CC BY
19Russian Journal of Nematology, 2016, 24 (1), 61 - 71
Effect of permanent partial root-zone irrigation on Meloidogyne ethiopica parasitising roots of Vitis
vinifera rootstock SO4
Juan C. Magunacelaya, Cecilia Ramírez and Sebastián González-Bernal
Instituto de Biología, Pontificia Universidad Católica de Valparaíso, Avenida Universidad 330, Curauma, Valparaíso, Chile
e-mail: juan.magunacelaya@pucv.cl
Accepted for publication 18 May 2016
Summary. In Chile Meloidogyne ethiopica often causes death of plants in vineyards with drip irrigation, where the dry season leaves part of the roots in dry soil. The effects of M. ethiopica on grapevine were evaluated in conditions of permanent partial irrigation. The study was conducted in series of experiments where roots were divided into two planters with sandy soil under glasshouse condition. The partial irrigation was simulated by watering only one of the two or both of the planters and with water treatments once or twice per day, and some infected with M. ethiopica. After 6 months, the quality and weight of roots and size of above ground plant parts were evaluated and measured. The permanent partial irrigation resulted in higher quality and weight of roots; however, it further aggravates the consequences of infection, especially when M. ethiopica was present in irrigated soil. Meloidogyne ethiopica decreases the ability of the plant to preserve plant roots in areas without irrigation. Key words: grapevine, host-parasitic relationship, hydraulic redistribution, soil moisture.
During the last decades grapevine (Vitis vinifera L.) plantations have tended to be established with a drip irrigation system, which gives them several advantages. Such technology promotes root concentration at the edge of irrigation zone growing towards the inter-row where higher oxygen and less water are found. During rainy season, the zone is bigger and, thus, roots can grow into it; during the dry season, the irrigated area is reduced, consequently causing many active roots to be left out the irrigated area (Magunacelaya, 2009).
It is known that if one part of the root system is in dry soil, the root wets the soil though hydraulic redistribution from the areas with water available for absorption, allowing the plant to cope with water stress (Eissenstat et al., 1999; Domec et al., 2004; Bauerle et al., 2008a; Bayala et al., 2008). However, when the root in the arid region of the soil detects drying, it produces hormonal changes, including an increase of up to 10 fold of abscisic acid (ABA) in the roots (Stoll et al., 2000), even when the amount of water in the plant is enough to meet the demand (Taiz & Zeiger, 2002). The ABA strengthens the root in drying conditions, maintaining growth (Sharp et al., 1994) and increases the hydraulic conductivity (Zhang et al., 1995).
Apart from the effects of irrigation on plant, the presence of root-knot nematodes, Meloidogyne spp.
should be also considered (Magunacelaya et al.,
2005). The effects of root-knot nematodes is proportional to the number of juveniles infesting the roots, which include altering the balance of nutrients, impaired branching and root extension, reducing the rate of photosynthesis, and inhibiting root and shoot growth (Magunacelaya & Dagnino, 1999). The cv. Chardonnay is especially sensitive to the effects of Meloidogyne spp. (Aballay et al., 2013; Howland et al., 2015), whereas SO4 rootstock is tolerant to Meloidogyne spp. (McKenry & Anwar,
2006).
Meloidogyne ethiopica Whitehead, 1968 is one of the most aggressive species infecting many plant species (Carneiro et al., 2007) and causing severe damage to agriculture (Magunacelaya et al., 2005). This nematode was described from Tanzania and it is considered an invasive species in Chile, where it is found from Copiapó Valley to Talca (Carneiro et al. , 2007). This species has also been reported in other South American countries, Brazil (Carneiro et al., 2003) and Perú (Murga-Gutierrez et al., 2012), and in South Africa and several Mediterranean countries, including Greece (Concei^ao et al., 2012) and Turkey (Aydinli et al., 2013), and in Slovenia (Sirca et al., 2004; Strajnar et al., 2009).
Among factors affecting root knot nematodes, irrigation is a main factor (Wallace, 1968). Water is
£ 16ÜÜ 'in
— 1750 O
17GC
1G5Ü
0 1 2 3 4 5 6
Days after irrigation
Fig. 1. Water retention in the sandy soil used in this study. In order to assess the soil water retention, three perforated planters with 1.5 l of sandy soil were used. They were weighed dry and irrigated with 250 ml every 5 minutes for 30 min. Subsequent measurements were taken after 1, 2, 3, 5, 7, and 9 h after irrigation. Two days later they were weighed three times a day and the subsequent four days just once a day.
necessary for hatching (Mohawesh & Karajeh, 2014). Water transports soluble root exudates, which induce chemotaxis of juveniles (Reynolds et al., 2011). Juveniles start to search for roots in water films on the surface of soil particles (Fujimoto et al., 2010); host infestation is reduced when there is less water in the soil (Mohawesh & Karajeh, 2014). With alternating partial root zone irrigation it has been shown that the population density of M. javanica decreased in comparison to treatments with daily watering (Shin et al., 2007); however, the alternating partial root zone irrigation every 2 weeks might produce a different effect when partial irrigation supplies were continuous.
