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Review

Bakanae Disease Resistance in Rice: Current Status and Future Considerations

by
Liwei Zhan
3,
Ling Chen
1,2,
Yuxuan Hou
1,
Yuxiang Zeng
1 and
Zhijuan Ji
1,2,*
1
China National Center for Rice Improvement, China National Rice Research Institute, No. 359 Tiyuchang Road, Hangzhou 310006, China
2
National Nanfan Research Institute (Sanya), Chinese Academy of Agricultural Sciences, Sanya 572025, China
3
Zhejiang Wuwangnong Seeds Shareholding Co., Ltd., No. 818 Jiansheyi Road, Hangzhou 310006, China
*
Author to whom correspondence should be addressed.
Agronomy 2024, 14(7), 1507; https://doi.org/10.3390/agronomy14071507
Submission received: 31 May 2024 / Revised: 9 July 2024 / Accepted: 10 July 2024 / Published: 11 July 2024
(This article belongs to the Special Issue Innovative Research on Rice Breeding and Genetics)
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Abstract

:
Bakanae disease is mainly caused by Fusarium fujikuroi and is a significant fungal disease with a number of disastrous consequences. It causes great losses in rice production. However, few studies have focused on the details of bakanae disease resistance in rice. Here, we summarize and discuss the progress of bakanae disease resistance in rice. Besides rice germplasm screening and resistance-related gene/quantitative trait locus (QTL) exploration, the route of pathogen invasion in rice plants was determined. We further discussed the regulation of phytohormone-related genes and changes in endogenous phytohormones in rice plants that are induced by the pathogen. To achieve better control of bakanae disease, the use of natural fungicides was assessed in this review. During rice—F. fujikuroi interactions, the infection processes and spatial distribution of F. fujikuroi in infected seedlings and adult plants exhibit different trends. Fungal growth normally occurs both in resistant and susceptible cultivars, with less abundance in the former. Generally, bakanae disease is seed-borne, and seed disinfection using effective fungicides should always be the first and main option to better control the disease. Besides the friendly and effective measure of using natural fungicides, breeding and utilization of resistant rice cultivars is also an effective control method. To some extent, rice cultivars with low grain quality, indica subspecies, and some dwarf or semi-dwarf rice germplasms are more resistant to bakanae disease. Although no highly resistant germplasms were obtained, 37 QTLs were located, with almost half of the QTLs being located on chromosome 1. Using omics methods, WRKYs and MAPKs were usually found to be regulated during rice—F. fujikuroi interactions. The regulation of certain phytohormone-related genes and changes in some endogenous phytohormones induced by the pathogen were clear, i.e., it downregulated gibberellin-related genes and repressed endogenous gibberellins in resistant genotypes, but the opposite results were noted in susceptible rice genotypes. Overall, exploring resistant germplasms or resistance-related genes/QTLs for the breeding of rice with bakanae disease resistance, expanding research on the complex mechanism of rice—F. fujikuroi interactions, and using cost-effective and eco-friendly innovative control methods against the disease are necessary for present and future bakanae disease management.

