Regionally Adapted Model of an Ideal Malus × domestica Borkh Apple Variety for Industrial-Scale Cultivation in European Russia

: Apple is one of the most common fruit crops in the Russian fruit-growing industry, with huge varietal diversity and a vast cultivation area. The key regions for industrial-scale apple culti-vation are the Central, Central Chernozem, and North Caucasian Districts. The main disadvantage of the relevant apple cultivars, especially the ones intended for intensiﬁed horticultural practices, is their low resistance against abiotic stresses and the fruit’s low quality and poor marketable condition. In Russia, apple is a crop of strategic importance that


Introduction
Given favorable conditions for industrial-scale cultivation, apple production is highly profitable by agricultural standards.Globally, apples rank fifth among all harvested crops following grapes, citrus fruits, bananas, and coconuts.According to the FAOSTAT website, the total area harvested for apples across all continents in 2020 was 4622.37K ha, with 984.51 K ha in European countries, 3135.37 in Asian countries, 305.92 in America, 170.27 in Africa, and 26.3 k ha elsewhere.In Russia, apple is a fruit crop of strategic importance that is consistently included in the household food basket [1][2][3].China is the world leader in apple production, with an average production quantity of 40.5 million tons a year (47.58% of the world production).Russia is among the top ten apple-producing countries in the world (2.0 M tons) and is ranked eighth following China (40.5 M tons), the United States (4.6 M tons), Turkey (4.3 M tons), Poland (3.5 M tons), India (2.7 M tons), Italy (2.5 M tons), and Iran (2.2 M tons).In 2016, the harvested area for apples in Russia was 197.7 K ha.In recent years, it has increased by 8.18%, reaching 215.3 K ha in 2020-see Table 1 [1].Despite the vast varietal diversity exceeding 7500 [4][5][6], the market is still dominated by the finest cultivars that originated early in the late 20th century (Delicious, Golden Delicious, Granny Smith, Fuji, Gala, etc.).However, in recent decades, a global trend for varietal adjustment has emerged.Such varieties as Golden Delicious, Jonagold, and Idared are being superseded by Red Jonaprince, Ligol, Cripps Pink, Pinova, and new regionally adapted varieties (a regionally adapted variety is a variety whose multiple features are balanced in such a way as to show maximum efficiency, when cultivated under specific regional conditions) [5].
This gradual replacement of regionally adapted cultivars leads to a loss of genetic diversity and may complicate plant breeding in the future [7].
The first reference whole-genome sequence (WGS) of the Golden Delicious (GD) cultivar was performed in 2010.Of the 16.9-fold genome coverage, 26% was obtained from Sanger sequencing of paired reads, and the remaining 74% from a total of 454 were sequenced by the synthesis of paired and unpaired reads [8].These data covered only ~89% of the genome's non-repeated part and had a relatively short contig N50 length (16.7 kBp), making it difficult to apply these results in transcription analysis or wholegenome re-sequencing.The apple tree was the third fruit crop, after the papaia, whose genome was investigated.In 2016, Li X et al. [9] conducted additional studies of GD, which made it possible to refine approximately 90% of the genome.This enabled scientists from 27 research institutes working under the FruitBreedomics project to advance their study of the genetic control of a number of economically valuable traits, such as scab resistance, shelf life, juiciness, crunchiness, and hardness, taking into account GD's allelic diversity [10].Currently, the traits that have been studied most include resistance to scabs [11][12][13] and fire blight [14][15][16][17] and fruit quality [18][19][20][21][22].Most of the economically valuable traits, whose totality determines the value of a cultivar, are controlled by minor polygenes or oligogenes.On the other hand, the set of processes to stipulate the phenotypic manifestation of a trait is determined by gene-environment interaction [23], so when the environmental parameters alter due to the response of the organism in the form of a change in the spectra of gene products determining the same trait, the manifestations of the effects of this interaction increase or decrease [24][25][26][27][28].
The objective of the present study was to summarize the data on the phenotypic manifestations of economically valuable traits of the apple cultivars approved for use in the Russian Federation depending on the region of cultivation; to determine the parametric characteristics of the most valuable traits in the form of a model of an "ideal" regionally adapted industrial cultivar, and to identify the sources of the traits in the regions suitable for their production.

