Germplasm Resources of Oaks (Quercus L.) in China: Utilization and Prospects

Simple Summary Oaks (Quercus spp.) are a major component of subtropical and temperate forests in the Northern Hemisphere. There are approximately 464 species, and they are dominant tree species in ecosystems. Oaks have a long history of cultivation in Europe, North America, and other continents. They are also cultivated and distributed in most provinces of China. In this paper, Quercus germplasm resource distribution, ecological adaptability, and utilization are explored. All evidence indicates that oaks have been widely distributed since ancient times and have greater functional value than other species in the Fagaceae family. This review will provide a deeper understanding of oak conservation, development, and utilization in China. Abstract Oaks exhibit unique biological characteristics and high adaptability to complex climatic and soil conditions. They are widely distributed across various regions, spanning 40 degrees latitude and 75 degrees longitude. The total area of oak forest in China is 16.72 million hm2. There are 60 lineages of Quercus in China, including 49 species, seven varieties, and four subgenera. Archaeological data indicate that oaks were already widely distributed in ancient times, and they are dominant trees in vast regions of China’s forests. In addition, the acorn was an important food for ancestral humans, and it has accompanied human civilization since the early Paleolithic. Diverse oak species are widely distributed and have great functional value, such as for greening, carbon sequestration, industrial and medicinal uses, and insect rearing. Long-term deforestation, fire, diseases, and pests have led to a continuous decline in oak resources. This study discusses the Quercus species and their distribution in China, ecological adaptation, and the threats facing the propagation and growth of oaks in a changing world. This will give us a better understanding of Quercus resources, and provide guidance on how to protect and better utilize germplasm resources in China. The breeding of new varieties, pest control, and chemical and molecular research also need to be strengthened in future studies.


Introduction
Oak trees refer to plants in the Quercus genus, which is the largest genus (accounting for approximately 50%) in the Fagaceae family [1]. There are approximately 450-500 species of oaks, which are dominant tree species in ecosystems throughout the Northern Hemisphere [2][3][4]. Based on the website Plants of the World Online (https://powo.science.kew. org/) (accessed on 27 December 2022), there are 464 accepted species of Quercus. Oak trees exhibit unique biological characteristics and high adaptability to complex climatic and soil conditions [5]. As such, they are widely distributed in tropical, temperate, and cold regions, spanning 40 degrees latitude and 75 degrees longitude [6]. Oaks have a long history of cultivation in Europe and other continents, and oak cultivation is practiced in most provincial regions of China. According to the State Forestry Administration of China, oaks accounts for 13% of natural forest in China. Oaks encompass diverse species and are have shown that these two species were introduced to China from North America in the early 20th century [30]. Until now, Q. palustris and Q. robur have been considered foreign-introduced species in most studies, while some reports believe they were transplanted from the Shandong Province and Northeast China. However, no wild trees have been reported in these areas. Recent studies have also classified Q. sichourensis and Q. edithiae as being in the Quercus genus [31]. In North and Northeast China, there are Q. wutaishanica, Q. mongolica, Q. dentata, Q. aliena var. acutiserrata, Q. aliena, and Q. variabilis, among other species. These species provide critical habitats for oak silkworms, and approximately 70,000 tons of tussah cocoons are produced each year. In the Henan and Shandong Province, Q. acutissima, Q. variabilis, Q. aliena var. acutiserrata, and Q. chenii are the main species of oak, with 50,000 tons of tussah cocoons produced each year. In the Southwest of China, including Guizhou, Sichuan, and Shanxi Province, Q. acutissima, Q. variabilis, Q. wutaishanica, and Q. fabri are distributed, and approximately 50,000 tons of tussah cocoons are produced annually [29,32].

