全基因组关联研究对玉米（Zea mays L.）抗大丽轮枝菌的分析-动脉网

Genome-wide association study for resistance to Macrophomina phaseolina in maize (Zea mays L.)

Nature 等信源发布 2025-03-06 12:56



可切换为仅中文







Abstract

摘要

Maize (

玉米（

Zea mays

玉米

L.) is a frequently used food source in human and animal nutrition.

L.) 是人类和动物营养中经常使用的食物来源。

Macrophomina phaseolina

大丽轮枝菌

is a fungal pathogen causing charcoal rot disease in many plants, especially maize. This pathogen causes high yield losses in maize. The development of resistant maize genotypes is of great importance in controlling this disease. In this study, the population structure of 120 different maize genotypes with varying levels of disease resistance was determined and genome-wide association studies were performed.

是一种引起多种植物尤其是玉米炭疽病的真菌病原体。该病原体会导致玉米的严重减产。培育抗病玉米基因型对控制此病害具有重要意义。本研究确定了120个不同抗病水平的玉米基因型的群体结构，并进行了全基因组关联分析。

Each genotype was subjected to the pathogen under controlled conditions and their phenotypic responses to the disease were analyzed. Afterwards, single nucleotide polymorphisms were determined by DArT-seq sequencing. After filtering the SNP data, 37,470 clean SNPs were obtained. The population structure was analyzed with STRUCTURE software, and it was determined that the population was divided into two subgroups.

每种基因型都在受控条件下接受病原体处理，并分析了它们对疾病的表型反应。随后，通过DArT-seq测序确定了单核苷酸多态性。在对SNP数据进行过滤后，获得了37,470个干净的SNP。使用STRUCTURE软件分析群体结构，确定该群体分为两个亚组。

The relationship between phenotypic and genotypic data was analyzed using the MLM (Q + K) model in TASSEL software. As a result, seven SNPs markers located on four different chromosomes were associated with disease resistance. The related markers can be used in the future for the development of maize varieties resistant to .

使用TASSEL软件中的MLM (Q + K) 模型分析了表型和基因型数据之间的关系。结果表明，位于四条不同染色体上的七个SNP标记与抗病性相关。这些相关标记未来可用于开发抗病玉米品种。

M. phaseolina

by marker-assisted selection.

通过标记辅助选择。

Introduction

介绍

Maize (

玉米（

Zea mays

玉米

L. or corn) is a cross-pollinated, annual, and diploid (2n = 20) member of Poaceae family

L. 或玉米）是禾本科家族中异花授粉、一年生、二倍体（2n=20）的成员。

and has an average genome size of 2.4 Gb

并且平均基因组大小为2.4 Gb

. Maize is frequently used in human and animal nutrition due to its high content of vitamins A, B, and C, carbohydrates, protein, and phytochemicals

。由于玉米富含维生素A、B和C、碳水化合物、蛋白质以及植物化学物质，因此常被用于人类和动物的营养中。

，

. In 2022, maize ranks as the second most produced cereal crop, covering a cultivation area of 43 million hectares globally. It is cultivated in 164 countries, where the annual harvest comes to the amount of about 1.16 billion tons

2022年，玉米是第二大产量的谷物作物，全球种植面积达4.3亿公顷。它在164个国家种植，年收获量约为11.6亿吨。

. Türkiye is one of the world’s important maize producers with approximately one million hectares and a production of 8.5 million tons annually. Considering the size of maize production worldwide, yield losses can have substantial economic consequences. Nevertheless, several factors negatively affect maize production with some of the major factors being diseases and pests..

土耳其是世界上重要的玉米生产国之一，拥有大约一百万公顷的种植面积，年产量达850万吨。考虑到全球玉米生产的规模，产量损失可能带来严重的经济后果。然而，有若干因素对玉米生产产生了负面影响，其中一些主要因素是病害和虫害。

Plant diseases caused by fungal infections are the most important pathogenic agents.

由真菌感染引起的植物病害是最重要的致病因素。

Macrophomina phaseolina

大丽轮枝菌

(

兆帕

) is a broad-host fungi that can infect hundreds of different plants and induce a root cancer called charcoal rot in its host

）是一种广寄主真菌，可以感染数百种不同的植物，并在其宿主中引发一种称为炭腐病的根癌。

. This pathogen is one of the most destructive diseases that can cause severe yield losses in maize plants and lead to 25–33% or more crop losses. Besides causing plant mortality, it adversely impacts the quality attributes of the product. A recent study observed that high disease severity caused by .

这种病原体是最具破坏性的疾病之一，可导致玉米植株严重减产，并造成25%-33%或更高的作物损失。除了导致植物死亡外，它还对产品质量产生负面影响。最近的一项研究观察到，由该病原体引起的高病害严重程度。

兆帕

caused a 30–70% decrease in the biophysical and biochemical properties of plants

导致植物的生物物理和生化特性下降了30-70%

. This highlights the significant adverse economic impact of the pathogen on plants, primarily due to reductions in both yield and quality.

这突显了该病原体对植物的重大不利经济影响，主要原因是产量和质量均有所下降。

兆帕

infection can cause mortality both before and after plant emergence. The most prominent symptom is ‘blackleg’ due to sclerotia at the plant crown. Infected plants are characterized by lesions with dark margins and light grey centres

感染可能在植物出苗前和出苗后都导致死亡。最显著的症状是由于植物根冠处的菌核引起的“黑脚病”。受感染的植物特征是具有深色边缘和浅灰色中心的病斑。

, wilted appearance and discoloured leaves

枯萎的外观和变色的叶子

. Furthermore, the phytotoxic metabolites released by

此外，释放的植物毒性代谢物

兆帕（MPa）

cause vascular obstructions that impede nutrient transport, leading to plant death. The ability of this pathogen to persist in soil for long periods and its wide genetic diversity contributes to its widespread in different climatic conditions

引起阻碍养分运输的血管阻塞，导致植物死亡。这种病原体在土壤中长时间存活的能力及其广泛的遗传多样性促成了其在不同气候条件下的广泛分布。

。

The development of resistant cultivars to control

抗性品种的开发与控制

兆帕

has become a critical requirement due to the limitations of current control methods. Chemical control can lead to resistance development of the pathogen and environmental problems; in addition, the effectiveness of systemic fungicides is limited due to their inability to reach the roots. Physical control methods require high cost and labour, which negatively affects agricultural productivity.

由于当前控制方法的局限性，这已成为一项关键需求。化学控制可能导致病原体产生抗药性并引发环境问题；此外，内吸性杀菌剂因无法到达根部，其效果有限。物理控制方法成本高、劳动强度大，对农业生产力产生负面影响。

. Although agronomic practices aim to reduce the density of microsclerotia, some methods such as irrigation are not effective

尽管农艺措施旨在减少微菌核的密度，但某些方法（如灌溉）却效果不佳。

，

. Biological control varies depending on environmental conditions and does not always give reliable results. Although plant defense stimulants trigger defense mechanisms, their effects vary depending on genotype and environmental conditions, and in some cases may negatively affect other plant traits.

生物防治因环境条件而异，并不总是产生可靠的结果。尽管植物防御刺激剂会触发防御机制，但其效果因基因型和环境条件而异，在某些情况下可能对其他植物性状产生负面影响。

. Consequently, due to the limitations of current methods, the development of resistant cultivars appears to be the most effective and sustainable strategy for permanent control of

. 因此，由于现有方法的局限性，培育抗性品种似乎是实现永久控制的最有效和可持续的策略。

兆帕（MPa）

。

Conventional breeding methods require many years to develop disease-resistant varieties in plants. However, modern molecular techniques such as genome-wide association studies (GWAS) accelerate this process and make significant contributions to breeding studies. GWAS reveals the relationship between genetic variants and plant traits using genotypic and phenotypic data.

传统育种方法需要多年时间来培育抗病植物品种。然而，全基因组关联研究（GWAS）等现代分子技术加速了这一进程，并为育种研究做出了重要贡献。GWAS利用基因型和表型数据揭示遗传变异与植物性状之间的关系。

Since this technique directly identifies the genetic factors affecting phenotypic variation, it provides more precise and efficient results compared to traditional methods.

由于该技术直接识别影响表型变异的遗传因素，因此与传统方法相比，它提供了更精确和高效的结果。

. In particular, in previous studies, diseases such as Fusarium-induced ear rot

特别地，在以前的研究中，镰刀菌引起的穗腐病等疾病

，

Aspergillus flavus

黄曲霉

infection

感染

，

Phytium aristosporum

富勒烯孢子植物

-induced stalk rot

诱导性茎腐病

and maize rough dwarfism

玉米粗矮病

were investigated by GWAS and resistance genes were identified. In addition, GWAS has also been used in the development of resistant varieties against the western corn rootworm

通过GWAS进行了研究，并鉴定了抗性基因。此外，GWAS还被用于开发针对西方玉米根虫的抗性品种。

. Thus, it enables a better understanding the genetic background of complex traits such as disease resistance. By measuring the contribution of specific genetic variants to a trait, GWAS accelerates the identification of genetic markers to be used in breeding programs. This allows the development of resistant varieties in a shorter time..

因此，它有助于更好地理解复杂性状（如抗病性）的遗传背景。通过测量特定遗传变异对性状的贡献，GWAS加速了可用于育种计划的遗传标记的识别。这使得抗性品种的开发时间大大缩短。

One of the technologies used to provide genotypic data for GWAS is Diversity Array Technology (DArT). DArT detects thousands of single nucleotide polymorphism (SNP) markers quickly and efficiently without the need for whole genome sequencing

提供GWAS基因型数据的技术之一是多样性阵列技术（DArT）。DArT能够快速高效地检测成千上万个单核苷酸多态性（SNP）标记，而无需进行全基因组测序。

. SNP markers produced by DArT are used for mapping gene loci that control phenotypic traits and for the identification of genetic variants. Therefore, DArT and similar technologies make breeding programs more effective by providing genetic data to GWAS studies.

