Rapeseed as an Ornamental

Abstract

Rapeseed (Brassica napus) is one of the most important oil crops worldwide. However, an intriguing new use for rapeseed has recently developed: as an ornamental. Tourism based on blossoming fields of these yellow flowers has become a new economic growth opportunity in China. From a breeding perspective, two main problems currently limit the potential of rapeseed as an ornamental. First, the flowering period is quite short (30 days on average), which limits economic income; second, the flower color in commercial cultivars is currently limited to bright yellow, which may pall quickly for sightseers. This review summarizes the possible problems of using rapeseed as an ornamental, and details factors affecting the flowering period, how the flowering period can be prolonged by integrating optimal cultivation measures or/and spraying with chemical reagents, and ways of creating and breeding rapeseed with diverse flower colors.

1. Introduction

Rapeseed (Brassica napus) is widely planted worldwide as an important source of edible oil, forage, condiments and vegetables. In China, rapeseed oil comprised 22.3% of edible oil production and accounted for 23.4% of the domestic consumption of vegetable oil in 2017–2018 [1]. However, with rapid urbanization and development and increasing labor costs, the relative economic benefits of planting rapeseed in China are progressively declining. Moreover, mechanized harvesting is often not feasible or easy to implement, such as in terrace cultivation. These factors have contributed to a recent major decline in the cultivation area of rapeseed in China [2]. Concurrently, the average income is increasing, along with work pressures and demand for recreational activities. Agricultural tourism is a new concept that is developing rapidly in China and around the world as a result of progressive urbanization, and rapeseed cultivation is perfectly suited to meet this demand.

Increasingly, rapeseed is becoming a well-known tourist attraction worldwide. Famous scenic spots include Jeju Island in Korea, and Takikawa, Tokyo and Yokohama in Japan, and Cambridgeshire in England. In China, there are at least 20 scenic spots which include rapeseed fields as a point of interest, and ten larger scenic spots which are well-known due to large-scale rapeseed cultivation: Hanzhong in Shanxi Province, Xinghua in Jiangsu Province, Jingmen in Hubei Province, Luoping in Yunnan Province, Tongnan in Chongqing, Menyuan in Qinghai Province, Rui’an in Zhejiang Province, Fengxian in Shanghai, Wuyuan in Jiangxi Province, and Guiding in Guizhou Province. The use of rapeseed as an ornamental is increasing across China. Each year, these scenic spots can attract over 5 million tourists. As an example, Wuyuan County, in Jiangxi Province, China, is considered the most beautiful village in China, due to its natural environmental surroundings and terrace agriculture, which includes rapeseed as a scenic attraction. Tourist income accounts for 51% of the yearly GDP of Wuyuan County (US$145 million each year), demonstrating the strong economic stimulus underlying the rapid development of rapeseed as an ornamental in China.

Rapeseed has a number of desirable qualities for exploitation as an ornamental. First of all, rapeseed is easy to grow and can be used for both agriculture and tourism at the same time. Compared with other tourism projects, the initial investment has a lower commercial risk and can promote farmers’ income and economic development. Second, rapeseed fields are impressive and eye-catching, particularly in terraces: the bright yellow color is striking and signals prosperity in China. Thirdly, rapeseed flowers are also in bloom for a relatively long period (30 days on average) compared to other plants, such as peach blossom, cherry blossoms, pear blossom and apricot flower (10–20 day bloom period), improving potential tourist income.

The desirable features for rapeseed as an ornamental include bright flower color, large petals, lodging resistance, strong pest/disease resistance, longer flowering period, more flowers per unit area, and increased height (preferably over one meter). Currently, there are several problems which are restricting development of ornamental rapeseed, each of which is worth investigating and resolving.

2. Relatively Short Flowering Period

2.1. Problem

The first important problem is that the flowering period of rapeseed is relatively short for an ornamental (approximately 30 days in a normal season). According to incomplete statistics, in China, a tourist attraction that uses rapeseed as an ornamental plant can create about US$1.57 million in ticket revenue each day. Here, the flowering period is defined as the time between the first flower opening and flowering finishing.

