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Introduction

The field elm (Ulmus minor) was formerly a major component of riparian forests and municipal planting in southern Europe. Valuable ornamental traits, adaptability to urban environments and simplicity of establishment and management are the notable features of this species. However, U. minor has virtually disappeared from urban landscaping due to the spread of the lethal Dutch elm disease (DED), which is caused by the pathogen Ophiostoma novo-ulmi ([2], [38]). The fungus is transmitted from diseased to healthy elms by elm bark beetles, in particular Scolytus scolytus and S. multistriatus, the two main vectors in southern Europe. Spray programmes to control insect vectors are now largely unacceptable. Systemic chemicals have proven too toxic for general use ([20], [22], [23]) and biological control treatments appear to be ineffective ([35], [42]). As a result, replanting efforts now focus on other tree genera.

From a genetic point of view, re-introducing elms into municipal landscaping appears to be both desirable and feasible. A genetic basis for disease resistance to DED has been established in Europe using native elm species and clones, especially in hybrid combinations between and within U. minor and U. pumila ([27], [25]). Ulmus pumila is not a European native and was probably introduced into Spain in the 16th century as an ornamental and into Italy in the 1930s to replace dying elms. Natural hybridization with U. minor trees in these countries has produced genetic introgression, leading to a complex taxonomy ([4]).

Screening has been used to identify European elms with low disease susceptibility ([29], [33], [36]). These studies have identified U. pumila individuals and U. minor × U. pumila hybrids with low susceptibility and rapid height growth. As ornamentals, however, U. pumila and U. minor × U. pumila have several features that compare unfavorably with U. minor, the species they are intended to replace. Excessively fine branching, excurrent habit, small leaves, branch brittleness and twig mortality are normally undesirable features in urban environmental planting ([11], [15]). The Spanish elm breeding programme has therefore begun a series of backcrosses using U. minor as the source of improved ornamental traits and U. minor × U. pumila as the source of disease resistance and rapid height growth. Fast growth is definitely a desirable trait for the common landscape use of trees in southern Europe. Delayed vegetative budburst is similarly desirable in areas with spring frosts or where early defoliating insects such as Euproctis chrysorrhoea cause considerable leaf damage. Flower and seed production are important characters to study in an F1 population, especially if successive breeding cycles are to be performed. Information on the incidence of elm bark beetles on crossings would allow breeders to rule out combinations that are most affected by this pest.

Phenotypic variation can be divided into two major components, one representing genetic factors and the other representing environmental influences or experimental errors (i.e., stochastic variation). Broad-sense heritability (H2) is the proportion of variance in a particular trait and population that is due to genetic components (Fig. 1). A common simplification in all genetic studies and models is to assume that all alleles and all genotypes act independently of each other. This type of model, known as an “additive model”, does not allow for dominant or recessive effects and gene × gene interactions, even though they are known to be numerous. Broad-sense heritability can be further divided into additive genetic components and gene × gene interaction components (Fig. 1). The contribution of additive genetic components is termed narrow-sense heritability (h2). In other words, h2 is the proportion of trait variance due to additive genetic factors, whereas H2 is the proportion of trait variance due to all the genetic effects ([5]). The difference between these two heritability parameters gives an estimate of the effect of interactions on a phenotype. If the difference is zero, it means there is no interaction and all phenotypic variations can be explained by additive components. A non-zero difference between the two heritability parameters suggests the role and degree of interaction effects on the phenotype ([1]). Heritability estimates of vegetative budburst, height growth and resistance to O. novo-ulmi have not previously been reported for a breeding population of U. minor and U. pumila elms. In this study it is hypothesized that heritability estimates of previous traits will be high enough to justify selection and breeding. The study was designed to estimate genetic variation and inheritance of U. minor and U. minor × U. pumila hybrids for budburst, growth and tolerance to O. novo-ulmi.

Fig. 1 - Components of phenotypic variation, including broad-sense heritability (H2) and narrow-sense heritability (h2).

Material and Methods

Plant material

Ten clones - eight Ulmus minor (m) and two U. minor × U. pumila (mp) hybrids - were used as parents for the mating design (Tab. 1). Each clone comprised one plant. Parents were randomly selected from the elm clone bank population at the Forest Breeding Center in Puerta de Hierro, Madrid (see Appendix 1). This bank includes more than 200 Iberian elm clones, obtained through vegetative (root cuttings) or sexual reproduction from elms selected in the countryside according to their good sanitary status, diversity (geographical, ecological and genetic) and distinctive ornamental traits. The 10 clones selected were characterized through isozyme markers before crossing ([4]).

