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Article

Identification and Characterization of Resistance to Rust in Lentil and Its Wild Relatives

by
Eleonora Barilli
and
Diego Rubiales
*
Institute for Sustainable Agriculture, CSIC, Avda. Menéndez Pidal s/n, 14004 Córdoba, Spain
*
Author to whom correspondence should be addressed.
Plants 2023, 12(3), 626; https://doi.org/10.3390/plants12030626
Submission received: 31 December 2022 / Revised: 18 January 2023 / Accepted: 26 January 2023 / Published: 31 January 2023
(This article belongs to the Section Plant Genetics, Genomics and Biotechnology)
Browse Figure
Versions Notes

Abstract

:
Lentil rust is a major disease worldwide caused by Uromyces viciae-fabae. In this study, we screened a large germplasm collection of cultivated lentils (Lens culinaris ssp. culinaris) and its wild relatives, both in adult plants in the field with a local rust isolate during 2 seasons and in seedlings under controlled conditions with four fungal isolates of worldwide origin. The main results from our study were the following: (1) a significant number of accessions with resistance based on hypersensitive reaction (reduced Infection Type (IT)) were identified in cultivated lentil and in L. ervoides, L. nigricans and L.c. orientalis. The IT scores showed a clear isolate-specific response suggesting race-specificity, so each fungal isolate might be considered a different race. Resistance was identified against all isolates what might be the basis to develop a standard differential set that should be a priority for rust definition and monitoring. (2) Interestingly, although at lower frequency than in L. ervoides and L. nigricans, the hypersensitive response was also observed within cultivated lentil, with accession 1561 (L.c. culinaris) displaying resistance to the four isolates making this accession a valuable ready-to-use resource for lentil resistance breeding. Resistance to all other rust isolates was also available within L.c. culinaris in an isolate-specific manner. Accession 1308 (L. ervoides) showed resistance against all isolates tested, as well as a reduced number of accessions belonging to other wild Lens species. (3) In addition, our screenings allowed the identification of several accessions with partial resistance (reduced Disease Severity (DS) despite high IT). Adult Plant Resistance resulting in reduced severity in adult plants in the field, despite high susceptibility in seedlings, was more frequently identified in L.c. culinaris, but also in L. nigricans and L.c. orientalis.

Highlights

►
Hypersensitive, partial and adult plant resistances have been identified within L.c. culinaris accessions, enabling their immediate use in lentil resistance breeding
►
Additional valuable sources of resistance have been identified in related species of the primary and secondary gene pools, crossable with cultivated lentils making feasible the transfer of rust resistance genes.

1. Introduction

Lentil (Lens culinaris Medik.) is an annual food legume cultivated over 5.5 million hectares [1]. Average yields are small (word average 1000 kg/ha) which might be ascribed to biotic and abiotic constraints and to the fact that lentil is generally produced under low input conditions [2,3]. Rust, caused by the fungus Uromyces viciae-fabae (Pers.) Schröt (syn. U. fabae (Pers.) de Bary) is regarded as one of the most important foliar diseases of lentil, widespread globally, with reported yield losses ranging from 25 to 100% [2,4,5]. Rust can be controlled by a number of fungicides but economic factors must be taken into consideration [6,7].
Breeding for rust resistance is regarded as the most cost-efficient method for rust control in legume crops [5,8]. Resistance to rust has been reported in lentil [9,10,11], even when the variable levels of detail hinder the comparison of results due to a lack of information details regarding the inoculation conditions, inoculum identity or the resistance components assessed. The few genetic studies available suggest monogenic control [12,13,14,15] that does not preclude the existence of polygenic resistance; variable levels of incomplete resistance have also been reported [9,11] although its inheritance is not yet studied. Stability and durability of resistance is one of the most important concerns for breeders, which reinforces the need to search and characterize additional sources of resistance.
Rust resistance breeding is hampered by insufficient knowledge of physiological specialization in the pathogen [16], which deserves urgent monitoring. In fact, even information on the causal agent is often misleading as Uromyces viciae-fabae is today acknowledged to be a complex species in which crop specialization is occurring [17,18,19]. The clear-cut crop specialization of isolates from faba bean (Vicia faba), common vetch (Vicia sativa) and lentil allowed subdivision of U. viciae-fabae into at least U.v-f ex Vicia faba, U.v-f ex V. sativa and U.v-f ex L. culinaris. Additionally, under favorable weather conditions, crop failure may also occur caused by pea rust incited by the fungus U. pisi [20,21].
Lentil suffers from relatively low genetic diversity due to a genetic bottleneck created during domestication with selection for a small number of traits [22]. This reinforces the interest in the incorporation of genetic diversity available in wild relatives where resistance to rust has been reported [23,24] such as L. culinaris ssp. orientalis, L. culinaris ssp. odemensis or L. ervoides which can be hybridized with cultivated lentil [25,26], making feasible the transfer of rust resistance genes.
The objectives of the present work were to identify and characterize additional sources of resistance to rust in lentil germplasm in its wild relatives and to test their stability in the field in different seasons and in seedlings under controlled conditions against contrasting isolates of the pathogen.

2. Materials and Methods

2.1. Lens sp. Germplasm Origin

This study used a worldwide germplasm collection containing 523 accessions kindly provided by CRF (Centro Nacional de Recursos Fitogenéticos, Spain), USDA-ARS (Department of Agriculture, USA) and ICARDA (International Centre for Agricultural Research in the Dry Areas, Syria). The collection represents the Lens genus in taxonomy, including 429 accessions of L. culinaris ssp. culinaris; 31 of L. culinaris ssp. orientalis; 5 of L. culinaris ssp. odomensis; 21 of L. ervoides; 2 of L. lamottei; and 34 of L. nigricans (Supplementary Table S1). All the accessions were multiplied at the Institute for Sustainable Agriculture—CSIC at Cordoba, Spain under field condition before the experiments.

2.2. Pathogen Isolate and Multiplication

Seedling experiments under controlled conditions were performed using isolates SPA, MOR, FRA and ALG of U. viciae-fabae ex L. culinaris which were previously collected from naturally infected lentil crops in Spain, Morocco, France and Algeria, respectively. The different fungal isolates were multiplied in susceptible lentils cv. Pardina in separate growth chambers (one different chamber per isolate) with filtered ventilation and conserved at −80 °C. Field experiments were only inoculated with the SPA isolate.