2.2. Factors Affecting Flowering Period and the Corresponding Countermeasures

In order to solve this problem and maximize the flowering period of rapeseed, it is necessary to clarify the general factors affecting the length of the flowering period. Three major factors regulate the flowering period in rapeseed (Figure 1): the natural environment, cultivation practices, and hormonal control of flowering.

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Natural environmental conditions

Temperature variation greatly affects plant growth and development, and the circadian clock below the threshold of the activating temperature stresses regulation networks [3]. In addition, higher temperatures can promote metabolic activity, cell growth, photosynthesis, and plant growth and development [4,5], while lower temperatures (e.g., 20 °C) may decrease enzymatic activities and biochemical reactions, with complex effects on flowering phenotypes [3]. Several signaling pathways involving gibberellins (GAs), auxin, brassinosteroids and transcription factor phytochrome-interacting factor 4 (PIF4) are predicted to be involved in the regulation of growth in response to temperature [6]. While the cold response of rapeseed flowering is complex, it is clear that low temperatures may slow down the flowering process. Generally speaking, rapeseed blossoms faster at temperatures over 15 °C, while the flowering period may be reduced from 30 days to 25 days or less with increasing temperatures. The flowering period of rapeseed is negatively correlated with the length of the growing period across varieties: namely, early-flowering rapeseed blooms at lower temperatures, with a longer flowering period than late-flowering rapeseed [7]. However, varieties which flower too early are highly likely to suffer injury (fading, damage or wilting) caused by the cold, such that the rapeseed flowers generally do not look good when the temperature is below 12 °C [8].

Altitude is the second factor affecting the flowering period, although ultimately the effect of altitude on the flowering period is also associated with the effect of temperature. Higher altitudes have lower temperatures, with an average decrease of 0.6 °C per 100 m above sea level [9]. For terracing in particular, flowering on the top of mountains will be slower than at the bottom, which requires us to adjust sowing times according to local land altitudes to achieve a simultaneous flowering effect. Generally speaking, it is best to sow from higher elevation to lower elevation. Thus, the sowing date is determined by the local climate and altitude. In the Yangtze River Valley, China, it is generally better to adopt a direct seeding mode from October 1st to October 10th and to use a transplanting mode of sowing from October 20th to November 1st.

Light is related to terrain or fog, and light intensity may affect plant growth and development. For example, low light conditions are beneficial for the flowering and growth of Arabidopsis thaliana [5]. Moreover, water availability is co-determined by climate, terrain, and irrigation management. Many other environmental factors, such as nutrition and different stresses, can affect the flowering period [10]. Many unfavorable environmental factors, such as water deficiency (drought) and water excess (flooding), can trigger earlier flowering in plants [10]. However, these effects may not always be significant. For example, various drought and flooding treatments do not affect flowering time in wild genotypes of Arabidopsis [11,12,13]. This may be because plants which initiate the reproductive stage (e.g., flowering) in a timely fashion regardless of environmental stresses have greater reproductive success [10,14,15].

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Cultivation practices

Fertilization is critical to the flowering period, although effective utilization of fertilizer depends on the soil type. In general, under low mineral nutrition, Arabidopsis plants tend to flower later [12], but rapeseed tends to flower earlier (Fu et al., unpublished data). In addition, under the prerequisite of non-lodging, the application of more nitrogen fertilizer may delay flowering time, and the total growth period in rapeseed slightly increases with increasing fertilizer application by 1 to 2 days [16]. The reason for this is likely that N signaling regulates nuclear CRY1 (blue-light receptor cryptochrome 1, CRY1) protein abundance, and affects the normal flowering process of the central circadian clock (e.g., GI and CO), as was observed in A. thaliana [17]. We know that Boron-deficient fertilizer may also lead to flowering rather than fruiting. Moderate and full fertilizer application, including organic manure or farm manure, are probably likely to ensure rapeseed flowers have brighter colors and that the rapeseed has a longer flowering period.

