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Association mapping for common bacterial blight in carioca beans

Abstract

Common bacterial blight (CBB) is an important disease in Phaseolus vulgaris L. A carioca diversity panel (CDP) composed of 149 cultivars of common bean was genotyped with 1,616 SNPs and evaluated for Xanthomonas phaseoli pv. phaseoli (Xap) resistance aiming to identify QTLs. Phenotypic evaluation was done in controlled conditions. The plants displayed in a randomized block design, with 3 replications were evaluated ten days after inoculation. GWAS analysis using the BLINK model identified one SNP on chromosome Pv07, with a different genomic location in relation to previous studies. Considering a confidence interval of 100 kb, gene annotation identified 13 candidate genes related to defense-associated genes, and their key functional motives were discussed. The marker identified may constitute an important resource for future marker assisted CBB resistance breeding.

Keywords:
Disease-resistance inheritance; Xap; GWAS

INTRODUCTION

Common bean accounts for a considerable proportion of daily nutrients (Assefa et al. 2019Assefa T, Assibi Mahama A, Brown AV, Cannon EKS, Rubyogo JC, Rao IM, Blair MW, Cannon BS2019 A review of breeding objectives, genomic resources, and marker-assisted methods in common bean (Phaseolus vulgaris L.). Molecular Breeding 39:20). Yield losses caused by plant diseases may reach up to 100%, depending on the aggressiveness of the pathogen (Simons et al. 2021Simons KJ, Oladzad A, Lamppa R, Maniruzzaman Maniruzzaman, McClean PE, Osorno JM, Pasche JS2021 Using breeding populations with a dual purpose: cultivar development and gene mapping - a case study using resistance to common bacterial blight in dry bean (Phaseolus vulgaris L.). Frontiers in Plant Science 12:621097). Xap is a gram-negative group of γ-proteobacteria. The symptoms of CBB are observable throughout the plant, manifesting effects from leaves to seeds (Rezene et al. 2018Rezene Y, Mitiku M, Tesfaye K, Male A, Gepts P2018 Analysis of the molecular diversity of common bacterial blight (Xanthomonas campestris pv. phaseoli and X. campestris pv. phaseoli var. fuscans) strains from Ethiopia revealed by Rep-PCR genomic fingerprinting. Journal of Biotechnology & Biomaterials 8:286, Belete and Bastas 2017Belete T, Bastas KK2017 Common bacterial blight (Xanthomonas axonopodis pv. phaseoli) of beans with special focus on Ethiopian condition. Journal of Plant Pathology & Microbiology 08:10). The pathogen has huge survivability, which can be enhanced by the low temperature conditions used in seed storage (Torres et al. 2009Torres JP, Silva Júnior TAF, Maringoni AC2009 Detecção de Xanthomonas axonopodis pv. phaseoli em sementes de feijoeiro provenientes do Estado do Paraná, Brasil. Summa Phytopathologica 35:136-139). The disease is present throughout Brazil and is found in all producing regions, especially in the rainy season (Torres et al. 2009Torres JP, Silva Júnior TAF, Maringoni AC2009 Detecção de Xanthomonas axonopodis pv. phaseoli em sementes de feijoeiro provenientes do Estado do Paraná, Brasil. Summa Phytopathologica 35:136-139).

Control of CBB includes crop management practices, use of chemical pesticides, and genetic resistance. Using chemical control as the main treatment is not effective as the pathogen is quite diverse (Rava and Sartorato 1994Rava CA, Sartorato A1994 Crestamento bacteriano comum. In Sartorato A and Rava CA (eds) Principais doenças do feijoeiro comum e seu controle. Embrapa, Brasília, p. 217-242). CBB genetic architecture involves both minor and major genes (Simons et al. 2021Simons KJ, Oladzad A, Lamppa R, Maniruzzaman Maniruzzaman, McClean PE, Osorno JM, Pasche JS2021 Using breeding populations with a dual purpose: cultivar development and gene mapping - a case study using resistance to common bacterial blight in dry bean (Phaseolus vulgaris L.). Frontiers in Plant Science 12:621097). Until now, up to 25 minor effect resistance loci have been identified across the common bean genome (Simons et al. 2021Simons KJ, Oladzad A, Lamppa R, Maniruzzaman Maniruzzaman, McClean PE, Osorno JM, Pasche JS2021 Using breeding populations with a dual purpose: cultivar development and gene mapping - a case study using resistance to common bacterial blight in dry bean (Phaseolus vulgaris L.). Frontiers in Plant Science 12:621097).