由DArT产生的SNP标记用于绘制控制表型性状的基因位点和鉴定遗传变异。因此，DArT及类似技术通过为GWAS研究提供遗传数据，使育种计划更加有效。

This study aimed to perform GWAS analysis to identify molecular markers for

本研究旨在进行GWAS分析以识别分子标记

兆帕

resistance using 120 different maize genotypes. The research aims to identify genetic variations contributing to

使用120种不同玉米基因型的抗性研究。该研究旨在识别导致

兆帕

resistance among different genotypes and specific SNPs associated with these variations. The identification of these molecular markers will facilitate future studies by providing an understanding of the genetic basis of

不同基因型之间的抗性以及与这些变异相关的特定SNPs。鉴定这些分子标记将通过提供对遗传基础的理解，促进未来的研究。

兆帕

resistance. Furthermore, the findings will contribute to the development of breeding programs for the development of resistant varieties, ultimately strengthening plant protection strategies against

抗性。此外，这些发现将有助于育种计划的开发，以培育抗性品种，最终加强植物保护策略以应对

兆帕

infection and contributing to sustainable agricultural practices.

感染并有助于可持续农业实践。

Results

结果

Phenotypic variations of the population

种群的表型变异

The resistance to

对...的抵抗

兆帕

for 120 different maize genotypes under controlled conditions was evaluated and disease symptoms were scored. The average disease score was calculated as 4.2. Out of 120 genotypes, 12 were classified as resistant, 43 as moderately resistant/tolerant, 48 as moderately susceptible/susceptible, and 17 as highly susceptible.

在受控条件下对120种不同的玉米基因型进行了评估，并对病害症状进行了评分。平均病害评分为4.2。在120个基因型中，12个被归类为抗病，43个为中度抗病/耐病，48个为中度感病/感病，17个为高度感病。

As a result of the examination of the disease response distribution, it was determined that the population used exhibited a normal distribution suitable for the GWAS study. The normal distribution of genotypes is depicted in the histogram graph in Fig. .

通过对疾病反应分布的检查，确定所使用的人群呈现出适合GWAS研究的正态分布。基因型的正态分布在图中的直方图中有所展示。

. Analysis of variance of

。方差分析

兆帕（MPa）

disease scores reveals significant effects of maize genotypes on disease severity. The results of the analysis of variance are presented in Table

疾病评分显示玉米基因型对疾病严重程度有显著影响。方差分析的结果见表

. Analysis of variance showed that the resistance reactions to

方差分析显示，抗性反应

兆帕（MPa）

among the 120 maize genotypes were statistically significant at

在120种玉米基因型中具有统计学显著性的是

≤ 0.05 level which shows that there are differences among the genotypes in terms of reaction to the pathogen infection. ANOVA assumptions, including homogeneity of variances and normality, were tested and confirmed to be accurate. In addition, the broad sense heritability score was calculated as 0.80..

在 ≤ 0.05 水平上，这表明基因型对病原体感染的反应存在差异。已检验并确认方差分析（ANOVA）的前提假设，包括方差齐性和正态性，均准确无误。此外，广义遗传力得分计算为 0.80。

Fig. 1

图1

Disease score distribution for the 120 maize genotypes based on 0–5 scores.

基于0-5分的120种玉米基因型的病害评分分布。

Full size image

全尺寸图像

Table 1 Analysis of variance results of disease severity and genotype.

表1 疾病严重程度和基因型的方差分析结果。

Full size table

全尺寸表格

Population structure analysis

种群结构分析

A total of 79,166 SNPs were obtained through DArT analysis. The initial SNP data were subjected to strict filtration criteria allowing only SNPs with 95% call rate and 5% minor allele frequency (MAF) to remain, resulting in 37,470 high-quality SNPs. This process was performed to ensure the reliability of subsequent analyses.

通过DArT分析共获得79,166个SNP。初始SNP数据经过严格过滤，仅保留具有95%呼叫率和5%次要等位基因频率（MAF）的SNP，最终得到37,470个高质量SNP。此过程旨在确保后续分析的可靠性。

SNPs are uniformly distributed among chromosomes, with an average of 2,500 SNPs per chr. The highest SNP number was found in chr 1 with 4,129 SNPs and the lowest SNP number was found in chr 10 with 1,639 SNPs. Furthermore, the polymorphism information (PIC) content values of SNPs ranged from 0.01 to 0.5, with an average of 0.31.

SNPs在染色体间均匀分布，平均每条染色体有2,500个SNPs。最高SNP数量出现在1号染色体，有4,129个SNPs，最低SNP数量出现在10号染色体，有1,639个SNPs。此外，SNPs的多态性信息含量（PIC）值范围为0.01到0.5，平均值为0.31。

This indicates a moderate level of genetic diversity within the population. Following filtration, clean SNP data were utilized in STRUCTURE analyses with 50,000 iterations. The ΔK value was determined by conducting calculations for each group ranging from 1 to 10 using STRUCTURE HARVESTER software, with the peak observed at K = 2 (Fig.

这表明该群体内具有中等水平的遗传多样性。过滤后，使用清洁的SNP数据进行STRUCTURE分析，迭代50,000次。通过STRUCTURE HARVESTER软件对每组从1到10进行计算，确定ΔK值，在K=2时观察到峰值（图。

。

). The population was divided into two groups: population 1 (green) and population 2 (red), as shown in Fig.

). 人口被分为两组：人口1（绿色）和人口2（红色），如图所示。

。

Fig. 2

图2

ΔK plot obtained from STRUCTURE HARVESTER software.

使用STRUCTURE HARVESTER软件获得的ΔK图。

Full size image

全尺寸图像

Fig. 3

图3

The population structure of the 120 maize genotypes was analyzed based on 37,470 DArT-seq markers using STRUCTURE.

基于37,470个DArT-seq标记，使用STRUCTURE对120种玉米基因型的群体结构进行了分析。

Full size image

全尺寸图像

Association analysis and candidate genes

关联分析和候选基因

GWAS analysis was carried out in TASSEL software. From the option, the MLM (Q + K) model was chosen to analyze associations between marker and trait data. The MLM (Q + K) model decreases the false positive rate in analysis by accounting for both population structure and genetic linkages. This model adjusts the population structure using the Q matrix and genetic relationships through the K matrix, thereby yielding more precise results.

GWAS分析在TASSEL软件中进行。从选项中，选择了MLM (Q + K) 模型来分析标记与性状数据之间的关联。MLM (Q + K) 模型通过考虑群体结构和遗传连锁来降低分析中的假阳性率。该模型利用Q矩阵调整群体结构，并通过K矩阵调整遗传关系，从而得出更精确的结果。

. According to the GWAS analysis, seven SNPs were detected along the four different chromosomesexceeding the FDR corrections. FDR corrections (-log

根据GWAS分析，检测到七个SNP分布在四个不同的染色体上，超过了FDR校正。FDR校正（-log

P value is ≥ 3.28) were utilized to filter the most likely SNPs to avoid false positives. The Manhattan plot illustrates the distribution of SNPs across various chromosomes and identifies significant SNPs concentrated in specific regions (Fig.

P值≥3.28被用于筛选最有可能的SNPs，以避免假阳性。曼哈顿图展示了SNPs在各染色体上的分布，并确定了集中在特定区域的显著SNPs（图。

). After the filtering process, seven SNP markers associated with resistance were identified. The -log

过滤过程后，鉴定出七个与抗性相关的SNP标记。-log

P, R², and PIC values of the SNPs found were used to evaluate the significance and effect of these markers (Table

使用发现的SNPs的P值、R²和PIC值来评估这些标记的重要性和效应（表

). The -log

). 负对数

P value indicates the statistical significance of the SNP’s association with the phenotype, while the R² value reflects the proportion of phenotypic variation explained by this SNP. The PIC value expresses the SNP’s capacity to reflect genetic variation. SNP6999, located on chr 2, was found to be the most associated marker with the highest -log.

P值表示SNP与表型关联的统计显著性，而R²值反映了该SNP解释的表型变异比例。PIC值表示SNP反映遗传变异的能力。位于2号染色体上的SNP6999被发现是关联最强的标记，具有最高的-log值。

P value (3.70). It was followed by SNP12080 and SNP34600 on chr 8 (-log

P值（3.70）。随后是8号染色体上的SNP12080和SNP34600（-log

P, 3.61 and 3.60, respectively). As seen in the Q-Q plot, most data points are positioned on the diagonal line, indicating that the observed P values show a good fit to the expected distribution. This fit suggests that the P values were appropriately adjusted for multiple testing and that the analysis was robust to control for potential false positives (Fig.

P值分别为3.61和3.60。正如Q-Q图中所见，大多数数据点位于对角线上，这表明观察到的P值与预期分布拟合良好。这种拟合表明P值已经过多重检验的适当校正，且分析在控制潜在假阳性方面具有鲁棒性（图。

。

). Candidate genes were identified by screening up and down 100,000 base pairs of SNP locations, and 33 different genes with various activities were found. These genes are involved in disease resistance and play important roles in plant defence mechanisms such as cell wall synthesis, phytohormone signalling and activation of transcription factors.

）。通过筛查SNP位点上下游10万个碱基对，鉴定了候选基因，发现了33个具有不同活性的基因。这些基因参与抗病性，并在植物防御机制中发挥重要作用，如细胞壁合成、植物激素信号传导和转录因子的激活等。

They also show the potential to alter cell wall composition, regulate stress responses and increase resistance to fungal pathogens. The candidate genes associated with the SNP markers and their functions are given in Supplementary Table .