2.3. Field Experiments and Data Assessments

The Lens sp. collection was phenotyped over two crop seasons (2014 and 2015) at Córdoba, Spain (Table 1) using the rust susceptible lentil cv. Pardina as control check, following an alpha lattice design with three replicates. The experimental unit consisted of a single 1 m-long row per accession with 15 plants per row, separated from the adjacent row by 0.7 m, with three replications. Accessions were sown in the field by late December each year and harvested by early June, according to local practices.
Plants were artificially inoculated by mid-March, at flowering stage, by spraying with an aqueous suspension of urediospores from isolate SPA to ensure high and uniform levels of rust infection. The urediospores were suspended in tap water (6 × 104 urediospores mL−1), to which Tween-20 (0.03%, v:v) was added as a wetting agent to reduce the surface tension of the urediospores and to obtain a homogeneous suspension. Plants were inoculated after sunset to benefit from the darkness and high relative humidity of the night. When rust development started, disease severity (DS) was assessed by a visual estimation of the percentage of plant canopy covered by rust pustules.

2.4. Controlled Condition Experiment and Assessments

The collection was inoculated with each of the four rust isolates separately. For this, each accession was represented by nine seedlings per round, planted 3 by 3 in 1 L pots, this repeated in four consecutive replications per isolate. Pots were placed in a randomized complete block design and seedlings were inoculated when the third leaf was completely expanded (±12 days after sowing). Two-week-old plants were inoculated by dusting with 1 mg urediospores per pot, mixed in pure talc (1:10, v:v) and incubated for 24 h at 20 °C in complete darkness and 100% relative humidity. Plants were then transferred to a growth chamber at 20 °C with a photoperiod of 14 h of light and 10 h of darkness and a light intensity of 148 µmol m−2 s−1. By 14 dpi, disease severity (DS) was visually estimated as the percentage of canopy covered by rust. In order to compare DS from different seasons and conditions, DS values from each trial were standardized by expressing each DS value as a percentage of the highest one in each location/experiment that is set at 100% (DSr) [27,28]. Infection Type (IT) was also assessed using the scale of Stakman et al. (1962) [29], where IT 0 = no symptoms, IT ; = necrotic flecks, IT 1 = minute pustules barely sporulating, IT 2 = necrotic halo surrounding small pustules, IT 3 = chlorotic halo and IT 4 = well-formed pustules with no associated chlorosis or necrosis.
All components of resistance among lentil accessions and fungal isolates were subjected to an ANOVA and mean values were separated by LSD test at p = 0.01. Pearson’s linear correlations between field and controlled conditions parameters were calculated.

3. Results

Phenotypic Response

Due to seed availability and differential germination capacity, not all accessions could be studied at all conditions, but 221 accessions were evaluated in the field in 2014, 454 in 2015, 510 in seedlings under controlled conditions against SPA isolate, 445 against MOR isolate, 373 against FRA isolate and 377 against ALG isolate, respectively (Figure 1). Large variation was identified for DS in the collections in all trials (Figure 1). Higher rust pressure was achieved in the field in 2014 than in 2015 (average DS 48% vs. 25%, respectively) which might have hidden quantitatively expressed slow rusting response that is typically better detected at moderate–low disease pressure [30]. The lower disease pressure achieved during the second season might be ascribed to the dryer conditions (342 mm of rain during first crop season compared to only 148 mm in the second season) (Table 1).
There was high variation for DS within each species, including cultivated lentil types (Table 2). However, both lower DS values (both average and range) were recorded in wild relatives although highly susceptible accessions were observed in all species. In any case, even when higher average DS values were observed in the field and under controlled conditions for cultivated lentil and the closer relative L.c. orientalis, accessions with high resistance were identified within both species as shown by the ranges of DS displayed in Table 2. The other way around, although average DS was low in the more distant relatives L. ervoides, L. nigricans and L. lamottei, susceptible accession were identified in all of them.
Adult plant responses in the field (DS%) in the two field seasons were significantly correlated (0.46, p < 0.001) (Table 3). DS in the field in 2015 were significantly correlated with seedling responses under controlled conditions with all isolates. However, DSfield2014 was not significantly correlated with seedling responses against isolates SPA and ALG. Seedling responses against all isolates were significantly correlated.
Hypersensitive response (IT < 3) was observed in accessions of L.c. culinaris in a frequency ranging from 1.4 to 3.4% depending on the isolate (Table 4). Frequency of occurrence in other species might be handled with care as lower numbers of accessions were studied, but it was more frequently identified in L. ervoides (9 to 21.4% of the accessions, depending on the isolate), followed by L. nigricans (0 to 8.3%). It was observed only against two isolates in L.c. orientalis, and not observed in L.c. odemensis or L. lamottei. However, this might be due to the lower number of accessions studied of these two species.
IT scores showed a clear isolate-specific response suggesting race specificity, so each isolate might be considered a different race, SPA being the most virulent one, followed by MOR and FRA, ALG being the less virulent. Hypersensitive resistance (IT < 3) was identified against all of them (Table 5 and Table 6 and Supplementary Table S1). Accessions 1308 (L. ervoides) and 1561 (L.c. culinaris) were resistant to the 4 isolates. Accession 1168 (L.c. culinaris) was resistant to isolates SPA, FRA and ALG, but susceptible to isolate MOR. Accessions 1515, 1559 (L.c. culinaris) were resistant to isolates SPA, MOR and ALG, but susceptible to isolate FRA. Accession 1599 (L. nigricans) was also resistant to isolates SPA, MOR and ALG, but could not be studied against isolate FRA. In addition, accession 1571 (L. ervoides) was resistant to isolates SPA and MOR, although it could not be studied against FRA and ALG. Accession 1145 (L.c. culinaris) was resistant to isolates FRA, ALG and MOR, but susceptible to isolate SPA. Accession 1413 (L.c. culinaris) was resistant to isolates SPA and MOR, but susceptible to FRA and ALG. Accession 1632 (L.c. orientalis) was resistant to isolates SPA and FRA, but susceptible to MOR and ALG. Accession 1656 (L. nigricans) was resistant to isolates MOR and ALG, but susceptible to SPA and FRA. Accessions 1165, 1324, 1331, 1351, 1361, 1430, 1552, 1553 (L.c. culinaris) were resistant to isolate ALG only, susceptible to SPA, MOR and FRA. Accessions 1288, 1470, 1471 (L.c. culinaris) were resistant to isolate FRA only, susceptible to SPA, MOR and ALG.
In addition to the hypersensitive response mentioned above, the screenings allowed identification of accessions with reduced rust severity in spite of a compatible interaction (high IT), fitting the definition of Partial Resistance [30,31] (Table 7 and Supplementary Table S1). There was a high variation for DSr values across accessions with high IT, but low levels of DSr at all environments (seasons and isolates) were not very frequent, suggesting isolate specificity also for DSr.
Screenings allowed identification of Adult Plant Resistance (APR) not based on hypersensitivity, with accessions 1660 (L. nigricans), 1613 (L.c. orientalis) and 1387, 1392, 1403, 1417, 1452, 1449, 1455, 1473, 1479, 1501, 1511, 1516, 1517, 1518, 1519, 1564, 1565 (L.c. culinaris) (Table 8) showing reduced severity in adult plants in the field (DSr < 20%), whereas they were highly susceptible in seedlings against all isolates (IT > 3, DSr > 50%).

