Control of inflorescence architecture in tomato by BTB/POZ transcriptional regulators

Abstract

Plant productivity depends on inflorescences, flower-bearing shoots that originate from the stem cell populations of shoot meristems. Inflorescence architecture determines flower production, which can vary dramatically both between and within species. In tomato plants, formation of multiflowered inflorescences depends on a precisely timed process of meristem maturation mediated by the transcription factor gene TERMINATING FLOWER (TMF), but the underlying mechanism is unknown. We show that TMF protein acts together with homologs of the Arabidopsis BLADE-ON-PETIOLE (BOP) transcriptional cofactors, defined by the conserved BTB (Broad complex, Tramtrack, and Bric-a-brac)/POZ (POX virus and zinc finger) domain. TMF and three tomato BOPs (SlBOPs) interact with themselves and each other, and TMF recruits SlBOPs to the nucleus, suggesting formation of a transcriptional complex. Like TMF, SlBOP gene expression is highest during vegetative and transitional stages of meristem maturation, and CRISPR/Cas9 elimination of SlBOP function causes pleiotropic defects, most notably simplification of inflorescences into single flowers, resembling tmf mutants. Flowering defects are enhanced in higher-order slbop tmf mutants, suggesting that SlBOPs function with additional factors. In support of this, SlBOPs interact with TMF homologs, mutations in which cause phenotypes like slbop mutants. Our findings reveal a new flowering module defined by SlBOP-TMF family interactions that ensures a progressive meristem maturation to promote inflorescence complexity.

Ideal crop plant architecture is mediated by tassels replace upper ears1, a BTB/POZ ankyrin repeat gene directly targeted by TEOSINTE BRANCHED1

“…Although BOP-like genes do not function as transcription factors, they have been shown to interact with them in Arabidopsis (25) as well as tomato. For example, the nuclear transport of tomato BTB/POZ genes is mediated by their interaction with transcription factors such as TERMINATING FLOWER (46), indicating that tru1 may be part of a transcriptional complex. Thus, the complex developmental changes conditioned by bop1 mutants in different species may be due to misexpression of multiple downstream target genes.…”

“…Members of the BTB/POZ clade of ankyrin repeat proteins have a wide range of functions (25) including establishment of floral and inflorescence meristem determinacy (45)(46)(47), but those most similar to tru1 appear to have a clear function in specifying leaf cell identities. The founding members of this clade, BLADE ON PETIOLE 1 and 2, display ectopic distal blade tissue growing down the petiole and lack of stipules (24,48).…”

Lotus japonicus NOOT‐BOP‐COCH‐LIKE1 is essential for nodule, nectary, leaf and flower development

“…In Arabidopsis, AtCUC1 promotes the expression of LIGHT‐DEPENDENT SHORT HYPOCOTYLS 3 ( AtLSH3 ) and its paralog AtLSH4 , which are members of the Arabidopsis LSH1 and Oryza G1 gene family ( ALOG ; Cho and Zambryski, ; Takeda et al ., ). Furthermore, in Lycopersicon esculentum it has been shown that ALOG proteins are able to interact with NBCL proteins (Xu et al ., ). Thus, in L. japonicus , boundary zone patterning and regulation might be carried out through a similar CUC/ALOG/NBCL module in which LjNBCL1 plays a major role.…”

Contribution of CaBPM4, a BTB Domain–Containing Gene, to the Response of Pepper to Phytophthora capsici Infection and Abiotic Stresses

“…In Arabidopsis, AtBPMs were expressed at a significantly higher level in floral buds and open flowers, and BPM-silenced plants exhibited altered flower development [17]. In tomato, SlBOPs (Solanum lycopersicum BLADE-ON-PETIOLE), which are BTB transcriptional regulators, can interact with the transcription factor TERMINATING FLOWER (TMF) to control inflorescence architecture [50]. This suggests that BTB-containing proteins may participate in flower development processes.…”