它们还显示出改变细胞壁组成、调节应激反应和增强对真菌病原体抗性的潜力。与SNP标记相关的候选基因及其功能见补充表。

。

Fig. 4

图4

Manhattan plot of

曼哈顿图

兆帕

resistance in 120 maize genotypes.

120种玉米基因型的抗性。

Full size image

全尺寸图像

Table 2 The list of SNP markers associated with

表2 与以下相关的SNP标记列表

兆帕（MPa）

resistance.

抵抗。

Full size table

全尺寸表格

Fig. 5

图5

Quantile-quantile plot for the

分位数-分位数图用于

兆帕

resistance.

电阻。

Full size image

全尺寸图像

Discussion

讨论

兆帕

is one of the most destructive pathogens of maize production, causing major losses in maize yields. It causes yield loss not only in maize but also in soya bean

是玉米生产中最具破坏性的病原体之一，导致玉米产量的重大损失。它不仅在玉米上造成减产，还在大豆上造成减产。

，

, canola

`, 油菜籽`

, sorghum

，高粱

，

and other plants

和其他植物

，

. For this reason, many studies have been carried out to determine the genetic factors that provide resistance in various plants. Statistical analysis of the disease resistance data obtained because of phenotypic observations revealed that there was significant diversity among the genotypes used in the study and that the data were normally distributed.

由于这个原因，许多研究被开展以确定在各种植物中提供抗性的遗传因素。对因表型观察而获得的抗病数据进行统计分析后发现，所用基因型之间存在显著的多样性，并且数据呈正态分布。

However, environmental factors and growth conditions were reported to have a significant effect on resistance to fungal infections.

然而，据报道，环境因素和生长条件对真菌感染的抵抗力有显著影响。

. In this study, variation between genotypes was analyzed by ANOVA on phenotypic data and this variation was attributed to genetic factors. Broad sense heritability indicates the proportion of total phenotypic variation attributable to genetic factors and was found to be 0.80 in this study; therefore, it can be concluded that broad sense heritability demonstrates that the disease resistance trait is generally inherited genetically.

在本研究中，通过ANOVA对表型数据进行基因型间变异分析，并将此变异归因于遗传因素。广义遗传力表示总表型变异中可归因于遗传因素的比例，本研究中发现为0.80；因此，可以得出结论，广义遗传力表明抗病性状通常是由遗传因素决定的。

This value was higher than those reported in the literature. The heritability value was determined as 0.54–0.67 in maize.

该值高于文献中报道的值。在玉米中，遗传力值被确定为0.54-0.67。

and approximately 0.6 in soybean

大豆中约为0.6

in GWAS studies for resistance to

在GWAS研究中对抗性进行

兆帕

. These values indicated that resistance to

。这些值表明对

兆帕（MPa）

is highly heritable. Therefore, the high heritability of disease resistance is an indication of the reproducibility of the study and the reliability of its use in breeding studies.

具有很高的遗传性。因此，疾病抗性的高遗传性是研究可重复性和其在育种研究中使用的可靠性的一个指标。

In this study, the MLM (Q + K) model is preferred to correct the population structure. This model effectively eliminates potential false positives by taking into account random and fixed effects according to Henderson’s notation and provides precision in analysing complex traits

在本研究中，优选MLM（Q+K）模型来校正群体结构。该模型根据亨德森的符号考虑了随机和固定效应，有效消除了潜在的假阳性，并在分析复杂性状时提供了精确性。

. Previous research has revealed that between the observed and expected -log

之前的研究表明，在观测值和预期值之间的-log

P values shown by the Q-Q plot, the G-test model exhibits the highest deviation, followed by the general linear model (GLM or G + Q model). However, the MLM model shows the least bias as it corrects for both population structure (Q) and relatedness (K)

Q-Q图显示的P值表明，G检验模型的偏差最大，其次是通用线性模型（GLM或G+Q模型）。然而，MLM模型由于同时校正了群体结构（Q）和亲缘关系（K），其偏差最小。

. Furthermore, FDR (False Discovery Rate) correction was applied to reduce false positive associations. These methods are critical for improving the reliability of results in large-scale GWAS studies.

此外，还应用了FDR（错误发现率）校正来减少假阳性关联。这些方法对于提高大规模GWAS研究结果的可靠性至关重要。

In the present study, a GWAS study was performed with a total of 37,470 SNPs by filtering SNPs obtained by the DArT-seq. As a result of the analyses, seven SNPs were identified with -log

在本研究中，通过对DArT-seq获得的SNP进行过滤，使用总计37,470个SNP进行了GWAS研究。分析结果表明，七个SNP被确定为-log。

P values ranging from 3.70 to 3.40, indicating the statistical significance of the effect of SNPs on phenotype. In addition, R

P值范围从3.70到3.40，表明SNPs对表型影响的统计显著性。此外，R

values, which indicate how much of the phenotypic variance is explained by genotypes, were found to vary between 0.12 and 0.11. Considering the genetic basis of complex characteristics such as disease resistance, a single SNP is not expected to explain a large proportion of the phenotypic variance.

这些值表示基因型能够解释多少表型变异，被发现介于0.12到0.11之间。考虑到复杂性状（如抗病性）的遗传基础，单个SNP不可能解释大部分表型变异。

Therefore, R² values around 0.1 can be predicted and the results obtained in this study are under the polygenic nature of complex traits. According to a study conducted in soybeans, 19 out of 35,683 clean SNPs obtained with Illumina Infinium SoySNP50K BeadChip were detected to be associated with the .

因此，可以预测R²值在0.1左右，本研究所得结果符合复杂性状的多基因特性。根据一项在大豆中进行的研究，使用Illumina Infinium SoySNP50K BeadChip获得的35,683个清晰SNP中，检测到19个与相关。

兆帕

. In a different study, 3,780 clean SNP data in soybeans were also obtained using the same method. Among the SNPs obtained, six SNPs with R

。在另一项研究中，也使用相同的方法获得了大豆中的3,780个清晰的SNP数据。在获得的SNP中，具有R值的六个SNP

values ranging between 9.5 and 11.8% were reported to be associated with resistance

据报道，介于9.5%到11.8%之间的值与耐药性有关。

. These R

。这些R

values align with the findings of the current study, supporting the consistency and reliability of the results. However, only one GWAS study in maize has been identified so far. In the study in which 396 maize varieties adapted to Asia were used, filtering was performed according to call rate > 0.7 and MAF > 0.05, resulting in 296 K clean SNPs obtained by Genotyping by Sequencing (GBS) method.

这些值与当前研究的发现一致，支持了结果的一致性和可靠性。然而，到目前为止，只有一项关于玉米的GWAS研究被确定。在该研究中，使用了适应亚洲的396个玉米品种，根据检出率>0.7和MAF>0.05进行过滤，最终通过测序基因分型（GBS）方法获得了296,000个高质量的SNP。

. In the present study, a more stringent call rate filter (> 0.95) was used to minimize false positives. A total of 19 SNP markers associated with disease resistance, with -log

在本研究中，使用了更为严格的检出率过滤器（> 0.95）以尽量减少假阳性。共有19个与抗病性相关的SNP标记，其-log

P values ranging from 5.23 to 4.32, were identified. While the reported -log

确定了P值范围从5.23到4.32。而报告的-log

P values in that study were statistically more significant than those observed here, lower heritability values (ranging from 0.67 to 0.54) were reported, likely due to the field conditions under which the study was conducted. Environmental factors beyond control may have negatively impacted the heritability estimates.

该研究中的P值在统计学上比这里观察到的更为显著，报告的遗传力值较低（范围从0.67到0.54），这很可能是由于研究进行时的田间条件所致。无法控制的环境因素可能对遗传力估计产生了负面影响。

. In contrast, the controlled conditions used in this study resulted in higher heritability values. Similar to the current study, most SNPs were identified on chromosomes 3, 6, and 8

相比之下，本研究中使用的受控条件导致了更高的遗传力值。与当前研究类似，大多数SNP是在3号、6号和8号染色体上鉴定出来的。

. Additionally, for the first time, genomic regions associated with

此外，首次发现了与之相关的基因组区域

兆帕（MPa）

resistance on chromosome 7 in maize were identified in this study.

本研究在玉米的7号染色体上鉴定了抗性。

Gene loci likely to be associated with disease resistance were identified through association mapping. However, candidate genes can only be predicted by association mapping studies, and further research is needed to determine the role of these genes in the resistance mechanism

通过关联作图，确定了可能与抗病性相关的基因位点。然而，候选基因只能通过关联作图研究进行预测，要确定这些基因在抗性机制中的作用，还需要进一步的研究。

. SNP6999, located on chr 2, is localized between several gene regions such as protein kinases, transcription factors, and ATP-DNA binders. The defense mechanisms of plants against pathogens are quite diverse. Among these, phytohormones such as salicylic acid and ethylene play an important role. The gene LOC100502174 has not yet been characterized in the maize genome, but the protein it expresses has an AP2/ERF domain.

SNP6999 位于 2 号染色体上，处于多个基因区域之间，例如蛋白激酶、转录因子和 ATP-DNA 结合蛋白。植物对病原体的防御机制非常多样。其中，植物激素如水杨酸和乙烯发挥了重要作用。基因 LOC100502174 在玉米基因组中尚未被表征，但它表达的蛋白质具有 AP2/ERF 结构域。

Ethylene-containing elements, also known as Ethylene-Responsive Elements (ERE), induce the expression of some plant defense-related genes.

