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The Genetic Diversity of Strawberry Species, the Underutilized Gene Pool and the Need for Cultivars with New Quality and Agronomic Attributes

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Pedro Antonio Dávalos-González, Ramón Aguilar-García, Alejandro Rodríguez-Guillén and Alba Estela Jofre-y-Garfias

Submitted: November 29th, 2021 Reviewed: January 31st, 2022 Published: May 10th, 2022

DOI: 10.5772/intechopen.102962

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Strawberries Edited by Nesibe Ebru Kafkas

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Strawberries [Working Title]

Prof. Nesibe Ebru Yaşa Kafkas

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Abstract

The growing increase in global strawberry production and consumption has been spectacular during this century. In 2019, 396,401 ha were planted, and 8.9 million tons of fruit were produced globally, and more than 50% of that volume was in the subtropical climate. The problems and losses caused by diseases and pests are of global importance, particularly with root and crown diseases, the severity and spread of which has been magnified by the cancelation of certain soil fumigants, and by the susceptibility to one or more of the parasites of the group of cultivars currently planted. The use of the genetic reservoir available both in the cultivated species, as in the 26 wild species, is a formidable wealth of genes, partially collected, and characterized, which can be of fundamental importance to introduce new genetic combinations into modern commercial cultivars and to redesign them, so that they have a greater adaptation to stresses caused by biotic and abiotic factors, in addition to an important improvement in the nutraceutical quality of the fruit. This chapter documents the importance of this gene pool in the development of elite cultivars with these qualities.

Keywords

  • Fragaria spp.
  • resistance to biotic agents
  • resistance to abiotic agents
  • nutraceuticals
  • breeding

1. Introduction

Global strawberry production grew at a rate close to 5% per year in the first two decades of the twenty-first century. At the beginning of this century, 4.57 million tons were produced annually, on an area of 40,000 ha versus 8.9 million tons and 396,401 ha in 2019 [1]. The origin of the production was given as follows: Asia and America are the continents with the highest contribution, where, in decreasing order, China, USA, Mexico, Turkey and Egypt are the five largest producers in the world. The statistics of the last 40 years stand out several factors (1) The cultivation spread from 53 countries in 1980 to 77 in 2000 and 79 in 2019; (2) More than half of the current fruit production is in the subtropical climate; (3) Emerging countries such as: Turkey, Egypt and Morocco, became important production poles; and, (4) The high altitude tropics whose typical case is Mexico, showed its climatic benignity, which placed Mexico as the world’s leading producer of fresh strawberries in autumn-winter, a period in which there is a deficit in the global market.

Other factors that are changing the role in the production-demand binomial are the cancelation of methyl-bromide [2], the promotion of organic cultivation, the interest in developing cultivars rich in bioactive and nutraceutical compounds [3], and the increasing importance of day-neutral cultivars [4]. These global trends are changing the profile of the strawberry industry, ultimately creating new technological demands of all kinds, especially for the main component, which are cultivars. In a holistic context, broadening the genetic base for new attributes and the formation of elite cultivars could have a major impact on better use of water, fertilizers, and adaptation to various stresses such as: alkaline pH, excessive heat, tolerance to frost damage, etc., furthermore, to help mitigate and/or eliminate future demand for synthetic pesticides.

Developing elite genotypes will imply a greater exploration, collection, and characterization of wild strawberry germplasm to face global problems [5, 6], a deep scientific knowledge of the genetic complexities to use it, especially in the case of those with ploidy levels other than octoploid. Nevertheless, molecular biology is currently advancing rapidly, and must be an ally of classical improvement, to advance more quickly in the objective of enriching the genetic base of the crop and achieving the development of cultivars with new characteristics. This chapter will present a review of contemporary problems of this crop, the use of current genetic resources as the main strategy to design their management, the factors that affect the under-utilization of the genetic reservoir, the demands for elite cultivars, with genetic resistance to biotic and abiotic factors, and better nutraceutical qualities, and the limitations of this approach.

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2. Global context

The predominant plantation system in the subtropical environment is that developed by California, USA during the 20th century, it was adopted and/or adapted with certain variations in other countries from the equator to 42°latitude in both hemispheres [7]. Its technological support was the disinfection of soils with methyl-bromide + chloropicrin to eliminate soil diseases [8], the development of cultivars with high productivity and sensory quality of the fruit [9], and the optimization of the technological package for cultivation, fertigation, pest, disease and weed management practices [10]. The reproducibility of the previous production model, and the adoption of the macro-tunnel, located in Spain, Mexico, and other Mediterranean countries, among the largest producers of fresh strawberries.

