Multiple Selection of Potato Cyst Nematode Globodera pallida Virulence on a Range of Potato Species. I. Serial Selection on Solanum-hybrids

A series of selection experiments on potato cyst nematode Globodera pallida, pathotype Pa1, tested the virulence response of the nematode to a range of resistant potato Solanum genotypes. Alleles conferring virulence against all four Solanum sources used in the study (i.e. Solanum vernei, S. multidissectum, S. sanctae-rosae and S. tuberosum ssp. andigena) were detected. Selection for multiple virulence against a combination of resistant sources resulted in the originally-selected virulence genes being retained or lost. The mechanism, or basis, of potato cyst nematode resistance differs between the Solanum species. The appropriate use of resistance cultivars produced from a range of Solanum-resistant species offers a management tool for controlling potato cyst nematode levels in infested land.     

Durability of Resistance to Globodera pallida I. Changes in Pathogenicity, Virulence, and Aggressiveness During Reproduction on Partially Resistant Potato Cultivars

ABSTRACT We studied changes in pathogenicity, virulence, and aggressiveness of Globodera pallida populations over time. As a measure for pathogenicity, the reproduction factor on a partially resistant host was used; for aggressiveness, the reproduction factor on a susceptible reference host was used; and, for virulence, the ratio pathogenicity/aggressiveness was used. The G. pallida populations were reared in a glasshouse for four generations on potato cultivars with different levels of resistance. The cultivar Elkana did not increase pathogenicity significantly, but the more resistant cultivars Karakter and Darwina did. This increase in pathogenicity was caused by an increase in virulence, whereas aggressiveness generally was not altered significantly. The increase in virulence appeared to be caused by an enhanced ability of eggs to develop into cysts, and not by an increase in egg production per new cyst. The observed changes in virulence could be predicted reasonably well by a simple numerical model. The rate of selection depended strongly on the nematode population. Rearing a mix of two different populations on a susceptible host decreased the virulence strongly, as predicted by the Hardy-Weinberg equilibrium, but increased the aggressiveness because of heterosis.     

Quantitative approach for the early detection of selection for virulence of Meloidogyne incognita on resistant tomato in plastic greenhouses

Resistant tomato cultivars are an important tool to control Meloidogyne spp., which cause the highest yield losses attributed to plant‐parasitic nematodes. However, the repeated cultivation of Mi resistant cultivars can select virulent populations. In the present study, the susceptible tomato cv. Durinta and the resistant cv. Monika were cultivated from March to July in a plastic greenhouse for 3 years to determine the maximum multiplication rate, maximum nematode density, equilibrium density, relative susceptibility and population growth rate of M. incognita; these were used as proxy indicators of virulence and yield losses. The values of population dynamics and growth rate on the resistant tomato increased year by year and were higher when it was repeatedly cultivated in the same plot compared to when it was alternated with the susceptible cultivar and the level of resistance decreased from very to moderately resistant. The relationship between the nematode density at transplanting (P_i) and the relative yield of tomato fitted to the Seinhorst damage model for susceptible, but not resistant, cultivars. The tolerance limit and the relative minimum yield were 2–4 J2 per 250 cm³ of soil and 0.44–0.48, respectively. The tomato yield did not differ between cultivars at low P_i, but it did at higher P_i values, at which the resistant yielded 50% more than the susceptible. This study demonstrates the utility of population dynamics parameters for the early detection of selection for virulence in Meloidogyne spp., and that three consecutive years were not sufficient to select for a completely virulent population.     

Effectiveness and profitability of the <Emphasis Type="Italic">Mi</Emphasis>-resistant tomatoes to control root-knot nematodes