Our glasshouse study attempted to replicate some of the conditions observed in a vineyard growing cv. Cabernet Sauvignon producing 1 million kilos of fruit, equivalent to the production on 80 ha. The vineyard was located in Talca, in the Maule Region of Chile (35°26'00" S and 71°40'00" W) with a warm temperate climate and annual rainfall between 720 and 730 mm concentrated from May to August, favouring root growth outside the area moistened by
drip irrigation. However, after several years of the cumulative effect of drought, in 2008 only one-sixth part of the vineyard was irrigated. This situation leads to the questions: what was happening to the root when irrigation is continuously wetting only one part of the root zone leaving the other part without water, and how does this condition influence the effect of phytoparasitic nematodes on the plant. We hypothesised that M. ethiopica will be present in the most watered root zone of a plant, producing greater damage than in the zones with less irrigation, based on the previously described published data.
MATERIALS AND METHODS
Location and preparation of pots. The
experiment was conducted in a glasshouse under controlled conditions of temperature and humidity (26°C and 67% RH on average, respectively) located in Viña del Mar, Chile. A sandy soil was used (particle size see Table 1) with low water retention (Fig. 1) so as to heighten the effects of
frequent irrigation and to favour the movement of Meloidogyne sp. (Prot & Van Gundy, 1981; Magunacelaya & Dagnino, 1999; Fujimoto et al., 2010; Jaraba et al., 2014). Vitis vinifera cv. Chardonnay plants were used on rootstock SO4, described as tolerant to Meloidogyne spp. (McKenry & Anwar, 2006). The term tolerance is related to the ability of the host to support or recover from the harmful effects of nematode attack, allowing multiplication but the performance of the plant is not affected (Trudgill, 1991; Dalmasso et al., 1992).
Each vine was planted dividing its roots in two planters. Half of the root system was planted in a first planter, and the other half of the root was planted in a second planter (Fig. 2). Both planters held 2 l of soil with drainage. After planting, seedlings were watered daily for 1 month so that they would establish in the two planters. After a month, irrigation treatment was applied.
sf
SIDE 1 (S1) SIDE 2 (S2)
Fig. 2. Vitis vinifera with roots divided and tied up in Planter A and Planter B. This figure is a representation of an experimental unit. There were different irrigation management and nematode (Meloidogyne ethiopica) inoculations in each planter (see Table 2).
Treatments. One plant with root divided in two planters (containers) was considered as an experimental unit of treatment (Fig. 2). The
complete list of treatments is given in Table 2. The number of irrigations per day varied from one to two. Each watering included 250 ml of water per container, which is the equivalent of completely wetting the 2 l of soil. The irrigation was performed manually.
Meloidogyne ethiopica source and pot
inoculation. Meloidogyne ethiopica second-stage juveniles (J2) were obtained from infected vines from the Valle de Casablanca, Valparaiso, Chile by the blender technique (Magunacelaya, 2009) and inoculated 1 month after planting, when the roots were established and likely to be attractive for nematodes. Each planter was inoculated in three holes near the root with 400 J2 concentrated in 3 ml of water.
Measurements. Plants were evaluated after 6 months. The grafting without leaves was weighed to measure the growth of the aerial part of the vine. Live and dead roots were weighed separately. The root was considered dead when symptoms of necrosis were evident outside and inside plant tissues. In order to measure the quality of the roots, a root rating scale of 1-6 was used to assess the damage caused by nematodes (Fig. 3). Scale 1 represents the maximum deterioration, with galls induced by M. ethiopica and the absence of fine roots and great proportion of dead roots; scale 6 represents roots without galls and an abundance of fine roots. The roots divided into two planters were evaluated separately. The soil moisture was measured daily during the first month with a Grove Moisture Sensor (SKU: SEN92355P) connected to an Arduino Uno programmed with the open coded software (http: //seeedstudio.com/wiki/Grove_-_Moisture_Sensor) from Seeed Technology Inc. Three perforated planters with 1.5 l of sandy soil were used. They were weighed dry and irrigated with 250 ml every 5 minutes for 30 min. Subsequent measurements were taken after 1, 2, 3, 5, 7, and 9 h after irrigation. Two days later they were weighed three times a day and the subsequent four days just once a day.
Experimental design. The experiment was a completely randomised design with eight replications (plants) per treatment. The program Sigmastat 2.0 (Jandel Corp.) was used to analyse the data. For the statistical analysis of the weight of the live and dead roots, as well as the pruning weight, analysis of variance was used as a pathway with logarithmically data. The Kruskal Wallis test was used to compare the averages of root quality of the treatments (P < 0.05).
