Accessibility / Report Error

Pathogenicity of novel Monosporascus species in accessions of melon varietal groups

Patogenicidade de novas espécies de Monosporascus em acessos de grupos varietais de melão

Abstract

The objective of this work was to evaluate the pathogenicity of the following Monosporascus species: Monosporascus brasiliensis, Monosporascus caatinguensis, Monosporascus mossoroensis, Monosporascus nordestinus, and Monosporascus semiaridus in comparison with Monosporascus cannonballus, as well as the reaction to these pathogens of the A-16, C-32, 'Goldex', and 'Hales Best Jumbo' melon accessions, which belong to the acidulus, cantalupensis, conomon, and inodorus varietal groups, respectively. Vine decline severity was evaluated based on root damage and on the root dry matter reduction index. All studied Monosporascus species caused damage to the melon accessions, but only M. brasiliensis, M. nordestinus, and especialy M. caatinguensis were considered virulent. The A-16 accession shows higher resistance to M. nordestinus, M. caatinguensis, and M. cannonballus, whereas 'Goldex' presents susceptibility to M. caatinguensis, M. nordestinus, and M. semiaridus. The M. brasiliensis, M. caatinguensis, M. mossoroensis, M. nordestinus, and M. semiaridus species present varying levels of pathogenicity and diferent levels of infection severity, with M. semiaridus having the highest severity, and M. cannonballus, the lowest.

Index terms:
Cucumis melo ; germplasm; vine decline; virulence

Resumo

O objetivo deste trabalho foi avaliar a patogenicidade das seguintes espécies de Monosporascus: Monosporascus brasiliensis, Monosporascus caatinguensis, Monosporascus mossoroensis, Monosporascus nordestinus e Monosporascus semiaridus, em comparação com Monosporascus cannonballus, bem como a reação a esses patógenos dos acessos de melão A-16, C-32, 'Goldex' e 'Hales Best Jumbo', os quais pertencem aos grupos varietais acidulus, cantalupensis, conomon e inodorus, respectivamente. A severidade do declínio das ramas foi avaliada com base nos danos às raízes e no índice de redução da matéria seca das raízes. Todas as espécies de Monosporascus estudadas causaram danos aos acessos de melão, mas apenas M. brasiliensis, M. nordestinus e, especialmente, M. caatinguensis foram consideradas virulentas. O acesso A-16 apresenta maior resistência a M. nordestinus, M. caatinguensis e M. cannonballus, enquanto 'Goldex' apresenta susceptibilidade a M. caatinguensis, M. nordestinus e M. semiaridus. As espécies M. brasiliensis, M. caatinguensis, M. mossoroensis, M. nordestinus e M. semiaridus apresentam variados níveis de patogenicidade e diferentes níveis de severidade da infecção, com M. semiaridus tendo a maior severidade, e M. cannonballus a menor.

Termos para indexação:
Cucumis melo ; germoplasma; declínio das ramas; virulência

Introduction

The melon vine decline is a complex cucurbit syndrome caused by several species of soil-borne fungi, including Monosporascus cannonballus Pollack & Uecker, Acremonium cucurbitacearum Alfaro-García, W. Gams & García-Jim. 1996, Plectosporium tabacinum (J.F.H. Beyma) M.E. Palm, W. Gams & Nirenberg 1995, and Rhizopycnis vaga D.F. Farr [as 'vagum'], in Farr, Miller & Bruton (Chilosi et al., 2008CHILOSI, G.; REDA, R.; ALEANDRI, M.P.; CAMELE, I.; ALTIERI, L.; MONTUSCHI, C.; LANGUASCO, L.; ROSSI, V.; AGOSTEO, G.E.; MACRÌ, C.; CARLUCCI, A.; LOPS, F.; MUCCI, M.; RAIMONDO, M.L.; FRISULLO, S. Fungi associated with root rot and collapse of melon in Italy. EPPO Bulletin, v.38, p.147-154, 2008. DOI: https://doi.org/10.1111/j.1365-2338.2008.01200.x.
https://doi.org/10.1111/j.1365-2338.2008...
). Symptoms typically appear at the fruit maturity stage, which include initial yellowing and deterioration of the vine leaves, progressive defoliation, and partial or total collapse of the vines (Picó et al., 2008PICÓ, B.; ROIG, C.; FITA, A.; NUEZ, F. Quantitative detection of Monosporascus cannonballus in infected melon roots using real-time PCR. European Journal of Plant Pathology, v.120, p.147-156, 2008. DOI: https://doi.org/10.1007/s10658-007-9203-z.
https://doi.org/10.1007/s10658-007-9203-...
; Cluck et al., 2009CLUCK, T.W.; BILES, C.L.; DUGGAN, M.; JACKSON, T.; CARSON, K.; ARMENGOL, J.; GARCIA-JIMENEZ, J.; BRUTON, B.D. Association of dsRNA to Down-Regulation of Perithecial Synthesis in Monosporascus cannonballus. The Open Mycology Journal, v.3, p.9-19, 2009. DOI: https://doi.org/10.2174/1874437000903010009.
https://doi.org/10.2174/1874437000903010...
). This disease has been causing many losses around the world, especially in melon (Cucumis melo L.) and watermelon [Citrullus lanatus (Thunb.) Matsum. & Nakai] crops (Sales Jr et al., 2003SALES JR, R.; OLIVEIRA, O.F. de; SENHOR, R.F.; ALVES, M.Z. Monosporascus cannonballus agente causal do colapso em plantas de melão no Rio Grande do Norte, Brasil. Fitopatologia Brasileira, v.28, p.567, 2003. DOI: https://doi.org/10.1590/S0100-41582003000500020.
https://doi.org/10.1590/S0100-4158200300...
, 2010SALES JR, R.; SANTANA, C.V.S.; NOGUEIRA, D.R.S.; SILVA, K.J.P.; MICHEREFF, S.J.; ABAD-CAMPOS, P.; GARCÍA-JIMÉNEZ, J.; ARMENGOL, J. First Report of Monosporascus cannonballus on Watermelon in Brazil. Plant Disease, v.94, p.278, 2010. DOI: https://doi.org/10.1094/PDIS-94-2-0278B.
https://doi.org/10.1094/PDIS-94-2-0278B...
; Al-Mawaali et al., 2013AL-MAWAALI, Q.S.; AL-SADI, A.M.; AL-SAID, F.A.; DEADMAN, M.L. Etiology, development and reaction of muskmelon to vine decline under arid conditions of Oman. Phytopathologia Mediterranea, v.52, p.457-465, 2013.; Yan et al., 2016YAN, L.Y.; ZANG, Q.Y.; HUANG, Y.P.; WANG, Y.H. First report of root rot and vine decline of melon caused by Monosporascus cannonballus in Eastern Mainland China. Plant Disease, v.100, p.651, 2016. DOI: https://doi.org/10.1094/PDIS-06-15-0655-PDN.
https://doi.org/10.1094/PDIS-06-15-0655-...
; Markakis et al., 2018MARKAKIS, E.A.; TRANTAS, E.A.; LAGOGIANNI, C.S.; MPALANTINAKI, E.; PAGOULATOU, M.; VERVERIDIS, F.; GOUMAS, D.E. First report of root rot and vine decline of melon caused by Monosporascus cannonballus in Greece. Plant Disease, v.102, p.1036, 2018. DOI: https://doi.org/10.1094/PDIS-10-17-1568-PDN.
https://doi.org/10.1094/PDIS-10-17-1568-...
; Negreiros et al., 2019NEGREIROS, A.M.P.; SALES JÚNIOR, R.; RODRIGUES, A.P.M.S.; LEÓN, M.; ARMENGOL, J. Prevalent weeds collected from cucurbit fields in Northeastern Brazil reveal new species diversity in the genus Monosporascus. Annals of Applied Biology, v.174, p.349-363, 2019. DOI: https://doi.org/10.1111/aab.12493.
https://doi.org/10.1111/aab.12493...
; Sales Júnior et al., 2019SALES JÚNIOR, R.; SENHOR, R.F.; MICHEREFF, S.J.; NEGREIROS, A.M.P. Reaction of melon genotypes to the root´s rot caused by Monosporascus. Revista Caatinga, v.32, p.288-294, 2019. DOI: https://doi.org/10.1590/198321252019v32n130rc.
https://doi.org/10.1590/198321252019v32n...
).