Experiments were conducted to determine the effectiveness and profitability of the Mi-resistance gene in tomato in suppressing populations of Meloidogyne javanica in a plastic-house with a natural infestation of the nematode. Experiments were also conducted to test for virulence and durability of the resistance. Monika (Mi-gene resistant) and Durinta (susceptible) tomato cultivars were cropped for three consecutive seasons in non-fumigated or in soil fumigated with methyl bromide at 75 g m^–2 and at a cost of 2.44 euros m^–2. Nematode densities were determined at the beginning and end of each crop. Yield was assessed in eight plants per plot weekly for 6 weeks. The P_f/P_i values were 0.28 and 21.6 after three crops of resistant or susceptible cultivars, respectively. Growth of resistant as opposed to susceptible tomato cultivars in non-fumigated soil increased profits by 30,000 euros ha^–1. The resistant Monika in non-fumigated soil yielded similarly (P > 0.05) to the susceptible Durinta in methyl bromide fumigated soil but the resistant tomato provided a benefit of 8800 euros ha^–1 over the susceptible one because of the cost of fumigation. Selection for virulence did not occur, although the nematode population subjected to the resistant cultivar for three consecutive seasons produced four times more eggs than the population on the susceptible one. Such a difference was also shown when the resistant cultivar was subjected to high continuous inoculum pressure for 14 weeks. The Mi-resistance gene can be an effective and economic alternative to methyl bromide in plastic-houses infested with root-knot nematodes, but should be used in an integrated management context to preserve its durability and prevent the selection of virulent populations due to variability in isolate reproduction and environmental conditions.     

Relative susceptibilities of eleven potato cultivars and breeders' clones toGlobodera pallida pathotype Pa 3, with a discussion of the interpretation of data from pot experiments

Curves according to the equationPf=M (1-e ^–aPi/M ) fitted well to the relations according to Seinhorst's (1993) modelPf=y _e y _h M(1-e ^–aPi/M ) between initial egg densities of potato cyst nematodes (Globodera rostochiensis, G. pallida)Pi up to 5T _h (T _h =the tolerance limit of haulm weight) andPf at the end of the growing season (a=maximum rate of reproduction,M, M=different theoretical maximum egg densities). Variation of estimates ofM, due to variation of the parameters of the submodelsy _e andy _h for the effect of weight reduction of haulms (and, therefore, of roots) on cyst production and damage to root tissue on egg production, respectively, was small enough to be ignored relative to experimental error. Therefore, ratios of values ofM, determined in simultaneous pot experiments with different potato cultivars, are reliable measures of the relative host status of these cultivars at initial egg densitiesPi of these nematodes up to about 5T _h . Variation between potato cultivars of growth reduction and damage to root tissue by the nematodes reduces the reliability of ratios of rates of relative susceptibility of these cultivars.The ratios between the maximum rates of reproduction ofG. pallida, pathotype Pa 3, on 8 out of 9 cultivars and one breeder's clone of potatoes and this rate on the susceptible cvs Bintje and Irene (relative susceptibilitiesrs _a ) could be considered to be equal to the ratios of maximum population densitiesM on these cultivars (relative susceptibilitiesrs _M ) (relative susceptibilities independent of initial egg density). The latter ratios were 0.59 times the first (relative susceptibilities negatively correlated with initial egg density) in one cultivar and one breeder's clone. Relative susceptibilitiesrs _a andrs _M of the tested cultivars and breeders clones suggest the existence of continuous ranges of both relative susceptibilities between 0.50 and 0.15 with, in a great majority of cases,rs _a =rs _M .     

Selection of nematodes by resistant plants has implications for local adaptation and cross‐virulence

The variability of resistance durability in different potato genotypes harbouring the same resistance QTL but differing by their genetic background was explored. The indirect consequences of the resistance adaptation in terms of local (i.e. genotype‐specific) adaptation and cross‐virulence was also investigated. Following the virulence of the potato cyst nematode Globodera pallida in a long‐term experimental evolution protocol, the results showed that nematode populations were able to adapt to the resistance of four potato genotypes carrying the QTL GpaV from Solanum vernei, and that the plant genetic background has an impact upon the durability of resistance. The pattern of local adaptation observed here indicates that divergent selection has occurred during the experimental evolution performed from the same initial nematode population, and revealed a trade‐off between the adaptation to a resistant potato genotype and the adaptation to another resistant genotype differing in its genetic background. In terms of cross‐virulence between potato genotypes derived from different resistance sources (S. sparsipilum and S. spegazzinii), this study shows that the adaptation to resistance QTL GpaV_vrn does not necessarily allow the adaptation to collinear GpaV loci. The results presented here could be useful for predicting evolution of nematode populations in natural agro‐ecosystems and identifying durable strategies for resistance deployment.     