Fig. 3. Qualification scale from 1 to 6 to evaluate root quality, using the criteria: the root system size, abundance of fine roots and branches, proportion of dead roots and the abundance of galls produced by Meloidogyne ethiopica. Scale 1 represents the maximum deterioration, with galls induced by M. ethiopica and the absence of fine roots and great proportion of dead roots; scale 6 represents roots without galls and an abundance of fine roots. The roots divided into two planters were evaluated separately.
RESULTS
Treatments in which Planter A was irrigated twice daily, while Planter B was not irrigated (PA2i-PBni, PA2i-PBniMe, PA2iMe-PBni, PA2iMe-PBniMe). The section of roots that presented the highest quality and weight was that found in the watered Planter A; however, the section of the root that was not watered (Planter B) also achieved good quality: average 4.4 out of 6 (Treatment PA2i-PBni) (Fig. 4).
When only one section of root was infected, the quality of the complete root system was diminished, including the quality of the non-infected part of the root (Treatments PA2i-PBniMe and PA2iMe-PBni).
When the root section in Planter B was infected and without irrigation, its quality decreased and, consequently, there was a significant reduction of quality of the roots in Planter A. The damage in quality and weight of the root was significantly greater when the irrigated zone was with M. ethiopica (Planter A) in comparison to when it was infected without watering (Planter B) (Fig. 4).
The lower quality and weight of root in both Planter A and Planter B was obtained in treatment PA2iMe-PBniMe, where the entire root was infected with M. ethiopica. In this case, quality of the root in the irrigated zone was significantly higher than the area without irrigation (Fig. 4). The soil moisture in Planter A ranged between 85-95%, while it ranged 60 to 90% in Planter B.
Table 1. Soil granulometry (sample weight 250
Particle size (in mm) Particle type Weight (g) Percentage (%)
> 2.00 Large particles 3.1 1.3
0.6-2.0 Thick sand 8.1 3.3
0.25-0.59 Medium sand 105.9 43.2
0.106-0.24 Fine sand 111.7 45.6
0.053-0.105 Fine sand 13.4 5.5
0.045-0.052 Wafer-thin sand 2.3 0.9
< 0.045 Silt plus clay 0.5 0.2
Table 2. Treatments of the plants with divided roots in two planters.
Treatments
Planter A, 2 irrigations/day without M. ethiopica - Planter B, no irrigation without M. ethiopica Planter A, 2 irrigations/day without M. ethiopica - Planter B, no irrigation with M. ethiopica Planter A, 2 irrigations/day with M. ethiopica - Planter B, no irrigation without M. ethiopica Planter A, 2 irrigations/day with M. ethiopica - Planter B, no irrigation with M. ethiopica Planter A, 1 irrigation/day without M. ethiopica - Planter B, no irrigation without M. ethiopica Planter A, 1 irrigation/day without M. ethiopica - Planter B, no irrigation with M. ethiopica Planter A, 1 irrigation/day with M. ethiopica - Planter B, no irrigation without M. ethiopica Planter A, 1 irrigation/day with M. ethiopica - Planter B, no irrigation with M. ethiopica Planter A, 1 irrigation/day without M. ethiopica - Planter B, 1 irrigation/day without M. ethiopica Planter A, 1 irrigation/day with M. ethiopica - Planter B, 1 irrigation/day without M. ethiopica Planter A, 1 irrigation/day with M. ethiopica - Planter B, 1 irrigation/day with M. ethiopica
(PA2i-PBni) (PA2i-PBniMe) (PA2iMe-PBni) (PA2iMe-PBniMe) (PAli-PBni) (PA1i-PBniMe) (PA1iMe-PBni) (PAliMe-PBniMe) (PA1i-PB1i) (PA1iMe-PB1i) (PA1iMe-PB1iMe)
Treatments in which Planter A was irrigated once a day and Planter B was not irrigated (PA1i-PBni, PA1i-PBniMe, PA1iMe-PBni, PA1iMe-PBniMe). When comparing the non-infected treatments in which Planter B had no irrigation, whereas treatments of Planter B had irrigation twice per day (PA2i-PBni) and once per day (PA1i-PBni), results showed that the quality and weight of the roots obtained were significantly lower when Planter A was watered only once. This indicates that irrigation once per day is not the best option (Fig. 4). It should be pointed out that during the treatment period; the moisture on the soil surface was visible in Planter B, which did not receive watering, while Planter A, which held part of root system, was watered twice daily. Planter B was less
visibly wet in the treatments where Planter A was watered only once daily.
The quality and weight of root was higher in the portion of roots those were watered (Planter A) with statistical significance equal to the treatments PA2i-PBni, PA2i-PBniMe, PA2iMe-PBni, PA2iMe-PBniMe. However, the difference in these treatments is that the mass of the roots was more concentrated in Planter A, with the exception of the treatment where only the root of Planter B was infected with M. ethiopica, which significantly decreased the quality of the root in Planter A (watered).
