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Article

Genome-Wide Association Study and Transcriptome Analysis Provide Candidate Genes for Agronomic Traits of Agaricus bisporus

by
Yuanping Lu
,
Zhongjie Guo
,
Binrong Ke
,
Huiqing Zheng
,
Zhiheng Zeng
,
Zhixin Cai
,
Hui Zeng
,
Jianhua Liao
* and
Meiyuan Chen
*
Institute of Edible Mushroom, Fujian Academy of Agricultural Sciences, Fuzhou 350012, China
*
Authors to whom correspondence should be addressed.
Horticulturae 2024, 10(7), 691; https://doi.org/10.3390/horticulturae10070691
Submission received: 6 March 2024 / Revised: 14 May 2024 / Accepted: 23 May 2024 / Published: 28 June 2024
(This article belongs to the Special Issue The Edible Mushroom Industry: A Vital Component in Horticultural Production)
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Abstract

:
Agaricus bisporus, belonging to the genus Agaricus and the family Agaricaceae, is a popular commercially cultivated mushroom with rich nutritional and medical values. Cultivation of A. bisporus requires superior cultivars. Understanding the differences between wild and cultivated accession at the genetic level is crucial for mining loci and genes associated with cultivation-related traits, informing future breeding directions. Additionally, the identification of loci and genes associated with important agronomic traits (e.g., yield and quality) facilitates mushroom molecular breeding. In this study, we conducted sequencing of 200 strains of A. bisporus and analyzed genomic variations. Population structure and genetic relationships were investigated for 200 strains. Selection signs and genes were also obtained after selection sweep analysis. Thirteen candidate genes in the selective elimination regions had significantly different expression patterns at the fruit body stage. Moreover, six genes were identified for the esterase isozyme type through a combination of GWAS and RNA data. This study provides insight into environmental adaptation at the genetic base, providing valuable genetic resources for button mushroom molecular breeding to improve environmental adaptation, quality, or yield.

1. Introduction

Mushrooms with high nutritional value, delicious flavors, desirable taste, and medicinal properties are viewed as delicacies and sources of therapeutic bioactive compounds [1,2,3]. Agaricus bisporus (J.E. Lange), popularly known as the button mushroom, is one of the most widely cultivated mushrooms worldwide [4,5]. They have been consumed as a healthy food for their low calorie and fat intake and abundant proteins, vitamins, carbohydrates, and dietary fibers [4]. Moreover, some active ingredients, such as lectins, polysaccharides, triterpenoids, peptides, and essential amino acids imbue this mushroom with anti-cancer, antihypertensive, antidiabetic, and antioxidant properties [4]. Cultivation of button mushrooms originating from France provides ample fruiting bodies for mankind and economic benefits [6].
Wild germplasms are valuable resources used as parents by mushroom breeders and widely domesticated as cultivars through artificial selection processes. However, due to insufficient knowledge about the genetic basis of most characteristics, wild species can create long breeding programs with uncertain outcomes [7].
Isozymes, first defined by Markert and Moller in 1959 [8], are widely used as genetic markers. The application of mark-assisted selection can help us select traits of interest early, accelerating the breeding program. Since 1985, isozyme electrophoresis has been successfully used to characterize and distinguish strains, identify hybrids, assess genonomy, and analyze the rules of genetic variation in A. bisporus [9]. Currently, esterase isozyme electrophoresis is the most frequently used isozyme electrophoresis in button mushrooms. According to the electrophoretic phenotypes of esterase isozymes, strains of A. bisporus were divided into four types, including type H (high productive strain), type G (good quality strain), type HG (high yield and good quality), and type S (infertile strain) [9,10]. Among these strains, type H, which has high yield and early fruiting advantages, and type G, which has quality fruiting body characteristics, such as a smooth and tight cap, and taste advantages, were selected as breeding materials. Type HG, due to its advantages of high yield and good quality strains, is the target of breeders and is often used as cultivars. In short, the ester isozyme phenotype represents yield and quality traits.
Genome-wide association studies (GWAS) have been successfully adopted to map loci or genes for diseases or important traits [11,12]. These associations facilitate the identification of novel drug targets or targeted genetic selection. Previous studies focused on some typical agronomic traits such as cap color, firmness, and earliness using QTL in button mushrooms [7,13,14]. However, GWAS has not been reported in A. bisporus for its association with the esterase isozyme phenotype. Additionally, the genetic basis of artificial selection, which is important for precise molecular breeding [12], is still unclear in button mushrooms.
To explore genetic control, we sequenced 200 widely collected wild and cultivated button mushroom strains from around the world and generated a large genome variation dataset. Genetic relationships and selection signs were investigated using this resource. The expression patterns of genes in the selection region were also studied at the fruit body stage. The selection signs and expression analysis allowed us to understand the genetic basis behind cultivation and environmental adaptation, providing a reference for breeding cultivated strains. We also identified loci and genes associated with esterase isozyme phenotypes through a combination of GWAS and RNA data, which can guide breeders in selecting parents for breeding programs. This study provides valuable genetic resources for button mushroom molecular breeding and investigates genetic relationships.