Genome-wide association studies (GWAS) are a powerful tool to unveil disease-resistance inheritance (Uffelmann et al. 2021Uffelmann E, Huang QQ, Munung NS, de Vries J, Okada Y, Martin AR, Martin HC, Lappalainen T, Posthuma D2021 Genome-wide association studies. Nature Reviews Methods Primers 1:59). For CBB resistance, Shi et al. (2011Shi C, Navabi A, Yu K2011 Association mapping of common bacterial blight resistance QTL in Ontario bean breeding populations. BMC Plant Biology 11:52) found twelve SNPs (Single Nucleotide Polymorphisms) with similar map positions to other CBB QTLs (Quantitative Trait Loci). Wu et al. (2017Wu J, Zhu J, Wang L, Wang S2017 Genome-wide association study identifies NBS-LRR-Encoding genes related with anthracnose and common bacterial blight in the common bean. Frontiers in Plant Science 8:1398) explored the association mapping of NBS-LRR (nucleotide binding site-leucine rich repeat) microsatellites and seven of them also mapped by Shi et al. (2011Shi C, Navabi A, Yu K2011 Association mapping of common bacterial blight resistance QTL in Ontario bean breeding populations. BMC Plant Biology 11:52). Ambachew et al. (2021Ambachew D, Joshua J, Mmbaga MT, Blair MW2021 Sources of resistance to common bacterial blight and charcoal rot disease for the production of mesoamerican common beans in the southern United States. Plants 10:998) detected 14 significant SNPs connected to CBB and over Pv02, Pv04, Pv08, Pv10, and Pv11. Simons et al. (2021Simons KJ, Oladzad A, Lamppa R, Maniruzzaman Maniruzzaman, McClean PE, Osorno JM, Pasche JS2021 Using breeding populations with a dual purpose: cultivar development and gene mapping - a case study using resistance to common bacterial blight in dry bean (Phaseolus vulgaris L.). Frontiers in Plant Science 12:621097) identified 8 regions, including 6 previously mapped and two new loci (Pv11 and Pv10).

The goal of this work was to perform the identification of CBB resistance loci by GWAS in carioca diversity panel. From the whole genome-wide investigation, one significant SNP with no overlap in relation to previous studies was found on Pv07, probably addressed to a particular resistance CBB-QTL derived from Brazilian carioca germplasm.

MATERIAL AND METHODS

Plant material and SNP analysis

The CDP of 149 carioca accessions selected from the Germplasm Bank of the Instituto Agronômico, Campinas, SP, Brazil (Almeida et al. 2020Almeida CP, Paulino JFC, Carbonell SAM, Chiorato AF, Song Q, Di Vittori V, Rodriguez M, Papa R, Benchimol-Reis LL2020 Genetic diversity, population structure, and andean introgression in brazilian common bean cultivars after half a century of genetic breeding. Genes 11:1298, Almeida et al. 2021) was used in this study. The CDP consists of some ancient commercial cariocas to recent released cultivars (Almeida et al. 2021Almeida CP, Santos IL, Carvalho Paulino JF, Barbosa CCF, Pereira CCA, Carvalho CRL, Moraes Cunha Gonçalves G, Song Q, Carbonell SAM, Chiorato AF, Benchimol-Reis LL2021 Genome-wide association mapping reveals new loci associated with light-colored seed coat at harvest and slow darkening in carioca beans. BMC Plant Biology 21:343).

