Introduction

Root-knot nematodes (RKNs) Meloidogyne spp. are extremely polyphagous pests that develop on most crops and weeds. Among them, four species are considered to severely affect grapevines throughout the world: M. arenaria, M. incognita, M. javanica and M. ethiopica (Saucet et al., 2016). Those mitotic species are mainly located south of the Mediterranean and in hot climates, but their distribution area is extending to temperate climates because of global warming. Another RKN, the meiotic species M. hapla, has a temperate distribution and appears to be less destructive (Howland et al., 2015; Zasada et al., 2019). Meloidogyne spp. are sedentary endoparasitic nematodes with the second-stage juvenile (J2s) phase as the motile infecting stage. Juveniles hatch from an egg mass into the soil, penetrate root tips and move intercellularly to the vascular cylinder to induce a feeding site composed of multinucleated specialised cells designated as ‘giant cells' (Abad and Williamson, 2010). The vermiform juveniles develop into third- and fourth-stage juveniles, and into female adults, all stages being swollen, fixed and imbedded within a characteristic gall. Under optimal climatic conditions, the complete cycle is 4 to 5-weeks long and several generations per season may develop (Saucet et al., 2016).

Snyder (1936) looked for resistance (R) to RKN species within Vitis accessions in California, and the American species V. champinii, V. longii, V. doaniana and V. cinerea have been shown to be potential sources (Lider, 1954). A wider spectrum of resistance (including to M. arenaria, M. incognita and M. javanica) has been detected in diverse accessions of muscadine (Vitis rotundifolia syn. Muscadinia rotundifolia, referred to as M. rotundifolia in our manuscript) (Bloodworth et al., 1980; Firoozabadi and Olmo, 1982; Lider, 1954; Nesbitt, 1974; Walker et al., 1994). In the US, severe damage and nematicide removal have driven plant breeders to collaborate closely with nematologists in order to focus efforts on the development of hybrid rootstocks resistant to RKN species jointly with desirable agronomical traits. Vitis champinii was used as the main source in the first resistant rootstocks bred with this objective. Among them, the Harmony and Freedom rootstocks, both hybrids of V. champinii, were resistant in many RKN-infected locations (Loubser and Meyer, 1987; McKenry and Anwar, 2006). However, cases of severe local attacks by M. incognita have been reported in California since 1954 on accessions of V. champinii and V. longii (Cain et al., 1984; Lider, 1954; Lider, 1960), and on Harmony and Freedom in particular (McKenry, 1992; McKenry and Kretsch, 1995). These later authors also noticed severe damage by a virulent population of M. arenaria. Breeding efforts of Californian teams for resistance to this M. arenaria population and to other resistance-breaking biotypes then led to the release of accessions such as the RS (Ramsey x Schwarzmann) hybrids [V. champinii x (V. riparia x V. rupestris)] (Anwar et al., 2002), the complex hybrid accessions 6-19B, 10-23B and Demko 10-17A [this later accession is a cross between Edna (an interspecific Vitis crossing) and V. simpsoni] (Anwar and McKenry, 2002a, 2002b; Anwar et al., 2000; Anonymous, 2012), and the UCD GRN series (Ferris et al., 2012). The rootstock UCD GRN1, an F1 hybrid involving the muscadine accession ‘Cowart', was shown to be resistant to two populations of M. arenaria and M. incognita that were virulent to Harmony (Ferris et al., 2012).

Resistance to RKN species is commonly controlled by major genes either within annuals, such as the Mi genes from tomato (Williamson, 1998) and the Me genes from pepper (Djian-Caporalino et al., 2001), or within perennials (Saucet et al., 2016), such as the Ma gene from plum (Claverie et al., 2004, 2011), the RMia gene from peach (Duval et al., 2014) and the RMja gene from almond (Van Ghelder et al., 2010, 2018). A single dominant gene has been shown to confer resistance to M. incognita in V. champinii (Lider, 1954). This monogenic hypothesis has been confirmed for the Harmony and Freedom sources for a non-virulent M. incognita population (Cousins and Walker, 2002). In a V. mustangensis accession, a single dominant allele controlled this non-virulent population together with two virulent Meloidogyne sp. populations (Cousins et al., 2003). More recently a single dominant gene for resistance to M. javanica - designated MjR1 - has been identified in a V. cinerea accession and mapped on chromosome 18 (Smith et al., 2018). By contrast to Vitis sources, RKN resistance conferred by Muscadinia material has been poorly studied, presumably because high numbers of backcross 1 (BC1) individuals putatively segregating for the character of interest are difficult to obtain from most muscadine accessions. Using Vitis x Muscadinia hybrids, Bloodworth et al. (1980) observed that the resistance of M. rotundifolia to M. incognita, M. arenaria and M. javanica was most often dominant.