Imported Oak Tree Species
Although oaks are abundant in China, as a major forest tree species and urban greening species, they have not been extensively studied. In China, the number of tree species available for urban landscaping is quite low. To expand oak tree populations and utilize their resources effectively, China introduced oak trees as greening tree species. The oak trees were imported from Europe and America in the mid-19th century, through foreign missionaries, businessmen, and students [33]. However, oak trees were not systematically introduced or studied in China until in the 1960s, when the Chinese Academy of Forestry introduced more than 10 species of Quercus from the United States [34]. This provided abundant materials for the germplasm breeding improvement of oaks in China. Some companies and scientific research institutions have also conducted studies on species introduction. To date, approximately 35 species of Quercus have been imported from Europe and America (Table 1). The successful species introduction, domestication, and biological and ecological evaluation of these foreign oaks have been studied [35]. Many of them have been successfully domesticated; for example, Q. texana shows good tolerance to waterlogging, and Q. virginiana shows high tolerance to drought, salinity, and heavy metal stress [36]. These species have great potential for applications in coastal protection and mining area greening. Meanwhile, several foreign-introduced oaks (e.g., Q. cinerea also named Q. incana, Q. cuneata, and Q. fraineitto) were not suitable for the local climate [37]. Oaks are widely distributed in Asia, Europe, North America, and Africa, and are particularly abundant in China, the United States, Russia, and India. Fossils of oaks are also widely distributed throughout geological history, and they are a dominant plant group in strata in the Northern Hemisphere from the Eocene epoch [41]. Archaeological data indicate that oaks were already widely distributed in China in ancient times. The Eocene-epoch Q. rhombifolia fossil found in Fushun, Liaoning Province, is the earliest fossil record of oak tree leaves in China. Quercus sect. Heterobalanus (Oerst.) species are montane sclerophyllous oaks in the Hengduan Mountains and have high tolerance to low temperatures, drought, soil impoverishment, and strong ultraviolet radiation. They are the dominant species, and their fossil record extends back to the Miocene. Early fossils of this sclerophyllous oak were found in Xigaze, the Tibet Autonomous Region (late Miocene), which was named Quercus tibetensis H. Xu, T. Su et Z.K. Zhou sp. nov. [42]. Other Sect. Brachylepides oak fossils were found in Xiaolongtan Basin, Yunnan province [43]. The earliest fossil of a deciduous oak was found in the Miocene epoch flora in Dunhua, Jilin province. This origin is later than that of the evergreen oaks. From archaeological research, the origin of Quercus may have been in the early stages of the Palaeocene, followed by accelerated species differentiation in the Eocene or Oligocene in East Asia, Europe, and North America. Quercus praedelavayi Xing Y.W. et Zhou Z.K. sp. nov. s from the upper Miocene was found in southwestern China [44]. Quercus heqingensis n. sp. from the late Pliocene was found in Heqing, Yunan province, China [45].
Deciduous broad-leaved tree species (especially Quercus) were dominant in vast regions of China. This was confirmed by archeological discoveries, including the 7000-yearold Xinle site in Shenyang, and the Chahai site in Fuxin County, Liaoning [46]. The analysis of charcoal fragments excavated from the Xiajiadian site (3500-4000 years ago) in Chifeng, Inner Mongolia, showed that the loess hills had a relatively warm and humid climate at the time, and that the zonal vegetation consisted of Q. mongolica and Pinus tabulaeformis forests [47]. Starch grains found on the surface of stone tools from the Shangzhai site (7000 years ago) in Pinggu, Beijing, show that the North China Plain was inhabited by deciduous broad-leaved zonal vegetation, consisting of oak species (such as Q. mongolica, Q. aliena, and Q. acutissima). The charcoal remains from the Beiqian site in Jimo, Shandong, showed that Quercus plants (especially Q. acutissima) have been the dominant species in the Jiaodong Peninsula since the Beixin cultural period (7000 years ago) [46].