The carioca accessions were genotyped using a BARCBean6K_3 - Illumina composed of 5,398 SNPs and 1,616 SNPs were filtered and used. Genotypic data was analyzed by TASSEL 5.0 software (Bradbury et al. 2007Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES2007 TASSEL: Software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633-2635), and SNPs with MAF (minor allele frequency) < 3%, heterozygosity > 5%, and missing data > 10% were removed. The promising modern BLINK model (Huang et al. 2019Huang M, Liu X, Zhou Y, Summers RM, Zhang Z2019 BLINK: a package for the next level of genome-wide association studies with both individuals and markers in the millions. Gigascience 8: giy154.) was used for GWAS analysis. Clusters were absent from principal component analysis (PCA) (Figure 1S), and based on that, no correction for population structure was needed. The thresholds of 5% and 1% were applied on the Manhattan plot. ANOVA (analysis of variance) was carried out for comparing means between different groups (Ferreira et al. 2014Ferreira EB, Cavalcanti PP, Nogueira DA2014 ExpDes: An R package for ANOVA and experimental designs. Applied Mathematics 5:2952-2958), and the RBio software (Bhering 2017Bhering LL2017 Rbio: A tool for biometric and statistical analysis using the R platform. Crop Breeding and Applied Biotechnology 17:187-190) was used for estimating the selective accuracy. The REML/BLUE (Restricted Maximum Likelihood/Best Linear Unbiased Estimator) model was used to measure the genotypic values by the Be-Breeder package (Matias et al. 2018Matias FI, Granato I, Fritsche-Neto R2018 Be-Breeder: an R/Shiny application for phenotypic data analyses in plant breeding. Crop Breeding and Applied Biotechnology 18:241-243). Each marker´s flanking sequence was blasted against the Phaseolus vulgaris v2.1 (Schmutz et al. 2014Schmutz J, McClean PE, Mamidi S, Wu GA, Cannon SB, Grimwood J, Jenkins J, Shu S, Song Q, Chavarro C, Torres-Torres M, Geffroy V, Moghaddam SM, Gao D, Abernathy B, Barry K, Blair M, Brick MA, Chovatia M, Gepts P, Goodstein DM, Gonzales M, Hellsten U, Hyten DL, Jia G, Kelly JD, Kudrna D, Lee R, Richard MMS, Osorno JM, Rodrigues J, Thareau V, Urrea CA, Wang M, Yu Y, Zhang M, Wing RA, Cregan PB, Rokhsar DS, Jackson SA2014 A reference genome for common bean and genome-wide analysis of dual domestications. Nature Genetics 46:707-713, G19833 genome). For the Blast search, 100 kb (confidence window) was considered, lower than the CDP´s LD decay (rmean 2 = 0.046, Almeida et al. 2020Almeida CP, Paulino JFC, Carbonell SAM, Chiorato AF, Song Q, Di Vittori V, Rodriguez M, Papa R, Benchimol-Reis LL2020 Genetic diversity, population structure, and andean introgression in brazilian common bean cultivars after half a century of genetic breeding. Genes 11:1298). Unknown positioned markers were not considered, and the imputation performance was achieved by the Beagle 5.0 (Browning et al. 2018Browning BL, Zhou Y, Browning SR2018 A one-penny imputed genome from next-generation reference panels. The American Journal of Human Genetics 103:338-348).

Figure 1
Diagrammatic severity scale (percentage of diseased leaf area, Rava 1984Rava CA1984 Patogenicidade de isolados de Xanthomonas campestres pv. phaseoli. Pesquisa Agropecuária Brasileira 19:445-448) for CBB: Score 1: Green leaves and no symptoms; score 2: Slight yellowing in the cuts of the leaf; score 3: Yellowing extending slightly even between the cuts of the leaf; score 4: Necrosis in the cuts and strong yellowing between the cuts; score 5: Same aspect as 4, but with yellowing above and below the cuts; score 6: Totally damaged leaf.

Pathogenicity test

The pathogenicity of three isolates (Xap 19, from Ponta Grossa, PR, Brazil; Xap 96, from Guarapuava, PR, Brazil; and XFF 205, from an unknown source - all provided by EMBRAPA) was confirmed by artificially inoculating the isolates on the leaves of 18 common bean genotypes (Table 1). The plates with yeast dextrose carbonate (YDC) medium were stored at 30 °C for 48 h in a Biological Oxygen Demand incubator (BOD). The inoculum of each isolate was around 107 colony-forming units, CFU / ml. The plants were grown in pots under greenhouse conditions, and at ten days of age, their primary leaves were inoculated using the leaf incision method, which consists of making two cuts perpendicular to the midrib, without reaching it, at a spacing of only two centimeters, with the aid of a scissors previously dipped in the bacterial suspension (Rava 1984Rava CA1984 Patogenicidade de isolados de Xanthomonas campestres pv. phaseoli. Pesquisa Agropecuária Brasileira 19:445-448). Severity was evaluated using the 1-6 scoring scale proposed by Rava (1984Rava CA1984 Patogenicidade de isolados de Xanthomonas campestres pv. phaseoli. Pesquisa Agropecuária Brasileira 19:445-448).