Five novel Monosporascus species associated with the roots of Boerhavia diffusa L. and Trianthema portulacastrum Linn. were described in the Brazilian Northeastern region, namely Monosporascus brasiliensis, Monosporascus caatinguensis, Monosporascus mossoroensis, Monosporascus nordestinus, and Monosporascus semiaridus, as described by Negreiros et al. (2019)NEGREIROS, A.M.P.; SALES JÚNIOR, R.; RODRIGUES, A.P.M.S.; LEÓN, M.; ARMENGOL, J. Prevalent weeds collected from cucurbit fields in Northeastern Brazil reveal new species diversity in the genus Monosporascus. Annals of Applied Biology, v.174, p.349-363, 2019. DOI: https://doi.org/10.1111/aab.12493.
https://doi.org/10.1111/aab.12493...
, posing potential threats to cucurbit crops (Cavalcante et al., 2020CAVALCANTE, A.L.A.; NEGREIROS, A.M.P.; TAVARES, M.B.; BARRETO, E. dos S.; ARMENGOL, J.; SALES JÚNIOR, R. Characterization of Five New Monosporascus Species: Adaptation to Environmental Factors, Pathogenicity to Cucurbits and Sensitivity to Fungicides. Journal of Fungi, v.6, art.169, 2020. DOI: https://doi.org/10.3390/jof6030169.
https://doi.org/10.3390/jof6030169...
) and non-cucurbit crops, such as cowpea, jack bean, corn, sorghum, and bell pepper (Tavares et al., 2023TAVARES, M.B.; NEGREIROS, A.M.P.; CAVALCANTE, A.L.A.; OLIVEIRA, S.H.F. de; ARMENGOL, J.; SALES JÚNIOR, R. Reaction of non-cucurbitacea to Monosporascus spp. Revista Ciência Agronômica, v.54, e20218323, 2023. DOI: https://doi.org/10.5935/1806-6690.20230013.
https://doi.org/10.5935/1806-6690.202300...
). Althogh this information has been reiterated, the specific impact of these five new species on melon crops remains largely unexplored, requiring studies to assess the reaction of melon crops to Monosporascus species in Brazil, in order to develop resistant cultivars.

The objective of this work was to evaluate the pathogenicity of the following Monosporascus species: M. brasiliensis, M. caatinguensis, M. mossoroensis, M. nordestinus, and M. semiaridus in comparison with M. cannonballus, as well as the reaction to these pathogens of the A-16, C-32, 'Goldex', and 'Hales Best Jumbo' melon accessions, belonging to acidulus, cantalupensis, conomon, and inodorus varietal groups, respectively.

Materials and Methods

The research was conducted in a greenhouse located on the campus of Universidade Federal Rural do Semi-Árido (UFERSA), in the municipality of Mossoró, state of Rio Grande do Norte, Brazil. Mossoró has a dry, very hot climate, classified as BSwh’ according to the Köppen classification. The rainy season extends from summer to autumn, and the rainiest months are February, March, and Abril, with an average temperature of 27.5°C, an average annual rainfall of 670 mm, and an average relative humidity of 68.9%. The experimental period was from August 5, 2019 to September 23, 2019, during which the maximum and minimum temperatures were 34.4°C and 19°C, respectively, with an average of 26.7°C.

The melon genotypes evaluated included two commercial cultivars: Hales Best Jumbo (HBJ) and Goldex, as well as two accessions: A-16, C-32 syn. Pat 81, from the cucurbit germplasm bank at UFERSA. 'HBJ', 'Goldex', A-16, and C-32 belong to cantalupensis, inodorus, acidulous, and conomon varietal groups, respectively.

The isolates of Monosporascus spp. used were M. brasiliensis (CMM 4839), M. caatinguensis (CMM 4833), M. mossoroensis (CMM 4857), M. nordestinus (CMM 4846), M. semiaridus (CMM 4830), and M. cannonballus (CMM 2386), which were obtained from Profa. Maria Menezes Culture Collection of Phytopathogenic Fungi (CMM) at Universidade Federal Rural de Pernambuco (UFRPE).

The experiment followed a completely randomized design with five replicates, in a factorial arrangement of four melon acessions × six Monosporascus species, resulting in 24 treatments or pathosystems.

The seeds of the melon accessions were sown in trays with substrate autoclaved two times at 120°C with a 24-hour interval, composed of a 2:1 ratio of sand and Topstrato HT Hortaliças (Vida Verde, Mogi Mirim, SP, Brazil), which was also used to fill 500 mL pots for plant cultivation.

The seeds of the accessions from the Cucurbit Germplasm Bank of UFERSA were set to germinate in non-inoculated Topstrato. To produce the inocula, the mycelia of each Monosporascus species was multiplied in separate Petri dishes in sterilized potato dextrose agar (PDA) medium, using an adapted method by Ben Salem et al. (2015)BEN SALEM, I.; ARMENGOL, J.; BERBEGEL, M.; BOUGHALLEB-M’HAMDI, N. Development of a Screening Test for Resistance of Cucurbits and Cucurbita Hybrid Rootstocks to Monosporascus cannonballus. Tunisian Journal of Plant Protection, v.10, p.23-33, 2015.. The culture media containing the mycelia from each Petri dish was diluted in 300 mL of sterile distilled water and mixed using a blender. A 10 mL mycelial suspension of each Monosporascus species was inoculated into the substrate compound by 2:1 ratio of sand and Topstrato, which was incubated for seven days; then the seedlings of the melon accessions with 15 days old were transplanted to 500 mL pots, kept in a greenhouse, and irrigated daily.

The evaluations were performed 50 days after transplanting. The aerial part of the plants was removed, the roots were kept, and the substrate was washed off from the roots with tap water. The analyzed variables were: vine decline severity, using a rating scale proposed by Armengol et al. (1999)ARMENGOL, J.; SALES, R.; GARCÍA-JIMÉNEZ, J. Effects of soil moisture and water on survival of Acremonium cucurbitacearum. Journal of Phytopathology, v.147, p.737-741, 1999. DOI: https://doi.org/10.1046/j.1439-0434.1999.00448.x.
https://doi.org/10.1046/j.1439-0434.1999...
, and root dry matter. The rating scale ranged from 0 to 4, in which: 0 means no symptoms; 1, mild discoloration, or <10% root decay; 2, moderate discoloration, or 25-35% root decay; 3, death of secondary roots, or 50% root decay; and 4, total root necrosis, or plant death. The average reaction was calculated by summing the scores of each genotype and dividing them by the total number of evaluated plants. The following genotype classes were: 0, for similar to immune; 0.1-1.0, for highly resistant; 1.1-2.0, for moderately resistant; 2.1-3.0, for susceptible; and 3.1-4.0, for highly susceptible (Sales Júnior et al., 2019SALES JÚNIOR, R.; SENHOR, R.F.; MICHEREFF, S.J.; NEGREIROS, A.M.P. Reaction of melon genotypes to the root´s rot caused by Monosporascus. Revista Caatinga, v.32, p.288-294, 2019. DOI: https://doi.org/10.1590/198321252019v32n130rc.
https://doi.org/10.1590/198321252019v32n...
).

