Plant-specific GAGA-binding factors, BASIC PENTACYSTEINEs (BPCs; also called BARLEY B RECOMBINANTs, BBRs), are transcription factors that bind to GA-dinucleotide repeats frequently found in promoters of some Arabidopsis homeodomain genes (Sangwan et al., 2002, Santi et al., 2003, Meister et al., 2004, Kooiker et al., 2005, Montfarad et al., 2011, Hecker et al., 2015). These proteins were identified initially in soybean by their ability to bind to the (GA/TC)n - dinucleotide repeat enhancer element from the GSA1-promoter and they appear to play a role in basal transcription (Sangwan and O’Brian 2002).

In the dominant mutant Hooded (K), the barley gene BKn3 is overexpressed as a result of a duplication of 305 bp in intron IV. A one-hybrid screen using the 305 bp element as the DNA target led to the cloning of the barley b recombinant (BBR) protein, which binds specifically to the (GA/TC)8 repeat (Santi et al., 2003). BBR has properties of a GAGA-binding factor, but the corresponding gene has no sequence homology to Trl and Psq of Drosophila, which encode functionally analogous proteins. The 80 - 90 amino acids at the extreme C-terminus of the protein constitute the highly conserved basic DNA-binding domain (Santi et al., 2003).

In Arabidopsis genome there are 7 members of the BBR/BPC-family. Single BPC 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 (Montfarad et al., 2011). It was also found that two BBR/BPC-family members are involved in the expressional regulation of the homeotic MADS-box gene SEEDSTICK (STK) which controls ovule identity (Kooiker et al., 2005). BPCs form a meticulous repressor network for restricting their repressive functions to molecular mechanisms controlling plant growth and development (Lee at al., 2022).

In maize there are at least 4 BBR/BPC family members (Theune et al., 2019). A study was performed of the enhancer-driven regulatory network of two maize tissues at different stages: leaves at seedling stage (V2-IST) and husks (bracts) at flowering.  It was found that leaves at the V2-IST stage are characterized by the response to hormones and macromolecules biogenesis and assembly, which are regulated by the BBR/BPC and AP2/ERF TF families, respectively (Fagny et al., 2021). A QTL study in maize revealed a candidate gene for amylose content, namely GRMZM2G118690-encoding BBR/BPC transcription factor, which is used for the control of seed development (Sa et al., 2023).

Last updated June 2023 by John Gray and Ankita Abnave

References:

Sangwan I, O'Brian MR. Identification of a soybean protein that interacts with GAGA element dinucleotide repeat DNA. Plant Physiol. 2002 Aug;129(4):1788-94. doi: 10.1104/pp.002618. PMID: 12177492; PMCID: PMC166767.

Sangwan I, O'Brian MR. Identification of a soybean protein that interacts with GAGA element dinucleotide repeat DNA. Plant Physiol. 2002 Aug;129(4):1788-94. doi: 10.1104/pp.002618. PMID: 12177492; PMCID: PMC166767.

Santi L, Wang Y, Stile MR, Berendzen K, Wanke D, Roig C, Pozzi C, Müller K, Müller J, Rohde W, Salamini F. The GA octodinucleotide repeat binding factor BBR participates in the transcriptional regulation of the homeobox gene Bkn3. Plant J. 2003 Jun;34(6):813-26. doi: 10.1046/j.1365-313x.2003.01767.x. PMID: 12795701.

Lee YC, Tsai PT, Huang XX, Tsai HL. Family Members Additively Repress the Ectopic Expression of BASIC PENTACYSTEINE3 to Prevent Disorders in Arabidopsis Circadian Vegetative Development. Front Plant Sci. 2022 May 26;13:919946. doi: 10.3389/fpls.2022.919946. PMID: 35693178; PMCID: PMC9182635.

Meister RJ, Williams LA, Monfared MM, Gallagher TL, Kraft EA, Nelson CG, Gasser CS. Definition and interactions of a positive regulatory element of the Arabidopsis INNER NO OUTER promoter. Plant J. 2004 Feb;37(3):426-38. doi: 10.1046/j.1365-313x.2003.01971.x. PMID: 14731261.

Kooiker M, Airoldi CA, Losa A, Manzotti PS, Finzi L, Kater MM, Colombo L. BASIC PENTACYSTEINE1, a GA binding protein that induces conformational changes in the regulatory region of the homeotic Arabidopsis gene SEEDSTICK. Plant Cell. 2005 Mar;17(3):722-9. doi: 10.1105/tpc.104.030130. Epub 2005 Feb 18. PMID: 15722463; PMCID: PMC1069694.

Monfared MM, Simon MK, Meister RJ, Roig-Villanova I, Kooiker M, Colombo L, Fletcher JC, Gasser CS. Overlapping and antagonistic activities of BASIC PENTACYSTEINE genes affect a range of developmental processes in Arabidopsis. Plant J. 2011 Jun;66(6):1020-31. doi: 10.1111/j.1365-313X.2011.04562.x. Epub 2011 Apr 6. PMID: 21435046.

Hecker A, Brand LH, Peter S, Simoncello N, Kilian J, Harter K, Gaudin V, Wanke D. The Arabidopsis GAGA-Binding Factor BASIC PENTACYSTEINE6 Recruits the POLYCOMB-REPRESSIVE COMPLEX1 Component LIKE HETEROCHROMATIN PROTEIN1 to GAGA DNA Motifs. Plant Physiol. 2015 Jul;168(3):1013-24. doi: 10.1104/pp.15.00409. Epub 2015 May 29. PMID: 26025051; PMCID: PMC4741334.

Theune ML, Bloss U, Brand LH, Ladwig F, Wanke D. Phylogenetic Analyses and GAGA-Motif Binding Studies of BBR/BPC Proteins Lend to Clues in GAGA-Motif Recognition and a Regulatory Role in Brassinosteroid Signaling. Front Plant Sci. 2019 Apr 16;10:466. doi: 10.3389/fpls.2019.00466. PMID: 31057577; PMCID: PMC6477699.

Fagny M, Kuijjer ML, Stam M, Joets J, Turc O, Rozière J, Pateyron S, Venon A, Vitte C. Identification of Key Tissue-Specific, Biological Processes by Integrating Enhancer Information in Maize Gene Regulatory Networks. Front Genet. 2021 Jan 11;11:606285. doi: 10.3389/fgene.2020.606285. PMID: 33505431; PMCID: PMC7834273.

Sa KJ, Park H, Jang SJ, Lee JK. Association Mapping of Amylose Content in Maize RIL Population Using SSR and SNP Markers. Plants (Basel). 2023 Jan 4;12(2):239. doi: 10.3390/plants12020239. PMID: 36678952; PMCID: PMC9865990.