Abstract
Rice false smut (RFS) is the most important grain disease in rice production worldwide. Its epidemics not only lead to yield loss but also reduce grain quality because of multiple mycotoxins generated by the causative pathogen, Villosiclava virens (anamorph: Ustilaginoidea virens). The pathogen infects developing spikelets and specifically converts individual grain into a RFS ball that is established from mycelia covered with powdery chlamydospores, sometimes generating sclerotia. RFS balls seem to be randomly formed in some grains on a panicle of a plant in the paddy field. However, epidemics differ largely among varieties, fields, and seasons. This chapter introduces current understanding on the disease, mycotoxins, the biology of the pathogen, pathogenesis of RFS, rice resistance, the disease cycle, the disease control, and assay.
Keywords
- basal defense
- biotroph
- effector
- epiphytic growth
- grain filling gene
- mycotoxin
- sclerotium
1. Introduction
Rice production plays a crucial role in our food security. Rice security is not only an economic issue but also an important parameter to determine social and political stability [1]. Thus, rice research has to be geared up to develop strategies for alleviating losses due to pests and diseases. In the past decades, a number of minor diseases have attained the status of major importance in rice. One such disease is the rice false smut (RFS) disease that is a threat to yield and grain quality.
RFS was previously recorded as a minor disease of rice and considered as a symbol of good harvest in old times. In recent years, increasing occurrence of RFS has been reported in most major rice growing regions throughout the world, such as China, India, and USA [2, 3, 4, 5]. The emergence of this disease is believed to be partially due to wide application of hybrid rice varieties, which are mostly susceptible to the RFS. The causative agent of RFS is an ascomycete fungal pathogen
The disease induces considerable losses both in yield and quality [7, 8], due to the occurrence of RFS balls and increased sterility of kernels adjacent to the balls [9]. Moreover, RFS balls produce two types of mycotoxins, i.e., ustiloxin and ustilaginoidin, which are poisonous to both humans and animals and impose significant health hazards by contaminating rice grains and straws [10, 11, 12]. For example, ustiloxin A causes kidney and liver damage in mice, due to its inhibition activity on microtubule assembly and skeleton formation of the eukaryotic cells [11, 13].
RFS balls seem to be randomly formed in some grains of rice panicles in the paddy field and are inevitably collected during harvest (Figure 1E,F). The disease spread varies within a field or between fields and is considered to be more severe in the proximity of drainage channels [14]. Epidemics of RFS disease tend to occur when rice booting and heading stages meet with rainfall periods. However, epidemics differ largely among varieties, fields, and seasons. This chapter describes our current knowledge on the mycotoxins, biology of the pathogen, pathogenesis of RFS, rice resistance, disease cycle, disease control, and disease assay.
2. Mycotoxins
Ustiloxins could inhibit polymerization of microtubule proteins and cause abnormal mitosis resembling, which would result in acute necrosis of renal tubular cells and hepatocytes in mice [10]. Ustiloxins also show phytotoxicity, inhibiting elongation of radicle and germ and inducing swelling of seedling root in rice [10, 16]. Cytotoxic activities of ustiloxins have been demonstrated on human tumor cell lines, such as A375, A549, BGC-823, HCT116, and HepG2 [10, 16]. Similar phytotoxic and cytotoxic activities have been detected for ustilaginoidins [25, 27, 28]. In addition, ustilaginoidins show antibacterial activities against several human or plant pathogens, such as
3. Biology of the pathogen
The RFS pathogen belongs to the kingdom: Fungi, phylum: Ascomycota, class: Ascomycetes, subclass: Sordariomycetes, order: Hypocreales, family: Clavicipitaceae, genus:
Numerous efforts have been undertaken to optimize the culture media and culturing conditions for
4. Pathogenesis of RFS
4.1 Infection process of V. virens
The RFS pathogen
Although RFS disease symptoms are observed at rice grains due to pathogen infections of spikelets,
4.2 Genetic transformation of V. virens
Genetic manipulation is essential to clarify the pathogenicity of
4.3 Genome and pathogenicity of V. virens
The availability of
Effectors are powerful weapons possessed by pathogens to manipulate host immune system and metabolisms for successful colonization. Characterizing their roles is important for understanding pathogen-host interactions. In
Nevertheless, several virulence factors have been identified in
4.4 Host compatible interaction with V. virens
Monitoring host responses to
As a successful pathogen,
5. Resistance of rice
5.1 Sources and inheritance of RFS resistance
Various attempts have been made to screen rice cultivars resistant to RFS. Screening of 186 rice hybrids to RFS resistance was done by Liang and colleagues [64], which identified few hybrids with low disease incidence. They screened the commercial hybrids that had lower rates of diseased panicles and infected florets at Xindu and Qionglai (Sichuan Province, China) in 2011 together with newly registered varieties. Lore et al. [65] evaluated some hybrids and inbred cultivars growing across India for susceptibility/tolerance to RFS. Artificial inoculation of false smut was done by Kaur et al. [66], which identified nine hybrids resistant to RFS among 125 rice genotypes screened. More detailed evaluation of RFS resistance was performed by Huang and colleagues [67]. A total of 843 rice accessions were screened in disease nurseries in 3 years although some of those accessions were planted in different locations and on different dates. Finally, 36 accessions were found to show no disease incidence. A highly susceptible accession Pujiang 6 was identified in this study. Polymorphism analysis determined several resistant accessions which could be used for crossing with Pujiang 6 to construct gene mapping populations [67].