Current Distribution of Oaks in China
Deciduous oaks are widely distributed in China, and form narrow belts in northern areas; in contrast, evergreen oaks are moderately distributed in southern China [48]. Deciduous oaks are dominant and constructive species (the main species in forest construction) in deciduous broad-leaved forests and mixed broadleaf-conifer forests in temperate zone and warm temperate regions, especially in North China. Their altitudinal distribution ranges from a few meters to 3500 m above sea level. China has three regions with concentrated distributions of oaks: (1) the Liaodong and Jiaodong peninsulas are hilly areas inhabited by deciduous oaks (mainly Q. mongolica, Q. wutaishanica, and Q. acutissima); (2) the Funiu and Dabie mountain areas show the highest diversity of Quercus species in China (18 species in total, including almost all species found in eastern, western, southern, and northern China); and (3) a wide range of mountainous areas in Sichuan, Yunnan, and Guizhou, which are inhabited by several unique species of oak trees (18 species known to date) [8] (Figure 1).
The total oak forest area in China is 16.72 million hm 2 , based on the 8th National Forest Resources Survey. Most of these are natural forests, and the area of oak trees is 16.1 million hm 2 . The area of artificial oak forest is 0.61 million hm 2 . The land area occupied by oak tree forests exceeds 100,000 hm 2 in 17 provincial regions, 500,000 hm 2 in 10 regions, and 1000,000 hm 2 in five regions (including Heilongjiang, Jilin, Liaoning, Hebei, and Inner Mongolia) [8]. Oak tree forests account for the highest proportion of dominant tree forests.
The top ten tree species are oak, fir, larch, birch, poplar, masson pine, eucalyptus, spruce, Yunnan pine, and cypress, which account for 46.3% of the total forest area in China. There are about 20 species of deciduous oaks, being the main dominant species in temperate zones with broadleaved deciduous forest and mixed broadleaf-conifer forest. Q. acutissima, Q. variabilis, and Q. dentata are widely distributed in Northeast, Southeast, and Southern China. Q. wutaishanica and Q. mongolica, as representatives of deciduous oaks, are widely distributed in Northeast and North China and also located in Sichuan and Hubei provinces. In Yunnan Province, broadleaf oak timber reserves have reached 0.15 billion m 3 , which represents 43% of broadleaf tree timber reserves. Q. mongolica is mostly distributed in Northeast China and east Inner Mongolia. There are 411,000 hm 2 oak forests in Jilin Province, which accounts for 7% of the local forest area. In Liaoning Province, oak forests account for 43.5% of the local forest area, which is 1.06 million hm 2 . In Hebei Province, oak forests total 0.9 million hm 2 [49]. Based on the newest National Forest Resources Survey in 2019, Q. mongolica was the fifth most important tree (based on numbers), representing 8.294 billion trees and 0.583 billion m 3 timber reserves. Q. wutaishanica, in the thirteenth most important position, has 2.647 billion trees and 0.183 billion m 3 timber reserves.

Morphological and Physiological Adaptability of Oaks
Oak trees vary in their leaf size and shape ( Figure 2). This variation might reflect adaptations or plastic responses to different environments [50][51][52]. Leaf variation is influenced by genetic and environmental factors [53]. Oaks are deep-rooted plants. Their root systems are well-developed and deeply distributed, and the main roots of one-year-old trees can reach a soil depth of up to 100 cm [32]. In Q. variabilis, the main root length of young seedlings is 10 cm on the 58th day (no fibrous roots) and 50 cm on the 73rd day (with a large number of fibrous roots). The main roots of mature Q. variabilis can reach 6-7 m deep [8]. The well-developed root systems of oaks are important for soil and water conservation in mountainous areas. Roots also have varying degrees of plasticity, to adapt to environmental stress based on morphological or physiological plasticity and root chemical changes [54]. In addition, oak trees are obligate mycorrhizal symbionts. Their root hairs are 100-150 µm long and develop an ectomycorrhizal symbiosis with certain fungi. The mycelia of mycorrhizal fungi surround the root hair. They enter the cortex and invade the intercellular spaces. The mycelia extend outwards on the root surface in the form of villi and absorb water and nutrients from the soil, to maintain the growth of the oak [55]. Annual seedlings inoculated with mycorrhizal fungi can attain approximately double the biomass of control groups. For example, Q. wutaishanica inoculated with symbiotic fungi (such as Comphidius viscidus and Russula foeten) showed improved seedling growth, net photosynthetic rate, and total nitrogen and phosphorus contents [56]. Mycorrhizae affect the absorption of phosphorus fertilizers and have an antibiotic effect, thus protecting the roots of oaks from infestation by root rot fungi [8]. Mycelia can also secrete various types of extracellular enzymes that promote the decomposition of organic matter in the soil [57,58]. Based on these functions, mycorrhizal fungi can be used for the seedling culture and repopulation of oak trees. Most oaks are heliophilous or neutral species that do not have strict soil condition requirements for growth. They grow rapidly in moist, fertile, and well-drained neutral or slightly acidic sandy loam soil (particularly in ravines and foothills). They can also tolerate stress and soil infertility, because of their deep-rootedness and mycorrhizal formations. In addition, acorns have a strong sprouting ability, while trees are not transplantationresistant. Oaks are adaptable to a wide range of temperatures. Deciduous species of oak trees (such as Q. mongolica, Q. wutaishanica, and Q. dentata) are quite cold-resistant, whereas evergreen species are relatively demanding, requiring warmer temperature conditions [59]. Deciduous species are also relatively drought-resistant, whereas evergreen species are moisture-loving. The drought-tolerant species of oaks indigenous to China include Q. acutissima, Q. variabilis, Q. wutaishanica, and Q. mongolica. Moisture-loving species in southern China include Q. fabri, Q. serrata, and Q. chenii. Most foreign-introduced species of oaks are hygrocolous and highly moisture-resistant. In general, oaks exhibit strong resistance to wind, fire, pollution, and smoke. Species such as Q. variabilis, Q. acutissima, Q. wutaishanica, Q. suber, and Q. mongolica have a thick bark and exhibit fire resistance, which makes them ideal fire-resistant tree species [60]. Owing to its resistance to smoke and poisonous gas, Q. mongolica is a dominant tree species in the greening and isolation belts of industrial and mining areas [61]. Some species of oaks also exhibit saline-alkaline tolerance, such as Q. texana and Q. nigra [62]. In addition, Q. variabilis can absorb and accumulate heavy metals in suburban areas [63].

