Tetraploid wheats (Triticum turgidum L.), including durum wheat (T. turgidum ssp. durum (Desf.) Husn.), are important crops with high nutritional and cultural values. However, their production is constrained by sensitivity to environmental conditions. In search of adaptive genetic signatures tracing historical selection and hybridization events, we performed genome scans on two datasets: (1) Durum Global Diversity Panel comprising a total of 442 tetraploid wheat and wild progenitor accessions including durum landraces (n = 286), domesticated emmer (T. turgidum ssp. dicoccum (Schrank) Thell.; n = 103) and wild emmer (T. turgidum ssp. dicoccoides (Korn. ex Asch. & Graebn.) Thell.; n = 53) wheats genotyped using the 90K single nucleotide polymorphism (SNP) array, and (2) a second dataset comprising a total 121 accessions of nine T. turgidum subspecies including wild emmer genotyped with >100 M SNPs from whole-genome resequencing. The genome scan on the first dataset detected six outlier loci on chromosomes 1A, 1B, 3A (n = 2), 6A, and 7A. These loci harbored important genes for adaptation to abiotic stresses, phenological responses, such as seed dormancy, circadian clock, flowering time, and key yield-related traits, including pleiotropic genes, such as HAT1, KUODA1, CBL1, and ZFN1. The scan on the second dataset captured a highly differentiated region on chromosome 2B that shows significant differentiation between two groups: one group consists of Georgian (T. turgidum ssp. paleocolchicum A. Love & D. Love) and Persian (T. turgidum ssp. carthlicum (Nevski) A. Love & D. Love) wheat accessions, while the other group comprises all the remaining tetraploids including wild emmer. This is consistent with a previously reported introgression in this genomic region from T. timopheevii Zhuk. which naturally cohabit in the Georgian and neighboring areas. This region harbored several adaptive genes, including the thermomorphogenesis gene PIF4, which confers temperature-resilient disease resistance and regulates other biological processes. Genome scans can be used to fast-track germplasm housed in gene banks and in situ; which helps to identify environmentally resilient accessions for breeding and/or to prioritize them for conservation.
四倍体小麦(Triticum turgidum L.),包括硬粒小麦(T. turgidum ssp.)。硬质(Desf)。是具有高营养和文化价值的重要作物。然而,它们的生产受到对环境条件的敏感性的限制。为了寻找追踪历史选择和杂交事件的适应性遗传特征,我们对两个数据集进行了基因组扫描:(1)硬粒小麦全球多样性小组,包括442个四倍体小麦和野生祖先,包括硬粒小麦地方品种(n = 286)、驯化二粒小麦(T. turgidum ssp);dicoccum(名词);n = 103)和野生二聚体(T. turgidum ssp.)。dicoccoides(科恩。Asch交货。& Graebn)。Thell。n = 53)小麦,使用90K单核苷酸多态性(SNP)阵列进行基因分型;(2)第二个数据集包括9个T. turgidum亚种共121个,包括野生emmer,通过全基因组重测序获得bbb100 M SNP基因分型。对第一个数据集进行基因组扫描,在1A、1B、3A (n = 2)、6A和7A染色体上检测到6个异常位点。这些基因座包含了适应非生物胁迫、物候反应(如种子休眠、生物钟、开花时间)和关键产量相关性状的重要基因,包括多效基因(如HAT1、KUODA1、CBL1和ZFN1)。对第二个数据集的扫描捕获了2B染色体上高度分化的区域,显示了两组之间的显著分化:一组由格鲁吉亚(T. turgidum ssp)组成。古冷chicum A. Love和D. Love)和波斯语(T. turgidum ssp.)。carthlicum (Nevski) A. Love & D. Love)小麦品种,而另一组包括所有剩余的四倍体,包括野生二倍体。这与先前报道的timopheevi Zhuk在该基因组区域的渐渗一致。它们自然地生活在格鲁吉亚和邻近地区。该区域包含几个适应性基因,包括温度形态发生基因PIF4,该基因赋予温度抗逆性疾病抗性并调节其他生物过程。基因组扫描可用于快速追踪基因库和原位保存的种质;这有助于确定环境适应性强的物种进行繁殖和/或优先保护。
{"title":"Genome scans capture key adaptation and historical hybridization signatures in tetraploid wheat.","authors":"Demissew Sertse, Jemanesh K Haile, Ehsan Sari, Valentyna Klymiuk, Amidou N'Diaye, Curtis J Pozniak, Sylvie Cloutier, Sateesh Kagale","doi":"10.1002/tpg2.20410","DOIUrl":"10.1002/tpg2.20410","url":null,"abstract":"<p><p>Tetraploid wheats (Triticum turgidum L.), including durum wheat (T. turgidum ssp. durum (Desf.) Husn.), are important crops with high nutritional and cultural values. However, their production is constrained by sensitivity to environmental conditions. In search of adaptive genetic signatures tracing historical selection and hybridization events, we performed genome scans on two datasets: (1) Durum Global Diversity Panel comprising a total of 442 tetraploid wheat and wild progenitor accessions including durum landraces (n = 286), domesticated emmer (T. turgidum ssp. dicoccum (Schrank) Thell.; n = 103) and wild emmer (T. turgidum ssp. dicoccoides (Korn. ex Asch. & Graebn.) Thell.; n = 53) wheats genotyped using the 90K single nucleotide polymorphism (SNP) array, and (2) a second dataset comprising a total 121 accessions of nine T. turgidum subspecies including wild emmer genotyped with >100 M SNPs from whole-genome resequencing. The genome scan on the first dataset detected six outlier loci on chromosomes 1A, 1B, 3A (n = 2), 6A, and 7A. These loci harbored important genes for adaptation to abiotic stresses, phenological responses, such as seed dormancy, circadian clock, flowering time, and key yield-related traits, including pleiotropic genes, such as HAT1, KUODA1, CBL1, and ZFN1. The scan on the second dataset captured a highly differentiated region on chromosome 2B that shows significant differentiation between two groups: one group consists of Georgian (T. turgidum ssp. paleocolchicum A. Love & D. Love) and Persian (T. turgidum ssp. carthlicum (Nevski) A. Love & D. Love) wheat accessions, while the other group comprises all the remaining tetraploids including wild emmer. This is consistent with a previously reported introgression in this genomic region from T. timopheevii Zhuk. which naturally cohabit in the Georgian and neighboring areas. This region harbored several adaptive genes, including the thermomorphogenesis gene PIF4, which confers temperature-resilient disease resistance and regulates other biological processes. Genome scans can be used to fast-track germplasm housed in gene banks and in situ; which helps to identify environmentally resilient accessions for breeding and/or to prioritize them for conservation.</p>","PeriodicalId":49002,"journal":{"name":"Plant Genome","volume":" ","pages":"e20410"},"PeriodicalIF":3.9,"publicationDate":"2025-03-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11726425/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"136399967","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-03-01Epub Date: 2024-11-27DOI: 10.1002/tpg2.20533