4. Discussion

Lentil is an important pulse crop worldwide. However, the species suffers from relatively low genetic diversity due to a genetic bottleneck created during domestication when it underwent selection for a small number of traits [22]. This has limited the genetic variation available in the cultivated gene pool for improving important agronomic traits. This reinforces the value of exploring wild relatives as potential source of genes that might have been lost during the domestication process [32].
Resistance to rust in lentil has been identified both in cultivated lentils and its wild relatives and frequently reported to be monogenic [9,10,11,12,13,14,15,33] which does not exclude the existence of polygenic resistance. As for most cool season grain legumes [8,27], the phenotypic expression of the rust resistance reactions reported so far in lentils is poorly described. Rust resistance breeding in lentil, as in most cool season legumes, has been hampered by the relatively low investment in genetics, genomics and biotechnology of the legume crops which is impressively improving recently [34]. However, less attention has been paid to the understanding of the rust pathogen, with still little agreement on its host specialization and the existence of races [5,8], contrasting with the situation of rusts of other legumes such as common bean (Phaseolus vulgaris) and soybean (Glycine max) which have been largely studied leading to the identification of races and of resistance genes [35,36]. Surprisingly, knowledge on the existence of races or even host specialization in U. viciae-fabae is still very limited. Insights into the U. viciae-fabae genome have been initiated [37], which can help in the search for secreted proteins and effectors. However, basic knowledge of pathogenic variation is still insufficient. Race existence has been suggested within the faba bean infecting isolates [38,39] and in lentil isolates [40,41], indicating that pathogenic variation indeed might exist within the various U. viciae-fabae populations, but a standard differential set for race identification has not been agreed upon and currently races are not named, and their distributions are not monitored anywhere. Our IT scores showed a clear isolate-specific response suggesting race specificity, so each isolate might be considered a different race, SPA being the most virulent one, followed by MOR and FRA, ALG being the less virulent. Resistance was identified against all isolates, which might be the basis to develop a standard differential set what should be a priority for rust definition and monitoring [5].
In this study, we determined a significant number of accessions with resistance based on hypersensitive reaction (HR, low IT) in all Lens species studied. Hypersensitive response was more frequently identified in L. ervoides followed by L. nigricans. It was observed only against two isolates in L.c. orientalis, and not observed in L.c. odemensis or L. lamottei, but this might be due to the lower number of accessions studied of these two species. Interestingly, although at lower frequency than in L. ervoides and L. nigricans, hypersensitive response was also observed within cultivated lentil, with accession 1561 (L.c. culinaris) displaying resistance to the four isolates making this accession a valuable ready-to-use resource for lentil resistance breeding. Resistance to all other rust isolates was also available within L.c. culinaris in an isolate-specific manner. Accession 1308 (L. ervoides) was also resistant (low IT) to all isolates, and a number of accessions of other wild Lens species also displayed resistance against some of the isolates in an isolate-specific manner, calling the attention to the need to study their inheritance to discern whether novel resistance gene(s) are different from those in L.c. culinaris. Although we did not study the inheritance, a feasible starting hypothesis might be that they might be monogenic as is typically the case for HR. It is important to clarify that HR can be complete (IT 0) but also incomplete, allowing some sporulation and rust development (IT 1–2).
Both pre-haustorial- and post-haustorial-based types of resistance were earlier reported in lentil germplasm [10,11]. Post-haustorial resistance is typically based on hypersensitivity, whereas pre-haustorial resistance is not, and is typical in partial resistance causing a reduced DS with no host cell necrosis [42,43,44,45,46,47]. However, the use of “partial resistance” concept might be misleading as incomplete HR can often be confounded with partial resistance if not enough attention is paid to the presence/absence of macroscopically visible necrosis associated with developing rust pustules. This might be the case of reported single inheritance to rust in lentil, but we cannot draw a conclusion as these reports are often based on field screenings without detailed description of types of resistance responses but just on scales based on amount of pustules and plant damage, such as the 1–9 scale [48] without clear indications on actual presence or absence of necrosis indicative of HR. Therefore, care should be taken when interpreting published results based on different scales. A combination of a qualitative (such as IT based on presence/absence of necrosis) and a quantitative assessment (DS) should therefore be preferred for any rust screening to identify both partial and hypersensitive resistances to rust, as is nowadays commonly practiced [27,46,49]. Our screenings allowed identification of accessions with partial resistance (reduced DS in spite of high IT) [30,31], but this was not very frequent.
Race non-specific adult plant resistance (APR) associated with slow rusting has frequently been exploited in wheat [50,51,52]. APR is believed to be more durable for successful long-term rust control [53,54] as it is generally not affected by race, and keeps the disease below the threshold level and decreases the chances of selection of new pathotypes. APR has also been identified in a range on legume crops against their rust [55,56] plant resistance. We identified accessions with such adult plant resistance, showing reduced severity in adult plants in the field (DSr < 20%) in spite of high susceptibility in seedlings against all isolates. This was more frequently identified in L.c. culinaris, but also in L. nigricans and L.c. orientalis. Genetic analysis would be needed to conclude on the inheritance of the identified resistances.

5. Conclusions

The fact that hypersensitive, partial and adult plant resistance have been identified within L.c. culinaris enables immediate direct use in lentil resistance breeding. Additional valuable sources of resistance have been identified in related species of the primary and secondary gene pools, crossable with cultivated lentils [25,26], making feasible the transfer of rust resistance genes to cultivated lentil. These novel resistance sources should be the base of further studies to establish the genetic, biochemical, and molecular base of rust resistance in lentil. The interest in the incorporation of genetic diversity of wild lentils in pre-breeding and breeding programs is endorsed by recent studies targeting these species [23,57,58,59].

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/plants12030626/s1, Table S1: Response of the Lens germplasm accessions to U. viciae-fabae ex L. culinaris studied. DS = Disease Severity (%); IT = Infection Type according Stakman et al. (1962) [29], 6 where IT 0 = no symptoms, IT ; = necrotic flecks, IT 1 = minute pustules barely sporulating, IT 2 = necrotic halo surrounding small pustules, IT 3 = chlorotic halo and IT 4 = well-formed pustules with 7 no associated chlorosis or necrosis. 8 Ns = not studied

Author Contributions

Conceptualization, methodology, formal analysis and data curation, writing—review and editing, E.B. and D.R.; funding acquisition, D.R. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Spanish Agencia Estatal de Investigación (AEI) grant PID2020-114668RB-100.