2. Materials and Methods

2.1. Strains and Phenotype Evaluation

A total of 200 A. bisporus strains collected from China and other countries preserved at the Fujian Academy of Agricultural Sciences were used in this study. These 200 strains were cultivated at a standard white button mushroom cultivation house [14] and grown on commercial compost provided by a firm producing button mushrooms (Jinming Food Co., Ltd., Zhangzhou, China). Fruiting bodies were harvested at the harvesting stage according to Chen et al. [15].
Esterase isozyme electrophoresis was conducted to investigate strain properties according to the methods used by Wang et al. [9]. According to esterase isozyme patterns [8,9], we classified the 200 strains into three types, including H type, G type, and HG type (Supplementary Table S1), based on the electrophoresis analysis of the esterase isozyme (Supplementary Figure S1).

2.2. Sequencing and Alignment

Genomic DNA from individuals was isolated from fruit bodies using the cetyltrimethylammonium bromide method (CTAB) [16]. The DNA library was constructed using the Truseq Nano DNA HT sample preparation kit according to the manufacturer’s instructions (Illumina, San Diego, CA, USA) and sequenced by Biomics Biotech (Beijing, China) on the Illumina HiSeqX platform. Afterward, 150 bp paired-end reads of the 200 strains were generated.
Prior to alignment, we filtered low-quality paired reads with the following traits: (i) reads containing ≥ 10% of unidentified nucleotides (Ns); (ii) reads with more than 50% of bases with a Phred quality value ≤ 10; (iii) reads with adapter contaminations (≥15 bp overlap between the adapter and reads). Subsequently, high-quality reads were obtained and aligned to the genome of A. bisporus (http://fungi.ensembl.org/, accessed on 22 May 2024) using BWA-MEM (0.7.10-r789) with default parameters [17]. SAMTools 1.3 was employed to generate Binary Alignment Map (BAM) format files [18] and Mark Duplicate from Picard tools (v1.102) was used to remove duplicate reads.

2.3. Variant Detection and Annotation

After alignment, SNP (Single Nucleotide Polymorphism) calling at a population level was carried out using GATK (version 3.6) [19]. To ensure the quality of variants, low-quality SNPs were filtered out with thresholds such as quality depth (QD) < 2, mapping quality (MQ) < 40, quality value < 30, and minor allele frequencies (MAF) < 0.05, as described in [20], and high-quality SNPs were retained for further investigation. Moreover, SNPs around Indels within 5 bp were filtered out.
SNP annotation was implemented using ANNOVAR [21]. We categorized SNPs into upstream regions (within 1 kb upstream of transcription start site), exonic regions (overlap with a coding exon), intronic regions (overlap with an intron), splicing sites (within 2 bp of a splicing junction), 5′ UTRs and 3′ UTRs, downstream regions (within 1 kb downstream of transcription end site), and intergenic regions. SNPs in coding exons were further annotated as synonymous (mutations did not cause amino acid changes), or nonsynonymous (mutations caused amino acid changes). Moreover, mutations causing stop gains and losses were also classified as nonsynonymous.

2.4. Phylogenetic Tree and Population Structure Analyses

To investigate the genetic relationship between 200 button mushroom strains, a neighbor-joining tree was constructed with PHYLIP 3.68 [22] based on a distance matrix and displayed using the ETE python package (v3.1.3) [23]. The population structure was examined using Admixture software (1.3.0) [24] and 2–10 assumed genetic clusters were identified using K. Principal component analysis (PCA) was implemented using the smartpca program from EIGENSOFT software (3.0) [25]. Linkage disequilibrium (LD) was calculated using Haploview software (4.2) [26] with default parameters. The coefficients (r2) between SNP in a 500 kb window was calculated and averaged across the whole genome.