Consistent action of two partially effective loci conferring resistance to Globodera pallida Pa2/3 across multiple nematode field populations

The potato cyst nematodes (PCN) Globodera rostochiensis and Globodera pallida are significant pests of potatoes worldwide. The most effective control methods are crop rotation and the deployment of resistant varieties. Complete resistance to G. rostochiensis based on a single resistance gene has successfully been integrated into many varieties. However, resistance to G. pallida has not been as successful to date, with current varieties only exhibiting partial resistance. Combining partially effective quantitative trait loci (QTLs) for resistance can increase the strength and breadth of the resistance. An additive effect on resistance has previously been demonstrated on combining two QTLs from Solanum tuberosum subsp. andigena (GpaIV^s_adg) and Solanum vernei (Gpa5). However, populations of G. pallida can be quite divergent and it was unclear whether the relative effects of the individual QTLs and the combined additive effect would be consistent across different G. pallida Pa2/3 populations. Using a mapping population segregating for both QTLs, the effect of the QTLs individually and combined was examined on four UK‐derived field populations of G. pallida pathotype Pa2/3, and the relative effects of the individual QTLs and the additive effect of the combination found to be consistent across all populations.     

Selection for reproductive ability in Globodera pallida populations in relation to quantitative resistance from Solanum vernei and S. tuberosum ssp. andigena CPC2802

Four field populations of the nematode Globodera pallida were subjected to selection pressure for increased reproductive ability by rearing sub-populations continuously on four partially resistant potato genotypes for 12 generations. The resistance was derived from either Solanum vernei or from S. tuberosum spp. andigena CPC2802. After the 12th generation the original and sub-populations of nematodes were assessed for their reproductive ability on a susceptible genotype and on each of the partially resistant genotypes. Selection pressure was shown to have increased reproductive ability but the increases were specific to the source of resistance used. The average increase on the ex S. vernei clones was from 11% reproduction by the unselected populations to 35·5% reproduction after selection. On the clones derived from CPC2802, which had higher levels of resistance, the increases were larger with an average of 6·6% reproduction for the unselected but 47·4% reproduction after selection. The response to selection differed amongst the initial field populations with some rates of reproduction increased to as much as 79%. A RAPD based analysis of the original and sub-populations after selection indicated small but consistent changes in the genetic structure, which could have been a result of the selection pressure per se and/or the bottlenecks that the populations had gone though.     

Variability in infection and reproduction of Meloidogyne javanica on tomato rootstocks with the Mi resistance gene

The response of 10 commercial or experimental tomato rootstocks with the Mi resistance gene to an initial inoculum of a Mi‐avirulent population of Meloidogyne javanica was determined in pot tests conducted in spring and summer. In a field test, the rootstocks were subjected to continuous exposure to high initial population densities (2050 ± 900 second‐stage juveniles (J2) per 250 cm³ soil) of the nematode. The presence of the Mi locus in the resistant rootstocks and cultivars was confirmed using the PCR co‐dominant markers REX‐1 and Mi23. Nematode infectivity (egg masses) and reproduction (eggs g^?1 root) were highly variable in the spring tests. Rootstocks PG76, Gladiator and MKT‐410 consistently responded as highly resistant, with nematode multiplication rate (Pf/Pi) < 1 and reproduction index (RI) < 10%, and they were as efficient as standard resistant tomato cultivars at nematode suppression. The relative resistance levels of rootstocks Brigeor, 42851, 43965, Big Power and He‐Man varied depending on the susceptible standard used for reference or the duration of the test. Rootstocks Beaufort and Maxifort were susceptible to M. javanica (Pf/Pi > 50 and RI > 50%). Rootstocks PG76 and He‐Man, and the resistant tomato cv. Caramba showed high levels of resistance in the test conducted in summer, whereas MKT‐410 and 42851 and the resistant tomato cv. Monika were moderately resistant. In the field, seven rootstocks showed high levels of resistance and one (He‐Man) showed an intermediate level, whereas Beaufort and Maxifort were susceptible.     