含有乙烯的元素，也称为乙烯响应元件 (ERE)，会诱导某些植物防御相关基因的表达。

. ERE binding factors (ERF) are transcription factors that recognize ERE sites. In previous studies, the association of ERF sites with resistance to

. ERE结合因子（ERF）是识别ERE位点的转录因子。在之前的研究中，ERF位点与抗性之间的关联

兆帕

has been demonstrated

已被证明

，

. Moreover, the most basic defense mechanism of plants is the cell wall. Cell walls are composed of cellulose, hemicellulose, and pectins. The LOC103648302 gene is involved in the synthesis of xyloglucan (hemicellulose), an important component of the cell wall. In this regard, it may be related to disease resistance..

此外，植物最基本的防御机制是细胞壁。细胞壁由纤维素、半纤维素和果胶组成。LOC103648302基因参与了木葡聚糖（半纤维素）的合成，这是细胞壁的重要组成部分。在这方面，它可能与抗病性有关。

Only a small number of genes are physically close to SNP 22,096. The gene LOC100272653 is the most important of these. This region affects the morphology and physiology of the cell wall and contains domains of pectin methyltransferase. Cell respiration and photosynthetic efficiency can be changed by pectin methyltransferase.

仅有少数基因在物理位置上靠近SNP 22,096，其中最重要的是LOC100272653基因。该区域影响细胞壁的形态和生理，并包含果胶甲基转移酶的结构域。果胶甲基转移酶可以改变细胞呼吸和光合效率。

It can also change the plasticity of cell walls.

它还可以改变细胞壁的可塑性。

，

. This gene is likely to contribute to fungal pathogen resistance by modifying the cell wall

该基因可能通过修饰细胞壁来增强对真菌病原体的抗性。

。

SNP 892 and SNP 26,238 were found to be close to nine different gene regions, including various protein kinases, transmembrane proteins, and transcription factors. Prior research has indicated that ubiquitinated proteins

SNP 892 和 SNP 26,238 被发现接近九个不同的基因区域，包括各种蛋白激酶、跨膜蛋白和转录因子。先前的研究表明，泛素化蛋白

and protein kinases

和蛋白激酶

are involved in host defense. Moreover, pectin methylesterase activity was detected in LOC100274042, which hardens and consolidates the cell wall against various pathogens and generates damage signals to activate defense mechanisms

参与宿主防御。此外，在LOC100274042中检测到果胶甲酯酶活性，它能够加固和巩固细胞壁以抵御各种病原体，并生成损伤信号以激活防御机制。

四十三

。

The chr 8 was found to have a significant association with resistance to

8号染色体被发现与抗性显著相关

兆帕

. This region included three different SNPs that indicate ten different gene regions. SNP 12,080 was found to be close to the

该区域包括三个不同的SNP，指示十个不同的基因区域。发现SNP 12,080接近

mbd

101 gene, which expresses zinc-finger regions with proven activity in plant defense

101基因，该基因表达在植物防御中具有已证实活性的锌指区域

，

, and to the cytochrome P450 gene

，并且与细胞色素P450基因相关

, which is involved in secondary metabolite synthesis and oxidation and reduction reactions. SNP 23,394 was located generally close to genomic regions containing various kinases such as serine/threonine, cysteine, and rust resistance. All these kinases are associated with polysaccharides in the cell wall and thus contribute to the cell wall defense mechanism.

，它参与次生代谢物的合成以及氧化还原反应。SNP 23,394 通常位于包含各种激酶（如丝氨酸/苏氨酸、半胱氨酸和抗锈病激酶）的基因组区域附近。所有这些激酶都与细胞壁中的多糖有关，因此有助于细胞壁的防御机制。

。

Conclusion

结论

The genetic background of

遗传背景

兆帕

resistance in maize was investigated by GWAS. In this study, SNP markers were generated using DArT-seq technology for the first time among the association studies for

通过GWAS研究了玉米的抗性。在本研究中，SNP标记首次在关联研究中使用DArT-seq技术生成。

兆帕

. In GWAS analyses, seven SNPs were found to be significantly associated. Several candidate gene regions were identified on chromosomes 2, 3, 7, and 8 that contribute to disease resistance in different ways. The SNP markers associated with resistance to

在GWAS分析中，发现七个SNP显著相关。在染色体2、3、7和8上鉴定了几个候选基因区域，这些区域以不同方式对疾病抗性做出贡献。与抗性相关的SNP标记

兆帕

identified in this study could be used in marker-assisted selection (MAS), including MAS backcrossing and MAS for quantitative traits, to select lines resistant to

本研究中鉴定出的（标记）可用于标记辅助选择 (MAS)，包括MAS回交和针对数量性状的MAS，以筛选抗性品系。

兆帕

disease in future maize breeding programs. Moreover, 12 maize genotypes found to be resistant to the disease have the potential could be used as donor parents in breeding programs.

未来玉米育种计划中的疾病问题。此外，发现12种对病害具有抗性的玉米基因型可作为育种计划中的供体亲本使用。

Materials and methods

材料与方法

Plant material and DNA isolation

植物材料与DNA提取

The plant materials were kindly received from Polen Seed Co. in Türkiye. A list of 120 genotypes that were used listed in Supplementary Table

植物材料由土耳其的Polen种子有限公司友好提供。所使用的120个基因型列表见补充表。

. Liquid nitrogen was used to freeze fresh leaves that were obtained from the genotypes and weighed 0.1 g. After that, they were grounded to a fine powder using a tissue lyser (Technogene, Türkiye). The Qiagene DNA isolation kit (Catalogue No./ID: 69181) was applied to extract DNA from the powdered leaves.

液氮被用于冷冻从基因型获取的新鲜叶片，并称取0.1克。之后，使用组织研磨仪（Technogene，土耳其）将其研磨成细粉。应用Qiagene DNA分离试剂盒（目录编号/ID：69181）从粉末状叶片中提取DNA。

The quality of the extracted DNA was examined on an agarose gel, and the quantity was measured using a Nanodrop One (Thermo Sci. Co.). The isolates of the .

提取的DNA质量在琼脂糖凝胶上进行了检测，并使用Nanodrop One（Thermo Sci. Co.）测量了其数量。

兆帕

were collected from previous studies and pathogenicity was determined, and then the most aggressive pathogen was used for the determination of genotype reaction to

收集自以前的研究并确定了致病性，然后使用最具侵略性的病原体来确定基因型反应

兆帕

resistance. Following a 7-day incubation period of the fungus in potato dextrose agar medium, ten agar disks were added to each bottle containing oat medium. The bottles were then incubated at 25 ± 2 °C for 15–20 days. After the completion of incubation, a mixture of composted animal manure, sterilized (45 min at 121 °C) soil, and fine sand (2:1:1) was combined with 100 g of inoculum per 1 kg of soil and the mixture was then incubated for five days..

抗性。将真菌在马铃薯葡萄糖琼脂培养基中培养7天后，向每个含燕麦培养基的瓶子中加入十片琼脂圆盘。然后将瓶子置于25±2°C下培养15至20天。培养结束后，将腐熟的动物粪便、经过灭菌处理（121°C下45分钟）的土壤和细沙以2:1:1的比例混合，并每公斤土壤加入100克菌种，混合后继续培养五天。

Inoculum preparation and phenotypic analysis

接种物制备与表型分析

For the genotype reaction studies, the fungal inoculum was first developed by filling 500 ml glass bottles with a mixture of sand-water-cornmeal (9:2:1) or bran. Bottles with media were sterilized in an autoclave at 121 °C for 1 h on 2 consecutive days. Fungal isolates and sclerotia, developed in PDA, were placed in each bottle in the form of 10 agar discs, 5 mm in diameter, and incubated at 30 ± 2 °C for 15–20 days.

对于基因型反应研究，首先通过在500毫升玻璃瓶中填充沙子-水-玉米粉（9:2:1）或麦麸的混合物来制备真菌接种物。含有培养基的瓶子在高压灭菌器中于121°C下连续两天每天灭菌1小时。在PDA培养基上培养的真菌分离物和菌核以10个直径为5毫米的琼脂圆片形式放置在每个瓶子中，并在30±2°C下孵育15至20天。

Once the fungal incubation was completed, a mixture of sterilized garden soil (121 °C for 45 min), peat, perlite, and fine sand (2:1:1) was filled into trays. The inoculum, prepared in the bottles, was then mixed into the soil at a rate of 100 g inoculum per 1 kg of soil and incubated for 4–5 days. After the sterilization with 2% sodium hypochlorite 6 seeds of each genotype were sown in 21 cm diameter pots filled with a mixture of sterile soil, fine sand, peat (2:1:1) containing inoculum.

一旦真菌培养完成，将混合了经灭菌处理的园土（121°C下45分钟）、泥炭、珍珠岩和细沙（比例为2:1:1）填入托盘中。随后，将瓶中制备的接种物以每1公斤土壤加入100克接种物的比例混入土壤，并培养4至5天。用2%次氯酸钠消毒后，将每种基因型的6粒种子播种到直径为21厘米的盆中，盆中装有含接种物的无菌土壤、细沙和泥炭（比例为2:1:1）的混合物。

The cultivar P31G98 was utilized as a positive control due to its being known to be sensitive to .

由于已知该品种对敏感，因此使用了P31G98作为阳性对照。

兆帕

. Negative control plants were planted in disease-free pots.