Climate Change Influences
Oak is one of the most diverse and ecologically important trees in the Northern hemisphere. They exhibit high tolerance to different environments and have proved useful in evolutionary mechanism research [64,65]. Climate change effects the oak pollen season, especially the start dates and season lengths [66]. In the Mediterranean basin, Q. pubescens, as an downy oak, is often used for anti-drought research in morphoanatomy, physiology, and genetic evolution. A significantly earlier senescence increased the sugar content in leaves, to maintain a higher photosynthetic potential [67]. Drought induced an increase in oxidative pressure from the transcript level [68]. Under a constant CO 2 concentration, the net primary production was positively affected by longer vegetation periods and negatively by respiration costs in European oak trees [69]. In the Mediterranean region, climate change induces heat waves and droughts, disturbing forest species and affecting productivity. The cork oak (Q. suber) is resilient and cork growth rapidly recovers when droughts finish [70]. Under long-term environmental changes, trees mainly rely on phenotypic changes. In two oaks, Q. pyrenaica (more tolerant to drought) and Q. petraea (less tolerant to drought), Q. petraea displayed a greater response to moisture availability, by triggering a tighter stomatal control across genetic groups [71].
Oaks comprise 13% of the natural forest in China. Studies specifically addressing oaks adaptation to climate change in China are needed. Greenhouse gases will affect the species geographical distribution and change the richness distribution pattern. Based on 35 oak species and data of 19 bioclimatic variables in China, the Quercus distribution will migrate to high altitudes or high latitudes, from being primarily distributed in the area of southwestern China. A high percentage of species loss will happen in mountainous areas, while other regions will gain species due to a northward shift in the years 2050 and 2070 [72].

