The root-knot nematode Meloidogyne paranaensis is one of the main problems for coffee production in Latin American countries. In Mexico, this nematode is found damaging shaded coffee plantations, with a wide variety of associated vegetation. The plant species present in these agroecosystems could serve as nematode alternative hosts, helping to maintain and disperse the population of M. paranaensis even when control measures are carried out in coffee trees. The aim of this work was to evaluate the ability of M. paranaensis to reproduce in 13 plant species commonly associated with shade-grown coffee plantations. The plants were inoculated with eggs and J2 of M. paranaensis, 10 months later the population density, the multiplication rate, and the host susceptibility index were calculated. Meloidogyne paranaiensis reproduced in 11 of the evaluated plants at different levels. Citrus aurantium, Citrus reticulata, Inga jinicuil, Inga vera and Musa AA, were highly susceptible compared to Coffea arabica and Coffea canephora. On the other hand, Macadamia integrifolia and Psidium guajaba are considered resistant to moderately resistant with a reproduction rate less than one and a susceptibility index less than 10 with respect to C. arabica and less than 25 with respect to C. canephora. Persea schiedeana and Syzygium jambos did not allow the M. paranaensis reproduction, so they are considered highly resistant. The results of this study provide important information for the M. paranesnsis management in infested shade-grown coffee plantations. It is necessary to evaluate other woody and herbaceous plant species to improve control measures for this nematode.
Research Article
Host status of plants associated to coffee shady agroecosystems to Meloidogyne paranaensis
https://doi.org/10.21203/rs.3.rs-3098216/v1
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Journal Publication
published 27 Feb, 2024
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Root-knot nematodes
alternative hosts
coffee corky-root disease
The root-knot nematode Meloidogyne paranaensis is one of the main phytosanitary problems in coffee (Coffea spp.) production in Latin America. (Carneiro et al. 1996; Villain et al. 2013). This nematode is associated with the development of the coffee corky-root disease, which begins with the typical thickening and galls on the roots. However, as the infection progresses, more severe symptoms are seen, such as deep cracked cortical tissues with a cork-like appearance, along with the presence of fungi and bacteria inside the root tissues (López-Lima et al. 2020; Lamelas et al. 2020). The disease leads to necrosis and atrophy of the root system, causing the plant death in a period of 2 to 4 years, significantly affecting coffee production (Bertrand et al. 2000). Meloidogyne paranaensis has been detected in Brazil, Guatemala, Hawaii, and Mexico, where coffee production is affected due to the increased distribution of this nematode (Carneiro et al. 2004; Villain et al. 2013; López-Lima et al. 2020).
In Mexico, coffee corky-root has been recorded since the 1960s, however the disease was distributed only in small areas of the Veracruz and Chiapas states. In 2015, M. paranaensis was identified in heavily affected plants with corky-root in several shade-grown coffee plantations in the main producing areas of the Veracruz and Puebla states (López-Lima et al. 2015; Alcasio-Rangel et al. 2017). Currently, M. paranaensis is a threat to coffee production in Mexico, it is estimated that up to 35% of replanted Coffea arabica plants are lost every year in many municipalities of Veracruz, forcing producers to frequently replace affected plants (Téliz-Ortíz et al. 1993; INIFAP 2005; López-Lima 2021). In Mexico, most of the coffee plantations are found in different agroforestry schemes, with a variety of both native and introduced vegetation, which functions as shade for coffee plants and provides additional income to farmers (Licona-Vargas et al. 2006; Hernández-Martínez et al. 2009). This type of biodiverse agroecosystems also