As the severity variable did not have normally distributed residuals, the original values were transformed using the Aligned Rank Transformed (ART) method for non-parametric factorial analyses (Wobbrock et al., 2011WOBBROCK, J.O.; FINDLATER, L.; GERGLE, D.; HIGGINS, J.J. The aligned rank transform for nonparametric factorial analyses using only anova procedures. In: CONFERENCE ON HUMAN FACTORS IN COMPUTING SYSTEMS, 29., 2011, Vancouver. Proceedings. New York: ACM, 2011. p.143-146. CHI 2011. DOI: https://doi.org/10.1145/1978942.1978963.
https://doi.org/10.1145/1978942.1978963...
). Analysis of variance was performed for the severity rank variable and for the root dry matter reduction index (RI(DM)), calculated using the following equation: RI(DM) = (DMu - DMi)/(DMu), where DMu is the dry matter of the uninoculated access; and DMi, the dry matter of the access inoculated with one of the species. The Scott Knott’s test, at 5% probability, was used for grouping the means of the accessions and species. The Spearman correlation coefficient was estimated to assess the association between severity and dry matter index.

The GGE Biplot method, proposed by Yan & Kang (2003)YAN, W.; KANG, M. GGE biplot analysis: a graphical tool for breeders. In: YAN, W.; KANG, M.S. GGE Biplot Analysis: a graphical tool for breeders, geneticists, and agronomists. Boca Raton: CRC Press, 2003. p.229-239. DOI: https://doi.org/10.1201/9781420040371-10.
https://doi.org/10.1201/9781420040371-10...
, assesses the non-additive effects, specifically interactions, between pathogens and plant hosts. The GGE Biplot model considers multiplicative effect, this is, the effect of the genotype and the genotype-species interaction, without separating them, which is described as: Yij - µ - αi - βj = gi1ei1 + gi2ei1 + eij, where Yij is the performance of genotype i in species j; μ is the overall mean of the observations; αi is the main effect of genotype i; βj is the main effect of species j; gi1 and ei1 are the principal scores of genotype i and species j, respectively; gi2 and ei1 are the secondary scores of genotype i and species j, respectively; eij is the residual that cannot be explained by both effects.

All statistical analyses were performed using the R software (R Core Team, 2020R CORE TEAM. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing, 2020.).

Results and Discussion

Althouth the results did not show differences in the effect of melon accessions to the Monosporascus species studied, it was found an effect on the melon accessions response to the infection. This result is due to the diversity of plant materials assessed for severity and the influence of the accession-species interaction, which resulted in varied responses of the accessions to the six inoculated Monosporascus species.

The accessions were grouped according to the average ranks of infection severity of melon accessions to Monosporascus spp. inoculation (Table 1). Two groups were formed with the M. brasiliensis inoculation: the first was composed by the A-16 and 'HBJ' accessions, representing the highest average ranks of severity; and the second one consisted of C-32 and 'Goldex'. Two other groups of accessions were composed by M. caatinguensis and M. nordestinus inoculation, in which the A-16 accession presented the lowest average rank of severity.

Table 1
Scott-Knott’s test to average ranks and original averages of the severity of melon (Cucumis melo) accessions with Monosporascus spp. inoculation(1).

A-16 was the most resistant to the Monosporascus species evaluated. The accessions composed a single group with M. cannonballus, M. mossoroensis, and M. semiaridus inoculation. When inoculated in A-16, the fungal species grouped into two categories (Table 1): the first group comprised M. brasiliensis, M. mossoroensis, and M. semiaridus, showing higher aggressiveness. In 'HBJ', the species were divided into a primary group consisting of the most aggressive ones: M. brasiliensis and M. nordestinus. Subsequently, the remaining species formed the second group. However, when pathogens were inoculated in C-32 and 'Goldex', they formed a single group (Table 1).

In a related study on the interaction of 'Titanium' with Monosporascus spp., symptoms of vine decline were noted, confirming their pathogenicity to melons (Cavalcante et al., 2020CAVALCANTE, A.L.A.; NEGREIROS, A.M.P.; TAVARES, M.B.; BARRETO, E. dos S.; ARMENGOL, J.; SALES JÚNIOR, R. Characterization of Five New Monosporascus Species: Adaptation to Environmental Factors, Pathogenicity to Cucurbits and Sensitivity to Fungicides. Journal of Fungi, v.6, art.169, 2020. DOI: https://doi.org/10.3390/jof6030169.
https://doi.org/10.3390/jof6030169...
). 'Titanium' displayed susceptibility, with disease severity ranging from 1.2 to 1.6%. However, the authors found no significant variations in terms of disease severity and reductions in fresh and dry root weights (Cavalcante et al., 2020CAVALCANTE, A.L.A.; NEGREIROS, A.M.P.; TAVARES, M.B.; BARRETO, E. dos S.; ARMENGOL, J.; SALES JÚNIOR, R. Characterization of Five New Monosporascus Species: Adaptation to Environmental Factors, Pathogenicity to Cucurbits and Sensitivity to Fungicides. Journal of Fungi, v.6, art.169, 2020. DOI: https://doi.org/10.3390/jof6030169.
https://doi.org/10.3390/jof6030169...
).

According Marquez et al. (2023)MARQUEZ, S.A.; CROSBY, K.; PATIL, B.; AVILA, C.; IBRAHIM, A.M.H.; PESSOA, H.; SINGH, J. Hydroxy proline and gamma-aminobutyric acid: markers of susceptibility to vine decline disease caused by the fungus Monosporascus cannonballus in melons (Cucumis melo L.). PeerJ, v.11, e14932, 2023. DOI: https://doi.org/10.7717/peerj.14932.
https://doi.org/10.7717/peerj.14932...
the susceptibility of 'TAM-Uvalde' to M. cannonballus is linked to the production of hydroxyproline and gamma-aminobutyric acid (GABA), serving as susceptibility markers for vine decline. In contrast, the resistant genotype, USDA PI 124104, exhibited elevated levels of the amino acids glycine and glutamine after the inoculation, consequently, these amino acids could potentially serve as resistance markers for vine decline.

All accessions studied in this work presented moderate or total resistance to M. cannonballus (Table 2), which is among the most frequently isolated in melon roots in the Brazilian semiarid region, along with Macrophomina phaseolina (Tassi) Goid. and Fusarium solani (Mart.) Sacc. (Ambrósio et al., 2015AMBRÓSIO, M.M.Q.; DANTAS, A.C.A.; MARTÍNEZ-PEREZ, E.; MEDEIROS, A.C.; NUNES, G.H.S.; PICÓ, M.B. Screening a variable germplasm collection of Cucumis melo L. for seedling resistance to Macrophomina phaseolina. Euphytica, v.206, p.287-300, 2015. DOI: https://doi.org/10.1007/s10681-015-1452-x.
https://doi.org/10.1007/s10681-015-1452-...
), whose literature on resistance is lacking.

Table 2
Melon (Cucumis melo) accession reaction to six species of Monosporascus.