Threats to Oak Trees
There are several diseases that can influence oak trees, including leaf, trunk, root, and acorn diseases. Leaf diseases are the most common, and most pathogens are fungi. The infected leaves exhibit growth deficiencies and death. Powdery mildew [73], brown leaf spot, rust disease, and "frog eye" disease mainly affect healthy leaves [74] (Figure 3). White rot disease is found in the trunk and roots.
There were 624 kinds of pests reported in 2010 as damaging the leaves, trunks, and acorns in oak trees [75]. Regarding leaf pests, Malacosoma neustria, Camptoloma interiorata, Parasa consocia, Phalera assimilis, Phalerodonta albibasis, and Fentonia ocypete greatly impact leaf growth. In recent years, an emerging oak pest, Rhynchaenus maculosus, has caused spectacular damage in Jilin, Heilongjiang, and Liaoning Province. The morphology, life cycle, and biology of this pest were studied in our laboratory. This pest had no reports till 2012 from when it was first recorded as a new species in China in 1987. It can induce leaf damage symptoms, including blister-like blotches on leaf margins. This pest is an univoltine insect and overwinters as an adult in the leaf litter. Both the larvae and adults can influence leaf growth. The leaf damage in Liaoning province increased from 6.9% in 2016 to 15.4% in 2018 [76,77]. Common trunk and acorn pests include Mallambyx raddei, Laspeyresia splendana, and Curculio arakawai (Figure 3). Other than disease, the illegal timber trade and harvesting for charcoal also threaten oak resources. Deforestation for farming and increasing mountain fires influence oak growth. For example, Quercus variabilis bark is widely used for cork production. Based on the red list statistics, these are 32 critically endangered species and 57 endangered species of Quercus (https://www.iucnredlist.org/) (accessed on 27 November 2022). In China, there are 12 species of oak trees whose numbers are decreasing, including Q. chenii, Q. edithiae, Q. fimbriata, Q. kingiana, Q. lodicosa, Q. marlipoensis, Q. mongolica, Q. sichourensis, Q. utilis, Q. macrocarpa, Q. alba, and Q. libani. Two of them, Q. fimbriata and Q. marlipoensis, are listed as critically endangered species. Four of these, Q. edithiae, Q. kingiana, Q. lodicosa, and Q. utilis, are listed as endangered species (https://www.iucnredlist.org/) (accessed on 27 November 2022).

Utilization of Oak Trees
The utilization of oak trees has a long history in China. Oak timber was used as charcoal and a building material, and acorns were an important source of food for ancient people. The Dadiwan site (7300-7800 years ago), Yangshao site (25,000 years ago), and the Qijia cultural period (approximately 4000 years ago) show the presence of oaks in the surroundings of the sites. Around the Erlitou site (3500-3800 years ago) in Luoyang city, there are many Q. acutissima and Q. aliena, accounting for 81.8% of the biomass in the local forest, and they are used for charcoal [78]. The above archaeological findings indicate that oaks were an important component of the vegetation in the Yellow River Basin in ancient times.
Acorn was an important food for ancestral humans. In the Peiligang site (8500~7000 years ago), 1800 starch granules were found in 15 stone mills, and most of them were acorn starch [79]. In the Shangshan site, Xiaohuangshan site, and Hemudu site of Zhejiang province, and the Songze site in Shanghai, acorns and oak trees were found. In the Kuahuqiao site in Xiaoshan city and the Hemudu site in Yuyao city of Zhejiang province, a whole pit of stored acorns was found. The charcoal of Q. acutissima was also found at the Diaolongbei site (6200 years ago) in Zaoyang, Hubei province, confirming previous findings and indicating that the Yangtze River Basin had a warm and humid climate in remote antiquity [80].
Quercus spp. were widely used in different places and periods. They had various Chinese popular names, which were used in different places and periods, including Li, Xiang, Hu, Xiangdou, Liqiu, Zuoli, Zuozi, Xiangshi, Xiangzi, Xu, Zhu, and Zaodou [81]. Indeed, oak trees were used as charcoal materials and as timber. In modern times, oaks are wildly used in energy, edible fungus cultivation, insect rearing, and industrial and food production ( Figure 4).

Oak Trees as Sources of Timber
Oak wood has excellent mechanical properties, including high levels of hardness, beautiful wood grains, corrosion resistance, and high resilience. These timbers are widely used for the construction of buildings, bridges, furniture, and textile equipment [82]. Some oak woods are used as raw materials for gun stocks, planer stocks, and tool handles. Oak species with high timber quality include Q. wutaishanica, Q. variabilis, Q. aliena, Q. mongolica, Q. fabri, Q. serrata, Q. aliena, Q. acutissima, Q. chenii, and Q. stewardii [83]. The wood densities of Q. wutaishanica, Q. aliena, Q. chenii, and Q. stewardii can exceed 0.8 g/cm 3 , and the modulus of rupture of oak trees exceeds 1201 kg/cm 2 [83]. Based on these qualities, oak wood is generally considered a high-strength material. With the exception of Q. acutissima and Q. aliena, all species of oaks have a longitudinal compressive strength of at least 560 kg/cm 2 [84]. In most oak species, the tensile strength parallel to the grain exceeds 1500 kg/cm 2 , especially in Q. chenii, where it exceeds 2000 kg/cm 2 . The wood of Q. wutaishanica, Q. aliena, Q. fabri, Q. chenii, and Q. stewardii is classified as having a high Brinell hardness [85].