2.5. Genome Scanning for Selective Elimination Analysis and Functional Enrichment Analysis

To identify selective elimination regions, VCFtools (0.1.14) [27] was adopted to calculate nucleotide diversity (π) and genetic differentiation (Fst) using a 40 kb sliding window with 5 kb steps across the whole genome. The top 5% of windows were chosen as candidate regions within which candidate genes were selected for further investigation. Functional annotation of the obtained candidate genes were implemented by BLAST against public databases including NR, Swiss-Prot, Gene Ontology (GO), and Kyoto Encyclopedia of Genes and Genomes (KEGG) databases [28].

2.6. Association Analyses

High-quality SNPs (MAF > 0.05) were used to perform GWAS on different traits. Association analyses were carried out using TASSEL 5.0 [29] and the compressed mixed linear model (y = Xɑ + Qβ + Kμ + e). The significant association threshold was set to 0.01/n (n, total number of SNP).

2.7. Expression Analyses

To understand the expression of candidate genes for selection signatures and association signals, the total RNA of 43 strains (Supplementary Table S1) was isolated using TriZol reagent; then, RNA sequences were conducted on the Illumina HiSeq platform by Biomics Biotech (Beijing, China). TopHat (v2.1.1) were used to align clean reads as well as reference. Gene expression was calculated with cuffquant and cuffnorm from Cufflinks software (2.2.1). Afterward, differential gene expression was analyzed using EBseq (1.12.0) with the cutoff threshold, fold change ≥ 2, and false discovery rate (FDR) < 0.01. The GOseq R package (2.12) [30] and KOBAS (2.0) [31] were adopted for GO and KEGG enrichment analyses, respectively.

3. Results

3.1. High-Quality Button Mushroom SNP

Through sequencing 200 strains, consisting of 94 wild germplasms and 106 cultivars, a total of 324 Gb of sequences with an average depth of ≥18× and a coverage of ≥92.33% for each strain were generated. In total, 166,644 high-quality SNP were obtained, 102,238 of which including 84,645 synonymous and 17,484 nonsynonymous were in coding regions.

3.2. Characterization of a Population and Linkage Disequilibrium

To investigate population characterization, construction of the phylogenetic tree (Figure 1A), principal component analysis (PCA) (Figure 1B), and population structure analysis (Figure 1C) was carried out among 200 accessions. The neighbor-joining phylogenetic tree and PCA results classified button mushroom strains into two major groups: In group Ⅰ (cultivated group), four cultivates from Japan, two from Australia, and one from the Philippines were grouped with cultivates from Europe or America, indicating that those seven cultivated relatives originated from Europe or America. Group Ⅱ included all wild lines and some cultivars from Europe. We further classified group Ⅱ into two subclades: Group Ⅱ-1 consisted of all wild relatives from China, a few cultivated accessions from Europe, and wild strains (white ARP lines, named mg79, mg85, mg377, and mg382) from America, indicating a close relationship between these white ARP strains and wild relatives from China. By contrast, there were relatively significant genetic differences between these strains and American brown ARP strains. Group Ⅱ-2 contained almost all wild accessions from America and a few cultivars from Europe. We interpreted the interspersing of cultivars in the wild group due to the domestication degree. When K = 2, the population structure (Figure 1C) generated patterns similar to PCA and the phylogenetic tree in which wild and cultivated accessions were divided into two groups.
According to the SNP data, sequence diversity (π) was calculated as 0.0021 for wild strains and 0.0013 for cultivars, suggesting that wild germplasms had higher genetic diversity than cultivars. The genetic differentiation statistic (Fst) between these two groups was estimated at 0.2079, suggesting moderate population differentiation, possibly resulting from artificial selection. Linkage disequilibrium (LD, indicated by r2) displayed a higher LD in cultivars than in wild germplasms (Figure 1D), suggesting that cultivated strains undergo strong artificial selection, whereas wild strains retain their abundant genetic diversity (Figure 1D).

