Disruption of NAP1 genes supresses the fas1 mutant phenotype and enhances genome stability

Abstract

Histone chaperones mediate assembly and disassembly of nucleosomes and participate in essentially all DNA-dependent cellular processes. In Arabidopsis thaliana, loss-of-functions of FAS1 or FAS2 subunits of the H3-H4 histone chaperone complex CHROMATIN ASSEMBLY FACTOR 1(CAF-1) has a dramatic effect on plant morphology, growth and overall fitness. Altered chromatin compaction, systematic loss of repetitive elements or increased DNA damage clearly demonstrate the severity of CAF-1 dysfunction. How histone chaperone molecular networks change without a functional CAF-1 remains elusive. Here we present an intriguing observation that disruption of the H2A-H2B histone chaperone NUCLEOSOME ASSEMBLY PROTEIN 1 (NAP1) supresses FAS1 loss-of function. The quadruple mutant fas1nap1;1-3 shows wild-type growth and decreased sensitivity to genotoxic stress. Chromatin of fas1nap1;1-3 plants is less accessible to micrococcal nuclease and progressive loss of telomeres and 45S rDNA is supressed. Interestingly, the strong genetic interaction between FAS1 and NAP1 does not occur via direct protein-protein interaction. We propose that NAP1;1-3 play an essential role in nucleosome assembly in fas1, thus their disruption abolishes fas1 defects. Our data altogether reveal a novel function of NAP1 proteins, unmasked by CAF-1 dysfunction. It emphasizes the importance of a balanced composition of chromatin and shed light on the histone chaperone molecular network.