Planting density is another factor affecting the flowering period. Higher planting density (e.g., over 300 thousand plants per hectare in the Yangtze Valley, China) is negatively correlated with the flowering period, possibly because it may decrease the number of flowers produced per individual plant or on the main inflorescence, resulting in faster completion of the flowering period. When planting density increases, the total rapeseed growth period has been observed to shorten by three to five days [18]. As a result of increasing planting density, the plant height, the stem diameter, the numbers of effective branches and the length of the main inflorescence decrease, while the effective branching position increases [19,20]. Hence, increasing planting density could promote faster rapeseed growth, especially in early sowing, while sparser planting (e.g., less than 105,000 plants per hectare in the Yangtze Valley, China) may increase the flowering period. In addition, we know that in rapeseed, early seeding results in earlier flowering with a longer flowering period, due to blooming in lower temperatures. Therefore, late sowing times (e.g., sowing after October 25th in the Yangtze River Valley, China) require a higher planting density (e.g., over 300,000 plants per hectare) to make up for the reduction in branches per individual plant.

Moreover, topping after rapeseed bolting (when the plant reaches 30 cm, mechanically remove the top 2–3 cm of the stem) can delay the early flowering period by 7–10 days, and can delay the final flowering period by 3–8 days [21]. Partial topping (topping a certain percentage of plants, e.g., every second plant) may delay the whole flowering period for three to eight days, as the early flowering stage does not change. However, this is a suboptimal strategy for prolonging rapeseed flowering in terms of the use of rapeseed as an ornamental, because fewer flowers will be in bloom across the flowering period in fields that have been topped (as a matter of personal observation). Hence, the optimal time (sunny morning), stage (plant height reaches 30 cm) and proportion (30–50%) of topping should be carefully chosen in order to prolong flowering time, but not to cause a detrimental ornamental effect.

Finally, changing the planting mode also can be a means to prolong the flowering period. In many scenic spots, rapeseed can potentially be used as green manure after the tourism period is over, rather than being harvested as an oil crop, because the tourism income is far higher than the profits of rapeseed oil. To prolong the flowering period, a mixed sowing model of early, middle and later flowering varieties in a ratio of 1:1:1 or 1:3:1 has been applied, and has been shown to achieve higher economic value by prolonging the total rapeseed flowering time (over 5 days, even over 7 days) in Wuyuan, China (Figure 2) [22]. Hence, planting different cultivars with diverse flowering periods should be considered a viable strategy for prolonging the total flowering period.

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Hormonal control of flowering

Targeted breeding of flowering traits should provide an efficient and economic means of prolonging the flowering period in rapeseed. The three main factors impacting the flowering period which should be amenable to trait improvement are the number of flowers per plant, the number of branches per plant and lifetime per flower. Lifetime per flower is the most important factor, and is associated with regulation of flower senescence and abscission. Flower senescence and abscission are affected by several environmental factors, such as seasonal changes (e.g., dark and low-light conditions), insect-mediated pollination, and stresses such as water scarcity, salt, cold and high temperature, wounding and pathogen attack [23,24,25]. However, the timing of flower senescence is mostly regulated by individual or multiple plant hormones, such as ethylene, cytokinins and abscisic acid.

Flower abscission in almost all monocotyledonous and eudicotyledonous plant species is highly sensitive to ethylene [26]. Therefore, mutating or silencing the key genes related to flower abscission may prolong flower longevity. Little research has been done in this area on rapeseed. However, in Japanese morning glory, an NAC transcription factor, designated EPHEMERAL1 (EPH1), was induced to expression independently by ethylene signaling, and it positively controlled programmed cell death during petal senescence to cause flowers to bloom for a second day [27]. Similarly, in petunia, silencing of PhFBH4 (a basic helix-loop-helix transcription factor) using virus-induced gene silencing or an antisense approach prolonged flower longevity by modulating the ethylene biosynthesis pathway [28]. Also, in Campanula, a naturally occurring 7 bp frameshift of a key ethylene insensitive homologous gene (Cmeil2) in the ethylene signaling pathway may be used to screen for flower longevity [29]. Similarly, transgenic Torenia plants incorporating a fragment of a 1-aminocyclopropane-1-carboxylic acid (ACC) oxidase gene had a two day extension of flower longevity [30]. In addition, Petunia hybrida plants transformed with boers, a mutated ethylene receptor sensor gene of Brassica oleracea, showed extended flower longevity and apparently larger flowers [31].