3.3. Selection Signatures during Breeding and Expression Analysis of Candidate Genes

To identify selection signatures between wild and cultivated populations, we used the Fst and π methods. Using the upper 5% of the Fst and π intersection as the threshold value (Figure 2A,B), we identified 144 cultivated signals harboring 573 genes. Functional information about the identified genes was annotated after alignment with NR, Pfam, Swiss-Prot, and TrEMBL annotation databases. In total, 558 genes were annotated. Enrichment analysis classified the associated genes into two categories including biological processes and molecular functions (Figure 2C). The enriched GO terms were associated with O-methyltransferase activity, inorganic anion transmembrane transporter activity, hydrolase activity, phosphorus–oxygen lyase activity, G-protein beta/gamma-subunit complex binding, peptidase activity, antiporter activity, signal transducer activity, transmembrane transport, proteasome assembly, inorganic anion transport, cyclic nucleotide biosynthetic processes, methylation, regulation of transcription from RNA polymerase II promoter, and so on.
KEGG pathway (Figure 2C) analysis showed that the KEGG pathways were involved in ubiquitin-mediated proteolysis, sphingolipid metabolism, RNA transport, pyruvate metabolism, protein processing in the endoplasmic reticulum, phagosome, peroxisome, other glycan degradation, nucleotide excision repair, nitrogen metabolism, glyoxylate and dicarboxylate metabolism, fructose and mannose metabolism, endocytosis, citrate cycle (TCA cycle), biosynthesis of unsaturated fatty acids, arginine and proline metabolism, amino sugar and nucleotide sugar metabolism, aminoacyl-tRNA biosynthesis, alanine, aspartate and glutamate metabolism, and 2-Oxocarboxylic acid metabolism.
To understand the expression of candidate genes for selection signatures at the fruit body stage, 43 strains including 23 cultivars and 20 wild strains were selected randomly for RNA-seq data. A total of 13 differentially expressed genes (DEGs) were obtained from the cultivated signals. Of these, nine candidate genes were downregulated and four candidate genes were upregulated in the wild vs. cultivar strains comparison group (Table 1). The functional prediction of these genes is described in Table 1.

3.4. Identification of Candidate Genes for Esterase Isozyme Type by Integrating Genome-Wide Association Studies and RNA-Seq Analysis

Using a compressed mixed linear model, we conducted GWAS on 200 strains based on 166,644 SNPs. A total of 16 esterase isozyme type-related loci distributed at scaffolds 3, 6, 10, and 17 (Figure 3) were identified with a p-value of less than 6 × 10−8. Among these associated loci, 167 candidate genes were obtained with a cut-off of 0.01. Functional analysis of the identified genes showed that a total of 165 genes were identified after alignment with NR, Pfam, Swiss-Prot, and TrEMBL annotation databases.
Combined with the RNA-seq data of 43 strains (Supplementary Table S1), we obtained six differentially expressed genes associated with the esterase isozyme type. Comparing groups H and HG, the expression of these six genes was downmodulated (Table 2). In the H and G comparison groups, we only identified one down-regulated gene (AGABI2DRAFT_123388). By contrast, in the group G and HG groups, no DEG was identified. Functional predictions showed that AGABI2DRAFT_183745, AGABI2DRAFT_191000, and AGABI2DRAFT_151295 encoded 8-amino-7-oxononanoate synthase, high-affinity methionine permease, and calcium-independent phospholipase A2-gamma, respectively. Nevertheless, the other three genes were predicted to be hypothetical proteins. GO analysis showed that two of the six genes were enriched in three GO categories. The first type participated in biological processes including biosynthetic processes (GO:0009058), sulfur amino acid transport (GO:0000101), amino acid transmembrane transport (GO:0003333), and cation transport (GO:0006812). In terms of molecular function, the two genes were enriched in transferase activity (GO:0016740), pyridoxal phosphate binding (GO:0030170), and amino acid transmembrane transporter activity (GO:0015171). In terms of cellular components, AGABI2DRAFT_191000 was associated with the membrane (GO:0016020).

