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. 2021 Mar 25:12:628443.
doi: 10.3389/fpls.2021.628443. eCollection 2021.

NAC Candidate Gene Marker for bgm-1 and Interaction With QTL for Resistance to Bean Golden Yellow Mosaic Virus in Common Bean

Alvaro Soler-Garzón  1 , Atena Oladzad  2 , James Beaver  3 , Stephen Beebe  4 , Rian Lee  2 , Juan David Lobaton  4   5 , Eliana Macea  4 , Phillip McClean  2 , Bodo Raatz  4 , Juan Carlos Rosas  6 , Qijian Song  7 , Phillip N Miklas  1   8
Affiliations

NAC Candidate Gene Marker for bgm-1 and Interaction With QTL for Resistance to Bean Golden Yellow Mosaic Virus in Common Bean

Alvaro Soler-Garzón et al. Front Plant Sci. .

Abstract

Genetic resistance is the primary means for control of Bean golden yellow mosaic virus (BGYMV) in common bean (Phaseolus vulgaris L.). Breeding for resistance is difficult because of sporadic and uneven infection across field nurseries. We sought to facilitate breeding for BGYMV resistance by improving marker-assisted selection (MAS) for the recessive bgm-1 gene and identifying and developing MAS for quantitative trait loci (QTL) conditioning resistance. Genetic linkage mapping in two recombinant inbred line populations and genome-wide association study (GWAS) in a large breeding population and two diversity panels revealed a candidate gene for bgm-1 and three QTL BGY4.1, BGY7.1, and BGY8.1 on independent chromosomes. A mutation (5 bp deletion) in a NAC (No Apical Meristem) domain transcriptional regulator superfamily protein gene Phvul.003G027100 on chromosome Pv03 corresponded with the recessive bgm-1 resistance allele. The five bp deletion in exon 2 starting at 20 bp (Pv03: 2,601,582) is expected to cause a stop codon at codon 23 (Pv03: 2,601,625), disrupting further translation of the gene. A T m -shift assay marker named PvNAC1 was developed to track bgm-1. PvNAC1 corresponded with bgm-1 across ∼1,000 lines which trace bgm-1 back to a single landrace "Garrapato" from Mexico. BGY8.1 has no effect on its own but exhibited a major effect when combined with bgm-1. BGY4.1 and BGY7.1 acted additively, and they enhanced the level of resistance when combined with bgm-1. T m -shift assay markers were generated for MAS of the QTL, but their effectiveness requires further validation.

Keywords: Phaseolus vulgaris; frameshift mutation; geminivirus; genome-wide association study; marker-assisted selection.

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Conflict of interest statement

The handling editor RP and the author PNM declare that they are affiliated with the INCREASE consortium on genetic resources in legumes. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
Candidate Phvul.003G027100 NAC gene model for bgm-1 in Phaseolus vulgaris: (A) Four primer pairs designed for amplifying the six exons of candidate gene Phvul.003G027100 (Supplementary Table 1B). Physical positions from reference genome v2.1 (G19833). (B) Tm-shift-assay marker (PvNAC1) designed for amplification of 5 bp indel region in second exon of Phvul.003G027100 in accessions G19833 (Bgm-1), BAT 93 (Bgm-1) and Tio Canela 75 (bgm-1). (C) Protein alignment of Phvul.003G027100 candidate gene for bgm-1 (DOR 476) revealed a stop-gain mutation in position 23. Effect of the indel frameshift mutation on transcription of the candidate gene among ten lines—three with and seven without bgm-1 modeled by Geneious® 9.1.8 software.
FIGURE 2
FIGURE 2
The CB_475_v3 marker developed for the five bp indel region in exon 2 of the candidate. (A) Phvul.003G027100 NAC gene for bgm-1 visualized by melting curve Tm-shift assay and (B) by gel electrophoresis.
FIGURE 3
FIGURE 3
Manhattan and QQ plots from GWAS (Supplementary Table 3B) in 412 CIAT breeding lines evaluated (1–9 disease score) in El Salvador (2015). With an LD heat-map view of the significant genomic region from 2.52 to 2.63 Mbp for bgm-1 on Pv03. The positions of candidate genes are shown.
FIGURE 4
FIGURE 4
Manhattan plot from GWAS (Supplementary Table 3C) in BASE_120 evaluated for % infection in Honduras in 2014. Tepary and Andean beans were excluded.
FIGURE 5
FIGURE 5
Manhattan plot from GWAS (Supplementary Table 3D) in BASE_Meso evaluated (R vs. S reactions) in Honduras in 2015.
FIGURE 6
FIGURE 6
Genetic mapping for resistance to BGYMV (1–9) evaluated in the DOR 364 x XAN 176 (DX) recombinant inbred population in Puerto Rico in spring 1994 (Miklas et al., 1996): (A) LOD profiles obtained by two-dimensional genome scans. The BGY4.1 and BGY7.1 QTL models were fitted and refined using the multiple imputation method. Dashed line denotes significance at the 0.05 probability level and (B) interaction between BGY4.1 and BGY7.1 QTL for resistance to BGYMV (see also Supplementary Figure S1).
FIGURE 7
FIGURE 7
Genetic mapping for resistance to BGYMV (1–9) evaluated in El Salvador in 2012 in DOR 476/SE. (DS) recombinant inbred population: (A) LOD profiles obtained by one-dimensional and two-dimensional genome scans. QTL models were fitted and refined using the multiple imputation method. Dashed line denotes significance at the 0.05 probability level and (B) interaction between bgm-1 and BGY8.1 for resistance to BGYMV.
FIGURE 8
FIGURE 8
Manhattan plot for a subpopulation of 128 lines from the CIAT population with bgm-1 (PvNAC1 gene marker) used for detection of QTL (BGY8.1) needing bgm-1 for expression.
FIGURE 9
FIGURE 9
Boxplot showing interaction between bgm-1 (PvNAC1 marker) and BGY8.1 QTL (SNP S08_9202267) in the CIAT population of 412 lines.
See this image and copyright information in PMC

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