A novel Filamentous Flower mutant suppresses brevipedicellus developmental defects and modulates glucosinolate and auxin levels.

Eiji Nambara,C. Daniel Riggs,Baohua Li,Daniel J. Kliebenstein,Scott J. Douglas,Miguel A Blazquez

doi:10.1371/journal.pone.0177045

Eiji Nambara, C. Daniel Riggs + Show 4 more

Open Access

https://doi.org/10.1371/journal.pone.0177045

Copy DOI

Abstract

BREVIPEDICELLUS (BP) encodes a class-I KNOTTED1-like homeobox (KNOX) transcription factor that plays a critical role in conditioning a replication competent state in the apical meristem, and it also governs growth and cellular differentiation in internodes and pedicels. To search for factors that modify BP signaling, we conducted a suppressor screen on bp er (erecta) plants and identified a mutant that ameliorates many of the pleiotropic defects of the parent line. Map based cloning and complementation studies revealed that the defect lies in the FILAMENTOUS FLOWER (FIL) gene, a member of the YABBY family of transcriptional regulators that contribute to meristem organization and function, phyllotaxy, leaf and floral organ growth and polarity, and are also known to repress KNOX gene expression. Genetic and cytological analyses of the fil-10 suppressor line indicate that the role of FIL in promoting growth is independent of its previously characterized influences on meristem identity and lateral organ polarity, and likely occurs non-cell-autonomously from superior floral organs. Transcription profiling of inflorescences revealed that FIL downregulates numerous transcription factors which in turn may subordinately regulate inflorescence architecture. In addition, FIL, directly or indirectly, activates over a dozen genes involved in glucosinolate production in part by activating MYB28, a known activator of many aliphatic glucosinolate biosynthesis genes. In the bp er fil-10 suppressor mutant background, enhanced expression of CYP71A13, AMIDASE1 (AMI) and NITRILASE genes suggest that auxin levels can be modulated by shunting glucosinolate metabolites into the IAA biosynthetic pathway, and increased IAA levels in the bp er fil-10 suppressor accompany enhanced internode and pedicel elongation. We propose that FIL acts to oppose KNOX1 gene function through a complex regulatory network that involves changes in secondary metabolites and auxin.

Highlights

Growth and development of terrestrial plants is guided by events occurring at meristems, zones where pluripotent stem cells perpetuate themselves and generate raw material for organ production
Class 1 KNOTTED1-like homeobox (KNOX) genes play integral roles in many of these processes, and their expression is subject to activation or repression, spatially and/or temporally, by several well-characterized factors and auxin [3]
The KNOX1 proteins condition a replication competent state and prevent differentiation in the meristem, and their expression is downregulated as cells are recruited into lateral organ primorida, yet other studies have revealed that reactivation of KNOX genes occurs in leaves of compound leaf species [23]

Summary

Introduction

Growth and development of terrestrial plants is guided by events occurring at meristems, zones where pluripotent stem cells perpetuate themselves and generate raw material for organ production. The shoot apical meristem (SAM) elaborates leaf, stem and flower anlagen at specific regions depending on complex temporal and spatial interactions between proteins, microRNAs and hormones [1,2]. Leaf blades of the kn dominant mutant display knots of undifferentiated cells around lateral veins due to ectopic expression of the KN1 gene product [4,5]. In numerous monocot and dicot species, the expression of a variety of KNOX1 proteins in leaves conditions the production of ectopic meristems, implicating the factors as critical regulators of meristem function in a diverse array of plants [6,7,8]

Methods

Results

Conclusion