Data Availability Statement

All relevant data are within the paper and its Supporting Information Files.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. FAOSTAT. Available online: http://www.fao.org/faostat (accessed on 20 December 2022).
  2. Muehlbauer, F.J.; Cho, S.; Sarker, A.; McPhee, K.E.; Coyne, C.J.; Rajesh, P.N.; Rebecca, R. Application of biotechnology in breeding lentil for resistance to biotic and abiotic stress. Euphytica 2006, 147, 149–165. [Google Scholar]
  3. Rubiales, D.; Moral, A.; Flores, F. Heat Waves and Broomrape Are the Major Constraints for Lentil Cultivation in Southern Spain. Agronomy 2021, 11, 1871. [Google Scholar] [CrossRef]
  4. Chen, W.; Basandrai, A.K.; Basandrai, D.; Banniza, S.; Bayaa, B.; Buchwaldt, L.; Davidson, J.; Larsen, R.; Rubiales, D.; Taylor, P. Lentil Diseases and Their Management. In The Lentil: Botany, Production and Uses; Erskine, W., Muehlbauer, F.J., Sarker, A., Sharma, B., Eds.; CABI: Wallingfore, UK, 2009; pp. 262–281. ISBN 13 978-1-84593-487-3. [Google Scholar]
  5. Negussie, T.; Pretorius, Z.A. Lentil rust: Present status and future prospects. Crop Prot. 2012, 32, 119–128. [Google Scholar] [CrossRef]
  6. Emeran, A.A.; Sillero, J.C.; Fernández-Aparicio, M.; Rubiales, D. Chemical Control of Faba Bean Rust (Uromyces Viciae-Fabae). Crop Prot. 2011, 30, 907–912. [Google Scholar] [CrossRef]
  7. Sharma, R.B.; Singh, A.K.; Thakur, M.B.; Ahmad, M.R. Fungicidal Management of Lentil Rust (Uromyces fabae (Pers.) de Bary). Int. J. Pure App. Biosci. 2018, 6, 729–731. [Google Scholar]
  8. Rubiales, D.; Castillejo, M.A.; Madrid, E.; Barilli, E.; Rispail, N. Legume breeding for rust resistance: Lessons to learn from the model Medicago truncatula. Euphytica 2011, 180, 89–98. [Google Scholar] [CrossRef] [Green Version]
  9. Negussie, T.G.; Pretorius, Z.A.; Bender, C.M. Components of rust resistance in lentil. Euphytica 2005, 142, 55–64. [Google Scholar]
  10. Negussie, T.G.; Bender, C.M.; van Wyk, P.W.J.; Pretorius, Z.A. Hypersensitivity of rust resistance in lentil. S. Afr. J. Plant Soil 2012, 29, 25–29. [Google Scholar]
  11. Rubiales, D.; Rojas-Molina, M.M.; Sillero, J.C. Identification of pre and posthaustorial resistance to rust (Uromyces viciae-fabae) in lentil (Lens culinaris) germplasm. Plant Breed. 2013, 132, 676–680. [Google Scholar] [CrossRef]
  12. Saha, G.C.; Sarker, A.; Chen, W.; Vandemark, G.J.; Muehlbauer, F.J. Identification of markers associated with genes for rust resistance in Lens culinaris Medik. Euphytica 2010, 175, 261–265. [Google Scholar] [CrossRef]
  13. Mekonnen, F.; Mekbib, F.; Kumar, S.; Ahmed, S.; Chahota, R.K.; Sharma, T.R.; Singh, S.; Gill, R.K.; Kumar, A. Identification of molecular markers associated with rust (Uromyces vicia-fabae Pers.) resistance genes in lentil (Lens culinaris sub sp. culinaris). Can. J. Plant Prot. 2014, 2, 27–36. [Google Scholar]
  14. Dikshit, H.K.; Singh, A.; Singh, D.; Aski, M.; Jain, N.; Hedge, V.S.; Basandrai, A.K.; Basandrai, D.; Sharma, T.R. Tagging and mapping of SSR marker for rust resistance in lentil (Lens culinaris Medikus subsp. culinaris). Indian J. Exp. Biol. 2016, 54, 394–399. [Google Scholar]
  15. Singh, J.; Sirari, A.; Singh, H.; Kumar, A.; Jaidka, M.; Mandahal, K.S.; Kumar, S.; Singh, S. Identifying and validating SSR markers linked with rust resistance in lentil (Lens culinaris). Plant Breed. 2021, 140, 477–485. [Google Scholar] [CrossRef]
  16. Chen, W.; Sharma, H.; Muehlbauer, F. Compendium of Chickpea and Lentil Diseases and Pests; American Phytopathological Society (APS Press): St. Paul, MN, USA, 2011. [Google Scholar]
  17. Emeran, A.A.; Sillero, J.C.; Niks, R.E.; Rubiales, D. Infection Structures of Host-Specialized Isolates of Uromyces viciae-fabae and of Other Species of Uromyces Infecting Leguminous Crops. Plant Dis. 2005, 89, 17–22. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  18. Emeran, A.A.; Roman, B.; Sillero, J.C.; Satovic, Z.; Rubiales, D. Genetic Variation among and within Uromyces Species Infecting Legumes. J. Phytopathol. 2008, 156, 419–424. [Google Scholar] [CrossRef] [Green Version]
  19. Barilli, E.; Satovic, Z.; Sillero, J.C.; Rubiales, D.; Torres, A.M. Phylogenetic analysis of Uromyces species infecting grain and forage legumes by Sequence analysis of Nuclear Ribosomal Internal Transcribed Spacer Region. J. Phytopathol. 2011, 159, 137–145. [Google Scholar]
  20. Barilli, E.; Moral, A.; Sillero, J.C.; Rubiales, D. Clarification on rust species potentially infecting pea (Pisum sativum L.) crop and host range of Uromyces pisi (Pers.) Wint. Crop Prot. 2012, 37, 65–70. [Google Scholar]
  21. Rubiales, D.; Sillero, J.C.; Emeran, A.A. Response of vetches (Vicia spp.) to specialized forms of Uromyces vicia-fabae and to Uromyces pisi. Crop Prot. 2013, 46, 38–43. [Google Scholar]
  22. Zohary, D. Pulse domestication and cereal domestication: How different are they? Econ. Bot. 1989, 43, 31–34. [Google Scholar] [CrossRef]
  23. Singh, M.; Kumar, S.; Basandrai, A.K.; Basandrai, D.; Malhotra, N.; Saxena, D.R.; Gupta, D.; Sarker, A.; Singh, K. Evaluation and identification of wild lentil accessions for enhancing genetic gains of cultivated varieties. PLoS ONE 2020, 15, e0229554. [Google Scholar] [CrossRef] [Green Version]
