Allelic diversity of NAC18.1 is a major determinant of fruit firmness and harvest date in apple (Malus domestica)

AbstractSoftening 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 ripening and associated textural changes 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, 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 NAC18.1 to three other ripening-related markers currently used by breeders (ACS1, ACO1, and PG1), and found that the effect of the NAC18.1 genotype on both traits greatly exceeded that observed for the other markers. By sequencing NAC18.1 across 18 accessions, we revealed two predominant haplotypes containing the 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 with high similarity to the NON-RIPENING (NOR) transcription factor, an early regulator of ripening in tomato (Solanum lycopersicum). To test whether these genes are functionally orthologous, we introduced NAC18.1 transgenes 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 underlie substantial variation in apple firmness and harvest time through modulation of a conserved ripening program.HighlightNAC18.1 is a member of a family of conserved transcriptional regulators of ripening that underlies variation in fruit firmness and harvest date in diverse apple accessions.

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Apple Ripening Is Controlled by a NAC Transcription Factor

Frontiers in Genetics ◽

10.3389/fgene.2021.671300 ◽

2021 ◽

Vol 12 ◽

Author(s):

Zoë Migicovsky ◽

Trevor H. Yeats ◽

Sophie Watts ◽

Jun Song ◽

Charles F. Forney ◽

...

Keyword(s):

Transcription Factor ◽

Association Studies ◽

Genome Wide Association Studies ◽

Nucleotide Polymorphism ◽

Transcription Factor Gene ◽

Single Nucleotide ◽

Promoter Sequences ◽

Genome Wide ◽

Apple Ripening ◽

Textural Changes

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.

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Hybrid allele-specific ChIP-Seq analysis links variation in transcription factor binding to traits in maize

10.21203/rs.3.rs-543958/v1 ◽

2021 ◽

Author(s):

Thomas Hartwig ◽

Michael Banf ◽

Gisele Prietsch ◽

Julia Engelhorn ◽

Jinliang Yang ◽

...

Keyword(s):

Transcription Factor ◽

Target Genes ◽

Phenotypic Diversity ◽

Association Studies ◽

Chromatin Accessibility ◽

Genome Wide Association Studies ◽

Functional Variants ◽

Genome Wide ◽

Allele Specific ◽

Hybrid Allele

Abstract Variation in transcriptional regulation is a major cause of phenotypic diversity. Genome-wide association studies (GWAS) have shown that most functional variants reside in non-coding regions, where they potentially affect transcription factor (TF) binding and chromatin accessibility to alter gene expression. Pinpointing such regulatory variations, however, remains challenging. Here, we developed a hybrid allele-specific chromatin binding sequencing (HASCh-seq) approach and identified variations in target binding of the brassinosteroid (BR) responsive transcription factor ZmBZR1 in maize. Chromatin immunoprecipitation followed by sequencing (ChIP-seq) in B73xMo17 F1s identified thousands of target genes of ZmBZR1. Allele-specific ZmBZR1 binding (ASB) was observed for about 14.3% of target genes. It correlated with over 550 loci containing sequence variation in BZR1-binding motifs and over 340 loci with haplotype-specific DNA methylation, linking genetic and epigenetic variations to ZmBZR1 occupancy. Comparison with GWAS data linked hundreds of ASB loci to important yield, growth, and disease-related traits. Our study provides a robust method for analyzing genome-wide variations of transcription factor occupancy and identified genetic and epigenetic variations of the BR response transcription network in maize.

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Predicting the effects of SNPs on transcription factor binding affinity

Bioinformatics ◽

10.1093/bioinformatics/btz612 ◽

2019 ◽

Author(s):

Sierra S Nishizaki ◽

Natalie Ng ◽

Shengcheng Dong ◽

Robert S Porter ◽

Cody Morterud ◽

...

Keyword(s):

Transcription Factor ◽

Binding Affinity ◽

Association Studies ◽

Transcription Factor Binding ◽

Supplementary Information ◽

Genome Wide Association Studies ◽

Nucleotide Polymorphisms ◽

Single Nucleotide ◽

Factor Binding ◽

Genome Wide

Abstract Motivation Genome-wide association studies have revealed that 88% of disease-associated single-nucleotide polymorphisms (SNPs) reside in noncoding regions. However, noncoding SNPs remain understudied, partly because they are challenging to prioritize for experimental validation. To address this deficiency, we developed the SNP effect matrix pipeline (SEMpl). Results SEMpl estimates transcription factor-binding affinity by observing differences in chromatin immunoprecipitation followed by deep sequencing signal intensity for SNPs within functional transcription factor-binding sites (TFBSs) genome-wide. By cataloging the effects of every possible mutation within the TFBS motif, SEMpl can predict the consequences of SNPs to transcription factor binding. This knowledge can be used to identify potential disease-causing regulatory loci. Availability and implementation SEMpl is available from https://github.com/Boyle-Lab/SEM_CPP. Supplementary information Supplementary data are available at Bioinformatics online.