The accessions were classified according to the reaction severity to the six inoculated species (Table 2). A-16 was highly resistant to M. nordestinus, M. caatinguensis, and M. cannonballus, moderately resistant to M. mossoroensis and M. semiaridus, but susceptible to M. brasiliensis. C-32 was susceptible to M. caatinguensis, but moderately resistant to the other species. 'Goldex' was susceptible to M. caatinguensis, M. nordestinus, and M. semiaridus, and moderately resistant to M. brasiliensis, M. cannonballus, and M. mossoroensis. 'HBJ' was susceptible to M. brasiliensis and M. nordestinus and moderately resistant to M. cannonballus, M. caatinguensis, M. mossoroensis, and M. semiaridus.

In one of the first efforts to identify sources of resistance to M. cannonballus, Mertely et al. (1993)MERTELY, J.C.; MARTYN, R.D.; MILLER, M.E.; BRUTON, B.D. An expanded host range for the muskmelon pathogen Monosporascus cannonballus. Plant Disease, v.77, p.667-673, 1993. DOI: https://doi.org/10.1094/pd-77-0667.
https://doi.org/10.1094/pd-77-0667...
concluded that 'HBJ', 'Honey Dew Green Flesh', 'Improved', 'Cruiser', 'Durango', PI 12411, and 'Laredo' were tolerant to this fungal species. However, 'HBJ' was susceptible to M. brasiliensis and M. nordestinus.

In Spain, under field conditions and through greenhouse artificial inoculation, the accession Pat 81 (C. melo ssp. agrestis) presented a high level of tolerance (Iglesias & Nuez, 1998IGLESIAS, A.; NUEZ, F. Caracterización de diversas entradas de melón frente al colapso o muerte súbita. Actas de Horticultura, v.22, p.139-147, 1998.; Iglesias et al., 2000IGLESIAS, A.; PICÓ, B.; NUEZ, F. A temporal genetic analysis of disease resistance genes: resistance to melon vine decline derived from Cucumis melo var. agrestis. Plant Breeding, v.119, p.329-334, 2000. DOI: https://doi.org/10.1046/j.1439-0523.2000.00507.x.
https://doi.org/10.1046/j.1439-0523.2000...
), playing an important role in a breeding program involving backcrosses and leading to the development of resistant lines in the piel de sapo group (Fita et al., 2009FITA, A.; PICÓ, B.; DIAS, R.C.S.; NUEZ, F. 'Piel de Sapo' breeding lines tolerant to melon vine decline. HortScience, v.44, p.1458-1460, 2009. DOI: https://doi.org/10.21273/HORTSCI.44.5.1458.
https://doi.org/10.21273/HORTSCI.44.5.14...
). The accession C-32, derived from Pat 81, presented susceptibility to M. caatinguensis and moderate resistance to the other species. Therefore, C-32 can be a source of resistance; however, for the first time, it presented susceptibility to a Monosporascus species.

'Goldex' was susceptible to M. caatinguensis, M. nordestinus, and M. semiaridus (Table 2), presented high values of root dry matter reduction index (Table 3), and is highly susceptible to powdery mildew [Podosphaera xanthii (Castagne) U. Braun & Shishkoff] and leafminer (Liriomyza sativae Blanchard). However, it is still the preferred one due to its high quality and long shelf life, which turns out to be the melon with the largest cultivated area in the Brazilian semiarid region, with approximately 22,000 ha per year in the past 20 years. Therefore, despite the potential fragility of the hybrid, a strategy is to obtain yellow melon cultivars resistant to the main pathogens with a 'Goldex' background.

Table 3
Root matter reduction index of melon (Cucumis melo) accession inoculated with Monosporascus.(1)

The dry matter reduction index of the roots showed no significant effect in either accessions or species; however, it was observed a notable effect of the interaction among factors (Table 3). In the case of M. brasiliensis, accessions formed two distinct groups: A-16 constituting the first group and the remaining accessions comprising the second. When subjected to M. cannonballus infection, accessions were again divided into two groups based on the extent of root dry matter reduction. 'Goldex' was in the first group, exhibiting the greatest reduction, while the other accessions formed the second group. With M. mossoroensis inoculation, A-16 had the lowest reduction, segregating it from the other accessions with higher averages, which formed another group. For M. nordestinus, accessions were grouped into two, with the highest averages being performed by 'Goldex' and 'HBJ', similarly occurring for M. caatinguensis and M. semiaridus.

Monosporascus brasiliensis species caused a reduction of more than 50% in the A-16 root dry matter, so it was allocated in a separate group (Table 3). The species were gathered in the same group when inoculated the accession C-32. The M. cannonballus, M. brasiliensis, M. mossoroensis, and M. nordestinus species were gathered in the same group, because they were more virulent with 'Goldex'. The species were combined into two groups when inoculated 'HBJ', in which the first group was formed by M. nordestinus, more virulent, while the second group was formed by the other species.

A-16, which had the lowest root dry matter reduction index (Table 3), has fruits with high mesocarp firmness, high titratable acidity, low content of soluble solids (Dantas et al., 2015DANTAS, A.C. de A.; HOLANDA, I.S.A.; ESTERAS, C.; NUNES, G.H. de S.; PICÓ, M.B. Diversity of Melon Accessions from Northeastern Brazil and Their Relationships with Germplasms of Diverse Origins. Journal of the American Society for Horticultural Science, v.140, p.504-517, 2015. DOI: https://doi.org/10.21273/jashs.140.5.504.
https://doi.org/10.21273/jashs.140.5.504...
), and is resistant to Myrothecium roridum Tode (Nascimento et al., 2012NASCIMENTO, Í.J.B.; NUNES, G.H.S.; SALES JÚNIOR, R.; SILVA, K.J.P.; GUIMARÃES, I.M.; MICHEREFF, S.J. Reaction of melon accessions to crater rot and resistance inheritance. Horticultura Brasileira, v.30, p.459-465, 2012. DOI: https://doi.org/10.1590/s010205362012000300017.
https://doi.org/10.1590/s010205362012000...
). It belongs to the acidulus group, whose varieties are cultivated in India and Sri Lanka. Several genotypes within this group, such as PI 313970 (90625), PI 164323, PI 164723, and Kekiri, present resistance to various viruses and diseases, such as powdery mildew and downy mildew [Pseudoperonospora cubensis (Berk. & M.A. Curtis) Rostovzev], as well as insects, such as Aphis gossypii Glover (Dhillon et al., 2011DHILLON, N.P.S.; MONFORTE, A.J.; PITRAT, M.; PANDEY, S.; SINGH, P.K.; REITSMA, K.R.; GARCIA-MAS, J.; SHARMA, A.; MCCREIGHT, J.D. Melon landraces of India: contributions and importance. In: JANICK, J. (Ed.). Plant Breeding Reviews. Hoboken: John Wiley & Sons, 2011. v.35, p.85-150. DOI: https://doi.org/10.1002/9781118100509.ch3.
https://doi.org/10.1002/9781118100509.ch...
; Pitrat, 2016PITRAT, M. Melon genetic resources: phenotypic diversity and horticultural taxonomy. In: GRUMET, R.; KATZIR, N.; GARCIA-MAS, J. (Ed.). Genetics and Genomics of Cucurbitaceae. Cham: Springer, 2016. p.25-60. (Plant genetics and genomics: crops and models, 20). DOI: https://doi.org/10.1007/7397_2016_10.
https://doi.org/10.1007/7397_2016_10...
).