Tab. 1 - Clones and number of controlled pollinated seedlings used in the partial diallel cross design. (m): Ulmus minor; (mp): U. minor × U. pumila; (-): controlled pollinated crosses not performed; (0): controlled pollination performed but no seedlings obtained.

Female Males
AL-AN1 (m) AL-JR1 (m) GR-AL3 (m) M-PZ3 (mp) SE-CT4 (m) VA-VV5 (mp) TO-AL1 (m) CC-VG2 (m) M-IN5 (m) V-JR1 (m)
AL-AN1 (m) - 6 15 17 9 - - - - -
AL-JR1 (m) - - 2 9 6 17 - - - -
GR-AL3 (m) - - - 17 20 22 15 - - -
M-PZ3 (mp) - - - - 29 23 6 11 - -
SE-CT4 (m) - - - - - 17 38 0 10 -
VA-VV5 (mp) - - - - - - 22 18 28 23
TO-AL1 (m) 5 - - - - - - 6 18 4
CC-VG2 (m) 0 0 - - - - - - 0 0
M-IN5 (m) 0 0 0 - - - - - - 0
V-JR1 (m) 0 0 0 0 - - - - - -

Selected clones were crossed in 2000 following a partial diallel cross design ([3]). Forty cross-combinations were planned (Tab. 1), but 13 failed to provide full-sib progeny (combinations marked “0” in Tab. 1) due to the presence of three previously undetected aborting U. minor individuals (CC-VG2, M-IN5 and V-JR1) ([18]). Pollination was conducted through traditional tree breeding techniques using greenhouse-forced pollen (Fig. 2a) and isolation bags on trees ([26]). When a clone was used as female parent, the flowers were chosen on different branches of the same tree and bagged separately. Pollen from one male parent was used to pollinate the flowers of one or two bagged branches. To protect seeds from birds, bags were not removed from the branches until mature seeds had been collected. Isolated flowers were pollinated by inserting a syringe into the bag (Fig. 2b), after checking pollen viability by fluorochromatic reaction ([10]). Flowers in each bag were pollinated twice when possible, allowing four to five days between pollinations.

Fig. 2 - Methods: (a) forced pollen sampling from greenhouse flowering twigs in February 2000; (b) controlled pollinations performed by insufflating pollen into isolation bags; (c) plantation of the experimental plot in March 2002; (d) tree growth assessment in October 2004; (e) artificial inoculations with Ophiostoma novo-ulmi in May 2005; (f) leaf wilting assessment in July 2005.

Results

At age five years, only 30 out of 491 seedlings (6.1%) and 10 out of 58 ramets (17.2%) produced flowers, accounting for 7.3% of total trees (Tab. 2). Two out of six U. minor × (U. minor × U. pumila) progenies included flowering trees (mean = 2.0%). However, all seven (U. minor × U. pumila) × U. minor progenies produced at least one flowering tree (mean = 10.2%). Approximately 14.2% of trees had trunk feeding grooves caused by elm bark beetles (Tab. 2).

Mean leaf wilting percentages (± SD) 15, 30, 60 and 120 dpi were 19 ± 20, 34 ± 25, 37 ± 26 and 33 ± 31, respectively. Because vegetative budburst on April 9 and wilting 60 dpi provided the highest F-ratio values in the ANOVAs (results not shown), these measurements were used for further statistical analyses. Means for vegetative budburst, annual height growth and disease response for progeny combinations differed at a probability of 99% for each trait (Tab. 2). Cross-pollinated families with VA-VV5 and M-PZ3 as female parent had the highest annual height growth rates. Lowest height growth occurred when SE-CT4 was female parent (Tab. 3). Height growth was greater when GR-AL3 and AL-JR1 were used as female rather than male parents (Tab. 3). Controlled pollinated families of U. minor showed fast growth when CC-VG2 was used as male parent and low susceptibility when M-IN5 was the male parent (Tab. 3). Most crosses resulted in progenies with similar traits to their parents or intermediate traits. However, AL-AN1 × GR-AL3 and AL-JR1 × GR-AL3 showed heterosis in annual height growth, and AL-AN1 × AL-JR1, M-PZ3 × TO-AL1, TO-AL1 × AL-AN1 and TO-AL1 × V-JR1 showed heterosis in resistance to O. novo-ulmi (Tab. 2). Several elm trees obtained from GR-AL3 × SE-CT4, M-PZ3 × CC-VG2 and VA-VV5 × M-IN5 crossings showed growth rates above 80 cm yr-1 and wilting levels under 20%. Some ramets were especially heterogeneous for certain traits, i.e., M-PZ3 for wilting and TO-AL1 for growth (Tab. 2).

