Roses (
Rosa hybrida) are cultivated throughout the world and are an economically important ornamental plant worldwide. Roses are most admired for their beauty and fragrance, and they exhibit alluring colors. Within the
Rosa genus, there are more than 200 rose species and over 30,000 cultivars. They are used as cut flowers, pot plants, and garden plants
[23]. Rose-petal essential oils consist of beneficial secondary metabolites that are used in the natural medicine, cosmetics, and perfume industries
[24]. However, rose cultivation is severely impaired by major fungal diseases such as powdery mildew, black spots, botrytis blight, downy mildew, and rust that adversely affect yields and product quality
[25]. Despite the economic importance of the rose as an ornamental crop, breeding progress for fungal resistance is lagging in roses due to insufficient information regarding disease-resistant traits. Moreover, a higher level of heterozygosity, sterility, and polyploidy are the major limitations of traditional breeding for fungal disease resistance in roses
[26]. Hence, genetic engineering is a desirable approach to induce resistance against fungal diseases. Powdery mildew caused by the obligate ascomycete pathogen
Podosphaera pannosa (Wallr.: Fr.) is one of the predominant fungal diseases of rose. It causes distortion and senescence of the leaves and shoots. Approximately 40% of the fungicide sprayed on cut and potted roses is used to control powdery mildew
[27]. It is known that PR genes, including
β-1,3-glucanase,
chitinase,
ribosome-inactivating protein (
RIP), and
cysteine-rich antimicrobial protein (
AMP), are triggered during fungal pathogen infections
[28][29]. These antifungal proteins, including chitinases, glucanases, RIPs, plant defensins, and proteinase inhibitors, function by disrupting or suppressing the synthesis of the fungal cell wall. Some of these proteins interact with potential intracellular targets and the plasma membrane of fungi, thus leading to changes in membrane potential and cell death
[30]. Plant defensins, including AMPs, are known to interact with glucosylceramides within fungal membranes to induce membrane permeabilization, ultimately leading to fungal cell death
[31]. An antimicrobial protein gene (
Ace-AMP1) isolated from onion seeds that possessed higher plant pathogenic inhibition activity, was introduced into the
Rosa hybrida cv. Carefree Beauty. The transgenic rose, overexpressing the
Ace-AMP1 gene, was developed to induce fungal disease resistance, and the rose showed enhanced resistance to powdery mildew disease
[32]. Furthermore, the transgenic rose, overexpressing antifungal genes such as
class II chitinase and
type I ribosome inhibiting protein (
RIP), exhibited reduced susceptibility to fungal diseases
[25]. Transgenic rose plants possessing a high level of expression of the rice
chitinase gene displayed improved resistance to powdery mildew
[33]. Previous studies suggested that loss-of-function mutations in mildew resistance locus- o (
Mlo) genes confer broad-spectrum resistance against pathogens, and hence,
Mlo genes can confer an effective race-independent resistance in several crops
[34][35]. Although the mechanism underlying
MLO-based disease resistance remains unclear, some of their family members function by regulating fungal-penetration resistance by controlling vesicle fusion events
[36]. Indeed, Qiu et al. (2015) generated transgenic
Rosa multiflora expressing an antisense
RhMLO1 that exhibited enhanced resistance to powdery mildew
[37]. Xiang et al. (2019) recently identified two
MLO members,
RgMLO6 and
RlMLO7, that are potential candidate genes that can induce resistance to powdery mildew in
Rosa species
[38]. Black spot disease is another major fungal disease caused by
Diplocarpon rosae Wolf, a hemibiotrophic ascomycete. It is one of the most devastating and widespread fungal diseases of the rose and leads to huge economic losses
[39]. Black and brown spots appear on leaves as the representative symptoms of the disease and, eventually, immature leaves become weak and fall from the plant. Defoliation decreases the photosynthetic area of plants, thus leading to a reduction in plant vibrance, thereby drastically lowering its ornamental value. A rice
chitinase gene introduced into the rose-susceptible cultivar ‘Glad Tidings’ by particle bombardment conferred reduced susceptibility to black spot disease
[40]. The black-spot-susceptible rose cultivars ‘Heckenzauber’ and ‘Pariser Charme’ were transformed with
chitinases,
glucanases, and
RIPs from barley, and the transgenic plants exhibited a reduction of 40% in black spot diseases compared to that of the control
[25]. Terefe-Ayana et al. (2011) reported the
Rdr1 locus as important for resistance to black spot diseases in roses, and this is useful for applications in rose breeding, including the use of genetic modification technology
[41]. Recently, transcriptomic analyses of roses responding to the two fungal pathogens,
D. rosae (black spot) and
P. pannosa (powdery mildew), demonstrated that the genes related to common defense mechanisms were upregulated in black spot and that those related to photosynthesis and cell-wall modification were downregulated for powdery mildew, thus implying that distinct cellular responses are stimulated by different fungal pathogens, even in the same host
[42].
B. cinerea is a notorious fungal pathogen responsible for gray mold disease in roses.
B. cinerea conidia secretes phytotoxins and secondary metabolites during penetration into the host epidermis, ultimately causing host cell death
[43]. Necrotic local lesions on petals are the major symptoms of
B. cinerea infection in roses, and these infections rapidly develop during postharvest transport when the flowers are packed in boxes with a high relative humidity
[44]. Petals are economically important organs, and when they are damaged, this causes large commercial losses in the rose industry. Despite its economic importance as a predominant pathogen, studies examining
B. cinerea infections in roses are limited to the comparisons of pathogen behavior in model plants such as
Arabidopsis [45]. Recently, transcriptomic analyses of rose petals infected by
B. cinerea determined that
RcERF099, a gene that encodes member of the AP2/ERF transcription factor family, is involved in the regulation of resistance against
B. cinerea in rose flowers, and this finding can provide a stepping stone for further studies aiming to improve gray mold disease resistance in roses
[46].