1. Background

Rice is one of the most important staple food crops globally. It is planted under diverse ecological conditions and thus suffers different biotic and abiotic stresses. Among the biotic stresses, bakanae disease (BD) is an important fungal disease that is mainly caused by Fusarium fujikuroi. It is one of the most serious and widespread problems in rice-growing countries in Asia, Africa, North America, and Europe. The incidence of BD is predicted to increase with the temperature due to global warming [1]. To date, no rice cultivars have been reported to be completely resistant to this disease.
Research on BD has a long history, and the disease was first reported in 1828 in Japan [2]. Bakanae means “foolish seedling”, “naughty seedling”, or “stupid rice crop”, and it was named so due to the abnormal growth of rice plants it caused after infection. This disease is typically seed-borne but may occur when the pathogen is present in plant materials or soils [3]. Infected seeds/plants result in secondary infections, which spread through wind or water. The disease occurs both in the nursery and transplanted stage, with typical symptoms of abnormal elongation, tall and lanky tillers, pale green flag leaves, dried-up leaves, infertile panicles with an angle of leaf insertion that is wider than in healthy seedlings, and the formation of adventitious roots at the nodes of adult plants (Figure 1, [4,5,6,7]). Losses in rice production caused by BD range from 30% to 95% [8,9,10,11,12].
There are various management practices to control BD, which include thermal seed treatment through hot water immersion, chemical fungicides, natural fungicides (biocontrol agents, plant-derived biomolecules, and abiotic elicitors), and breeding of resistant rice cultivars. The method of immersing infected rice seeds in hot water for 10–20 min at 58–60 °C effectively disinfects the seeds. However, it was demonstrated to be ineffective on severely infected rice seeds, because the thermal effect is usually not efficiently transmitted to the pericarp layers [13] or because there is no guarantee of a precise water temperature to completely eliminate the pathogenic fungi on the infected rice seeds [14]. Chemical control is the most effective method [14,15,16,17,18,19,20,21,22], including single or combined application of benzimidazoles, sterol demethylase inhibitors, or other fungicides, and has been widely used in most rice-growing areas [14]. During seed disinfection with chemical fungicides, using a higher-temperature disinfectant solution or mixed solution of seed disinfectants tends to achieve better effects in controlling BD [23]. The mycelial growth and spore germination of F. fujikuroi are rapidly inhibited under such treatment. However, the pathogenic fungi constantly develop resistance to fungicides through point mutations and threaten rice production. The effect of seed disinfection using chemical fungicides can be lowered by resistant strains at any time.
Therefore, the efficacy of these methods is often insufficient, and developing alternative and innovative control methods is imperative. Natural fungicides include biocontrol agents, plant-derived biomolecules, abiotic elicitors, etc. Controls using natural fungicides are effective against bacteria and fungi, with the benefits of being safe and environmentally friendly, which means that they can efficiently suppress the spore formation, spore germination, and mycelial growth of F. fujikuroi. In addition to the methods mentioned above, breeding resistant rice cultivars is an eco-friendly and cost-effective way to control the disease, though there are currently few resistant rice resources. Screening resistant germplasms and excavating resistant genes/QTLs are the foundations of breeding cultivars with BD resistance. Based on these, rice cultivars can be improved with resistant genes and applied as effective and durable controls of BD.
In this paper, in addition to rice germplasm screening and resistance-related gene/QTL exploration, we review aspects of the invasion route of the pathogen to rice plants, the regulation of phytohormone-related genes, changes in endogenous phytohormones in the rice plants induced by the pathogen, and natural fungicide controls of the disease to pave the way for a better management of BD.

2. Fungal Invasion and Colonization during F. fujikuroi—Rice Interactions

Four anamorphs in the Gibberella fujikuroi species complex, F. fujikuroi, Fusarium proliferatum, Fusarium Verticillioides, and Fusarium andiyazi have been associated with BD in rice [11]. However, F. fujikuroi is the most predominant and virulent of these species associated with disease induction and is considered the major cause of this disease in field conditions [24]. In addition, it is the only species that can secrete gibberellins (GAs), which is a family of hormones. Gibberellic acid (GA3) could result in an abnormal elongation of seedlings, which is a typical symptom of BD.
Upon receiving chemical signals exuded from the roots of a germinated seedling, especially sugar and amino acids, F. fujikuroi started invading the plant through the root or crown/basal tissues [25]. With further invasion, the infection processes of F. fujikuroi were different at different growth stages of the rice plants. In rice seedlings, F. fujikuroi hyphae were found to directly penetrate the epidermis of basal stems and roots and then extend inter- and intracellularly to invade the vascular bundles. However, in adult plants, the occlusion of vascular bundles and radial hyphal expansion from vascular bundles to the surrounding parenchyma were observed [4]. With the use of light microscopy and scanning electron microscopy (SEM), different types of infectious structures, such as swollen tip hyphae, infection cushions, and appressoria, were found to be formed during the infection [26].
In the process of F. fujikuroi infection and colonization, the levels of fungal growth were different between susceptible and resistant cultivars. Using laser scanning confocal microscopy (LSCM) and gfp-expressing F. fujikuroi isolates, the fungal growth was shown to occur in both resistant and susceptible cultivars, with abundance in the stem of susceptible rice cultivars [27] and less abundance in resistant cultivars [3,27,28] during F. fujikuroi—rice interactions. Carneiro et al. [29] obtained the same result while developing a TaqMan real-time PCR assay to detect F. fujikuroi in different rice tissues. However, Chen et al. [4] found that the severity of symptoms did not necessarily correlate with the quantity of F. fujikuroi, since similar infection processes and F. fujikuroi biomasses were observed within 21 dpi (days post inoculation) in susceptible and resistant rice cultivars. Chen et al. [30] observed a weak correlation between the disease’s severity index and colonization rate.
Elshafey et al. [31] demonstrated that F. fujikuroi preferentially grew in the aerenchym, pith, cortex, and vascular bundle of both the sheath and stem of rice. An investigation showed that the spatial distributions of F. fujikuroi were characteristic at different rice-growing stages. In the seedling stages, F. fujikuroi was largely confined to the embryo, basal stem, and basal roots, while it was distributed unevenly in the lower aerial parts (including nodes and internodes) of adult plants, with the maximum level of colonization occurring in the middle portion of the stem [4]. The distributions of F. fujikuroi in infected seeds were predominantly reported in the lemma and palea, followed by the embryo [32]. The transmission of F. fujikuroi was different at different rice-growing stages. After artificial inoculation on the rice seeds, seedlings, and florets, i.e., the three stages of rice growth, the maximum transmission of the pathogen was on the florets (45.00%, air-borne inoculum), followed by seedlings (33.25%, soil-borne inoculum) and seeds (30.50%), in a highly susceptible genotype, Pusa Basmati 1509 [26].
Infected plant parts such as seeds, dead culms, kernels, stubble, roots, and crowns serve as the carrier materials for the pathogen from one cropping season to another. However, the dispersal of infected seeds with rice hulls (lemma and palea), which is the central component of the BD cycle, is the predominant source of primary inoculum, which induces the disease [25]. When infection occurs during the heading stage, it contaminates rice seeds [9], which might result in the following year’s new inoculum.
As a result, it is suggested that different control methods against BD should be adopted due to the different styles of fungal invasion and colonization of F. fujikuroi at different rice-growing stages, and seed disinfection should always be the first and main method of disease control.

