Genome-wide association study and pathway analysis to decipher loci associated with Fusarium ear rot resistance in tropical maize germplasm

Genet Resour Crop Evol https://doi.org/10.1007/s10722-023-01793-4 RESEARCH ARTICLE Genome‑wide association study and pathway analysis to decipher loci associated with Fusarium ear rot resistance in tropical maize germplasm Stella Bigirwa Ayesiga · Patrick Rubaihayo · Bonny Michael Oloka · Isaac Ozinga Dramadri · Julius Pyton Sserumaga Received: 4 August 2023 / Accepted: 25 October 2023 © The Author(s) 2023 Abstract Breeding for host resistance is the most efficient and environmentally safe method to curb the spread of fusarium ear rot (FER). However, conventional breeding for resistance to FER is hampered by the complex polygenic nature of this trait, which is highly influenced by environmental conditions. This study aimed to identify genomic regions, single nucleotide polymorphisms (SNPs), and putative candidate genes associated with FER resistance as Supplementary Information The online version contains supplementary material available at https://doi. org/10.1007/s10722-023-01793-4. S. B. Ayesiga · P. Rubaihayo · I. O. Dramadri Department of Agricultural Production, College of Agriculture and Environmental Sciences, Makerere University, P. O. Box 7062, Kampala, Uganda e-mail: P. Rubaihayo e-mail: I. O. Dramadri e-mail: S. B. Ayesiga · J. P. Sserumaga (*) National Livestock Resources Research Institute, National Agricultural Research Organization, PO Box 5704, Kampala, Uganda e-mail: B. M. Oloka Department of Horticultural Sciences, North Carolina State University, Raleigh, NC, USA e-mail: well as candidate metabolic pathways and pathway genes involved in it. A panel of 151 tropical inbred maize lines were used to assess the genetic architecture of FER resistance over two seasons. During the study period, seven SNPs associated with FER resistance were identified on chromosomes 1, 2, 4, 5, and 9, accounting for 4–11% of the phenotypic variance. These significant markers were annotated into four genes. Seven significant metabolic pathways involved in FER resistance were identified using the Pathway Association Study Tool, the most significant being the superpathway of the glyoxylate cycle. Overall, this study confirmed that resistance to FER is indeed a complex mechanism controlled by several small to medium-effect loci. Our findings may contribute to fast-tracking the efforts to develop disease-resistant maize lines through marker-assisted selection. Keywords Genome-wide association study · Metabolic pathways · Fusarium verticillioides · SNPs · Zea mays Introduction Fusarium ear rot (FER), which is caused by Fusarium verticillioides (Saccardo) Nirenberg, is a significant disease that affects maize worldwide (Stagnati et al. 2019) targeting almost all of its growth stages (Lanubile et al. 2014). FER leads to significant yield losses, which are estimated between 10 and 30% and can Vol.: (0123456789) 13 Genet Resour Crop Evol reach 50% or more in severely infected regions (Yao et al. 2020). In addition, this disease leads to poor grain quality and contamination of the infected kernels with fumonisin, a mycotoxin and known carcinogen reported to be harmful to both animal and human health (Czembor et al. 2019; Stagnati et al. 2019). In areas where maize is a staple food, such as subSaharan Africa, FER infection has been reported to be high (Bigirwa et al. 2007; Tembo et al. 2022). Traditional FER management methods primarily involve the use of fungicides or other agronomic approaches, but these have been reported to be ineffective and environmentally unfriendly, and to increase the costs of maize production (Lanubile et al. 2017). Breeding for disease resistance is recommended because it is an efficient and ecologically safe strategy (Chen et al. 2016; Lanubile et al. 2017). Despite the benefits of using resistant cultivars, only a few resistant genotypes are available because of the complex genetic architecture of FER resistance (de Jong et al. 2018). This complexity is attributed to the fact that the resistance mechanism is controlled by multiple genes with minor effects that are highly influenced by the environment and are not consistent between populations (Butrón et al. 2015; Chen et al. 2012; Clements et al. 2004; de Jong et al. 2018; Holland et al. 2020; Samayoa et al. 2019; Zila et al. 2013). Genome-Wide Association Studies (GWASs) are particularly suitable for the identification of markertrait associations in complex quantitative traits using diverse germplasm lines (Cui et al. 2016; Samayoa et al. 2019). GWASs based on genetic linkage disequilibrium (LD) are preferred to traditional linkagebased analyses because of their excellent mapping resolution that allows to capture and map small effect loci (Sitonik et al. 2019). In maize, GWASs have successfully been used to detect genomic regions (Chen et al. 2016; Wang et al. 2012; Zila et al. 2013, 2014) and analyze the genetic architecture of various important and complex traits, such as resistance to aflatoxin and ear rot caused by Aspergillus flavus (Tang et al. 2015; Warburton et al. 2015), common maize rust caused by Puccinia sorghi Schwein (Kibe et al. 2020; Olukolu et al. 2016), northern corn leaf blight (Ding et al. 2015; Rashid et al. 2020), oil biosynthesis (Li et al. 2013), resistance to head smut (Wang et al. 2012), and seedling root development (Pace et al. 2015). Vol:. (1234567890) 13 In addition to identifying genomic regions and genes involved in disease resistance, GWASs also assist in identifying resistance pathways and associated genes. Metabolic pathway analysis focuses on the combined effects of many genes clustered together because of their shared biological functions (Tang et al. 2015; Warburton et al. 2022). This type of research complements the study of the most significant marker-trait associations in addition to giving clues on the genetic basis of specific traits (Tang et al. 2015). Combining FER resistance data derived from GWASs in a pathway analysis allows to jointly consider all the genetic sequences positively associated with resistance to this disease and consequently to potentially identify pathways and associated genes involved in it. Identifying these genes will eventually lead to more efficient breeding procedures and the development of FER-resistant maize hybrids. A better understanding of the pathways involved in resistance will also lead to a broader understanding of plant defense mechanisms against other fungi. The aim of this study was to identify genomic regions, single nucleotide polymorphisms (SNP), and putative candidate genes as well as candidate metabolic pathways and associated genes involved in FER resistance. Materials and methods Plant materials and field management A total of 151 inbred maize lines were evaluated at the National Livestock Resources Research Institute (NaLIRRI) of the National Agricultural Research Organization of Uganda, which is located in a midaltitude agroecological zone (0° 32’N and 32° 35´E) at 1150 m above sea level (Sserumaga (...truncated)