Infection with M. ethiopica only in the irrigated Planter A (treatment PA1iMe-PBni) produced a higher level of damage in the plant root system than
when plants were infected only in the non-irrigated Planter B (treatment PA1i-PBnMe). Generally, quality and root weight showed the same trend, but it was less pronounced than that obtained in the treatments in which the Planter A was watered twice per day (Figs 4 & 5).
In treatments where both Planters A and B were infected (PA1iMe-PBniMe), a high weight of live roots was obtained in Planter A; however, these infected roots had low quality similar to the treatment in which only Planter A was infected. The other part of its root system in Planter B had the lowest root weight in this group of treatments and one of the worst qualities (Figs 4 & 5). The soil moisture in Planter A ranged from 75 to 90% and in Planter B it ranged from 44 to 80%.
Treatments in which Planters A and B were irrigated once a day (PA1i-PB1i, PA1iMe-PB1i, PA1iMe-PB1iMe). The root quality and root weight was similar in Planters A and B (Figs 4 & 5). It serves to highlight that the total root mass in both containers was much more inferior to that found only in Planter A (watered) from treatments PA2i-PBni and PA1i-PBni. Soil moisture in both planters ranged between 81 and 96%.
Aerial part weight. There were no significant differences between treatments (Table 3), the mean weight of the aerial part was generally low and highest weight was obtained from plants watered twice per day in the non-infected Planter A (treatments PA2i-PBni and PA2i-PBniMe).
Table 3. Aerial part results.
Treatment Aerial part weight (g)
PA2i-PBni 3.5a
PA2i-PBniMe 3.63a
PA2iMe-PBni 2.63a
PA2iMe-PBniMe 2.75a
PAli-PBni 3.13a
PAli-PBniMe 1.75a
PAliMe-PBni 3.25a
PAliMe-PBniMe 1.63a
PAli-PBli 2.75a
PAliMe-PBli 2.0a
PAliMe-PBliMe 2.0a
Note. Each number represents the average of the 8 repetitions. Numbers are followed by the same letter do not differ significantly.
Fig. 4. Quality of roots of both Planter A and Planter B for each treatment, evaluated on a scale of 1-6 (see Fig. 3 legend). Bars followed by the same letter do not differ significantly.
Weight of Roots (g) Planter A
Weight of Roots (g) Planter В
PAli-PBni
PAli-PBni/We
PAli/We-PBni
PAliMe-PBniMe
PAli-PBli
PAliMe-PBli
PAltMe-PBliMe
aC
bC
be be
cde
] def
60,0 50,0 40,0 30,0 20,0 10,0 0,0 10,0 20,0 30,0
PA2i-PBrii PA2i-PBniMe PA2i/We-PBni PA2iMe-PBniMe
ШШШШШШ
ЩШШЩШШШ cd
ef
W////////W
ШШ f
f
а уммшт//ж///мж//м/жмтш/шт f
ef
]f f
'¿.-Ж/Ж.У/т
def ЩШШЖЖШй
_L
ef
ef
□ without irrigation h irrigation once a day n irrigation twice a day 123 infested with Meloidogyne ethiopjeo
Fig. 5. Weight of live roots of both Planter A and Planter B for each treatment. Bars followed by the same letter do not differ significantly.
DISCUSSION
Our study showed that the weight of roots does not always correlate with their quality. Heavy root systems were obtained but had an excess of thick roots or galls; by contrast, roots with a lighter weight had an abundance of fine roots and branches, without galls.
The root system. Treatments in which Planter A were irrigated twice daily, while Planter B was not irrigated (PA2i-PBni, PA2i-PBniMe, PA2iMe-PBni, PA2iMe-PBniMe). The irrigation process in this group of treatments allowed the highest root quality, which is explained by the fact that watering Planter A twice a day was enough to cover the demand in both the aerial portion and the roots that were also in the soil that did not receive irrigation; however, the roots in Planter B without irrigation presumably detected a water deficit triggering the synthesis of ABA (Barcelo Coll et al., 1990), which stimulated the root growth (Waisel et al., 2003) explaining the excellent root quality.
However, by including M. ethiopica in treatments, the water condition in the soil became a
factor that aggravated the condition of the root. The state of the root was very different if the infected portion was the root received irrigation (Planter A) than if the infected area was the part of the root without irrigation (Planter B). This can be explained though the sensory and motor system of the M. ethiopica J2, which use water for movement, facilitating the capture of soluble root exudates and increases survival (Magunacelaya & Dagnino, 1999). Once installed in their feeding sites, root-knot nematodes substantially decrease the absorption of water and nutrients by the host plants (Caillaud et al., 2008).