Tab. 3 - Mean values of annual height growth and leaf wilting (60 days after inoculations with Ophiostoma novo-ulmi) of cross-pollinated families with different female and male parents. Within the same column, different letters indicate differences between means (P

Parent Families with a female parent Families with a male parent
Annual height growth (cm) Leaf wilting (%) Annual height growth (cm) Leaf wilting (%)
AL-AN1 (m) 40.7 a 35.9 bc 42.2 abcd 12.7 abc
AL-JR1 (m) 49.5 b 37.9 bc 37.3 a 16.3 abc
GR-AL3 (m) 47.8 b 19.1 a 37.3 a 29.7 abc
M-PZ3 (mp) 51.3 bc 22.0 a 48.1 bc 20.2 bc
SE-CT4 (m) 36.6 a 37.9 c 49.5 bc 25.0 a
VA-VV5 (mp) 57.2 c 19.7 a 47.4 bc 21.5 abc
TO-AL1 (m) 38.9 a 27.7 ab 39.4 a 26.4 c
CC-VG2 (m) - - 58.9 d 25.7 abc
M-IN5 (m) - - 49.9 bc 18.7 a
V-JR1 (m) - - 53.2 cd 17.8 ab

Ulmus minor ramets showed earlier mean vegetative budburst, lower mean height growth rates and higher mean wilting values than U. minor × U. pumila ramets (P ). Differences in traits between U. minor and U. minor × U. pumila open pollinated progenies were statistically significant only for leaf wilting, and U. minor × U. pumila was more resistant than U. minor (P ). A notable result of controlled pollinated seedlings was the leaf wilting values obtained depending on whether the male parent was U. minor or U. minor × U. pumila (21.5 and 30.6%, respectively). Resistance was higher when U. minor was used as male parent (P

Tab. 4 - Mean values of five traits measured on ramets and open pollinated progenies (op). Different letters indicate differences between means (P

Plant materiala No. trees Flowering trees (%) Beetle affected trees (%)b Vegetative budburstc Annual height growth (cm) Leaf wilting (%)d
m ramets 46 2.2 4.3 4.1 bc (1-5) 27.7 a (6-68) 46.4 d (5-100)
mp ramets 12 75.0 75.0 2.9 a (2-4) 73.3 d (36-102) 28.8 ab (0-70)
m op 52 5.7 17.3 4.5 bc (2-5) 45.3 bc (7-95) 38.0 cd (0-100)
mp op 26 3.8 3.8 4.2 bc (1-5) 50.5 bc (15-80) 22.9 ab (0-60)

Heritability estimates from the regression (Tab. 5) and analysis of variance (Tab. 6) methods ranged from 0.13 to 0.69 and 0.06 to 0.71, respectively. Disease resistance heritability values were higher when estimated 60 dpi than 15, 30 or 120 dpi (results not shown). Expected genetic gains for height by selection in progenies from the M-PZ3 × TO-AL1 and VA-VV5 × CC-VG2 cross-combinations would be 3.07 and 3.07 cm, respectively. Expected genetic gains to reduce leaf wilting by selection in progenies from the M-PZ3 × SE-CT4, VA-VV5 × M-IN5 and VA-VV5 × V-JR1 cross-combinations would be 7.16, 9.46 and 7.83%, respectively.

Tab. 5 - Heritability estimates (± SE) of Ulmus minor and U. pumila hybrids for vegetative budburst, height growth, and resistance to Ophiostoma novo-ulmi obtained from regression between ramets and open pollinated families, and between ramets and controlled pollinated families. (a): average values of two x and y clones were correlated to their respective x × y families.

Plant material Vegetative budburst Height growth Disease resistance
Ramets vs open pollinated families 0.38 ± 0.34 0.41 ± 0.32 0.13 ± 0.32
Ramets vs controlled pollinated families a 0.64 ± 0.18 0.69 ± 0.17 0.36 ± 0.35

Tab. 6 - Variance components and heritability estimates (± SE) in the broad (H2) and narrow (h2) sense of Ulmus minor and U. pumila hybrids for vegetative budburst, height growth, and resistance to Ophiostoma novo-ulmi. (a): the average number of seedlings for each family was assumed to be r = 8.