When the use of methyl bromide ended in 2005 and 2015 in developed and developing countries, respectively, ended the relatively simple Era to eradicate biotic agents from the soil, since to date substitutes or alternatives are being investigated to replace it, being chemical, physical, microbiological agents, or a combination of them, that exerts action on a wide spectrum of biological entities [2].

Strawberries are grown in a wide variety of environments. In terms of latitude, it can be said that, from the equator to the polar zone [11], mainly in the northern hemisphere. Regarding altitude, from sea level to altitudes above 2000 meters above sea level [12]. These macroenvironments, with their different photoperiod, temperature, and rainfall regimes, as well as different pH and soil texture, are the genesis of an infinite series of microenvironments, and give rise to the so-called geographical and regional adaptation, a situation that affects cultivars. They can be adapted to a better or lesser degree to a certain environment [11].

The strawberry industry is experiencing a continuous varietal change. Except for China, where cultivars from Japan predominate [7], in the nine main strawberry producing countries, perhaps no more than 15 cultivars, generated by the Universities of California and Florida and, a few others from private companies are used. However, these genotypes share a close relationship since they descend from common or related parentals. Modern cultivars stand out for their productive qualities, good adaptation, and high sensory quality. The risky facet is associated with genetic uniformity and genetic erosion for traits that can confer tolerance and adaptation to biotic and abiotic factors, and their clonal spread, which is a risk of transmission of infectious agents.

The genetic vulnerability was shown since the end of the last century, both for nuclear genes [13] and for the cytoplasm [14] and becomes more valid in contemporary times, before the first signs of the globalization of phytosanitary problems of strawberry. During the twentieth century, biotic problems were caused by 20 pests, 108 diseases, and eight nematodes, in addition to five abiotic agents [15]. It was anticipated that others could arise [16] and this was the case in this century with Drosophila suzukii[17], and the diseases caused by Colletotrichumspp. [18], Fusarium oxysporumf. sp. fragariae, Macrophomina phaseolina, and probably Neopestalotiopsisspp.

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3. Global challenges

Based on the available information, experiences of classical genetic improvement for the development of cultivars tolerant or resistant to diseases, pests, abiotic factors and recently to improve the nutraceutical quality of the fruit, will be addressed. An important aspect is that, for each goal of incorporating tolerance or resistance to a certain problem, the required sequence is to search for sources of genetic resistance [19], or of the richness of nutraceutical compounds [3], and then transfer it to the new cultivars. The commercial strawberry is octoploid, and wild plant populations of the 26 species known to date are found in nature [20], including their ancestors, and the newly discovered F. emeiensis[21]. The availability and use of this genetic wealth in the formation of cultivars were derived from the international literature. The ease of use of these genes depends on the chromosomal level of the species, the nuclear and cytoplasmic genetic compatibility between them, the type of inheritance of the resistance (qualitative or quantitative) and the availability of an appropriate technique to identify the resistant individuals.

3.1 Disease resistance

The development of cultivars with tolerance or resistance to certain diseases has been an approach of limited use in strawberries. Root and crown diseases are the group of parasites that cause the most economic damage. In the last century and the current one, the presence of at least seven important diseases has been reported: Phytophthora fragariae, Verticilliumspp., Phytophthora cactorum[15]. In the latter, Colletotrichumspp. [18], Fusarium oxysporumf. sp. fragariaein Chile [22]; China [23]; Spain [24]; California, USA [25]; Iraq [26]; Serbia [27]; Turkey [28]; Iran [29]; Bangladesh [30]; Ecuador [31]; Macrophomina phaseolinain Florida, USA [32]; Israel [33]; California, USA [34]; Spain [35]; Argentina [36]; Iran [37]; Australia [38]; Chile [39]; Tunisia [40]; Italy [41]; and probably Neopestalotiopsisspp., emerging parasite whose presence has been reported in 17 countries during this century in Brazil [42], Egypt [43]; Morocco [44]; Spain [45]; Iran [46]; Vietnam [47]; Belgium [48]; Argentina [49]; India [50]; Korea [51]; Uruguay [52]; Italy [53]; Mexico [54]; China [55]; Ecuador [56]; Finland [57]; Taiwan [58], and that it could acquire global importance if the damage persists in future years. It is important to highlight that Colletotrichumspp. [59], Fusarium oxysporumf. sp. fragariae(FOF), Macrophomina phaseolina[60, 61, 62], and Neopestalotiopsisspp. [63, 64, 65] were reported since the twentieth century, but only FOF was important in Australia [66], Japan [67], Argentina [68], Korea [69], and Mexico [70].