Aside from ethylene-related genes, the mutation or silencing of other related genes in the same flowering pathway can have similar effects. For instance, ectopically-expressed TERMINAL FLOWER 1 in transgenic Arabidopsis plants can greatly prolong the vegetative and reproductive phases [32,33]. As well, the anthocyanin regulator ANTHOCYANIN1 mutant an1 in petunia led to an increase of flower longevity compared to wild-type flowers [34]. Ethylene is thought to primarily regulate flower senescence in ethylene-sensitive flowers, while abscisic acid (ABA) is considered to be the primary regulator in ethylene-insensitive flowers [25]. ABA (abscisic acid) negatively regulated the ethylene biosynthetic pathway in all flower tissues of Hibiscus rosa-sinensis L. [35]. In addition, cytokinins can delay petal senescence [36]. Both an increase in ethylene and a reduction in cytokinin determine the initiation of senescence, which directly or indirectly leads to an increase in levels of reactive oxygen species [37]. Furthermore, signal transduction during the process of floral senescence may be associated with G-proteins, changes in calcium activity and the adjustment of protein phosphorylation and dephosphorylation [23]. The flowering period is comprehensively regulated by multiple hormones, and thus, the flowering period may be regulated by spraying with hormone reagents (as described separately below) or by genetic means.

In addition, compatible pollination triggers a series of post-pollination events such as petal senescence [38]. Therefore, lack of pollination or reduced pollination may hypothetically prolong the flowering period. In fact, using male sterile lines with normal flower organs (e.g., Ogu cytoplasmic male sterility in B. napus with both the sterile plant rate and sterility reaching 100%), grown at a distance from fertile lines which may act as pollinators, has recently been demonstrated to delay the flowering period by five to seven days [39].

Certainly, lines or cultivars with long flowering periods can also be screened for or explored, because different varieties exhibit diverse flowering periods, particularly in low temperatures [7]. This approach by the authors yielded a particularly desirable accession (Figure 3) which can continuously flower for about two months: new flowers are in bloom while old flowers on some branches wither away or pods grow. Although the yield of this accession is 15% less than common varieties because the different maturity times for pods on different branches results in loss of some seeds prior to harvest, this is not a consideration in some areas where rapeseed is used as an ornamental.

2.3. Prolonging the Flowering Period by Chemical Reagents

There are three main approaches and reagents for prolonging the flowering period in rapeseed (Figure 4). Firstly, the final flowering stage can be delayed; secondly, the early flowering stage can be extended, and thirdly, both the first and second approaches can be applied simultaneously. A number of reagents are used to adjust the flowering period in horticultural plants, but these are not frequently reported in agronomic crops. Some chemicals are applied to regulate the life of fresh flowers by interfering with the floral development process via hormones: for instance, the ingredients in the liquids that maintain freshness of cut flowers include sucrose, bactericide, organic acids, inorganic salts, and plant growth regulators.

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Ethylene

In a large number of ornamental species, flower longevity can be efficiently enhanced by hindering the plant response to ethylene [40]. Erysimum linifolium (wallflower) senescence can be accelerated by rises in the endogenous ethylene level, and by application of exogenous ethylene released by 2-chloroethylphosphonic acid, but can be delayed by exogenously applied cytokinin, 6-methyl purine (which is an inhibitor of cytokinin oxidase), or treatments with the ethylene signaling inhibitor silver thiosulphate [37]. Silver nano-particles (SNP) and silver thiosulfate (STS) can prolong the vase life of cut carnation flowers by decreasing oxidative stress, enhancing anti-oxidant systems, lowering bacterial populations and delaying flowering [41]. Similarly, silver nanoparticles and chlorophenol may be used to prolong vase life and increase the postharvest quality of cut gerbera flowers [42]. In the same species, either 50 or 100 mg/L carvacrol and either 1 or 2 mg/L silver nanoparticles (SNP) can prolong the vase life of gerbera flowers from 8.3 to 16 days [43]. In addition, either by itself or in combination with silver nano-particles (2–5 nm diameter) and antimicrobial agents, boric acid, as an inhibitor of ethylene production, can significantly extend the vase life and decrease ethylene production, with 9.7 days as the highest cut flower longevity achieved [44]. Moreover, a gaseous compound, 1-methylcyclopropene (1-MCP), hindered a series of plant responses to ethylene, with the result of extending the senescence of cut flowers [40]. In conclusion, although regulating ethylene by treatment with various chemicals is efficient in prolonging vase life, many of these chemicals (in particular heavy metals such as silver nanoparticles) are not suitable for use in prolonging flowering time in the field, as these chemicals are costly to produce and can result in environmental pollution. Therefore, selecting environmental-friendly, low cost, and low toxicity reagents is necessary for prolonging flowering life in the field.