Variance components and heritability estimates Vegetative budburst Height growth Disease resistance
σ2g ± SE 0.0602 ± 0.0406 48.2 ± 26.7 81.3 ± 25.1
σ 2 e 0.9030 456.2 270.2
H2 single-plant basis ± SE 0.06 ± 0.04 0.10 ± 0.05 0.23 ± 0.07
H2 family mean basis ± SE 0.35 ± 0.23 0.46 ± 0.25 0.71 ± 0.22
σ2males ± SE 0.0366 ± 0.011 0.0 ± 3.8 9.1 ± 7.1
σ 2 females 0.0064 32.0 23.3
σ 2 males × females 0.0669 48.7 0.0
σ 2 add 0.0860 64.0 64.8
σ 2 dom 0.2676 194.8 0.0
σ 2 e 0.3504 47.5 412.1
h2 single-plant basis ± SE 0.12 ± 0.06 0.21 ± 0.05 0.14 ± 0.06
h2 family mean basis ± SE 0.22 ± 0.11 0.24 ± 0.06 0.56 ± 0.24

Annual height was phenotypically related to vegetative budburst, as budburst occurred earlier in seedlings with low rather than high growth rates (P = 0.0007 - Tab. 7). Wilting percentage was negatively related to early budburst (Prp = 0.44; P = 0.0042), percentage of flowering trees and vegetative budburst (rp = -0.53; P = 0.0004), and percentage of beetle affected-trees and annual height growth (rp = 0.60; P

Tab. 7 - Phenotypic correlations (above the diagonal) between traits assessed in Ulmus minor and U. minor × U. pumila controlled pollinated seedlings. (a): indicates significance at P

- Annual height growth Vegetative budburst Leaf wilting
Annual height growth x -0.26 a 0.06
Vegetative budburst - x -0.17 a
Leaf wilting - - x

Discussion

To our knowledge, this is the first study to report heritability values and non-additive genetic variances of vegetative budburst, height growth and resistance to O. novo-ulmi in a breeding population of elms. Although the breeding of DED resistant elms began in the Netherlands in 1928 and the United States in 1933 ([27]), little is known about inheritance of DED resistance in elms ([41]). Genetically based resistance of trees to other forest diseases, such as poplar leaf rust ([13]), birch rust ([9]), Armillaria root rot ([45]) and pitch canker ([43]), suggests that breeding trees for resistance is possible. In the Ulmus genus, the response of backcross hybrids of U. pumila, U. japonica and U. rubra hybrids to inoculation with O. novo-ulmi has been reported ([14], [15], [16]), although heritability values were not quantified. Within a U. minor population, narrow-sense heritability for wilting percentages was 0.54 ([41]). Heritability values reported here confirm the hypothesis that vegetative budburst, height growth and DED resistance are genetically controlled.

Our first assessments of height growth, vegetative budburst and disease resistance in the controlled pollinated progenies were based on plant means. The primary functions of heritability estimates on a single-plant basis are to predict genetic progress through phenotypic selection and provide the relative magnitude of the genetic basis of height growth, vegetative budburst and disease resistance. However, the selection of families is probably based on family means and therefore the appropriate heritability for predicting genetic gain is the ratio of the variance component due to families to total phenotypic variance among family means, i.e., family mean heritability.

The estimates of heritability for resistance reported here are probably conservative due to the moderate levels of wilting obtained. The cell density used in the inoculum, lower than the density generally used in resistance tests for breeding purposes (= 106 conidia ml-1 - [33], [36]), was chosen to avoid high mortality. If we had observed a wider range of wilt symptoms, the genetic variability would have been readily expressed and the heritability values would probably have been higher ([39], [12]). We acknowledge that the number of replicates should have been higher, but unfortunately some clones used for the diallel design, coded CC-VG2, M-IN5 and V-JR1 and later characterized as female-sterile trees ([17], [18]), provided no seeds.

Ulmus minor flushes earlier in spring than other European elms ([31]) and U. pumila flushes even earlier, at least in the conditions in Madrid. However, vegetative budburst occurred later in U. minor × U. pumila than in U. minor ramets. This finding must be considered with caution, as the U. minor × U. pumila sample was constituted by just one clone (M-PZ3). The late vegetative budburst in U. minor × U. pumila hybrids could be related to the fact that hybrid ramets have greater fruit production than U. minor ramets. In the clonal bank at Puerta de Hierro Forest Breeding Center, it was observed that vegetative budburst is generally delayed if elms have abundant samara production, probably because of the energy cost required for fruit production. The significant relation observed between the percentage of flowering and late vegetative budburst could support this hypothesis. This relation would prevent proper comparison of budburst values between elms at a different juvenile or adult stage.