4. Discussion

Agaricus bisporus, regarded as a delicacy, is one of the most cultivated and consumed mushrooms. Cultivation of A. bisporus began in France during the 16th century [6], when a spawn of wild mushrooms was adopted. Wild A. bisporus strains usually produce small brown fruit bodies whose caps easily open. Large-scale cultivation of mushrooms, however, requires superior varieties. Breeders and cultivators consider superior varieties to have good agronomic and quality characteristics. Perfect cultivars have characteristics of high yield, firmness, round shape, long shelf life, disease-resistant ability, strong resistance, and high substrate adaptability. Generally, conventional breeding methods include tissue culture, single- and multi-spore cultures, and cross-breeding. Long-term domestication of wild germplasms may change their adaptive traits and transform wild mushrooms into cultivars suitable for artificial cultivation.
Investigation of genomic changes during the breeding process of mushrooms may contribute to the discovery of genes controlling cultivation-related traits. In this study, we resequenced 200 button mushroom strains, yielding 324 Gb of sequences with an average depth of ≥18× for each strain, which is higher than 4× the appropriate depth for GWAS as demonstrated by Reumers et al. [32]. In total, we obtained 166,644 high-quality SNPs from wild mushrooms and cultivars. All high-quality SNPs were adopted for further investigation. The results of genetic diversity and LD analysis demonstrated that wild mushrooms remained abundant in genetic diversity. The phylogenetic tree classified all wild strains into the wild group; however, some cultivars were also classified into the wild group, which may be due to different terms and degrees of domestication.
Domestication and breeding enable species to adapt to specific ecological environments and satisfy human demands. After prolonged artificial selection, alleles related to desirable traits show an increase in frequency and a decrease in nucleotide diversity [33,34]. Selective sweep analysis, the main method for detecting selection signatures, has been adopted to identify candidate genes in several species; for instance, genes controlling organic fruit acid metabolism and sugar content [35], genes involved in jujube fruit size [36], and freezing tolerance in peas [37]. Comparative assessment of genomes in cultivated and wild button mushrooms may help identify candidate domestication genes. In this study, 144 cultivated signals and 573 genes were identified in selective sweep regions. KEGG analysis showed that genes in selection sweep regions were enriched in pyruvate metabolism, glyoxylate, and dicarboxylate metabolism, fructose and mannose metabolism, citrate cycle (TCA cycle), arginine and proline metabolism, amino sugar and nucleotide sugar metabolism, nitrogen metabolism, and so on. This analysis suggested that genes involved in nitrogen and carbohydrate catabolism processes may provide cultivars with important nutrients and energy, helping them adapt to the cultivation environment. Among these 573 genes, a total of 13 DGEs were identified using RNA-seq data from fruit bodies at the harvesting stage. In particular, AGABI2DRAFT_194428 was predicted to encode the G-protein alpha subunit (guanine nucleotide-binding protein, alpha subunit), which regulates growth, development of fruit bodies, sporulation, and stress resistance [38,39]. Differential expression of AGABI2DRAFT_194428 between wild strains and cultivars implies that this gene plays an important role in cultivar growth, development, and adaptation to environmental conditions.
Understanding the properties of button mushroom strains can help select excellent germplasms for breeding and/or cultivation. Previously, the methods used to assess A. bisporus strain characteristics were cultivation and observation. Prolonged, repeated cultivation and observation, however, is labor intensive and slow. Isozyme electrophoresis, a useful and rapid approach, allows the identification of A. bisporus strain traits at the mycelium stage. In this study, we assessed the characteristics of 200 strains using the ester isozyme phenotype, from which three types (H, G, and HG) were obtained.
GWAS or RNA-seq has been widely implemented to identify genes associated with waterlogging tolerance [40], disease [41], growth, and development [42,43]. However, some problems remain unsolved; for example, false positives in GWAS and significant numbers of DEGs forbidding the identification of potential key candidate genes [11]. Recently, a combination of GWAS and RNA-seq has been employed to mine candidate genes, such as genes involved in low-temperature tolerance [11] and drought stress [44]. In our research, GWAS analysis exhibited 167 candidate genes associated with the ester isozyme phenotype. After integrating RNA-seq, a total of six DGEs were identified as downregulated in the H and HG comparison group.
Among the six DGEs associated with the ester isozyme phenotype, AGABI2DRAFT_183745 was predicted as 8-amino-7-oxononanoate synthase, which is required for biotin biosynthesis. Previous studies demonstrated that is involved with fruiting body formation [45]. Compared to the HG type, AGABI2DRAFT_183745 was upregulated in type H strains, implying that this gene could be associated with production of fruiting body rather than quality. Calcium-independent phospholipase A2 (iPLA2), one type of phospholipase A2, are esterases and were previously suggested to play roles in cell regulation, growth, and death and signal transduction pathways (e.g., MAPK) [46,47,48,49]. AGABI2DRAFT_151295-encoding calcium-independent phospholipase A2-gamma (iPLA2γ) was deferentially expressed, implying that it may contribute to the difference of the easter isozyme phenotype and morphology between H and HG strains. High-affinity methionine permease participates in amino acid transport and metabolism for morphogenesis [50]. Up-expression of AGABI2DRAFT_191000-encoding high-affinity methionine permease in the H type may be involved in the morphogenesis of H strains. However, three other genes obtained by a combination of GWAS and RNA-seq data were predicted as hypothetical proteins and their function is still unclear. Compared to the HG type, the expressions of three genes were upregulated in the H type, suggesting they may also have roles in the yield of H strains.
A selective sweep analysis generated 144 cultivated signals and 573 genes. Of these, 13 candidate genes were found to have significantly different expression patterns at the fruit body stage. Additionally, a combination of GWAS and RNA-seq analyses revealed six promising genes for further study. These loci and candidate genes provide a reference for future molecular breeding to improve button mushroom environmental adaptation, yield, and quality. Future experimental work such as short hairpin RNA and genetic transformations should be implemented to validate the function or effect of these genes.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/horticulturae10070691/s1, Figure S1: Electrophoresis analysis of the esterase isozyme of partial strains selected randomly. Strain As2796 belong to HG tpye used as reference; Table S1: Description of Agaricus bisporus strains.