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8-HQC

8-hydroxyquinoline citrate has a bactericidal effect that prevents degradation of cut flowers by bacteria and fungi. Cut carnation flowers treated with 8-HQC, copper coin, and leaf extracts of P. guajava and P. betle exhibit longer vase life and larger flower diameter [45]. Treatment with the extract of Mentha pulegium and 8-hydroxy quinoline sulphate (8-HQS) can increase the vase life of cut rose (R. hybrida L.) flowers and lower total chlorophyll (SPAD value), with the greatest vase life longevity reaching 11.2 and 10.3 days using 400 mg/L 8-HQS and 10% of Mentha pulegium extract [46]. Similarly, the application of 8-hydroxyquinoline sulfate (8-HQS) with 2% sucrose can retard the degradation of chlorophyll and carbohydrate, delay flower senescence and extend the vase-life of sweet pea cut flowers up to 17 days [47].

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Citric acid

Citric acid is a common ingredient in vase solution formulations, but pre-harvest use of citric acid is a novel method to extend vase life of cut flowers which has previously been reported in tuberose [48]. Treatment with 0.15% citric acid significantly extended the vase life of Lilium flowers from 11.8 days to 14 days [49].

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6-BA and sucrose

In petunia, 6-benzylaminopurine (BA) treatment can prolong flower life for 2.3 to 3.3 days, and promotes increased concentrations of phenols and anthocyanins, but lower total carotenoids [36]. In addition, flower longevity in isolated flowers of Dianthus chinensis was successfully extended by treatment with sucrose for 5 days followed by 3 days in d-glucose [50]. Sucrose treatment also promoted lily flower opening and extended flower life, but did not affect tepal abscission [51].

Since many chemical reagents efficiently prolong the flowering period in various plant species, it is necessary to assess the effects of these reagents on prolonging the flowering period, in addition to the optimal reagent dosage, treatment, time of application, and the possible adverse effects of reagent application. Subsequently, the best reagent can be chosen according to the following standards: simple formulation, low cost, low residuals, high solubility, long-lasting effects, low toxicity and ease of application. Optimal management practices also need to be determined, including dosage, timing, method, location and frequency of spraying. Both the reagents and the spraying management practices can be effectively combined for best effect.

Under the financial support of the key research and development program of Jiangxi Province, our group screened 15 types of chemical reagents for effect in prolonging the flowering period of B. napus. Rapeseed flowering was prolonged by 4 days with 2,4-D(2,4-Dichlorophenoxyacetic acid), by 5 days with indole acetic acid, and by 6 days with growth retardants (a mixture of uniconazole, nitrogen, potassium, phosphate, sulphur, zinc, calcium and magnesium fertilizers), and the optimal spraying time was one week before flowering. However, 2,4-D led to a small amount of rapeseed withering. Therefore, a combination of indole acetic acid and growth retardant reagents was found to be optimal for extending rapeseed flowering for 6 days without side effects, an important guideline for the chemical regulation of rapeseed flowering [52,53,54].

This research is beneficial for prolonging flowering time in an ornamental context short-term, but there are several problems which need to be addressed in the long run. Firstly, the effect and feasibility of spraying with reagents is affected by the rapeseed developmental stage, reagent dosage and frequency of spraying, and environmental conditions such as temperature, weather, terrain, and, in particular, labor. Certainly, unmanned planes are commonly used to spray reagents, but specialized conditions such as terraces still require more labor. Environmental conditions can also significantly reduce the efficacy of spraying, for example, in the spring in the south of China, too much rain often reduces the effectiveness of reagent sprays. Secondly, chemical reagents may cause environmental pollution, including soil and water pollution, despite the selection of reagents with low toxicity. Repeated applications may also cause reagent residue. It is therefore necessary to screen for reagents without environmental residue, and which have permissible environmental impacts under the scope of national law. Therefore, developing long-flowering cultivars is a more efficient goal in the long term to prolong flowering in rapeseed than spraying with chemical reagents.