Genetic resistance in strawberries has a history dating back to the last century, and valuable experiences that confirm the goodness of this strategy. In this sense, the United States Department of Agriculture, released a multitude of cultivars resistant to various races of P. fragariae, adapted to the cold climate of various countries in the world, whose commercial use and/or as sources of resistance, were used to obtain cultivars in other countries. The resistance genes used by the USDA were transferred from F. chiloensisclones Yaquina and Del Norte; and Fragariax ananassathrough the cultivars ‘Md 683’ and ‘Aberdeen’ (Table 1) [71, 72]. In populations of F. chiloensisfrom California, USA there is also resistance to this fungus [73, 74].

Disease-causing agentSpecies/resistance genesPloidy levelGenes used in cultivarsReferences
Phytophthora fragariaeF.x ananassa
Fragaria chiloensisOregon
F. chiloensisCalifornia
F. virginiana
8x
8x
8x
8x
Yes
Yes
Yes
Yes
[11, 71]
[11, 71]
[73, 74]
[11, 71]
Verticillium dahliaeF.x ananassa
F. chiloensisCalifornia
F. virginiana
F. vesca
F. nipponica
F. iinumae
8x
8x
8x
2x
2x
2x
Yes
?
?
No
No
No
[75, 77]
[76]
[77]
[77]
[77]
[77]
Phytophthora cactorumF.x ananassa
F. vesca
F. nilgerrensis
8x
2x
2x
Yes
No
No
[78, 79, 80, 81]
[82]
[82]
Colletotrichumspp.F.x ananassa
F. chiloensis
F. virginiana
8x
8x
8x
Yes
?
?
[83, 85]
[86, 87]
[86, 87]
Fusarium oxysporumf. sp. fragariaeF.x ananassa
F. chiloensisspp. pacifica
8x
8x
Yes
In progress
[69, 88, 89]
[89, 90]
Macrophomina phaseolinaFragariax ananassa8xYes[93, 94]
Botrytis cinereaF.x ananassa
Fragaria chiloensis ssp. chiloensisf. chiloensis
F. virginiana
Fragaria vesca ssp. bracteata
8x
8x
8x
2x
Yes
?
No
No
[95, 96]
[97]
[98]
[98]
Xanthomonas fragariaeF.x ananassa
F. virginiana
F. moschata
F. pentaphylla
F. vesca
F. nilgerrensis
8x
8x
6x
2x
2x
2x
Si
In progress
No
No
No
No
[99]
[99, 100]
[101, 102]
[101]
[102]
[102]
PodosphaeraaphanisF. x ananassa
F. virginianassps. Grayana and virginiana
8x
8x
Yes
?
[103]
[104]
Other foliar diseases*F. x ananassa
F. virginiana
F. viridis
F. pentaphylla
F. nilgerrensis
8x
8x
2x
2x
2x
Yes
No
No
No
No
[11]
[105]
[106]
[107]
[108]
VirusF.x ananassa
F. chiloensisssps. Lucida, and pacifica
8x
8x
Yes
Yes
[11, 109]
[73, 74, 90]

Table 1.

Sources of disease resistance in F. x ananassaand other species of wild strawberry.

Refer to Mycosphaerella fragariae and Diplocarpon earlianum.


Other diseases of the twentieth century that justified the development of resistant cultivars were Verticilliumspp., and P. cactorum. For the first disease, in the last century sources of genetic resistance were detected in Fragariax ananassa[75], and F. chiloensis[76], but more recent studies also found resistance in F. virginianaand three diploid species [77]. The same situation occurred for P. cactorum, where resistance genes have been tracked back in commercial cultivars from the USA and Germany [78, 79, 80, 81], and in two diploid species [82] (Table 1).

Root diseases that acquired global importance from the XXI century, have been the subject of research that allowed to strengthen the efforts made regionally during the twentieth century, such was the case of anthracnose. The disease can be caused by the species C. fragariae, (CF), C. gloesporioides(CG) and C. acutatum(CA), also affecting all organs, among them flower and fruit rot [18]. The following cultivars resistant to CF were developed: ‘Florida Belle’ [83]; to CF and CG ‘Treasure’ [84]; and resistant to CF and CA ‘Pelican’ [18] and at least one race of CG [85]; and resistant to CA, ‘Flavorfest’ [86]. Subsequent studies identified sources of resistance to CG in octoploid species [86, 87].