  24. Rubio-Teso, M.L.; Lara-Romero, C.; Rubiales, D.; Parra-Quijano, M.; Iriondo, J.M. Searching for abiotic tolerant and biotic stress resistant wild lentils for introgression breeding through predictive characterization. Front. Plant Sci. 2022, 13, 817849. [Google Scholar] [CrossRef] [PubMed]
  25. Fratini, R.; Ruiz, M.L. Wide Crossing in Lentil through Embryo Rescue. In Plant Embryo Culture. Methods in Molecular Biology; Thorpe, T., Yeung, E., Eds.; Humana Press: Totowa, NJ, USA, 2011; Volume 710. [Google Scholar] [CrossRef]
  26. Tullu, A.; Bett, K.; Banniza, S.; Vail, S.; Vandenberg, A. Widening the genetic base of cultivated lentil through hybridization of Lens culinaris “Eston” and L. ervoides accession IG 72815. Can. J. Plant Sci. 2013, 93, 1037–1047. [Google Scholar] [CrossRef]
  27. Sillero, J.C.; Fondevilla, S.; Davidson, J.; Vaz Patto, M.C.; Warkentin, T.D.; Thomas, J.; Rubiales, D. Screening techniques and sources of resistance to rusts and mildews in grain legumes. Euphytica 2006, 147, 255–272. [Google Scholar]
  28. Sillero, J.C.; Rojas-Molina, M.M.; Emeran, A.A.; Kharrat, M.; Winkler, J.; Khan, H.R.; Flores, F.; Rubiales, D. Identification and multi-environment validation of resistance to rust (Uromyces viciae-fabae) in Vicia faba. Crop Pasture Sci. 2017, 68, 1013–1023. [Google Scholar] [CrossRef]
  29. Stakman, E.C.; Stewart, D.M.; Loegering, W.Q. Identification of Physiologic Races of Puccinia graminis var. tritici; United States Department of Agriculture, Agricultural Research Service: Beltsville, MD, USA, 1962; p. 54. [Google Scholar]
  30. Niks, R.E.; Rubiales, D. Potentially durable resistance mechanisms in plants to specialised fungal pathogens. Euphytica 2002, 124, 201–216. [Google Scholar]
  31. Parlevliet, J.E.; van Ommeren, A. Partial resistance of barley rust, Puccinia hordei. II. Relationship between field trials, microplot tests and latent period. Euphytica 1975, 24, 293–303. [Google Scholar] [CrossRef]
  32. Warschefsky, E.; Penmetsa, R.V.; Cook, D.R.; von Wettberg, E.J.B. Back to the wilds: Tapping evolutionary adaptations for resilient crops through systematic hybridization with crop wild relatives. Am. J. Bot. 2014, 101, 1791–1800. [Google Scholar] [CrossRef]
  33. Erskine, W.; Tufail, M.; Russell, A.; Tyagi, M.C.; Arman, M.M.; Saxena, M.C. Current and future strategies in breeding lentil for resistance to biotic and abiotic stresses. Euphytica 1994, 73, 127–135. [Google Scholar] [CrossRef]
  34. Kumar, J.; Gupta, D.S.; Tiwari, P. Lentil Breeding in Genomic Era: Present Status and Future Prospects. In Accelerated Plant Breeding; Food Legumes; Springer: Cham, Switzerland, 2020; Volume 3, pp. 193–209. [Google Scholar] [CrossRef]
  35. Miklas, P.N.; Kelly, J.D.; Beebe, S.E.; Blair, M.W. Common bean breeding for resistance against biotic and abiotic stresses: From classical to MAS breeding. Euphytica 2006, 147, 105–131. [Google Scholar]
  36. Hyten, D.L.; Hartman, G.L.; Nelson, R.L.; Frederick, R.D.; Concibido, V.C.; Narvel, J.M.; Cregan, P.B. Map location of the locus that confers resistance to soybean rust in soybean. Crop Sci. 2007, 47, 837–838. [Google Scholar]
  37. Link, T.; Seibel, C.; Voegele, R.T. Early insights into the genome sequence of Uromyces fabae. Front. Plant Sci. 2014, 5, 587. [Google Scholar]
  38. Rojas-Molina, M.M.; Rubiales, D.; Sillero, J.C. Pathogenic specialization of Uromyces viciae-fabae in Spain and Portugal. In International Workshop on Faba Bean Breeding and Agronomy; Cubero, J.I., Moreno, M.T., Suso, M.J., Torres, A.M., Avila, C.M., Eds.; IFAPA: Córdoba, Spain, 2006; pp. 154–156. [Google Scholar]
  39. Ijaz, U.; Adhikari, K.N.; Stoddard, F.L.; Trethowan, R.M. Rust resistance in faba bean (Vicia faba L.): Status and strategies for improvement. Aust. Plant Pathol. 2018, 47, 71–81. [Google Scholar] [CrossRef]
  40. Singh, S.J.; Sokhi, S.S. Pathogenic variability in Uromyces viciae fabae. Plant Dis. 1980, 64, 671–672. [Google Scholar] [CrossRef] [Green Version]
  41. Singh, K.; Singh, R.S.; Gumber, R.K. Physiologic specialization in Uromyces fabae causing lentil rust. LENS Newsl. 1995, 22, 46–57. [Google Scholar]
  42. Niks, R.E.; Walther, U.; Jaiser, H.; Martínez, F.; Rubiales, D.; Andersen, O.; Flath, K.; Gymer, P.; Heinrichs, F.; Jonsson, R.; et al. Resistance against barley leaf rust (Puccinia hordei) in West-European spring barley germplasm. Agronomie 2000, 20, 769–778. [Google Scholar] [CrossRef] [Green Version]
  43. Sillero, J.C.; Moreno, M.T.; Rubiales, D. Characterization of new sources of resistance to Uromyces viciae-fabae in a germplasm collection of Vicia faba. Plant Pathol. 2000, 49, 389–395. [Google Scholar] [CrossRef]
  44. Rubiales, D.; Moral, A. Prehaustorial resistance against alfalfa rust (Uromyces striatus) in Medicago truncatula. Eur. J. Plant Pathol. 2004, 110, 239–243. [Google Scholar] [CrossRef]
  45. Sillero, J.C.; Moreno-Alías, I.; Rubiales, D. Identification and characterization of resistance to rust (Uromyces ciceris-arietini (Grognot) Jacz. & Boyd) in a germplasm collection of Cicer spp. Euphytica 2012, 188, 229–238. [Google Scholar] [CrossRef]
  46. Barilli, E.; Sillero, J.C.; Fernández-Aparicio, M.; Rubiales, D. Identification of resistance to Uromyces pisi (Pers.) Wint. in Pisum spp. germplasm. Field Crops Res. 2009, 114, 198–203. [Google Scholar] [CrossRef]