When the non-irrigated root in Planter B was infected, damage to the entire root of the plant resulted and functionality was affected because the irrigated portion was not able to sustain the entire root system; it is difficult to explain how J2 moved to damage the root system in the absence of water in the soil. The redistributed water can passively leave the root into the dry soil and hydrate the rhizosphere (Richards & Caldwell, 1987; Caldwell et al., 1998). Therefore, the hydraulic redistribution could be low enough in the soil of Planter B to allow the mobility of the J2 nematodes to invade the roots and
eventually form galls. Hans-Holger & White (2008) consider that the water escaping from the roots for hydraulic redistribution may benefit soil organisms.
The hydraulic redistribution has the ability to mitigate the water stress of the portion of the root without irrigation, increasing the survival of the roots and allowing the fine roots to continue their functions (Williams et al., 1993; Matzner & Richards, 1996; Warren et al., 2007), similar to the results of Bauerle et al. (2008a) where the root's survival in the non-irrigated zone was similar to the watered root zone.
In treatment infected with M. ethiopica in the irrigated planter (PA2iMe-PBni and PA2iMe-PBniMe), the quality of roots in Planter A was significantly reduced. Such roots with reduced quality and weight would have less capacity for water absorption and less water available to redistribute to the non-irrigated part of the roots. This interpretation is supported by comparing the results of Planter B's roots, where there were no statistical differences between treatments PA2iMe-PBni, PA2iMe-PBniMe, and PA1i-PBni, the last treatment being non-infected.
Treatment PA2iMe-PBni shows that the most damaged part of the root is not necessarily the nematode infected part. This may explain why the translocation of water decreases the resistance to water flow generated by the hypertrophied cells of the feeding sites of M. ethiopica (Magunacelaya & Dagnino, 1999), when the lack of water results in the hydraulic redistribution to the roots in Planter B becoming more difficult (Bauerle et al., 2008a).
Treatments in which Planter A was irrigated once a day and Planter B was not irrigated (PA1i-PBni, PA1i-PBniMe, PA1iMe-PBni, PA1iMe-PBniMe). The plants in these treatments, while receiving only one watering per day, have less water available than the plants in treatments PA2i-PBni, PA2i-PBniMe, PA2iMe-PBni, PA2iMe-PBniMe. Root growth of these plants was stimulated in the soil that received a watering, which is consistent with the results of Bauerle et al. (2008b), demonstrating that a plant of enhanced vigour has greater morphological plasticity in response to lateral heterogeneity in soil moisture, but similar tolerance to moisture stress as indicated by root survivorship in dry soil.
The hydraulic redistribution could not have been as high as it was in treatments PA2i-PBni, PA2i-PBniMe, PA2Me-PBni, PA2Me-PBniMe, since watering only once daily means less stock of water to redistribute to the roots of Planter B which received no irrigation. In this regard, Bauerle et al. (2008a) considered that the plants with a higher
level of hydric stress would have greater difficulty to rehydrate the dry tissue overnight. This could explain the lower root mass in Planter B, equivalent to the root mass in Planter B from treatments PA2iMe-PBni and PA2iMe-PBniMe, which also would have received less water due to the nematode infection in Planter A.
The effect of M. ethiopica in the root quality of this group of treatments is less drastic than in treatments PA2i-PBni, PA2i-PBniMe, PA2iMe-PBni and PA2iMe-PBniMe, the water conditions based on irrigation performed only once per day in Planter A, disadvantaged the nematode, preventing expression of a higher level of damage as seen in the treatments with the highest frequency of irrigation in Planter A. The more frequent irrigation facilitates movement and host location by M. ethiopica (Magunacelaya, 2009; Magunacelaya & Dagnino, 1999, Van Gundy et al., 1967).
Comparison of the quality of roots of Planter B from treatments PA1i-PBni and PA1i-PBniMe shows that the presence of M. ethiopica in the Planter B resulted in significant increase in the quality of the root in the Planter B; this observation warrants further studies to explain the link between partial irrigation and the effect of the nematodes.
In treatment PA1iMe-PBniMe, with both planters infected with M. ethiopica, a greater weight of concentrated roots was obtained in Planter A; however, the other measurements indicate that it was not a vigorous root. The combination of high weight and low quality in Planter A of treatment PA1iMe-PBniMe could be explained by a combination of the effects of a lack of water in the Planter B, and the stimulated root growth in the areas with access to water (Bauerle et al., 2008b) and the infestation with M. ethiopica that caused an increase in the root's weight (Magunacelaya & Dagnino, 1999). In this treatment, in addition to the increased weight in Planter A, the lowest pruning weight of the plant of all treatments was obtained.