3. Screening of Rice Germplasms That Are Resistant to BD

As is well known, the most eco-friendly and cost-efficient control method is the use of resistant rice cultivars. However, to date, most rice cultivars are susceptible or only moderately resistant to BD, and no highly resistant germplasms have been reported [33,34,35].
It was found that fine aromatic Basmati rice was more susceptible to BD than coarse rice genotypes [36]. Recently, 90 short-grained aromatic rice genotypes were evaluated against the bakanae disease. Of these, 21 genotypes—Kankjeer A, Lectimanchi-A, Sumati, Pankhali-203, GR-102, NWGR-3042, Geetanjali, R 1432-261-105-2-1-2, Khaskani, C-4-63-G, Calrose 76, JJ 92, Koliha, Hari Shankar, Kusuma, IR 74717-3-3-1-3, IR 74725-115-3-3-3, IR 74728-134-1-1-3, Hansraj, Anterved, and GAR-1—were identified as moderately resistant. Different parameters of disease severity were used for the evaluation, including the root length, shoot length, number of fibers/threads in roots, days of symptom appearance, and area under disease progress curve (AUDPC). Only the AUDPC evaluation method revealed no disease or zero AUDPC in the moderately resistant genotypes such as Chanan, JJ 92, Koliha, IR 74725-115-3-3-3, IR 74728-134-1-1-3, and Anterved. The results suggested that disease severity criteria alone would easily lead to wrong conclusions [37]. We recommend that BD resistance should be evaluated using resistant and susceptible genotype controls and multiple parameters of the disease severity to ensure a relatively accurate conclusion.
Chen et al. [30] observed lower BD severity indices for the indica subgroup than for the japonica subgroup, which is consistent with the comment by Ji [38] that “indica better defends from the invasion of pests and diseases than japonica”. Lee et al. [27] reported a BD-resistant japonica cultivar, Wonseadaesoo, with a proportion of healthy plants of 65.7% compared to the 11.0% proportion of healthy plants in the susceptible japonica cultivar Junam. Lee et al. [39] found that Tung Ting Wan Hien1 was resistant and Ilpum was highly susceptible, with proportions of healthy plants of 77% and 36.9%, respectively. In any case, there were still certain percentages of unhealthy plants in resistant cultivars, and highly resistant cultivars or germplasms have not been reported to date.
Due to GA3 secretion by F. fujikuroi and the abnormal elongation of seedlings, germplasms with different dwarf genes with different sensitivities to GA3 have been evaluated for BD resistance [4,40]. The treatment of rice seeds with 0.5 mg/L GA3 resulted in more significant elongation of seedlings in the susceptible rice cultivar ZK than in a resistant TNG67, suggesting that the susceptibility of ZK to bakanae is associated with its higher sensitivity to GA3 [4]. However, Ma et al. [40] found that materials carrying the sd1 gene, which is sensitive to GA3, and materials carrying the d1 gene, which is insensitive to GA3, were both susceptible to BD. Materials carrying the d29, sd6, or sdq(t) genes showed resistance to BD, of which only materials carrying sd6 were insensitive to GA3. Therefore, BD resistance may not be directly attributable to the GA response in some rice genotypes [41]. Hence, the efficiency of the method that Hossain et al. [42] used, in which they screened resistant rice cultivars from huge germplasm collections using different concentrations of GA instead of the pathogen to assess disease induction, is debatable.