  47. Martins, D.C.; Rubiales, D.; Vaz Patto, M.C. Association Mapping of Lathyrus sativus Disease Response to Uromyces pisi Reveals Novel Loci Underlying Partial Resistance. Front. Plant Sci. 2022, 13, 842545. [Google Scholar] [CrossRef]
  48. Bejiga, G.; Anbessa, Y. Development of rust-resistant lentil cultivars in Ethiopia. LENS Newsl. 1999, 26, 33–34. [Google Scholar]
  49. Rubiales, D.; Fondevilla, S.; Chen, W.; Gentzbittel, L.; Higgins, T.J.V.; Castillejo, M.A.; Singh, K.B.; Rispail, N. Achievements and Challenges in Legume Breeding for Pest and Disease Resistance. CRC Crit. Rev. Plant Sci. 2015, 34, 195–236. [Google Scholar] [CrossRef] [Green Version]
  50. Bai, B.; Li, Z.; Wang, H.; Du, X.; Wu, L.; Du, J.; Lan, C. Genetic Analysis of Adult Plant Resistance to Stripe Rust in Common Wheat Cultivar “Pascal”. Front. Plant Sci. 2022, 13, 918437. [Google Scholar] [CrossRef] [PubMed]
  51. Zhao, R.; Liu, B.; Wan, W.; Jiang, Z.; Chen, T.; Wang, L.; Bie, T. Mapping and characterization of a novel adult-plant leaf rust resistance gene LrYang16G216 via bulked segregant analysis and conventional linkage method. Theor. Appl. Genet. 2023, 136, 1–13. [Google Scholar] [CrossRef]
  52. Kumar, S.; Bhardwaj, S.C.; Gangwar, O.P.; Sharma, A.; Qureshi, N.; Kumaran, V.V.; Khan, H.; Prasad, P.; Miah, H.L.; Singh, G.P.; et al. Lr80: A new and widely effective source of leaf rust resistance of wheat for enhancing diversity of resistance among modern cultivars. Theor. Appl. Genet. 2021, 134, 849–858. [Google Scholar] [CrossRef] [PubMed]
  53. Marone, D.; Del Olmo, A.I.; Laido, G.; Sillero, J.C.; Emeran, A.A.; Russo, M.A.; Ferragonio, P.; Giovanniello, V.; Mazzucotelli, E.; De Leonardis, A.M.; et al. Genetic analysis of durable resistance against leaf rust in durum wheat. Mol. Breed. 2009, 24, 25–39. [Google Scholar] [CrossRef]
  54. Huerta-Espino, J.; Singh, R.; Crespo-Herrera, L.A.; Villaseñor-Mir, H.E.; Rodriguez-Garcia, M.F.; Dreisigacker, S.; Barcenas-Santana, D.; Lagudah, E. Adult Plant Slow Rusting Genes Confer High Levels of Resistance to Rusts in Bread Wheat Cultivars from Mexico. Front. Plant Sci. 2020, 11, 824. [Google Scholar] [CrossRef]
  55. Santos, C.; Martins, D.C.; González-Bernal, M.J.; Rubiales, D.; Vaz Patto, M.C. Integrating Phenotypic and Gene Expression Linkage Mapping to Dissect Rust Resistance in Chickling Pea. Front. Plant Sci. 2022, 13, 837613. [Google Scholar] [CrossRef]
  56. Omara, R.I.; Kamel, S.M.; El-Ganainy, S.M.; Arafa, R.A.; Mostafa, Y.S.; Alamri, S.A.; Alrumman, S.A.; Hashem, M.; Elsharkawy, M.M. Host Resistance to Uromyces appendiculatus in Common Bean Genotypes. Plants 2022, 11, 628. [Google Scholar] [CrossRef]
  57. Kumar, J.; Srivastava, E.; Singh, M.; Mahto, D.; Pratap, A.; Kumar, S. Lentil alien gene transf. Crop Plants 2014, 2, 191–205. [Google Scholar] [CrossRef]
  58. Coyne, C.J.; Kumar, S.; von Wettberg, E.J.B.; Marques, E.; Berger, J.D.; Redden, R.J.; Ellis, T.H.N.; Brus, J.; Zablatzká, L.; Smýkal, P. Potential and limits of exploitation of crop wild relatives for pea, lentil, and chickpea improvement. Legum. Sci. 2020, 2, e36. [Google Scholar] [CrossRef] [Green Version]
  59. Civantos-Gómez, I.; Rubio-Teso, M.L.; Galeano, J.; Rubiales, D.; Iriondo, J.M.; García-Algarra, J. Climate change conditions the selection of rust-resistant candidate wild lentil populations for in situ conservation. Front. Plant Sci. 2022, 13, 1010799. [Google Scholar] [CrossRef] [PubMed]
Plants 12 00626 g001 550
Figure 1. Phenotypic variation in rust response (DS) among Lens collection (525 accessions, different numbers studied on the different trials) after inoculation with U. viciae-fabae ex L. culinaris. Field2014 = adult plants in the field 2014; Field2015 = adult plants in the field 2015; ccSPA = seedlings under controlled conditions inoculated with isolate SPA; ccMOR = seedlings under controlled conditions inoculated with isolate MOR; ccFRA = seedlings under controlled conditions inoculated with isolate FRA; ccALG = seedlings under controlled conditions inoculated with isolate ALG.
Figure 1. Phenotypic variation in rust response (DS) among Lens collection (525 accessions, different numbers studied on the different trials) after inoculation with U. viciae-fabae ex L. culinaris. Field2014 = adult plants in the field 2014; Field2015 = adult plants in the field 2015; ccSPA = seedlings under controlled conditions inoculated with isolate SPA; ccMOR = seedlings under controlled conditions inoculated with isolate MOR; ccFRA = seedlings under controlled conditions inoculated with isolate FRA; ccALG = seedlings under controlled conditions inoculated with isolate ALG.
Plants 12 00626 g001
Table
Table 1. Description of the sites for field testing. Climatic data correspond to the field seasons only (1 December to 30 June).
Table 1. Description of the sites for field testing. Climatic data correspond to the field seasons only (1 December to 30 June).
ExperimentSeasonSiteLatit.Longit.Type of SoilSoil pHAltit.Average Tmin (°C)Average Tmax (°C)Rain (mm)
Field142013–2014Córdoba, Spain37°86′ N4°78′ WCambisol7.8948.323.5342.4
Field152014–2015Córdoba, Spain37°86′ N4°78′ WCambisol7.8947.723.3148.8
Table
