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Article: Genetic analysis of cassava brown streak disease root necrosis using image analysis and genome-wide association studies.

Nandudu, Leah / Strock, Christopher / Ogbonna, Alex / Kawuki, Robert / Jannink, Jean-Luc

2024 Volume 15, Page(s) 1360729

Abstract: Cassava brown streak disease (CBSD) poses a substantial threat to food security. To address this challenge, we used PlantCV to extract CBSD root necrosis image traits from 320 clones, with an aim of identifying genomic regions through genome-wide ... ...

Abstract	Cassava brown streak disease (CBSD) poses a substantial threat to food security. To address this challenge, we used PlantCV to extract CBSD root necrosis image traits from 320 clones, with an aim of identifying genomic regions through genome-wide association studies (GWAS) and candidate genes. Results revealed strong correlations among certain root necrosis image traits, such as necrotic area fraction and necrotic width fraction, as well as between the convex hull area of root necrosis and the percentage of necrosis. Low correlations were observed between CBSD scores obtained from the 1-5 scoring method and all root necrosis traits. Broad-sense heritability estimates of root necrosis image traits ranged from low to moderate, with the highest estimate of 0.42 observed for the percentage of necrosis, while narrow-sense heritability consistently remained low, ranging from 0.03 to 0.22. Leveraging data from 30,750 SNPs obtained through DArT genotyping, eight SNPs on chromosomes 1, 7, and 11 were identified and associated with both the ellipse eccentricity of root necrosis and the percentage of necrosis through GWAS. Candidate gene analysis in the 172.2kb region on the chromosome 1 revealed 24 potential genes with diverse functions, including ubiquitin-protein ligase, DNA-binding transcription factors, and RNA metabolism protein, among others. Despite our initial expectation that image analysis objectivity would yield better heritability estimates and stronger genomic associations than the 1-5 scoring method, the results were unexpectedly lower. Further research is needed to comprehensively understand the genetic basis of these traits and their relevance to cassava breeding and disease management.
Language	English
Publishing date	2024-03-18
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2613694-6
ISSN	1664-462X
ISSN	1664-462X
DOI	10.3389/fpls.2024.1360729
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Article: Genetic complexity of cassava brown streak disease: insights from qPCR-based viral titer analysis and genome-wide association studies.

Nandudu, Leah / Sheat, Samar / Winter, Stephan / Ogbonna, Alex / Kawuki, Robert / Jannink, Jean-Luc

Frontiers in plant science

2024 Volume 15, Page(s) 1365132

Abstract: Cassava, a vital global food source, faces a threat from Cassava Brown Streak Disease (CBSD). CBSD results from two viruses: Cassava brown streak virus (CBSV) and Ugandan cassava brown streak virus (UCBSV). These viruses frequently pose challenges to the ...

Abstract	Cassava, a vital global food source, faces a threat from Cassava Brown Streak Disease (CBSD). CBSD results from two viruses: Cassava brown streak virus (CBSV) and Ugandan cassava brown streak virus (UCBSV). These viruses frequently pose challenges to the traditional symptom-based 1-5 phenotyping method due to its limitations in terms of accuracy and objectivity. Quantitative polymerase chain reaction (qPCR) offers precise virus quantification, although high costs hinder its widespread adoption. In this research, we utilized qPCR to measure the viral titer/load of CBSV and UCBSV. The objectives were to evaluate titer variability within the Cycle 2 (C2) population in two different environments, establish connections between viral titers and CBSD severity scores from the 1-5 scoring method, perform Genome-Wide Association Studies (GWAS) to identify genomic regions associated with CBSV and UCBSV titers, and investigate the functional annotated genes. The results demonstrated a significantly higher prevalence of CBSV (50.2%) in clones compared to UCBSV (12.9%) with mixed infections in some cases. Genotypic effects, particularly concerning UCBSV, were significant, with genotype-by-environment effects primarily influencing CBSV titer. GWAS Studies identified genomic regions associated with CBSV and UCBSV titers. Twenty-one SNP markers on chromosomes 10, 13, 17, and 18 exhibited significant associations with CBSV titer, collectively explaining 43.14% of the phenotypic variation. Additionally, 25 SNP markers on chromosomes 1, 2, 4, 5, 8, 11, 12, 13, 16, and 18 were associated with UCBSV titer, and explained 70.71% of the phenotypic variation. No shared genomic regions were identified between CBSV and UCBSV viral titers. Gene ontology analysis also revealed diverse gene functions, especially in transport and catalytic activities. These findings enhance our understanding of virus prevalence, genetics, and molecular functions in cassava plants, offering valuable insights for targeted breeding strategies.
Language	English
Publishing date	2024-03-13
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2613694-6
ISSN	1664-462X
ISSN	1664-462X
DOI	10.3389/fpls.2024.1365132
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Article: Genetic dissection of cassava brown streak disease in a genomic selection population.