4. Mapping of QTLs Related to BD Resistance in Rice

Traditional QTL mapping methods were used to explore QTLs related to BD resistance. The first report about QTLs associated with BD resistance was that by Yang et al. [43], who reported two QTLs located on chromosome 1 and chromosome 10 (qB1 and qB10) by means of in vitro evaluation of the Chunjiang 06/TN1 doubled haploid (DH) population. After ten years, Hur et al. [27] identified a major QTL (qBK1) on chromosome 1 using near-isogenic lines (NILs) and further delimited the location of the qBK1 to the 35 kb interval between two InDel markers, InDel 18 (23.637 Mbp) and InDel 19-14 (23.672 Mbp), within four candidate genes [44]. One candidate gene, LOC_Os01g41800, encodes a putative cytochrome P450 monooxygenase and appears to be a positive regulator of BD resistance. Subsequently, using different recombinant inbred lines (RILs), a series of QTLs were identified [3,27,38,45].
GWAS (Genome-Wide Association Study), SNP (single-nucleotide polymorphism), and KASP (competitive allele-specific polymerase chain reaction) approaches were applied to the QTL mapping as well. Using the GWAS approach, 17 QTLs were identified [5,30,39]. Therein, a candidate QTL (qBK1.7) was colocalized with the previously identified QTLs, qBK1 and qFfR1. Through resequencing and SNP analysis, Ji et al. [1] mapped a major QTL (qFfR1) on chromosome 1, and Kang et al. [46] discovered a QTL, qFfR9, on chromosome 9. Cheon et al. [47] revealed a major QTL, qFfR1-1 (21.36–24.37 Mb), which overlapped with the qFfR1 (23.32–23.34 Mb) region, and a novel QTL, qFfR6, on chromosome 6 after designing KASP assays.
In summary, using different mapping populations and approaches, a total of 37 QTLs with PVEs ranging from 4.8% to 65.0% for BD resistance were mapped on chromosomes 1, 3, 4, 6, 8, 9, 10, and 11 (Figure 2; Table 1). The QTL distribution on chromosomes is partially consistent with the distribution of DEGs, with the highest number of QTLs being found on chromosomes 1, 3, and 10 of a resistant genotype [48]. Chromosome 1, where 17 QTLs were mapped, appears to be particularly important.
Although it was thought that QTL-assisted breeding suffers from certain limitations, Lee et al. [27] applied QTL pyramiding to rice breeding for BD resistance and obtained a positive result. They pyramided two QTLs (qBK1WD and qBK1) into a single rice plant and found that its BD resistance was significantly higher than those plants with only one QTL. The two QTLs accounted for 20.2% and 65.0% of the total phenotypic variation (Table 1), respectively, which might be why the QTL pyramiding worked. Hence, further QTL mapping is necessary to mine QTLs with high PVEs.

