NODULIN HOMEOBOX is required for heterochromatin homeostasis in Arabidopsis

Zsolt Karányi, Ágnes Mosolygó-L, Orsolya Feró, Adrienn Horváth, Beáta Boros-Oláh, Éva Nagy, Szabolcs Hetey, Imre Holb, Henrik Mihály Szaker, Márton Miskei, Tibor Csorba () and Lóránt Székvölgyi ()
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Zsolt Karányi: University of Debrecen
Ágnes Mosolygó-L: University of Debrecen
Orsolya Feró: University of Debrecen
Adrienn Horváth: University of Debrecen
Beáta Boros-Oláh: University of Debrecen
Éva Nagy: University of Debrecen
Szabolcs Hetey: University of Debrecen
Imre Holb: University of Debrecen
Henrik Mihály Szaker: MATE University, Genetics and Biotechnology Institute
Márton Miskei: University of Debrecen
Tibor Csorba: MATE University, Genetics and Biotechnology Institute
Lóránt Székvölgyi: University of Debrecen

Nature Communications, 2022, vol. 13, issue 1, 1-20

Abstract: Abstract Arabidopsis NODULIN HOMEOBOX (NDX) is a nuclear protein described as a regulator of specific euchromatic genes within transcriptionally active chromosome arms. Here we show that NDX is primarily a heterochromatin regulator that functions in pericentromeric regions to control siRNA production and non-CG methylation. Most NDX binding sites coincide with pericentromeric het-siRNA loci that mediate transposon silencing, and are antagonistic with R-loop structures that are prevalent in euchromatic chromosomal arms. Inactivation of NDX leads to differential siRNA accumulation and DNA methylation, of which CHH/CHG hypomethylation colocalizes with NDX binding sites. Hi-C analysis shows significant chromatin structural changes in the ndx mutant, with decreased intrachromosomal interactions at pericentromeres where NDX is enriched in wild-type plants, and increased interchromosomal contacts between KNOT-forming regions, similar to those observed in DNA methylation mutants. We conclude that NDX is a key regulator of heterochromatin that is functionally coupled to het-siRNA loci and non-CG DNA methylation pathways.

Date: 2022
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DOI: 10.1038/s41467-022-32709-y

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