3. Development of a Range of Flower Colors in Rapeseed

3.1. Problem

Most rapeseed petals are yellow, with a few varieties of white (such as green-white, milk-white and pure white) and orange-red [55]. In contrast to white flowers, yellow flowers are more attractive to pollinating insects, and have a higher utilization ratio of light energy. Yellow flower color in rapeseed is recessive compared to white flower color in rapeseed, and is maintained in evolution. The petals of almost all rapeseed cultivars are yellow, which can result in aesthetic fatigue from an ornamental perspective, and is hence not beneficial to sustained development of the ornamental rapeseed industry. The addition of another bright color system, e.g., pure red, purple or even blue, would greatly improve the prospects for development of rapeseed as an ornamental attraction. The development of additional flower colors in rapeseed is therefore a high priority.

3.2. The Molecular Mechanisms of Flower Color

Pigments can generally be classified into three groups: carotenoids, flavonoids, and alkaloids. The presence of pigments, such as blue to red anthocyanins, yellow to reddish carotenoids, or red betalains, make flowers exhibit different colors [56]. Carotenoids may exhibit brilliant red, orange and yellow [57]. The processes of both anthocyanin synthesis and carotenoid synthesis and degradation are highly conserved across angiosperms [58]. The presence, type, and amount of carotenoid pigment contribute to substantial variation in flower color [59]. Petals of many different species contain carotenoids, but the exact compositions vary between and sometimes within species [60]. Carotenoids and flavonoids are deposited in the cytoplasmic plastids, and in vacuoles, respectively. Carotenoids are one of the most widely distributed pigments, and are found in many organs in higher plants, such as flowers, fruits, leaves and roots. Carotenoids contain two major categories: carotene and lutein. In Osmanthus fragrans, yellow petals have less β-carotene, golden yellow petals contain a large quantity of lutein, but a small quantity of α-carotene and β-carotene, and orange–red petals contain a high level of α-carotene and β-carotene [61].

Flavonoids, which are widely distributed in plants, belong to a large class of secondary metabolites [62]. Water soluble flavonoids, as one of most important pigment groups, show the full spectrum of colors, varying from pale yellow to blue-purple [60]. Anthocyanin, as a major class of flavonoid, exhibits a wide range of colors, from red and pink series to blue-violet [60]. Other flavonoids produce a pure yellow series, from deep yellow, controlled by chalcone and aurone, to light yellow or nearly colorless, regulated by flavones, flavonols and flavanones [60].

The regulation of key rate-limiting enzymes (e.g., chalcone synthase, CHS) may change flower colors in the flavonoid biosynthetic pathway. Transgenic petunia expressing FhCHS1 from Freesia hybrida changed flower color from white to pink [63]. Similarly, transgenic tobacco plants constitutively expressing McCHS from Malus (crabapple) had increased anthocyanin accumulation and a deeper red petal color in contrast to untransformed control lines [64].

