Overlapping and antagonistic activities of BASIC PENTACYSTEINE genes affect a range of developmental processes in Arabidopsis

Abstract

SUMMARYThe BASIC PENTACYSTEINE (BPC) proteins are a plant-specific transcription factor family that is present throughout land plants. The Arabidopsis BPC proteins have been categorized into three classes based on sequence similarity, and we demonstrate that there is functional overlap between classes. Single gene mutations produce no visible phenotypic effects, and severe morphological phenotypes occur only in higher order mutants between members of classes I and II, with the most severe phenotype observed in bpc1-1 bpc2 bpc4 bpc6 plants. These quadruple mutants are dwarfed and display small curled leaves, aberrant ovules, altered epidermal cells and reduced numbers of lateral roots. Affected processes include coordinated growth of cell layers, cell shape determination and timing of senescence. Disruption of BPC3 function rescues some aspects of the bpc1-1 bpc2 bpc4 bpc6 phenotype, indicating that BPC3 function may be antagonistic to other members of the family. Ethylene response is diminished in bpc1-1 bpc2 bpc4 bpc6 plants, although not all aspects of the phenotype can be explained by reduced ethylene sensitivity. Our data indicate that the BPC transcription factor family is integral for a wide range of processes that support normal growth and development.

BASIC PENTACYSTEINE Proteins Mediate MADS Domain Complex Binding to the DNA for Tissue-Specific Expression of Target Genes in Arabidopsis

“…This is not surprising, considering that BPC1 shares sequence similarity to BPC2 and BPC3. Redundancy between these genes was further supported by the findings of Monfared et al (2011), who showed that all the ubiquitously expressed BPC genes are likely to have overlapping functions. Furthermore, the analysis of the bpc1-3 bpc2 bpc3 triple mutant that we show here revealed that the profile of STK promoter activity in this triple mutant was the same as in wild-type plants, which further strengthens the idea that redundancy occurs between BPC genes of different classes.…”

“…Recently, functional analysis of different classes of BPC genes in Arabidopsis showed that they have redundant functions in plant developmental processes (Monfared et al, 2011). Analysis of STK expression in the bpc1-1 mutant confirmed this, because STK was only slightly upregulated, but its expression profile was not affected (Kooiker et al, 2005).…”

“…This is further strengthened by the following observations: (1) many genes contain C-boxes in their putative promoter regions, (2) plants having multiple bpc genes mutated show a broad range of phenotypic effects (Monfared et al, 2011), and (3) BPC genes are ubiquitously expressed in plants.…”

“…All genes, except for BPC5, which is probably a pseudogene, are expressed ubiquitously. BPC genes belonging to these different classes were shown to be functionally redundant, and combining multiple bpc mutant alleles together results in a wide range of developmental defects (Monfared et al, 2011). Recently, we identified BPC1 as a regulator of the ovule identity gene SEEDSTICK (STK), which is specifically expressed in ovules (Rounsley et al, 1995;Pinyopich et al, 2003;Brambilla et al, 2007).…”

“…Recently, a new class of transcription factors, named BASIC PENTACYSTEINE (BPC), was identified (Meister et al, 2004). In Arabidopsis thaliana, BPCs belong to a small gene family of seven members that encode activators and repressors of transcription (Meister et al, 2004;Monfared et al, 2011;Berger and Dubreucq, 2012). Based on their sequence similarity, they were divided into three classes: class I (containing BPC1 to BPC3), class II (containing BPC4 to BPC6), and class III (containing only BPC7) (Meister et al, 2004).…”