The negative association between vegetative budburst date and plant height, confirming earlier studies ([16]), should be considered with caution. Low trees, with buds close to soil level, would be exposed to higher temperatures during the day due to soil irradiation and would therefore flush earlier than taller trees ([46]). Considering only trees taller than 1.5 m, unaffected by soil irradiation, the phenotypic relation between vegetative budburst and plant height is not significant (rp = 0.09; P > 0.1). Similar findings on the phenotypic relations between vegetative budburst and susceptibility to DED have been reported ([16], [7]). This relation seems to be independent of tree height, as the same calculation made for trees above 1.5 m still shows significance (rp = -0.15; P = 0.0061). Elms with early vegetative budburst could be more resistant because they may develop latewood earlier than elms with delayed budburst. Early latewood formation has been related to DED resistance ([30], [34]), as small diameter vessels and pits are thought to compartmentalize the disease better and be less vulnerable to cavitation than large diameter vessels and pits ([34], [21], [24]).

The high frequency of beetle feeding grooves in elms with U. minor × U. pumila as a parent may be related to the higher growth rates found in these individuals and not to their greater attractiveness to beetles. It would be interesting to test this hypothesis when all trees have reached larger size and maturity.

For most purposes, fast growth of elms is highly desirable ([11]). However, one difficulty of this is that fast-growing trees often show high susceptibility to O. novo-ulmi ([16], [37]), although this relation is not universal ([11], [36]), as confirmed here. Annual growth quantification of seedlings in the juvenile stage is sometimes erratic. Moderate growth in youth may be followed by subsequent fast growth, whereas fast growth in youth may later decline. Long-term field trials would be required to properly quantify this trait. Breeders should take advantage of height growth heterosis and select the most appropriate combination. Heterosis was observed in elm growth in crosses where U. glabra and U. wallichiana were used as parent trees ([11]), as height was 50% greater in progenies than in parents.

Response to DED varied significantly depending on whether U. minor × U. pumila was used as female or male parent. The higher resistance of (U. minor × U. pumila) × U. minor hybrids may result from using U. minor × U. pumila as female parent. This combination could contain more germplasm from U. pumila than U. minor × (U. minor × U. pumila), although this statement needs experimental support. The result obtained is of practical interest in breeding programmes because it provides information about the optimal choice for obtaining resistant progenies. As crosses are time-consuming, choosing the option of (U. minor × U. pumila) × U. minor rather than U. minor × (U. minor × U. pumila) would save both time and effort. Breeding strategies should therefore concentrate on combinations such as M-PZ3 × SE-CT4, VA-VV5 × TO-AL1, VA-VV5 × M-IN5 and VA-VV5 × V-JR1. The high genetic variation of height growth and disease response within some (U. minor × U. pumila) × U. minor combinations (e.g., VA-VV5 × TO-AL1) may be of great value in advanced stages of breeding. The timing of vegetative budburst should also be taken into account: in sites with a severe continental climate or a large population of defoliating insects, care must be taken with combinations that result in seedlings with early budburst.

In this study, it was possible to obtain satisfactory gains for the three traits assessed. Estimated gains for growth and tolerance to DED were promising and, as far as we know, they are probably the first to be reported in an elm population. Further re-selection of other elm trees for height and disease resistance will improve the existing population, allowing a considerable increase in the predicted gains.

Conclusions

Evidence on the effect of genes from U. pumila in terms of resistance to O. novo-ulmi is limited but encouraging. This species has frequently been used in European breeding programmes because of its greater DED resistance than U. minor. This study confirms the suitability of this practice. Resistance to O. novo-ulmi increased significantly as a function of increased amounts of U. pumila germplasm from the female parent, suggesting that DED resistance may be transmitted mainly by the mother. In (U. minor × U. pumila) × U. minor combinations, with U. pumila contributing approximately 25% to the germplasm, response to DED was sufficient to recommend this backcross for breeding purposes. DED resistance heritability estimates and genetic gains reported here indicate a high degree of additive genetic control and show that selection for DED resistance and rapid tree growth is effective.