Marco Antônio Peixoto, Rodrigo Rampazo Amadeu, Leonardo Lopes Bhering, Luís Felipe V Ferrão, Patrício R Munoz, Márcio F R Resende
Selecting parents and crosses is a critical step for a successful breeding program. The ability to design crosses with high means that will maintain genetic variation in the population is the goal for long-term applications. Herein, we describe a new computational package for mate allocation in a breeding program. SimpleMating is a flexible and open-source R package originally designed to predict and optimize breeding crosses in crops with different reproductive systems and breeding designs. Divided into modules, SimpleMating first estimates the cross performance (criterion), such as mid-parental value, cross total genetic value, and/or usefulness of a set of crosses. The second module implements an optimization algorithm to maximize a target criterion while minimizing next-generation inbreeding. The software is flexible, enabling users to specify the desired number of crosses, set maximum and minimum crosses per parent, and define the maximum allowable parent relationship for creating crosses. As an outcome, SimpleMating generates a mating plan from the target parental population using single or multi-trait criteria. For example, we implemented and tested SimpleMating in a simulated maize breeding program obtained through stochastic simulations. The crosses designed via SimpleMating showed a large genetic mean over time (up to 22% more genetic gain than conventional genomic selection programs, with lesser loss of genetic diversity over time), supporting the use of this tool, as well as the use of data-driven decisions in breeding programs.
选择亲本和杂交种是成功育种计划的关键步骤。长期应用的目标是能够设计出维持种群遗传变异的高手段杂交。在此,我们将介绍一个用于育种计划中配偶分配的新计算软件包。SimpleMating 是一个灵活的开源 R 软件包,最初设计用于预测和优化具有不同生殖系统和育种设计的作物的杂交育种。SimpleMating 分成几个模块,首先估算杂交性能(标准),如中间亲本值、杂交总遗传值和/或一组杂交的有用性。第二个模块采用优化算法,在最大限度地提高目标标准的同时,最大限度地降低下一代近交率。该软件非常灵活,用户可以指定所需的杂交次数,设置每个亲本的最大和最小杂交次数,并定义创建杂交的最大允许亲本关系。其结果是,SimpleMating 会使用单性状或多性状标准从目标亲本群体中生成交配计划。例如,我们在通过随机模拟获得的模拟玉米育种计划中实施并测试了 SimpleMating。通过 SimpleMating 设计的杂交随着时间的推移显示出较大的遗传平均值(与传统的基因组选择程序相比,遗传增益高达 22%,随着时间的推移,遗传多样性的损失较小),支持使用这一工具,以及在育种计划中使用数据驱动决策。
{"title":"SimpleMating: R-package for prediction and optimization of breeding crosses using genomic selection.","authors":"Marco Antônio Peixoto, Rodrigo Rampazo Amadeu, Leonardo Lopes Bhering, Luís Felipe V Ferrão, Patrício R Munoz, Márcio F R Resende","doi":"10.1002/tpg2.20533","DOIUrl":"10.1002/tpg2.20533","url":null,"abstract":"<p><p>Selecting parents and crosses is a critical step for a successful breeding program. The ability to design crosses with high means that will maintain genetic variation in the population is the goal for long-term applications. Herein, we describe a new computational package for mate allocation in a breeding program. SimpleMating is a flexible and open-source R package originally designed to predict and optimize breeding crosses in crops with different reproductive systems and breeding designs. Divided into modules, SimpleMating first estimates the cross performance (criterion), such as mid-parental value, cross total genetic value, and/or usefulness of a set of crosses. The second module implements an optimization algorithm to maximize a target criterion while minimizing next-generation inbreeding. The software is flexible, enabling users to specify the desired number of crosses, set maximum and minimum crosses per parent, and define the maximum allowable parent relationship for creating crosses. As an outcome, SimpleMating generates a mating plan from the target parental population using single or multi-trait criteria. For example, we implemented and tested SimpleMating in a simulated maize breeding program obtained through stochastic simulations. The crosses designed via SimpleMating showed a large genetic mean over time (up to 22% more genetic gain than conventional genomic selection programs, with lesser loss of genetic diversity over time), supporting the use of this tool, as well as the use of data-driven decisions in breeding programs.</p>","PeriodicalId":49002,"journal":{"name":"Plant Genome","volume":" ","pages":"e20533"},"PeriodicalIF":3.9,"publicationDate":"2025-03-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11726409/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142741056","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-03-01Epub Date: 2024-07-23DOI: 10.1002/tpg2.20490
Yichen Kang, Samir Alahmad, Shanice V Haeften, Oluwaseun Akinlade, Jingyang Tong, Eric Dinglasan, Kai P Voss-Fels, Andries B Potgieter, Andrew K Borrell, Manar Makhoul, Christian Obermeier, Rod Snowdon, Emma Mace, David R Jordan, Lee T Hickey