Effect of Juglone on Active Oxygen Species and Antioxidant Enzymes in Susceptible and Partially Resistant Banana Cultivars to Black Leaf Streak Disease

The black leaf streak disease (BLSD), caused by Mycosphaerella fijiensis, is the most destructive disease of bananas and plantains around the world. Breeding for resistance is the most promising strategy to fight this disease especially in small farmer plantations. Mycosphaerella fijiensis produces many phytotoxins such as juglone, which can be used, jointly with field and inoculations under controlled conditions, for screening banana cultivars for BLSD-resistance. This non-host specific phytotoxin has been shown to act on chloroplasts and disturbs the proton electrochemical gradient across the plasmalemma membrane. Moreover, an involvement of the oxidative burst during the interaction has been suggested. The present study was carried out using two cultivars that differed for either their juglone-responses or their resistance to BLSD (cv. Grande Naine susceptible to BLSD and juglone and cv. Fougamou partially resistant to BLSD and highly tolerant to juglone). The production of active oxygen species (AOS) and the enhancement of the enzymatic and/or non-enzymatic AOS-scavenging systems were investigated after treatment of the two cultivars with juglone. The time-course of AOS-production and AOS-scavenging was shown to be the key difference between these two tested cultivars after treatment with juglone. Thus, an early release of AOS (O₂⁻ radical and H₂O₂) and a quick stimulation of a preferment anti-oxidant system (superoxide dismutases, catalases, and peroxidases) was observed for cv. Fougamou as compared to cv. Grande Naine for which a late and weak generation of AOS accompanied by a late stimulation of the anti-oxidant systems were detected.     

Seed-potato production of cultivars resistant to Globodera rostochiensis in Poland1

Changes in the production of Polish seed potatoes of cultivars that are resistant to potato cyst nematodes have been followed. Over the period from 1972 to 1998, 35 cultivars resistant to Globodera rostochiensis (pathotype RO₁) were introduced. Among them, one (Drop) was also resistant to Globodera pallida (PA₃) and a number had multiple resistance to diseases and nematodes. Planting of seed potatoes of these resistant cultivars concerned only 0.4% of the total potato area. Against a background of much reduced seed-potato production, the area planted with resistant cultivars fell by 47% over the years 1989/1997). However, the share of resistant cultivars in the total seed-potato area increased from 16% in 1989 to 47% in 1997, the most important cultivars being Lawina, Orlik, Ibis and Irga. In 1992/1993, resistant cultivars occupied only 6–8% of the total potato area.     

Development of Globodera rostochiensis pathotype Ro1 in resistant and susceptible cultivars of potato1

Studies on the development of Globodera rostochiensis in potato cultivars with different levels of resistance have shown that both males and females of the nematode complete their whole cycle of development in susceptible cv. Svitanok Kyivskii in 61 days. In resistant cv. Vodograi, only males complete their development. Development of females is interrupted at the third larval instar, and mature females do not appear.     

Characterization ofRhizoctonia solani isolates from potatoes in turkey and screening potato cultivars for resistance to AG-3 isolates

A total of 304Rhizoctonia solani isolates and 60 binucleateRhizoctonia-like fungi were recovered from stems and tubers of infected potato plants over a 2-yr period in northeast Turkey.R. solani isolates were identified to 11 anastomosis groups (AGs): AG-1 (0.66%), AG-2-1 (5.6%), AG-2-2 (0.99%), AG-3 (83.9%), AG-5 (4.6%), AG-6 (0.66%), AG-8 (1.32%), AG-9 (0.33%), AG-10 (1.32%), AG-12 (0.33%), and AG-13 (0.33%). In the greenhouse tests, most of the AG-3 isolates were significantly more virulent than isolates belonging to other AGs on potato cv. Batum. Isolates of other anastomosis groups differed in their virulence. Results indicated that AG-3 is an important pathogen on potatoes grown in the study area. Five of 22 commercial and local potato cultivars evaluated for their reaction toR. solani AG-3 isolates (TP-2) under greenhouse conditions were highly resistant; the remaining cultivars exhibited different levels of susceptibility to the pathogen isolate. http://www.phytoparasitica.org posting July 14, 2005.     

Breeding for viral resistance: conventional methods

Conventional breeding methods based primarily on the principles of Mendelian genetics have provided the basis for the majority of resistance to viruses in potato cultivars. This development of resistant cultivars has resulted from sexual hybridisation followed by selection of the best genetic recombinant. Selection is one of the most powerful tools available for crop improvement. Successful selection depends on reproducible genetic variability, ability to identify genetically superior individual plants or families, populations large enough to ensure the likely occurrence of rare genetic combinations, and the combination of resistance expression with commercial utility. Resistance to the major potato viruses namely potato virus A, potato virus M, potato virus S, potato virus X, potato virus Y and potato leafroll virus has been studied and selected for. A number of different types of resistance have been identified including (a) major gene resistance; (b) minor gene resistance; and (c) immunity. With the exception of potato leafroll virus, stable resistance to the other viruses has been achieved either singly or in combination in a range of potato cultivars. In addition for both potato leafroll virus and potato virus Y, the focus has been on the development of resistance to aphid transmission of the viruses.     