5. BD-Resistance-Related Genes Explored Using Omics Methods

With the development of omics technologies and bioinformatics approaches, transcriptome and proteome analyses were used to dissect rice plants’ responses to F. fujikuroi [48,50,51,52], and a series of key transcription factors were detected.
WRKY transcription factors and mitogen-activated protein kinases (MAPKs) play important roles in many resistance-mediated defense responses to plant pathogens [53]. Through RNA-seq profiling, defense-related genes, such as OsWRK1, −28, −107, −13, −71, −62, −76, −19, and −50; OsMAPKKK63; OsMKKK55; OsMKK4; and OsMPK3, were commonly induced during rice—F. fujikuroi interactions [48,50,52]. Moreover, Matić et al. [52] found that some cytochrome P450 genes involved in the production of defense-related metabolites were only highly expressed in the resistant cultivar Selenio.
Chitinases are proteins that are involved in plant defenses against pathogens due to their ability to hydrolyze chitin in the cell wall of fungi [54]. After F. fujikuroi infection, chitinases were upregulated at 3 dpi in the resistant cultivar Selenio during the incompatible interactions between rice and F. fujikuroi [28,52], which has also been reported during the incompatible interactions between rice and M. oryzae [55]. However, besides the upregulation of chitinase expression in the resistant cultivar Selenio, this was also demonstrated in the susceptible Dorella with more upregulated chitinase genes, which might be a result of fungal colonization of plant cells and the subsequent activation of fungal cell wall degradation [52].
With the development of proteomics, Ji et al. [51] first investigated rice—F. fujikuroi interactions employing the tandem mass tag (TMT) technique. The aquaporin protein PIP2-2 and vacuolar-sorting receptor 3 were significantly upregulated in resistant 93–11. Antifungal proteins such as defensin, peroxidase, and ribonuclease were moderately regulated in both 93–11 and the susceptible Nipponbare. Furthermore, a correlation analysis of the available transcriptomic and proteomic data revealed an intriguing result, with a significant positive correlation in the resistant 93-11 but not in the susceptible Nipponbare, which was hypothesized to be due to the difference in codon usage between the two genotypes under disease stress.

6. Phytohormone-Related Genes and Endogenous Phytohormones during Rice—F. fujikuroi Interactions

Endogenous phytohormones such as jasmonic acid (JA), salicylic acid (SA), and GA are reported to be involved in defense processes [52,56,57]. In addition, GA is antagonistic against JA, and they both play central roles in rice—F. fujikuroi interactions [58].
During rice—F. fujikuroi interactions, host plants are regulated by JA-dependent signaling, and GAs suppress the JA signaling pathway. GAs produced by F. fujikuroi and the host plant could also participate in the regulation of JA signaling through the degradation of DELLA proteins (the repressors of OsJAZs) [50]. The OsJAZ genes encode negative regulators of JA signaling that confer immunity against F. fujikuroi.
By modulating the production of GAs, rice plants are coordinating their level of tolerance to BD, possibly through interactions of the GA-signaling molecules with components of the JA signaling pathway [52]. It has been reported that 7 dpi might be too early to detect the difference in JA signaling pathway genes between resistant and susceptible cultivars [50]. At 21 dpi, genes associated with JA signaling were upregulated in resistant cultivars but downregulated in susceptible cultivars, and genes related to the GA metabolic process were upregulated in susceptible cultivars but downregulated in resistant cultivars [52]. Song et al. [58] demonstrated that OsWRKY114 increased resistance to F. fujikuroi by repressing GA signaling and downregulating OsJAZ genes.
Concerning the chemical response of rice to F. fujikuroi infection, it was elucidated that Sakuranetin (one kind of phytoalexin) was induced, and GAs and ABAs (abscisic acids) were repressed in resistant cultivars. Furthermore, the inverse situation was demonstrated in susceptible genotypes with induced GAs and ABAs following the inhibition of JA production [59]. In our recent research, following overexpression (OE) of a bakanae-resistance-related gene, resistance to bakanae was demonstrated in the OE lines compared with their wild genotypes. An assay of endogenous phytohormones of seedlings after 7 dpi showed that the OE lines demonstrated about a 5-fold increase in GA3 content, but only about 20 percent of the over 25-fold increase in the wild line. Furthermore, no significant variation was found in the contents of JA and ABA between the OE and wild lines (data not published).
Therefore, more studies on phytohormone-related genes and endogenous phytohormones are needed to clarify the complicated yet ordered interplay between the endogenous phytohormones and rice—F. fujikuroi interactions.