Table 1
Pathogenicity test with 18 genotypes and three isolates of common bacterial blight: XAP 19, XAP 96, XAFF 205. Reactions were divided in resistant plants (R) scored as 1; moderately resistant (MR) plants with scores between 1.1 and 3; and susceptible (S) plants, with scores between 3.1 and 6

CBB´s severity assessment in the CDP

The experiment was executed with an experimental design of a randomized block design with three replications at the Instituto Agronômico (IAC, Campinas, SP) in a greenhouse. The Xap 19 inoculum was prepared as reported above. Plants with ten days of age were inoculated using the same approach as described in the pathogenicity test item above, making 4 cuts per leaf (Figure 1). The rest of the inoculum was sprayed on the plants. The pots, with 2 plants each, were distributed in trays. A control genotype was used within each block (‘IAC Formoso’). An automatic sprinkler irrigation system was set up in the greenhouse, as high humidity promotes the disease. Ten days after inoculation, the severity of CBB was evaluated (Rava 1984Rava CA1984 Patogenicidade de isolados de Xanthomonas campestres pv. phaseoli. Pesquisa Agropecuária Brasileira 19:445-448). Scores were assigned to each plant in the plot, and the mean values of the block were subsequently calculated. The Scott-Knott test was used in the application of ANOVA. Data was transformed using the Box-Cox technique, with a lambda (λ) = 0.16.

RESULTS AND DISCUSSION

All isolates were pathogenic when inoculated onto susceptible bean cultivars (Table 1), and the cultivars exhibited visual symptoms. However, there was no carioca plant resistant (score 1) to Xap 19 among the 18 carioca bean genotypes. Xap 19 was the most aggressive isolate, and it was chosen to evaluate the severity of the CDP. Concerning phenotypical evaluation of the CPD, original and normalized results were presented (Figure 2).

Figure 2
Histogram with (A) original CDP severity average scores and (B) normalized distribution of phenotypical CDP severity scores. Due to the non-normality of the data, the transformation was performed using the BoxCox test, with a lambda (λ) = 0.16.

The mean scores of the genotypes of the CPD (Table 1S) show that no carioca genotype was fully resistant (score 1), only 22 (15%) were moderately resistant (score 1.1-3), and the remaining 127 (85%) were susceptible (score >3) to CBB disease. Statistical analysis (Table 2) showed a low CV (coefficient of variation, 2.4%) and, consequently, high accuracy for the experiment. In addition, ANOVA showed significant difference between treatments (Table 2). The BoxPlot offered a comparison of the mean scores between blocks 1, 2, and 3 (Figure 3). Block 2 contained a larger number of susceptible genotypes.

Table 2
Two-way ANOVA for the CBB phenotypical severity data referred to the 149 beans from the carioca diversity panel (CDP)

Figure 3
BoxPlot for the scores obtained for each block (1, 2 and 3) for the phenotypical severity evaluation of CBB resistance on the 149 carioca genotypes from the CDP panel.

This study used the same carioca diversity panel (CDP) as Almeida et al. (2020Almeida CP, Paulino JFC, Carbonell SAM, Chiorato AF, Song Q, Di Vittori V, Rodriguez M, Papa R, Benchimol-Reis LL2020 Genetic diversity, population structure, and andean introgression in brazilian common bean cultivars after half a century of genetic breeding. Genes 11:1298). Considering the Phaseolus genome (~587 Mb) size and the LD decay reported by Almeida et al. (2020), the minimum number of SNPs required for a study like this would be 995. In this study, through the BLINK association model, a SNP (ss715650404) was identified on chromosome Pv07 at position 46.7 Mb (Figure 4). A total of 1,616 SNPs were used to perform GWAS for CBB resistance (Table 2S), the same number of markers of other studies (Almeida et al. 2020Almeida CP, Paulino JFC, Carbonell SAM, Chiorato AF, Song Q, Di Vittori V, Rodriguez M, Papa R, Benchimol-Reis LL2020 Genetic diversity, population structure, and andean introgression in brazilian common bean cultivars after half a century of genetic breeding. Genes 11:1298, Almeida et al. 2021Almeida CP, Santos IL, Carvalho Paulino JF, Barbosa CCF, Pereira CCA, Carvalho CRL, Moraes Cunha Gonçalves G, Song Q, Carbonell SAM, Chiorato AF, Benchimol-Reis LL2021 Genome-wide association mapping reveals new loci associated with light-colored seed coat at harvest and slow darkening in carioca beans. BMC Plant Biology 21:343).

Figure 4
A) Manhattan plot for 1,616 SNPs using the carioca diversity panel (CDP) for Xanthomonas axonopodis pv. phaseoli resistance and B) Q-Q Plot generated by the Blink model. The green lines correspond to the cut-off lines obtained by bootstrapping and by the Bonferroni method (α =0.05 and 0.01).

