RESUMEN
In the model plant Arabidopsis (Arabidopsis thaliana), endogenous and environmental signals acting on the shoot apical meristem cause acquisition of inflorescence meristem fate. This results in changed patterns of aerial development seen as the transition from making leaves to the production of flowers separated by elongated internodes. Two related BEL1-like homeobox genes, PENNYWISE (PNY) and POUND-FOOLISH (PNF), fulfill this transition. Loss of function of these genes impairs stem cell maintenance and blocks internode elongation and flowering. We show here that pny pnf apices misexpress lateral organ boundary genes BLADE-ON-PETIOLE1/2 (BOP1/2) and KNOTTED-LIKE FROM ARABIDOPSIS THALIANA6 (KNAT6) together with ARABIDOPSIS THALIANA HOMEOBOX GENE1 (ATH1). Inactivation of genes in this module fully rescues pny pnf defects. We further show that BOP1 directly activates ATH1, whereas activation of KNAT6 is indirect. The pny pnf restoration correlates with renewed accumulation of transcripts conferring floral meristem identity, including FD, SQUAMOSA PROMOTER-BINDING PROTEIN LIKE genes, LEAFY, and APETALA1. To gain insight into how this module blocks flowering, we analyzed the transcriptome of BOP1-overexpressing plants. Our data suggest a central role for the microRNA156-SQUAMOSA PROMOTER BINDING PROTEIN-LIKE-microRNA172 module in integrating stress signals conferred in part by promotion of jasmonic acid biosynthesis. These data reveal a potential mechanism by which repression of lateral organ boundary genes by PNY-PNF is essential for flowering.
Asunto(s)
Proteínas de Arabidopsis/metabolismo , Arabidopsis/genética , Regulación de la Expresión Génica de las Plantas , Proteínas de Homeodominio/metabolismo , Proteínas Represoras/metabolismo , Arabidopsis/crecimiento & desarrollo , Arabidopsis/fisiología , Proteínas de Arabidopsis/genética , Ciclopentanos/metabolismo , Flores/genética , Flores/crecimiento & desarrollo , Flores/fisiología , Proteínas de Homeodominio/genética , Meristema/genética , Meristema/crecimiento & desarrollo , Meristema/fisiología , MicroARNs/genética , Mutación , Proteínas Nucleares/genética , Proteínas Nucleares/metabolismo , Oxilipinas/metabolismo , Reguladores del Crecimiento de las Plantas/metabolismo , Proteínas Represoras/genética , Reproducción , Transducción de SeñalRESUMEN
Inflorescence architecture varies widely among flowering plants, serving to optimize the display of flowers for reproductive success. In Arabidopsis thaliana, internode elongation begins at the floral transition, generating a regular spiral arrangement of upwardly-oriented flowers on the primary stem. Post-elongation, differentiation of lignified interfascicular fibers in the stem provides mechanical support. Correct inflorescence patterning requires two interacting homeodomain transcription factors: the KNOTTED1-like protein BREVIPEDICELLUS (BP) and its BEL1-like interaction partner PENNYWISE (PNY). Mutations in BP and PNY cause short internodes, irregular spacing and/or orientation of lateral organs, and altered lignin deposition in stems. Recently, we showed that these defects are caused by the misexpression of lateral organ boundary genes, BLADE-ON-PETIOLE1 (BOP1) and BOP2, which function downstream of BP-PNY in an antagonistic fashion. BOP1/2 gain-of-function in stems promotes expression of the boundary gene KNOTTED1-LIKE FROM ARABIDOPSIS THALIANA6 (KNAT6) and shown here, ARABIDOPSIS THALIANA HOMEOBOX GENE1 (ATH1), providing KNAT6 with a BEL1-like co-factor. Our further analyses show that defects caused by BOP1/2 gain-of-function require both KNAT6 and ATH1. These data reveal how BOP1/2-dependent activation of a boundary module in stems exerts changes in inflorescence architecture.
Asunto(s)
Proteínas de Arabidopsis/genética , Arabidopsis/anatomía & histología , Arabidopsis/genética , Genes de Plantas/genética , Inflorescencia/anatomía & histología , Inflorescencia/genética , Arabidopsis/crecimiento & desarrollo , Proteínas de Arabidopsis/metabolismo , Tipificación del Cuerpo/genética , Regulación de la Expresión Génica de las Plantas , Silenciador del Gen , Proteínas de Homeodominio/genética , Proteínas de Homeodominio/metabolismo , Modelos Biológicos , Fenotipo , Tallos de la Planta/citología , Tallos de la Planta/genética , Tallos de la Planta/crecimiento & desarrollo , ARN Mensajero/genética , ARN Mensajero/metabolismo , Factores de Transcripción/genética , Factores de Transcripción/metabolismoRESUMEN
The transition to flowering in many plant species, including Arabidopsis (Arabidopsis thaliana), is marked by the elongation of internodes to make an inflorescence upon which lateral branches and flowers are arranged in a characteristic pattern. Inflorescence patterning relies in part on the activities of two three-amino-acid loop-extension homeodomain transcription factors: BREVIPEDICELLUS (BP) and PENNYWISE (PNY) whose interacting products also promote meristem function. We examine here the genetic interactions between BP-PNY whose expression is up-regulated in stems at the floral transition, and the lateral organ boundary genes BLADE-ON-PETIOLE1 (BOP1) and BOP2, whose expression is restricted to pedicel axils. Our data show that bp and pny inflorescence defects are caused by BOP1/2 gain of function in stems and pedicels. Compatible with this, inactivation of BOP1/2 rescues these defects. BOP expression domains are differentially enlarged in bp and pny mutants, corresponding to the distinctive patterns of growth restriction in these mutants leading to compacted internodes and clustered or downward-oriented fruits. Our data indicate that BOP1/2 are positive regulators of KNOTTED1-LIKE FROM ARABIDOPSIS THALIANA6 expression and that growth restriction in BOP1/2 gain-of-function plants requires KNOTTED1-LIKE FROM ARABIDOPSIS THALIANA6. Antagonism between BOP1/2 and BP is explained in part by their reciprocal regulation of gene expression, as evidenced by the identification of lignin biosynthetic genes that are repressed by BP and activated by BOP1/2 in stems. These data reveal BOP1/2 gain of function as the basis of bp and pny inflorescence defects and reveal how antagonism between BOP1/2 and BP-PNY contributes to inflorescence patterning in a model plant species.