7. Natural Fungicides for Controlling Bakanae

The current situation, which includes a lack of rice resources that are highly resistant to BD and the high cost of chemical fungicides and their negative impact on the environment, prompted the search for natural fungicides such as biocontrol agents or abiotic elicitors. Natural fungicides are derived from a natural source such as microorganisms, bacteria, fungi, plants, animals, and certain minerals [60]. The agents are effective against bacteria and fungi, etc., with the benefits of being safe and environmentally friendly. They therefore efficiently suppress the spore formation, spore germination, and mycelial growth of F. fujikuroi.
Biocontrol agents are mainly indigenous antagonistic pathogens obtained from certain crop rhizospheres. They produce various secondary metabolites, including siderophores, hydrolytic enzymes, and antibiotics, to effectively control BD in rice [61,62]. For example, the crude extract of the RC2 strain of endophytic Streptomyces albus isolated from plants led to strong growth inhibition of F. fujikuroi and suppression of its spore germination to 87.4% ± 1.9%. The biocontrol potential of S. albus RC2 was highlighted due to its ability to produce various secondary metabolites [63]. Another novel endophytic bacterial strain, Bacillus oryzicola YC7007, isolated from rice roots, exhibited good biocontrol activity against BD, with direct decreases in disease severity ranging from 46% to 78%. Meanwhile, the strain was capable of inducing systemic resistance against the pathogen via primed induction of the JA pathway and could also promote rice plant growth [64]. Two highly antagonistic bacterial strains, viz Bacillus sp. KFP7 and KFP17, effectively reduced BD through the elicitation of peroxidase (POD) activity and increased grain yield in treated plants. POD is a major defense-related enzyme that scavenges reactive oxygen species (ROS) by acting as a high antioxidant. The strains induced the activity of POD and resulted in a reduced infection rate with F. fujikuroi [65]. Besides the endophytic bacteria mentioned above, certain endophytic fungi can also control rice bakanae disease effectively. It was reported that preinoculation of rice with the endophytic fungus Phomopsis liquidambaris B3 significantly reduced BD in rice by 21.45% by triggering the SA-dependent defense pathways of rice plants. Simultaneously, it promoted plant growth [66]. Saito H et al. [67] used nonpathogenic Fusarium commune W5 samples that were isolated from rice plant tissues to treat rice flowers by imitating the disease cycle of the bakanae pathogen. Their results showed that W5 inhibited the hyphal extension of F. fujikuroi on/in rice flowers and seedlings, possibly through competition, and W5 sprayed on flowers could survive on/in rice seeds for at least 6 months to control the disease in plants of the next generation. Shakeel Q et al. [14] summarized effectively that a series of bacteria and fungi could inhibit BD in rice, with decreases in disease severity ranging from 59.21% to 78% and 40.5 to 97.4%, respectively, through the application of dual culture, seed treatment, aerial spray, etc. The bacteria were different Pseudomonas species and Bacillus species, and the fungi were mainly Trichoderma, Penicillium, yeast, and included some other fungi.
Natural products also include extracts from plants and microbes. Microbial extracts such as Bacillus sp. extracts, i.e., surfactin A [61], or extracts of Paenibacillu polymyxa in the form of crude protein [68] effectively reduced F. fujikuroi growth. Plant-derived biomolecules such as aqueous extracts and essential oil from Tithonia diversifolia leaves were found to exhibit antimicrobial activities, with F. fujikuroi being sensitive to them under certain concentrations, which means that T. diversifolia is a potential source of natural fungicides against BD [69]. Other extracts from plants, such as Artemisia judaica, Eucalyptus globulus, Coriandrum sativum, Ammi visnaga [70], Cinnamomum tamala [71], Eucalyptus citriodora [72], Cymbopogon martini [73], and Mentha piperita [74], could also effectively suppress F. fujikuroi activity. After the onset of the F. fujikuroi infection, the application of silica nanoparticles formed from the husks of rice as a foliar spray could effectively decrease bakanae incidence [75].
Abiotic elicitors are being used as predisposing defense chemicals against plant pathogens [76] as they can stimulate the inherent defense mechanisms of the host plant against an invading pathogen and are environmentally safe and economically viable options for farmers [77]. For instance, potassium silicate (PS) and salicylic acid (SA) are known to play key roles in enhancing plant defense while being harmless to the environment. SA elicits plant resistance by including bi-signals that mediate the phenylpropanoid pathway to activate the acquired systemic resistance [78]. Meanwhile, silica mechanically thickens the cuticular layers in plants after a certain conversion to protect plants from pathogen infections [79]. It was reported that seed priming combined with SA (100 mg/L) and PS (1.0%) effectively controlled BD incidence through induced systemic resistance (ISR), with improved germination, root and shoot length, plant biomass, and seedling vigor in the rice plants [80].
Certain natural fungicides have multifunctional capacities, such as plant growth promotion and protection; however, besides antifungal effects, their unknown impacts on the soil microbiome and possible risks to food should also be considered. In summary, a thorough risk analysis before the application and marketing of fungicides regarding the application area’s surroundings is imperative.