Food and Feed Value of Oaks
The annual acorn resources in China total 6-7 million tons. Acorns are rich in nutrients and have a starch content of 50-70%, which makes them an important starch resource [24]. Moreover, acorns are the most important wild woody food resource in China, and have been a major source of food since prehistoric times [86].
The leaves of oak trees are rich in nutrients, vitamins, and minerals, and contain 1.84-5.73% crude protein, 0.23-0.42% crude fat, 1.04-3.87% crude polysaccharides, 9.50-18.67% crude fiber, and 0.34-1.27% total flavonoids [87]. Oaks, especially Q. dentata with its broad leaves, are used for a traditional Manchu delicacy, a pancake that is prevalent in Northeast China and northeastern Hebei province. The cake is wrapped in the tender leaves of Q. dentata and has the special fragrance of the leaves. Oak timber is also used to cultivate edible mushrooms. As mentioned above, oak trees are the main host plants for tussah larvae. At present, tussahs are mainly fed the leaves of Q. wutaishanica, Q. acutissima, Q. mongolica, and Q. variabilis. Most (accounting for 70%) are in Northeast China. Approximately 5000 t of tussahs are produced in Henan and Shandong, fed by Q. acutissima, Q. variabilis, Q. aliena, and Q. chenii. Approximately 2500 t of tussahs are produced in Guizhou, Sichuan, and Shanxi, fed by Q. acutissima, Q. variabilis, Q. wutaishanica, and Q. fabri [88].

Medicinal Value and Chemical Extracts of Oaks
The bark, leaves, acorns, and acorn shells of oaks can be used for medicinal purposes. Their bark is effective in relieving dampness, reducing heat, and detoxification, and can be used to treat enteritis, diarrhea, dysentery, jaundice, and hemorrhoids (Jilin Chinese Herbal Medicine). Purpurogallin, a compound from nutgalls and oak bark, has antioxidant, anticancer, and anti-inflammatory effects [89]. The leaves can be used to treat bacterial dysentery, pediatric dyspepsia, painful swelling, and hemorrhoids (Heilongjiang Manual of Common Chinese Herbal Medicine). Acorn shells have astringent and hemostatic properties and can be used to treat proctoptosis in diarrhea and dysentery, intestinal bleeding, metrorrhagia, and leukorrhagia. Acorns can relieve diarrhea, due to their astringent properties, and can be used to treat dysentery and hemorrhoidal bleeding (Tang Materia Medica and the Herbal Medicine of Rihuazi).
A clinical study used a decoction of oak tree bark to treat 48 patients with infectious diarrhea and the response rate was 93.75%, indicating a significant therapeutic effect. Aqueous extracts from Q. mongolica leaves reduced histopathological changes in type II diabetic mouse models [90]. Modern studies have shown that oak trees are rich in diverse functionally active substances. A review summarized the phytoconstituents from oak extracts and their biological applicability from data of PubMed, Scopus, and Science Direct (2010-2020). Some chemicals can be used as antioxidant, antimicrobial, antiobesity, antidiabetic, and anticancer agents, etc. The most studied oaks, including Q. brantii, Q. infectoria, and Q. robur, have had their biomolecules and biological activity identified. The main bioactive phytochemicals include phenolic compounds, sterols, volatile organic compounds, aliphatic alcohols, and fatty acids [91]. A study revealed that the bark of Q. mongolica contained 7-xylosyl-10-deacetyltaxol, 10-deacetyltaxol, and 7-epi-10-deacetyltaxoll [92], and can be used as a raw material for the synthesis of paclitaxel. Subsequently, 23 and 27 volatile chemical compounds were identified in the bark of Q. wutaishanica and Q. acutissima, respectively [93].
Oak trees can also be used to make wood vinegar. Wood vinegar made from Q. mongolica had a pH of 4.06, an organic acid mass fraction of 5.20%, a density of 1.0260 g/cm 3 , and a refined yield of 90.7% [96]. This wood vinegar was shown to inhibit Staphylococcus aureus and Escherichia coli, and the antibacterial components are presumed to be guaiacol and phenol [97]. An extracted solution of oak bark can be used to treat black spots and body ulcers in fish, as well as for burn injuries, empyrosis, trauma, animal and insect bites, and acne in humans. This extract also has significant curative activity in inflammatory, infectious, and suppurative diseases of the human skin and has been shown to be safe and non-genotoxic [98].