阴性对照植物种植在无病菌的盆中。

The pots were maintained in climate chambers at 30 °C, 30–45% humidity, and a 16-hour light/8-hour dark cycle. Plants were watered as necessary, ensuring that the soil moisture was not too high

这些盆栽被放置在气候室中，保持在30°C、30-45%湿度，并设置16小时光照/8小时黑暗周期。根据需要给植物浇水，确保土壤湿度不会过高。

. The pathogenicity trials were set up in a randomized complete block design with 3 replicates. Each pot was considered one replicate. The disease severity in the plants was be assessed using a 0–5 scale

病理试验采用随机完全区组设计，设3个重复。每个盆栽视为一个重复。植物的病害严重程度使用0-5级尺度进行评估。

(Fig.

（图。

). After 40 days under the controlled conditions, 40-day-old plants were uprooted, disease symptoms were scored and the disease severity index (DSI) on roots and stems was calculated using the Townsend-Heuberger formula (S = score, P = number of plants, TP = total number of plants, HS = highest score) (Table .

）。在受控条件下40天后，将40天大的植物连根拔起，对病害症状进行评分，并使用Townsend-Heuberger公式（S = 分数，P = 植物数量，TP = 植物总数，HS = 最高分数）计算根和茎的病害严重指数（DSI）（表。

)

。

Fig. 6

图6

Plants representing the 0–5 scale used for scoring corn genotypes. 0: No disease symptoms observed in the plant (

代表0-5级评分标准的植物，用于玉米基因型的评分。0：植株未观察到病害症状 (

); 1: General growth retardation in the plant (

); 1：植物整体生长迟缓 (

); 2: Growth retardation in the plant, chlorosis in the leaves, and mild root rot (

）；2：植物生长迟缓，叶片黄化，根部轻微腐烂（

); 3: Growth retardation in the plant, severe root rot, wilting, and intense chlorosis (

）；3：植物生长迟缓，严重的根腐病、萎蔫和严重黄化（

); 4: Significant growth retardation, complete root rot in the plant (

）；4：严重生长迟缓，植物根部完全腐烂（

); 5: No germination observed.

）；5：未观察到发芽。

Full size image

全尺寸图像

Table 3 Criteria used in phenotyping and corresponding values

表3 用于表型分析的标准及其对应值

。

Full size table

全尺寸表格

$$Disease\;Severity\;\%=\sum \frac{S\times P}{TP\times HS}\times 100$$

$$疾病严重程度\;\%=\sum \frac{S\times P}{TP\times HS}\times 100$$

Genotype reactions were defined according to DSI and phenotypes were arranged in 6 groups (Table

基因型反应根据DSI定义，表型被分为6组（表

）。

Statistical analysis of phenotypic data

表型数据的统计分析

Variance analyses (ANOVA) were conducted using the SPSS software package (version 12.0 J; SPSS Inc., Chicago, IL, USA). At the

使用SPSS软件包（版本12.0 J；SPSS Inc.，芝加哥，伊利诺伊州，美国）进行方差分析（ANOVA）。在

≤ 0.05 significance level, the variances according to the disease severity and genotype interactions were identified. Broad sense heritability score calculated as described by

在≤0.05显著性水平下，根据疾病严重程度和基因型交互作用的方差被识别。广义遗传力分数按照所述方法计算。

。

Molecular marker analysis

分子标记分析

SNP markers were determined using DArT analysis (Diversity Arrays Technology Pty. Ltd., Canberra, Australia). Extracted DNA was cut with

使用DArT分析（Diversity Arrays Technology Pty. Ltd.，堪培拉，澳大利亚）确定SNP标记。提取的DNA被切割

Pst

密码

I-

我-

Mse

鼠标

I enzymes and ligated to adapters compatible with these enzymes as described previously

我酶并连接到与这些酶兼容的适配器，如前所述

. PCR and adapter ligation were performed following established protocols

按照既定协议进行了PCR和接头连接。

. Sequencing was conducted using Illumina HiSeq 2000 (Illumina Inc., USA).

. 测序使用Illumina HiSeq 2000（Illumina Inc.，美国）进行。

Population structure and genome-wide association mapping

种群结构和全基因组关联分析

The raw SNP data obtained from sequencing were filtered based on a 95% call rate and a minor allele frequency (MAF) greater than 5%. Subsequently, the population structure was determined using STRUCTURE software to identify groups within the population that exhibited discriminant allele frequencies.

测序获得的原始SNP数据根据95%的检出率和次等位基因频率（MAF）大于5%进行了过滤。随后，使用STRUCTURE软件确定群体结构，以识别等位基因频率具有差异的群体内组别。

The number of groups in the population is indicated by the K value, which is defined as the allele frequencies at each locus. For every group, a range of 1 to 10 was calculated to find the most favorable K value. Ten replicates were analyzed for every K value, and 50,000 Markov Chain Monte Carlo (MCMC) replicates were performed for the burn-in length and burn-in period.

群体中的组数由K值表示，K值定义为每个位点的等位基因频率。对于每个组，计算了1到10的范围以找到最合适的K值。对每个K值进行了十次重复分析，并执行了50,000次马尔可夫链蒙特卡罗（MCMC）重复用于燃烧长度和燃烧周期。

The STRUCTURE HARVESTER.

结构收集器。

software was utilized to determine the ΔK value with the highest probability for every K value that was obtained.

软件被用来确定每个获得的K值所对应的最高概率的ΔK值。

The association between SNP markers and resistance of maize genotypes to

SNP标记与玉米基因型抗性之间的关联

兆帕

was determined in the TASSEL software

是在TASSEL软件中确定的

. For this purpose, the significance levels of the relationship between phenotypic data, marker data, and Q matrix, which represents the population structure, were analyzed with TASSEL software. The Mixed Linear Model (MLM) model was employed in this study to minimize false positives by integrating population structure and genetic relationships.

为此，使用TASSEL软件分析了表型数据、标记数据与代表群体结构的Q矩阵之间关系的显著性水平。本研究采用了混合线性模型（MLM）以通过整合群体结构和遗传关系来尽量减少假阳性。

It utilizes the Q matrix for population adjustments and the K matrix for genetic linkage, resulting in enhanced accuracy in the analysis.

它利用Q矩阵进行群体调整，利用K矩阵进行遗传连锁，从而提高了分析的准确性。

. FDR (False Discovery Rate) is a method used to control the proportion of false positive results in statistical testing

FDR（错误发现率）是一种用于控制统计检验中假阳性结果比例的方法。

. The FDR correction threshold was calculated to minimize the likelihood of detecting false positive SNPs

FDR校正阈值的计算旨在最小化检测到假阳性SNP的可能性。

. This approach enables a more accurate identification of significant SNPs while maintaining the integrity of the analysis. When FDR Correction was exceeded, SNP markers were considered statistically significant. The visual representation of these markers exceeding the FDR threshold line was drawn using Manhattan blocks.

这种方法能够在保持分析完整性的同时，更准确地识别显著的SNPs。当超出FDR校正阈值时，SNP标记被认为具有统计学显著性。这些超过FDR阈值线的标记的可视化表示是使用曼哈顿图绘制的。

In order to visualize the relationship between observed and expected phenotypic data and P values, quantile-quantile (Q-Q) plots were also drawn.

为了可视化观察到的与预期的表型数据及P值之间的关系，还绘制了分位数-分位数（Q-Q）图。

。

Candidate genes

候选基因

SNP markers linked to

与...连锁的SNP标记

兆帕

in maize were examined using Sequence Viewer 3.49.0 on the National Center for Biotechnology (NCBI) database to identify potential genes. Analysis of candidate genes was carried out 100 K upstream and 100 K downstream of the marker’s positions.

使用国家生物技术信息中心（NCBI）数据库的Sequence Viewer 3.49.0对玉米中的序列进行了分析，以识别潜在基因。候选基因的分析是在标记位置上游100K和下游100K范围内进行的。

Data availability

数据可用性

The data generated from the study will be provided by the corresponding author upon request.

研究生成的数据将由通讯作者在请求时提供。

References

参考文献

del Molina, M., Naranjo, C. A. & C. & Cytogenetic studies in the genus Zea.

德尔莫利纳，M.，纳兰霍，C. A. & C. & 玉米属的细胞遗传学研究。

Theor. Appl. Genet.

理论与应用遗传学

, 542–550 (1987).

，542-550页（1987年）。

PubMed

Google Scholar

谷歌学术

Haberer, G. et al. Structure and architecture of the maize genome.

哈贝雷尔，G. 等。玉米基因组的结构与架构。

Plant Physiol.

植物生理学。

139

一百三十九

, 1612–1624 (2005).

，1612-1624（2005）。

CAS

中国科学院

PubMed

PubMed Central

MATH

数学

Google Scholar

谷歌学术

Kehinde, A. D., Ojo, T. O. & Ogundeji, A. A. Impact of participation in social capital networks on the technical efficiency of maize producers in Southwest Nigeria.

Kehinde, A. D., Ojo, T. O. & Ogundeji, A. A. 参与社会资本网络对尼日利亚西南部玉米生产者技术效率的影响。

Agric. Food Secur.

农业与粮食安全

, 12 (2024).

，12（2024）。

Google Scholar

谷歌学术

Mishra, M., Sharma, S. & Sharma, R. Corn (

米什拉，M.，夏尔马，S. & 夏尔马，R. 玉米 (

Zea mays

玉米

) as a nutrient source and diet: a review.

）作为营养源和饮食：综述。

J. Pharm. Res. Int.

国际药物研究杂志

, 299–303 (2021).

，299-303页（2021年）。

MATH

数学

Google Scholar

谷歌学术索

FAO Statistical database - Food and Agriculture Organization of the United Nations, Rome Italy (2024).

联合国粮食及农业组织统计数据库 - 联合国粮食及农业组织，意大利罗马（2024）。

Kaur, S. et al. Emerging phytopathogen

考尔，S. 等。新兴植物病原体

Macrophomina phaseolina

大丽轮枝菌

: Biology, economic importance and current diagnostic trends.

