Mutations in a Zea mays alanyl-tRNA synthetase condition an albino phenotype and suggest retrograde signaling affects replication-dependent histone transcription.

We isolated a nuclear recessive, seedling-lethal albino mutant manifesting yellowish-white plantlets. Employing bulk-segregant analysis and whole-genome re-sequencing, we examined 89 homozygous mutant individuals and 205 wild-type relatives from B73 backcrossed pedigrees. We called de novo SNPs and indel variants using Genome Analysis ToolKit. Using QTLseqr BSA software, we fine mapped the alb-605F mutant locus to end of short arm of Chr. 9 within an interval of ~ 10 Mbp. The causal gene Alanyl-tRNA synthetase , predicted to localize to chloroplasts but not mitochondria, was fine-mapped by flanking indel PCR markers and validated by failure to complement the albino phenotype in progeny of test cross with a heterozygous Mutator transposon reverse-genetics allele which also segregated albino progeny when selfed. Both homozygous mutant allele ZmAlaRS plants showed reduction of chloroplast ribosomal rRNAs but were variably leaky for mature plastid rRNA accumulation associated with variable greenhouse and growth chamber environments. A two-nucleotide frameshift deletion and/or retrotransposon insertion discovered in the alb-605F mutant haplotype altered transcript variant abundances versus control sibling samples assayed by BSA RNAseq. Relative genomic DNA read abundances mapping to the organellar genomes were significantly higher in alb-605F mutants compared to wild-type, interpreted as evidence of retrograde signaling processes associated with stalled leaf development. Analysis of Gene Ontology bins showed significant impact of the alb-605F mutation on transcripts associated with retrograde signals from chlorophyll-mediated oxidative stress and/or mitochondrial and nuclear genetic compartments. We identified a novel target of organelle retrograde signaling: replication-dependent histones.