Host status of stinking passion flower and yellow passion fruit to Rotylenchulus reniformis, Meloidogyne javanica and Pratylenchus brachyurus

Reação de maracujazeiro-de-cheiro e maracujazeiro-amarelo a Rotylenchulus reniformis, Meloidogyne javanica e Pratylenchus brachyurus

Abstract

Stinking passion flower (Passiflora foetida L.) is an herbaceous vine used due its medicinal properties. It could be an option to be used as a rootstock for sour passion fruit (P. edulis). This interest was especially motivated by its resistance to Fusarium oxysporum f. sp. passifloraeand F. solani, two soilborne pathogens that severely limit the sour passion fruit cultivation in Brazil. Phytonematodes are other important soil pathogens to most crops, including Passiflora species, and they often interact synergistically with pathogenic Fusarium spp. strains. However, the host status of stinking passion flower to phytonematodes was not assessed yet. Therefore, three pot experiments were carried out in order to assess the reproduction of Rotylenchulus reniformis, Meloidogyne javanica and on Pratylenchus brachyurusstinking passion flower and sour passion fruit. Both P. foetida and P. edulis were susceptible to R. reniformis, but immune (or highly resistant) to both M. javanica and P. brachyurus. Based on previous and the present work, R. reniformis stands out and could be pointed as the most important species to species of Passiflora.

Index terms
lesion nematode; Passiflora edulis; Passiflora foetida; reniform nematode; root-knot nematode

Resumo

O maracujá-de-cheiro (Passiflora foetida L.) é uma trepadeira herbácea com propriedades medicinais. Pode ser uma opção a ser utilizada como porta-enxerto para o maracujazeiro-azedo (P. edulis Sims). O interesse foi especialmente motivado pela sua resistência a Fusarium oxysporum f. sp. passiflorae e F. solani, dois fitopatógenos de solo que limitam severamente o cultivo do maracujazeiro-azedo no Brasil. Os fitonematoides são outros importantes patógenos de solo para a maioria das culturas, incluindo espécies de Passiflora, e muitas vezes interagem sinergicamente com isolados patogênicos de Fusarium spp.Entretanto, a reação de P. foetida aos nematoides fitoparasitas ainda não foi avaliada. Dessa forma, três experimentos em vasos foram realizados em casa de vegetação, com o objetivo de avaliar a reprodução de Rotylenchulus reniformis, Meloidogyne javanica e Pratylenchus brachyurus em maracujazeiro-de-cheiro e maracujazeiro-azedo. Tanto P. foetida quanto P. edulis foram suscetíveis a R. reniformis, mas imunes (ou altamente resistentes) a M. javanica e P. brachyurus. Com base em trabalhos anteriores e no presente, R. reniformis se destaca e pode ser apontada como a espécie mais importante para as espécies de Passiflora.

Termos para indexação
fusariose; nematoide-das-lesões-radiculares; Passiflora edulis; Passiflora foetida; nematoide-reniforme; nematoide-das-galhas

Introduction

Passion fruits plants belong to the genus Passiflora L., which groups about 500 species mostly distributed in tropical and subtropical regions. Brazil has about 150 native species with some of them exploited in agriculture. Passiflora edulis Sims is the main commercial species in Brazil, especially the sour passionfruit (Passiflora edulis). It is widely appreciated due to its flavor, aroma and calming properties (BERNACCIet al., 2015; MUNHOZ et al., 2018).Sour passion fruit is very susceptible to soilborne pathogens, mainly Fusarium oxysporum f. sp. passsiflorae(FOP), causing fusarium wilt, and Fusarium solani (FS), causing collar rot (FISCHER;REZENDE, 2016).

To manage these root diseases, the safest strategy would be avoided infested areas, but it is not possible in many situations. Thereafter, the most efficient option in infested areas would be the use of resistant cultivars or rootstocks (DARIVA etal., 2015). The studies carried out by Santos et al. (2016) confirmed that grafting using re-sistant rootstocks is an excellent alternative to reducethe harmful effects of Fusarium in sour passion fruit vines. The most valuable rootstocksare wild Passiflora species, such as P. foetida (CARVALHO et al., 2021; CHAVES et al., 2004; SILVA et al., 2017).

Stinking passion flower (P. foetida L.) is widely used due its medicinal properties and could also be used as rootstock to sour passion fruit in areas infested with FOP and FS.

This wild Passiflora species showed resistance to FOP even when cultivated in areas with previous reports of fusarium wilt (SILVA et al., 2017). According to Preisigke et al. (2017), P. foetida, P. nitida, P. morifolia and P. mucronata werethe most resistant to FOP among 14 wild species of Passiflora, which were maintained in Hoagland’s nutrient solution for 40 days. However, P. foetida is susceptible to Meloidogyne incognita (Kofoid and White) Chitwood (SAUER; ALEXANDER, 1979), apolyphagous phytonematode widespread in tropical and subtropical countries (EISENBECK, 2020). Additionally, Meloidogyne spp. (including M. incognita) are known to increase the incidence of fusarium wilt (HILLOCKS, 1985). Therefore, the presence of root-knot nematode is a considerable risk for implantation of vine of P. foetida, or even vines of P. edulisgrafted on P. foetida.