生物学、经济重要性及当前诊断趋势。

Crit. Rev. Microbiol.

微生物学评论

, 136–151 (2012).

，136-151页（2012年）。

CAS

中国科学院

PubMed

MATH

数学

Google Scholar

谷歌学术

Ahmed, M. J. & Shoaib, A. Unveiling the biocontrol potential of

艾哈迈德，M. J. 和舒艾卜，A. 揭示生物防治潜力

Pseudomonas syringae

丁香假单胞菌

through seed biopriming against charcoal rot disease in maize.

通过种子生物引发对抗玉米炭疽病。

Physiol. Mol. Plant Pathol.

植物生理与分子病理学

133

, 102370 (2024).

，102370（2024）。

CAS

中国科学院

Google Scholar

谷歌学术

Baird, R. E., Watson, C. E. & Scruggs, M. Relative longevity of

贝尔德，R. E.，沃森，C. E. & 斯克鲁格斯，M. 相对寿命

Macrophomina phaseolina

大丽轮枝菌

and associated mycobiota on residual soybean roots in soil.

并关联土壤中残留大豆根部的真菌群落。

Plant Dis.

植物病害。

, 563–566 (2003).

，563-566页（2003年）。

PubMed

Google Scholar

谷歌学术

Khalili, E. et al. Evaluation of Trichoderma isolates as potential biological control agent against soybean charcoal rot disease caused by

Khalili, E. 等。评估木霉分离株作为潜在生物防治剂对抗由大豆炭疽病引起的病害

Macrophomina phaseolina

大丽轮枝菌

。

Biotechnol. Biotechnol. Equip.

生物技术。生物技术设备。

, 479–488 (2016).

，479-488页（2016年）。

MathSciNet

数学评论

CAS

中国科学院

Google Scholar

谷歌学术

Marquez, N., Giachero, M. L., Declerck, S. & Ducasse, D. A.

马奎兹，N.，吉亚切罗，M. L.，德克莱尔克，S.，杜卡斯，D. A.

Macrophomina phaseolina

大丽轮枝菌

: General characteristics of pathogenicity and methods of control.

：致病性的一般特征及控制方法。

Front. Plant Sci.

植物科学前沿

, 634397 (2021).

，634397（2021）。

PubMed

PubMed Central

MATH

数学

Google Scholar

谷歌学术

Jordaan, E., van der Waals, J. E. & McLaren, N. W. Effect of irrigation on charcoal rot severity, yield loss and colonization of soybean and sunflower.

乔达安，E.，范德瓦尔斯，J. E.，麦克拉伦，N. W. 灌溉对炭疽病严重程度、产量损失及大豆和向日葵的定殖影响。

Crop Prot.

作物保护

122

, 63–69 (2019).

，63-69页（2019年）。

Google Scholar

谷歌学术索

Kendig, S. R., Rupe, J. C. & Scott, H. D. Effect of,rrigation and soil water stress on densities of

肯迪格，S. R.，鲁普，J. C.，斯科特，H. D. 灌溉和土壤水分胁迫对密度的影响

Macrophomina phaseolina

大丽轮枝菌

in soil and roots of two soybean cultivars.

在两种大豆栽培品种的土壤和根系中。

Plant Dis.

植物病害

, 895–900 (2000).

，895-900页（2000年）。

CAS

中国科学院

PubMed

Google Scholar

谷歌学术索

Pawlowski, M. L., Bowen, C. R., Hill, C. B. & Hartman, G. L. Responses of soybean genotypes to pathogen infection after the application of elicitors.

帕沃斯基，M. L.，鲍恩，C. R.，希尔，C. B.，哈特曼，G. L. 大豆基因型在激发子施用后对病原体感染的反应。

Crop Prot.

作物保护

, 78–84 (2016).

，78-84页（2016年）。

CAS

中国科学院

MATH

数学

Google Scholar

谷歌学术

Lango Allen, H. et al. Hundreds of variants clustered in genomic loci and biological pathways affect human height.

Lango Allen, H. 等。数百种变异聚集在基因组位点和生物通路中，影响人类身高。

Nature

自然

467

, 832–838 (2010).

，832-838页（2010年）。

ADS

CAS

中国科学院

PubMed

PubMed Central

MATH

数学

Google Scholar

谷歌学术索

Guo, Z. et al. Complex Genetic System involved in Fusarium ear rot resistance in Maize as revealed by GWAS, Bulked Sample Analysis, and genomic prediction.

郭，Z. 等。通过GWAS、混合样本分析和基因组预测揭示的与玉米镰刀菌穗腐病抗性相关的复杂遗传系统。

Plant Dis.

植物病害。

104

, 1725–1735 (2020).

，1725–1735（2020）。

CAS

中国科学院

PubMed

MATH

数学

Google Scholar

谷歌学术索

Warburton, M. L. et al. Comparative analysis of multiple GWAS results identifies metabolic pathways associated with resistance to

Warburton, M. L. 等。对多个GWAS结果的比较分析确定了与抗性相关的代谢通路

A. flavus

黄曲霉

infection and aflatoxin accumulation in maize.

感染和黄曲霉毒素在玉米中的积累。

Toxins

毒素

, 738 (2022).

，738页（2022年）。

CAS

中国科学院

PubMed

PubMed Central

Google Scholar

谷歌学术

Hou, M. et al. Genome-wide association study of maize resistance to

侯，M. 等。玉米抗性全基因组关联研究

Pythium aristosporum

尖孢腐霉

stalk rot.

茎腐病。

Front. Plant Sci.

植物科学前沿

, 1239635 (2023).

，1239635（2023）。

PubMed

PubMed Central

Google Scholar

谷歌学术索

Zhao, M. et al. Identification of genetic loci associated with rough dwarf disease resistance in maize by integrating GWAS and linkage mapping.

赵，M. 等。通过整合GWAS和连锁作图鉴定与玉米粗矮病抗性相关的遗传位点。

Plant Sci.

植物科学

315

, 111100 (2022).

，111100（2022）。

CAS

中国科学院

PubMed

MATH

数学

Google Scholar

谷歌学术

Washburn, J. D. et al. GWAS analysis of maize host plant resistance to western corn rootworm (Coleoptera: Chrysomelidae) reveals candidate small effect loci for resistance breeding.

沃什伯恩，J. D. 等。玉米宿主植物对西方玉米根虫（鞘翅目：叶甲科）抗性的GWAS分析揭示了抗性育种的候选小效应位点。

J. Econ. Entomol.

经济昆虫学杂志

116

, 2184–2192 (2023).

，2184-2192（2023）。

CAS

中国科学院

PubMed

MATH

数学

Google Scholar

谷歌学术

Jaccoud, D., Peng, K., Feinstein, D. & Kilian, A. Diversity arrays: A solid state technology for sequence information independent genotyping.

Jaccoud, D., Peng, K., Feinstein, D. & Kilian, A. 多样性阵列：一种不依赖序列信息的固态基因分型技术。

Nucleic Acids Res.

核酸研究

, e25–e25 (2001).

，e25–e25（2001）。

CAS

中国科学院

PubMed

PubMed Central

Google Scholar

谷歌学术

Wen, J. et al. Association mapping of major economic traits and exploration of elite alleles in

温杰等。主要经济性状的关联分析及优良等位基因的挖掘

Prunus sibirica

西伯利亚杏

。

Euphytica

育种学

219

, 1–13 (2023).

，1–13（2023）。

Google Scholar

谷歌学术索

Mengistu, A., Smith, J. R., Ray, J. D. & Bellaloui, N. Seasonal progress of charcoal rot and its impact on soybean productivity.

门吉斯特，A.，史密斯，J. R.，雷，J. D.，贝拉卢伊，N. 木炭腐烂的季节性进展及其对大豆生产力的影响。

Plant Dis.

植物病害

, 1159–1166 (2011).

，1159-1166（2011）。

PubMed

MATH

数学

Google Scholar

谷歌学术

Ruzmetov, D. R., Sherimbetov, A. G. & Adilov, B. S. First report of

鲁兹梅托夫，D. R.，谢林贝托夫，A. G. & 阿迪洛夫，B. S. 首次报告

Macrophomina phaseolina

大丽轮枝菌

causing сharcoal rot in soybean (

导致大豆炭腐病 (

Glycine max

大豆

(L.) Merr.) plants in Uzbekistan.

乌方的(L.) Merr.)植物。

Plant Dis.

植物病害。

, 108 (2024).

，108（2024）。

Google Scholar

谷歌学术索

Gaetán, S. A., Fernandez, L. & Madia, M. Occurrence of charcoal rot caused by

盖坦、S.A.、费尔南德斯、L. 和马迪亚、M. 木炭腐烂的发生由

Macrophomina phaseolina

大丽轮枝菌

on canola in Argentina.

阿根廷的油菜籽。

Plant Dis.

植物病害。

, 524 (2006).

，524页（2006年）。

PubMed

Google Scholar

谷歌学术

Mahmoud, A. F., Abou-Elwafa, S. F. & Shehzad, T. Identification of charcoal rot resistance QTLs in sorghum using association and in silico analyses.

马哈茂德，A. F.，阿布-埃尔瓦法，S. F. & 谢扎德，T. 使用关联和计算机模拟分析鉴定高粱中炭疽病抗性QTL。

J. Appl. Genet.

应用遗传学杂志

, 243–251 (2018).

，243-251页（2018年）。

PubMed

Google Scholar

谷歌学术

Mughogho, L. K. & Pande, S. Charcoal rot of sorghum (1983).

