A Role for APETALA1/FRUITFULL Transcription Factors in Tomato Leaf Development  

Abstract

Flexible maturation rates underlie part of the diversity of leaf shape, and tomato (Solanum lycopersicum) leaves are compound due to prolonged organogenic activity of the leaf margin. The CINCINNATA -TEOSINTE BRANCHED1, CYCLOIDEA, PCF (CIN-TCP) transcription factor LANCEOLATE (LA) restricts this organogenic activity and promotes maturation. Here, we show that tomato APETALA1/FRUITFULL (AP1/FUL) MADS box genes are involved in tomato leaf development and are repressed by LA. AP1/FUL expression is correlated negatively with LA activity and positively with the organogenic activity of the leaf margin. LA binds to the promoters of the AP1/FUL genes MBP20 and TM4. Overexpression of MBP20 suppressed the simple-leaf phenotype resulting from upregulation of LA activity or from downregulation of class I knotted like homeobox (KNOXI) activity. Overexpression of a dominant-negative form of MBP20 led to leaf simplification and partly suppressed the increased leaf complexity of plants with reduced LA activity or increased KNOXI activity. Tomato plants overexpressing miR319, a negative regulator of several CIN-TCP genes including LA, flower with fewer leaves via an SFTdependent pathway, suggesting that miR319-sensitive CIN-TCPs delay flowering in tomato. These results identify a role for AP1/FUL genes in vegetative development and show that leaf and plant maturation are regulated via partially independent mechanisms.

Leaf development and morphogenesis

“…The suppression of the activity of FUL-like genes results in reduced leaf complexity and in a partial suppression of the phenotype caused by miR319 overexpression. Overexpression of one of the genes from this family suppressed the La gain-of-function phenotype (Burko et al, 2013). This suggests that AP1/FUL proteins promote the morphogenetic activity of the tomato leaf margin, in agreement with accumulating evidence pointing to a role for FUL-like genes in leaf development in Arabidopsis, poppy, pea and Aquilegia (Ferrandiz et al, 2000;PabonMora et al, 2012PabonMora et al, , 2013Teper-Bamnolker and Samach, 2005).…”

“…In the leaf, a high SFT/FT ratio promotes maturation, leading to a simplified leaf form. This effect is enhanced in conjunction with the trifoliate (tf ) mutant and is suppressed by miR319 overexpression (Burko et al, 2013;Shalit et al, 2009).…”

Global Transcriptome Profiling of Developing Leaf and Shoot Apices Reveals Distinct Genetic and Environmental Control of Floral Transition and Inflorescence Development in Barley

“…Pleiotropic effects of flowering time regulators might be a consequence of changes in source-sink relationships triggered by the transition from vegetative to reproductive growth. However, studies in Arabidopsis and tomato also suggested that FT-like genes and the downstream targets SOC1 and AP1/FUL may control the activity of leaf meristems (Teper-Bamnolker and Samach, 2005;Melzer et al, 2008;Shalit et al, 2009;Burko et al, 2013). For example, Melzer et al (2008) showed that FT and its downstream targets SOC1 and FUL controlled determinacy of leaf and axillary meristems independent of flowering time in Arabidopsis.…”

Regulation of Compound Leaf Development by PHANTASTICA in Medicago truncatula

“…In C. hirsuta and tomato, the down-regulation of KNOXI genes results in compound leaves with reduced leaflets Shani et al, 2009;Burko et al, 2013). In tomato, overexpression of the KNOXI gene, LeT6, results in supercompound leaves (Hareven et al, 1996).…”