The same happened for FOF, resistant cultivars were detected in Korea [69], Japan [88]. Genetic resistance to FOF strains was detected in Mexico in cultivars from the United States and, also in F. chiloensisssp. pacifica[89, 90] (Figure 1). The ‘Ventana’ cv is FOF resistant in California, USA [91]. In Mexico, there are selections in an intermediate stage of advance, which carry genes from both the cultivated species and F. chiloensisfor resistance to FOF, adapted to the tropical high-altitude climate in Mexico [92] (Table 1; Figure 2). Recent investigations detected genotypes resistant to Macrophomina phaseolinain Australia and Egypt, although some are out of date cultivars [93, 94].

Figure 1.

Root system from clones ofFragaria chiloensisssp.pacificashowing different degrees of resistance, 60 days after being inoculated withfusarium oxysporumf. sp.fragariae.

Figure 2.

Comparison of an experimental clone carrying genes ofF. chiloensisresistant tofusarium oxysporumf. sp.fragariae, and the viral complex of Irapuato, Gto. (central furrow), and two susceptible genotypes (left and right furrows).

Other diseases that attack foliage, flower, and fruit, caused mainly by fungi and a bacterium, are documented in Table 1. The damage due to Botrytis cinereais globally important [15], and there have been detected although commercial cultivars are only moderately susceptible [95, 96], and apparently, the diversity and genetic variation for tolerance or resistance to the fungus is absent in the commercial species, which has been an impediment to develop tolerant cultivars. However, in this century sources of genetic resistance were identified in progenitor species of cultivated strawberry and in a diploid species [97, 98] (Table 1).

The case of the bacterium Xanthomonas fragariaeis quite similar to that of Botrytis, except that until recently resistance was detected in F. virginiana, since no sources of resistance were found in the commercial species [99, 100]. Additionally, evidence of immunity genes found in F. moschata[100, 101, 102], and resistance genes in the diploids F. nilgerrensisand F. vescaf. alba,and ‘Illa Martin’ and in the diploid F. pentaphylla[102], but not in F. nilgerrensis, F. daltoniana, F. iinumae, F. vesca, F. viridis, F. gracilis; F. nubicolaand F. orientalis[101].

For other foliage diseases such as powdery mildew [103, 104], Mycosphaerella fragariaeand Diplocarpon earliana[11, 105]; since the previous century, resistance genes were found in cultivated species and in F. virginiana, and tolerant or resistant cultivars were developed. Subsequently, knowledge has been enriched with the detection of resistance genes in other octoploid and diploid species [106, 107, 108] (Table 1).

A scientifically important and economically transcendental case, for the strawberry industry in California, during the twentieth century, was the practical demonstration that genetic tolerance was the best alternative to avoid economic losses, caused by the yellowing viral complex [109]. Around 1945, the University of California released the cultivars ‘Shasta’ and ‘Lassen’, tolerant to the viral complex. This event marked the beginning of the Era of the formation of cultivars with high yield potential and sensory quality of strawberry, adapted to the subtropical climate of California. The tolerance genes introduced in these cultivars were derived from a cultivar called ‘Ettersburg 121’, which had within its ancestors’ genes from Fragaria chiloensisof the central coast of California, USA (Table 1) [73, 74]. In Irapuato, Gto., Mexico, there are advanced clones with tolerance to the local viral complex, which carry genes of F. chiloensisssp. pacificafrom California USA, [92] (Figure 3).

Figure 3.

Comparison between a resistant clone (upper furrow), and a susceptible one to the viral complex present in Irapuato’s region.

3.2 Pest resistance

Pests of greatest global importance and causing major economic damage, are the two-spotted spider mite (Tetranychus urticae), lygus bug (L. lineolaris, L. hesperus) and possibly other genus of bugs, in addition to thrips (Frankliniella occidentalis). The aphid Chaetosiphonspp. is a pest that transmits at least five viruses and for that reason, it is also important [15].

The genetic improvement in strawberries for tolerance or resistance to some of these pests was almost null in the previous century, for several reasons. Partly because of the availability of synthetic pesticides, which at first allowed easy control. Also due to the technical difficulty, time invested and economic cost of maintaining a genetic improvement program to achieve this objective, and in another, because there was a lot of pressure to develop cultivars with high yield potential and good sensory quality, even if they were susceptible to the most important pests of the crop.

Despite this unfavorable environment, there were pioneering scientists in spider mite and aphid resistance research. By far, the two-spotted spider mite has always been the main pest of strawberries and for this reason, the first studies evaluated the reaction of cultivars of the time to the mite. Experience showed that it developed larger populations on certain genotypes, which confirmed the presence of genetic variation in the host, with various degrees of damage, from tolerant to susceptible [110].