穆戈戈，L. K. 和潘德，S. 高粱炭疽病（1983）。

Mayek-PÉrez, N., GarcÍa-Espinosa, R., López-CastaÑeda, C., Acosta-Gallegos, J. A. & Simpson, J. Water relations, histopathology and growth of common bean (

Mayek-Pérez, N., GarcÍa-Espinosa, R., López-CastaÑeda, C., Acosta-Gallegos, J. A. & Simpson, J. 普通豆的水分关系、组织病理学和生长 (

Phaseolus vulgaris

普通菜豆

L.) during pathogenesis of

L.) 在发病机制期间

Macrophomina phaseolina

大丽轮枝菌

under drought stress.

在干旱胁迫下。

Physiol. Mol. Plant Pathol.

生理学与分子植物病理学

, 185–195 (2002).

，185-195页（2002年）。

Google Scholar

谷歌学术搜索

Zveibil, A., Mor, N., Gnayem, N. & Freeman, S. Survival, host-pathogen interaction, and management of

Zveibil, A., Mor, N., Gnayem, N. & Freeman, S. 存活、宿主-病原体相互作用及管理

Macrophomina phaseolina

大丽轮枝菌

on strawberry in Israel.

在以色列的草莓上。

Plant Dis.

植物病害。

, 265–272 (2012).

，265-272页（2012年）。

PubMed

Google Scholar

谷歌学术

Fuhlbohm, M. J., Ryley, M. J. & Aitken, E. A. B. Infection of mungbean seed by

富尔博姆，M. J.，莱利，M. J. & 艾特肯，E. A. B. 绿豆种子的感染

Macrophomina phaseolina

大丽轮枝菌

is more likely to result from localized pod infection than from systemic plant infection.

比起系统性植物感染，更可能由局部荚果感染导致。

Plant Pathol.

植物病理学。

, 1271–1284 (2013).

，1271–1284（2013）。

CAS

中国科学院

Google Scholar

谷歌学术

Adeyanju, A., Little, C., Yu, J. & Tesso, T. Genome-wide association study on resistance to stalk rot diseases in grain sorghum.

阿德亚努，A.，利特尔，C.，余，J.，特索，T. 高粱抗茎腐病的全基因组关联研究。

G3 Genes Genomes Genetics

G3 基因组学遗传学

, 1165–1175 (2015).

，1165-1175（2015）。

PubMed

PubMed Central

Google Scholar

谷歌学术搜索

Rashid, Z. et al. Identification and validation of genomic regions associated with charcoal rot resistance in tropical maize by genome-wide association and linkage mapping.

拉希德，Z. 等。通过全基因组关联和连锁定位鉴定与热带玉米炭疽病抗性相关的基因组区域并进行验证。

Front. Plant Sci.

植物科学前沿

, 1–13 (2021).

，1-13页（2021年）。

MATH

数学

Google Scholar

谷歌学术

Coser, S. M. et al. Genetic architecture of charcoal rot (

科瑟，S. M. 等。炭疽病的遗传结构 (

Macrophomina phaseolina

大丽轮枝菌

) resistance in soybean revealed using a diverse panel.

) 大豆中的抗性通过多样化面板揭示。

Front. Plant Sci.

植物科学前沿

, 1–12 (2017).

，1-12页（2017年）。

ADS

MATH

数学

Google Scholar

谷歌学术

Cappa, E. P. et al. Impacts of population structure and analytical models in genome-wide association studies of complex traits in forest trees: a case study in

Cappa, E. P. 等。群体结构和分析模型对森林树木复杂性状全基因组关联研究的影响：一项案例研究

Eucalyptus globulus

蓝桉

。

PLoS ONE

, e81267 (2013).

，e81267（2013）。

ADS

PubMed

PubMed Central

MATH

数学

Google Scholar

谷歌学术索

Vinholes, P., Rosado, R., Roberts, P., Borém, A. & Schuster, I. Single nucleotide polymorphism-based haplotypes associated with charcoal rot resistance in Brazilian soybean germplasm.

Vinhole, P., Rosado, R., Roberts, P., Borém, A. & Schuster, I. 基于单核苷酸多态性的单倍型与巴西大豆种质中炭疽病抗性相关。

Agron. J.

农学杂志

111

, 182–192 (2019).

，182-192页（2019年）。

CAS

中国科学院

Google Scholar

谷歌学术

Gu, X. et al. Genome-wide association of single nucleotide polymorphism loci and candidate genes for frogeye leaf spot (

顾晓燕等。单核苷酸多态性位点和候选基因的全基因组关联分析与蛙眼叶斑病相关

Cercospora sojina

大豆尾孢菌

) resistance in soybean.

大豆中的抗性。

BMC Plant Biol.

BMC植物生物学。

, 588 (2021).

，588页（2021年）。

CAS

中国科学院

PubMed

PubMed Central

MATH

数学

Google Scholar

谷歌学术索

Broglie, K. E., Biddle, P., Cressman, R. & Broglie, R. Functional analysis of DNA sequences responsible for ethylene regulation of a bean chitinase gene in transgenic tobacco.

Broglie, K. E., Biddle, P., Cressman, R. & Broglie, R. 转基因烟草中负责乙烯调控豆类几丁质酶基因的DNA序列功能分析。

Plant Cell.

植物细胞。

, 599–607 (1989).

，599-607页（1989年）。

CAS

中国科学院

PubMed

PubMed Central

MATH

数学

Google Scholar

谷歌学术

Chowdhury, S., Basu, A. & Kundu, S. Biotrophy-necrotrophy switch in pathogen evoke differential response in resistant and susceptible sesame involving multiple signaling pathways at different phases.

乔杜里，S.，巴苏，A. & 昆杜，S. 生物营养-坏死营养转换在病原体引发抗性与感病芝麻的差异反应涉及多个信号通路在不同阶段。

Sci. Rep.

科学报告

, 17251 (2017).

，17251（2017）。

ADS

PubMed

PubMed Central

Google Scholar

谷歌学术索

Gaige, A. R., Ayella, A. & Shuai, B. Methyl jasmonate and ethylene induce partial resistance in

改革，A. R.，艾耶拉，A. & 帅，B. 茉莉酸甲酯和乙烯诱导部分抗性在

Medicago truncatula

蒺藜苜蓿

against the charcoal rot pathogen

对抗炭疽病病原体

Macrophomina phaseolina

大丽轮枝菌

。

Physiol. Mol. Plant Pathol.

植物生理学与分子植物病理学

, 412–418 (2010).

，412-418页（2010年）。

CAS

中国科学院

Google Scholar

谷歌学术

Shirai, M. & Eulgem, T. Molecular interactions between the soilborne pathogenic fungus

白井，M. & Eulgem，T. 土壤传播的致病真菌与分子间的相互作用

Macrophomina phaseolina

大丽轮枝菌

and its host plants.

及其寄主植物。

Front. Plant Sci.

植物科学前沿

, 1264569 (2023).

，1264569（2023）。

PubMed

PubMed Central

MATH

数学

Google Scholar

谷歌学术搜索

Kim, S. J., Held, M. A., Zemelis, S., Wilkerson, C. & Brandizzi, F. CGR2 and CGR3 have critical overlapping roles in pectin methylesterification and plant growth in

Kim, S. J., Held, M. A., Zemelis, S., Wilkerson, C. & Brandizzi, F. CGR2 和 CGR3 在果胶甲酯化和植物生长中具有至关重要的重叠作用。

Arabidopsis thaliana

拟南芥

。

Plant J.

植物杂志

, 208–220 (2015).

，208-220页（2015年）。

CAS

中国科学院

PubMed

Google Scholar

谷歌学术

Weraduwage, S. M. et al. Pectin methylesterification impacts the relationship between photosynthesis and plant growth.

Weraduwage, S. M. 等。果胶甲酯化影响光合作用与植物生长的关系。

Plant Physiol.

植物生理学。

171

, 833–848 (2016).

，833-848页（2016年）。

CAS

中国科学院

MATH

数学

Google Scholar

谷歌学术

Marino, D., Peeters, N. & Rivas, S. Ubiquitination during plant immune signaling.

马里诺，D.，彼得斯，N. & 里瓦斯，S. 植物免疫信号传导期间的泛素化。

Plant Physiol.

植物生理学。

160

, 15–27 (2012).

，15-27页（2012年）。

CAS

中国科学院

PubMed

PubMed Central

Google Scholar

谷歌学术

Coculo, D. et al. Arabidopsis subtilases promote defense-related pectin methylesterase activity and robust immune responses to botrytis infection.

Coculo, D. 等。拟南芥中的枯草杆菌蛋白酶促进防御相关的果胶甲酯酶活性以及对灰霉菌感染的强免疫反应。

Plant Physiol. Biochem.

植物生理学与生物化学

201

, 107865 (2023).

，107865（2023）。

CAS

中国科学院

PubMed

MATH

数学

Google Scholar

谷歌学术

Guo, Y. H. et al. GhZFP1, a novel CCCH-type zinc finger protein from cotton, enhances salt stress tolerance and fungal disease resistance in transgenic tobacco by interacting with GZIRD21A and GZIPR5.

郭亚华等。GhZFP1，一种来自棉花的新型CCCH型锌指蛋白，通过与GZIRD21A和GZIPR5相互作用，增强转基因烟草的盐胁迫耐受性和真菌病害抗性。

New Phytol.

新植物学家。

183

, 62–75 (2009).

，62-75页（2009年）。

CAS

中国科学院

PubMed

MATH

数学

Google Scholar

谷歌学术

Gupta, S. K., Rai, A. K., Kanwar, S. S. & Sharma, T. R. Comparative analysis of zinc finger proteins involved in plant disease resistance.

古普塔，S.K.，赖，A.K.，康瓦尔，S.S.，夏尔马，T.R. 植物抗病相关的锌指蛋白的比较分析。

PLoS ONE

, e42578 (2012).