We report here results related to the genetics of resistance to RKN species in plant material derived from the muscadine accession ‘NC184-4' (Esmenjaud et al., 2010). Our study aimed at identifying and mapping R factor(s) carried by ‘VRH8771', which is a ‘V. vinifera x NC184-4' hybrid accession already shown to carry the QTLs XiR2, XiR3 and XiR4 for resistance to X. index (Rubio et al. 2020). We evaluated segregating BC1 material derived from ‘NC184-4' for its resistance to an isolate of the four grapevine RKN species, M. incognita, M. arenaria, M. javanica and M. ethiopica, predominant on a worldwide scale. We also evaluated the resistance of this material to a mixture of two populations of M. arenaria and M. incognita that are virulent to the Harmony rootstock, as well as its resistance to a pure isolate of each RKN species obtained from these mixed populations. After the complete RKN resistance phenotyping of the BC1 progeny, a single major dominant gene was proposed and located on the map of accession VRH8771.

Material and methods

1. Plant material

The pseudo-testcross (referred to hereafter as a backcross 1 (BC1)) between the hybrid VRH8771 (V. vinifera x M. rotundifolia; female parent) and V. vinifera cv. Cabernet-Sauvignon (CS; male parent) was used (Figure 1). This cross was initiated by Alain Bouquet at INRAE Montpellier in 2005 and was continued at INRAE Bordeaux (UMR EGFV) after 2008; it has been used in a previous study on the genetics and mapping of resistance to X. index in muscadine (Rubio et al., 2020). VRH8771 is a hybrid between the V. vinifera accession ‘Cabernet-Sauvignon x Alicante-Bouschet' and the M. rotundifolia accession ‘NC184-4'. VRH8771 is resistant to all tested RKN species, whereas CS is susceptible. Three reference genotypes were also tested: i) ‘Nemadex Alain Bouquet' (NAB), a X. index-resistant rootstock from the cross VRH8773 (a brother clone of VRH8771) x 140 Ru (V. berlandieri x V. rupestris) (Figure. 1); ii) VRH8624, an F1 hybrid accession between V. vinifera ‘Carignan x CS' and M. rotundifolia ‘Trayshed', which is moderately susceptible to X. index (Esmenjaud et al., 2010); and iii) V. rupestris cv. du Lot (RL), an X. index-susceptible accession. In the experiments on the two created and evaluated Harmony-virulent RKN isolates (see ‘Nematode material section' hereafter), the Harmony rootstock accession was also included. All plant material (parental and reference genotypes, BC1 progeny) originated from the INRAE germplasm conservatory in UMR EGFV (Villenave d'Ornon, France).

Figure 1. Pedigree of the plant material used in the study (R resistant, S susceptible).

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Results

6. Location of resistance on the map of VRH8771

A preliminary mapping of resistance was performed applying an in silico BSA approach with 10 S individuals and 5 R individuals and the two parental SSR maps. Four microsatellite markers (MRBX-08, VVIN16, VMC7F2 and UDV-108) that were linked to resistance were thereby detected in a region of chromosome 18 (Figure. S1). Then, using 38 common individuals phenotyped for their resistance to M. arenaria, M. incognita and M. javanica and the first version of the high-density VRH8771 GBS/SSR map (Lalanne-Tisné, unpublished)), it was possible to identify a putative resistance factor in an interval of ~5.4 Mb of the VRH8771 map between SNP markers 18_18034398 and 18_23400980 (Figure S2). The heterozygous status of SNP markers of the R individuals (and the cognate homozygous status of the S individuals) in the region of this R factor is in line with the hypothesis that resistance is dominantly inherited from the muscadine-derived resistant parent VRH8771 (Figure S2).