Nandudu, Leah / Kawuki, Robert / Ogbonna, Alex / Kanaabi, Michael / Jannink, Jean-Luc

Frontiers in plant science

2023 Volume 13, Page(s) 1099409

Abstract: Introduction: Cassava brown streak disease (CBSD) is a major threat to food security in East and central Africa. Breeding for resistance against CBSD is the most economical and sustainable way of addressing this challenge.: Methods: This study seeks ... ...

Abstract	Introduction: Cassava brown streak disease (CBSD) is a major threat to food security in East and central Africa. Breeding for resistance against CBSD is the most economical and sustainable way of addressing this challenge. Methods: This study seeks to assess the (1) performance of CBSD incidence and severity; (2) identify genomic regions associated with CBSD traits and (3) candidate genes in the regions of interest, in the Cycle 2 population of the National Crops Resources Research Institute. Results: A total of 302 diverse clones were screened, revealing that CBSD incidence across growing seasons was 44%. Severity scores for both foliar and root symptoms ranged from 1.28 to 1.99 and 1.75 to 2.28, respectively across seasons. Broad sense heritability ranged from low to high (0.15 - 0.96), while narrow sense heritability ranged from low to moderate (0.03 - 0.61). Five QTLs, explaining approximately 19% phenotypic variation were identified for CBSD severity at 3 months after planting on chromosomes 1, 13, and 18 in the univariate GWAS analysis. Multivariate GWAS analysis identified 17 QTLs that were consistent with the univariate analysis including additional QTLs on chromosome 6. Seventy-seven genes were identified in these regions with functions such as catalytic activity, ATP-dependent activity, binding, response to stimulus, translation regulator activity, transporter activity among others. Discussion: These results suggest variation in virulence in the C2 population, largely due to genetics and annotated genes in these QTLs regions may play critical roles in virus initiation and replication, thus increasing susceptibility to CBSD.
Language	English
Publishing date	2023-01-13
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2613694-6
ISSN	1664-462X
ISSN	1664-462X
DOI	10.3389/fpls.2022.1099409
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Article ; Online: Corrigendum to: Genomic mating in outbred species: predicting cross usefulness with additive and total genetic covariance matrices.

Wolfe, Marnin D / Chan, Ariel W / Kulakow, Peter / Rabbi, Ismail / Jannink, Jean-Luc

Genetics

2022 Volume 220, Issue 2

Language	English
Publishing date	2022-01-31
Publishing country	United States
Document type	Published Erratum
ZDB-ID	2167-2
ISSN	1943-2631 ; 0016-6731
ISSN (online)	1943-2631
ISSN	0016-6731
DOI	10.1093/genetics/iyab225
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Article: Multi-Species Genomics-Enabled Selection for Improving Agroecosystems Across Space and Time.

Wolfe, Marnin D / Jannink, Jean-Luc / Kantar, Michael B / Santantonio, Nicholas

Frontiers in plant science

2021 Volume 12, Page(s) 665349

Abstract: Plant breeding has been central to global increases in crop yields. Breeding deserves praise for helping to establish better food security, but also shares the responsibility of unintended consequences. Much work has been done describing alternative ... ...

Abstract	Plant breeding has been central to global increases in crop yields. Breeding deserves praise for helping to establish better food security, but also shares the responsibility of unintended consequences. Much work has been done describing alternative agricultural systems that seek to alleviate these externalities, however, breeding methods and breeding programs have largely not focused on these systems. Here we explore breeding and selection strategies that better align with these more diverse spatial and temporal agricultural systems.
Language	English
Publishing date	2021-06-23
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2613694-6
ISSN	1664-462X
ISSN	1664-462X
DOI	10.3389/fpls.2021.665349
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Article ; Online: Sexual dimorphism and the effect of wild introgressions on recombination in cassava (Manihot esculenta Crantz) breeding germplasm.

Chan, Ariel W / Villwock, Seren S / Williams, Amy L / Jannink, Jean-Luc

G3 (Bethesda, Md.)

2021 Volume 12, Issue 1

Abstract: Recombination has essential functions in meiosis, evolution, and breeding. The frequency and distribution of crossovers dictate the generation of new allele combinations and can vary across species and between sexes. Here, we examine recombination ... ...