Seminal root angle (SRA) is an important root architectural trait associated with drought adaptation in cereal crops. To date, all attempts to dissect the genetic architecture of SRA in durum wheat (Triticum durum Desf.) have used large association panels or structured mapping populations. Identifying changes in allele frequency generated by selection provides an alternative genetic mapping approach that can increase the power and precision of QTL detection. This study aimed to map quantitative trait loci (QTL) for SRA by genotyping durum lines created through divergent selection using a combination of marker-assisted selection (MAS) for the major SRA QTL (qSRA-6A) and phenotypic selection for SRA over multiple generations. The created 11 lines (BC1F2:5) were genotyped with genome-wide single-nucleotide polymorphism (SNP) markers to map QTL by identifying markers that displayed segregation distortion significantly different from the Mendelian expectation. QTL regions were further assessed in an independent validation population to confirm their associations with SRA. The experiment revealed 14 genomic regions under selection, 12 of which have not previously been reported for SRA. Five regions, including qSRA-6A, were confirmed in the validation population. The genomic regions identified in this study indicate that the genetic control of SRA is more complex than previously anticipated. Our study demonstrates that selection mapping is a powerful approach to complement genome-wide association studies for QTL detection. Moreover, the verification of qSRA-6A in an elite genetic background highlights the potential for MAS, although it is necessary to combine additional QTL to develop new cultivars with extreme SRA phenotypes.
{"title":"Mapping quantitative trait loci for seminal root angle in a selected durum wheat population.","authors":"Yichen Kang, Samir Alahmad, Shanice V Haeften, Oluwaseun Akinlade, Jingyang Tong, Eric Dinglasan, Kai P Voss-Fels, Andries B Potgieter, Andrew K Borrell, Manar Makhoul, Christian Obermeier, Rod Snowdon, Emma Mace, David R Jordan, Lee T Hickey","doi":"10.1002/tpg2.20490","DOIUrl":"10.1002/tpg2.20490","url":null,"abstract":"<p><p>Seminal root angle (SRA) is an important root architectural trait associated with drought adaptation in cereal crops. To date, all attempts to dissect the genetic architecture of SRA in durum wheat (Triticum durum Desf.) have used large association panels or structured mapping populations. Identifying changes in allele frequency generated by selection provides an alternative genetic mapping approach that can increase the power and precision of QTL detection. This study aimed to map quantitative trait loci (QTL) for SRA by genotyping durum lines created through divergent selection using a combination of marker-assisted selection (MAS) for the major SRA QTL (qSRA-6A) and phenotypic selection for SRA over multiple generations. The created 11 lines (BC<sub>1</sub>F<sub>2:5</sub>) were genotyped with genome-wide single-nucleotide polymorphism (SNP) markers to map QTL by identifying markers that displayed segregation distortion significantly different from the Mendelian expectation. QTL regions were further assessed in an independent validation population to confirm their associations with SRA. The experiment revealed 14 genomic regions under selection, 12 of which have not previously been reported for SRA. Five regions, including qSRA-6A, were confirmed in the validation population. The genomic regions identified in this study indicate that the genetic control of SRA is more complex than previously anticipated. Our study demonstrates that selection mapping is a powerful approach to complement genome-wide association studies for QTL detection. Moreover, the verification of qSRA-6A in an elite genetic background highlights the potential for MAS, although it is necessary to combine additional QTL to develop new cultivars with extreme SRA phenotypes.</p>","PeriodicalId":49002,"journal":{"name":"Plant Genome","volume":" ","pages":"e20490"},"PeriodicalIF":3.9,"publicationDate":"2025-03-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11733660/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141753188","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-03-01Epub Date: 2024-10-02DOI: 10.1002/tpg2.20520
Adedayo O Adeyanju, Patrick J Rich, Gebisa Ejeta
The parasitic weed Striga (Striga hermonthica) limits productivity of sorghum (Sorghum bicolor) and other cereals in sub-Saharan Africa and elsewhere. Improved host plant genetics is an effective control method but verified loci contributing to Striga resistance are limited. LOW GERMINATION STIMULANT 1 remains the only known sorghum locus affecting resistance to Striga. Functional loss (lgs1) alleles at this locus result in low Striga germination stimulant activity. We developed a robust polymerase chain reaction (PCR)-based LGS1 marker that detects all known natural lgs1 alleles. We have successfully used this marker to improve Striga resistance in our sorghum breeding program. To check its utility among diverse sets of germplasm, we genotyped 406 lines of the sorghum association panel (SAP) with the marker and phenotyped them for Striga germination stimulant activity. The SAP contains 23 lines (6%) with lgs1 mutations that involve a complete loss of this gene. Three previously described deletion alleles (lgs1-1, lgs1-2, and lgs1-3) ranging from 28.5 to 34 kbp are present among SAP members with a new one, lgs1-6, missing nearly 50 kbp relative to the reference genome. All 23 members of the SAP carrying lgs1 alleles had low Striga germination stimulant activity. The smaller previously described intragenic deletion mutations lgs1-4 and lgs1-5 are not present in the SAP. The LGS1 marker is useful for both detecting sources of lgs1 and introgressing Striga resistance into new genetic backgrounds.