Results
A total of 496 apple varieties have been approved for use in 12 cultivation regions of the Russian Federation, identified based on climatic conditions; see Table 2.The varieties are divided into nine groups depending on their harvest maturity period: early summer, summer, late summer, early autumn, autumn, late autumn, early winter, winter, and late winter.Commercially relevant varieties for winter consumption amount to 34% of this varietal diversity [29].The North Caucasian, Central, and Central Chernozem Districts are the leaders in the number of released varieties [30].Geographically, these districts fall into the zone where the industrial-scale cultivation of apples with different harvest maturity periods is viable; see Figure 1.The State Register of Breeding Achievements Approved for Use (2022) currently includes 136 domestic and foreign apple cultivars approved for the North Caucasian District, with 88 of them added in the past decade, of which 53 are intended for winter consumption, 17 for autumn consumption, and 18 for summer consumption.The varietal diversity is regularly updated, but of the 33 cultivars added to the register for cultivation region 6 in the past two years, only five have been regionally adapted, including the Delishes Marii and Renet Platona late winter varieties and the Yunona late summer variety cultivated by the North Caucasian Federal Scientific Center of Horticulture, Viticulture, and Wine-Making (NCFSCHVW, Krasnodar); the Alla winter variety, being a product of a collaborative effort by the N.I.Vavilov All-Russian Institute of Plant Genetic Resources (VIR, St-Petersburg) and ZAO Plodovod; and the Medeya winter variety, cultivated by the Nikita Botanical Garden, National Scientific Center of the Russian Academy of Sciences (Crimea).At the same time, foreign varieties quite often demonstrate poor adaptation to the natural and climatic conditions of the North Caucasus.
A total of 123 cultivars have been approved for the Central Chernozem District; among these, 61% (76) are winter varieties, while autumn and summer varieties amount to 21% and 18%, respectively.In the past decade, 34 new apple cultivars have been added, with 22 of them intended for winter consumption, 8 for autumn consumption, and 4 for summer consumption.From 2020 to 2022, seven cultivars were added, including three   The Central District is among the leaders in the number of approved cultivars (104).Varieties intended for winter consumption (early winter, winter, and late winter) amount to 64% of the varietal diversity.In the past decade, 11 cultivars have been added (seven of them regionally adapted), with five of them intended for winter consumption, four for autumn consumption, and two for summer consumption.Moreover, 55% of the apple cultivars (e.g., Desertnoe Kichiny late summer and Chekhovskoe late winter varieties) were cultivated by the Federal Horticultural Center for Breeding, Agrotechnology and Nursery (Moscow).
The stricter requirements of producers for new varieties pave the way for more extensive and strenuous breeding projects.New breeding achievements are expected to outperform their predecessors in yield per plant, resistance against abiotic and biotic stresses, and fruit quality, as well as show strong competitiveness and a more rapid return on investment [31 -34].There are over 100 breeding programs in progress around the world to develop promising apple cultivars [35], which would be essentially impossible without The Central District is among the leaders in the number of approved cultivars (104).Varieties intended for winter consumption (early winter, winter, and late winter) amount to 64% of the varietal diversity.In the past decade, 11 cultivars have been added (seven of them regionally adapted), with five of them intended for winter consumption, four for autumn consumption, and two for summer consumption.Moreover, 55% of the apple cultivars (e.g., Desertnoe Kichiny late summer and Chekhovskoe late winter varieties) were cultivated by the Federal Horticultural Center for Breeding, Agrotechnology and Nursery (Moscow).
The stricter requirements of producers for new varieties pave the way for more extensive and strenuous breeding projects.New breeding achievements are expected to outperform their predecessors in yield per plant, resistance against abiotic and biotic stresses, and fruit quality, as well as show strong competitiveness and a more rapid return on investment [31][32][33][34].There are over 100 breeding programs in progress around the world to develop promising apple cultivars [35], which would be essentially impossible without visualizing the end result in the form of an ideal variety model.An ideal variety model is a scientific projection identifying a combination of features and properties to ensure a desired level of yield, resistance, and other parameters [36].
The ideal variety should satisfy required yield levels, flexibility (suitability for cultivation in a broad range of environmental settings), proneness to technology (suitability for mechanized cultivation and harvesting), and high fruit quality.While developing a cultivar, meeting all the stated requirements seems impossible; successful breeding for specific agro-environmental conditions relies substantially on the unbiased determination of the model parameters of a regionally adapted variety, which makes it possible to obtain the closest approximation of an ideal variety in the most efficient and cost-effective way.
Here, the model is interpreted as a set of specific quantitative and qualitative values of key economically relevant features and properties of plants achieved in a particular soil and climatic zone.
The descriptive model of an ideal commercial apple variety includes 28 parameters divided into three groups, including resistance against abiotic and biotic stresses, yield per plant, product quality, and proneness to technology; see Figure 2.With regional environmental features identified, a regionally adapted model is developed and compared to the released varieties, which makes it possible to calculate the possibilities and risks involved in their production.