Resistance of genes against
5.2 Molecular basis of RFS resistance
Since many rice cultivars with high RFS resistance or high susceptibility have been identified, comparative transcriptome analysis is a promising method to mine resistance- or susceptibility-related genes in rice. For instance, time-course RNA-seq was carried out on susceptible cultivar LYP9 and resistant cultivar IR28 upon
Accumulation of H2O2 is a typical plant basal defense fighting against pathogen infections [73]. During a compatible interaction between rice and
Based on the current findings that
6. Disease cycle
With regard to the asexual cycle, chlamydospores from RFS balls are easily transmitted by wind and rainfall, and attack developing rice spikelets of late ripening rice cultivars. This is supported by the fact that fresh chlamydospores have high germination rate and could successfully infect rice flowers to form RFS balls [79, 80]. Chlamydospores can overwinter in soil and on dead plants, or on harvested RFS balls and rice seeds, and survive up to several months; however, the germination rate decreases rapidly [81]. In the next rice planting season, chlamydospores overwintered in fields and on rice seeds may germinate with hyphae to infect coleoptiles of germinating rice seeds and roots of seedlings [43, 44, 45]. Since chlamydospores could not be trapped in fields until RFS balls appear [35], it is unclear how chlamydospore germination time couples with rice booting stage for infecting rice flowers. Studies suggest that coleoptile and root infections may lead to asymptomatic colonization of the pathogen in rice plants at subsequent stages. Sensitive PCR methods have been applied to successfully detect
Epiphytic growth of
Alternative hosts of a pathogen commonly play an important role in disease cycle. Earlier, paddy field weeds such as
7. Disease control
In recent years, the RFS disease has become a severe threat to rice production due to its epidemics. In order to minimize direct economic loss, suitable management practices have to be made to manage the disease. Breeding and utilization of resistant cultivar is the most effective and economical way to control RFS disease and ensure the high yield of rice. Attempts have been made to identify sources of resistance against
Culture managements have been studied to reduce incidence of RFS. Early planted rice has less RFS balls rather than the late planted rice. Excess application of nitrogenous fertilizer should be avoided. Since high rate of nitrogen increases the disease incidence, sensible use of nitrogen is recommended. Fertilizer ratio is often a reasonable parameter for growers to adjust, so as to enhance the stress tolerance of rice plants, and ultimately reduce the RFS incidence. Field ridges and irrigation channels should be kept clean to eliminate alternative hosts. Conservation tillage and furrow irrigation have some effects on suppressing the disease index [2, 89]. Using suitable plant spacing and utilizing uncontaminated rice seeds are also recommended.
Chemical control, i.e., fungicide application, can be effective but is often not economical and environment-friendly. Using fungicides with high efficiency, low toxicity, and low residue is currently the best choice to control RFS disease. Fungicides, such as Wenquning (a suspension of
8. Disease assay
8.1 Natural infection
To evaluate RFS sensitivity of rice under natural infection, several classification standards of disease incidence have been reported. For example, in 1996, the International Rice Research Institute (IRRI) [93] classified RFS into 6 scales based on incidence of severely infected tillers or infected spikelets, i.e. 0, no incidence; 1, less than 1%; 3, 1–5%; 5, 6–25%; 7, 26–50%; and 9, 51–100%. Later on, Tang and colleagues [94] established a new classification standard, and developed Disease Index to determine RFS incidence. The classification standard was based on aspect ratio and 100-weight of RFS ball, grain weight, seed setting rate, and yield loss of single diseased panicle. Six scales were classified: 0, no RFS ball; 1, one RFS ball; 2, two RFS balls; 3, 3–5 RFS balls; 4, 6–9 RFS balls; and 5, ≥10 RFS balls. Disease index = ∑ (Disease scale value × Diseased plant number)/(Total plant number × Highest disease scale) × 100. Note that only the highest disease scale value is adopted for each plant. This classification standard has been widely applied in recent studies [70, 71, 72]. When using natural infection method, disease incidence should be evaluated for multiple years at multiple locations, with multiple sowing dates.
8.2 Artificial inoculation
Due to uncertainty of environmental conditions under natural infection, a high efficient artificial inoculation method is desired for evaluating
The above-mentioned classification standard and Disease Index [94] can also be applied to evaluation of disease incidence under artificial inoculation. Alternatively, the following method can be adopted when the disease scale is reaching the highest (i.e., scale 5, ≥10 RFS balls) for each plant. This situation is often encountered when using susceptible rice cultivars to evaluate
9. Future aspects
RFS is an emerging disease threatening the production safety of rice grains worldwide. Great progresses have been made to understand the RFS pathogen and its interaction with rice. However, many important questions are yet to be addressed. How much the mycotoxins produced by
Acknowledgments
We thank Drs Dongwei Hu (Zhejiang University) and Junjie Yu (Jiangsu Academy of Agricultural Sciences) for kindly providing images as indicated in figure legends. We apologize to the colleagues whose work could not be included in this book chapter due to space limitation. This work was supported by grants from the National Natural Science Foundation of China (grant no. 31501598 and 31772241) and Key Projects of Sichuan Provincial Education Department.
Conflict of interest
The authors declare no conflict of interest.
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