Delphinidin-based anthocyanins are the major constituents of violet and blue flowers. Six major classes of anthocyanidins are predominant in nature, including pelargonidin, cyanidin, peonidin, delphinidin, petunidin and malvidin [65]. More than 600 anthocyanins have been found, with core anthocyanidins varying in their side chain decorations [65]. The anthocyanin color is affected by the number of hydroxyl groups on the B-ring of the anthocyanidins: the more hydroxyl groups present, the bluer the color. A flavonoid 3’,5’-hydroxylase gene, as a key enzyme controlling delphinidin biosynthesis, has previously been genetically engineered to establish an exclusive accumulation of delphinidin (Dp)-type anthocyanins and make petals bluish in some plants, such as carnations, roses and chrysanthemums, but appearance of a true blue color was developed by modifying anthocyanins with multiple aromatic acyl groups (often referred to as polyacylated anthocyanins) [66]. Two cytochrome P450s, flavonoid 3’-hydroxylase (F3’H) and flavonoid 3’,5’-hydroxylase (F3’5’H), determine the hydroxylation pattern which controls flower color. Most F3’H and F3’5’H are CYP75B and CYP75A, respectively, with the exception of the F3’5’Hs arising from gene duplication and variation of CYP75B in Compositae [67]. The lack of delphinidin-related F3’5’Hs results in a lack of naturally occurring blue/violet flower colors in roses and carnations. Therefore, expressing F3’5’H coding regions can result in the emergence of carnations and roses with novel blue colors [67]. Similarly, expressing violet F3’5’H genes in some Rosa hybrida cultivars led to the accumulation of numerous delphinidins and the appearance of a novel bluish flower color [68]. Suppression of an enzyme (flavonoid 3’, 5’-hydroxylase (F3’5’H)) in the flavonoid pathway of cyclamen flowers via antisense inhibition led to reduction of delphinidin-derived pigment levels, but an increase in cyanidin-derived pigment content, resulting in a shift of the petal color from purple to red/pink [69]. In addition, RNAi-mediated suppression of anthocyanin 5,3’-aromatic acyltransferase (5/3’AT) and flavonoid 3’,5’-hydroxylase (F3’5’H) expression led to lilac and pale-blue flower colors [70].

The color stability of anthocyanins can also be affected by light, temperature, pH, oxidants and reducing reagents [71,72]. For instance, acidic pH makes anthocyanins red, neutral or nearly neutral pH leads to lack of color and alkaline pH produces blue colors. A vacuolar iron transporter, TgVit1, plays an important role in blue coloration in tulip petals through iron accumulation [73]. Mutation of PH5 (a P(3A)-ATPase proton pump) decreased vacuolar acidification in petunia petals, also resulting in a blue flower color [74].

3.3. How to Breed Rapeseed of Different Colors

To date, research related to flower color in rapeseed has mainly focused on the genetics of white and orange flowers, with a few reports related to genetic mechanisms and gene identification. For example, in Brassica species, the insertion of a CACTA-like transposable element in a coding region of a carotenoid cleavage dioxygenase 4 gene was found to lead to disruption of gene expression, switching flower color from white to yellow [75]. In addition, the major volatile apocarotenoid in white rapeseed petals was determined to be alpha-ionone, which is not the case for yellow petals [75]. In the molecular mechanism of yellow to orange flower formation in rapeseed, a zeaxanthin epoxidase encoding gene was discovered, which catalyzes the conversion of zeaxanthin to antherxanthin and violaxanthin, knocked out this gene by CRISPR/Cas9 technique, it was found that the accumulation of lutein in the petals increased, and the petals were changed from yellow to orange [76]. A mutation in a phytoene desaturase 3 gene in the yellow-white petal mutant interrupted the carotenoid biosynthesis pathway in ywf, resulting in a decrease in carotenoid content and a yellow-white petal phenotype [55].

There are two major avenues to produce new flower colors in rapeseed. The first method is to alter the intrinsic pigment composition and content in the petals. For this method, it is important to know how the genes in the carotenoid synthesis pathway mutate or can be mutated to modify flower color without affecting basic plant physiology [59]. Many ornamental plant species show a limited range of flower color because of the presence of limited kinds of flavonoids. Overexpressing heterologous genes and/or down regulating endogenous genes in flavonoid biosynthesis pathways can be used to alter flower color [77,78]. The well-characterized flavonoid biosynthesis pathway is often metabolically engineered to change anthocyanin profiles and then to enrich flower color, as previously discussed. However, little research in this area has been reported in rapeseed.