The key limiting factors for apple cultivation are temperature extremities, diseases, pests, and viruses.Temperature conditions are the prevailing factor responsible for the growth and development of fruit crops affecting all physiological processes, including photosynthesis, respiration, transpiration, biochemical transformation, and the transport of substances and compounds [37,38].Depending on the cultivation region, full ripening of apple fruits with the accumulation of bioactive substances requires the sum of active temperature (SAT, >10 • C) from 2000 (Central region) to 3000 • C (Southern region) [39].In Central Russia, the varieties adapted for intensified horticultural practices are expected to develop optimally and produce high-quality crops of up to 25-30 ton/ha at SATs of 1990-2000 • C, with a vegetation period of 190 days and solar intensity of up to 12 thousand lux.These varieties are also expected to withstand early winter frosts of −25 • C, mid-winter temperatures of −40 • C, daily temperature differences of −25 • C, and recurring frosts of −35 • C, without crop losses [40].
Winter hardiness is another limiting factor for all industry-scale horticultural areas; its most damaging component depends on the region [41,42].An ideal variety is expected to show high resistance against all winter hardiness components as follows: early winter frosts of −25 • C, maximum resistance to frosts of −40 • C in mid-winter after organic rest, resistance in the thaw season with stem heating to −25 • C due to solar exposure, and the ability to restore resistance to frosts of −35 • C during rehardening after the thaw period [43,44].High frost resistance (−40 • C) in mid-winter and average frost resistance after the thaw period (down to −37 • C) in a controlled environment have been demonstrated by the Marat Busurin, Antonovka Obyknovennaya, and Podarok Grafskomu cultivars released for cultivation in the Central District.
average fruit mass from -≤ 120 g and > 220 g juicy and shattering crisp pulp, fruit taste ≥ 4.8 points, richly aroma, content of sugar > 10%, ascorbic acid content > 15 mg/100 g, content of organic acids for dessert fruits ≤ 1 the color of the fruit is mostly red, with a sheen.fruit shape -regular, symmetrical, varied one-dimensionality, % ->80 seed chamber -small consumption period -winter and late winter long term storage capability ≥ 210 days transportabilityhigh A winter hardiness study of apple cultivars in a controlled environment, carried out in the Central Chernozem District in January (component II) at a temperature as low as −40 • C, showed that the Bolotovskoe and Antonovka Obyknovennaya varieties had relatively high winter hardiness, while triploid varieties Zhilinskoe, Vavilovskoe, Osipovskoe, Patriot, Spasskoe, and Turgenevskoe, and diploid varieties Orlovskij Pioner, Rannee Aloe, Sokovinka, and Sinap Orlovskij, significantly outperformed the Melba reference variety in this respect and demonstrated reversible leaf bud and tissue damage (up to 2.0 points).The winter hardiness of bark and buds in triploid varieties Aleksandr Bojko, Maslovskoe, Orlovskij Partizan, and Prazdnichnoe matched that of Antonovka Obyknovennaya (frostnip up to 2.0 points), while their wood winter hardiness matched that of Melba (2.2 to 2.4 points) [45].The optimal adaptation level of apple varieties in the North Caucasian District implies the ability of the plants to withstand early winter frosts (−15 • C), maximum frosts (below −40 • C), and post-thaw frosts (−25 • C) without damage [46].The higher frost threat in April-May leads to stricter requirements for apple variety resistance against low temperatures of down to −23 • C in early spring and down to −8 • C during flower bud breakage.According to E.V. Ulyanovskaya and E.A. Belenko [47], apple varieties Feya, Soyuz, Orfej, Margo, Sirius, Noktyurn, Vasilisa, and Karmen, cultivated by the NCF-SCHVW, and foreign varieties Florina, Dayton, Early Mac, Gala, and Gala Schniga have shown high resistance against springtime weather anomalies and come closest to the developed locally adapted variety model among all the apple varieties currently included in the State Register of Breeding Achievements Approved for Use in the North Caucasian District.Their prolonged bloom period acts as a protective adaptive response to low-temperature stress [40].
Drought resistance (hot dry winds during bloom period, air temperature above +25 • C; wind speed above 8 m/s; drought during fruit formation of over 20 days, drought during flower bud differentiation of over 35 days, drought during fruit filling of over 40 days) is less damaging than winter frosts and is mostly relevant for southern regions, where high air temperatures lead to crop reductions even with proper watering [37,48].An ideal commercial variety is expected to have high drought resistance.O.E.Merezhko identified the genotypes showing high drought resistance in the South Urals' conditions in varieties Persiyanka, Bolotovskoe, and Anis Sverdlovskij, which can be successfully introduced into production and used in breeding [49].N.I.Nenko et al. assessed heat and drought resistance and identified the apple varieties (Prikubanskoe, Fortuna, Soyuz, and Rodnichok) that can be used as sources of drought resistance in breeding [50].In addition, apple varieties Renet Platona, Iskra, Yuzhnye Nochi, and Solnce Kubani seem promising as sources of drought resistance, and the Atlasnoe variety as a drought resistance donor [51].
