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Transcriptional repression in multicellular organisms orchestrates dynamic and precise gene expression changes that enable complex developmental patterns. Here, we present phenotypic and molecular characterization of the maize ( Zea mays ) transcriptional corepressor RAMOSA1 ENHANCER LOCUS2 (REL2), a unique member of the highly conserved TOPLESS (TPL) family. Analysis of single recessive mutations in rel2 revealed an array of vegetative and reproductive phenotypes, many related to defects in meristem initiation and maintenance. To better understand how REL2-mediated transcriptional complexes relate to rel2 phenotypes, we performed protein interaction assays and transcriptional profiling of mutant inflorescences, leading to the identification of different maize transcription factors and regulatory pathways that employ REL2 repression to control traits directly impacting maize yields. In addition, we used our REL2 interaction data to catalog conserved repression motifs present on REL2 interactors and showed that two of these, RLFGV- and DLN-type motifs, interact with the C-terminal WD40 domain of REL2 rather than the N terminus, which is known to bind LxLxL EAR motifs. These findings establish that the WD40 domain of TPL family proteins is an independent protein interaction surface that may work together with the N-terminal domain to allow the formation of large macromolecular complexes of functionally related transcription factors., (© 2019 American Society of Plant Biologists. All Rights Reserved.)

In a previous study aimed at identifying regulators of Nicotiana attenuata responses against chewing insects, a 26-nucleotide tag matching the HSPRO (ORTHOLOG OF SUGAR BEET Hs1(pro)(-)(1)) gene was found to be strongly induced after simulated herbivory (Gilardoni et al., 2010). Here we characterized the function of HSPRO during biotic interactions in transgenic N. attenuata plants silenced in its expression (ir-hspro). In wild-type plants, HSPRO expression was not only induced during simulated herbivory but also when leaves were inoculated with Pseudomonas syringae pv tomato DC3000 and roots with the growth-promoting fungus Piriformospora indica. Reduced HSPRO expression did not affect the regulation of direct defenses against Manduca sexta herbivory or P. syringae pv tomato DC3000 infection rates. However, reduced HSPRO expression positively influenced early seedling growth during interaction with P. indica; fungus-colonized ir-hspro seedlings increased their fresh biomass by 30% compared with the wild type. Grafting experiments demonstrated that reduced HSPRO expression in roots was sufficient to induce differential growth promotion in both roots and shoots. This effect was accompanied by changes in the expression of 417 genes in colonized roots, most of which were metabolic genes. The lack of major differences in the metabolic profiles of ir-hspro and wild-type colonized roots (as analyzed by liquid chromatography time-of-flight mass spectrometry) suggested that accelerated metabolic rates were involved. We conclude that HSPRO participates in a whole-plant change in growth physiology when seedlings interact with P. indica.