Developmental events leading to peltate leaf structure in Tropaeolum majus (Tropaeolaceae) are associated with expression domain changes of a YABBY gene

Abstract

Peltate leaf architecture has evolved from conventional bifacial leaves many times in flowering plant evolution. Characteristics of peltate leaves, such as the differentiation of a cross zone and of a radially symmetric, margin-less petiole, have also been observed in mutants of genes responsible for adaxial-abaxial polarity establishment. This suggests that altered regulation of such genes provided a mechanism for the evolution of peltate leaf structure. Here, we show that evolution of leaf peltation in Tropaeolum majus, a species distantly related to Arabidopsis thaliana, was associated with altered expression of Tropaeolum majus FILAMENTOUS FLOWER (TmFIL), a gene conferring abaxial identity. In situ hybridization indicates that adaxial and abaxial domains are established in early leaf primordia as in species with bifacial leaves. Upon initiation of the cross zone by fusion of the blade margins, localized expansion of TmFIL to the upper leaf side could be seen, indicating a local loss of adaxial leaf identity. The observed changes in expression are consistent with a role of TmFIL in radialization of the petiole and circularization of the leaf blade margin by the cross zone. In addition, expression was observed in segment primordia and during expansion of the bifacial blade, suggesting additional roles for TmFIL in leaf development.

Adaxial–abaxial polarity: The developmental basis of leaf shape diversity

“…Another example of expression rearrangement is found in the peltate‐leaved species Tropaeolum majus . In leaf primordia, TmFIL mRNA is localized to the abaxial side at an early stage, reminiscent of FIL / YAB1 localization in conventional bifacial leaves of Arabidopsis (Gleissberg et al ., ). This expression pattern is concordant with the observation that peltate leaves of this species arise from fully bifacial primordia (Hagemann and Gleissberg, ).…”

“…This expression pattern is concordant with the observation that peltate leaves of this species arise from fully bifacial primordia (Hagemann and Gleissberg, ). Later, the TmFIL expression domain expands into the adaxial side of the petiole (Gleissberg et al ., ) and the initially bifacial petiole is secondarily compensated by additional growth to form radially symmetric structure (Hagemann and Gleissberg, ). This suggests that the TmFIL expression domain is rearranged to generate a new adaxial–abaxial boundary at the cross‐zone, where growth activity is induced (Fig.…”

Molecular characterization the YABBY gene family in Oryza sativa and expression analysis of OsYABBY1

“…Likewise, PROLONGATA, an ortholog of Arabidopsis YAB5, is expressed in a polar manner in Antirrhinum . A gene orthologous to FIL is expressed abaxially in leaf primordia in Tropaeloum majus, which like Arabidopsis belongs to the Brassicales, but unlike Arabidopsis has a peltate leaf architecture (Gleissberg et al 2005). Thus, polar regulation of the spatial expression of YABBY genes may be conserved across eudicots, suggesting that they may have similar roles in leaf development.…”

Identification and expression analysis of YABBY family genes associated with fruit shape in tomato (Solanum lycopersicum L.)

“…As an ortholog of the CRC/DL genes, the lily LiYAB1 gene can rescue the phenotype of the rice dl mutant (Wang et al, 2009). Similar to CRC in Arabidopsis, the altered expression of the TmFIL gene is related to the peltate leaf structure in Tropaeolum majus (Gleissberg et al, 2005). The INO gene plays a significant role in the formation and asymmetric growth of the ovule outer integument in Arabidopsis (Villanueva et al, 1999).…”