Apple scab is among the most harmful apple diseases across all cultivation zones in Russia, capable of reducing crops down to 50%.Moreover, it significantly reduces the marketable quality of fruits, deteriorates the assimilation apparatus activity, and impairs the general condition of a tree, thereby affecting its winter hardiness and yield [11][12][13][52][53][54][55][56].The disease is caused by the pathogenic fungus V. inaequalis (Cooke) G. Winter.At present, over 280 apple cultivars have been obtained in Russia using sources and donors of oligogenic scab resistance, in most of whom the immunity is controlled by the Vf resistance gene.In the Central District, high resistance against the disease is found in varieties with a normal fruiting type, such as Arkadik, Imrus, Mayak Zagor'ya, etc.; in the Centra Chernozem District, it is found in diploid varieties such as Bolotovskoe, Ven'yaminovskoe, Kandil' Orlovskij, Solnyshk, Start, Stroevskoe, and Yubilej Moskvy; triploid varieties such as Aleksandr Bojko, Vavilovskoe, Maslovskoe, Rozhdestvenskoe, Yubilyar, and Yablochnyj Spas [57], and varieties Vympel, Uspenskoe, Fregat, Bylina, Flagman, and Akademik Kazakov [58].Scab resistance (damage of 1 point or less in epiphytotic years) is demonstrated by varieties Arkadik, Mayak Zagor'ya, Imant, Imrus, Rozhdestvenskoe, and Gordeevskoe.
In foreign breeding practices, the highly scab-resistant transgenic lines of the Marshall McIntosh variety were obtained by transforming the apple genome with genes of Trichoderma atroviride P. Karst.fungus encoding the expression of antifungal proteins endochitinase and exochitinase (N-acetyl-β-D-hexosaminidase) using the modified CaMV35S promoter [59].The barley hordothionin gene (hth) was introduced into the Elstar and Gala plants to produce two transgenic lines consistently not susceptible to the disease in the case of artificial infestation in a natural environment during a four-year period [60].Transgenic lines resistant to Rvi6 and other races were obtained by transforming Gala with a wheat-encoding Puroindoline-b (pinB) under a CaMV35S promoter [61] and HcrVf2 resistance gene [62].Transgenic lines of the Gala and McIntosh varieties were obtained by transformation after introducing three full-length Vfa genes into plant cloning vector pCAMBIA2301.The lines expressing Vfa1 or Vfa2 showed partial resistance against apple scab [63].
Recently, monilia disease and European canker (Neonectria ditissima Bres) have been observed to cause significant damage to apple trees.Monilia disease or fruit rot is caused by two similar pathogens: M. fructigena with conidial stage M. fructigena Pers.and M. cinerea Pers.with conidial stage M. cinerea Bon.The autumn form of the conidial stage damages a significant portion of crops when it encounters mature fruits in gardens and then harvested crops in storage.A pathogenic fungus causing the so-called monilial burn (M.cinerea, a springtime form of the conidial stage), leading to branch drying and death in trees, is a major threat as well [64].
The amount of soluble solids in fruits is what eventually determines their quality in storage.Dry soluble substances are mostly represented by sugars (fructose, glucose, and sucrose), organic acids (whose total is determined as a titratable acid), water-soluble vitamins (ascorbic acid and vitamin P-active catechins and leuco-anthocyanins), tannins and dyes, pectins, and mineral salts [67,68].Sugars and organic acids determine the taste and technological qualities of fruits, participate in the physiological processes of plants, stimulate appetite, are easily digestible, and delay ageing [69,70].The amount of sugar depends on the vegetation period conditions and significantly affects the quality of the obtained product.The less the chemical composition of a fruit changes depending on the weather conditions, the more promising it appears from a commercial perspective [71].Acids in fruits are mostly represented by malic (72%), citric (17%), and succinic (6.8%) acids, while all the other acids amount to approximately 4% [72].The total content of mineral substances in fruits falls within 0.2-1.5% of the wet weight basis.The mineral composition includes over 60 elements, such as potassium, sodium, calcium, magnesium, iron, aluminum, manganese, phosphorus, copper, nickel, molybdenum, boron, etc. [66,67,73].Apple trees can synthesize useful vitamins.For instance, provitamin A, folic acid, and vitamin P-active compounds in fruits, combined with vitamin C and pectin, bind radioactive substances and remove them from the human body.The thiamine and riboflavin content varies from 0.017 to 0.030 mg/100 g, and carotene content from 0.015 to 0.035 mg/100 g.Polyphenols, including catechins, flavanols, and leuco-anthocyanins, affect the capillary porosity and maintain wall elasticity, which reduces the risk of internal hemorrhage [74].According to multiple authors, the catechin content varies from 127 to 173 mg/100 g, flavanols from 7.1 to 15.1 mg/100 g, anthocyanins up to 42 mg%, and leuco-anthocyanins from 89 to 168 mg/100 g [75][76][77][78][79][80].The highest content of common polyphenols at picking maturity has been observed in new scab-resistant varieties Margo and Lyubava, and introduced variety Florina, which may be used to derive genotypes with high content of vitamin P-active substances [47].