Abstract	Recombination has essential functions in meiosis, evolution, and breeding. The frequency and distribution of crossovers dictate the generation of new allele combinations and can vary across species and between sexes. Here, we examine recombination landscapes across the 18 chromosomes of cassava (Manihot esculenta Crantz) with respect to male and female meioses and known introgressions from the wild relative Manihot glaziovii. We used SHAPEIT2 and duoHMM to infer crossovers from genotyping-by-sequencing data and a validated multigenerational pedigree from the International Institute of Tropical Agriculture cassava breeding germplasm consisting of 7020 informative meioses. We then constructed new genetic maps and compared them to an existing map previously constructed by the International Cassava Genetic Map Consortium. We observed higher recombination rates in females compared to males, and lower recombination rates in M. glaziovii introgression segments on chromosomes 1 and 4, with suppressed recombination along the entire length of the chromosome in the case of the chromosome 4 introgression. Finally, we discuss hypothesized mechanisms underlying our observations of heterochiasmy and crossover suppression and discuss the broader implications for plant breeding.
MeSH term(s)	Alleles ; Manihot/genetics ; Plant Breeding ; Recombination, Genetic ; Sex Characteristics
Language	English
Publishing date	2021-11-17
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2629978-1
ISSN	2160-1836 ; 2160-1836
ISSN (online)	2160-1836
ISSN	2160-1836
DOI	10.1093/g3journal/jkab372
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Article ; Online: If it ain't broke, don't fix it: evaluating the effect of increased recombination on response to selection for wheat breeding.

Taagen, Ella / Jordan, Katherine / Akhunov, Eduard / Sorrells, Mark E / Jannink, Jean-Luc

G3 (Bethesda, Md.)

2022 Volume 12, Issue 12

Abstract: Meiotic recombination is a source of allelic diversity, but the low frequency and biased distribution of crossovers that occur during meiosis limits the genetic variation available to plant breeders. Simulation studies previously identified that ... ...

Abstract	Meiotic recombination is a source of allelic diversity, but the low frequency and biased distribution of crossovers that occur during meiosis limits the genetic variation available to plant breeders. Simulation studies previously identified that increased recombination frequency can retain more genetic variation and drive greater genetic gains than wildtype recombination. Our study was motivated by the need to define desirable recombination intervals in regions of the genome with fewer crossovers. We hypothesized that deleterious variants, which can negatively impact phenotypes and occur at higher frequencies in low recombining regions where they are linked in repulsion with favorable loci, may offer a signal for positioning shifts of recombination distributions. Genomic selection breeding simulation models based on empirical wheat data were developed to evaluate increased recombination frequency and changing recombination distribution on response to selection. Comparing high and low values for a range of simulation parameters identified that few combinations retained greater genetic variation and fewer still achieved higher genetic gain than wildtype. More recombination was associated with loss of genomic prediction accuracy, which outweighed the benefits of disrupting repulsion linkages. Irrespective of recombination frequency or distribution and deleterious variant annotation, enhanced response to selection under increased recombination required polygenic trait architecture, high heritability, an initial scenario of more repulsion than coupling linkages, and greater than 6 cycles of genomic selection. Altogether, the outcomes of this research discourage a controlled recombination approach to genomic selection in wheat as a more efficient path to retaining genetic variation and increasing genetic gains compared with existing breeding methods.
MeSH term(s)	Triticum/genetics ; Plant Breeding ; Selective Breeding ; Alleles ; Genetic Linkage ; Selection, Genetic
Language	English
Publishing date	2022-11-04
Publishing country	England
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2629978-1
ISSN	2160-1836 ; 2160-1836
ISSN (online)	2160-1836
ISSN	2160-1836
DOI	10.1093/g3journal/jkac291
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Article ; Online: Homeologous Epistasis in Wheat: The Search for an Immortal Hybrid.

Santantonio, Nicholas / Jannink, Jean-Luc / Sorrells, Mark

Genetics

2019 Volume 211, Issue 3, Page(s) 1105–1122

Abstract: Hybridization between related species results in the formation of an allopolyploid with multiple subgenomes. These subgenomes will each contain complete, yet evolutionarily divergent, sets of genes. Like a diploid hybrid, allopolyploids will have two ... ...

Abstract	Hybridization between related species results in the formation of an allopolyploid with multiple subgenomes. These subgenomes will each contain complete, yet evolutionarily divergent, sets of genes. Like a diploid hybrid, allopolyploids will have two versions, or homeoalleles, for every gene. Partial functional redundancy between homeologous genes should result in a deviation from additivity. These epistatic interactions between homeoalleles are analogous to dominance effects, but are fixed across subgenomes through self pollination. An allopolyploid can be viewed as an immortalized hybrid, with the opportunity to select and fix favorable homeoallelic interactions within inbred varieties. We present a subfunctionalization epistasis model to estimate the degree of functional redundancy between homeoallelic loci and a statistical framework to determine their importance within a population. We provide an example using the homeologous dwarfing genes of allohexaploid wheat,
MeSH term(s)	Epistasis, Genetic ; Hybrid Vigor ; Hybridization, Genetic ; Plant Breeding/methods ; Triticum/genetics ; Triticum/growth & development
Language	English
Publishing date	2019-01-24
Publishing country	United States
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2167-2
ISSN	1943-2631 ; 0016-6731
ISSN (online)	1943-2631
ISSN	0016-6731
DOI	10.1534/genetics.118.301851
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Article ; Online: Prediction of Subgenome Additive and Interaction Effects in Allohexaploid Wheat.