functions as a refuge for many species of plants and animals, in addition to contributing to the recharge of groundwater tables and carbon sequestration (Ruelas-Monjardín et al. 2014). Among the main plant species associated with shade coffee plantations are Persea americana, Persea schiedeana, Inga vera, Inga jinicuil, Quercus spp. and some introduced species such as Musa spp. Macadamia spp., and Citrus spp. (Moguel and Toledo 1999; López-Gómez et al. 2008; Castro-Luna and Galindo-González 2012; Ramos-Reyes et al., 2019). Recently, M. paranaensis was found parasitizing roots of Musa spp. in infested coffee plantations, this is important for the nematode management, since the plants associated with shaded-coffee agroecosystems could contribute to the dispersion and maintenance of M. paranaensis populations and to the infection of replanted coffee trees, even when prophylactic measures are taken. In addition to C. arabica, C. canephora and Musa spp., the nematode M. paranaensis has been recorded parasitizing 36 plants, mainly herbaceous such as Brachiaria plantaginea, Galinsoga cilliata, Impatiens balsamina, Ilex paraguariensis and Raphanus raphanistrum (Carneiro et al. 1996; Santiago et al. 2000; Roese and Oliviera 2004; Campos and Villain 2005; Machado et al. 2014; Da Silva et al. 2015; Mendoca et al. 2017). However, the hosts of M. paranaensis in plants associated with coffee agroecosystems, which is where this nematode is currently most widely distributed, are not known. Knowing the status of M. paranaensis hosts in coffee agroecosystems will provide important information for decision-making when implementing coffee corky-root disease management strategies. Therefore, the objective of this work is to determine the host status of M. paranaensis in 13 plant species commonly associated with shaded-coffee agroecosystems.
Meloidogyne paranaensis population
The eggs and J2 used for the plants inoculation were obtained from infested coffee roots collected in the La Lagunilla town, municipality of Cosautlán de Carvajal, Veracruz, Mexico. Population was previously identified with specific SCAR markers (Randig et al. 2002; López-Lima et al. 2015) and reproduced in tomato plants (Solanum lycopersicum cv Rio Grande).
Plant species
Thirteen plant species commonly associated with coffee plantations were selected, either as shade or for use: Citrus aurantium, Citrus reticulata, Enterolobium cyclocarpum, Eriobotrya japonica, Inga jinicuil, Inga vera, Macadamia integrifolia, Musa AA, Persea americana, Persea schiedeana, Psidium guajaba, Quercus xalapensis and Syzygium jambos. The plants were obtained at the Tierra Vital nursery (Coatepec, Veracruz). Likewise, C. arabica CV Costa Rica 95 and common C. canephora plants were obtained from Paso Grande nursery (La Estanzuela, Veracruz) and were included as susceptible controls, the age of the plants was 12 months on average. All the plants were taken out from their original pots to remove the remains substrate with running water and verify the health of the roots. Subsequently, they were transplanted into 25x40 cm polypropylene bags with a sterile substrate composed by soil, peat moss and perlite in 1.5 1 and 0.5 proportions. The plants were distributed in a completely random design in a shade house in the experimental area of the Faculty of Agricultural Sciences of the Universidad Veracruzana, campus Xalapa and were allowed to acclimatize for 45 days. To stimulate the roots and foliage development, 100 mL of rooting fertilizer were applied to the base of the stem at a concentration of 2 gr L− 1 (Rotex®, Cosmocell) and 20 mL of foliar fertilizer (Bayfolan® Bayer) at a concentration of 4 mL L− 1 to each plant three times with 15-day intervals. Likewise, to control the insects and phytopathogenic fungi populations, the insecticide imidacloprid (Dinastia® Agroquimica Tridente 0.5 mL L− 1), the fungicides methyl thiophanate (Cerfutrin 70® Agroquimica Tridente 3 g L− 1) and cyproconazole (Alto100® Syngenta 0.5 mL L− 1) were applied once. The plants were watered every 72 hours.
