The flattening of leaves to form broad blades is an important adaptation that maximizes photosynthesis. However, the molecular mechanism underlying this process remains unclear. The WUSCHEL-RELATED HOMEOBOX (WOX) genes WOX1 and PRS are expressed in the leaf marginal domain to enable leaf flattening, but the nature of WOX expression establishment remains elusive. Here, we report that adaxial-expressed MONOPTEROS (MP) and abaxial-enriched auxin together act as positional cues for patterning the WOX domain. MP directly binds to the WOX1 and PRS promoters and activates their expression. Furthermore, redundant abaxial-enriched ARF repressors suppress WOX1 and PRS expression, also through direct binding. In particular, we show that ARF2 is redundantly required with ARF3 and ARF4 to maintain the abaxial identity. Taken together, these findings explain how adaxial-abaxial polarity patterns the mediolateral axis and subsequent lateral expansion of leaves.
Stem cells are responsible for organogenesis, but it is largely unknown whether and how information from stem cells acts to direct organ patterning after organ primordia are formed. It has long been proposed that the stem cells at the plant shoot apex produce a signal, which promotes leaf adaxial-abaxial (dorsoventral) patterning. Here we show the existence of a transient low auxin zone in the adaxial domain of early leaf primordia. We also demonstrate that this adaxial low auxin domain contributes to leaf adaxial-abaxial patterning. The auxin signal is mediated by the auxin-responsive transcription factor MONOPTEROS (MP), whose constitutive activation in the adaxial domain promotes abaxial cell fate. Furthermore, we show that auxin flow from emerging leaf primordia to the shoot apical meristem establishes the low auxin zone, and that this auxin flow contributes to leaf polarity. Our results provide an explanation for the hypothetical meristem-derived leaf polarity signal. Opposite to the original proposal, instead of a signal derived from the meristem, we show that a signaling molecule is departing from the primordium to the meristem to promote robustness in leaf patterning. Extensive molecular genetic studies of more than a decade have identified a transcriptional regulatory network containing several adaxially or abaxially expressed leaf abaxial-and adaxialpromoting genes (1-6). These genes encode transcription factors and small RNAs, and their domain-specific expression patterns are required for adaxial-abaxial asymmetric cell differentiation and lamina expansion. Regulatory genes expressed in the abaxial domain suppress those expressed in the adaxial domain and vice versa. MicroRNAs 165 and 166 (MiR165/166) and transcription factor-encoding KANADI (KAN) genes are expressed in the abaxial domain and restrict the expression of class III homeo-
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