Leaning on the hypothesis that there is a single and common R factor for all four RKN species considered in our study, we used the 48 individuals genotyped and phenotyped for resistance to a representative RKN, the species M. javanica (the highest number), to complete our results; to this end, we carried out a QTL analysis based on the second version of the high-density VRH8771 GBS/SSR map (Rubio et al., 2020). The binary mapping detected a strong QTL that peaked near marker MRBX-12 on linkage group 18, between 125.8 cM and 134.2 cM. This QTL was supported by a LOD score of 10.35, explaining 77.8 % of the phenotypic variance (Figure 2). The confidence interval of the R factor and the SNP and SSR markers that it contains are shown in Figure 3.

Figure 2. QTL analysis of the location of resistance to M. javanica (MJ) performed on 48 segregating individuals. The curves in the plot indicate the genetic coordinate in the 19 linkage groups of the VRH8771 map (x-axis) and the LOD score obtained by the binary mapping (y-axis). The horizontal dotted line shows the LOD significant threshold estimated with 1000 permutations (P ≤ 0.05). The box is the zoom-in image of the peak on chromosome 18. The horizontal line at the basis of the peak shows the confidence interval detailed in Figure 3.

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Figure 3. Location of the RKN MsppR1 locus on the chromosome 18 (shown in two parts) of VRH8771. Genetic distances in cM are displayed on the left-hand side and marker names (SNP and SSR markers) are displayed on the right-hand side. The detailed map shows the region encompassing MsppR1 (this study) and the XiR4 QTL for resistance to X. index (Rubio et al., 2020).

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Discussion

This study aimed to identify and map the R factor(s) carried by ‘VRH8771' relative to the globally predominant grapevine RKN species (McKenry et al., 2001; Nicol et al., 1999; Saucet et al., 2016). Using an isolate of each of the M. arenaria, M. incognita, M. javanica, and M. ethiopica species, together with Harmony-virulent RKN material, we showed that accession VRH8771, derived from the muscadine source NC184-4, has a wide resistance spectrum (Table S8). Our genetic study based on the VRH8771 x CS progeny found a clear R/S segregation, which indicates that VRH8771 is heterozygous for resistance. The independence of this segregation from the different RKN species that were evaluated shows that VRH8771 carries (an) R factor(s) that control(s) all tested RKN species. For the highest number of individuals evaluated for resistance to M. javanica (n = 51, Table S8), the segregation ratio was 22R:29S. To determine whether this ratio was statistically different from the 1R:1S segregation expected for monogenic resistance, we performed a Chi-2 test (one degree of freedom). The Chi-2 value (0.483) corresponded to a p-value of 0.487, a probability that is much higher than the threshold value p=0.05 (3.841). Consequently, our data support the hypothesis that resistance is conferred by a single major dominant factor at the heterozygous state in the accession VRH8771. Nevertheless, a distorted segregation ratio in favour of S individuals was observed, which might be due to a higher survival of S seedlings. Indeed, the overall survival rate of the seedlings of the VRH8771 x CS progeny was only 37%, and after eliminating the plants which did not root well from the analysis, only 31% could be phenotyped. No genetic information is available for the 63 % of dead seedlings.

Only a low-resolution location of the R factor was obtained due to the small number of phenotyped individuals (38 in common for the different nematode species); the analysis of a larger population would have resulted in higher resolution data. The missing 13 individuals needed to reach a total of 51 available individuals are under evaluation at the time of writing to confirm these results. Despite these limitations, using the high-density map from VRH8771 (Rubio et al., 2020), we were able to clearly locate the R factor in a single region of chromosome 18. We named it the MsppR1 gene (for ‘Meloidogyne spp. Resistance 1' including M. arenaria, M. incognita, M. javanica and M. ethiopica), given that the different mapping steps support the hypothesis of a single factor controlling all tested RKN species. MsppR1 is located within a ~5.4-Mb interval that contains the microsatellite markers MRBX-08, MRBX-12, VMC6F11 and VVIN16, which could be interesting tools for marker-assisted breeding (Figure 3). Few major RKN R genes have been identified and mapped in perennial plants (Saucet et al., 2016), and only one, the MjR1 gene, has been mapped in grapevine (Smith et al., 2018); this gene from V. cinerea (accession C2-50) controls M. javanica and is also located on chromosome 18, but using another map, it was located in a more telomeric position between the SNP flanking markers, S18_31160355 and S18_33954011. In VRH8771, this telomeric region also contains XiR4 QTL for resistance to X. index (Rubio et al., 2020) (Figure 3, Figure S2). In M. rotundifolia, chromosome 18 has also been shown to contain other R genes for resistance to downy mildew (Rpv2/Plasmopara viticola) and powdery mildew (Run2.1, Run2.2 /Erysiphe necator) (Delrot et al., 2020; Dry et al., 2019; Merdinoglu et al., 2018).

