Molecular mechanisms in the developmental regulation of the maize Suppressor-mutator transposable element.

Abstract

The maize Suppressor-mutator (Spm) element can exist in one of three heritable forms: (1) a stably active form, (2) a stably inactive form, termed cryptic, and (3) a labile form, here termed programmable, in which the element exhibits one of a variety of heritable developmental programs of expression. Active elements are transcribed and are hypomethylated at sites upstream of the transcription start site, whereas inactive elements are transcriptionally silent and largely methylated at the upstream sites. Active (both stable and programmable), inactive programmable, and cryptic elements are unmethylated, partially methylated, and fully methylated, respectively, at sites within an 0.35-kb 80% G + C region just downstream from the transcription start site. An active Spin element in a genome with a cryptic element promotes its partial demethylation but not its transcriptional activation. In contrast, a trans-acting Spin promotes extensive demethylation and transcriptional activation of an inactive programmable element, as well as its heritable reactivation. These observations define the molecular components of the Spin element's developmental regulatory mechanism. We discuss their general relevance to the developmental regulation of gene expression.[ 1957, 1958, 1959, 1965aPeterson 1966;Fowler and Peterson 1978). These include the cryptic form, in which the element is genetically silent. Both McClintock and Peterson also identified elements that were capable of undergoing reversible transitions between the active and inactive phases in a characteristic and heritable pattern during development (McClintock 1957(McClintock , 1958(McClintock , 1962(McClintock , 1965a(McClintock , b, 1971Peterson 1966;Fowler and Peterson 1978). We showed recently that the genetic mechanism responsible for the developmental control of Spin expression has two components, which we designated the phase setting and the phase program (Fedoroff and Banks 1988). The phase setting determines whether the element is genetically active or inactive. The phase program determines the heritability of the phase setting, as well as when, where, and how frequently it will be reversed during plant development. The underlying genetic mechanism is heritable, reversible, and capable of promoting the incremental transition of the element from a stably active to a stably inactive (cryptic) form, implying the involvement of multiple epigenetic events (Fedoroff and Banks 1988). In view of the accumulating evidence that the inactivation of gene expression, in general (for reviews, see Razin et al. 1984;Adams and Burdon 1985;Holliday 1987;Cedar 1988), and maize transposable elements, in particular Bennetzen 1985;Chandler and Walbot 1986;Schwartz and Dennis 1986;Chomet et al. 1987; Fedoroff et al. 1988a, b)

Epigenetic Transcriptional Silencing and 5-Azacytidine-Mediated Reactivation of a Complex Transgene in Rice

“…7B). Studies on the developmental regulation of the maize Suppressor-mutator (Spm) transposable element revealed that its phase setting is determined by the methylation of sequences 5' of the transcription start site, whereas the developmental program is determined by the methylation pattern within the 80% GC-rich sequence of its first untranslated exon (Banks et al, 1988). However, to our knowledge, methylation of the 5' untranslated region in a silenced transgene locus has not been reported previously in plants.…”

“…Gene silencing is a concern for biotechnological applications, in which reliable expression of an introduced gene is essential for maintenance of the desired trait(s) (Meyer, 1995 (Banks et al, 1988;Fedoroff, 1989) and paramutation in maize (Brink, 1973;Martienssen, 1996;Matzke et al, 1996). By providing data concerning methylation of the introduced sequences, our study not only adds transgenes to this category but also suggests the existence of common mechanisms for instigating methylation.…”

“…Methylation has been implicated as a component of a dynamic developmental regulatory system responsible for the change of state and transcriptional repression of maize transposable elements (Banks et al, 1988;Fedoroff, 1989). It has also been associated with paramutation (a natural example of trans-inactivation; Brink, 1973;Martienssen, 1996;Matzke et al, 1996) in maize.…”

Analysis of DNA methylation of perennial ryegrass under drought using the methylation-sensitive amplification polymorphism (MSAP) technique

“…DNA methylation is a key event associated with transposon activity, suggesting that DNA methylation is an important factor in the evolution and adaptation of plants (Saze et al 2012). Transposons have reportedly shown changes in methylation status during plant development and adverse stresses (Banks et al 1988;Slotkin et al 2009;Li et al 2010). The methylation/demethylation of transposons can affect programmed genome epigenetic regulation and the expressions of downstream genes in plants, which can be altered by environmental stresses (Yaish 2013;Cokus et al 2008;Hashida et al 2003Hashida et al , 2006.…”

The Birth of a Black Rice Gene and Its Local Spread by Introgression

“…Epialleles have been reported in several plant species, including maize (Brink, 1956;Banks et al, 1988;Das and Messing, 1994;Hollick and Chandler, 2001) and rice (Miura et al, 2009(Miura et al, , 2010Wang et al, 2010;Zhang et al, 2012;Li et al, 2014). The phenotypes of these epialleles are affected by DNA methylation status and/or histone modification resulting in the alteration of gene expression.…”