Infection caused by Monosporascus spp. is contingent upon imbalanced soil conditions and exacerbated by elevated temperatures, such as 35°C in the greenhouse. Furthermore, in the field, intensive melon cultivation system results in the onset of vine decline, and the absence of appropriate crop rotation practices allows these fungi to extend beyond their natural habitat, like spontaneous plant roots such as those of B. diffusa and T. portulacastrum (Negreiros et al., 2019NEGREIROS, A.M.P.; SALES JÚNIOR, R.; RODRIGUES, A.P.M.S.; LEÓN, M.; ARMENGOL, J. Prevalent weeds collected from cucurbit fields in Northeastern Brazil reveal new species diversity in the genus Monosporascus. Annals of Applied Biology, v.174, p.349-363, 2019. DOI: https://doi.org/10.1111/aab.12493.
https://doi.org/10.1111/aab.12493...
), causing damage to cucurbit crops.

In the biplot graph (Figure 1), the two axes together explained 97.25% of the total variation in the accession-species interaction, and the polygon formed was composed of four vertices. In each vertex, there is an inoculated accession, which has the highest average rank in its respective sector, being, therefore, the one with the highest severity. The first vertex shows that the species M. nordestinus, M. brasiliensis, and M. semiaridus were more virulent to 'HBJ' in relation to the others. The second vertex indicates that 'Goldex' has the highest average rank in relation to M. caatinguensis. The third vertex presents that C-32 was associated with the highest average rank (highest severity) when inoculated with M. cannonballus and M. mossoroensis. The fourth vertex shows that A-16 did not interact with the species and showed less severity, consequently, it presented higher performance.

Figure 1
GGE biplot showing: A, the distribution of the melon (Cucumis melo) genotypes (on the vertices) inoculated with six species of Monosporascus spp.; and B, the distribution of the species of the genus Monosporascus (on the vertices) inoculated in four genotypes of melon ('HBJ', 'Goldex', A-16, and C-32). MBRA, Monosporascus brasiliensis; MCAN, Monosporascus cannonballus; MCAT, Monosporascus caatinguensis; MMOS, Monosporascus mossoroensis; MNOR, Monosporascus nordestinus; and MSAR, Monosporascus semiaridus.

The Biplot modeling also can be set in the opposite direction, i.e., setting the species in the vertices. Therefore, the six species were set into five vertices of the polygon of the Biplot graph (Figure 1). In the counterclockwise direction: the species M. brasiliensis, in the second vertex, interacted more with A-16; M. nordestinus, in the third vertex, interacted with 'Goldex' and 'HBJ'; and M. caatinguensis species, located in the fourth vertex, interacted only with C-32. The latter species presented greater virulence because it was more to the right-hand side on the x-axis, i.e., it can be seen as the species that best interacted with C-32, due to the proximity in the graph indicating good association between pathogen and accession. Constrastingly, M. brasiliensis had less virulence because it was more to the left-hand side on the x-axis, followed by M. semiaridus. The other species showed higher severity, due to the greater distance from the origin (o) on the y-axis. The length of the vector can also reflect high disease incidence and good level of discriminative ability of the varietal groups in regard of the pathogens.

The representation of species at various distances from the origin along the y-axis highlights their diverse associations with genotypes, demonstrating their virulence within the experimental environment. This biplot analysis avoids redundancy and enhances understanding of complex interactions. In contrast to the behavior of varietal groups, the absence of M. semiaridus in a distinct vertex of the biplot (Figure 1) can be attributed to intricate interactions between species and accessions in the experimental context (Yan & Falk, 2002YAN, W.; FALK, D.E. Biplot analysis of host-by-pathogen data. Plant Disease, v.86, p.1396-1401, 2002. DOI: https://doi.org/10.1094/PDIS.2002.86.12.1396.
https://doi.org/10.1094/PDIS.2002.86.12....
).

To date, there are no known reports on the virulence of other species of Monosporascus in melon varietal groups, being known only vine decline caused by the species M. cannonballus and M. eutypoides worldwide (Castro et al., 2020CASTRO, G.; PERPIÑÁ, G.; ESTERAS, C.; ARMENGOL, J.; PICÓ, B.; PÉREZ-DE-CASTRO, A. Resistance in melon to Monosporascus cannonballus and M. eutypoides: Fungal pathogens associated with Monosporascus root rot and vine decline. Annals of Applied Biology, v.177, p.101-111, 2020. DOI: https://doi.org/10.1111/aab.12590.
https://doi.org/10.1111/aab.12590...
). Despite this, five novel species of Monosporascus isolated from weed roots of B. diffusa and T. portulacastrum, usually found in melon production fields in the Northeastern region of Brazil, were identified (Negreiros et al., 2019NEGREIROS, A.M.P.; SALES JÚNIOR, R.; RODRIGUES, A.P.M.S.; LEÓN, M.; ARMENGOL, J. Prevalent weeds collected from cucurbit fields in Northeastern Brazil reveal new species diversity in the genus Monosporascus. Annals of Applied Biology, v.174, p.349-363, 2019. DOI: https://doi.org/10.1111/aab.12493.
https://doi.org/10.1111/aab.12493...
).

Therefore, the present work is the first report of the pathogenicity and virulence of the species M. brasiliensis, M. caatinguensis, M. mossoroensis, M. nordestinus, and M. semiaridus in melon varietal groups, as well as observing that the species have a different behavior according to each accession. It also found that the species M. cannonballus, notoriously the agent of vine decline worldwide (Sarpeleh, 2008SARPELEH, A. The role of Monosporascus cannonballus in melon collapse in Iran. Australasian Plant Disease Notes, v.3, p.162-164, 2008. DOI: https://doi.org/10.1007/BF03211279.
https://doi.org/10.1007/BF03211279...
; Al-Mawaali et al., 2013AL-MAWAALI, Q.S.; AL-SADI, A.M.; AL-SAID, F.A.; DEADMAN, M.L. Etiology, development and reaction of muskmelon to vine decline under arid conditions of Oman. Phytopathologia Mediterranea, v.52, p.457-465, 2013.; Yan et al., 2016YAN, L.Y.; ZANG, Q.Y.; HUANG, Y.P.; WANG, Y.H. First report of root rot and vine decline of melon caused by Monosporascus cannonballus in Eastern Mainland China. Plant Disease, v.100, p.651, 2016. DOI: https://doi.org/10.1094/PDIS-06-15-0655-PDN.
https://doi.org/10.1094/PDIS-06-15-0655-...
; Markakis et al., 2018MARKAKIS, E.A.; TRANTAS, E.A.; LAGOGIANNI, C.S.; MPALANTINAKI, E.; PAGOULATOU, M.; VERVERIDIS, F.; GOUMAS, D.E. First report of root rot and vine decline of melon caused by Monosporascus cannonballus in Greece. Plant Disease, v.102, p.1036, 2018. DOI: https://doi.org/10.1094/PDIS-10-17-1568-PDN.
https://doi.org/10.1094/PDIS-10-17-1568-...
; Sales Júnior et al., 2019SALES JÚNIOR, R.; SENHOR, R.F.; MICHEREFF, S.J.; NEGREIROS, A.M.P. Reaction of melon genotypes to the root´s rot caused by Monosporascus. Revista Caatinga, v.32, p.288-294, 2019. DOI: https://doi.org/10.1590/198321252019v32n130rc.
https://doi.org/10.1590/198321252019v32n...
) and the novel species M. mossoroensis were the least virulent, since none of the accessions was classified as susceptible to both species. Particularly, A-16 was highly resistant to M. cannonballus, and of moderate or high resistance when inoculated with each of these species. Nevertheless, the other species of Monosporascus caused a susceptibility reaction in, at least, one of the accessions (Table 2).

