Abstract
AbstractMitochondria produce signals besides energy and metabolites that influence plant growth and fitness. However, how mitochondrial signals are relayed to other cellular compartments is largely unknown. By applying poly(A)-site RNA-sequencing (PAS-seq) to wildtype Arabidopsis seedlings and a mutant in the histone demethylase JMJ30 treated with the mitochondrial electron transfer chain inhibitor antimycin A (AA), we identified a previously undefined mitochondrion-to-nucleus communication pathway by which mitochondrial functional state regulates co-transcriptionally alternative polyadenylation (APA) of nuclear mRNA. We observed a global shortening of 3′ untranslated regions (UTRs) as a molecular signature of AA-activated mitochondrial retrograde response (MRR), which contributed in part to translational regulation of auxin response and cell wall biogenesis. JMJ30 regulated AA-induced 3′ UTR shortening, resulting in more transcripts with shortened 3′ UTRs upon AA treatment in a JMJ30 gain-of-function mutant and overexpression lines. We also report on the JMJ30-interacting protein CPSF30, a cleavage and polyadenylation specificity factor that recruits JMJ30 to modulate H3K27me3 status at its target loci. Our study illustrates how epigenetic modification and APA coordinate mitochondrion-to-nucleus communication to allow cells to rapidly respond to changes in mitochondrial functional state and shape plant growth and fitness.One-sentence summaryEpigenetic modification and APA coordinate mitochondrion-to-nucleus communication to allow cells to rapidly respond to changes in mitochondrial functional state and shape plant growth and fitness.
Publisher
Cold Spring Harbor Laboratory