Leaflet initiation and blade expansion are separable in compound leaf development

Abstract

Compound leaves are composed of multiple separate blade units termed leaflets. In tomato (Solanum lycopersicum) compound leaves, auxin promotes both leaflet initiation and blade expansion. However, it is unclear how these two developmental processes interact. With highly variable complexity, tomato compound leaves provide an ideal system to address this question. In this study, we obtained and analyzed mutants of the WUSCHEL-RELATED HOMEOBOX (WOX) family gene SlLAM1 from tomato, whose orthologs in tobacco (Nicotiana sylvestris) and other species are indispensable for blade expansion. We show that SlLAM1 is expressed in the middle and marginal domains of leaves, and is required for blade expansion in leaflets. We demonstrate that sllam1 mutants cause a delay of leaflet initiation and slightly alter the arrangement of first-order leaflets, whereas the overall leaflet number is comparable to that of wild-type leaves. Analysis of the genetic interactions between SlLAM1 and key auxin signaling components revealed an epistatic effect of SlLAM1 in determining the final leaf form. Finally, we show that SlLAM1 is also required for floral organ growth and affects the fertility of gametophytes. Our data suggest that SlLAM1 promotes blade expansion in multiple leaf types, and leaflet initiation can be largely uncoupled from blade expansion during compound leaf morphogenesis.

Leaf form diversification in an ornamental heirloom tomato results from alterations in two different HOMEOBOX genes

“…CR-wox1-1 plants showed narrower leaves (Figures 4B and 4C) and lower LVD than M82 (Figure 4D), matching the phenotype described in wox1 mutants in other species 18,19 and tomato mutants, unfused flower (uf), and SlLAM1. [21][22][23] We noticed that these phenotypes were similar to those of the classical tomato mutant, solanifolia (sf). sf is known to have narrower leaflets and reduced vascular density, 24 and our rough mapping of the sf mutation identified a genomic location close to that known for the WOX1 locus (at the end of chromosome 3; Figure S4A).…”

“…sf single mutants with truncated WOX1 protein, such as CR-wox1-1, sf^wl, and e1862, do not have any lobes on their leaves, whereas a weaker phenotype mutant, sf, had lobed leaves (Figure 4B), suggesting that sf regulated tomato leaf development in a dosage-dependent manner. Although a previous study showed that sf was involved in floral organ growth with mutants showing severe defects in fruit development, 23 SiFT produced normal edible fruits (Figure S5E). This difference in fruit development might be related to the SF level.…”

“…33 A recent study demonstrated that sllam1 failed to establish auxin response maxima along the leaf margin. 23 Hence, we proposed that SF functions in leaf lamina outgrowth and couples this growth feature with vascular patterning. WOX1 is present in the early diverging angiosperm Amborella trichopoda, 34 but its function in basal angiosperms remains unknown.…”

“…WOX1 is expressed in leaf primordia and is involved in leaf lamina expansion in various plant species, including tomato. [18][19][20][21][22][23] In the Medicago truncatula wox1 mutant, leaf vein density was lower than that in the wild type (WT). 19,23 Therefore, Sl WOX1 is likely to be a candidate gene for controlling both leaflet width and leaf vein density in the tomato.…”

Coordination of differentiation rate and local patterning in compound‐leaf development

“…For example, Arabidopsis CUC2 and CUC3 were dispensable for the miR‐TCP‐NGA overexpression phenotype (Alvarez et al ., 2016), while the current study shows that in tomato the increase in leaf complexity caused by downregulation of the TCP factor LA depends on intact GOB activity. Additional factors such as the WUSCHEL‐related homeobox (WOX1) and (PRESSED FLOWER) PRS also appear to have conserved roles in marginal elaboration (Lin et al ., 2013; Zhang et al ., 2014; Alvarez et al ., 2016; Guan et al ., 2017; Du et al ., 2020). It will therefore be interesting to investigate whether these are coordinated with other differentiation and patterning regulators in tomato and whether here too different species represents variations on a common theme in the precise interaction among the regulators.…”