We consider the isolates of the four species and the two Harmony isolates to be representative of the different grapevine RKNs in nature. Nevertheless, they do not guarantee that the resistance inherited from NC184-4 will be active against each of their specific populations or a mixture of them. For example, despite its resistance in separate tests to a M. incognita population, a M. javanica isolate and a Harmony-virulent M. arenaria isolate, the X. index-resistant rootstock VR 039-16 (V. vinifera x M. rotundifolia) (Walker et al., 1991) was found to be susceptible to a field mixture of populations of M. incognita, M. arenaria and M. javanica (McKenry and Anwar, 2006). However, our results are in line with those that have been obtained since 1954 for diverse muscadine-derived materials that have all been shown to be resistant to the various RKN species (Bloodworth et al., 1980; Ferris et al., 2012; Firoozabadi and Olmo, 1982; Lider, 1954; Nesbitt, 1974).

In addition to the four main species parasitising grapevine, a particular focus of our study was the ‘Harmony’ populations. We phenotyped the resistance of segregating progeny to a mixture of the two populations M. arenaria Harmony A and M. incognita Harmony C, and then to an isolate obtained from each of these populations. The data obtained from the mixed Harmony populations suggest a high level of resistance conferred by the MsppR1 gene. Testing each of the obtained isolates separately then allowed us to assess their aggressiveness more accurately. The aggressiveness of the Harmony isolate of M. arenaria towards the reference Harmony rootstock was confirmed by the marked galling that was induced and the high number of J2s recovered on this accession (Table S5, Table 5). By contrast, the M. incognita isolate was less aggressive towards this rootstock (Table S6). This particular difference in aggressiveness is in line with our data, illustrating that the M. incognita isolate induces lower plant mortality than the M. arenaria one. Nevertheless, regardless of the Harmony isolate considered, we observed a complete survival of the resistant individuals (heterozygous state: MsppR1/msppR1) in contrast to the elevated mortality of the susceptible individuals (homozygous recessive state: msppr1/msppr1); this indicates that the MsppR1 allele inherited from VRH8771 might be associated with a mechanism of high resistance to RKNs.

Besides the parental accession VRH8771, we also evaluated other muscadine or muscadine-derived reference accessions. Accession VRH8624 displayed the same complete-spectrum resistance to the isolates and tested populations as VRH8771. This might signify that VRH8624 has inherited (from its muscadine parent ‘Trayshed’) an MsppR1 R allele expressing a similar efficiency to the VRH8771 allele. The BC1 rootstock NAB (Figure 1) was also found to have wide-spectrum resistance. Nevertheless, it often showed a very low, but non-null gall index rating (Tables S1, S4 to S7), although its pedigree should make it express the same gall-free phenotype as the R segregating individuals (i.e., carrying the MsppR1 R allele of VRH8771), with which it shares the same resistant grandparent NC184-4. Given that NC184-4 is presumably homozygous for resistance, a plausible hypothesis for the slightly weaker phenotypic expression of resistance in NAB is that its parent VRH8773 (Figure 1) inherited the other R allele of the MsppR1 gene, and that this latter allele would confer a slightly lower protection.

The histological mechanisms underlying resistance in muscadine NC184-4 are unknown. Nevertheless, studies conducted on a M. arenaria population breaking the resistance carried by Harmony found that the resistant accession Demko 10-17A expressed an early hypersensitive response (Anwar and McKenry, 2002b) with no root galling, a mechanism that might be shared by NC184-4 and other muscadine accessions. Within Vitis spp., an equivalent hypersensitive response has been observed for the gene MjR1 in V. cinerea (Smith et al., 2018); meanwhile, in the rootstock RS9 (a Vitis hybrid of V. champinii), a late resistance mechanism has been found to occur, inducing slight galling with undersized adult females and little or no egg production (Anwar and McKenry, 2002a).

