Floral homeotic C function genes repress specific B function genes in the carpel whorl of the basal eudicot California poppy (Eschscholzia californica)

Abstract

BackgroundThe floral homeotic C function gene AGAMOUS (AG) confers stamen and carpel identity and is involved in the regulation of floral meristem termination in Arabidopsis. Arabidopsis ag mutants show complete homeotic conversions of stamens into petals and carpels into sepals as well as indeterminacy of the floral meristem. Gene function analysis in model core eudicots and the monocots rice and maize suggest a conserved function for AG homologs in angiosperms. At the same time gene phylogenies reveal a complex history of gene duplications and repeated subfunctionalization of paralogs.ResultsEScaAG1 and EScaAG2, duplicate AG homologs in the basal eudicot Eschscholzia californica show a high degree of similarity in sequence and expression, although EScaAG2 expression is lower than EScaAG1 expression. Functional studies employing virus-induced gene silencing (VIGS) demonstrate that knock down of EScaAG1 and 2 function leads to homeotic conversion of stamens into petaloid structures and defects in floral meristem termination. However, carpels are transformed into petaloid organs rather than sepaloid structures. We also show that a reduction of EScaAG1 and EScaAG2 expression leads to significantly increased expression of a subset of floral homeotic B genes.ConclusionsThis work presents expression and functional analysis of the two basal eudicot AG homologs. The reduction of EScaAG1 and 2 functions results in the change of stamen to petal identity and a transformation of the central whorl organ identity from carpel into petal identity. Petal identity requires the presence of the floral homeotic B function and our results show that the expression of a subset of B function genes extends into the central whorl when the C function is reduced. We propose a model for the evolution of B function regulation by C function suggesting that the mode of B function gene regulation found in Eschscholzia is ancestral and the C-independent regulation as found in Arabidopsis is evolutionarily derived.

Functional Analysis of All AGAMOUS Subfamily Members in Rice Reveals Their Roles in Reproductive Organ Identity Determination and Meristem Determinacy

“…Interestingly, in both these basal eudicots and in the asterid A. majus, the inhibition of AG-like gene function led to the homeotic conversion of the gynoecium into petal-like organs, rather than into sepal-like organs as would be predicted by the classic ABC model, suggesting an involvement of AG-like genes in the repression of B-function genes in the fourth whorl of these species (Davies et al, 1999;Yellina et al, 2010;Hands et al, 2011).…”

“…Recently, the functional conservation of AG-like genes in mediating the C-function, which means the determination of stamen and carpel identity, and the regulation of FM determinacy has also been demonstrated by virus-induced gene silencing experiments in the basal eudicots California poppy (Eschscholzia californica) and opium poppy (Papaver somniferum), both belonging to the Papaveraceae family (Hands et al, 2011;Yellina et al, 2010). Interestingly, in both these basal eudicots and in the asterid A. majus, the inhibition of AG-like gene function led to the homeotic conversion of the gynoecium into petal-like organs, rather than into sepal-like organs as would be predicted by the classic ABC model, suggesting an involvement of AG-like genes in the repression of B-function genes in the fourth whorl of these species (Davies et al, 1999;Yellina et al, 2010;Hands et al, 2011).…”

TheseirenaB Class Floral Homeotic Mutant of California Poppy (Eschscholzia californica) Reveals a Function of the Enigmatic PI Motif in the Formation of Specific Multimeric MADS Domain Protein Complexes

“…AG1 and AG2 are the two known C class genes in California poppy (Zahn et al, 2005;Yellina et al, 2010). Both are expressed in mature stamens (Figure 2A), and the levels are higher in inner stamens compared with outer stamens.…”

Aislamiento y caracterización de genes MADS-box en Medicago truncatula: duplicaciones génicas y subfuncionalización en el linaje euAGAMOUS

“…En Antirrhinum majus, el ortólogo de SHP1/SHP2, PLE, es funcionalmente similar a AG (Carpenter y Coen, 1990), mientras que el gen del linaje euAG, FAR, tiene un papel menor en la identidad de órganos y la determinación meristemática, pero juega un papel en el desarrollo tardío de estambres (Davies et al, 1999). La duplicación de genes de clase C seguida de diversificación también se ha descrito, entre otros, en Zea mays (Mena et al, 1996), Cucumis sativus (Kater et al, 1998), Petunia hybrida , Oryza sativa (Yamaguchi et al, 2006) y Eschscholzia californica (Yellina et al, 2010). Así pues, puede deducirse que tras la duplicación de los genes de clase C en Medicago truncatula, ocurrieron cambios en su expresión temporal y espacial, lo que sugiere que han sufrido varios grados de sub-y/o neofuncionalización en sus funciones en la regulación del desarrollo de las estructuras reproductoras.…”

“…AG es el único gen de clase C en Arabidopsis thaliana, pero se han aislado dos genes de clase C en Antirrhinum majus (Bradley et al, 1993;Davies et al, 1999), Lotus japonicus (Dong et al, 2005), Petunia hybrida (Angenent et al, 1993;Tsuchimoto et al, 1993), Nicotiana tabacum (Kempin et al, 1993), Populus trichocarpa (Brunner et al, 2000), Eschscholzia californica (Yellina et al, 2010) y Papaver somniferum (Hands et al, 2011), entre otras. En la mayoría de estos casos, los patrones de expresión de ambos genes son casi idénticos.…”