Treatments in which Planters A and B were irrigated once a day (PA1i-PB1i, PA1iMe-PB1i, PA1iMe-PB1iMe). Statistically, M. ethiopica did not affect the results of the quality and weight of the roots, which proves the hypothesis that the damage caused by M. ethiopica is greater when part of the root system is in the non-irrigated soil. When the entire root system with access to water does not tend to be concentrated in one place and roots can be more widespread and reach more nutrients (Keller, 2005), the nematodes may also be dispersed in the roots and not concentrated in the damaged part. In the treatments, in that part of the root system that was not watered, the infection was more damaging
in the roots that were only absorbing water. The total mass of the root system obtained in these treatments is less than that of the partial irrigation treatment PA1i-PBniMe, which indicates that when part of the root system is in the non-irrigated soil, the root grows more, possibly due to the lack of water detected by the non-irrigated roots that stimulates root growth (Barceló Coll et al., 1990; Waisel et al., 2003; Bauerle et al., 2008b).
Aerial part weight. Although no statistically significant differences were demonstrated, one can predict that the root condition would eventually be expressed in the aerial part of the plant if the study had lasted longer. The aerial part of plant is an expression of the functionality of root, it is known that if the roots have difficulty absorbing water and nutrients, a lower pruning weight is produced (Gregory, 2006) and if a water deficit induces the production of ABA, this will reduce growth of the aerial part of plant (Barceló Coll et al., 1990; Waisel et al., 2003; Shellie, 2006) favouring the root (Azcon-Bieto & Talón, 2000; Taiz & Zeiger, 2002; Waisel et al., 2003). In the case where the plant is infected with M. ethiopica, it will diminish aerial growth (Magunacelaya & Dagnino, 1999). Dry & Loveys (1999) have shown that in drying part of root, leaving one part very well irrigated so that the hydric state of the buds are not altered, the vegetative growth is reduced significantly and the stomatic conductivity changes. Based on these precedents, one can expect that if the treatments had been for several seasons, differences in root condition between treatments eventually would be presented in the weight of aerial part.
The risk of phytosanitary problems using the drip irrigation system is higher than when watered in the traditional fashion, by irrigation trenches or by flood irrigation. The risk is by providing water when it is unnecessary, thereby affecting the activity of the roots. The highest quality and weight of roots is obtained by leaving a portion of the soil without watering, compared to when the entire root zone is irrigated, possibly because partial irrigation takes advantage of the mechanisms to stimulate plant root growth (Barceló Coll et al., 1990; Waisel et al., 2003; Bauerle et al., 2008b). It is important that the irrigated zone has good aeration so as to allow growth of the roots.
However, when M. ethiopica is added to the system, permanent partial irrigation becomes a less attractive option, since the quality and weight of roots is decreased significantly compared with a full watering of the root zone is performed. These latter conditions can be found in the vineyards irrigated with drip irrigation during a dry season, which could
better protect the roots of the plant from a parasitic nematodes attack by applying a homogeneous irrigation to wet the entire root zone. The nematode generates more damage when found in soil that receives more frequent irrigation, given that the nematode is favoured by the constant presence of water in the soil (Magunacelaya & Dagnino, 1999; Fujimoto et al., 2010; Reynolds et al., 2011, Mohawesh & Karajeh, 2014); thus, to decrease the level of nematode damage, irrigation should be conducted less frequently to allow good root production. When a root section is infected with M. ethiopica, the quality and weight of the entire root system can be jeopardised, including the roots of the plant that are not within reach of nematodes.
Roots that are more frequently watered may maintain parts of the root system that is in a non-irrigated zone, thus producing higher quality and root weight through hydraulic redistribution (Bauerle et al., 2008a). These roots can be crucial for the plant, which allows them to use soil nutrients more effectively (Caldwell et al., 1998). However, M. ethiopica drastically reduces the ability of plants to maintain root growth in dry areas, so infested vineyards should seek to irrigate the maximum volume of the soil as possible.
REFERENCES
Aballay, E., Ordenes, P., Martensson, A. & Persson, P. 2013. Effects of rhizobacteria on parasitism by Meloidogyne ethiopica on grapevines. European Journal of Plant Pathology 135: 137-145. Aydinli, G., Mennan, S., Devran, Z., Sirca, S. & Urek, G. 2013. First report of the root-knot nematode Meloidogyne ethiopica on tomato and cucumber in Turkey. Plant Disease 97: 1262. Azcon-bieto, J. & Talón, M. 2000. Fundamentos de Fisiología Vegetal. Spain, McGraw-Hill Interamericana. 522 pp. Barceló Coll, J., Nicolás Rodrigo, G., Sabater García, B. & Sánchez Tamés, R. 1990. Fisiología Vegetal. Spain, Ediciones Pirámide. 662 pp. Bauerle, T.L., Richards, J.H., Smart, D.R. & Eissenstat, D.M. 2008a. Importance of internal hydraulic redistribution for prolonging the lifespan of roots on dry soil. Plant, Cell & Environment 31: 177-186. Bauerle, T.L., Smart, D.R., Bauerle, W.L., Stockert, C. & Eissenstat, D.M. 2008b. Root foraging in response to heterogeneous soil moisture in two grapevines that differ in potential growth rate. New Phytologist 79: 857-866. Bayala, J., Heng, L.K., van Noordwijk, M. & Ouedraogo, S.J. 2008. Hydraulic redistribution study in two native tree species of agroforestry
parklands of West African dry savanna. Acta Oecologica 34: 370-378.