Author Contributions

Investigation, funding acquisition, writing—original draft, Y.L.; investigation, Z.G., B.K., H.Z. (Huiqing Zheng)., Z.Z. and Z.C.; investigation, funding acquisition, H.Z. (Hui Zeng); conceptualization, writing—review and editing, funding acquisition, J.L.; conceptualization, supervision, funding acquisition, writing—review and editing, M.C. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Natural Science Foundation of Fujian Province (Grant No. 2023J01203), the earmarked fund for the China Agriculture Research System (Grant No. CARS-20), Fundamental Research Project for Public Welfare Scientific Research Institutes in Fujian (Grant No. 2022R1035006), and 5511 Collaborative innovation project of Fujian Province, China (Grant No. XTCXGC2021007).

Data Availability Statement

The original contributions presented in the study are included in the article/Supplementary Material, further inquiries can be directed to the corresponding authors.

Conflicts of Interest

The authors declare no conflict of interest.

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Horticulturae 10 00691 g001aHorticulturae 10 00691 g001b
Figure 1. Population characterization of 200 A. bisporus accessions and the decay of linkage disequilibrium (LD). (A) Neighbor-joining phylogenetic tree using whole-genome SNPs. (B) PCA of wild and cultivated strains based on whole-genome SNPs. (C) Population structure of 200 strains showing two subpopulations at K = 2. (D) linkage disequilibrium (LD) patterns.
Figure 1. Population characterization of 200 A. bisporus accessions and the decay of linkage disequilibrium (LD). (A) Neighbor-joining phylogenetic tree using whole-genome SNPs. (B) PCA of wild and cultivated strains based on whole-genome SNPs. (C) Population structure of 200 strains showing two subpopulations at K = 2. (D) linkage disequilibrium (LD) patterns.
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Figure 2. Genome-wide selection and functional annotation of selected genes. (A) Genome-wide selection based on Fst and π values. Red plots represent genomic regions with strong selective sweep signals using the top 5% of Fst and π values. (B) Manhattan plots of selective signals. (C) GO term enrichment analysis of selected genes. (C) KEGG pathway enrichment analysis of selected genes.
Figure 2. Genome-wide selection and functional annotation of selected genes. (A) Genome-wide selection based on Fst and π values. Red plots represent genomic regions with strong selective sweep signals using the top 5% of Fst and π values. (B) Manhattan plots of selective signals. (C) GO term enrichment analysis of selected genes. (C) KEGG pathway enrichment analysis of selected genes.
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Figure 3. GWAS for esterase isozyme type. (A) Manhattan plot of genomic region associated with esterase isozyme type. (B) Quantile–quantile plot.
Figure 3. GWAS for esterase isozyme type. (A) Manhattan plot of genomic region associated with esterase isozyme type. (B) Quantile–quantile plot.
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Table 1. Differentially expressed candidate genes in selected regions.
