Pyramiding of resistance alleles to grape powdery mildew assisted by molecular markers

Abstract

Disease resistance gene pyramiding is a widely used strategy to enhance resistance durability. Marker-assisted selection (MAS) was applied to pyramide the alleles Run1 and Ren3, which confer resistance against grape powdery mildew (Erysiphe necator). Two F₁ full-sibs carrying Run1 and Ren3 in heterozygosity were selfed to develop the breeding populations used in the analysis. From the 637 genotyped plants, 313 (50.6%) had the Run1 and Ren3 pyramided. Seven (1.1%) of them exhibited the two resistance alleles in homozygosity. Plants without any resistance alleles had the highest disease severity ( = 7.3), while the ones with the Run1 allele both in homozygosity and heterozygosity were highly resistant ( = 1.5). Similar level of resistance was observed in the plants containing Run1 and Ren3 pyramided ( = 1.3). Plants containing Run1 and Ren3 pyramided in homozygosity are important genetic resources for grape breeding programs in Brazil.

Keywords: Vitis vinifera; plant breeding; Erysiphe necator; disease resistance; sustainability

INTRODUCTION

Powdery mildew is a major fungal grapevine disease worldwide. The disease is caused by Erysiphe necator Schwein [syn. Uncinula necator (Schwein) Burrill], an obligate biotrophic fungus belonging to ascomycetes and the Erysiphaceae family (Kunova et al. 2021). When not adequately managed, it reduces grape yield and quality and compromises wine quality (Scott 2021). The infection and colonization of susceptible hosts result in abundant production of mycelium, conidiophores and asexual conidia at the adaxial leaf surface, which are initially visualized as roughly circular whitish spots, and later assuming a typical powdery appearance (Kunova et al. 2021).

The pathogen is predominantly found in dry and warm regions (Zendler et al. 2021). Tropical regions in Brazil produce either table and wine grapes. The São Francisco River Valley region is the most prominent of these areas. These regions are frequently characterized by a dry climate throughout the year, and powdery mildew is one of the major challenges for grape production (Camargo et al. 2011). In the Southern region of Brazil, E. necator is not epidemic, because the climatic conditions are not conducive to E. necator infection and development. However, in this region, some vineyards are grown in protected environments (plastic cover). That measure reduces the wetting on the grape tissues and favors the occurrence of powdery mildew (Almança et al. 2017).

The current main strategy for controlling powdery mildew in commercial vineyards is based on preventive fungicide application. This practice increases the production costs, generates health and environmental concerns, and may result on the selection of fungicide-resistant E. necator strains (Merdinoglu et al. 2018, Kunova et al. 2021).

Host genetic resistance is considered the most sustainable alternative for grape powdery mildew management (Qiu et al. 2015). Many loci containing alleles associated with resistance to the pathogen have been genetically mapped: Run1 (Barker et al. 2005); Run1.2 (Riaz et al. 2011); Run2.1 and Run2.2 (Riaz et al. 2011); Ren1 (Hoffmann et al. 2008); Ren1.2 (Possamai et al. 2021); Ren2 (Dalbó et al. 2001); Ren3 (Welter et al. 2007); Ren4 (Ramming et al. 2011); Ren5 (Blanc et al. 2012); Ren6 and Ren7 (Pap et al. 2016); Ren8 (Zyprian et al. 2016); Ren9 (Zendler 2017); Ren10 (Teh et al. 2017); and Ren11 (Karn et al. 2021).

The construction of resistance genes pyramids is considered one of the best strategies to achieve durable resistance against pathogens (Rex Consortium 2016). Resistance allele pyramiding against E. necator is being widely used in grape: Run1 and Ren3 heterozygous plants (Eibach et al. 2007, Calonnec et al. 2013), Run1.2 and Run2 in the Trayshed cultivar (homozygous only for the Run1.2 locus) and Thomas genotype (heterozygous lines) (Feechan et al. 2015), Run1 and Ren1 (Agurto et al. 2017), and Ren6 and Ren7 (Pap et al. 2016).

We aimed in the present investigation to apply the MAS to pyramid the resistance alleles associated to the loci Run1 and Ren3 and to assess the level of resistance conferred by Run1 and Ren3, isolated or combined, in homozygote and heterozygote state.

MATERIAL AND METHODS

Plant materials

The full-sibs ‘2000-305-134’ and ‘2000-305-97’, selected from the cross ‘VHR-3082-1-42’ and ‘Regent’, were selfed to develop two segregating populations UFSC-2013-1 (420 progenies) and UFSC-2013-2 (217 progenies). They carry the resistance alleles Run1 (Barker et al. 2005), and Ren3 (Welter et al. 2007), pyramided in heterozygosity.

