ASYMMETRIC-LEAVES2 and an ortholog of eukaryotic NudC domain proteins repress expression of AUXIN-RESPONSE-FACTOR and class 1 KNOX homeobox genes for development of flat symmetric leaves in Arabidopsis

Leaf primordia form around the shoot apical meristem, which consists of indeterminate stem cells. Upon initiation of leaf development, adaxial-abaxial patterning is crucial for appropriate lateral expansion, via cellular proliferation, and the formation of flat symmetric leaves. Many genes that specify such patterning have been identified, but regulation by upstream factors of the expression of relevant effector genes remains poorly understood. In Arabidopsis thaliana, ASYMMETRIC LEAVES2 (AS2) and AS1 play important roles in repressing transcription of class 1 KNOTTED1-like homeobox (KNOX) genes and leaf abaxial-determinant effector genes. We report here a mutation, designated enhancer of asymmetric leaves2 and asymmetric leaves1 (eal), that is associated with efficient generation of abaxialized filamentous leaves on the as2 or as1 background. Levels of transcripts of many abaxial-determinant genes, including ETTIN (ETT)/AUXIN RESPONSE FACTOR3 (ARF3), and all four class 1 KNOX genes were markedly elevated in as2 eal shoot apices. Rudimentary patterning in as2 eal leaves was suppressed by the ett mutation. EAL encodes BOBBER1 (BOB1), an Arabidopsis ortholog of eukaryotic NudC domain proteins. BOB1 was expressed in plant tissues with division potential and bob1 mutations resulted in lowered levels of transcripts of some cell-cycle genes and decreased rates of cell division in shoot and root apices. Coordinated cellular proliferation, supported by BOB1, and repression of all class 1 KNOX genes, ETT/ARF3 by AS2 (AS1) and BOB1 might be critical for repression of the indeterminate state and of aberrant abaxialization in the presumptive adaxial domain of leaf primordia, which might ensure the formation of flat symmetric leaves.