An important aspect for breeding programs is that the tolerance in melon to M. cannonballus is strictly related to the root system. In the present work, only the root dry matter reduction index of the genotypes was estimated. There was a positive and significant association between the severity and the root dry matter reduction index, that is, the greater the severity, the lower the dry matter of the roots of the inoculated plants when compared with the non-inoculated plants (Figure 2). Crosby et al. (2000)CROSBY, K.; WOLFF, D.; MILLER, M. Comparisons of Root Morphology in Susceptible and Tolerant Melon Cultivars before and after Infection by Monosporascus cannonballus. HortScience, v.35, p.681-683, 2000. DOI: https://doi.org/10.21273/hortsci.35.4.681.
https://doi.org/10.21273/hortsci.35.4.68...
observed that resistant cultivars have higher averages of total root length, root diameter, number of root branches, number of thin roots (0.0-0.5 mm), and number of small roots (0.5-1.0 mm) compared with susceptible cultivars. The tolerance of the C-32 may be explained by the high vigor and pronounced branching of its root system. This accession has high root mass, even infected, when compared to the susceptible 'Pioñet' (Dias et al., 2002DIAS, R. de C.S.; PICÓ, B.; HERRAIZ, J.; ESPINÓS, A.; NUEZ, F. Modifying root structure of cultivated muskmelon to improve vine decline resistance. HortScience, v.37, p.1092-1097, 2002. DOI: https://doi.org/10.21273/hortsci.37.7.1092.
https://doi.org/10.21273/hortsci.37.7.10...
).

Figure 2
Estimations of the coefficient of Spearman’s correlation between the severity and the root matter reduction index among each melon (Cucumis melo) accession (A) and species of Monosporascus spp. (B). 'HBJ', 'Hales Best Jumbo'; MBRA, Monosporascus brasiliensis; MCAN, Monosporascus cannonballus; MCAT, Monosporascus caatinguensis; MMOS, Monosporascus mossoroensis; MNOR, Monosporascus nordestinus; and MSAR, Monosporascus semiaridus.

Several methods can be developed to evaluate the virulence of pathogens, by observing the severity of attacks on plant tissues, such as damage to the hypocotyl, in primary and secondary roots and reduction of leaf area (Bruton et al., 2000BRUTON, B.D.; GARCIA-JIMENEZ, J.; ARMENGOL, J.; POPHAM, T.W. Assessment of Virulence of Acremonium cucurbitacearum and Monosporascus cannonballus on Cucumis melo. Plant Disease, v.84, p.907-913, 2000. DOI: https://doi.org/10.1094/PDIS.2000.84.8.907.
https://doi.org/10.1094/PDIS.2000.84.8.9...
). Therefore, several inoculation methods can be adopted, such as inoculating the soil with agar colonized with the fungus (Tsay & Tung, 1995TSAY, J.; TUNG, B. The occurrence of Monosporascus root rot/vine decline of muskmelon in Taiwan. Plant Pathology Bulletin, v.4, p.25-29, 1995.; Martyn & Miller, 1996MARTYN, R.D.; MILLER, M.E. Monosporascus root rot and vine decline: an emerging disease of melons worldwide. Plant Disease, v.80, p.716-725, 1996. DOI: https://doi.org/10.1094/pd-80-0716.
https://doi.org/10.1094/pd-80-0716...
; Pivonia et al., 1997PIVONIA, S.; COHEN, R.; KAFKAFI, U.; BEN ZE’EV, I.S.; KATAN, J. Sudden wilt of melons in southern Israel: fungal agents and relationship with plant development. Plant Disease, v.81, p.1264-1268, 1997. DOI: https://doi.org/10.1094/pdis.1997.81.11.1264.
https://doi.org/10.1094/pdis.1997.81.11....
), oat husks mixed with sand in pots (Mertely et al., 1993MERTELY, J.C.; MARTYN, R.D.; MILLER, M.E.; BRUTON, B.D. An expanded host range for the muskmelon pathogen Monosporascus cannonballus. Plant Disease, v.77, p.667-673, 1993. DOI: https://doi.org/10.1094/pd-77-0667.
https://doi.org/10.1094/pd-77-0667...
; Karlatti et al., 1997KARLATTI, R.S.; ABDEEN, F.M.; AL-FEHAID, M.S. First report of Monosporascus cannonballus on melons in Saudi Arabia. Plant Disease, v.81, p.1215, 1997. DOI: https://doi.org/10.1094/PDIS.1997.81.10.1215B.
https://doi.org/10.1094/PDIS.1997.81.10....
; Pivonia et al., 1997PIVONIA, S.; COHEN, R.; KAFKAFI, U.; BEN ZE’EV, I.S.; KATAN, J. Sudden wilt of melons in southern Israel: fungal agents and relationship with plant development. Plant Disease, v.81, p.1264-1268, 1997. DOI: https://doi.org/10.1094/pdis.1997.81.11.1264.
https://doi.org/10.1094/pdis.1997.81.11....
), which proved the effectiveness of the different inoculation methods. In the present study, it was used a mycelial suspension, since some species of Monosporascus could not be induced to sporulation (Negreiros et al., 2019NEGREIROS, A.M.P.; SALES JÚNIOR, R.; RODRIGUES, A.P.M.S.; LEÓN, M.; ARMENGOL, J. Prevalent weeds collected from cucurbit fields in Northeastern Brazil reveal new species diversity in the genus Monosporascus. Annals of Applied Biology, v.174, p.349-363, 2019. DOI: https://doi.org/10.1111/aab.12493.
https://doi.org/10.1111/aab.12493...
).

Significant values were found in practically all accessions and species by means of Spearman’s correlations coefficients, but there were some exceptions, such as C-32 (Figure 2), which may indicate that the increase in severity does not cause a significant reduction in dry matter. The positive sign indicates the two variables grow in the same direction, this is, they are directly proportional. When the severity increases, there is a reduction in the dry matter of the plant. The correlation, considering all the data, also followed the same fashion, positive and significant value (r=0.58*).

This study confirmed the susceptibility of the melon groups cantalupensis, inodorus, acidulous, and conomon to five new Monosporascus spp. Given the natural presence of these species in melon-producing regions, managing melon vine decline requires awareness of these new species, thus, it is important to produce cultivars resistant to vine decline.

Future breeding strategies should aim at enhancing resistance against pathogens so future research should focus on developing yellow melon cultivars resistant to major pathogens, particularly to specific Monosporascus species. Continued investigation into the host-pathogen dynamics will contribute to the development of resilient melon varieties for sustainable cultivation.

Conclusions

  1. The A-16 melon (Cucumis melo) accession shows higher resistance to Monosporascus nordestinus, Monosporascus caatinguensis, and Monosporascus cannonballus, whereas 'Goldex' presents susceptibility to M. caatinguensis, M. nordestinus, and Monosporascus semiaridus.

  2. The species Monosporascus brasiliensis, M. caatinguensis, Monosporascus mossoroensis, M. nordestinus, and M. semiaridus present varying levels of pathogenicity and diferent levels of infection severity, with M. semiaridus having the highest severity, and M. cannonballus the lowest.

Acknowledgments

To Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), for financing, in part, this study (Finance Code 001); and to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), for support.