{"title":"A powerful molecular marker to detect mutations at sorghum LOW GERMINATION STIMULANT 1.","authors":"Adedayo O Adeyanju, Patrick J Rich, Gebisa Ejeta","doi":"10.1002/tpg2.20520","DOIUrl":"10.1002/tpg2.20520","url":null,"abstract":"<p><p>The parasitic weed Striga (Striga hermonthica) limits productivity of sorghum (Sorghum bicolor) and other cereals in sub-Saharan Africa and elsewhere. Improved host plant genetics is an effective control method but verified loci contributing to Striga resistance are limited. LOW GERMINATION STIMULANT 1 remains the only known sorghum locus affecting resistance to Striga. Functional loss (lgs1) alleles at this locus result in low Striga germination stimulant activity. We developed a robust polymerase chain reaction (PCR)-based LGS1 marker that detects all known natural lgs1 alleles. We have successfully used this marker to improve Striga resistance in our sorghum breeding program. To check its utility among diverse sets of germplasm, we genotyped 406 lines of the sorghum association panel (SAP) with the marker and phenotyped them for Striga germination stimulant activity. The SAP contains 23 lines (6%) with lgs1 mutations that involve a complete loss of this gene. Three previously described deletion alleles (lgs1-1, lgs1-2, and lgs1-3) ranging from 28.5 to 34 kbp are present among SAP members with a new one, lgs1-6, missing nearly 50 kbp relative to the reference genome. All 23 members of the SAP carrying lgs1 alleles had low Striga germination stimulant activity. The smaller previously described intragenic deletion mutations lgs1-4 and lgs1-5 are not present in the SAP. The LGS1 marker is useful for both detecting sources of lgs1 and introgressing Striga resistance into new genetic backgrounds.</p>","PeriodicalId":49002,"journal":{"name":"Plant Genome","volume":" ","pages":"e20520"},"PeriodicalIF":3.9,"publicationDate":"2025-03-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11726417/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142367054","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-03-01Epub Date: 2024-12-04DOI: 10.1002/tpg2.20541
Anthony Piot, Yousry A El-Kassaby, Ilga Porth
Forest trees may harbor naturally occurring exon disruptive variants (DVs) in their gene sequences, which potentially impact important ecological and economic phenotypic traits. However, the abundance and molecular regulation of these variants remain largely unexplored. Here, 24,420 DVs were identified by screening 1014 Populus trichocarpa full genomes. The identified DVs were predominantly heterozygous with allelic frequencies below 5% (only 26% of DVs had frequencies greater than 5%). Using common garden-grown trees, DVs were assessed for gene expression variation in the developing xylem, revealing that their gene expression can be significantly altered, particularly for homozygous DVs (in the range of 27%-38% of cases depending on the studied common garden). DVs were further investigated for their correlations with 13 wood quality traits, revealing that, among the 148 discovered DV associations, 15 correlated with more than one wood property and six genes had more than one DV in their coding sequences associated with wood traits. Approximately one-third of DVs correlated with wood property variation also showed significant gene expression variation, confirming their non-spurious impact. These findings offer potential avenues for targeted introduction of homozygous mutations using tree biotechnology, and while the exact mechanisms by which DVs may directly influence wood formation remain to be unraveled, this study lays the groundwork for further investigation.
{"title":"Exon disruptive variants in Populus trichocarpa associated with wood properties exhibit distinct gene expression patterns.","authors":"Anthony Piot, Yousry A El-Kassaby, Ilga Porth","doi":"10.1002/tpg2.20541","DOIUrl":"10.1002/tpg2.20541","url":null,"abstract":"<p><p>Forest trees may harbor naturally occurring exon disruptive variants (DVs) in their gene sequences, which potentially impact important ecological and economic phenotypic traits. However, the abundance and molecular regulation of these variants remain largely unexplored. Here, 24,420 DVs were identified by screening 1014 Populus trichocarpa full genomes. The identified DVs were predominantly heterozygous with allelic frequencies below 5% (only 26% of DVs had frequencies greater than 5%). Using common garden-grown trees, DVs were assessed for gene expression variation in the developing xylem, revealing that their gene expression can be significantly altered, particularly for homozygous DVs (in the range of 27%-38% of cases depending on the studied common garden). DVs were further investigated for their correlations with 13 wood quality traits, revealing that, among the 148 discovered DV associations, 15 correlated with more than one wood property and six genes had more than one DV in their coding sequences associated with wood traits. Approximately one-third of DVs correlated with wood property variation also showed significant gene expression variation, confirming their non-spurious impact. These findings offer potential avenues for targeted introduction of homozygous mutations using tree biotechnology, and while the exact mechanisms by which DVs may directly influence wood formation remain to be unraveled, this study lays the groundwork for further investigation.</p>","PeriodicalId":49002,"journal":{"name":"Plant Genome","volume":" ","pages":"e20541"},"PeriodicalIF":3.9,"publicationDate":"2025-03-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11726415/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142780906","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
White mold, caused by the fungus Sclerotinia sclerotiorum (Lib.) de Bary, is a devastating disease affecting common bean (Phaseolus vulgaris L.) production worldwide. Breeding for resistance to white mold is challenging due to its quantitative inheritance and intricate genetic mechanisms. This research aimed to validate and characterize physiological resistance in the pinto dry bean market class through greenhouse straw tests under controlled conditions and field assessments under natural environments. Classical quantitative trait locus (QTL) mapping and Khufu de novo QTL-seq were employed to detect and narrow QTL intervals and identify candidate genes associated with white mold resistance in two pinto bean recombinant inbred line populations, PT9-5-6/USPT-WM-12 (P2) and PT12-37/VCP-13 (P3). Eleven QTL, five in P2 and six in P3, conditioning white mold resistance were identified. New QTL were discovered including WM1.4 and WM11.5 in P2, and WM1.5 and WM7.7 in P3. Existing major-effect QTL were validated: WM5.4 (34%-phenotypic variation explained) and WM7.4 (20%) in straw tests, and WM2.2 (15%) and WM3.1 (27%) under field conditions. QTL for avoidance traits such as resistance to lodging and late maturity overlapped WM2.2 in P2 and WM1.5, WM3.1, WM5.4, and WM7.7 in P3. WM5.4 (Pv05: 7.0-38.7 Mb) was associated with a large Phaseolus coccineus L. genome introgression in the resistant parent VCP-13. These findings offer narrowed genomic intervals and putative candidate genes for marker-assisted selection targeting white mold resistance improvement in pinto beans.