A survey with a greater number of cultivars and clones of octoploid species, allowed us to locate sources of resistance in the cultivated species, in F. chiloensisfrom North America [111, 112] and from South America and in F. virginiana[113]. However, an important aspect was that in the wild clones of both octoploid species, a higher level of resistance was identified than in the cultivars. In addition, and very important, is that some F. chiloensisclones, that were resistant to the spider mite, were also resistant to the aphid C. fragaefolii, which is a vector of at least five economically important viruses (Table 2).

PestSpecies/resistance genesPloidy levelGenes used in cultivarsReferences
Tetranychus urticaeF.x ananassa
Fragaria chiloensisssps. Lucida, and pacifica
Fragaria chiloensis ssp. chiloensis
F. virginiana
8x
8x
8x
8x
Yes
No
No
No
[110]
[111, 112]
[112]
[113]
Chaetosiphon fragaefoliiF. chiloensis8x?[112]
Lygus spp.F.x ananassa8xYes[114]
Frankliniella occidentalisF. x ananassa8x?[115]
Drosophila suzukiiF. x ananassa
F. vesca
8x
2x
?
Yes
[17]

Table 2.

Sources of resistance to pests of global importance in F. x ananassaand other species of wild strawberry.

For the other pests of global importance, genetic variation is generally mentioned at the cultivar level, and this is the case of Lygusspp. [114] and Frankliniella occidentalis[115], although the information available for both pests is still very limited, and many aspects of the host–parasite relationship are unknown.

An outstanding case is a problem with the oriental fly Drosophila suzukii, a pest that has spread throughout the main strawberry-producing countries, which parasitizes other small fruits as well, in which the damage could be considered in the future. A study carried out in Germany, with octoploid and diploid genotypes, identified that in the diploid F. vescacertain clones had a low mosquito emergence [17] (Table 2).

3.3 Outstanding characters of adaptation and resistance to abiotic factors

In this section, a series of agronomic attributes are presented and discussed, which allow the plant a better adaptation to the environment and/or mitigate its adverse effect on it and eventually result in higher productivity and quality of the fruit and therefore are attributed with high economic importance.

Among the 11 listed attributes, those related to wide adaptation, low chilling requirements, resistance to low temperatures and versatility for different photoperiod regimes, have had primary importance with the evolution under cultivation of the octoploid strawberry and consequently with the already cited adaptation to environments as contrasting as the duration of the photoperiod, temperature regime, cold-chilling needs, rainfall, soil texture, etc. [11, 74, 116, 117, 118, 119, 120].

Previous characters present in one, or both, octoploid parental species of cultivated strawberry were surely transferred to it during the synthesis of both species in Europe in the seventeenth century, as well as with the introduction of these ancient European cultivars into the USA, and its numerous introgressions of F. chiloensisand F. virginianagenes, by amateur breeders in the United States during the eighteenth century, which originated a multitude of cultivars more rustic and adaptable to the environments of that country, where the availability at first of short-day cultivars, over the years and due to this introgression, originated long-day octoploid cultivars [11] and later, as explained below, the day-neutral cultivars. Other sources of cyclical flowering have been documented in F. virginiana[118, 119].

One of the classic examples of the impact on the strawberry industry is the incorporation of genes that confer the day-neutral character and allow continuous flowering in the subtropical environment. The original source of the day-neutral character was found in F. virginianassp. glauca,in a plant collected in Utah [74]. These genes were introduced through the cultivar ‘Shasta’ and by means of a carefully modified backcross program, after three cycles of crossing and selection, the first cultivars with the day-neutral trait were released in 1979. In contemporary times most day-neutral cultivars carry those genes transferred by Bringhurst [4, 9].

Resistance of the plant and its different organs to low temperatures is another attribute, which allows minimizing the damage with temperatures below 0°C and is crucial to mitigate the damage of these organs. In the tropical climate at altitudes above 1500 meters above sea level, temperatures below the mentioned threshold can cause large yield losses during autumn and winter in cultivation without a macro-tunnel. However, the fore effect is probably maximized by the sudden increase in temperature up to 25°C in three hours, so this wide thermal oscillation could be the cause of the damage to the plant, flower, and fruit. Among the genotypes sown in Mexico, it has been observed that the most susceptible to this thermal shock are the day-neutral cultivars of California, compared to the short-day cultivars of California and Florida, respectively.