Industrial Value of Oak Trees
Oak is one of main raw materials for producing tannin extract, which is an important industrial raw material with diverse applications and a high economic value. The acorn cups, bark, and leaves of Q. variabilis can be used to produce tannin extracts with a tannin content of 15.7-15.9%, 8.7-9.3%, and 6.6-7.2%, respectively [99]. Oak trees, including Q. variabilis and Q. suber, are raw materials for the cork industry. Corks are applied in many industrial fields, because of their light weight, high elasticity, hydrophobicity, chemical stability, and superb physical properties [100]. Oak trees also act as high-quality wood resources for developing biomass energy. Acorn starch (accounting for 50-60% of the total weight) can be made into fuel alcohol, the branches and leaves of oak trees can be fermented to produce methane fuel, and the timber can be processed into solid fuel [101]. Oak species such as Q. phillyraeoides, Q. glauca, and Q. acutissima are used as raw materials for producing fine charcoal, and oak barrels are widely used to store wine [102].

Greening and Ornamental Value of Oaks
Oak trees are characterized by a strong vitality, longevity, a tall form, lush canopy, and broad and colorful leaves. Despite their great value for greening and as ornamental tree species, oak trees have not been widely used in urban or rural areas in China [103]. Poplar trees were commonly used for urban landscaping in the past; however, their pollen can cause various allergic diseases that severely impact the lives of residents. At present, oak trees are receiving attention as a suitable tree species for urban landscaping. European and American countries can provide a reference for urban landscaping uses of oak tree species [104]. Q. suber, as an evergreen tree, is the basis of an ecological system, contributing to the survival of many native species and also preventing desertification in vulnerable areas. Many cork forests are recognized as protected ecosystems [105]. Besides this ecological importance, the cork oak has the ability to produce a continuous and renewable cork layer. These cork woods are widely used in building, industry, and wine corks, due to fine physical and chemical properties [106]. Chinese cork oak (Q. variabilis) is also an ecologically and economically important deciduous tree species [107]. Together with other East Asian oak species, Q. acutissima and Q. chenii, they are used as indicator species for local forest health [108].

Collecting, Protecting, and Utilizing the Germplasm Resources of Oaks
Although oaks are abundant and have a long history of cultivation in China, most trees currently exist in wild forest, and their utilization is not diversified. At present, oak trees are primarily used to make timber, produce charcoal, raise tussahs, and cultivate edible mushrooms. Long-standing deforestation has led to a continued decline in oak resources. It is important to collect and protect the germplasm resources and ascertain the resource distribution in China. Molecular studies to evaluate the germplasm resources of oaks at the molecular level have been performed. To date, the nuclear genomes of eight species of Quercus have been sequenced (Q. lobata [109], Q. robur [4], Q. suber [106], Q. mongolica [19], Q. gilva, Q. wutaishanica, Q. wislizeni, Q. glauca, and Q. aquifolioides (unpublished)), and the chloroplast genomes of 25 species of Quercus have been analyzed [110]. This provides basic genetic information for diverse studies on oaks, including studies on their classification, evolution, and breeding. These accumulated findings provide a valuable reference for the evaluation, protection, and effective utilization of oak resources [107].

Promoting the Comprehensive Utilization of Oaks
Evaluating the functional, nutritional, and medicinal value of oaks would provide a reference for their effective utilization. Landscaping projects involving the use of oak trees should consider their ecological adaptability and ornamental properties. Therefore, it is necessary to evaluate the characteristics of different oak tree species, including their stress tolerance (such as tolerance to cold, water, moisture, drought, and salinity), and rapid propagation. The application of oak leaves as a feedstuff for tussahs should focus on improving their quality and yield; therefore, it is important to identify species suitable for the production and growth in different stages of tussah rearing [111]. To effectively utilize oak trees for soil and water conservation, sand fixation, and as wind breaks, it is necessary to identify fast-growing species with high stress tolerance, good adaptability, and excellent performance in soil and water conservation [112].