白霉是由菌核菌(Sclerotinia sclerotiorum (Lib.) de Bary)引起的一种世界性的影响普通豆(Phaseolus vulgaris L.)生产的毁灭性病害。由于白霉病的数量遗传和复杂的遗传机制,抗性育种具有挑战性。本研究旨在通过控制条件下的温室秸秆试验和自然环境下的田间评价,验证和表征平托干豆市场类的生理抗性。采用经典数量性状位点(QTL)定位和Khufu de novo QTL-seq技术,检测和缩小pinto bean重组自交系PT9-5-6/USPT-WM-12 (P2)和PT12-37/VCP-13 (P3)的QTL间隔,鉴定抗白霉相关候选基因。鉴定出11个调节白霉抗性的QTL,其中P2 5个,P3 6个。新发现的QTL包括P2中的WM1.4和WM11.5, P3中的WM1.5和WM7.7。对现有的主效QTL进行验证:秸秆试验中WM5.4(34%-表型变异解释)和WM7.4(20%),田间条件下WM2.2(15%)和WM3.1(27%)。抗倒伏和晚熟等回避性状的QTL在P2中与WM2.2重叠,在P3中与WM1.5、WM3.1、WM5.4和WM7.7重叠。WM5.4 (Pv05: 7.0-38.7 Mb)与耐药亲本VCP-13中Phaseolus coccineus L.基因组大量渗入相关。这些发现为标记辅助选择提供了缩小的基因组间隔和假定的候选基因,以提高斑豆的抗白霉性。
{"title":"Mapping resistance to Sclerotinia white mold in two pinto bean recombinant inbred line populations.","authors":"Alvaro Soler-Garzón, Fernanda Souza Lopes, Jayanta Roy, Josh Clevenger, Zachary Myers, Walid Korani, Welison Andrade Pereira, Qijian Song, Timothy Porch, Phillip E McClean, Phillip N Miklas","doi":"10.1002/tpg2.20538","DOIUrl":"10.1002/tpg2.20538","url":null,"abstract":"<p><p>White mold, caused by the fungus Sclerotinia sclerotiorum (Lib.) de Bary, is a devastating disease affecting common bean (Phaseolus vulgaris L.) production worldwide. Breeding for resistance to white mold is challenging due to its quantitative inheritance and intricate genetic mechanisms. This research aimed to validate and characterize physiological resistance in the pinto dry bean market class through greenhouse straw tests under controlled conditions and field assessments under natural environments. Classical quantitative trait locus (QTL) mapping and Khufu de novo QTL-seq were employed to detect and narrow QTL intervals and identify candidate genes associated with white mold resistance in two pinto bean recombinant inbred line populations, PT9-5-6/USPT-WM-12 (P2) and PT12-37/VCP-13 (P3). Eleven QTL, five in P2 and six in P3, conditioning white mold resistance were identified. New QTL were discovered including WM1.4 and WM11.5 in P2, and WM1.5 and WM7.7 in P3. Existing major-effect QTL were validated: WM5.4 (34%-phenotypic variation explained) and WM7.4 (20%) in straw tests, and WM2.2 (15%) and WM3.1 (27%) under field conditions. QTL for avoidance traits such as resistance to lodging and late maturity overlapped WM2.2 in P2 and WM1.5, WM3.1, WM5.4, and WM7.7 in P3. WM5.4 (Pv05: 7.0-38.7 Mb) was associated with a large Phaseolus coccineus L. genome introgression in the resistant parent VCP-13. These findings offer narrowed genomic intervals and putative candidate genes for marker-assisted selection targeting white mold resistance improvement in pinto beans.</p>","PeriodicalId":49002,"journal":{"name":"Plant Genome","volume":" ","pages":"e20538"},"PeriodicalIF":3.9,"publicationDate":"2025-03-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11726412/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142802886","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-03-01Epub Date: 2024-07-31DOI: 10.1002/tpg2.20485
Renan Uhdre, Clarice J Coyne, Britton Bourland, Julia Piaskowski, Ping Zheng, Girish M Ganjyal, Zhiwu Zhang, Rebecca J McGee, Dorrie Main, Nonoy Bandillo, Mario Morales, Yu Ma, Chengci Chen, William Franck, Adam Thrash, Marilyn L Warburton
Pea (Pisum sativum L.) is a key rotational crop and is increasingly important in the food processing sector for its protein. This study focused on identifying diverse high seed protein concentration (SPC) lines in pea plant genetic resources. Objectives included identifying high-protein pea lines, exploring genetic architecture across environments, pinpointing genes and metabolic pathways associated with high protein, and documenting information for single nucleotide polymorphism (SNP)-based marker-assisted selection. From 2019 to 2021, a 487-accession pea diversity panel, More protein, More pea, More profit, was evaluated in a randomized complete block design. DNA was extracted for genomic analysis via genotype-by-sequencing. Phenotypic analysis included protein and fat measurements in seeds and flower color. Genome-wide association study (GWAS) used multiple models, and the Pathways Association Study Tool was used for metabolic pathway analysis. Significant associations were found between SNPs and pea seed protein and fat concentration. Gene Psat7g216440 on chromosome 7, which targets proteins to cellular destinations, including seed storage proteins, was identified as associated with SPC. Genes Psat4g009200, Psat1g199800, Psat1g199960, and Psat1g033960, all involved in lipid metabolism, were associated with fat concentration. GWAS also identified genes annotated for storage proteins associated with fat concentration, indicating a complex relationship between fat and protein. Metabolic pathway analysis identified 20 pathways related to fat and seven to protein concentration, involving fatty acids, amino acid and protein metabolism, and the tricarboxylic acid cycle. These findings will assist in breeding of high-protein, diverse pea cultivars, and SNPs that can be converted to breeder-friendly molecular marker assays are identified for genes associated with high protein.