Wu et al. (2017Wu J, Zhu J, Wang L, Wang S2017 Genome-wide association study identifies NBS-LRR-Encoding genes related with anthracnose and common bacterial blight in the common bean. Frontiers in Plant Science 8:1398), surveying NBS-LRR-encoding genes associated with CBB, found that NSSR245 (Pv7, 49260558-49310456 bp in G19833) was associated with CBB architecture and may be in the similar genomic regions (Yu et al. 2004Yu K, Park SJ, Zhang B, Haffner M, Poysa V2004 An SSR marker in the nitrate reductase gene of common bean is tightly linked to a major gene conferring resistance to common bacterial blight. Euphytica 138:89-95, Shi et al. 2011Shi C, Navabi A, Yu K2011 Association mapping of common bacterial blight resistance QTL in Ontario bean breeding populations. BMC Plant Biology 11:52). Zhu et al. (2016Zhu J, Wu J, Wang L, Blair MW, Zhu Z, Wang S2016 QTL and candidate genes associated with common bacterial blight resistance in the common bean cultivar Longyundou 5 from China. The Crop Journal 4:344-352) revealed two markers, BMp10s174 and BMp10s244, on Pv10 (39,730,677 and 40,002,585 bp in G19833). Ambachew et al. (2021Ambachew D, Joshua J, Mmbaga MT, Blair MW2021 Sources of resistance to common bacterial blight and charcoal rot disease for the production of mesoamerican common beans in the southern United States. Plants 10:998) found SNPs with minor effects associated with common bacterial blight resistance on Pv02 (8,541,089 bp), Pv04 (29,756,136 bp), Pv08 (24,383,486; 55,730,740; 55,730,740; 8,738,278 bp), Pv10 (1,437,174 bp), and Pv11 (25,981,923 bp). Among them, Pv08 and Pv10 concentrated most of the CBB resistance genes. Simons et al. (2021Simons KJ, Oladzad A, Lamppa R, Maniruzzaman Maniruzzaman, McClean PE, Osorno JM, Pasche JS2021 Using breeding populations with a dual purpose: cultivar development and gene mapping - a case study using resistance to common bacterial blight in dry bean (Phaseolus vulgaris L.). Frontiers in Plant Science 12:621097) reported a SNP on Pv07 associated with CBB susceptibility at a different location (28.50-28.84 Mb) from the one detected in this study (46.7 Mb).

Considering a confidence interval of 100 kb (Table 3) used to search the candidate genes on both side of the SNP detected as significant, gene annotation identified 13 putative candidate genes related to disease response. Allene oxide synthase (AOS, Phvul. 007.G055700.1) contributes to the biosynthesis of the jasmonic acid (JA). The Castanea crenata allene oxide synthase transformed in Arabidopsis improves defense against soilborne pathogen Phytophthora cinnamomi (Serrazina et. al. 2021Serrazina S, Machado H, Costa RL, Duque P, Malhó R2021 Expression of Castanea crenata allene oxide synthase in Arabidopsis improves the defense to Phytophthora cinnamomi. Frontiers in Plant Science 12:628697). HAD hydrolases, subfamily I (Phvul.007G056300.1) is modulated by Pi starvation and cyclopentenone oxylipins induction (Caparrós-Martín et al. 2013Caparrós-Martín JA, McCarthy-Suárez I, Culiáñez-Macià FA2013 HAD hydrolase function unveiled by substrate screening: enzymatic characterization of Arabidopsis thaliana subclass I phosphosugar phosphatase AtSgpp. Planta 237:943-954).

Table 3
Gene annotation in a 100 kb window for the significative SNP (ss715650404) mapped for Xanthomonas axonopodis pv. phaseoli (Xap19) evaluation on the CDP of 149 genotypes of common beans

The establishment of Pseudomonas syringae in Arabidopsis (Jones et al. 2006Jones AM, Thomas V, Bennett MH, Mansfield J, Grant M2006 Modifications to the Arabidopsis defense proteome occur prior to significant transcriptional change in response to inoculation with Pseudomonas syringae. Plant Physiology 142:1603-1620) and indicated that components of PSII had been modified during the R-gene-mediated hypersensitive reaction (HR). In this study, we identified photosystem I, subunit D-2 (Phvul.007G055900.1) as a candidate gene mediating the CBB defense response. Medina-Puche et al. (2020Medina-Puche L, Tan H, Dogra V, Wu M, Rosas-Diaz T, Wang L, Ding X, Zhang D, Fu X, Kim C, Lozano-Duran R2020 A defense pathway linking plasma membrane and chloroplasts and co-opted by pathogens. Cell 182:1109-1124) affirm the role of chloroplasts due to biotic threat initiating a signaling pathway that bursts of the pathogenesis-related proteins. Another candidate gene annotation was S-Adenosyl-L-methionine (SAM) (Phvul.007G056100.1), a universal biological cofactor that is involved with salicylic acid, a key enzyme in many important biological processes (Ross et al. 1999Ross JR, Nam KH, D'Auria JC, Pichersky E1999 S-Adenosyl-L-methionine: salicylic acid carboxyl methyltransferase, an enzyme involved in floral scent production and plant defense, represents a new class of plant methyltransferases. Archives of Biochemistry and Biophysics 367:9-16).