Santantonio, Nicholas / Jannink, Jean-Luc / Sorrells, Mark

G3 (Bethesda, Md.)

2019 Volume 9, Issue 3, Page(s) 685–698

Abstract: Whole genome duplications have played an important role in the evolution of angiosperms. These events often occur through hybridization between closely related species, resulting in an allopolyploid with multiple subgenomes. With the availability of ... ...

Abstract	Whole genome duplications have played an important role in the evolution of angiosperms. These events often occur through hybridization between closely related species, resulting in an allopolyploid with multiple subgenomes. With the availability of affordable genotyping and a reference genome to locate markers, breeders of allopolyploids now have the opportunity to manipulate subgenomes independently. This also presents a unique opportunity to investigate epistatic interactions between homeologous orthologs across subgenomes. We present a statistical framework for partitioning genetic variance to the subgenomes of an allopolyploid, predicting breeding values for each subgenome, and determining the importance of inter-genomic epistasis. We demonstrate using an allohexaploid wheat breeding population evaluated in Ithaca, NY and an important wheat dataset from CIMMYT previously shown to demonstrate non-additive genetic variance. Subgenome covariance matrices were constructed and used to calculate subgenome interaction covariance matrices for variance component estimation and genomic prediction. We propose a method to extract population structure from all subgenomes at once before covariances are calculated to reduce collinearity between subgenome estimates. Variance parameter estimation was shown to be reliable for additive subgenome effects, but was less reliable for subgenome interaction components. Predictive ability was equivalent to current genomic prediction methods. Including only inter-genomic interactions resulted in the same increase in accuracy as modeling all pairwise marker interactions. Thus, we provide a new tool for breeders of allopolyploid crops to characterize the genetic architecture of existing populations, determine breeding goals, and develop new strategies for selection of additive effects and fixation of inter-genomic epistasis.
MeSH term(s)	Epistasis, Genetic ; Genome, Plant ; Genomics/methods ; Polyploidy ; Software ; Triticum/genetics
Language	English
Publishing date	2019-03-07
Publishing country	United States
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2629978-1
ISSN	2160-1836 ; 2160-1836
ISSN (online)	2160-1836
ISSN	2160-1836
DOI	10.1534/g3.118.200613
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Article ; Online: A Low Resolution Epistasis Mapping Approach To Identify Chromosome Arm Interactions in Allohexaploid Wheat.

Santantonio, Nicholas / Jannink, Jean-Luc / Sorrells, Mark

G3 (Bethesda, Md.)

2019 Volume 9, Issue 3, Page(s) 675–684

Abstract: Epistasis is an important contributor to genetic variance. In inbred populations, pairwise epistasis is present as additive by additive interactions. Testing for epistasis presents a multiple testing problem as the pairwise search space for modest ... ...

Abstract	Epistasis is an important contributor to genetic variance. In inbred populations, pairwise epistasis is present as additive by additive interactions. Testing for epistasis presents a multiple testing problem as the pairwise search space for modest numbers of markers is large. Single markers do not necessarily track functional units of interacting chromatin as well as haplotype based methods do. To harness the power of multiple markers while minimizing the number of tests conducted, we present a low resolution test for epistatic interactions across whole chromosome arms. Epistasis covariance matrices were constructed from the additive covariances of individual chromosome arms. These covariances were subsequently used to estimate an epistatic variance parameter while correcting for background additive and epistatic effects. We find significant epistasis for 2% of the interactions tested for four agronomic traits in a winter wheat breeding population. Interactions across homeologous chromosome arms were identified, but were less abundant than other chromosome arm pair interactions. The homeologous chromosome arm pair 4BL/4DL showed a strong negative relationship between additive and interaction effects that may be indicative of functional redundancy. Several chromosome arms appeared to act as hubs in an interaction network, suggesting that they may contain important regulatory factors. The differential patterns of epistasis across different traits demonstrate that detection of epistatic interactions is robust when correcting for background additive and epistatic effects in the population. The low resolution epistasis mapping method presented here identifies important epistatic interactions with a limited number of statistical tests at the cost of low precision.
MeSH term(s)	Chromosomes, Plant/metabolism ; Epistasis, Genetic ; Genomics/methods ; Polyploidy ; Triticum/genetics
Language	English
Publishing date	2019-03-07
Publishing country	United States
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2629978-1
ISSN	2160-1836 ; 2160-1836
ISSN (online)	2160-1836
ISSN	2160-1836
DOI	10.1534/g3.118.200646
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