There are reports about sources of resistance to low temperatures in the progenitor species of the cultivated strawberry [6, 11], and also in some diplo, tetra and hexaploid species, [11, 108, 117, 120] as can be seen in the summary of Table 3. This desirable quality could acquire more relevance as more strawberry is grown in the tropics, as macro trends in crop expansion suggest for the near future. The opposite character, which is resistant to high temperatures during summer, could be important in certain latitudes, although except for Darrow [11], there was only recently interest in this stress as a cause of inhibition of flowering in short-day and day-neutral cultivars, when daytime temperatures are around 26°C [4].

FactorSpecies/resistance genesPloidy levelGenes used in cultivarsReferences
Wide adaptationF. x ananassa
Fragaria chiloensis
F. vesca
8x
8x
2x
Yes
?
No
[11]
[116]
[117]
Low chilling requirementsF. chiloensisssps. Pacificaand lucida
Fragaria chiloensis ssp. chiloensis
F. virginiana
8x
8x
8x
Yes
Yes
?
[73]
[118]
[118]
Photoperiod responseF. virginiana
Day neutral (DN)
Other sources of DN
Short day and long day
F. chiloensisssps. Pacifica and. Lucida
F. vesca
8x
8x
8x
2x
Yes
In progress?
?
No
[74]
[4, 119]
[11]
[119]
Cold resistanceF. virginiana
F. chiloensisssp. chiloensisf. patagonica
F. moschata
F. orientalis
F. moupinensis
F. viridis
F. daltoniana
F. iinumae
F. nipponica
Fraxinus mandshurica
8x
8x
6x
4x
4x
2x
2x
2x
2x
2x
?
No
No
No
No
No
No
No
No
No
[11]
[6, 11]
[117]
[108, 117]
[117]
[117]
[11, 117]
[120]
[117]
[117]
Heat resistanceF. virginiana8x?[4, 11]
Drought resistanceF. chiloensisNorth America
F. chiloensisSouth America
F. virginiana
F. orientalis
8x
8x
8x
4x
?
?
?
No
[76]
[6]
[11]
[117]
Resistance to waterloggingF. viridis
F. nilgerrensis
F. pentaphylla
2x
2x
2x
No
No
No
[108]
[108]
[108]
Resistance to salinityF. chiloensisssps. Pacificaand lucida
F. chiloensisssp. chiloensis
8x
8x
Yes
¿
[76]
[6]
Resistance to alkaline pHF.x ananassa
F. virginiana
F. chiloensis
F. viridis
8x
8x
8x
2x
Yes
?
?
No
[11]
[117]
[117]
[117]
Iron deficiency resistanceF. x ananassa
Fragaria chiloensis ssp. pacifica
8x
8x
Yes
In progress
[122]
[122, 123]
Low nutrient requirementsF. chiloensisssps. Chiloensis and pacifica8xNo[74, 124]

Table 3.

Genetic diversity for traits associated with abiotic factors of global importance in F. x ananassaand other species of wild strawberry.

Adaptation to deficits and excesses of moisture is documented for some strawberry species [6, 11, 108, 117, 121] (Table 3), and considering the current and future growing environments, both characteristics can be valuable, particularly a gradient related to the efficient use of water, or in other words, cultivars that require the fewer amount of water per kg of fruit produced, since most of the strawberries are grown under irrigation, and this is an input whose availability for agricultural use is less and less.

Other qualities that are found in wild species and are of great economic and environmental importance are those related to resistance to alkaline pH, salinity, and efficient use of iron in those soils [6, 11, 117]. In many of the countries where strawberries are grown, there are problems of iron deficiencies (Figure 4), induced by the alkaline pH of the soils, a problem that is partially solved with the application of iron in different forms. It has been observed that there is genetic variation for the efficient use of iron by certain cultivars and octoploid species of strawberry [122, 123], but unfortunately, on many occasions, there are no genotypes available that have this quality and are also adapted and productive to cultivation environments, where these nutritional deficiencies are manifested [122] (Figure 5).

Figure 4.

Iron deficiency in a commercial plantation planted in soil with alkaline pH in Irapuato, Gto., Mexico.

Figure 5.

Clones with genes ofFragaria chiloensisresistant to iron deficiencies planted in an alkaline pH soil of Irapuato, Gto., Mexico.

On the other hand, non-renewable inputs such as the use of synthetic fertilizers, could be better used by incorporating in modern cultivars the genes that confer a more efficient use of them, qualities present in certain wild species [73, 124, 125] and that until now have not been used (Table 3).