Due this context, the host status of P. foetida to other species of phytonematodes is an important step for risk assessment in infested areas. The reniform nematode (Rotylenchulus reniformis Linford and Oliveira) are the most important nematodesof Passiflora species (INOMOTO; FONSECA, 2020).

The root-lesion nematode Pratylenchus brachyurus (Filipjev) is prevalent in soybean and common bean crop fields of Brazil (BONFIM JUNIOR et al., 2021; DEBIASI et al., 2016; MÁRQUEZ et al., 2021), but it is widespread in the country, and the hoststatus of species of Passiflora to this nematode was not evaluated yet. According to Sauer and Alexander (1979), M. javanica (Treub) caused small galls in P. foetida roots, but did not reproduce.Therefore, the present work aims to assess the host status of stinking passion flower and sour passion fruit to R. reniformis M. javanica and P. brachyurus, which are three of the most widespread plant parasitic nematodes in Brazilian crop fields.

Material and methods

Nematode isolates

The isolate of R. reniformis was obtained from sour passion fruit roots collected in Piracicaba (SP - Brazil) and maintained on the same plant in a glasshouse. The isolate of M. javanica was obtained from soybean roots [Glycine max(L.) Merr.] collected in Londrina (PR - Brazil) and maintained on spring onion (Allium fistulosum L.). The isolate of P. brachyurus was obtained from cotton roots (Gossypium hirsutum L.) in Sapezal (MT – Brazil) and maintained on cotton. Theinocula of the three phytonematodes were obtained byhomogenizing infected roots in a blender and the resultant suspension was poured through three sieves stacked (60-200-500 Mesh, corresponding to 0.250-0.074-0.25mm aperture), resulting in an aqueous suspension containing: eggs and motile forms(eggs, juveniles, males and immature females) of R. reniformis; eggs and second stage juveniles of M. javanica ; eggs and a mix mobilelife stages (juveniles and females) of P. brachyurus.

Plant material

Seeds of P. foetida and P. edulis ‘BRS-Gigante-Amarelo’ (‘BRS-GA1’) were provided by Dr. Fabio G. Faleiro (Embrapa Cer-rados, Planaltina DF - Brazil), and sowed in a 500-cm3 plastic pots (R=4,5cm / r=2,75cm / h=13,5cm) filled with autoclaved sandysoil (121oC/2h) in Apr 5, 2021 (P. foetida) and Jun 17, 2021 (P. edulis). The Passiflora spp.P. foetida seedlings were transplanted in Sep 8, 2021 into pots containing 450 cm3 of an autoclaved sandyloam soil (83% sandy / 2% silt / 15% clay), keeping one plant per pot. Cotton ‘Del-tapine-1730’ was included to check the infectiveness of R. reniformis and P. brachyurus, and muskmelon ‘Asturia’ (Cucumis melo L.) to check M. javanica.

Reniform nematode (experiment 1)

Each seedling was inoculated with an initial population density (Pi) of 1,000 specimens of R. reniformis by pouring the inoculum in a 2-cm-hole made in the soil (Sep 9, 2021 / 1 day after transplanting). The plants were main-tained in a greenhouseuntil the evaluation (Dec 1, 2021 / 83 days after inoculation -DAI). Using a 10-liter bucket containing 4 liters of tap water, the soil and roots were separated. The nematodes from soil were recovered by centrifugal-flotation method (JENKINS, 1964). The resultant aqueous suspension contained adults (males andimmature females) and juveniles of R. reniformis. Nematodes within roots(eggs, juveniles, males and immature females) were recovered as described above for R. reniformisJENKINS, 1964noculum production. The nematodes were preserved alive at 10 oC, andcounted twice in a Peters’ counting slide (1mL aliquot) at 100xmagnification using a light microscope (Olympus CH2, Japan). The R. reniformis final population (Pf) was the sum of the population recovered from the soil (Pf soil) and the populationfrom the roots (Pf Roots); thereafter, the reproduction rate (R=Pf/Pi) was estimated.

Root-knot nematode (experiment 2)

Each seedling was inoculated with 1,000 specimens of M. javanica by pouring the inoculum in a 2-cm-hole made in the soil (Sep 9, 2021). The plants were maintained in a glasshouse until the evaluation (Nov 29, 2021 / 81 DAI), which procedure wassimilar to the described above for R. reniformis.