We identified a Sec14p-like phosphatidylinositol transfer family protein (Phvul.007G056700.1) among the annotated genes. The expression of NbSEC14 (Sec14 phospholipid transfer protein) from Nicotiana benthamiana was induced by PAMPs (pathogen-associated molecular pattern), such as those including flg22 and chitin (Kiba et al. 2018Kiba A, Nakano M, Ohnishi K, Hikichi Y2018 The SEC14 phospholipid transfer protein regulates pathogen-associated molecular pattern-triggered immunity in Nicotiana benthamiana. Plant Physiology and Biochemistry 125:212-218). Major facilitator superfamily (MFS, Phvul.007G055200.1; Phvul.007G055500.1) transporters plays a central role in pathogenesis-related processes (Paulsen 2003Paulsen IT2003 Multidrug efflux pumps and resistance: Regulation and evolution. Current Opinion in Microbiology 6:446-451). Amine oxidases are multifunctional enzymes that catalyze the oxidative deamination of polyamines (Cona et al. 2006Cona A, Rea G, Angelini R, Federico R, Tavladoraki P2006 Functions of amine oxidases in plant development and defense. Trends in Plant Science 11:80-88; Phvul.007G056600.1). Polyamine oxidases (PAOs) can be oxidatively deaminated by amine oxidases, leading to ROS-dependent stress signaling (Moschou 2018Moschou PN2018 Determination of di−/Polyamine oxidase activity in plants by an in-gel spermidine oxidation assay. In Alcázar R and Tiburcio A (eds) Polyamines. Humana Press, New York, p. 183-194). One class of amine oxidases is the copper-containing amine oxidase (CuAO, Liu et al. 2020Liu C, Atanasov KE, Arafaty N, Murillo E, Tiburcio AF, Zeier J, Alcázar R2020 Putrescine elicits ROS-dependent activation of the salicylic acid pathway in Arabidopsis thaliana. Plant, Cell & Environment 43:2755-2768, Phvul.007G056200.1; Phvul.007G056400.2; Phvul.007G056500.1), and it has a confirmed role in defense response (Angelini et al. 1993Angelini R, Bragaloni M, Federico R, Infantino A, Portapuglia A1993 Involvement of polyamines, diamine oxidase and peroxidase in resistance of chickpea to Ascochyta rabiei. Journal of Plant Physiology 142:704-709). The PLAT/LH2 (Phvul.007G055600.1; Phvul.007G055800.1) domain conciliates enzyme-membrane interaction (Newcomer and Brash 2015Newcomer ME, Brash AR2015 The structural basis for specificity in lipoxygenase catalysis. Protein Science 24:298-309). Pingault et al. (2021Pingault L, Varsani S, Palmer N, Ray S, Williams WP, Luthe DS, Ali JG, Sarath G, Louis J2021 Transcriptomic and volatile signatures associated with maize defense against corn leaf aphid. BMC Plant Biology 21:138) reported that plant LOXs (Lipoxygenases) production may be modulated by plant diseases. A LOX-1 ortholog on Pv10 was related to common bacterial blight resistance (Simons et al. 2021Simons KJ, Oladzad A, Lamppa R, Maniruzzaman Maniruzzaman, McClean PE, Osorno JM, Pasche JS2021 Using breeding populations with a dual purpose: cultivar development and gene mapping - a case study using resistance to common bacterial blight in dry bean (Phaseolus vulgaris L.). Frontiers in Plant Science 12:621097).

Using a carioca diversity panel, GWAS identified a new genomic region connected with common bacterial blight in Phaseolus vulgaris. The SNP ss715650404 identified offers potential in selecting candidate genes that may be useful markers for screening of carioca lines with superior common bacterial blight resistance in the plant breeding process.

ACKNOWLEDGEMENTS

The authors thank to the CNPq for the financial aid conceded. Supplemental files (Tables 1S, 2S and Figure 1S) are available with the corresponding author.