3.4 Characters associated with sensory and nutraceutical quality

Strawberry has a long history of genetic improvement for traits associated with the sensory quality of the fruit. Certainly, since ancient times, the aborigines of the new world [12, 120, 125, 126], practiced selection for some organoleptic characteristics such as fruit weight, color, firmness and flavor, outstanding attributes that have been reported in the landrace’s varieties of Chile [124, 125, 126, 127]. These qualities, which are under genetic control, have been incorporated into commercial cultivars of F.xananassa. The large fruit size and firmness undoubtedly came from F. chiloensisssp. chiloensisf. chiloensis[11]. Clones with large fruit have been identified in other species such as F. daltonianaand F. nilgerrensis[11, 117]. The firmness of fruit, which is a highly appreciated quality in strawberries, derived from F. chiloensis[125, 126] has also been found in certain diploid species [107, 117] (Table 4).

CharacterSpeciesPloidy levelUsed genes in cultivarsReferences
Big fruitFragaria chiloensis
F. daltoniana
F. nilgerrensis
8x
2x
2x
Yes
No
No
[11]
[11, 117]
[11, 117]
Fruit firmnessFragaria chiloensis ssp. chiloensis
F. pentaphylla
F. viridis
8x
2x
2x
Yes
No
No
[124, 126]
[107]
[117]
Aromatic fruitF. moschata
F. nilgerrensis
F. viridis
6x
2x
2x
No
Yes
No
[11, 117]
[128]
[117]
Fruit color
Almost white to red
Unusual bright red
F. chiloensisssp. chiloensis
F. pentaphylla
8x
2x
Yes
No
[11]
[107]
High nutraceutical contentFragaria virginiana ssp. glauca
Fragaria chiloensis ssp. lucida(cyanidin)
F. vesca
8x
8x
2x
In process
No
No
[3]
[134]
[133]

Table 4.

Characteristics of sensory and nutraceutical qualities of strawberry in F.x ananassa, and other wild species of strawberry.

Color, flavor and aroma are attributes of the fruit that influence consumer acceptance [128]. The genetic diversity for these traits is partially documented. For example, for color it is possible to find a range of tones from albino to red in some species [11, 129, 130], the same happens with the flavor where outstands certain octoploids and diploids, while aroma F. moschatais recognized as a species that is above all [117] (Table 4).

Nutritional qualities of strawberries were documented since the previous century for the high content of vitamin C, as much or more than some citrus fruits, and Hansen and Waldo demonstrated in 1944 its genetic control in commercial strawberry cultivars [75]. Evaluations of California’s cultivars showed a range of 50 to 100 mg of vitamin C per 100 g fresh weight, with ‘Tufts’ standing out [131] (Table 4).

With the medical recognition of the benefits for human health of certain bioactive compounds such as flavonoids and polyphenols [132], in addition to the already known properties of vitamins and minerals, and with the confirmation that the strawberry belongs to the group of fruits with high content of these substances, its consumption increased and there was an interest in increasing the nutraceutical properties of strawberries, through genetic improvement [3].

Research groups of some prestigious institutions have identified some important compounds, their presence in cultivars [133], and certain cases, which are the strawberry species whose contents are higher and can be the appropriate genetic source for these traits to be transferred to new cultivars. For example, wild plants with a high content of cyanidin, a type of anthocyanin, that helps to reduce risks of type 2 diabetes, certain types of cancer and heart problems, were identified in F. chiloensis[134] (Table 4).

Diamanti et al. [3], identified certain wild clones of F. virginianassp. glaucawith high antioxidant content, and through interspecific hybridization, followed by three cycles of backcrosses, managed to recombine strawberry genotypes with high potential yield and with a higher content of anthocyanins, polyphenols and greater antioxidant capacity, than the cultivar ‘Romina’. This is a cutting-edge genetic improvement approach, since the results suggest that it is possible to reconcile in this particular case, a high biomass yield with a higher content of bioactive compounds.

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4. Expanding the use of the genetic pool

As a corollary of the information gathered from the available literature on the subject under discussion, it was evident that genetic improvement in strawberries was fundamentally aimed at increasing productivity, the sensory quality of strawberries, and adaptation to various environments [9], and in certain countries, there were also relevant experiences in the formation of varieties with resistance to root diseases [71, 135], foliar diseases [11] and to viral complexes [74]. Among the wide genetic diversity existing in the 26 species, only a part of the reservoir has been used, basically from Fragariax ananassa[11], infrequently, from other octoploid species [74136], and exceptionally, with a lower of ploidy level [128].