Conclusion

Resistance from the ‘NC184-4’ muscadine source in the Vitis x Muscadinia accession VRH8771 controls an isolate of each of the RKNs M. arenaria, M. incognita, M. javanica and M. ethiopica, together with M. arenaria and M. incognita’s Californian populations virulent to the Harmony rootstock. This wide-spectrum resistance is presumably conferred by a dominant gene designated as MsppR1 and mapped on grapevine chromosome 18. In the ~5.4-Mb interval encompassing MsppR1, SNP and SSR markers (MRBX-08, MRBX-12, VMC6F11 and VVIN16 in particular) can be used for marker-assisted breeding.

The wide spectrum resistance conferred by MsppR1 meets the needs of worldwide viticulture - in particular in California for the control of M. arenaria, M. incognita, M. javanica and the Harmony-virulent populations (Saucet et al. 2016), in South America against the predominant M. ethiopica species (Meza et al., 2016) and in Australia against the prevalent M. javanica species (Smith et al., 2017, 2018). In the genetic background of VRH8771, this gene also appears to confer high-level resistance, a feature which is worth promoting in the context of increased RKN pressure due to global warming. In VRH8771, marker-assisted breeding of MsppR1 together with the X. index R QTLs XiR2, XiR3 and XiR4 should allow us to select highly performing grapevine rootstocks derived from muscadine sources.

The similar wide-spectrum resistance inherited from another muscadine source in VRH8624 suggests that many muscadine accessions carry other highly beneficial R alleles of the MsppR1 gene. Nevertheless, as V. vinifera x M. rotundifolia hybrids may be sensitive to Phylloxera (Bouquet, 1983; Rubio et al., 2020), the interest of such genotypes as genitors of rootstocks should be carefully assessed through marker-assisted selection and in planta tests for the soil-borne aphid Daktulosphaera vitifoliae.

Abbreviations

ANOVA: Analysis of variance; BSA: Bulked segregant analysis; GBS: Genotyping-by-sequencing; GI: Gall index; J2: Second-stage juvenile; LG: Linkage group; LOD: Logarithm of odds ratio; LSD: Least significant difference; ML: maximum likelihood; QTL: Quantitative trait locus; SNP: Single nucleotide polymorphism; SSR: Simple sequence repeats

Acknowledgments

We are grateful to our colleagues Jean-Pierre Petit and Laure Morgadinho for maintaining the 8771 x CS progeny and preparing the phenotyped cuttings. We acknowledge Guillaume Lalanne-Tisne for his contribution to the mapping work. We also thank Dr Sarah Cookson for her contribution to checking the English, and Dr Pierre-François Bert and Nabil Girollet for uploading the GBS data online.

Declarations

Ethics approval and consent to participate

The plants used in this study are available in the germplasm conservatory in UMR EGFV (Villenave d’Ornon, France). Experimental research and plant studies, including the collection of plant material, comply with relevant institutional, national, and international guidelines and legislation.

Availability of data

All the data analysed during this study are included in the article and in its supplementary information (data files S1 to S4).

GBS data obtained using the PN40024 12X.v2 grapevine reference genome can be retrieved from BioProject PRJNA553991 (https://dataview.ncbi.nlm.nih.gov/object/PRJNA553991)

Competing interests

The authors declare that they have no competing interests.

Funding

This work was partly funded by the French Ministry of Agriculture and Fisheries through the Projects ‘RemuneX’, from contract CTPS n° C-2014-09 (2015–2018) and ‘REDUNEM’ from contract CTPS n°C-2019-07 (2019-2022). Complementary funding was from the contracts between ‘INRAE Department of Biology and Plant Breeding (BAP)’ and ‘Agri-Obtentions (AO)’ through the projects IVD3 (2016-2020) and IVD4 (RESGRAPE III-PG 2021-2025).

Authors’ contributions

DE, MYB, CVG and NO contributed to the design of the study. JPT and ML obtained the progenies and multiplied the plant material. AW collected and provided the Californian ‘Harmony’ populations. UP performed nematode identification and multiplication. DE and MYB collected and analysed the phenotypic data. DE and BR analysed the mapping data. DE and MYB wrote the manuscript. All the authors read and approved the final manuscript.

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