Arabidopsis JAGGED LATERAL ORGANS Acts with ASYMMETRIC LEAVES2 to Coordinate KNOX and PIN Expression in Shoot and Root Meristems

Abstract

Organ initiation requires the specification of a group of founder cells at the flanks of the shoot apical meristem and the creation of a functional boundary that separates the incipient primordia from the remainder of the meristem. Organ development is closely linked to the downregulation of class I KNOTTED1 LIKE HOMEOBOX (KNOX) genes and accumulation of auxin at sites of primordia initiation. Here, we show that Arabidopsis thaliana JAGGED LATERAL ORGANS (JLO), a member of the LATERAL ORGAN BOUNDARY DOMAIN (LBD) gene family, is required for coordinated organ development in shoot and floral meristems. Loss of JLO function results in ectopic expression of the KNOX genes SHOOT MERISTEMLESS and BREVIPEDICELLUS (BP), indicating that JLO acts to restrict KNOX expression. JLO acts in a trimeric protein complex with ASYMMETRIC LEAVES2 (AS2), another LBD protein, and AS1 to suppress BP expression in lateral organs. In addition to its role in KNOX regulation, we identified a role for AS2 in regulating PINFORMED (PIN) expression and auxin transport from embryogenesis onwards together with JLO. We propose that different JLO and AS2 protein complexes, possibly also comprising other LBD proteins, coordinate auxin distribution and meristem function through the regulation of KNOX and PIN expression during Arabidopsis development.

Alternate wiring of a KNOXI genetic network underlies differences in leaf development of A. thaliana and C. hirsuta

“…Leaf length, area, and perimeter were calculated from silhouettes using Fijii software (Schindelin et al 2012). The petiole cell length and number was measured as described (Rast and Simon 2012;Vlad et al 2014).…”

Leaf development and morphogenesis

“…In addition, the AS1-AS2 complex has recently been shown to recruit POLYCOMB-REPRESSIVE COMPLEX 2 (PRC2), a complex involved in chromatin structure modification, to the promoters of two KNOXI genes, possibly enabling their stable repression at later stages of leaf development (Lodha et al, 2013). The expression of KNOXI genes is also regulated by BLADE ON PETIOLE (BOP) (Ha et al, 2007;Ichihashi et al, 2014), JAGGED LATERAL ORGANS (JLO) (Rast and Simon, 2012) and auxin . KNOXI proteins, in turn, feedback to regulate the auxin response (Bolduc et al, 2012;Scanlon et al, 2002;Tsiantis et al, 1999).…”

Leaf Development

“…Many genetic factors are involved in the suppression of class I KNOX genes expression in leaf primordia: Byrne et al 2000;Semiarti et al 2001;Iwakawa et al 2002;Ha et al 2003;Kumar et al 2007;Guo et al 2008;Schiessl et al 2012). Some of these factors form protein complexes and function in the same genetic pathway (Xu et al 2003;Li et al 2012;Rast and Simon 2012). Others, however, are not specific repressors of the class I KNOX pathway; they have other specific roles, e.g., in separate components of protein complexes.…”

“…3, 5); it functions in suppression of class I KNOX genes, such as STM and KNAT1, in the basal parts of leaf primordia through formation of the JLO-AS2 heteromer (Rast and Simon 2012). If JLO activity is lost, the SAM becomes inactive; weak alleles result in leaflet-like structures when combined with the as2 mutation, owing to mis-expression of the KNOX genes in leaves (Rast and Simon 2012). Curiously, ectopic expressions of STM and KNAT1 are induced in leaves under the influence of the 35S promoter, resulting in serrated and deformed leaves (Borghi et al 2007).…”