Several avant-garde approaches have been besought and applied to use the genetic richness of wild species, to expand the genetic base of cultivated strawberries. One is the use of synthetic octoploids to take advantage of the genes of different levels of ploidy and bring them to the octoploid level [137], another is to perform the synthesis of Fragariax ananassaagain, but using a select group of progenitors of both, F. chiloensisas well as F. virginiana, which have been chosen for many characters such as: yield, quality and resistance to adverse factors [4, 6, 105, 138], and one more, is to form synthetic decaploids to introduce the complete genome of both, octoploid and diploid species [128, 139]. The introgression of genes of octoploid species towards the cultivated one [74] has been practiced successfully and with economically impressive results, but its contribution to broadening the genetic base is minimal. The first three day-neutral cultivars released, contributed only 6.25% of F. virginianassp. glaucagenes.

The collected germplasm of F. chiloensis[117, 140, 141, 142, 143] and F. virginiana[142, 144, 145], are available in the gene banks of certain countries [140], they have been characterized for certain attributes of cyclic flowering [4, 146], horticultural [5], resistance to diseases [89], resistance to pests [111, 112, 147], and at the molecular level [148, 149, 150]. However, it is important to characterize them to deal with global problems like pests, diseases, adaptation, and tolerance to abiotic factors, as well as for their nutraceutical properties. Among the global problems that the strawberry industry is facing, the best cultivars are susceptible to the most important pests and diseases, and regarding genetics, it stands out that there is little information on the sources of resistance to pests. The same situation occurs, towards resistance to low temperatures and there is also a great deficit of information on the richness of nutraceuticals in wild species.

Researchers from Michigan University [4] evaluated 2500 F. virginianaclones and 6000 F. chiloensisclones collected in California, the Pacific coast of North America and Chile. Among them, 38 elite parents were identified, and used to synthesized populations of F.x ananassa. If this germplasm were available, it could be characterized and used to deal with the global problems mentioned. If no sources of resistance are found for all the problems mentioned, the collection of octoploid species should be expanded. The populations of F. chiloensisfrom Alaska, whose genotypes withstand temperatures of −10°C and whose usefulness for that purpose was mentioned last century [11].

Little documented is the gene pool in species other than the octoploid level. There are likely valuable genes of economic importance that do not exist in octoploid species, that are currently underutilized, and that could contribute to solve emerging problems in the strawberry industry. As an example, the immunity reported to Xanthomonas fragariae, in F. moschata[102], and also, about the resistance in F. pentaphylla[101], and F. vesca[102], for the probable tolerance to Drosophila suzukiiin F. vesca[17], to name just a few cases already published.

Under the above-mentioned needs, it is important to continue with the germplasm collections of Asian species [108, 151] since, to date, it is the region with the highest number of reported species, where all levels of ploidy are found, except the hexa and, octoploids. Due to the contrasting environments where they are found, and the molecular genetic diversity existing in regions such as Tibet [152]; the presence of genes for resistance to low temperatures is potentially suspected, and certain indications reinforce this hypothesis. Luo et al. [153] demonstrated the possibility of transferring resistance at low temperatures from a wild pentaploid parent from China. It is also possible that, in Chinese species, there is resistance to moisture deficits and excesses, and resistance to foliar diseases [102, 108]. Tetraploid species are particularly interesting and hypothetically important, since if there were genes for outstanding traits absent in the octoploids [154], their transfer to these in some evolutionarily related species would be relatively less genetically complicated [138]. There is a lack of knowledge of the degree of genetic affinity between the five tetraploid and octoploid species, for the use of the possible genetic richness of the tetraploids at the octoploid level. Classic breeding methods for crosses between species of the same and different ploidy levels have been widely described [11, 74, 75, 137, 139], and they should be surely complemented with recently developed biotechnological techniques [155].

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5. Conclusions

During the present century, except for explorations in China, strawberry germplasm collections have ceased. In attention to the serious phytosanitary problems of strawberries, international collaboration is important to take advantage of the germplasm collections and populations derived from them, deposited in different repositories, and characterize them for those cases of global problems. Simultaneously with the above, evaluation techniques must be developed to rigorously characterize the germplasm reaction and identify the sources of valuable genes.

Faced with the need to mitigate global phytosanitary problems, genetic resources must provide part of the solution, and use those underused genes to form more rustic strawberry genotypes for biotic and abiotic factors, and with better nutraceutical quality of the fruit.

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Acknowledgments

The authors acknowledge the generosity of Dr. R.S. Bringhurst (RIP) for donating the germplasm of F. chiloensisfor the detection of sources of genetic resistance to Fusarium oxysporumf. sp. Fragariae.

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Written By

Pedro Antonio Dávalos-González, Ramón Aguilar-García, Alejandro Rodríguez-Guillén and Alba Estela Jofre-y-Garfias

Submitted: November 29th, 2021 Reviewed: January 31st, 2022 Published: May 10th, 2022