The dominant and poorly penetrant phenotypes of maize unstable factor for orange1 are caused by DNA methylation changes at a linked transposon

Authors: WITTMEYER, KAMERON - Pennsylvania State University; CUI, JIN - Pennsylvania State University; CHATERJEE, DEBAMALYA - Pennsylvania State University; LEE, TZUU-FEN - Danforth Plant Science Center; TAN, QIXIAN - Pennsylvania State University; JIAO, YINPING - Cold Spring Harbor Laboratory; WANG, POHAO - Pennsylvania State University; GAFFOORA, IFFA - Pennsylvania State University; Ware, Doreen; MEYERS, BLAKE - Danforth Plant Science Center; CHOPRA, SURINDER - Pennsylvania State University

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/11/2018
Publication Date: 12/1/2018
Citation: Wittmeyer, K., Cui, J., Chaterjee, D., Lee, T., Tan, Q., Jiao, Y., Wang, P., Gaffoora, I., Ware, D., Meyers, B., Chopra, S. 2018. The dominant and poorly penetrant phenotypes of maize unstable factor for orange1 are caused by DNA methylation changes at a linked transposon. The Plant Cell. https://doi.org/10.1105/tpc.18.00546.
DOI: https://doi.org/10.1105/tpc.18.00546

Interpretive Summary: Originally, Ufo1-1 was identified for the loss of tissue-specific expression of the P1-wr gene. Here we describe the widespread gene expression changes associated with Ufo1-1 and identify an elevated stress response in Ufo1-1 plants that likely explains many of the pleiotropic defects associated with the mutation. We also put forth a model in which p1 expression is induced as a result of this constitutive stress in Ufo1-1 plants. The identification of both the causal gene and the molecular mechanism of ‘unstable’ Ufo1 solves one puzzle of this classical maize mutant, but has also opened several more.

Technical Abstract: The maize mutant Unstable factor for orange1 (Ufo1) has been implicated in the epigenetic modifications of the MYB transcription factor pericarp color1 (p1), which regulates the production of phlobaphenes. Here we show that the ufo1 gene maps to a genetically recalcitrant region near the centromere on chromosome 10 which is historically resistant to recombination in 13 inbred lines. Transcriptional analysis of the Ufo1-1 mutant allele and wild type plants identified a candidate gene using a k-mer based approach. The candidate gene, GRMZM2G053177, found in the mapping region is overexpressed by > 45-fold in multiple tissues. Ectopic expression of this gene also explains the dominance of Ufo1-1 and its phenotypes. We found that GRMZM2G053177 has a unique transcript in the mutant stock and this transcript originates from within a CACTA transposon inserted within the first intron of the gene. Regulation of expression of GRMZM2G053177 by the DNA methylation status of the CACTA transposon also explains the incomplete penetrance and poor expressivity of Ufo1-1. Transgenic overexpression lines of GRMZM2G053177 were able to phenocopy the p1 induced pigment production in coleoptile, tassel, leaf sheath, husk, pericarp, and cob glumes. Finally, we find that altered expression of carbohydrate metabolic genes translates into elevated levels of soluble sugars in leaves and light-induced lesions found in mature Ufo1-1 leaves. In this study we have thus uncovered the mystery of Ufo1 that has been unsolved for over ~40 years.