8. Conclusions and Future Prospects

Although BD has been recognized for almost two decades and various aspects of BD have been well studied by different researchers, no highly resistant germplasms or genes/QTLs have been discovered for BD resistance in rice. Wide screening of more germplasms should be carried out. Research using GWASs, whole-genome techniques, and other new techniques to achieve BD resistance should be further promoted. Identifying new resistant genes from diverse resources is important for rice-breeding programs to acquire durable resistance against BD. In any case, breeding rice cultivars with a high resistance to BD is always the best strategy.
The correlation between the disease severity index and colonization rate for F. fujikuroi is disputable, whereas it is characteristic of the infection processes and spatial distribution of the pathogen, the regulation of BD-resistance-related genes, and the variation in endogenous phytohormones in the rice plants during plant–pathogen interactions. Further evaluation of not only morphological changes but also the complex mechanisms of rice—F. fujikuroi interactions will help to more accurately understand BD and better protect plants against it.
In terms of disease control, blocking the pathogen by using natural fungicides is an eco-friendly and effective method. However, the antifungal effects of these natural agents or fungicides occasionally showed a low and inconsistent efficacy under field conditions. Moreover, their mechanisms should be further explored as well. In addition, further analysis is required on the aspects of biosafety, compatibility with other beneficial organisms, regulatory issues for commercialization, etc., before they can be adopted in large-scale field applications [81].
In summary, blocking this disease in time, breeding resistant cultivars, and acquiring more effective antagonistic products as fungicides are three long-term goals for the development of BD control methods.

Author Contributions

Conceptualization, Z.J.; methodology, L.Z., Y.H. and Y.Z.; software, L.C.; validation, L.Z., L.C. and Z.J.; investigation, L.Z.; resources, L.Z.; data curation, Z.J., L.Z., Y.H. and Y.Z.; writing—original draft preparation, L.Z. and Z.J.; writing—review and editing, L.Z. and Z.J.; visualization, L.Z. and Z.J.; supervision, Z.J.; project administration, Z.J.; funding acquisition, Z.J. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the “Pioneer” and “Leading Goose” R&D Program of Zhejiang (2023C04024), the Zhejiang Provincial Natural Science Foundation (LY22C130007), Hainan Province Science and Technology Special Fund (ZDYF2023XDNY086), Nanfan Special Project, CAAS (YDLH2302), and the Project of Sanya Yazhou Bay Science and Technology City (SCKJ-JYRC-2022-87).

Data Availability Statement

No new data were created or analyzed in this study.

Conflicts of Interest

Author Liwei Zhan was employed by the company Zhejiang Wuwangnong Seeds Shareholding Co., Ltd. The remaining authors declare that this research was conducted in the absence of any commercial or financial relationships that could be construed as potential conflicts of interest.