Meloidogyne paranaensis inoculation
Nematodes were extracted from the tomato roots by crushing in sodium hypochlorite, sieving, and centrifuging to obtain eggs and second stage juveniles (J2) (Carneiro et al. 2004). Subsequently, the number of viable eggs was quantified according to their morphology (Calderón-Urrea et al. 2016) and live J2 juveniles according to their mobility in a Sedgwick-Rafter counting chamber (Wildlife Supply Company, Model 1801-A10) under a light microscope (Nikon, Alphaphot YS2), at 100X. Once the number of viable specimens in the sample was determined, the suspension was adjusted with sterile water to 200 eggs and J2 mL− 1. Prior to inoculation, the plants were watered, and two holes were made in the substrate near to the stem base to expose the roots. Subsequently, 50 mL of the M. paranaensis eggs and J2 suspension were added to each plant divided into the two holes with the help of a 25 mL syringe (10,000 eggs and J2 per plant). After inoculation, the plants remained in the shade house for 10 months, with irrigation every 72 hours and foliar fertilization every 30 days (20 mL of Bayfolan® at 4 mL L− 1).
Evaluation of galling and reproduction of M. paranaensis
After the experimental period, the plants were removed from the pots, the roots were washed with running water and dried with absorbent paper to obtain the fresh weight and observe the galls formation or corky symptoms and assign a number on the galling scale (Coyne and Rose 2014). Afterwards, the roots were cut into fragments of 1–2 cm and 50 gr were taken to extract eggs and J2 by the crushing, sieving and centrifuging technique (Carneiro et al. 2004). The roots that weighed less than 50 gr were processed whole. A 10 mL suspension of eggs and J2 was obtained from which three one mL aliquots were taken and counted in a Sedgwick-Rafter chamber under a 100X light microscope. The average of the nematode count and the total root weight was used to calculate the population density, the final population, and the reproduction rate in each plant species.
Host susceptibility index and resistance level
The host susceptibility index (HSI) expressed as a percentage was calculated taking as reference the population density in the roots of the main hosts C. arabica and C. canephora and comparing it with the nematode population density in the other evaluated plant species. From this parameter, the plants were classified by their resistance level (RL) according to the criteria used by Shigueoka et al. (2016), where: 0 to 1% = highly resistant (HR); 1.01 to 10% = resistant (R); 10.01 to 25% = moderately resistant (MR); 25.01 to 50% = moderately susceptible (MS); 50.01 to 75% = susceptible (S); 75.01 to 100% = highly susceptible (HS). Resistance indicates the ability of the plant to suppress the nematode reproduction and susceptibility is determined by the normal nematode reproduction in the main host.
Data analysis
Data on population density and final population were analyzed for normality by the Shapiro-Wilk test and homogeneity of variances by Levene's test at 5%. The data were subjected to a Kruskal-Wallis analysis of variance and the test of multiple comparisons of means at 1% probability in the Statistica 12 program for Windows.
The plants presented different symptomatology on the roots (Table 1). Numerous light and elongated thickenings were observed in the roots of C. aurantium and C. reticulata, but without evidence of necrosis. Coffea arabica, C. canephora, I. jinicuil (Fig. 1a), I. vera (Fig. 1b) and M. integrifolia (Fig. 1c) showed light to medium galling and developed characteristic symptoms of corky-root disease as hyperplasia in the cortical tissue with cracks. Musa AA showed a medium to high galling level, with elongated galls and beginnings of necrosis (Fig. 1d). When making cuts in the galls, numerous females and egg masses embedded in the tissue were observed (Fig. 1e-h). The highest population density of M. paranaensis was recorded in I. vera plants, followed by Musa AA, C. aurantium and the main host C. arabica. The highest final population (Table 1) and reproduction rate (Table 2) was found in Musa AA followed by I. vera, C. aurantium, C. reticulata and C. arabica. Taking as reference the population density values of C. arabica to calculate the HSI and RL, C. aurantium, C. reticulata, I. jinicuil, I. vera and Musa AA were highly susceptible, since allowed the nematode reproduction above 80%. On the other hand, C. canephora and E. cyclocarpum were moderately resistant, while E. japonica, M. integrifolia, P. americana, P. guajaba and Q. xalapensis were classified as resistant (Table 2). Likewise, when the values of the population density in C. canephora were taken to calculate the HSI and the RL, C. arabica, C. aurantium, C. reticulata, E. cyclocarpum, I. jinucuil, I. vera and Musa AA resulted highly susceptible, while M. integrofolia and P. guajaba were classified as moderately resistant. Meloidogyne paranaensis could not reproduce in P. schiedeana and S. jambos, so were classified as highly resistant (Table 2).