Table 1. Differentially expressed candidate genes in selected regions.
Gene IDRegulatedGO Annotationnr_Annotation
AGABI2DRAFT_196124downGO:0004571, GO:0005509, GO:0016020 Endoplasmic reticulum mannosyl-oligosaccharide 1,2-alpha-mannosidase
AGABI2DRAFT_117541down--hypothetical protein
AGABI2DRAFT_62224upGO:0010181, GO:001649, GO:0055114Putative NADPH dehydrogenase
AGABI2DRAFT_176301down--hypothetical protein
AGABI2DRAFT_190117down--ferritin-like domain-containing protein
AGABI2DRAFT_203715upGO:0015103, GO:0015297, GO:0015698, GO:0055085, GO:0016021Arsenite resistance protein ArsB, partial
AGABI2DRAFT_181624down--hypothetical protein AN958_00352
AGABI2DRAFT_181629downGO:0008233, GO:0006508L-amino acid amidase
AGABI2DRAFT_178110down--predicted protein
AGABI2DRAFT_178286up--hypothetical protein AN958_04611
AGABI2DRAFT_192454downGO:0004342, GO:0016787, GO:0005975, GO:0006044Glucosamine-6-phosphate isomerase
AGABI2DRAFT_208542up--hypothetical protein AN958_12461
AGABI2DRAFT_194428downGO:0005488, GO:0007165 guanine nucleotide binding protein, alpha subunit
Table 2. Candidate genes associated with esterase isozyme type obtained by an integrated approach of GWAS and transcriptome analysis.
Table 2. Candidate genes associated with esterase isozyme type obtained by an integrated approach of GWAS and transcriptome analysis.
Gene IDRegulatedGO Annotationnr_Annotation
AGABI2DRAFT_143474down--hypothetical protein AN958_07900
AGABI2DRAFT_183745downGO:0009058, GO:0016740, GO:00301708-amino-7-oxononanoate synthase
AGABI2DRAFT_191000downGO:0000101, GO:0003333, GO:0006812, GO:0015171, GO:0016020High-affinity methionine permease
AGABI2DRAFT_123388down--hypothetical protein AN958_01095
AGABI2DRAFT_120988down-hypothetical protein BP6252_06823
AGABI2DRAFT_151295down--Calcium-independent phospholipase A2-gamma
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Lu, Y.; Guo, Z.; Ke, B.; Zheng, H.; Zeng, Z.; Cai, Z.; Zeng, H.; Liao, J.; Chen, M. Genome-Wide Association Study and Transcriptome Analysis Provide Candidate Genes for Agronomic Traits of Agaricus bisporus. Horticulturae 2024, 10, 691. https://doi.org/10.3390/horticulturae10070691

AMA Style

Lu Y, Guo Z, Ke B, Zheng H, Zeng Z, Cai Z, Zeng H, Liao J, Chen M. Genome-Wide Association Study and Transcriptome Analysis Provide Candidate Genes for Agronomic Traits of Agaricus bisporus. Horticulturae. 2024; 10(7):691. https://doi.org/10.3390/horticulturae10070691

Chicago/Turabian Style

Lu, Yuanping, Zhongjie Guo, Binrong Ke, Huiqing Zheng, Zhiheng Zeng, Zhixin Cai, Hui Zeng, Jianhua Liao, and Meiyuan Chen. 2024. "Genome-Wide Association Study and Transcriptome Analysis Provide Candidate Genes for Agronomic Traits of Agaricus bisporus" Horticulturae 10, no. 7: 691. https://doi.org/10.3390/horticulturae10070691

APA Style

Lu, Y., Guo, Z., Ke, B., Zheng, H., Zeng, Z., Cai, Z., Zeng, H., Liao, J., & Chen, M. (2024). Genome-Wide Association Study and Transcriptome Analysis Provide Candidate Genes for Agronomic Traits of Agaricus bisporus. Horticulturae, 10(7), 691. https://doi.org/10.3390/horticulturae10070691

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