Variation in leaf transcriptome responses to elevated ozone corresponds with physiological sensitivity to ozone across maize inbred lines

Authors: NANNI, ADALENA - University Of Florida; MORSE, ALISON - University Of Florida; NEWMAN, JEREMY - University Of Florida; CHOQUETTE, NICOLE - University Of Illinois; WEDOW, JESSICA - University Of Illinois; LIU, ZIHAO - University Of Florida; LEAKEY, ANDREW D B - University Of Illinois; CONESA, ANA - University Of Florida; Ainsworth, Elizabeth - Lisa; MCINTYRE, LAUREN - University Of Florida

Submitted to: Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/27/2022
Publication Date: 5/17/2022
Citation: Nanni, A., Morse, A., Newman, J., Choquette, N., Wedow, J., Liu, Z., Leakey, A.D.B,, Conesa, A., Ainsworth, E.A., McIntyre, L.M. 2022. Variation in leaf transcriptome responses to elevated ozone corresponds with physiological sensitivity to ozone across maize inbred lines. Genetics. Article iyac080. https://doi.org/10.1093/genetics/iyac080.
DOI: https://doi.org/10.1093/genetics/iyac080

Interpretive Summary: Ozone is damaging air pollutant that contributes to global climate change and decreases crop yields. This study investigated whether variation in the response to ozone of different maize inbreds was caused by variation in gene content within the diverse genomes or to variation in the expression of genes. Five inbred lines representing some of the diversity within maize were studied. We sequenced the transcriptomes of the five lines and found that the expressed genes were part of a shared genome, with nearly 95% of genes from co-localized locations in the genome. Investigation of the expression of genes uncovered significant differences in the transcriptional response to ozone. Inbred line B73 was tolerant to ozone and showed a limited transcriptional response. In contrast, more than 3000 genes were significantly differentially expressed in the line NC338. The results of the study showed that differences in response to ozone among inbred lines are likely associated with regulation of gene expression and not divergence in gene content.

Technical Abstract: We examine the impact of sustained elevated ozone concentration on the leaf transcriptome of 5 diverse maize inbred genotypes, which vary in physiological sensitivity to ozone (B73, Mo17, Hp301, C123, and NC338), using long reads to assemble transcripts and short reads to quantify expression of these transcripts. More than 99% of the long reads, 99% of the assembled transcripts, and 97% of the short reads map to both B73 and Mo17 reference genomes. Approximately 95% of the genes with assembled transcripts belong to known B73–Mo17 syntenic loci and 94% of genes with assembled transcripts are present in all temperate lines in the nested association mapping pan-genome. While there is limited evidence for alternative splicing in response to ozone stress, there is a difference in the magnitude of differential expression among the 5 genotypes. The transcriptional response to sustained ozone stress in the ozone resistant B73 genotype (151 genes) was modest, while more than 3,300 genes were significantly differentially expressed in the more sensitive NC338 genotype. There is the potential for tandem duplication in 30% of genes with assembled transcripts, but there is no obvious association between potential tandem duplication and differential expression. Genes with a common response across the 5 genotypes (83 genes) were associated with photosynthesis, in particular photosystem I. The functional annotation of genes not differentially expressed in B73 but responsive in the other 4 genotypes (789) identifies reactive oxygen species. This suggests that B73 has a different response to long-term ozone exposure than the other 4 genotypes. The relative magnitude of the genotypic response to ozone, and the enrichment analyses are consistent regardless of whether aligning short reads to: long read assembled transcripts; the B73 reference; the Mo17 reference. We find that prolonged ozone exposure directly impacts the photosynthetic machinery of the leaf.