Table 2. Average and range of DS (%) observed at each trial, grouped by Lens species. Field2014 = adult plants in the field 2014; Field2015 = adult plants in the field 2015; ccSPA = seedlings under controlled conditions inoculated with isolate SPA; ccMOR = seedlings under controlled conditions inoculated with isolate MOR; ccFRA = seedlings under controlled conditions inoculated with isolate FRA; ccALG = seedlings under controlled conditions inoculated with isolate ALG; s.d. = standard deviation; ns: not studied.
Table 2. Average and range of DS (%) observed at each trial, grouped by Lens species. Field2014 = adult plants in the field 2014; Field2015 = adult plants in the field 2015; ccSPA = seedlings under controlled conditions inoculated with isolate SPA; ccMOR = seedlings under controlled conditions inoculated with isolate MOR; ccFRA = seedlings under controlled conditions inoculated with isolate FRA; ccALG = seedlings under controlled conditions inoculated with isolate ALG; s.d. = standard deviation; ns: not studied.
Disease Severity (DS %)
Season/IsolateL.c. culinarisL.c. orientalisL.c. odemensisL. ervoidesL. lamotteiL. nigricans
DS (Range) s.d.DS (Range) s.d.DS(Range) s.d.DS(Range) s.d.DS(Range) s.d.DS(Range) s.d.
Adult plants in field trialsField201448 (1–85) 22nsns23 (12–30) 149 (0–20) 12nsns10 (10–11) 9
Field201525 (0–55) 1616 (0–40) 135 (1–9) 49 (0–40) 128 (1–15) 1116 (0–23) 15
Seedlings under controlled conditionsccSPA42 (8–73) 1335 (10–60) 1331 (23–40) 1423 (0–40) 1318 (10–25) 1525 (5–45) 15
ccMOR38 (4–70) 1428 (0–45) 1117 (8–18) 1319 (1–50) 1416 (15–17) 422 (0–40) 10
ccFRA43 (0–80) 1741 (5–70) 1518 (6–21) 1124 (3–50) 178 (5–10) 328 (5–60) 14
ccALG32 (0–65) 1728 (3–50) 145 (1–28) 1016 (0–30) 1625 (25) -21 (0–60) 16
Table
Table 3. Pearson’s linear correlation coefficient between DS accessed under field and controlled conditions trials. ***, **, * = p < 0.001, <0.01, <0.1, respectively; ns = not significant.
Table 3. Pearson’s linear correlation coefficient between DS accessed under field and controlled conditions trials. ***, **, * = p < 0.001, <0.01, <0.1, respectively; ns = not significant.
DSfield14DSfield15DSccSPADSccMORDSccFRA
DSfield150.46 ***
DSccSPA0.09 ns0.27 ***
DSccMOR0.26 ***0.22 ***0.43 ***
DSccFRA0.24 **0.19 *0.36 ***0.42 ***
DSccALG0.10 ns0.17 *0.37 ***0.42 ***0.21 **
Table
Table 4. Number of accessions showing hypersensitive response (IT < 3) across the various Lens species against the various isolates of U. viciae-fabae ex L. culinaris. Seedling tests under controlled conditions.
Table 4. Number of accessions showing hypersensitive response (IT < 3) across the various Lens species against the various isolates of U. viciae-fabae ex L. culinaris. Seedling tests under controlled conditions.
IsolateL.c. culinarisL.c. orientalisL.c. odemensisL. ervoidesL. lamotteiL. nigricans
SPA7 in 510 (1.4%)1 in 29 (3.4%)0 in 6 (0%)2 in 16 (12.5%)0 in 2 (0%)1 in 32 (3.1%)
MOR7 in 445 (1.6%)0 in30 (0%)0 in 6 (0%)3 in 19 (15.8%)0 in 2 (0%)2 in 31 (6.4%)
FRA6 in 373 (1.6%)1 in 21 (4.8%)0 in 5 (0%)1 in 11 (9%)0 in 2 (0%)0 in 19 (0%)
ALG13 in 377 (3.4%)0 in 26 (0%)0 in 5 (0%)3 in 14 (21.4%)0 in 1 (0%)2 in 24 (8.3%)
Table
Table 5. Selection of accessions carrying hypersensitive response to any of the isolates of U. viciae-fabae ex L. culinaris studied. CcSPA = seedlings under controlled conditions inoculated with isolate SPA; ccMOR = seedlings under controlled conditions inoculated with isolate MOR; ccFRA = seedlings under controlled conditions inoculated with isolate FRA; ccALG = seedlings under controlled conditions inoculated with isolate ALG; ns: not studied; IT = Infection Type according to Stakman et al. (1962) [29], where IT 0 = no symptoms, IT ; = necrotic flecks, IT 1 = min pustules barely sporulating, IT 2 = necrotic halo surrounding small pustules, IT 3 = chlorotic halo and IT 4 = well-formed pustules with no associated chlorosis or necrosis. Response R (IT < 3), S (IT ≥ 3).
Table 5. Selection of accessions carrying hypersensitive response to any of the isolates of U. viciae-fabae ex L. culinaris studied. CcSPA = seedlings under controlled conditions inoculated with isolate SPA; ccMOR = seedlings under controlled conditions inoculated with isolate MOR; ccFRA = seedlings under controlled conditions inoculated with isolate FRA; ccALG = seedlings under controlled conditions inoculated with isolate ALG; ns: not studied; IT = Infection Type according to Stakman et al. (1962) [29], where IT 0 = no symptoms, IT ; = necrotic flecks, IT 1 = min pustules barely sporulating, IT 2 = necrotic halo surrounding small pustules, IT 3 = chlorotic halo and IT 4 = well-formed pustules with no associated chlorosis or necrosis. Response R (IT < 3), S (IT ≥ 3).
Accession SpeciesccSPAccMORccFRAccALG
ITDSResponseITDSResponseITDSResponseITDSResponse
1308ILWL40L. ervoides1+6R13R23R;0R
1561PI518734L.c. culinaris;0R17R;0R;0R
1168BGE034194L.c. culinaris1+21R411S1+12R14R
1515PI451763L.c. culinaris238R228R345S210R
1559PI518732L.c. culinaris18R25R45S;0R
1599PI572349L. nigricans15R;0Rnsnsns;0R
1145BGE026701L.c. culinaris327S1+12R17R;0R
1571PI572316L. ervoides;0R15Rnsnsnsnsnsns
1413PI320944L.c. culinaris2+13R18R460S458S
1632PI612249L.c. orientales2+10R417S25R410S
1656BCU001428L. nigricans428S1+15R45S25R
1324W6 277757L.c. culinaris343S329S470S115R
1331W6 27765L.c. culinaris328S437S450S225R
1165BGE031070L.c. culinaris440S417S423S24R
1318ILWL271L. ervoidesnsnsns410S447S;0R
1351PI209858L.c. culinaris445S425S460S;0R