|
Specie |
Corky-root symptoms |
Galling index |
Population density (eggs and J2 gr root− 1) |
Final population |
|---|---|---|---|---|
|
Citrus aurantium |
No |
2 |
656.5 def |
60631 de |
|
Citrus reticulata |
No |
2 |
315.7 def |
41660 cde |
|
Enterolobium cyclocarpum |
No |
1.1 |
76.7 cdef |
5553 bcde |
|
Eriobotrya japonica |
No |
1.1 |
14.4 abcd |
1096 abc |
|
Inga jinicuil |
Yes |
2 |
334.8 abcde |
18655 abcd |
|
Inga vera |
Yes |
2.5 |
3804.3 f |
570548 e |
|
Macadamia integrifolia |
Yes |
2.1 |
12.6 abc |
1652 ab |
|
Musa AA |
No |
3.5 |
1923.4 f |
1521423 e |
|
Persea americana |
No |
1 |
21.2 abcd |
2756 abcd |
|
Persea schiedeana |
No |
1 |
0 a |
0 a |
|
Psidium guajaba |
No |
1 |
9.1 ab |
1525 abc |
|
Quercus xalapensis |
No |
1 |
20.1 abcde |
955 abc |
|
Syzygium jambos |
No |
1 |
0 a |
0 a |
|
Coffea canephora |
Yes |
2 |
55.156 bcde |
2514 bcd |
|
Coffea arabica |
Yes |
2.5 |
390.586 ef |
31413 de |
|
Different letters in the columns indicate significant differences in the population density and final population of M. paranaensis between the plant species after the Kruskal-Wallis test and multiple comparisons of means at 0.01%. |
||||
Coffee agroecosystems in Mexico are main socioeconomic and environmental importance, conserving them is a priority for many people and private and public organizations. However, coffee corky-root disease represents a threat to the continuity of these plantations. The focus of this study was to determine the host status of some plant species commonly associated with shade coffee plantations in Veracruz, the observations indicate the potential of M. paranaensis to reproduce adequately in at least 5 species evaluated with different degrees of susceptibility. In general, Meloidogyne species are polyphagous, which makes their management difficult because they can remain in other plants in the absence of the main host; however, in the case of M. paranaensis, knowledge about the host range is still limited.
Meloidogyne paranaensis was able to reproduce in the two evaluated citrus species. Another species, such as Meloidogyne indica, causes significant damage to citrus in India, causing the dieback of the plants in one year (Kumar and Arthurs 2021). Likewise, Meloidogyne javanica, Meloidogyne incognita and Meloidogyne arenaria affect citrus species in Asian and African countries (Bakr et al. 2011; Onkendi et al. 2014). In this work, despite the high reproduction rate in Citrus spp., no major damage to the roots or aerial symptoms were observed; however, we do not recommend the use of this plants in M. paranaensis infested fields since they allow reproduction even more than the main host.
Our results indicate that M. paranaensis was able to reproduce in E. cyclocarpon. This plant is very common in coffee plantations due to its wide crown, which leaves extensive shaded areas. Although other species of this genus are highly susceptible to Meloidogyne spp., E. cyclocarpon has no recorded significant problems with nematodes (Falkowski et al. 2019).
Erythrobotria japonica limited the reproduction of M. paranaensis, according to our bibliographical review, there are no records of significant affectations by Meloidogyne or other nematode genera on this plant. In contrast, whole plant ethanolic extracts have been reported to cause Meloidogyne J2 mortality in vitro (Sultana et al. 2014). It is possible that the plant has defense mechanisms against nematodes, so it is necessary to investigate its possible nematicidal effect in the field.