，e42578（2012）。

ADS

CAS

中国科学院

PubMed

PubMed Central

MATH

数学

Google Scholar

谷歌学术

Schuler, M. A. & Werck-Reichhart, D. Functional genomics of P450s.

Schuler, M. A. & Werck-Reichhart, D. P450s的功能基因组学。

Annu. Rev. Plant Biol.

植物生物学年度评论

, 629–667 (2003).

，629-667页（2003年）。

CAS

中国科学院

PubMed

MATH

数学

Google Scholar

谷歌学术索

Lannoo, N. & Van Damme, E. J. M. Lectin domains at the frontiers of plant defense.

兰诺，N. & 范达姆，E. J. M. 植物防御前沿的凝集素结构域。

Front. Plant Sci.

植物科学前沿

, 397 (2014).

，397页（2014年）。

PubMed

PubMed Central

MATH

数学

Google Scholar

谷歌学术

Talapov, T. Determination of sunflower (

塔拉波夫，T. 向日葵的测定 (

Helianthus annuus

向日葵

) ve soybean (

) 和大豆 (

Glycine max

大豆

) variety reactions to

) 多种反应

Macrophomina phaseolina

大丽轮枝菌

and characterization of the agent.

以及对该因素的特性描述。

Master’s Thesis, Gaziantep University

硕士学位论文，加济安泰普大学

(2020).

（2020）。

Twizeyimana, M., Hill, C. B., Pawlowski, M., Paul, C. & Hartman, G. L. A cut-stem inoculation technique to evaluate soybean for resistance to

特维泽伊马纳，M.，希尔，C. B.，帕沃斯基，M.，保罗，C.，哈特曼，G. L. 一种切割茎接种技术用于评估大豆抗性

Macrophomina Phaseolina

大丽轮枝菌

。

Plant Dis.

植物病害

, 1210–1215 (2012).

，1210-1215（2012）。

CAS

中国科学院

PubMed

Google Scholar

谷歌学术

Townsend, G. K. & Heuberger, J. W. Methods for estimating losses caused by diseases in fungicide experiments.

Townsend, G. K. & Heuberger, J. W. 估算杀菌剂试验中病害所致损失的方法。

Plant Dis. Rep.

植物病害报道

, 340–343 (1943).

，340-343页（1943年）。

CAS

中国科学院

MATH

数学

Google Scholar

谷歌学术索

Ma, L. et al. GWAS with a PCA uncovers candidate genes for accumulations of microelements in maize seedlings.

马立群等。GWAS结合PCA分析揭示了玉米幼苗中微量元素积累的候选基因。

Physiol. Plant

植物生理学

172

, 2170–2180 (2021).

，2170-2180（2021）。

CAS

中国科学院

PubMed

MATH

数学

Google Scholar

谷歌学术搜索

Erdogmus, S. et al. Genome-wide association studies of ca and mn in the seeds of the common bean (

埃尔多格穆斯，S. 等。全基因组关联研究关于普通豆种子中的钙和锰含量（

Phaseolus vulgaris L.

普通菜豆

）。

Genomics

基因组学

112

, 4536–4546 (2020).

，4536–4546（2020）。

CAS

中国科学院

PubMed

MATH

数学

Google Scholar

谷歌学术

Kilian, A. et al. Diversity arrays technology: A generic genome profiling technology on open platforms.

Kilian, A. 等。多样性阵列技术：开放平台上的通用基因组分析技术。

Methods Mol. Biol.

分子生物学方法

888

, 67–89 (2012).

，67-89页（2012年）。

PubMed

MATH

数学

Google Scholar

谷歌学术

Earl, D. A. & VonHoldt, B. M. Structure harvester: A website and program for visualizing STRUCTURE output and implementing the Evanno method.

Earl, D. A. & VonHoldt, B. M. Structure Harvester：一个用于可视化STRUCTURE输出并实施Evanno方法的网站和程序。

Conserv. Genet. Resour.

保护遗传学资源

, 359–361 (2012).

，359-361页（2012年）。

Google Scholar

谷歌学术索

Bradbury, P. J. et al. TASSEL: Software for association mapping of complex traits in diverse samples.

布拉德伯里，P. J. 等。TASSEL：用于在多样化样本中进行复杂性状关联分析的软件。

Bioinformatics

生物信息学

, 2633–2635 (2007).

，2633–2635页（2007年）。

CAS

中国科学院

PubMed

MATH

数学

Google Scholar

谷歌学术

Karaca, N. et al. Association mapping of magnesium and manganese concentrations in the seeds of C. Arietinum and C. Reticulatum.

卡拉贾，N. 等。C. Arietinum 和 C. Reticulatum 种子中镁和锰浓度的关联分析。

Genomics

基因组学

112

, 1633–1642 (2020).

，1633–1642（2020）。

CAS

中国科学院

PubMed

MATH

数学

Google Scholar

谷歌学术

Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing.

Benjamini, Y. & Hochberg, Y. 控制错误发现率：一种实用且强大的多重检验方法。

J. R. Stat. Soc. Ser. B

英国皇家统计学会期刊B辑

, 289–300 (1995).

，289-300页（1995年）。

MathSciNet

数学评论

MATH

数学

Google Scholar

谷歌学术

Karaca, N. et al. Genome-wide association studies of protein, lutein, vitamin c, and fructose concentration in wild and cultivated chickpea seeds.

Karaca, N. 等。野生和栽培鹰嘴豆种子中蛋白质、叶黄素、维生素C和果糖浓度的全基因组关联研究。

Crop Sci.

作物科学

, 2652–2666 (2019).

，2652-2666（2019）。

CAS

中国科学院

MATH

数学

Google Scholar

谷歌学术

Download references

下载参考资料

Acknowledgements

致谢

We gratefully acknowledge the Scientific and Technological Research Council of Türkiye for their support, under grant number 121O537.

我们衷心感谢土耳其科学技术研究委员会的支持，项目编号为121O537。

Author information

作者信息

Authors and Affiliations

作者与所属机构

Department of Bioengineering, Ege University, Izmir, Turkey

土耳其伊兹密尔埃格大学生物工程系

Gizem Oder, Muhammed Bahattin Tanyolac & Duygu Ates

吉泽姆·奥德，穆罕默德·巴哈丁·塔尼奥拉克，杜伊古·阿特斯

Phytopathology Department, Biological Control Research Institute, Adana, Turkey

植物病理学系，生物防治研究所，阿达纳，土耳其

Semiha Yuceer

半月·尤切希尔

Department of Biology, Gaziantep University, Gaziantep, Turkey

土耳其加济安泰普大学生物系

Canan Can

卡南·詹

Authors

作者

Gizem Oder

吉泽姆·奥德爾

View author publications

查看作者的出版物

You can also search for this author in

您还可以搜索此作者在

PubMed

Google Scholar

谷歌学术

Semiha Yuceer

半哈·尤切希尔

View author publications

查看作者出版物

You can also search for this author in

您还可以搜索此作者在

PubMed

Google Scholar

谷歌学术

Canan Can

卡南·詹

View author publications

查看作者的出版物

You can also search for this author in

您还可以搜索此作者在

PubMed

Google Scholar

谷歌学术索

Muhammed Bahattin Tanyolac

穆罕默德·巴哈丁·坦尤拉克

View author publications

查看作者的出版物

You can also search for this author in

您还可以搜索此作者在

PubMed

Google Scholar

谷歌学术索

Duygu Ates

杜伊古·阿特斯

View author publications

查看作者的出版物

You can also search for this author in

您还可以搜索此作者在

PubMed

Google Scholar

谷歌学术索

Contributions

贡献

G.O. Bioinformatic analysis, writing manuscript; S.Y. collection of Mp pathogens and determination of resistance reaction of genotypes to Mp; C.C. Collection of pathogens; M.B.T. GWAS analysis, principal investigator; D.A. Corresponding author, GWAS analysis, Bioinformatic analysis.

G.O. 生物信息学分析，撰写手稿；S.Y. 收集Mp病原体并确定基因型对Mp的抗性反应；C.C. 病原体收集；M.B.T. GWAS分析，主要研究者；D.A. 通讯作者，GWAS分析，生物信息学分析。

Corresponding author

通讯作者

Correspondence to

联系方式

Duygu Ates

杜伊古·阿特斯

。

Ethics declarations

伦理声明

Competing interests

竞争利益

The authors declare no competing interests.

作者声明不存在竞争性利益。

Additional information

附加信息

Publisher’s note

出版商说明

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Springer Nature 对已发布地图中的管辖权声明和机构隶属关系保持中立。

Electronic supplementary material

电子补充材料

Below is the link to the electronic supplementary material.

以下是电子补充材料的链接。

Supplementary Material 1

补充材料1

Rights and permissions

权利与许可

Open Access

开放获取

This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made.

本文根据知识共享署名4.0国际许可证获得许可，该许可证允许您在任何媒介或格式中使用、分享、改编、分发和复制，只要您对原作者和来源给予适当的署名，提供知识共享许可证的链接，并说明是否进行了修改。

The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.

本文中的图像或其他第三方材料包含在文章的Creative Commons许可证中，除非材料的信用标线另有说明。如果材料未包含在文章的Creative Commons许可证中，且您的预期用途未被法律规定允许或超出了允许的使用范围，您需要直接从版权持有人处获得许可。

To view a copy of this licence, visit .

要查看此许可证的副本，请访问。

http://creativecommons.org/licenses/by/4.0/

。

Reprints and permissions

重印和许可

About this article

关于本文

Cite this article

引用本文

Oder, G., Yuceer, S., Can, C.