Ancestral expression patterns and evolutionary diversification of YABBY genes in angiosperms

Abstract

SUMMARYLateral organ growth in seed plants is controlled in part by members of the YABBY (YAB) and class III homeodomain/leucine zipper (HD-ZIPIII) families of transcription factors. HD-ZIPIII genes appear to play a conserved role in such organs, but YAB genes have diversified, with some members of the family having specialized functions in leaves, carpels or ovule integuments. The ancestral expression patterns and timing of divergence of the various classes of YAB genes remain to be established. We isolated and evaluated the expression of one HD-ZIPIII and five YAB genes representing the five major YAB gene classes from Cabomba caroliniana, a member of the earliest-diverging angiosperms. Consistent with observations in eudicots, the FILAMENTOUS FLOWER (FIL) and YABBY5 (YAB5) genes of C. caroliniana were expressed in the abaxial regions of the leaf where new laminar segments arise, and the patterns of expression were mutually exclusive to those of HD-ZIPIII, indicating that these expression patterns are ancestral. Expression of CRABS CLAW (CRC) in the abaxial carpel wall, and of INNER NO OUTER (INO) in the abaxial outer integument of ovules was also conserved between eudicots and C. caroliniana, indicating that these patterns are primitive. However, the CRC gene was also expressed in other floral organs in C. caroliniana, and expression in stamens was also observed in another early-diverging species, Amborella trichopoda, indicating that carpel-specific expression was acquired after divergence of the Nymphaeales. The expression data and phylogeny for YAB genes suggest that the ancestral YAB gene was expressed in proliferating tissues of lateral organs.

A Gene for Genetic Background in Zea mays: Fine-Mapping enhancer of teosinte branched1.2 to a YABBY Class Transcription Factor

“…Previous studies in Arabidopsis revealed that members of the YABBY gene family act redundantly to regulate complex patterning and growth decisions in lateral organ development (Bowman and Smyth 1999;Eshed et al 1999;Sawa et al 1999;Siegfried et al 1999;Villanueva et al 1999;Bowman 2000;Sarojam et al 2010;Finet et al 2016 (Yamada et al 2011). FIL and YAB3 act together to promote leaf growth and expansion, including some aspects of adaxialabaxial polarity (Siegfried et al 1999).…”

“…The YABBY gene family consists of five clades, namely CRABS CLAW (CRC), INNER NO OUTER (INO), YABBY3/FILAMENTOUS FLOWER (YAB3/FIL), YABBY2 (YAB2), and YABBY5 (YAB5) (Yamada et al 2011). FIL and YAB3 act together to promote leaf growth and expansion, including some aspects of adaxialabaxial polarity (Siegfried et al 1999).…”

“…We performed Bayesian phylogenetic analysis of the extracted YABBY peptide sequences using MrBayes v3.1.2 on XSEDE provided by the CIPRES Science Gateway (Miller et al 2010). Parameters used in this phylogenetic analysis were kept the same as the parameters originally used by Yamada et al (2011). The model for amongsite rate variation (rates=) was set to invariant + gamma and rate matrix for amino acids (aamodelpr=) was set to Jones (Jones et al 1992).…”

“…Of these 107 YABBY peptide sequences, 101 were taken from Yamada et al (2011) and six others were taken from UniProt (The UniProt Consortium 2015) and Lin et al (2012). We aligned all 107 YABBY peptide sequences using Clustal X2.1 (Larkin et al 2007) and Se-Al v2.0a11 (Rambaut 2002).…”

“…We also found a similar, but not identical, insertion in W22 at a different position between the first and second exons ( Figure S7). Phylogenetic analysis revealed that GRMZM2G085873 belongs to the YAB2 clade of the five known clades in the YABBY gene family ( Figure S8) (Siegfried et al 1999;Bowman 2000;Yamada et al 2011). Given this result, we designated GRMZM2G085873 as ZmYAB2.1.…”