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Genome‐Wide Association Studies in Apple Reveal Loci for Aroma Volatiles, Sugar Composition, and Harvest Date

The Plant Genome ◽

10.3835/plantgenome2018.12.0104 ◽

2019 ◽

Vol 12 (2) ◽

pp. 180104 ◽

Cited By ~ 9

Author(s):

Bjarne Larsen ◽

Zoë Migicovsky ◽

Anne Aae Jeppesen ◽

Kyle M. Gardner ◽

Torben Bo Toldam‐Andersen ◽

...

Keyword(s):

Association Studies ◽

Harvest Date ◽

Genome Wide Association ◽

Genome Wide Association Studies ◽

Sugar Composition ◽

Aroma Volatiles ◽

Genome Wide

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Chromosome-level genome assemblies of five Prunus species and genome-wide association studies for key agronomic traits in peach

Horticulture Research ◽

10.1038/s41438-021-00648-2 ◽

2021 ◽

Vol 8 (1) ◽

Author(s):

Qiuping Tan ◽

Sen Li ◽

Yuzheng Zhang ◽

Min Chen ◽

Binbin Wen ◽

...

Keyword(s):

Transcription Factor ◽

Prunus Persica ◽

Association Studies ◽

Fruit Shape ◽

Nac Transcription Factor ◽

Genome Wide Association ◽

Genome Wide Association Studies ◽

Structural Variant ◽

Genome Wide ◽

Genome Assemblies

AbstractPrunus species include many important perennial fruit crops, such as peach, plum, apricot, and related wild species. Here, we report de novo genome assemblies for five species, including the cultivated species peach (Prunus persica), plum (Prunus salicina), and apricot (Prunus armeniaca), and the wild peach species Tibetan peach (Prunus mira) and Chinese wild peach (Prunus davidiana). The genomes ranged from 240 to 276 Mb in size, with contig N50 values of 2.27−8.30 Mb and 25,333−27,826 protein-coding gene models. As the phylogenetic tree shows, plum diverged from its common ancestor with peach, wild peach species, and apricot ~7 million years ago (MYA). We analyzed whole-genome resequencing data of 417 peach accessions, called 3,749,618 high-quality SNPs, 577,154 small indels, 31,800 deletions, duplications, and inversions, and 32,338 insertions, and performed a structural variant-based genome-wide association study (GWAS) of key agricultural traits. From our GWAS data, we identified a locus associated with a fruit shape corresponding to the OVATE transcription factor, where a large inversion event correlates with higher OVATE expression in flat-shaped accessions. Furthermore, a GWAS revealed a NAC transcription factor associated with fruit developmental timing that is linked to a tandem repeat variant and elevated NAC expression in early-ripening accessions. We also identified a locus encoding microRNA172d, where insertion of a transposable element into its promoter was found in double-flower accessions. Thus, our efforts have suggested roles for OVATE, a NAC transcription factor, and microRNA172d in fruit shape, fruit development period, and floral morphology, respectively, that can be connected to traits in other crops, thereby demonstrating the importance of parallel evolution in the diversification of several commercially important domesticated species. In general, these genomic resources will facilitate functional genomics, evolutionary research, and agronomic improvement of these five and other Prunus species. We believe that structural variant-based GWASs can also be used in other plants, animal species, and humans and be combined with deep sequencing GWASs to precisely identify candidate genes and genetic architecture components.

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Multi-species, multi-transcription factor binding highlights conserved control of tissue-specific biological pathways

eLife ◽

10.7554/elife.02626 ◽

2014 ◽

Vol 3 ◽

Cited By ~ 56

Author(s):

Benoit Ballester ◽

Alejandra Medina-Rivera ◽

Dominic Schmidt ◽

Mar Gonzàlez-Porta ◽

Matthew Carlucci ◽

...

Keyword(s):

Transcription Factor ◽

Association Studies ◽

Specific Gene ◽

Genome Wide Association Studies ◽

Tissue Specific ◽

Genome Wide ◽

Multiple Species ◽

Lipid Metabolism Genes ◽

Genomic Regions ◽

Regulatory Dna

As exome sequencing gives way to genome sequencing, the need to interpret the function of regulatory DNA becomes increasingly important. To test whether evolutionary conservation of cis-regulatory modules (CRMs) gives insight into human gene regulation, we determined transcription factor (TF) binding locations of four liver-essential TFs in liver tissue from human, macaque, mouse, rat, and dog. Approximately, two thirds of the TF-bound regions fell into CRMs. Less than half of the human CRMs were found as a CRM in the orthologous region of a second species. Shared CRMs were associated with liver pathways and disease loci identified by genome-wide association studies. Recurrent rare human disease causing mutations at the promoters of several blood coagulation and lipid metabolism genes were also identified within CRMs shared in multiple species. This suggests that multi-species analyses of experimentally determined combinatorial TF binding will help identify genomic regions critical for tissue-specific gene control.

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