Caillaud, M.C., Dubreuil, G., Quentin, M., Perfus-Barbeoch, L., Lecomte, P., de Almeida Engler, J., Abad, P., Rosso, M.N. & Favery, B. 2008. Root-knot nematodes manipulate plant cell functions during a compatible interaction. Journal of Plant Physiology 165: 104-113.
Caldwell, M.M., Dawson, T.E. & Richards, J.H. 1998. Hydraulic lift: consequences of water efflux
from the roots of plants. Oecologia 113: 151-161.
Carneiro, R.M.D.G., Gomes, C.B., Almeida, M.R.A., Gomes, A.C.M.M. & Martins, I. 2003. Primeiro registro de Meloidogyne ethiopica Whitehead 1968, em plantas de quivi no Brasil e reagao de diferentes plantas hospedeiras. Nematologia Brasileira 27: 151-158.
Carneiro, R., Almeida, M., Cofcewicz, E., Magunacelaya, J.C. & Aballay, E. 2007. Meloidogyne ethiopica, a major root-knot nematode parasiting Vitis vinifera, other crops in Chile. Nematology 9: 635-641.
Conceiqao, I. L., Tzortzakakis, E., Gomes, P., Abrantes, I. & da Cunha, M.J. 2012. Detection of the root-knot nematode Meloidogyne ethiopica in Greece. European Journal of Plant Pathology 134: 451-457.
Dalmasso, A., Castagnone-Sereno, P. & Abad, P. 1992. seminar: tolerance and resistance of plants to nematodes - knowledge, needs and prospects. Nematologica 38: 466-472.
Domec, J.C., Warren, J.M., Meinzer, F.C., Brooks, J.R. & Coulombe, R. 2004. Native root xylem embolism and stomatal closure in stands of Douglas-fir and ponderosa pine: mitigation by hydraulic redistribution. Oecologia 141: 7-16.
Dry, P.R. & Loveys, B.R. 1999. Grapevine shoot growth and stomatal conductance are reduced when part of the root system is dried. Vitis 38: 151-156.
Eissenstat, D.M., Whaley, E.L., Volder, A. & Wells, C.E. 1999. Recovery of citrus surface roots following prolonged exposure to dry soil. Journal of Experimental Botany 50: 1845-1854.
Fujimoto, T., Hasegawa, S., Otobe, K. & Mizukubo, T. 2010. The effect of soil water flow and soil properties on the motility of second-stage juveniles of the root-knot nematode (Meloidogyne incognita). Soil Biology and Biochemistry 42: 1065-1072.
Gregory, P. 2006. Plant Roots: their Growth, Activity, and Interaction with Soils. UK, Blackwell Publishing Ltd. 318 pp.
Hans-Holger, L. & White, J.C. 2008. Plant hydraulic lift of soil water - implications for crop production and land restoration. Plant and Soil 313: 1-17.
Howland, A.D., Skinkis, P.A., Wilson, J.H., Riga, E., Pinkerton, J.N., Schreider, R.P. & Zasada, I.A. 2015.
Impact of grapevine (Vitis vinifera) varieties on reproduction of the northern root-knot nematode (Meloidogyne hapla). Journal of Nematology 47: 141-147.
Jaraba, J., Rothrock, C.S., Kirkpatrick, T.L. & Brye, K.R. 2014. Soil texture influence on Meloidogyne incognita and Thielaviopsis basicola and their interaction on cotton. Plant Disease 98: 336-343.
Keller, M. 2005. Deficit irrigation, vine mineral nutrition. American Journal of Enolology Viticulture 56: 267-283.
Magunacelaya, J.C. 2009. Concepts in management of tree crops nematodes in fruit production systems. In: Integrated Management of Fruit Crops and Forest Nematodes (A. Ciancio & K.G. Mukerji Eds). pp 85100. Dordrecht, The Netherlands, Springer Science + Business Media B.V.
Magunacelaya, J.C. & Dagnino, E. 1999. Nematologia Agrícola en Chile (Serie Ciencias Agronómicas no. 2.). Chile, Universidad de Chile. 288 pp.
Magunacelaya, J.C., Pacheco, H. & Ahumada, M.T. 2005. Aspectos generales para el manejo de nemátodos fitoparásitos de importancia agrícola en viñedos de Chile. RedAgricola 8: 17-20.
Matzner, S.L. & Richards, J.H. 1996. Sagebrush (Artemisia tridentata Nutt.) roots maintain nutrient uptake capacity under water stress. Journal of Experimental Botany 47: 1045-1056.
McKenry, M.V. & Anwar, S.A. 2006. Nematode, grape rootstock interactions including an improved understanding of tolerance. Journal of Nematology 38: 312-318.