References

  • AL-MAWAALI, Q.S.; AL-SADI, A.M.; AL-SAID, F.A.; DEADMAN, M.L. Etiology, development and reaction of muskmelon to vine decline under arid conditions of Oman. Phytopathologia Mediterranea, v.52, p.457-465, 2013.
  • AMBRÓSIO, M.M.Q.; DANTAS, A.C.A.; MARTÍNEZ-PEREZ, E.; MEDEIROS, A.C.; NUNES, G.H.S.; PICÓ, M.B. Screening a variable germplasm collection of Cucumis melo L. for seedling resistance to Macrophomina phaseolina Euphytica, v.206, p.287-300, 2015. DOI: https://doi.org/10.1007/s10681-015-1452-x
    » https://doi.org/10.1007/s10681-015-1452-x
  • ARMENGOL, J.; SALES, R.; GARCÍA-JIMÉNEZ, J. Effects of soil moisture and water on survival of Acremonium cucurbitacearum Journal of Phytopathology, v.147, p.737-741, 1999. DOI: https://doi.org/10.1046/j.1439-0434.1999.00448.x
    » https://doi.org/10.1046/j.1439-0434.1999.00448.x
  • BEN SALEM, I.; ARMENGOL, J.; BERBEGEL, M.; BOUGHALLEB-M’HAMDI, N. Development of a Screening Test for Resistance of Cucurbits and Cucurbita Hybrid Rootstocks to Monosporascus cannonballus Tunisian Journal of Plant Protection, v.10, p.23-33, 2015.
  • BRUTON, B.D.; GARCIA-JIMENEZ, J.; ARMENGOL, J.; POPHAM, T.W. Assessment of Virulence of Acremonium cucurbitacearum and Monosporascus cannonballus on Cucumis melo Plant Disease, v.84, p.907-913, 2000. DOI: https://doi.org/10.1094/PDIS.2000.84.8.907
    » https://doi.org/10.1094/PDIS.2000.84.8.907
  • CASTRO, G.; PERPIÑÁ, G.; ESTERAS, C.; ARMENGOL, J.; PICÓ, B.; PÉREZ-DE-CASTRO, A. Resistance in melon to Monosporascus cannonballus and M. eutypoides: Fungal pathogens associated with Monosporascus root rot and vine decline. Annals of Applied Biology, v.177, p.101-111, 2020. DOI: https://doi.org/10.1111/aab.12590
    » https://doi.org/10.1111/aab.12590
  • CAVALCANTE, A.L.A.; NEGREIROS, A.M.P.; TAVARES, M.B.; BARRETO, E. dos S.; ARMENGOL, J.; SALES JÚNIOR, R. Characterization of Five New Monosporascus Species: Adaptation to Environmental Factors, Pathogenicity to Cucurbits and Sensitivity to Fungicides. Journal of Fungi, v.6, art.169, 2020. DOI: https://doi.org/10.3390/jof6030169
    » https://doi.org/10.3390/jof6030169
  • CHILOSI, G.; REDA, R.; ALEANDRI, M.P.; CAMELE, I.; ALTIERI, L.; MONTUSCHI, C.; LANGUASCO, L.; ROSSI, V.; AGOSTEO, G.E.; MACRÌ, C.; CARLUCCI, A.; LOPS, F.; MUCCI, M.; RAIMONDO, M.L.; FRISULLO, S. Fungi associated with root rot and collapse of melon in Italy. EPPO Bulletin, v.38, p.147-154, 2008. DOI: https://doi.org/10.1111/j.1365-2338.2008.01200.x
    » https://doi.org/10.1111/j.1365-2338.2008.01200.x
  • CLUCK, T.W.; BILES, C.L.; DUGGAN, M.; JACKSON, T.; CARSON, K.; ARMENGOL, J.; GARCIA-JIMENEZ, J.; BRUTON, B.D. Association of dsRNA to Down-Regulation of Perithecial Synthesis in Monosporascus cannonballus The Open Mycology Journal, v.3, p.9-19, 2009. DOI: https://doi.org/10.2174/1874437000903010009
    » https://doi.org/10.2174/1874437000903010009
  • CROSBY, K.; WOLFF, D.; MILLER, M. Comparisons of Root Morphology in Susceptible and Tolerant Melon Cultivars before and after Infection by Monosporascus cannonballus HortScience, v.35, p.681-683, 2000. DOI: https://doi.org/10.21273/hortsci.35.4.681
    » https://doi.org/10.21273/hortsci.35.4.681
  • DANTAS, A.C. de A.; HOLANDA, I.S.A.; ESTERAS, C.; NUNES, G.H. de S.; PICÓ, M.B. Diversity of Melon Accessions from Northeastern Brazil and Their Relationships with Germplasms of Diverse Origins. Journal of the American Society for Horticultural Science, v.140, p.504-517, 2015. DOI: https://doi.org/10.21273/jashs.140.5.504
    » https://doi.org/10.21273/jashs.140.5.504
  • DHILLON, N.P.S.; MONFORTE, A.J.; PITRAT, M.; PANDEY, S.; SINGH, P.K.; REITSMA, K.R.; GARCIA-MAS, J.; SHARMA, A.; MCCREIGHT, J.D. Melon landraces of India: contributions and importance. In: JANICK, J. (Ed.). Plant Breeding Reviews Hoboken: John Wiley & Sons, 2011. v.35, p.85-150. DOI: https://doi.org/10.1002/9781118100509.ch3
    » https://doi.org/10.1002/9781118100509.ch3
  • DIAS, R. de C.S.; PICÓ, B.; HERRAIZ, J.; ESPINÓS, A.; NUEZ, F. Modifying root structure of cultivated muskmelon to improve vine decline resistance. HortScience, v.37, p.1092-1097, 2002. DOI: https://doi.org/10.21273/hortsci.37.7.1092
    » https://doi.org/10.21273/hortsci.37.7.1092
  • FITA, A.; PICÓ, B.; DIAS, R.C.S.; NUEZ, F. 'Piel de Sapo' breeding lines tolerant to melon vine decline. HortScience, v.44, p.1458-1460, 2009. DOI: https://doi.org/10.21273/HORTSCI.44.5.1458
    » https://doi.org/10.21273/HORTSCI.44.5.1458
  • IGLESIAS, A.; NUEZ, F. Caracterización de diversas entradas de melón frente al colapso o muerte súbita. Actas de Horticultura, v.22, p.139-147, 1998.
  • IGLESIAS, A.; PICÓ, B.; NUEZ, F. A temporal genetic analysis of disease resistance genes: resistance to melon vine decline derived from Cucumis melo var. agrestis Plant Breeding, v.119, p.329-334, 2000. DOI: https://doi.org/10.1046/j.1439-0523.2000.00507.x
    » https://doi.org/10.1046/j.1439-0523.2000.00507.x
  • KARLATTI, R.S.; ABDEEN, F.M.; AL-FEHAID, M.S. First report of Monosporascus cannonballus on melons in Saudi Arabia. Plant Disease, v.81, p.1215, 1997. DOI: https://doi.org/10.1094/PDIS.1997.81.10.1215B
    » https://doi.org/10.1094/PDIS.1997.81.10.1215B
  • MARKAKIS, E.A.; TRANTAS, E.A.; LAGOGIANNI, C.S.; MPALANTINAKI, E.; PAGOULATOU, M.; VERVERIDIS, F.; GOUMAS, D.E. First report of root rot and vine decline of melon caused by Monosporascus cannonballus in Greece. Plant Disease, v.102, p.1036, 2018. DOI: https://doi.org/10.1094/PDIS-10-17-1568-PDN
    » https://doi.org/10.1094/PDIS-10-17-1568-PDN
