Genome wide association study identifies novel single nucleotide polymorphic loci and candidate genes involved in the expression of sudden death syndrome resistance in soybean

Authors: SWAMINATHAN, SIVAKUMAR - Iowa State University; DAS, ANINDYA - Iowa State University; ASSEFA, TESHALE - Iowa State University; KNIGHT, JOSHUA - Iowa State University; FERREIRA DA SILVA, AMILTON - Iowa State University; Hartman, Glen; HUANG, XIAOQIU - Iowa State University; LEANDRO, LEONOR - Iowa State University; CIANZIO, SILVIA - Iowa State University; BHATTACHARYYA, MADAN - Iowa State University

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/15/2019
Publication Date: 2/26/2019
Citation: Swaminathan, S., Das, A., Assefa, T., Knight, J.M., Ferreira Da Silva, A., Hartman, G.L., Huang, X., Leandro, L.F., Cianzio, S.R., Bhattacharyya, M.K. 2019. Genome wide association study identifies novel single nucleotide polymorphic loci and candidate genes involved in the expression of sudden death syndrome resistance in soybean. PLoS One. https://doi.org/10.1371/journal.pone.0212071.
DOI: https://doi.org/10.1371/journal.pone.0212071

Interpretive Summary: A soil borne fungus causes sudden death syndrome of soybean in North America. It is a serious fungal pathogen that suppresses soybean yield by over $0.5 billion annually. The fungus infects the roots and causes root rot, and it secretes toxin(s) that causes chlorosis and necrosis in leaves. Resistance to the fungal pathogen in soybean is partial and quantitative and governed by more than 80 loci. A genome-wide association study using 254 soybean plant introduction (PI) lines and disease ratings of sudden death syndrome foliar and root rot symptoms revealed 14 quantitative trait loci associated with resistance to foliar sudden death syndrome and eight with root rot resistance. Ten PI lines identified with high levels of resistance to foliar disease and root rot will be good donors in breeding programs to enhance sudden death syndrome resistance in soybean. The four candidate genes for foliar sudden death syndrome and root rot resistance identified in this study can be used as genetic markers in breeding soybean for sudden death syndrome resistance. The information in this study will be useful to soybean breeders, geneticists, and pathologists interested in developing elite soybean lines with sudden death syndrome resistance.

Technical Abstract: Fusarium virguliforme causes sudden death syndrome (SDS) of soybean [Glycine max (L.) Merrill] in North America. It is a serious fungal pathogen that suppresses soybean yield to a value of over $0.5 billion annually. F. virguliforme infects the roots and causes root rot. Once the fungus invades the xylem tissues, it secretes toxin(s) that causes chlorosis and necrosis in foliar tissues. Resistance to F. virguliforme in soybean is partial and quantitative and governed by quantitative trait loci (QTL). More than 80 SDS resistance QTL, each contributing small effects, have been reported. QTL for both foliar SDS and root rot resistances should be considered in breeding SDS resistant soybean cultivars. We have conducted genome-wide association study (GWAS) for a group of 254 plant introductions (PI) lines preselected from over 6,000 lines to identify genetic loci associated with both foliar SDS and root rot resistance. GWAS revealed 14 single nucleotide polymorphic loci (SNPL) that are significantly associated with foliar SDS and eight SNPL with root rot resistance. Of the identified 22 SNPL for SDS resistance, six SNPL for foliar SDS resistance and two SNPL for root rot resistance co-mapped to prior QTL for SDS resistance. Thus, this study identified 14 novel SNPL, eight governing foliar SDS resistance and six root-rot resistance. In three foliar SDS resistance SNPL and two root rot resistance SNPL, the nonsynonymous mutations most likely altered immunity functions of five proteins by changing their (i) regulation or (ii) structure and function. Of these five genes containing nonsynonymous mutations, Glyma.01G222900.1 encodes a soybean-specific LEA protein and Glyma.10G058700.1 encodes a heparan-alpha-glucosaminide N-acetyltransferase, which are strong candidates for expressing root rot resistance. In the LEA protein a conserved serine residue was substituted with asparagine, and in the heparan-alpha-glucosaminide N-acetyltransferase a conserved histidine residue was substituted with an arginine residue presumably resulting in loss of regulation of both proteins through phosphorylation. The study also identified two strong candidates for foliar SDS resistance genes, one encoding an LRR-receptor and the other one encoding a novel protein with unknown function. This investigation identified 10 PI lines with foliar disease scores < 2 and 10% or less root rot, making them suitable donors of foliar SDS and root rot resistance genes to enhance SDS resistance in soybean. The four candidate genes for foliar SDS and root rot resistance identified in this study can be used as perfect markers in breeding soybean for SDS resistance.