Mohawesh, O. & Karajeh, M. 2014. Effects of deficit irrigation on tomato and eggplant and their infection with the root-knot nematode under controlled environmental conditions. Archives of Agronomy and Soil Science 60: 1091-1102.
Murga-Gutierrez, S.N., Colagiero, M., Rosso, L.C., Finetti-Sialer, M.M. & Ciancio, A. 2012. Root-knot nematodes from Asparagus and associated biological antagonists in Peru. Nematropica 42: 57-62.
Prot, J.C. & Van Gundy, S.D. 1981. Effect of soil texture and the clay component on migration of Meloidogyne incognita second-stage juveniles. Journal of Nematology 13: 213-217.
Reynolds, A.M., Dutta, T.K., Curtis, R.H.C., Powers, S.J., Gaur, H.S. & Kerry, B.R. 2011. Chemotaxis can take plant-parasitic nematodes to the source of a chemo-attractant via the shortest possible routes. Journal Royal Society Interface 57: 568-577.
Richards, J.H. & Caldwell, M.M. 1987. Hydraulic lift: substantial nocturnal water transport between soil layers by Artemisia tridentata roots. Oecologia 73: 486-489.
Sharp, R.E., Wu, Y., Voetberg, G.S., Saab, I.N. & LeNoble, M.E. 1994. Confirmation that abscisic acid
accumulation is required for maize primary root elongation at low water potentials. Journal of Experimental Botany 45: 1743-1751.
Shellie, K.C. 2006. Vine and berry response of merlot (Vitis vinifera L.) to differential water stress. American Journal of Enology and Viticulture 57: 514-518.
Shin, H.S., Ki, K.K., Hijo, H.J., Shin, T.P., Choi, Y.H., Lee, J.J. & Park, H.C. 2007. Effect of partial root zone drying on Meloidogyne and Pratylenchus multiplication and their impact on grapevine. Economic and Information: Agriculture and Life Sciences Research 41: 25-31.
Stoll, M., Loveys, B. & Dry, P. 2000. Hormonal changes induced by partial root zone drying of irrigated grapevine. Journal of Experimental Botany 51: 1627-1634.
Strajnar, P., Sirca, S., Stare, B.G. & Urek, G. 2009. Characterization of the root-knot nematode, Meloidogyne ethiopica Whitehead, 1968, from Slovenia. Russian Journal of hematology 17: 135-142.
Taiz, L. & Zeiger, E. 2002. Plant Physiology. USA, Sinauer Associates Inc. 690 pp.
Trudgill, D.L. 1991. Resistance to and tolerance of plant-parasitic nematodes in plants. Annual Review of Phytopathology 29: 167-192.
Van Gundy, S.D., Bird, A.F. & Wallace, H.R. 1967. Aging and starvation in larvae of Meloidogyne javanica and Tylenchulus semipene trans. Phytopathology 57: 559-571.
Waisel, Y., Eshel, A. & Kafkafi, U. 2003. Plant Roots - the Hidden Half USA, Marcel Dekker Inc. 1136 pp.
Wallace, H.R. 1968. The dynamics of nematode movement. Annual Review of Phytopathology 6: 91-114.
Warren, J.M., Meinzer, F.C., Brooks, J.R., Domec, J.-C. & Coulombe, R. 2007. Hydraulic redistribution of soil water in two old growth coniferous forests: quantifying patterns, controls. New Phytologist 173: 753-765.
Williams, K., Caldwell, M.M. & Richards, J.H. 1993. The influence of shade and clouds on soil water potential: the buffered behavior of hydraulic lift. Plant and Soil 157: 83-95.
Zhang, J., Zhang, X. & Liang, J. 1995. Exudation rate and hydraulic conductivity of maize roots are enhanced by soil drying and abscisic acid treatment. New Phytologist 131: 329-336.
J.C. Magunacelaya, C. Ramírez and S. González-Bernal. Воздействие постоянного орошения части корневой зоны на развитие нематод Meloidogyne ethiopica на корнях Vitis vinifera с подвоем группы SO4.
Резюме. В Чили Meloidogyne ethiopica вызывает гибель растений винограда на плантациях с капельным орошением, если в сухой сезон часть корней остается в сухой почве. Вредоносность M. ethiopica на винограде оценивали в условиях постоянного орошения части корней. Были поставлены эксперименты с разделением корней одного растения между двумя емкостями с песчаной почвой. При этом, капельное орошение было подведено либо к обеим, либо лишь к одной емкости с почвой, в которые вносили или не вносили инвазионный материал M. ethiopica. После 6 месяцев оценивали и измеряли состояние и вес корней, а также размер надземной части растений. Постянное орошение части корневой зоны давало здоровые корни большего веса, однако орошение также усиливало вредоносный эффект, при наличии M. ethiopica в орошаемой почве. Показано, что Meloidogyne ethiopica снижает способность растений к сохранению здоровой корневой системы при недостатке влаги.