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Agronomy 14 01507 g001
Figure 1. Symptoms of BD in the field: (a) elongated rice plants with pale green leaves in the field (red arrows), a symptom of BD; (b) infected seedlings with symptoms of elongation, reduced tillers, pale green leaves, and wider angles of leaf insertion.
Figure 1. Symptoms of BD in the field: (a) elongated rice plants with pale green leaves in the field (red arrows), a symptom of BD; (b) infected seedlings with symptoms of elongation, reduced tillers, pale green leaves, and wider angles of leaf insertion.
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Figure 2. Chromosome position of the bakanae-disease-resistance-related QTLs.
Figure 2. Chromosome position of the bakanae-disease-resistance-related QTLs.
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Table 1. QTLs related to BD resistance in rice.
Table 1. QTLs related to BD resistance in rice.
QTLChromosomeQTL Region (Mb)PVE (%) aMapping Population/MethodMapping Population SizeParents or Type of PopulationReferences
qB1134.10–34.9513.4DH/QTL mapping120Chunjiang 06 (indica)/TN1 (japonica)[43]
qB101018.72–19.2313.3DH/QTL mapping120Chunjiang 06 (indica)/TN1 (japonica)[43]
qBK1123.21–23.7265.0NIL/QTL mapping168YR24982-9-1 (indica)/Ilpum (japonica)[49]
123.64–23.67-NIL/QTL mapping168YR24982-9-1 (indica)/Ilpum (japonica)[44]
qBK1.1123.32–23.344.8RIL/QTL mapping168Pusa 1342 (indica)/Pusa Basmati 1121 (indica)[45]
qBK1.213.10–3.3624.7RIL/QTL mapping168Pusa 1342 (indica)/Pusa Basmati 1121 (indica)[45]
qBK1.314.65–8.416.5RIL/QTL mapping168Pusa 1342 (indica)/Pusa Basmati 1121 (indica)[45]
qBK3.1321.43–21.789.1RIL/QTL mapping168Pusa 1342 (indica)/Pusa Basmati 1121 (indica)[45]
qBE1.1111.91–13.7115.3RIL/QTL mapping132Peiai 64S (indica)/9311 (indica)[38]
qBE996.38–8.2811.0RIL/QTL mapping132Peiai 64S (indica)/9311 (indica)[38]
qBW110.56–5.6212.8RIL/QTL mapping132Peiai 64S (indica)/9311 (indica)[38]
qBW3334.95–35.6012.8RIL/QTL mapping132Peiai 64S (indica)/9311 (indica)[38]
qBW6624.40–25.8811.5RIL/QTL mapping132Peiai 64S (indica)/9311 (indica)[38]
qBE1.210.30–4.5618.7RIL/QTL mapping159Nipponbare (japonica)/9311 (indica)[38]
qBE3328.68–35.7722.3RIL/QTL mapping159Nipponbare (japonica)/9311 (indica)[38]
qBK1_62809110.62–1.04-japonica rice accessions/GWAS138tropical and temperate japonica[5]
qBK4_31750955431.16–31.75-japonica rice accessions/GWAS138tropical and temperate japonica[5]
qBK1WD113.54–15.1320.2RIL/QTL mapping200Wonseadaesoo (japonica)/Junam (japonica)[27]
qFfR1122.56–24.10-F2:F3/Genome resequencing180Nampyeong (japonica)/DongjinAD (japonica)[1]
qFfR997.24–7.56-F2:F3/Genome resequencing188Samgwang (japonica)/Junam (japonica)[46]
qBK1.410.4–0.43-Parts of RDP 1 b/GWAS76indica subgroup from RDP 1[30]
qBK1.512.25–2.33-RDP 1/GWAS231accessions from RDP 1[30]
qBK1.6122.09–22.25-RDP 1/GWAS231accessions from RDP 1[30]
qBK1.7123.63–23.64-Parts of RDP 1/GWAS76indica subgroup from RDP 1[30]
qBK3.2327.48–27.64-RDP 1/GWAS231accessions from RDP 1[30]
qBK4.1422.37–22.43-RDP 1/GWAS231accessions from RDP 1[30]
qBK6.163.28–3.64-RDP 1/GWAS231accessions from RDP 1[30]
qBK6.264.87–5.06-RDP 1/GWAS231accessions from RDP 1[30]
qBK6.3625.30–25.64-Parts of RDP 1/GWAS76indica subgroup from RDP 1[30]
qBK8.186.14–6.24-RDP 1/GWAS231accessions from RDP 1[30]
qBK10.1105.68–6.02-Parts of RDP 1/GWAS76indica subgroup from RDP 1[30]
qBK10.2106.85–6.86-RDP 1/GWAS231accessions from RDP 1[30]
qBK10.3109.09–9.34-Parts of RDP 1/GWAS76indica subgroup from RDP 1[30]
qBK11.11122.577–22.583-RDP 1/GWAS231accessions from RDP 1[30]
qFfR1-1121.36–24.37-F2:F3/QTL mapping205Junam (japonica)/Nampyeong (japonica)[47]
qFfR6615.20–16.22-F2:F3/QTL mapping188Saenuri (japonica)/Nampyeong (japonica)[47]
qBK1z11.43–2.1630.9RIL/QTL mapping180Zenith (indica)/Ilpum (japonica)[3]
qBK4T433.12–33.4434.4RIL/QTL mapping and GWAS143Ilpum/Tung Ting Wan Hien1[39]
a PVE represents the percentage of phenotypic variation explained. b RDP 1 represents Rice Diversity Panel 1. - Hyphens represents no PVEs were reported in the references.
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Zhan, L.; Chen, L.; Hou, Y.; Zeng, Y.; Ji, Z. Bakanae Disease Resistance in Rice: Current Status and Future Considerations. Agronomy 2024, 14, 1507. https://doi.org/10.3390/agronomy14071507

AMA Style

Zhan L, Chen L, Hou Y, Zeng Y, Ji Z. Bakanae Disease Resistance in Rice: Current Status and Future Considerations. Agronomy. 2024; 14(7):1507. https://doi.org/10.3390/agronomy14071507

Chicago/Turabian Style

Zhan, Liwei, Ling Chen, Yuxuan Hou, Yuxiang Zeng, and Zhijuan Ji. 2024. "Bakanae Disease Resistance in Rice: Current Status and Future Considerations" Agronomy 14, no. 7: 1507. https://doi.org/10.3390/agronomy14071507

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