REFERENCES

  • Almeida CP, Paulino JFC, Carbonell SAM, Chiorato AF, Song Q, Di Vittori V, Rodriguez M, Papa R, Benchimol-Reis LL2020 Genetic diversity, population structure, and andean introgression in brazilian common bean cultivars after half a century of genetic breeding. Genes 11:1298
  • Almeida CP, Santos IL, Carvalho Paulino JF, Barbosa CCF, Pereira CCA, Carvalho CRL, Moraes Cunha Gonçalves G, Song Q, Carbonell SAM, Chiorato AF, Benchimol-Reis LL2021 Genome-wide association mapping reveals new loci associated with light-colored seed coat at harvest and slow darkening in carioca beans. BMC Plant Biology 21:343
  • Ambachew D, Joshua J, Mmbaga MT, Blair MW2021 Sources of resistance to common bacterial blight and charcoal rot disease for the production of mesoamerican common beans in the southern United States. Plants 10:998
  • Angelini R, Bragaloni M, Federico R, Infantino A, Portapuglia A1993 Involvement of polyamines, diamine oxidase and peroxidase in resistance of chickpea to Ascochyta rabiei. Journal of Plant Physiology 142:704-709
  • Assefa T, Assibi Mahama A, Brown AV, Cannon EKS, Rubyogo JC, Rao IM, Blair MW, Cannon BS2019 A review of breeding objectives, genomic resources, and marker-assisted methods in common bean (Phaseolus vulgaris L.). Molecular Breeding 39:20
  • Belete T, Bastas KK2017 Common bacterial blight (Xanthomonas axonopodis pv. phaseoli) of beans with special focus on Ethiopian condition. Journal of Plant Pathology & Microbiology 08:10
  • Bhering LL2017 Rbio: A tool for biometric and statistical analysis using the R platform. Crop Breeding and Applied Biotechnology 17:187-190
  • Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES2007 TASSEL: Software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633-2635
  • Browning BL, Zhou Y, Browning SR2018 A one-penny imputed genome from next-generation reference panels. The American Journal of Human Genetics 103:338-348
  • Caparrós-Martín JA, McCarthy-Suárez I, Culiáñez-Macià FA2013 HAD hydrolase function unveiled by substrate screening: enzymatic characterization of Arabidopsis thaliana subclass I phosphosugar phosphatase AtSgpp. Planta 237:943-954
  • Cona A, Rea G, Angelini R, Federico R, Tavladoraki P2006 Functions of amine oxidases in plant development and defense. Trends in Plant Science 11:80-88
  • Ferreira EB, Cavalcanti PP, Nogueira DA2014 ExpDes: An R package for ANOVA and experimental designs. Applied Mathematics 5:2952-2958
  • Huang M, Liu X, Zhou Y, Summers RM, Zhang Z2019 BLINK: a package for the next level of genome-wide association studies with both individuals and markers in the millions. Gigascience 8: giy154.
  • Jones AM, Thomas V, Bennett MH, Mansfield J, Grant M2006 Modifications to the Arabidopsis defense proteome occur prior to significant transcriptional change in response to inoculation with Pseudomonas syringae. Plant Physiology 142:1603-1620
  • Kiba A, Nakano M, Ohnishi K, Hikichi Y2018 The SEC14 phospholipid transfer protein regulates pathogen-associated molecular pattern-triggered immunity in Nicotiana benthamiana. Plant Physiology and Biochemistry 125:212-218
  • Liu C, Atanasov KE, Arafaty N, Murillo E, Tiburcio AF, Zeier J, Alcázar R2020 Putrescine elicits ROS-dependent activation of the salicylic acid pathway in Arabidopsis thaliana. Plant, Cell & Environment 43:2755-2768
  • Matias FI, Granato I, Fritsche-Neto R2018 Be-Breeder: an R/Shiny application for phenotypic data analyses in plant breeding. Crop Breeding and Applied Biotechnology 18:241-243
  • Medina-Puche L, Tan H, Dogra V, Wu M, Rosas-Diaz T, Wang L, Ding X, Zhang D, Fu X, Kim C, Lozano-Duran R2020 A defense pathway linking plasma membrane and chloroplasts and co-opted by pathogens. Cell 182:1109-1124
  • Moschou PN2018 Determination of di−/Polyamine oxidase activity in plants by an in-gel spermidine oxidation assay. In Alcázar R and Tiburcio A (eds) Polyamines. Humana Press, New York, p. 183-194