Acknowledgments

This work is dedicated to Hans Heybroek, Lorenzo Mittempergher, Alberto Fagnani, Fabio Ferrini and Alberto Santini, who kindly shared their knowledge of elm breeding with AS, JCLA and LG. We thank Margarita Burón† for superb technical assistance, Christine Cahalan (University of Wales, Bangor) for help with the statistical analysis, Esther Merlo for a critical review, and Jane McGrath for language editing. Pictures (a) and (b) from Fig. 2 were taken by S. Dominguez and E. Martínez. AS was funded by the Regional Government of Extremadura Department of Education and Technology (Junta de Extremadura - Consejería de Educación y Tecnología) and the European Social Fund during a visit to C. Cahalan in Bangor. The study was funded by the Spanish Directorate-General of Rural Development and Forestry Policy, Ministry of Agriculture, Food and Environmental Affairs (Dirección General de Desarrollo Rural y Política Forestal, Ministerio de Agricultura, Alimentación y Medio Ambiente).

(1) Bloom JS, Ehrenreich IM, Loo W, Vo Lite TL, Kruglyak L (2013). Finding the sources of missing heritability in a yeast cross. Nature 494: 234-237.

(2) Brasier CM (2000). Intercontinental spread and continuing evolution of the Dutch elm disease pathogens. In “The Elms: Breeding, Conservation and Disease Management” (Dunn CP ed). Kluwer Academic Publishers, New York, NY, USA, pp. 61-72.

(3) Bridgewater F (1992). Mating designs. In: “Handbook of quantitative forest genetics” (Fins L, Friedman ST, Brotschol JV eds). Kluwer Academic Publisher, Dordrecht, The Netherlands, pp. 69-95.

(4) Cogolludo-Agustín MA, Agúndez D, Gil L (2000). Identification of native and hybrid elms in Spain using isozyme gene markers. Heredity 85: 157-166.

(5) Falconer DS, Mackay TFC (1996). Introduction to quantitative genetics. Longmann & co, London, UK, pp. 464. Gscholar

(6) Fehr WR (1987). Principles of cultivar development’theory and technique (vol. 1). Iowa State University Press, Ames, USA, pp. 539. Gscholar

(7) Ghelardini L, Santini A (2009). Avoidance by early flushing: a new perspective on Dutch elm disease research. iForest 2: 143-153.

(8) Hallauer AR, Miranda JB (1988). Quantitative genetics in maize breeding. Iowa State University Press, Ames, IA, USA, pp. 468. Gscholar

(9) Helander ML, Vuorinen P, Saikkonen K, Lappalainen J (1998). Evidence for resistance of mountain birch (Betula pubescens ssp. czerepanovii) to birch rust (Melampsoridium betulinum). Mycological Research 102: 63-66.

(10) Heslop-Harrison J, Heslop-Harrison Y (1970). Evaluation of pollen viability by enzymatically induced fluorescence: intracellular hydrolysis of fluorescein diacetate. Stain Technology 45: 115-120. - Online | Gscholar

(11) Heybroek HM (1957). Elm breeding in the Netherlands. Silvae Genetica 6: 112-117. Gscholar

(12) Le Cocq TL, Quiring D, Verrez A, Park YS (2005). Genetically based resistance of black spruce (Picea mariana) to the yellowheaded spruce sawfly (Pikonema alaskensis). Forest Ecology and Management 215: 84-90.

(13) Lefevre F, Pichot C, Pinon J. (1994). Intraspecific and interspecific inheritance of some components of the resistance to leaf rust (Melampsora-larici populina Kleb) in poplars. Theoretical and Applied Genetics 88: 501-507.

(14) Lester DT, Smalley EB (1972a). Response of backcross hybrids and three-species combinations of Ulmus pumila, Ulmus japonica, and U. rubra to inoculation with Ceratocystis ulmi. Phytopathology 62: 845-848.

(15) Lester DT, Smalley EB (1972b). Response of Ulmus pumila and Ulmus pumila × rubra hybrids to inoculation with Ceratocystis ulmi. Phytopathology 62: 848-852.

(16) Lester DT, Smalley EB (1972c). Variation in ornamental traits and disease resistance among crosses of Ulmus pumila, U. rubra, and putative natural hybrids. Silvae Genetica 21: 193-197. Online | Gscholar

(17) López-Almansa JC, Pannell JR, Gil L (2003). Female sterility in Ulmus minor (Ulmaceae): a hypothesis invoking the cost of sex in a clonal plant. American Journal of Botany 90: 603-609.