Studies on Species Introduction, Domestication, Breeding, and Propagation of Oak Trees
Broad-leaved forests dominated by oaks will be gradually replaced by conifer forests, due to fire, drought, or fell threats, such as for Q. ilex and Q. suber [113], resulting in environmental degradation and severe soil erosion. Moreover, transplanting oak trees from mountains and plains into cities can destabilize the phytocommunity of forest areas. In recent years, China has predominantly used foreign-introduced oaks with differently colored leaves, but has neglected the selection and breeding of indigenous species. This has resulted in the hybridization of oak species. In addition, biotechnologies (such as in genetic engineering) should be used to select and breed new and superior varieties of oaks that are suitable for afforestation, insect feeding, timber production, landscaping, and ecological conservation. Some oak species have undergone transgene editing, such as for herbicide resistance or to enhance tolerance to Phytophthora cinnamomi through CsTL1 gene editing a thaumatin-like protein [114,115]. Species introduction and identification should be executed in a planned manner.

Promoting the Utilization of Oak Trees in Urban and Rural Landscaping
Drought and water shortages are the primary constraints on urban ecological landscaping in northern China. Planting drought-tolerant ornamental trees is one of the most effective means of water conservation. Oak trees are preferred as water-conserving and drought-tolerant ornamental trees. In addition, oak trees are of great ornamental value because of their graceful posture, long life, and color variation during autumn. Some oak tree species (such as Q. texana and Q. nigra) exhibit strong tolerance to salinity stress and are suitable for growth in seasonally flooded low-humidity bottomlands [62]. Owing to its evergreen nature, large canopy, and high tolerance to wind and heavy metals, Q. virginiana can be used for the greening of mining wastelands [116]. Thick bark, cork tissues, and leathery leaves are present in Q. variabilis, Q. acutissima, and Q. mongolica. These species are suitable for firebreak forest construction due to their fire and smoke tolerance. After a fire, they will germinate and regenerate quickly. In industrial and mining areas, smoke and harmful gases can be absorbed by Q. brantii and Q. mongolica [117].

Developing Ecological Rearing of Tussah in Oak Forests
To improve the yield of oak leaves and the ecological conditions of oak forests, it is necessary to improve the soil and water conservation and manage fertilization and breeding strategies. In addition, it is advisable to plant oak tree species that are suited to local ecological conditions. Which kinds of oaks are suitable for tussah rearing? How should suitable oak species for tussah varieties in different larvae stages be chosen [111]? Further investigations are needed. Ecological breeding (a balanced breeding objective to maximize the rearing of insects, whilst not impacting the productivity and fitness of the host tree) and oak forest management are both important for tussah rearing.

Improving the Utilization of the Pruning Material of Oak Trees
Small-diameter timbers of oaks can be used as mushroom sticks, and their smashed branches can be used as a substrate and filling material. They are an ideal raw material for cultivating edible mushrooms, such as shii-take and Ganoderma lucidum, which are often found under wild oaks. Oak forests of Q. acutissima have been used for artificial G. lucidum cultivation in China. Other valuable mushrooms, such as porcini, black truffle, and white truffle (also known as "white diamond"), are also grown under oak trees [118,119].

Conclusions
Oaks play an important role in structuring forest communities, which are a source of wood, firewood, charcoal, and food. They are widely distributed throughout the world and play roles in carbon sinks, greening, soil conservation, energy development, and tussah rearing. In the modern times, oak germplasm resources have been destroyed in some regions of China by excessive utilization in the timber and edible mushroom industries, and as landscaping transplants. At present, more systemic research into existing germplasm resources, plant cultivation, and economic application is needed. Different natural variabilities in resistance to environmental conditions or pathogens from a phenotypic characteristic or genome level should be investigated. Future studies on oaks should focus on the breeding of new varieties, rapid propagation of seedlings, chemical extract investigation, and comprehensive utilization. Molecular technologies, including transgenic technology, gene editing, and tissue culture, should be used in future research. Fully realized oak resource utilization would encompass their ecological, dietary, medicinal, landscaping, and cultural value.