{"title":"Association study of crude seed protein and fat concentration in a USDA pea diversity panel.","authors":"Renan Uhdre, Clarice J Coyne, Britton Bourland, Julia Piaskowski, Ping Zheng, Girish M Ganjyal, Zhiwu Zhang, Rebecca J McGee, Dorrie Main, Nonoy Bandillo, Mario Morales, Yu Ma, Chengci Chen, William Franck, Adam Thrash, Marilyn L Warburton","doi":"10.1002/tpg2.20485","DOIUrl":"10.1002/tpg2.20485","url":null,"abstract":"<p><p>Pea (Pisum sativum L.) is a key rotational crop and is increasingly important in the food processing sector for its protein. This study focused on identifying diverse high seed protein concentration (SPC) lines in pea plant genetic resources. Objectives included identifying high-protein pea lines, exploring genetic architecture across environments, pinpointing genes and metabolic pathways associated with high protein, and documenting information for single nucleotide polymorphism (SNP)-based marker-assisted selection. From 2019 to 2021, a 487-accession pea diversity panel, More protein, More pea, More profit, was evaluated in a randomized complete block design. DNA was extracted for genomic analysis via genotype-by-sequencing. Phenotypic analysis included protein and fat measurements in seeds and flower color. Genome-wide association study (GWAS) used multiple models, and the Pathways Association Study Tool was used for metabolic pathway analysis. Significant associations were found between SNPs and pea seed protein and fat concentration. Gene Psat7g216440 on chromosome 7, which targets proteins to cellular destinations, including seed storage proteins, was identified as associated with SPC. Genes Psat4g009200, Psat1g199800, Psat1g199960, and Psat1g033960, all involved in lipid metabolism, were associated with fat concentration. GWAS also identified genes annotated for storage proteins associated with fat concentration, indicating a complex relationship between fat and protein. Metabolic pathway analysis identified 20 pathways related to fat and seven to protein concentration, involving fatty acids, amino acid and protein metabolism, and the tricarboxylic acid cycle. These findings will assist in breeding of high-protein, diverse pea cultivars, and SNPs that can be converted to breeder-friendly molecular marker assays are identified for genes associated with high protein.</p>","PeriodicalId":49002,"journal":{"name":"Plant Genome","volume":" ","pages":"e20485"},"PeriodicalIF":3.9,"publicationDate":"2025-03-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11726435/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141861363","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-03-01Epub Date: 2024-08-28DOI: 10.1002/tpg2.20498
Prabin Bajgain, Hannah Stoll, James A Anderson
The perennial grass Thinopyrum intermedium (intermediate wheatgrass [IWG]) is being domesticated as a food crop. With a deep root system and high biomass, IWG can help reduce soil and water erosion and limit nutrient runoff. As a novel grain crop undergoing domestication, IWG lags in yield, seed size, and other agronomic traits compared to annual grains. Better characterization of trait variation and identification of genetic markers associated with loci controlling the traits could help in further improving this crop. The University of Minnesota's Cycle 5 IWG breeding population of 595 spaced plants was evaluated at two locations in 2021 and 2022 for agronomic traits plant height, grain yield, and spike weight, and domestication traits shatter resistance, free grain threshing, and seed size. Pairwise trait correlations were weak to moderate with the highest correlation observed between seed size and height (0.41). Broad-sense trait heritabilities were high (0.68-0.77) except for spike weight (0.49) and yield (0.44). Association mapping using 24,284 genome-wide single nucleotide polymorphism markers identified 30 main quantitative trait loci (QTLs) across all environments and 32 QTL-by-environment interactions (QTE) at each environment. The genomic prediction model significantly improved predictions when parents were used in the training set and significant QTLs and QTEs used as covariates. Seed size was the best predicted trait with model predictive ability (r) of 0.72; yield was predicted moderately well (r = 0.45). We expect this discovery of significant genomic loci and mostly high trait predictions from genomic prediction models to help improve future IWG breeding populations.