(18) López-Almansa JC, Yeung EC, Gil L (2004). Abortive seed development in Ulmus minor (Ulmaceae). Botanical Journal of the Linnean Society 145: 455-467.

(19) Martín JA, Solla A, Woodward S, Gil L (2005). FT-IR spectroscopy as a new method for evaluating host resistance in the Dutch elm disease complex. Tree Physiology 25: 1331-1338.

(20) Martín JA, Solla A, Domingues MR, Coimbra MA, Gil L (2008). Exogenous phenol increase resistance of Ulmus minor to Dutch elm disease through formation of suberin-like compounds on xylem tissues. Environmental and Experimental Botany 64: 97-104.

(21) Martín JA, Solla A, Esteban LG, de Palacios P, Gil L (2009). Bordered pit and ray morphology involvement in elm resistance to Ophiostoma novo-ulmi. Canadian Journal of Forest Research 39: 420-429.

(22) Martín JA, Solla A, Witzell J, Gil L, García-Vallejo MC (2010). Antifungal effect and reduction of Ulmus minor symptoms to Ophiostoma novo-ulmi by carvacrol and salicylic acid. European Journal of Plant Pathology 127: 21-32.

(23) Martín JA, Solla A, García-Vallejo MC, Gil L (2012). Chemical changes in Ulmus minor xylem tissue after salicylic acid or carvacrol treatments are associated with enhanced resistance to Ophiostoma novo-ulmi. Phytochemistry 83: 104-109.

(24) Martín JA, Solla A, Ruiz-Villar M, Gil L (2013). Vessel length and conductivity of Ulmus branches: ontogenetic changes and relation to resistance to Dutch elm disease. Trees 27: 1239-1248.

(25) Martín JA, Solla A, Venturas M, Collada C, Domínguez J, Miranda E, Fuentes P, Burón M, Iglesias S, Gil L (2014). Seven Ulmus minor clones tolerant to Ophiostoma novo-ulmi registered as forest reproductive material in Spain. iForest (early view): e1-e9.

(26) Mittempergher L, La Porta N (1991). Hybridization studies in the Eurasian species of elm (Ulmus spp.). Silvae Genetica 40: 237-243. Gscholar

(27) Mittempergher L, Santini A (2004). The history of elm breeding. Investigación Agraria: Sistemas y Recursos Forestales 13: 161-177. Online | Gscholar

(28) Nyquist WE (1991). Estimation of heritability and prediction of selection response in plant populations. Critical Reviews in Plant Sciences 10: 235-322.

(29) Pinon J, Husson C, Collin E (2005). Susceptibility of native French elm clones to Ophiostoma novo-ulmi. Annals of Forest Science 62: 689-696.

(30) Pope SA (1943). Some studies on the Dutch Elm Disease and the causal organism. Doctoral thesis, Cornell University, Ithaca, NY, USA, pp. 61. Gscholar

(31) Richens RH (1983). Elm. Cambridge University Press, Cambridge, UK, pp. 347. Online | Gscholar

(32) Santini A, Ghelardini L, Falusi M, Bohnens J, Buron M, Collin E, Solla A, Vanden Broeck A (2004). Vegetative budburst variability of European elms. Investigación Agraria: Sistemas y Recursos Forestales 13: 37-45. Online | Gscholar

(33) Santini A, Fagnani A, Ferrini F, Ghelardini L, Mittempergher L (2005). Variation among Italian and French elm clones in their response to Ophiostoma novo-ulmi inoculation. Forest Pathology 35: 183-193.

(34) Solla A, Gil L (2002). Influence of water stress on Dutch elm disease symptoms in Ulmus minor Miller. Canadian Journal of Botany 80: 810-817.

(35) Solla A, Gil L (2003). Evaluating Verticillium dahliae for biological control of Ophiostoma novo-ulmi in Ulmus minor. Plant Pathology 52: 579-585.

(36) Solla A, Bohnens J, Collin E, Diamandis S, Franke A, Gil L, Burón M, Santini A, Mittempergher L, Pinon J, Vanden Broek A (2005a). Screening European elms for resistance to Ophiostoma novo-ulmi. Forest Science 51: 134-141. Online | Gscholar

(37) Solla A, Martín JA, Ouellette G, Gil L (2005b). Influence of plant age on symptom development in Ulmus minor following inoculation by Ophiostoma novo-ulmi. Plant Disease 89: 1035-1040.