Inga species are the shade trees most used by coffee growers in Veracruz, due to their rapid growth, shade level, and nitrogen fixation in the soil (Ávila-Bello et al. 2023). According to our bibliographic review, there are no records of nematodes associated with Inga species; however, our results indicate that the two species evaluated are very susceptible to M. paranaensis, so we do not recommend their use in infested sites.
Macadamia integrifolia limited the reproduction of M. paranaensis compared to the main hosts, however, some root areas development galling and initial symptoms similar to those of corky-root disease. In another study, seven macadamia varieties were evaluated against M. paranaensis and none of them reproduced adequately or developed galls (Costa et al. 2020). However, these authors used a lower population density and shorter interaction period (120 days) than in this work. It is possible that the nematode requires more time for the development of galling symptoms as occurs in common C. canephora (Sera et al. 2006), but it can cause damage to macadamia plants in the medium or long term. Pathogenicity studies should be carried out with different infestation levels and interaction periods to determine the macadamia susceptibility, since this is one of the most widespread crops associated with coffee plantations and could be at risk from this nematode.
The susceptibility of banana plants was confirmed. This crop was highly susceptible due to its non-woody root and rapid development. It is known that M. paranaensis affects banana plants in coffee plantations (Villain et al. 2013; Lopez-Lima et al. 2015). Musa spp. are very susceptible to nematodes, mainly of the genera Radopholus, Pratylenchus and Meloidogyne (Seenivasan and Senthilnathan 2018; Peraza-Padilla et al. 2020). However, it is necessary to carry out pathogenicity tests with M. paranaensis to know if it can represent a risk for banana plantations.
The Persea spp. plants did not show damage symptoms, although P. americana allowed reproduction at low levels. Low populations of Meloidogyne hapla and Meloidogyne trifoliophila are known to be associated with Persea sp. in New Zealand orchards, but no major damage reported (Knight 2001). Likewise, another study indicates that Meloidogyne incognita race 2 cannot reproduce or cause galling in potted avocado seedlings. Persea spp. seems to be more susceptible to genera such as Pratylenchus, Radopholus and Helicotylenchus (El-Borai and Duncan 2005). According to these results, we think that P. ameriacana and P. schiedeana are an option for planting in M. paranaensis infested sites.
Psidium guajaba, is severely affected by M. enterolobii, which together with Fusarium spp. cause the guava decline and similar symptoms to those of coffee corky-root disease (Khan et al. 2022). However, our results indicate that it is not susceptible to M. paranaensis. This plant is commonly associated with coffee plantations in Mexico, as part of the shade vegetation. This work indicates that its use is viable in infested coffee plantations.
There are records of Meloidogyne species parasitizing Quercus spp. (Brito et al. 2015; Sohrabi et al. 2015; Brito et al. 2016). However, under the conditions of this work it seems that Q. xalapensis is not very susceptible to M. paranaensis. As a native species, its maintenance in coffee agroecosystems is environmentally important.
Syzygium jambos is suitable for use in infested coffee plantations since not allow the reproduction of M. paranaensis, also there are no records of nematode involvement in this plant. In addition, the S. jambos extracts of leaves and bark have antimicrobial activity, however it is necessary to investigate its nematicidal activity (Djipa et al. 2000; Mohanty and Cock 2010).
Knowing the M. paranaensis hosts within the plants present in the shade-grown coffee agroecosystems is important since it influences the permanence and increase of nematode populations. Management strategies should consider possible alternative hosts for M. paranaensis, even when using tolerant rootstocks, since avoiding exposure to high population densities is crucial to maintaining the productivity and longevity of new plantings. The results of this study provide important information for the management of M. paranesnsis in infested shade-grown coffee plantations. It is necessary to evaluate the pathogenicity of M. paranaensis in plants that were susceptible, as well as in other woody and herbaceous plant species present in coffee agroecosystems.
Competing Interests: The authors declare that they have no conflict of interest.
Acknowledgments
The first author thanks the National Council of Humanities, Sciences and Technologies (CONAHCYT) for the scholarship granted to carry out her postgraduate studies (PhD in Agricultural Sciences) at the Universidad Veracruzana (UV).
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