Genotyping

DNA preparation and quantification followed the methodology described by Sanchez-Mora et al. (2017). For marker-assisted selection, microsatellite markers closely flanking the Run1 and Ren3 loci were used. Run1 is closely linked to Rpv1. Therefore, for Run1 we used the same microsatellite markers (Sc34_8 and Sc35_2) described by Sanchez-Mora et al. (2017). For Ren3 we used the markers GF15-28 and GF15-30 (Zyprian et al. 2016). The forward primers were labeled with the fluorescent dyes 6-FAM, VIC, and PET. The four microsatellite markers were combined into a single multiplex, amplified with the Kapa2G Fast Multiplex Mix (Kapa Biosystems Inc., Boston, MA, USA) and the fragments separated by capillary electrophoresis in a 3500 XL sequencer (Thermo Fisher Scientific, Waltham, MA, USA), as described by Sanchez-Mora et al. (2017). Gene Mapper Version 4.1 software (Thermo Fisher Scientific, Waltham, MA, USA) was used to call the microsatellite alleles. Based on the genotypic information, the progenies were discriminated into the nine possible allelic combinations of the two independently segregating loci Run1 and Ren3 (Figure 1).

Figure 1
Frequency distribution (%) of individuals segregating for two loci conferring resistance to powdery mildew in 619 plants of the UFSC-2013-1 (χ² = 107.86, df = 8, p value < 0.001) and UFSC-2013-2 (χ² = 80.604, df = 8, p value < 0.001) selfing populations. Numbers above the bars indicate the number of plants in each genotypic class.

Phenotyping

To validate the genotyping data, a subset of plants from both segregating populations representing the nine different genotypes were scored for resistance for powdery mildew resistance in greenhouse in two locations and three years. Plants of the two populations were propagated by cuttings and established in a greenhouse at the Videira Experimental Station of Epagri, Videira, SC, and in the Agricultural Experimental Station of the Federal University of Santa Catarina, Curitibanos Campus, Curitibanos, SC. The resistance assays were performed under natural conditions of powdery mildew infection in February in the 2014/15 and 2015/16 crop years in Videira and in 2016/17 in Curitibanos.

The level of resistance to powdery mildew was rated according to the OIV-455 scale of the International Organisation of Vine and Wine (OIV 2009), where each score corresponds to the sporulation intensity of the disease: 1) very low sporulation: small spots or no symptoms, not visible; 3) low sporulation: limited spots < 2 cm in diameter, limited sporulation and mycelium, the presence of E. necator is only indicated by a slight ripple in the leaf blade; 5) average sporulation: normally limited spots with diameter of 2-5 cm; 7) high sporulation: vast spots, some limited, abundant mycelium sporulation; and 9) very high sporulation: unlimited stains with entire leaf blade under attack, high mycelium sporulation and abundant mycelium.

Statistical analysis

The genotype data were organized in frequency distribution, and the chi-square (χ²) goodness of fit test was applied to verify if there are allelic and genotypic segregation distortions. The nature of segregation distortion was defined using the methodology described by Lorieux et al. (1995). For the phenotypic data, the frequency of progenies in each resistance class was calculated and plotted on graphs. The Fisher exact test (p value < 0.001) was applied after Bonferroni correction to compare the frequency distribution between the different progenies. When the genotypes had the same resistance score, they were considered dependent, that is, they have the same frequency distribution and therefore have the same level of resistance. In contrast, when the progenies have different scores, they are considered independent and are different. The R statistical program (R Development Core Team 2021) was used for statistical analyses.

RESULTS AND DISCUSSION

Genotyping

Based on the genotypic data, the 637 plants from the two segregating populations were distributed in nine genotypic classes (Figure 1). Plants were considered to have the resistance allele when no crossing-over was observed between the respective flanking markers. Two plants in the Run1 locus and 16 plants in the Ren3 locus showed recombination (2.8%) between the flanking microsatellite markers. From the remaining 619 plants, 313 (50.6%) exhibited the two alleles pyramided, 189 (30.5%) carried only Ren3, 78 (12.6%) had only the Run 1 allele, and 39 (6.3%) did not carry any of the resistance alleles (Figure 1).

Among the plants containing pyramided resistance alleles, 7 (1.1%) exhibited the two resistance alleles in homozygosity (Run1/Run1, Ren3/Ren3), 16 (2.6%) carried the Run1 allele in homozygosity and Ren3 in heterozygosity (Run1/Run1, Ren3/ren3), 103 (16.6%) had the Run1 allele in heterozygosity and Ren3 in homozygosity (Run1/run1, Ren3/Ren3), and 187 (30.2%) had the two resistance alleles in heterozygosity (Run1/run1, Ren3/ren3).