{"title":"Improving complex agronomic and domestication traits in the perennial grain crop intermediate wheatgrass with genetic mapping and genomic prediction.","authors":"Prabin Bajgain, Hannah Stoll, James A Anderson","doi":"10.1002/tpg2.20498","DOIUrl":"10.1002/tpg2.20498","url":null,"abstract":"<p><p>The perennial grass Thinopyrum intermedium (intermediate wheatgrass [IWG]) is being domesticated as a food crop. With a deep root system and high biomass, IWG can help reduce soil and water erosion and limit nutrient runoff. As a novel grain crop undergoing domestication, IWG lags in yield, seed size, and other agronomic traits compared to annual grains. Better characterization of trait variation and identification of genetic markers associated with loci controlling the traits could help in further improving this crop. The University of Minnesota's Cycle 5 IWG breeding population of 595 spaced plants was evaluated at two locations in 2021 and 2022 for agronomic traits plant height, grain yield, and spike weight, and domestication traits shatter resistance, free grain threshing, and seed size. Pairwise trait correlations were weak to moderate with the highest correlation observed between seed size and height (0.41). Broad-sense trait heritabilities were high (0.68-0.77) except for spike weight (0.49) and yield (0.44). Association mapping using 24,284 genome-wide single nucleotide polymorphism markers identified 30 main quantitative trait loci (QTLs) across all environments and 32 QTL-by-environment interactions (QTE) at each environment. The genomic prediction model significantly improved predictions when parents were used in the training set and significant QTLs and QTEs used as covariates. Seed size was the best predicted trait with model predictive ability (r) of 0.72; yield was predicted moderately well (r = 0.45). We expect this discovery of significant genomic loci and mostly high trait predictions from genomic prediction models to help improve future IWG breeding populations.</p>","PeriodicalId":49002,"journal":{"name":"Plant Genome","volume":" ","pages":"e20498"},"PeriodicalIF":3.9,"publicationDate":"2025-03-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11726416/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142094008","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
The Septoria tritici blotch (STB) [Zymoseptoria tritici (Desm.)] of wheat (Triticum aestivum L.) is characterized by its polycyclic and hemibiotrophic nature. It is one of the most dangerous diseases affecting wheat production worldwide. Durable resistance is largely decided by the combined effect of several quantitative trait loci (QTLs) having a minor effect. Currently, STB is not important in South Asia. However, STB expanding and wider adaptability, changing climatic conditions, and agronomic practices can create a situation of concern. Therefore, dissection of the genetic architecture of adult-plant resistance with genome-wide association mapping and selection of resistant sources for adult plant STB resistance were carried out on a panel of South Asian germplasm. We discovered the 91 quantitative trait nucleotides (QTNs) associated with STB resistance; 23 QTNs were repetitive across the different years and models. Many of these QTNs could differentiate the mapping panel into resistant versus susceptible groups and were linked to candidate genes related to disease resistance functions within linkage disequilibrium blocks. The repetitive QTNs, namely, Q.CIM.stb.2DL.2, Q.CIM.stb_dh.2DL.3, Q.CIM.stb.2AL.5, and Q.CIM.stb.7BL.1, may be novel due to the absence of co-localization of previously reported QTLs, meta-quantitative trait loci, and STB genes. There was a perfect negative correlation between the stacking of favorable alleles and STB susceptibility, and STB resistance response was improved by ∼50% with the stacking of ≥60% favorable alleles. The genotypes, namely, CIM20, CIM56, CIM57, CIM18, CIM44, WK2395, and K1317, could be used as resistant sources in wheat breeding programs. Therefore, this study could aid in designing the breeding programs for STB resistance before the onset of the alarming situation of STB in South Asia.
{"title":"Identification of resistance sources and genomic regions regulating Septoria tritici blotch resistance in South Asian bread wheat germplasm.","authors":"Manjeet Kumar, Xinyao He, Sudhir Navathe, Umesh Kamble, Madhu Patial, Pawan Kumar Singh","doi":"10.1002/tpg2.20531","DOIUrl":"10.1002/tpg2.20531","url":null,"abstract":"<p><p>The Septoria tritici blotch (STB) [Zymoseptoria tritici (Desm.)] of wheat (Triticum aestivum L.) is characterized by its polycyclic and hemibiotrophic nature. It is one of the most dangerous diseases affecting wheat production worldwide. Durable resistance is largely decided by the combined effect of several quantitative trait loci (QTLs) having a minor effect. Currently, STB is not important in South Asia. However, STB expanding and wider adaptability, changing climatic conditions, and agronomic practices can create a situation of concern. Therefore, dissection of the genetic architecture of adult-plant resistance with genome-wide association mapping and selection of resistant sources for adult plant STB resistance were carried out on a panel of South Asian germplasm. We discovered the 91 quantitative trait nucleotides (QTNs) associated with STB resistance; 23 QTNs were repetitive across the different years and models. Many of these QTNs could differentiate the mapping panel into resistant versus susceptible groups and were linked to candidate genes related to disease resistance functions within linkage disequilibrium blocks. The repetitive QTNs, namely, Q.CIM.stb.2DL.2, Q.CIM.stb_dh.2DL.3, Q.CIM.stb.2AL.5, and Q.CIM.stb.7BL.1, may be novel due to the absence of co-localization of previously reported QTLs, meta-quantitative trait loci, and STB genes. There was a perfect negative correlation between the stacking of favorable alleles and STB susceptibility, and STB resistance response was improved by ∼50% with the stacking of ≥60% favorable alleles. The genotypes, namely, CIM20, CIM56, CIM57, CIM18, CIM44, WK2395, and K1317, could be used as resistant sources in wheat breeding programs. Therefore, this study could aid in designing the breeding programs for STB resistance before the onset of the alarming situation of STB in South Asia.</p>","PeriodicalId":49002,"journal":{"name":"Plant Genome","volume":" ","pages":"e20531"},"PeriodicalIF":3.9,"publicationDate":"2025-03-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11726422/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142733655","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-03-01Epub Date: 2024-07-28DOI: 10.1002/tpg2.20493
Dhondup Lhamo, Genqiao Li, George Song, Xuehui Li, Taner Z Sen, Yong-Qiang Gu, Xiangyang Xu, Steven S Xu
Powdery mildew, caused by the fungal pathogen Blumeria graminis (DC.) E. O. Speer f. sp. tritici Em. Marchal (Bgt), is a constant threat to global wheat (Triticum aestivum L.) production. Although ∼100 powdery mildew (Pm) resistance genes and alleles have been identified in wheat and its relatives, more is needed to minimize Bgt's fast evolving virulence. In tetraploid wheat (Triticum turgidum L.), wild emmer wheat [T. turgidum ssp. dicoccoides (Körn. ex Asch. & Graebn.) Thell.] accessions from Israel have contributed many Pm resistance genes. However, the diverse genetic reservoirs of cultivated emmer wheat [T. turgidum ssp. dicoccum (Schrank ex Schübl.) Thell.] have not been fully exploited. In the present study, we evaluated a diverse panel of 174 cultivated emmer accessions for their reaction to Bgt isolate OKS(14)-B-3-1 and found that 66% of accessions, particularly those of Ethiopian (30.5%) and Indian (6.3%) origins, exhibited high resistance. To determine the genetic basis of Bgt resistance in the panel, genome-wide association studies were performed using 46,383 single nucleotide polymorphisms (SNPs) from genotype-by-sequencing and 4331 SNPs from the 9K SNP Infinium array. Twenty-five significant SNP markers were identified to be associated with Bgt resistance, of which 21 SNPs are likely novel loci, whereas four possibly represent emmer derived Pm4a, Pm5a, PmG16, and Pm64. Most novel loci exhibited minor effects, whereas three novel loci on chromosome arms 2AS, 3BS, and 5AL had major effect on the phenotypic variance. This study demonstrates cultivated emmer as a rich source of powdery mildew resistance, and the resistant accessions and novel loci found herein can be utilized in wheat breeding programs to enhance Bgt resistance in wheat.