1361PI251032L.c. culinaris322S313S450S1+18R
1430PI345627L.c. culinaris323S440S435S1+13R
1552PI477921L.c. culinaris337S415S420S;0R
1553PI486127L.c. culinaris340S435S450S210R
1586PI572331L. ervoides420S3-25Snsnsns;0R
1288BGE019580L.c. culinaris424S39S2-5R45S
1470PI431714L.c. culinaris443S440S2+30R440S
1471PI431717L.c. culinaris445S445S2+30R440S
1626PI572396L.c. orientalisnsnsns;0Rnsnsnsnsnsns
Table
Table 6. Summary of responses identified against the four rust isolates studied showing clear isolate-specific responses corresponding to minimum four races, with sources of resistance to each one.
Table 6. Summary of responses identified against the four rust isolates studied showing clear isolate-specific responses corresponding to minimum four races, with sources of resistance to each one.
AccessionsSpeciesResponse to
Isol SPA		Response to Isol MORResponse to Isol FRAResponse to Isol ALG
1308, 1561L. ervoides, L.c. culinarisRRRR
1145L.c. culinarisSRRR
1168L.c. culinarisRSRR
1515, 1559L.c. culinarisRRSR
1656L. nigricansSRSR
1165, 1324, 1331, 1351, 1361, 1430, 1552, 1553L.c. culinarisSSSR
1632L.c. orientalesRSRS
1288, 1470, 1471L.c. culinarisSSRS
1413L.c. culinarisRRSS
Most accessions SSSS
Table
Table 7. Selection of candidates for partial resistance against isolates of U. viciae-fabae ex L. culinaris. From full data provided in Supplementary Table S1, we highlight here accessions displaying a compatible interaction (IT > 3) but reduced infection at all conditions (DSr < 35%). Data with the same letter per column are not significantly different (LSD test, p < 0.01); ns = not studied.
Table 7. Selection of candidates for partial resistance against isolates of U. viciae-fabae ex L. culinaris. From full data provided in Supplementary Table S1, we highlight here accessions displaying a compatible interaction (IT > 3) but reduced infection at all conditions (DSr < 35%). Data with the same letter per column are not significantly different (LSD test, p < 0.01); ns = not studied.
Accession SpeciesAdult Plants in the FieldSeedlings Under Controlled Conditions
Isol SPAIsol MORIsol FRAIsol ALG
2014 DSr2015 DSrITDSrITDSrITDSrITDSr
1311ILWL38L. nigricans1 b2 b418 bc49 c424 ab33 d
1303ILWL31L. nigricans13 ans426 ab427 a419 ab431 a
1658BCU001430L. nigricansns0.5 c47 d47 cnsns423 ab
1673BCU001901L. nigricansns10 a421 abc410 bcnsnsnsns
1604PI572356L. nigricansnsns425 ab429 a413 ab412 c
1574PI572319L. ervoidesns0.5 c427 a3+29 ansns431 a
1593PI572338L. ervoidesnsns41 dnsns46 b415 c
1588PI572333L. ervoidesnsns421 abc417 abcnsns431 a
1661BCU001511L. lamotteins1 bc414 c421 ab46 bnsns
1317ILWL261L.c. odemensis33 a2 b432 a413 bc426 a32 d
1300BGE34196L.c. culinaris12 ans425 ab46 c410 abnsns
1446PI426784L.c. culinarisnsns432 a321 ab410 ab320 bc
Table
Table 8. Selection of candidates for adult plant resistance against U. viciae-fabae ex L. culinaris, susceptible in seedlings (IT > 3, DSr > 50%) but resistant in adult plants in the field (DSr < 20%). Data with the same letter per column are not significantly different (LSD test, p < 0.01).
Table 8. Selection of candidates for adult plant resistance against U. viciae-fabae ex L. culinaris, susceptible in seedlings (IT > 3, DSr > 50%) but resistant in adult plants in the field (DSr < 20%). Data with the same letter per column are not significantly different (LSD test, p < 0.01).
Accession SpeciesFieldSeedlings under Controlled Conditions
ccSPAccMORccFRAccALG
Field2015 DSrITDSrITDSrITITDSrITDSr
1660BCU001510L. nigricans9 a452 a450 ansns451 a
1613PI572374L.c. orientalis7 b462 a447 a450 a477 a
1455PI431631L.c. culinaris2 b468 a469 a488 a469 a
1518PI468899L.c. culinaris2 b466 a469 a475 a454 a
1517PI458503L.c. culinaris7 b479 a464 a463 a454 a
1519PI468900L.c. culinaris7 b468 a461 a463 a469 a
1374PI297287L.c. culinaris9 a475 a464 a463 a438 a
1411PI320940L.c. culinaris11 a479 a479 a475 a469 a
1565PI533693L.c. culinaris15 a478 a471 a488 a469 a
1392PI299177L.c. culinaris15 a459 a453 a463 a469 a
1449PI429369L.c. culinaris16 a455 a460 a450 a462 a
1501PI432147L.c. culinaris18 a473 a464 a463 a477 a
1511PI432259L.c. culinaris18 a468 a481 a475 a458 a
1417PI320953L.c. culinaris20 a462 a457 a450 a466 a
1387PI299120L.c. culinaris22 a486 a471 a450 a469 a
1452PI431618L.c. culinaris22 a473 a467 a450 a458 a
1564PI533691L.c. culinaris22 a458 a467 a463 a462 a
1473PI431731L.c. culinaris24 a459 a450 a463 a469 a
1516PI451766L.c. culinaris25 a464 a461 a456 a466 a
1479PI431809L.c. culinaris25 a452 a453 a450 a458 a
1403PI300250L.c. culinaris25 a451 a450 a450 a462 a
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Barilli, E.; Rubiales, D. Identification and Characterization of Resistance to Rust in Lentil and Its Wild Relatives. Plants 2023, 12, 626. https://doi.org/10.3390/plants12030626

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Barilli E, Rubiales D. Identification and Characterization of Resistance to Rust in Lentil and Its Wild Relatives. Plants. 2023; 12(3):626. https://doi.org/10.3390/plants12030626

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Barilli, Eleonora, and Diego Rubiales. 2023. "Identification and Characterization of Resistance to Rust in Lentil and Its Wild Relatives" Plants 12, no. 3: 626. https://doi.org/10.3390/plants12030626

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