  • Newcomer ME, Brash AR2015 The structural basis for specificity in lipoxygenase catalysis. Protein Science 24:298-309
  • Paulsen IT2003 Multidrug efflux pumps and resistance: Regulation and evolution. Current Opinion in Microbiology 6:446-451
  • Pingault L, Varsani S, Palmer N, Ray S, Williams WP, Luthe DS, Ali JG, Sarath G, Louis J2021 Transcriptomic and volatile signatures associated with maize defense against corn leaf aphid. BMC Plant Biology 21:138
  • Rava CA1984 Patogenicidade de isolados de Xanthomonas campestres pv. phaseoli. Pesquisa Agropecuária Brasileira 19:445-448
  • Rava CA, Sartorato A1994 Crestamento bacteriano comum. In Sartorato A and Rava CA (eds) Principais doenças do feijoeiro comum e seu controle. Embrapa, Brasília, p. 217-242
  • Rezene Y, Mitiku M, Tesfaye K, Male A, Gepts P2018 Analysis of the molecular diversity of common bacterial blight (Xanthomonas campestris pv. phaseoli and X. campestris pv. phaseoli var. fuscans) strains from Ethiopia revealed by Rep-PCR genomic fingerprinting. Journal of Biotechnology & Biomaterials 8:286
  • Ross JR, Nam KH, D'Auria JC, Pichersky E1999 S-Adenosyl-L-methionine: salicylic acid carboxyl methyltransferase, an enzyme involved in floral scent production and plant defense, represents a new class of plant methyltransferases. Archives of Biochemistry and Biophysics 367:9-16
  • Schmutz J, McClean PE, Mamidi S, Wu GA, Cannon SB, Grimwood J, Jenkins J, Shu S, Song Q, Chavarro C, Torres-Torres M, Geffroy V, Moghaddam SM, Gao D, Abernathy B, Barry K, Blair M, Brick MA, Chovatia M, Gepts P, Goodstein DM, Gonzales M, Hellsten U, Hyten DL, Jia G, Kelly JD, Kudrna D, Lee R, Richard MMS, Osorno JM, Rodrigues J, Thareau V, Urrea CA, Wang M, Yu Y, Zhang M, Wing RA, Cregan PB, Rokhsar DS, Jackson SA2014 A reference genome for common bean and genome-wide analysis of dual domestications. Nature Genetics 46:707-713
  • Serrazina S, Machado H, Costa RL, Duque P, Malhó R2021 Expression of Castanea crenata allene oxide synthase in Arabidopsis improves the defense to Phytophthora cinnamomi. Frontiers in Plant Science 12:628697
  • Shi C, Navabi A, Yu K2011 Association mapping of common bacterial blight resistance QTL in Ontario bean breeding populations. BMC Plant Biology 11:52
  • Simons KJ, Oladzad A, Lamppa R, Maniruzzaman Maniruzzaman, McClean PE, Osorno JM, Pasche JS2021 Using breeding populations with a dual purpose: cultivar development and gene mapping - a case study using resistance to common bacterial blight in dry bean (Phaseolus vulgaris L.). Frontiers in Plant Science 12:621097
  • Torres JP, Silva Júnior TAF, Maringoni AC2009 Detecção de Xanthomonas axonopodis pv. phaseoli em sementes de feijoeiro provenientes do Estado do Paraná, Brasil. Summa Phytopathologica 35:136-139
  • Uffelmann E, Huang QQ, Munung NS, de Vries J, Okada Y, Martin AR, Martin HC, Lappalainen T, Posthuma D2021 Genome-wide association studies. Nature Reviews Methods Primers 1:59
  • Wu J, Zhu J, Wang L, Wang S2017 Genome-wide association study identifies NBS-LRR-Encoding genes related with anthracnose and common bacterial blight in the common bean. Frontiers in Plant Science 8:1398
  • Yu K, Park SJ, Zhang B, Haffner M, Poysa V2004 An SSR marker in the nitrate reductase gene of common bean is tightly linked to a major gene conferring resistance to common bacterial blight. Euphytica 138:89-95
  • Zhu J, Wu J, Wang L, Blair MW, Zhu Z, Wang S2016 QTL and candidate genes associated with common bacterial blight resistance in the common bean cultivar Longyundou 5 from China. The Crop Journal 4:344-352

Publication Dates

  • Publication in this collection
    28 Oct 2022
  • Date of issue
    2022

History

  • Received
    18 Feb 2022
  • Accepted
    23 Aug 2022
  • Published
    13 Sept 2022
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