Lesion nematode (experiment 3)

Each seedling was inoculated with 1,000 specimens of P. brachyurus by pouring the inoculum in a 2-cm-hole made in the soil (Sep 9, 2021). Seedlings of cotton ‘DP-1730’ were also inoculated aiming to assess the infectiveness of the inoculum. Theplants were maintained in a glasshouse until the evaluation (Dec 11,2021 / 93 DAI), which procedure was similar to the described below for R. reniformis.

Experimental design

The trials were conducted in a completely randomized design (CRD), with three treatments (P. foetida, P. edulis and cotton/musk-melon) and seven replicates. Normality of the data was assesses using Shapiro-Wilk test, and when was not fulfilled,data was transformed. For experiment 1, the data obtained (R) weretransformed using log10 (x+1), using the R package (R Core Team) and the mean values were compared by the Tukeyhonest test at the 5% significance level.

Results and discussion

The results were presented in Table 1. The reproduction of R. reniformis and P. brachyurus on cotton, and of M. javanica on muskmelon, confirmed the infectiveness of the inocula. Although the reproduction of M. javanica onmuskmelon ‘Asturia’ could be considered low (R=3.97), it was similar to the values usually obtained previously. For example, the R of 14 genotypes ofmuskmelon ranged from 0.23 to 4.24 in a greenhouse experiment (DINIZ et al., 2016).

Table 1
Number of Passiflora foetida, Passiflora edulis, cotton and muskmelon evaluated plants (N), reproduction of Rotylenchulus reniformis (83 days after inoculation – DAI), Meloidogyne javanica (81 DAI) and Pratylenchus brachyurus (93 DAI) on P. foetida, P. edulis and standard hosts (cotton and muskmelon).

Plants	N	Reproduction Rate (R)
		R. reniformis	M. javanica	P. brachyurus
P. foetida	7	16.27 ab	0.00 a	0.00 a
P. edulis	7	23.04 a	0.00 a	0.01a
Cotton 'DP-1730'	7	8.29 b	-	18.21 b
Muskmelon 'Asturia'	7	-	3.97 b	-

• ^*
  Means followed by the same letter in column do not differ according to Tukey test at 5% significance. ¹Data were transformed using log10 (x+1) before performing the statistical analysis.

The reniform nematode reproduced equally well on both Passiflora species. The nematode population increased more on P. edulis than on cotton, probably because the R. reniformis was isolated and maintained on P. edulis plants. In addition to P. edulis, three other passion fruit species (P. cincinnata Mast., P. setacea DC. andP. alata Curtis) are susceptible to R. reniformis (INOMOTO; FONSECA, 2020).

However, to our knowledge, the present result is the first report of showing the reproduction of the reniform nematode on P. foetida. Thus, producers of stinking passion flower and of passion fruit grafted on P. foetida ought to selectcarefully the nurseries and avoid fields infested with this nematode.

Conversely, both P. foetida and P. edulis proved to be immune or highly resistant to M. javanica and P. brachyurus. The high re-sistance of stinking passion flower to M. javanica confirmed results obtained by Sauer and Alexander(1979), which tested P. foetida to M. javanica; M. incognita and M.hapla and noticed only the reproduction of M. incognita. Some passion fruitspecies, as P. nitida Kunth., P. ligularis Juss. and P. mucronata Lam. are susceptible to M. javanica, but others, including sour passion fruit are immune or highly resistant (GARCIA et al., 2008; ROCHA et al., 2013; SHARMA et al., 2003).

Based on our work and the available data, M. javanica is not a concerning pathogen to both stinking and sour passion fruit.

To our knowledge, the present results are the first work addressing the host status of these Passiflora species to P. brachyurus. Both P. foetida and P. edulis proved to be immune or highly resistant to this root lesion nematode. A survey carried out in an orchard the State of Amapá showed the occurrence of P. brachyurus on roots of murici (Byrsonima sp.) and soil around roots of murici and cupuaçu [Theobroma grandiflorum (Willd.ex Spreng. K. Schum.)], but not onthe roots of an unidentified species of passion fruit and in soilaround the roots (SANTOS; MARTINELLI, 2016).

The results about M. javanica and P. brachyurus, which are ubiquitous in Brazilian croplands, demonstrated that both P. foetida and P. edulis may be cultivated in infested areas with these nematodes. Conversely, R. reniformis maybe a limiting factor for stinking passion flower rootstock implementation and forstinking passion flower cultivation.

Acknowledgments

The authors thank to fellowships from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – CAPES (B. S. J. Paes) and Conselho Nacional de Desenvolvimento Ci-entífico e Tecnológico – CNPq (A. M. G. B. Silva), and to Dr. Fabio Gelape Faleiro for providing the Passiflora spp. seeds. The authors would like to thank Dr. Victor Hugo Moura de Souza for reviewing the manuscript.

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Publication Dates

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

History

• Received
  05 Apr 2022
• Accepted
  15 Aug 2022