Abstract
Softening is a hallmark of ripening in fleshy fruits, and has both desirable and undesirable implications for texture and postharvest stability. Accordingly, the timing and extent of pre-harvest ripening and associated textural changes following harvest are key targets for improving fruit quality through breeding. Previously, we identified a large effect locus associated with harvest date and firmness in apple (Malus domestica) using genome-wide association studies (GWAS). Here, we present additional evidence that polymorphisms in or around a transcription factor gene, NAC18.1, may cause variation in these traits. First, we confirmed our previous findings with new phenotype and genotype data from ∼800 apple accessions. In this population, we compared a genetic marker within NAC18.1 to markers targeting three other firmness-related genes currently used by breeders (ACS1, ACO1, and PG1), and found that the NAC18.1 marker was the strongest predictor of both firmness at harvest and firmness after 3 months of cold storage. By sequencing NAC18.1 across 18 accessions, we revealed two predominant haplotypes containing the single nucleotide polymorphism (SNP) previously identified using GWAS, as well as dozens of additional SNPs and indels in both the coding and promoter sequences. NAC18.1 encodes a protein that is orthogolous to the NON-RIPENING (NOR) transcription factor, a regulator of ripening in tomato (Solanum lycopersicum). We introduced both NAC18.1 transgene haplotypes into the tomato nor mutant and showed that both haplotypes complement the nor ripening deficiency. Taken together, these results indicate that polymorphisms in NAC18.1 may underlie substantial variation in apple firmness through modulation of a conserved ripening program.
Highlights
Despite their diverse structure, ontogeny, and biochemical composition, fleshy fruits from a taxonomically broad range of species undergo coordinated ripening processes that have many features in common
Fruit were harvested over a 65 day period and their firmness at harvest (N = 859) and after 3 months of cold storage (N = 535) was found to differ by 7-fold across the apple accessions from the Apple Biodiversity Collection (ABC)
Our results suggest that the markers in AMINOCYCLOPROPANE-1-CARBOXYLATE OXIDASE 1 (ACO1) and AMINOCYCLOPROPANE1-CARBOXYLATE SYNTHASE 1 (ACS1) have little to no predictive power for firmness-related traits across diverse apple germplasm (Figure 1; Supplementary Figure 2)
Summary
Ontogeny, and biochemical composition, fleshy fruits from a taxonomically broad range of species undergo coordinated ripening processes that have many features in common. Processes involved in ripening are regulated by conserved and convergently evolved networks of transcription factors and hormones, such as ethylene in climacteric fruit where a respiratory burst occurs at the beginning of ripening (Lü et al, 2018). While all NAC genes share a conserved DNA-binding (NAC) domain, specific functional clades are defined in terms of their more variable domains, the C-terminal transcriptional regulatory region. These domains can act directly as transcriptional activators, or can facilitate interaction with other transcription factors in order to fine-tune transcriptional control. NAC transcription factors have been implicated in ripening phenotypes in diverse species including tomato (Kumar et al, 2018), melon (Ríos et al, 2017), banana (Shan et al, 2012), peach (Pirona et al, 2013), and apricot (García-Gómez et al, 2019)
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