Significant segregation distortion was observed in both segregating populations (Table 1). It was particularly high for the microsatellite markers linked to Run1 (Table 1; Figure 1). In both populations occurred a suppression of the genotype homozygote for the resistance allele Run1 (Run1/Run1) and, consequently, an excess of heterozygotes (Run1/run1) and recessive homozygotes (run1/run1) (Table 1). The segregation distortion in this genomic region is due to zygotic selection against the homozygous genotype Run1/Run1. Segregation distortion in the Run1/Rpv1 locus was previously reported in other studies (e.g., Barker et al. 2005, Sánchez-Mora et al. 2017). The microsatellite markers linked to Ren3 showed weak segregation distortion (Table 1).

Table 1
Frequencies obtained of segregation and chi-square test revealed by SSR markers in the two populations segregating for resistance to powdery mildew

Locus	Populations
	UFSC-2013-1			UFSC-2013-2
	n	Genotype frequency	Allele frequency	n	Genotype frequency	Allele frequency
SSR markers: Sc34_8/Sc35_2 (Chr. 12)
Run1/Run1	21	0.05	Run1=0.33	11	0.05	Run1=0.36
Run1/run1	227	0.56	run1=0.67	132	0.62	run1=0.64
run1/run1	159	0.39		69	0.33
χ2 (1:2:1)	99.01***			44.49***
Distortion with one locus1			Zygotic		Zygotic
χ2 =[p (Run1) = q (run1)]			94.10***		33.24***
χ2 = p 2 +2pq+q 2			27.63***		25.60***
SSR markers: GF15-28/GF15-30 (Chr. 18)
Ren3/Ren3	92	0.23	Ren3=0.51	82	0.39	Ren3=0.63
Ren3/ren3	226	0.55	ren3=0.50	102	0.48	ren3=0.37
ren3/ren3	89	0.22		28	0.13
χ2 (1:2:1)	5.02			27.81***
Distortion with one locus1			Zygotic		Gametic
χ2 = [p (Ren3) = q (ren3)]			0.08		28.66***
χ2 = p 2 +2pq+q 2			4.99***		0.19
Distortion with two loci1			Zygotic		Zygotic
χ2 = [p (Run1) = q (run1), r (Ren3) = s (ren3)]			422.47***		223.44***
χ2 = [p 2 +2pq+q 2 ] x [r2+2rs+s2]			18031.2***		11560.5***

• ¹
  According to the methodology employed by Lorieux et al. (1995). *** P<0.001 by chi-square test (χ2).

Segregation distortion is frequently observed in interspecific crosses. In grape, it was reported in interspecific crosses e.g. Horizon x Illinois 547-1 (Dalbó et al. 2001), Muscadinia rotundifolia G52 × Malaga seedling No.1 (V. vinifera) (Pauquet et al. 2001), V. rupestris × V. arizonica/girdiana (Riaz et al. 2006), and M. rotundifolia cv. Fry × M. rotundifolia cv. Trayshed (Riaz et al. 2012).

Phenotyping

To determine the level of resistance to powdery mildew conferred by the loci Run1 and Ren3, individually and in pyramided form, about three-fourth of the genotyped plants were screened in greenhouses under natural infectious conditions of E. necator in two environments (Videira, SC, and Curitibanos, SC). Evaluation in greenhouse is a methodology widely used to phenotype resistance to grapevine powdery mildew (Eibach et al. 2007, Gao et al. 2016, Possamai et al. 2021). The greenhouse provides a drier environment that favors infection by the pathogen.

The three phenotyping evaluations (two in Videira and one in Curitibanos, SC) revealed no significant genotype × environment interaction (data not shown), and therefore, the results were analyzed together (Figure 2 and Table 2). The progenies without any resistance allele were susceptible to powdery mildew (average score of 7.0; p value < 0.001). Ren3 conferred partial resistance to the plants, significantly reducing incidence of the disease compared to the susceptible plants (average score of 5.4; p value < 0.001). The Ren3 allele displayed the widest variation in resistance level, ranging from 1 (12.3% of plants) to 9 (14% of plants). The frequencies of the intermediary scores were: 3 (8.8%), 5 (35.1%), and 7 (29.8%). Similar results were observed in previous investigations (e.g., Welter et al. 2007, Eibach et al. 2007, Zendler et al. 2017). The fine mapping of the original Ren3 genomic region of ‘Regent’ (Welter et al. 2007) revealed that two distinct loci (Ren3 and Ren9) mediate the partial resistance to E. necator (Zendler et al. 2017, Zendler et al. 2021). An impaired recombination frequency between both loci was observed, strongly suggesting that in the present investigation the two loci are operating together, since both selfing populations inherited Ren3 from ‘Regent’. Therefore, one possible explanation for the phenotypic variation is the recombination between the two loci. However, Zendler et al. (2021) found a recombination frequency of around 2%, which cannot explain the phenotypic variation. The most probable explanation for the variation is associated with the mode of operation of Ren3/Ren9 resistance alleles. For instance, Zendler et al. (2017) demonstrated that the defense mechanism mediated by Ren3/Ren9 is associated with a post-invasion reaction. The pathogen is able to build a dense mycelial net on plants carrying Ren3/Ren9, but rarely forms conidia. Mycelial density may also be influenced by genomic background, the presence of other minor QTLs, and/or small environmental variations.

