (KNOX1 ) meristematic genes to facilitate simple leaf formation. In inflorescences, I show that the expression of BOP genes and the KNOX1 family member K&barbelow;NOTTED-LIKE FROM A&barbelow;RABIDOPSIS T&barbelow;HALIANA6 (KNAT6) are confined to pedicel axils (a boundary that separates the pedicel from the stem) by the combined activities of the KNOX1 family member BREVIPEDILLUS (BP) and its interacting partner PENNYWISE (PNY). My data show that BOP2 and KNAT6 expression domains are differentially enlarged in bp and pny mutants, corresponding to the distinctive patterns of short internodes, clustered or downward-oriented siliques, and defects in epidermal cell differentiation characteristic of these mutants. These data indicate that BP-PNY and BOP1/2-KNAT6 have reciprocal functions in the inflorescence. Further evidence shows that BOP1/2 are positive regulators of KNAT6 expression and that this regulation may be direct. Collectively, my work shows that BOP1/2 are key regulators of determinacy in lateral shoot and organ primordia and illustrate that changes in determinacy lead to dramatic architectural variation in these structures. My data also indicate that BOP1/2-KNAT6 (boundary factors) and BP-PNY (meristematic factors) have antagonistic functions in the inflorescence stem: the combined activities of BP-PNY restrict BOP1/2-KNAT6 to pedicel axils to facilitate the production of an inflorescence in which lateral branches and flowers are equally spaced along elongated internodes. Future studies will determine if differences in BOP 1 /2 activity or expression pattern form a common module for creating architectural diversity in plant species.