Resistance of some barley cultivars to leaf rust,Puccinia hordei; polygenic,partial resistance hidden by monogenic hypersensitivity

Three cultivars, all carrying the Pa7 gene for low infection type were crossed with ‘L94’, a cultivar assumed to carry no genes for partial resistance. The latent period (LP), the most important component determining partial resistance, was measured on 111 F₂ plants not carrying the Pa7 gene and on four cultivars representing the known range in LP. Of 20 F₃ lines the LP was evaluated, too. The F₂ showed a continuous segregation for LP from nearly as short as ‘L94’ to as long as ‘Vada’. This was substantiated by the F₃ data. The cultivars possessing the Pa7 gene are assumed to carry a series of minor genes, covered by Pa7, which govern a LP at least as long as that of ‘Vada’, a cultivar with a very high level of partial resistance and a long LP.     

Race distribution of Phytophthora sojae on soybean in Hyogo, Japan

Since 1987, Phytophthora root and stem rot of soybean [Glycine max (L.) Merr. cv. Tanbakuro], caused by Phytophthora sojae Kaufman and Gerdemann, has been increasing in the Sasayama, Nishiwaki, and Kasai regions in Hyogo, the most famous soybean (cv. Tanbakuro)-producing areas in Japan. In 2002 to 2004, 51 isolates (one from each field) of P. sojae were recovered from 51 fields in Hyogo. These isolates were tested for virulence on six Japanese differential soybean cultivars used for race determination in Japan, and three additional ones containing four Rps genes used in Indiana, USA. Race E was the most prevalent from 2002 to 2004, followed by races A, C, D, and four new races (proposed as races K, L, M, and N). Interestingly, none of the new races had high virulence on the Japanese differential cultivars, compared with other races in each area. One (race N) was avirulent on all six soybean differentials. There was a difference in race distribution on each of three individual areas; race E seemed to be a major component of the P. sojae population in Sasayama, whereas race A and the new race M were the most prevalent in Nishiwaki and Kasai, respectively. Rps6 (cv. Altona) and Rps1a + Rps7 (cv. Harosoy 63) were infected by 90.2% and 33.3% of all isolates, respectively. However, Rps1d (cv. PI103091) was not susceptible to any of the 51 isolates, nor was cv. Gedenshirazu-1. These two soybean cultivars were considered to be potential sources of resistance to breed new resistant cultivars with the desirable characteristics of cv. Tanbakuro for this region.     

Effects of different potato cultivars on life history and demographic parameters of Phthorimaea operculella Zeller (Lepidoptera: Gelechiidae)

Potato tuber worm, Phothorimae operculella Zeller (Lepidoptera: Gelechiidae) is a common pest of potato which causes a heavy loss in yield either in fields or storage. The effect of six potato cultivars (Agria, Florida, Impala, Picasso, Satina, and Sprint) were evaluated on the life history, life table and demographic parameters of P.operculella under laboratory conditions, which could be appropriate indices in resistance and susceptibility evaluation of potato cultivars. The longest development time was on Picasso (28.76 ± 0.36d) cultivar. The male longevity ranged from 4.83 ± 0.44d on Sprint to 7.45 ± 0.60d on Picasso. Impala and Satina with 53.22 ± 7.78 and 28.74 ± 3.54 eggs/individual had the highest and the lowest net reproductive rates (R₀). The highest values for the intrinsic rate of increase (r_m) and finite rate of increase (λ) were on Impala (r_m: 0.119 day^?1, λ: 1.75 day^?1), and the lowest value was on Sprint (r_m: 0.090 day^?1, λ: 1.01 day^?1). The results indicated that Sprint was the most resistant cultivar for the feeding of P.operculella, which could be useful in the development of integrated pest management programs for this pest.     