Table 2
Results of Fisher's exact test (p < 0.01) comparing the phenotypic response of the allelic combinations of the Run1 (A) and Ren3 (B) loci to powdery mildew infection in grape

Loci	Aabb	aabb
AAbb	= p value=0.07	≠ (**) p value =0.00049
Aabb		≠ (**) p value =0.00049
	aaBb	aabb
aaBB	= p value =0.11	≠ (**) p value =0.00049
aaBb		≠ (**) p value =0.00549

• DIF: Significant difference indicated by Fisher's exact test at 5% significance level. ** p-value with a significance level lower than 0.01.

Figure 2
Phenotypic distribution of powdery mildew resistance according to the OIV-455 descriptor ranging from resistant (1) to susceptible (9) for each of the nine genotypic combinations of the loci Run1 (A) and Ren3 (B). The upper axis indicates the weighted average of the genetic resistance of the analyzed sample. The inferior axis indicates the distribution of the analyzed allele frequency grouped by the class of severity of powdery mildew infection (OIV-455). Above each column the observed frequency and the respective proportion are indicated.

The progenies carrying the Run1 allele were highly resistant (average score of 1.9), differing significantly from Ren3 (p value < 0.001). Almost 70% percent of the progenies carrying at least one Run1 allele did not show any symptom of the disease (score 1). This resistance level mediated by Run1 is already well documented and it is associated with programmed cell death (PCD) of epidermal cells penetrated by fungi, prohibiting pathogen colonization (Feechan et al. 2013). As Run1 mostly conferred complete resistance to powdery mildew, no significant difference was observed between progenies carrying Run1 alone or pyramided with Ren3 (average score of 1.3), as previously reported (Eibach et al. 2007, Zini et al. 2019, Possamai et al. 2021). Nevertheless, stacking the resistance allele of both loci is an important measure to promote resistance durability since the loci are inherited from different species and the mode of action is different (Feechan et al. 2013, Merdinoglu et al. 2018, Zendler et al. 2021). However, the long-term durability of Ren3 and Run1 should be a matter of concern, since isolates that have overcome the resistance of both loci have been reported (Cadle‐Davidson et al. 2011, Feechan et al. 2013, Feechan et al. 2015, Teh et al. 2017).

The progenies containing the resistance alleles in homozygosity did not show higher resistance level to powdery mildew compared to those with the alleles in heterozygosity for Run1, Ren3, and Run1+Ren3 (Table 2), suggesting a complete dominant allelic interaction in both loci. Although no dosage effect was observed, the development of “breeding lines” homozygous for resistance alleles is an interesting strategy to increase the breeding efficiency, since the use of homozygous lines in crosses would render all progenies with one copy of the resistance alleles, not requiring phenotyping and genotyping evaluations. However, grape commonly undergoes endogamic depression, and obtaining plants with desirable vigor is a challenge. It is noteworthy that the OIV-455 descriptor is more of a quality rating scale; therefore, small differences such as allele dosage effects or the contribution of Ren3 in increasing the resistance mediated by Run1 cannot be completely discarded.

In the present study, MAS was effectively used for pyramiding the loci Run1 and Ren3, which confer resistance to grape powdery mildew. The use of MAS, associated to segregating populations obtained by selfing, allowed the selection of plants containing Run1 and Ren3 alleles in homozygosity. The use of these plants in new crossing generations permits the obtention of 100% of the progenies containing both resistance alleles in heterozygosity, increasing the breeding efficiency.

ACKNOWLEDGMENTS

We are grateful to the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for funding (Grant number 480612/2010-2) and a scholarship to RON; to the Fundação de Amparo à Pesquisa e Inovação do Estado de Santa Catarina (FAPESC) for funding (Grant number TR201266), to the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) - Código de Financiamento 001; and to the Secretaria Nacional de Educación Superior Ciencia y Tecnologia - Ecuador (SENESCYT) for a scholarship to FDSM.

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Publication Dates

• Publication in this collection
  13 Feb 2023
• Date of issue
  2022

History

• Received
  05 May 2022
• Accepted
  04 Oct 2022
• Accepted
  22 Nov 2022