(38) Solla A, Dacasa MC, Nasmith C, Hubbes M, Gil L (2008). Analysis of Spanish populations of Ophiostoma ulmi and O. novo-ulmi using phenotypic characteristics and RAPD markers. Plant Pathology 57: 33-44.

(39) Strong DR, Larsson S, Gullberg U (1993). Heritability of host plant resistance to herbivory changes with gall midge density during an outbreak on willow. Evolution 47: 291-300.

(40) Tchernoff V (1965). Methods for screening and for the rapid selection of elms for resistance to Dutch elm disease. Acta Botanica Neerlandica 14: 409-452.

(41) Venturas M, López R, Martín JA, Gascó A, Gil L (2014). Heritability of Ulmus minor resistance to Dutch elm disease and its relationship to vessel size, but not to xylem vulnerability to drought. Plant Pathology 63: 500-509.

(42) Vivas M, Martín JA, Gil L, Solla A (2012a). Evaluating methyl jasmonate for induction of resistance to Fusarium oxysporum, F. circinatum and Ophiostoma novo-ulmi. Forest Systems 21: 289-299.

(43) Vivas M, Zas R, Solla A (2012b). Screening of Maritime pine (Pinus pinaster) for resistance to Fusarium circinatum, the causal agent of Pitch Canker disease. Forestry 25: 185-192.

(44) White TL, Adams WT, Neale DB (2007). Forest genetics. CABI Publications, Cambridge, MA, USA, pp. 682. Online | Gscholar

(45) Zas R, Solla A, Sampedro L (2007). Variography and kriging allow screening Pinus pinaster resistant to Armillaria ostoyae in field conditions. Forestry 80 (2): 201-209.

(46) Zürcher ER (1986). Sprossachsen-Ontogenie der Bergulme (Ulmus glabra Huds.), bei Normal- und Langtagbedingungen [Stem ontogeny of Wych elm (Ulmus glabra Huds.) under normal and long day conditions]. Vierteljahrsschrift der Naturforschenden Gesellschaft in Zürich 131: 235-294. Gscholar

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Abstract

Seedlings obtained by crossing Ulmus minor and U. minor × U. pumila clones were assessed for flowering, bark beetle damage, vegetative budburst, height growth and resistance to Ophiostoma novo-ulmi. Ramets and open pollinated seedlings obtained from the parent trees were assessed for the same traits. Most progenies had similar traits to their parents, but some presented heterosis in annual growth or resistance to O. novo-ulmi. Leaf wilting was significantly lower in progenies with U. minor × U. pumila rather than U. minor as female parent (21.5 and 30.6%, respectively; P<0.05). Resistance to O. novo-ulmi increased significantly as a function of increased amounts of U. pumila germplasm from the female parent, suggesting that resistance to Dutch elm disease is primarily transmitted from the mother. Budburst occurred earlier in seedlings with low rather than high growth rates (P=0.0007) and percentage of wilting was negatively related to early budburst (P<0.0001). Other phenotypic relations included percentage of flowering trees and annual height growth (rp=0.44; P=0.0042), percentage of flowering trees and vegetative budburst (rp=-0.53; P=0.0004) and percentage of beetle-affected trees and annual height growth (rp=0.60; P<0.0001). Heritability estimates obtained from the regression and variance components methods ranged from 0.06 ± 0.04 to 0.64 ± 0.18, 0.10 ± 0.05 to 0.69 ± 0.17, and 0.13 ± 0.32 to 0.71 ± 0.22 for budburst, growth and tolerance to O. novo-ulmi, respectively. Broad- and narrow-sense heritability values were higher when estimated 60 days post inoculation (dpi) than 15, 30 or 120 dpi. Heritability estimates and genetic gains reported indicate a high degree of additive genetic control and show the effectiveness of selection for Dutch elm disease resistance and rapid tree growth.

Details

Title
Genetic variation and heritability estimates of Ulmus minor and Ulmus pumila hybrids for budburst, growth and tolerance to Ophiostoma novo-ulmi
Author
Solla, Alejandro; López-Almansa, Juan Carlos; Martín, Juan A; Gil, Luis
Pages
422-430
Section
Research Articles
Publication year
2015
Publication date
2015
Publisher
The Italian Society of Silviculture and Forest Ecology (SISEF)
ISSN
19717458
Source type
Scholarly Journal
Language of publication
English
DOI
https://doi.org/10.3832/ifor1227-007
ProQuest document ID
2662017605
Copyright
© 2015. This work is licensed under https://creativecommons.org/licenses/by-nc/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.