The second major method for altering flower color in rapeseed is to import new genes or alleles affecting petal pigmentation using wide hybridization or transgenic techniques. The success of quite distant hybridization is critical for the introgression of flower color into rapeseed, as only wilder relatives contain useful variation in flower color. Hence, some additional biotechnological means are required to enhance the success rate of hybridization, such as embryo rescue, multiple pollinations and pollination after grafting. The crucifer Orychophragmus violaceus is widely cultivated as an ornamental plant for its beautiful purple flowers, and can be hybridized with rapeseed with some difficulty [22]. A homolog of AtPAP2 (Arabidopsis Production of Anthocyanin Pigment 2) was identified by transcriptomic analysis using a B. napus—O. violaceus disomic chromosome addition line exhibiting slightly red petals. The ectopic expression of the OvPAP2 gene can produce red-flowering oilseed rape, enhancing its ornamental value [22]. This approach successfully produced red-flowering rapeseed, but more research is still required to improve the color intensity, and application of this line in practice is limited by transgenic regulations.

According to the Announcement of Variety Rights on 1 September 2017 (No. 109) from the Office for the Protection of New Plant Varieties, the Ministry of Agriculture of China, the group of Xiaolan Li first developed rapeseed with red and purple flower colors, although with variation in not only the depth and shade of color observed, but also in production of normal pollen grains and in seed setting ability. They crossed one purple-flowering radish (Raphanus) landrace as a donor with rapeseed, and used backcrossing and self-pollination to obtain one plant with slightly red flower color. This plant was self-pollinated, crossed with common yellow and white B. napus with excellent comprehensive properties, and continuous rounds of selection were undertaken on the progeny to finally obtain more than ten colors, including purple, red, deep red and mottled flower colors (Figure 5). This process has resulted in five new protected plant varieties (Announcement of Variety Rights on 1 September 2017 (No. 109), which constitute the first rapeseed varieties with varying flower colors which can be widely applied in production.

Certainly, there are several other important Cruciferae species that are also used as ornamental plants (Figure 6), such as Matthiola incana, which has purple, pink or white flowers [79], Aubrieta x cultorum, with purple, violet or white flowers [80], Cheiranthus allionii, with yellow and orange flower types, Hesperis matronalis with white, lilac, or purple flowers [80], Iberis umbellata, with red and purple-red flowers and spherical inflorescences [81], radish (Raphanus sativus) with red, purple, and white flower types [82], and Heliophila coronopifolia with blue flowers [81]. These species can be used as donors of elite flowering color germplasm into rapeseed by hybridization or transgenic modification. As red- and purple-flowering rapeseed have now been developed, the major focus should be on creating blue-flowering rapeseed, although this is difficult because of the lack of pure blue flowers in Cruciferae species. One option could be to produce blue colors via manipulating the delphinidin-related F3’5’H gene derived from the pure blue flower of Delphinium ajacis (Figure 7).

4. Conclusions

Rapeseed has developed rapidly as an ornamental plant, and its economic value has risen sharply, especially in rural areas of China, bringing considerable economic value to rapeseed growers. However, there are two major hindrances to further development: a short flowering period and a monotonous flower color (Figure 8). To make full use of the ornamental value of rapeseed, the guiding principle is to produce rapeseed with optimal vegetative and flowering growth. First and foremost, this review discusses the factors that affect the flowering period, and proposes that each rapeseed variety produced as an ornamental plant should be grown in the optimal environment correspondingly, the flowering period can be adjusted by temperature, light, water and soil conditions, cultivation and planting methods, and cultivation systems (including sowing time, fertilization amount and fertilization time, thinning time and planting density). Secondly, cultivating rapeseed varieties with a long flowering period and rich color variety is the most direct and effective means to enhance the ornamental value of rapeseed. Creating new flower colors can be achieved through gene pyramiding, wide hybridization with other Cruciferae ornamental plants, or transgenic approaches. Red- and purple-flowering rapeseed varieties have already been developed (Xiaolan Li, pers. comm, 2018). The greatest difficulty is expected in creating blue-flowering rapeseed, but this may be possible by manipulating the delphinidin-related F3’5’H gene derived from blue-flowering Delphinium ajacis. More information is also required about the genetic determination of flower color in Brassica species, such as the number of genes controlling flower color, the dominant or recessive effects of genes and alleles, heritability and the corresponding molecular mechanisms. With the solution of these problems and the release of colorful and long-flowering cultivars, rapeseed can greatly increase its economic value as an ornamental as a novel functional utilization.