由真菌病原体 Blumeria graminis (DC.) E. O. Speer f. sp. tritici Em.Marchal (Bgt) 引起的白粉病,是全球小麦(Triticum aestivum L. )生产的一个长期威胁。虽然已在小麦及其近缘种中鉴定出 100 ∼ 100 个白粉病(Pm)抗性基因和等位基因,但要最大限度地降低 Bgt 快速演变的毒力,还需要做更多的工作。在四倍体小麦(Triticum turgidum L.)中,来自以色列的野生emmer小麦[T. turgidum ssp. dicoccoides (Körn. ex Asch. & Graebn.) Thell.然而,栽培小麦[T. turgidum ssp. dicoccum (Schrank ex Schübl.) Thell.]的多种基因库尚未得到充分利用。在本研究中,我们评估了 174 个栽培珙桐品种对 Bgt 分离物 OKS(14)-B-3-1 的反应,发现 66% 的品种,尤其是埃塞俄比亚(30.5%)和印度(6.3%)的品种表现出高度抗性。为了确定面板中 Bgt 抗性的遗传基础,利用逐基因型测序的 46,383 个单核苷酸多态性(SNPs)和 9K SNP Infinium 阵列的 4331 个 SNPs 进行了全基因组关联研究。研究发现了 25 个与 Bgt 抗性相关的重要 SNP 标记,其中 21 个 SNP 可能是新的基因位点,而 4 个可能代表emmer 衍生的 Pm4a、Pm5a、PmG16 和 Pm64。大多数新基因位点的影响较小,而染色体臂 2AS、3BS 和 5AL 上的三个新基因位点对表型变异的影响较大。本研究表明,栽培小麦是白粉病抗性的丰富来源,本研究发现的抗性品种和新基因座可用于小麦育种计划,以提高小麦对白粉病的抗性。
{"title":"Genome-wide association studies on resistance to powdery mildew in cultivated emmer wheat.","authors":"Dhondup Lhamo, Genqiao Li, George Song, Xuehui Li, Taner Z Sen, Yong-Qiang Gu, Xiangyang Xu, Steven S Xu","doi":"10.1002/tpg2.20493","DOIUrl":"10.1002/tpg2.20493","url":null,"abstract":"<p><p>Powdery mildew, caused by the fungal pathogen Blumeria graminis (DC.) E. O. Speer f. sp. tritici Em. Marchal (Bgt), is a constant threat to global wheat (Triticum aestivum L.) production. Although ∼100 powdery mildew (Pm) resistance genes and alleles have been identified in wheat and its relatives, more is needed to minimize Bgt's fast evolving virulence. In tetraploid wheat (Triticum turgidum L.), wild emmer wheat [T. turgidum ssp. dicoccoides (Körn. ex Asch. & Graebn.) Thell.] accessions from Israel have contributed many Pm resistance genes. However, the diverse genetic reservoirs of cultivated emmer wheat [T. turgidum ssp. dicoccum (Schrank ex Schübl.) Thell.] have not been fully exploited. In the present study, we evaluated a diverse panel of 174 cultivated emmer accessions for their reaction to Bgt isolate OKS(14)-B-3-1 and found that 66% of accessions, particularly those of Ethiopian (30.5%) and Indian (6.3%) origins, exhibited high resistance. To determine the genetic basis of Bgt resistance in the panel, genome-wide association studies were performed using 46,383 single nucleotide polymorphisms (SNPs) from genotype-by-sequencing and 4331 SNPs from the 9K SNP Infinium array. Twenty-five significant SNP markers were identified to be associated with Bgt resistance, of which 21 SNPs are likely novel loci, whereas four possibly represent emmer derived Pm4a, Pm5a, PmG16, and Pm64. Most novel loci exhibited minor effects, whereas three novel loci on chromosome arms 2AS, 3BS, and 5AL had major effect on the phenotypic variance. This study demonstrates cultivated emmer as a rich source of powdery mildew resistance, and the resistant accessions and novel loci found herein can be utilized in wheat breeding programs to enhance Bgt resistance in wheat.</p>","PeriodicalId":49002,"journal":{"name":"Plant Genome","volume":" ","pages":"e20493"},"PeriodicalIF":3.9,"publicationDate":"2025-03-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11733656/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141789607","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}