Histone variants and high mobility group non‐histone chromosomal proteins of higher plants: Their potential for forming a chromatin structure that is either poised for transcription or transcriptionally inert

Abstract

In order for the genes of higher plants to be transcribed, they must be in a transcriptionally poised chromatin structure – a structure that allows access of RNA polymerases and transcription factors to the DNA. The structural features of transcriptionally poised chromatin and what distinguishes it from transcriptionally incrt chromatin are as yet unknown. There are, however, two groups of proteins that have been implicated as determinants of such divergent chromatin structures – the high mobility group (HMG) non‐histone chromatin proteins and histone variants. In this paper I discuss what is known of these two groups of proteins in higher plants against the background of their suspected roles in chromatin structure in animal systems. Plants have a number of histone variants (particularly of the H2A and H2B histones) which have the potential to be the basis of nucleosome heterogeneity in divergent chromatin structures. There is a large body of evidence from animal systems suggesting that HMG proteins are structural proteins of transcriptionally poised chromatin. Plants have non‐histone chromosomal proteins that can be defined as HMG proteins based on operational criteria. That is, they are extracted from purified chromatin with 0.35 M NaCl, are soluble in 2% trichloroacetie acid and are very highly charged proteins with their charges being about evenly split between basic and acidic amino acid residues. Characterization of the plant HMG proteins by overall amino acid composition, peptide mapping, partial sequencing and immunological cross reactivity indicates that the plant HMG proteins are very different from their putative animal counterparts. Nevertheless, plant HMG proteins bind to monoucleosomes in the same manner as animal HMG proteins; they are released from chromatin by mild DNase I (EC 3.1.4.5) digestion under conditions that lead to preferential digestion of transcriptionally active sequences; and when chromatin is separated into fractions enriched or depleted in transcribed DNA sequences, the plant HMG proteins are found in the fraction enriched in transcribed sequences.

Plant chromosomal high mobility group (HMG) proteins

“…Pioneering work on plant HMG proteins was done by S. Spiker and co-workers who isolated and characterized the HMG proteins from wheat germ (reviewed by Spiker, 1988). Four major HMG proteins (HMGa-d), as in mammalian tissues (HMG1/2, HMG14/17), were identified in these studies, displaying a slightly higher mobility in SDS-PAGE than their animal counterparts (Spiker et al, 1978).…”

“…Further analysis of these proteins by amino acid analysis and peptide mapping revealed more dissimilarities than similarities to the animal proteins (Spiker, 1984). In addition, comparison of the immunological relationship between plant and animal HMG proteins (Spiker and Everett, 1987;Vanderbilt and Anderson, 1985) as well as amino-terminal peptide sequence analysis (Spiker, 1988) i nd icated su bsta ntial differences between the major plant and animal HMG proteins. Isolation and partial characterization of HMG proteins from other plants such as maize, barley, Arabidopsis thaliana and pea largely confirmed the results obtained from the wheat germ proteins (Grasser eta/., 1991;Moehs eta/., 1988;UII eta/., 1991;Vincentz and Gigot, 1985).…”

“…Furthermore, in contrast to wheat HMGa/b, HMGc/d displayed no specific binding to the naked A/l'-rich DNA probe in electrophoretic mobility shift assays (Pedersen et al, 1991). Amino-terminal peptide sequences of wheat HMGc and HMGd show no similarity to their putative animal counterparts (Spiker, 1988). The aminoterminal peptide sequence of the maize HMGc protein, however, is very similar to the wheat HMGc sequence (Grasser and Feix, unpublished).…”

Four differently chromatin‐associated maize HMG domain proteins modulate DNA structure and act as architectural elements in nucleoprotein complexes

“…Plant HMG proteins were first described in detail from wheat revealing significant differences to the animal proteins (Spiker, 1984(Spiker, , 1988. Unlike the vertebrate HMG1-like proteins which have two copies of the HMG domain, plant HMG1-like proteins (like invertebrate HMG1-like proteins) contain a single HMG domain.…”

Multiplicity of Histone H3 Variants in Wheat, Barley, Rice, and Maize

“…Genes for both histone H3 variants have been cloned (27). The existence of H3 variant genes and proteins has been suggested for other plants from a partial gene sequence in barley (6) and from protein gels of wheat (9), tobacco (1 1), and pea ( 1,16), although protein heterogeneity was not observed in other studies of wheat ( 18) and Arabidopsis thaliana ( 13). To date, multiple histone H3 clones have been isolated from wheat (19), maize (5), Arabidopsis (4), and rice (28), but all code for H3 proteins identical or virtually identical to the major H3.…”