The apple-breeding community has been able to select genetic sources to breed apple trees for specific features and then combine them in one genotype, which makes it possible to create hybrids satisfying the ideal variety requirements.For instance, cultivars Arkadik, Mayak Zagor'ya, Imant, Imrus, Rozhdestvenskoe, and Gordeevskoe demonstrate scab resistance (damage of 1 point or less in epiphytotic years).At the same time, cultivars Imant, Gordeevskoe, Belorusskoe Sladkoe, and Mayak Zagor'ya are characterized by good fruit quality and taste (taste rating of at least 4.5 points).
In the European part of Russia, the optimal parameters of a commercial apple tree cultivar are as follows: plant height on a medium-sized rootstock under 3 m; potential yield per plant of at least 25-50 kg; high fruit uniformity above 80%; winter and latewinter harvest maturity period; high storability of over 210 days and good transportability; average fruit mass from 120 g to 220 g; juicy and shattering crisp pulp; small seed cavity; fragrant fruits with taste rating of at least 4.5 points; appearance rating of 5 points and attractive, mostly red, glossy color with natural wax bloom; regular, symmetric, but diverse shapes; content of sugar above 10%, ascorbic acid above 15 mg/100 g, organic acids up to 1% (for dessert varieties); content of soluble dry solids of at least 20%.

Conclusions
The cultivars that come closest to the regionally adapted model of an ideal variety based on the set of features discussed are as follows: regionally adapted varieties Feya, Soyuz, Orfej, Margo, Sirius, Noktyurn, Vasilisa, and Karmen in the North Caucasian District, and foreign cultivars Florina, Dayton, Early Mac, Gala, and Gala Schniga [23]; regionally adapted varieties Svezhest', Orlovskoe Poles'e, Aprel'skoe, Ven'yaminovskoe, Bolotovskoe, Vympel, Uspenskoe, Fregat, Bylina, Flagman, and Akademik Kazakov in the North Caucasian District; varieties Imrus, Mayak Zagor'ya, and Bolotovskoe in the Central District.These cultivars are characterized by high resistance against weather anomalies, scab immunity, high yields, marketable quality, and storability.In addition, in southern regions, a prolonged bloom period acts as a protective adaptive response to low-temperature stress.
Combining optimal values of all features in a single genotype is a problem to be solved in the future by obtaining and gradually reconsidering donors of individual features using the broad genetic base and various species, forms, and cultivars from different regions, both domestic and foreign.
regionally adapted ones: the Den' Pobedy and Turgenevskoe winter varieties and the Prazdnichnoe late autumn variety cultivated by the Russian Research Institute of Fruit Crop Breeding (Orel).
summer consumption.From 2020 to 2022, seven cultivars were added, including three regionally adapted ones: the Den' Pobedy and Turgenevskoe winter varieties and the Prazdnichnoe late autumn variety cultivated by the Russian Research Institute of Fruit Crop Breeding (Orel).

Figure 1 .
Figure 1.Borders of the industrial-scale apple cultivation zone of the Russian Federation.Wavarieties for winter consumption; Oa-varieties for autumn consumption; A-varieties for summer consumption.

Figure 1 .
Figure 1.Borders of the industrial-scale apple cultivation zone of the Russian Federation.Wa-varieties for winter consumption; Oa-varieties for autumn consumption; A-varieties for summer consumption.

Figure 2 .
Figure 2. Optimal values of key economic and biological features of an ideal commercial apple variety recommended for breeding and cultivation activities in the Russian Federation.

Table 2 .
Distribution of the apple cultivars included in the State Register of Breeding Achievements Approved for Use in the Russian Federation depending on the consumption period, cultivation region, and originator.
® The right to a variety is protected by the Russian Federation and certified by a patent for a selection achievement.