NODULIN HOMEOBOX is required for heterochromatin homeostasis in Arabidopsis

Karányi, Zsolt and Mosolygó-L, Ágnes and Feró, Orsolya and Horváth, Adrienn and Boros-Oláh, Beáta and Nagy, Éva and Hetey, Szabolcs and Holb, Imre and Szaker, Henrik Mihály and Miskei, Márton and Csorba, Tibor and Székvölgyi, Lóránt (2022) NODULIN HOMEOBOX is required for heterochromatin homeostasis in Arabidopsis. NATURE COMMUNICATIONS, 13 (1). ISSN 2041-1723

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Abstract

Arabidopsis NODULIN HOMEOBOX (NDX) is a nuclear protein described as a regulator of specific euchromatic genes within transcriptionally active chro- mosome arms. Here we show that NDX is primarily a heterochromatin reg- ulator that functions in pericentromeric regions to control siRNA production and non-CG methylation. Most NDX binding sites coincide with pericen- tromeric het-siRNA loci that mediate transposon silencing, and are antag- onistic 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 pericen- tromeres where NDX is enriched in wild-type plants, and increased inter- chromosomal contacts between KNOT-forming regions, similar to those observed in DNA methylation mutants. We conclude that NDX is a key reg- ulator of heterochromatin that is functionally coupled to het-siRNA loci and non-CG DNA methylation pathways.

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