Photosynthesis,transpiration and plant growth characters of different potato cultivars at various densities of Globodera pallida

Plants of four potato (Solanum tuberosum L.) cultivars were grown in pots in a greenhouse at five densities ofGlobodera pallida between 0 and 300 eggs per gram of soil. Photosynthesis and transpiration of selected leaves were measured at 30, 37, 49 and 60 days after planting. Stem length was recorded at weekly intervals. Plants were harvested 70 days afteer planting and various plant variables were determined.At 30 days after planting, when second and third stage juveniles were present in roots, both photosynthesis and transpiration rates were severely reduced byG. pallida. In the course of time these effects became less pronounced. Water use efficiency was reduced byG. pallida between 30 and 49 days, but not at 60 days after planting. The results suggest independent effects ofG. pallida on stomatal opening and on photosynthesis reactions. There were no consistent differences among cultivars in the response of leaf gas exchange rates and water use efficiency to nematode infection. Reduction of photosynthesis byG. pallida appeared additive to photosynthesis reduction due to leaf senescence.Total dry weight was reduced by 60% at the highestG. pallida density. Weights of all plant organs were about proportionally affected. Shoot/root ratio was not affected and dry matter content was reduced. Stem length and leaf area were most strongly reduced during early stages of plant-nematode interaction. The number of leaves formed was only slightly reduced byG. pallida, but flowering was delayed or inhibited. Reduction of total dry weight correlated with reduction of both leaf area and photosynthesis rate. Leaf area reduction seems the main cause of reduction of dry matter production. Tolerance differences among cultivars were evident at 100 eggs per gram of soil only, where total dry weight of the intolerant partially resistant cv. Darwina was lower than that of the tolerant partially resistant cv. Elles and of the tolerant susceptible cv. Multa. The tolerance differences were not correlated with leaf photosynthesis and transpiration. Apparently these processes are not part of tolerance of plants.     

Components of resistance to late blight (Phytophthora infestans) in eight South AmericanSolanum species

Four components of partial resistance toPhytophthora infestans were measured after inoculation in the greenhouse and in the field ofSolanum arnezii x hondelmannii, S. berthaultii, S. circaeifolium, S. leptophyes, S. microdontum, S. sparsipilum, S. sucrense andS. vernei, and four hybrid progenies ofS. microdontum withS. tuberosum. The four components were infection efficiency, lesion growth rate, generation time and sporulation capacity. The results were compared with resistance ratings derived from field experiments, and with observations made on the potato cultivars Bintje, Bildstar, Libertas and Pimpernel. Genetic variation for all components was found, while the relative importance of the components of partial resistance appeared to vary between the species. InS. microdontum, generation time, infection efficiency and lesion growth rate, and inS. tuberosum infection efficiency, lesion growth rate and sporulation capacity appeared positively associated, but in other species no such association was found. A strong hypersensitive reaction, the expression of which appeared to depend on environmental conditions, was found inS. microdontum. ForS. berthaultii, infection efficiency appeared to be the main resistance component.Abbreviations ADPC area under the disease progress curve - IE infection efficiency - LGR lesion growth rate - GT generation time - SC sporulation capacity     

Plant resistance to aphid feeding: behavioral,physiological, genetic and molecular cues regulate aphid host selection and feeding

Aphids damage major world food and fiber crops through direct feeding and transmission of plant viruses. Fortunately, the development of many aphid‐resistant crop plants has provided both ecological and economic benefits to food production. Plant characters governing aphid host selection often dictate eventual plant resistance or susceptibility to aphid herbivory, and these phenotypic characters have been successfully used to map aphid resistance genes. Aphid resistance is often inherited as a dominant trait, but is also polygenic and inherited as recessive or incompletely dominant traits. Most aphid‐resistant cultivars exhibit constitutively expressed defenses, but some cultivars exhibit dramatic aphid‐induced responses, resulting in the overexpression of large ensembles of putative aphid resistance genes. Two aphid resistance genes have been cloned. Mi‐1.2, an NBS‐LRR gene from wild tomato, confers resistance to potato aphid and three Meloidogyne root‐knot nematode species, and Vat, an NBS‐LRR gene from melon, controls resistance to the cotton/melon aphid and to some viruses. Virulence to aphid resistance genes of plants occurs in 17 aphid species – more than half of all arthropod biotypes demonstrating virulence. The continual appearance of aphid virulence underscores the need to identify new sources of resistance of diverse sequence and function in order to delay or prevent biotype development. © 2013 Society of Chemical Industry