  • MARQUEZ, S.A.; CROSBY, K.; PATIL, B.; AVILA, C.; IBRAHIM, A.M.H.; PESSOA, H.; SINGH, J. Hydroxy proline and gamma-aminobutyric acid: markers of susceptibility to vine decline disease caused by the fungus Monosporascus cannonballus in melons (Cucumis melo L.). PeerJ, v.11, e14932, 2023. DOI: https://doi.org/10.7717/peerj.14932
    » https://doi.org/10.7717/peerj.14932
  • MARTYN, R.D.; MILLER, M.E. Monosporascus root rot and vine decline: an emerging disease of melons worldwide. Plant Disease, v.80, p.716-725, 1996. DOI: https://doi.org/10.1094/pd-80-0716
    » https://doi.org/10.1094/pd-80-0716
  • MERTELY, J.C.; MARTYN, R.D.; MILLER, M.E.; BRUTON, B.D. An expanded host range for the muskmelon pathogen Monosporascus cannonballus Plant Disease, v.77, p.667-673, 1993. DOI: https://doi.org/10.1094/pd-77-0667
    » https://doi.org/10.1094/pd-77-0667
  • NASCIMENTO, Í.J.B.; NUNES, G.H.S.; SALES JÚNIOR, R.; SILVA, K.J.P.; GUIMARÃES, I.M.; MICHEREFF, S.J. Reaction of melon accessions to crater rot and resistance inheritance. Horticultura Brasileira, v.30, p.459-465, 2012. DOI: https://doi.org/10.1590/s010205362012000300017
    » https://doi.org/10.1590/s010205362012000300017
  • NEGREIROS, A.M.P.; SALES JÚNIOR, R.; RODRIGUES, A.P.M.S.; LEÓN, M.; ARMENGOL, J. Prevalent weeds collected from cucurbit fields in Northeastern Brazil reveal new species diversity in the genus Monosporascus Annals of Applied Biology, v.174, p.349-363, 2019. DOI: https://doi.org/10.1111/aab.12493
    » https://doi.org/10.1111/aab.12493
  • PICÓ, B.; ROIG, C.; FITA, A.; NUEZ, F. Quantitative detection of Monosporascus cannonballus in infected melon roots using real-time PCR. European Journal of Plant Pathology, v.120, p.147-156, 2008. DOI: https://doi.org/10.1007/s10658-007-9203-z
    » https://doi.org/10.1007/s10658-007-9203-z
  • PITRAT, M. Melon genetic resources: phenotypic diversity and horticultural taxonomy. In: GRUMET, R.; KATZIR, N.; GARCIA-MAS, J. (Ed.). Genetics and Genomics of Cucurbitaceae Cham: Springer, 2016. p.25-60. (Plant genetics and genomics: crops and models, 20). DOI: https://doi.org/10.1007/7397_2016_10
    » https://doi.org/10.1007/7397_2016_10
  • PIVONIA, S.; COHEN, R.; KAFKAFI, U.; BEN ZE’EV, I.S.; KATAN, J. Sudden wilt of melons in southern Israel: fungal agents and relationship with plant development. Plant Disease, v.81, p.1264-1268, 1997. DOI: https://doi.org/10.1094/pdis.1997.81.11.1264
    » https://doi.org/10.1094/pdis.1997.81.11.1264
  • R CORE TEAM. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing, 2020.
  • SALES JR, R.; OLIVEIRA, O.F. de; SENHOR, R.F.; ALVES, M.Z. Monosporascus cannonballus agente causal do colapso em plantas de melão no Rio Grande do Norte, Brasil. Fitopatologia Brasileira, v.28, p.567, 2003. DOI: https://doi.org/10.1590/S0100-41582003000500020
    » https://doi.org/10.1590/S0100-41582003000500020
  • SALES JR, R.; SANTANA, C.V.S.; NOGUEIRA, D.R.S.; SILVA, K.J.P.; MICHEREFF, S.J.; ABAD-CAMPOS, P.; GARCÍA-JIMÉNEZ, J.; ARMENGOL, J. First Report of Monosporascus cannonballus on Watermelon in Brazil. Plant Disease, v.94, p.278, 2010. DOI: https://doi.org/10.1094/PDIS-94-2-0278B
    » https://doi.org/10.1094/PDIS-94-2-0278B
  • SALES JÚNIOR, R.; SENHOR, R.F.; MICHEREFF, S.J.; NEGREIROS, A.M.P. Reaction of melon genotypes to the root´s rot caused by Monosporascus Revista Caatinga, v.32, p.288-294, 2019. DOI: https://doi.org/10.1590/198321252019v32n130rc
    » https://doi.org/10.1590/198321252019v32n130rc
  • SARPELEH, A. The role of Monosporascus cannonballus in melon collapse in Iran. Australasian Plant Disease Notes, v.3, p.162-164, 2008. DOI: https://doi.org/10.1007/BF03211279
    » https://doi.org/10.1007/BF03211279
  • TAVARES, M.B.; NEGREIROS, A.M.P.; CAVALCANTE, A.L.A.; OLIVEIRA, S.H.F. de; ARMENGOL, J.; SALES JÚNIOR, R. Reaction of non-cucurbitacea to Monosporascus spp. Revista Ciência Agronômica, v.54, e20218323, 2023. DOI: https://doi.org/10.5935/1806-6690.20230013
    » https://doi.org/10.5935/1806-6690.20230013
  • TSAY, J.; TUNG, B. The occurrence of Monosporascus root rot/vine decline of muskmelon in Taiwan. Plant Pathology Bulletin, v.4, p.25-29, 1995.
  • WOBBROCK, J.O.; FINDLATER, L.; GERGLE, D.; HIGGINS, J.J. The aligned rank transform for nonparametric factorial analyses using only anova procedures. In: CONFERENCE ON HUMAN FACTORS IN COMPUTING SYSTEMS, 29., 2011, Vancouver. Proceedings New York: ACM, 2011. p.143-146. CHI 2011. DOI: https://doi.org/10.1145/1978942.1978963
    » https://doi.org/10.1145/1978942.1978963
  • YAN, L.Y.; ZANG, Q.Y.; HUANG, Y.P.; WANG, Y.H. First report of root rot and vine decline of melon caused by Monosporascus cannonballus in Eastern Mainland China. Plant Disease, v.100, p.651, 2016. DOI: https://doi.org/10.1094/PDIS-06-15-0655-PDN
    » https://doi.org/10.1094/PDIS-06-15-0655-PDN
  • YAN, W.; FALK, D.E. Biplot analysis of host-by-pathogen data. Plant Disease, v.86, p.1396-1401, 2002. DOI: https://doi.org/10.1094/PDIS.2002.86.12.1396
    » https://doi.org/10.1094/PDIS.2002.86.12.1396
  • YAN, W.; KANG, M. GGE biplot analysis: a graphical tool for breeders. In: YAN, W.; KANG, M.S. GGE Biplot Analysis: a graphical tool for breeders, geneticists, and agronomists. Boca Raton: CRC Press, 2003. p.229-239. DOI: https://doi.org/10.1201/9781420040371-10
    » https://doi.org/10.1201/9781420040371-10

Publication Dates

  • Publication in this collection
    13 Sept 2024
  • Date of issue
    2024

History

  • Received
    08 June 2023
  • Accepted
    12 June 2024
Embrapa Secretaria de Pesquisa e Desenvolvimento; Pesquisa Agropecuária Brasileira Caixa Postal 040315, 70770-901 Brasília DF Brazil, Tel. +55 61 3448-1813, Fax +55 61 3340-5483 - Brasília - DF - Brazil
E-mail: pab@embrapa.br