Countries reported with the presence of bacterial panicle blight (BPB) caused by
Bacterial panicle blight (BPB) is present in more than 18 countries and has become a global disease in rice. BPB is highly destructive and can cause significant losses of up to 75% in yield and milling quality. BPB is caused by Burkholderia glumae or B. gladioli, with the former being the primary cause of the disease. Outbreaks of BPB are triggered by conditions of high temperatures in combination with high relative humidity at heading. The disease cycle starts with primary infections from infected seed, soil, and irrigation water, and subsequent secondary infections result from rain splash and panicle contact. Limited management options are available for control of BPB. There are only several cultivars including hybrids with partial resistance available currently. Twelve quantitative trait loci (QTLs) associated with the partial resistance have been identified. Oxolinic acid is an effective antibacterial compound for control of BPB in Japan, but it is not labeled for use on rice in the USA and many other countries. Sustainable control of BPB relies on integrated use of available management strategies of exclusion, genetic resistance, chemical control, biocontrol, and cultural practice. Developing and use of resistant cultivars is the best strategy to minimize the damage caused by BPB and maximize rice production in the long term.
- bacterial panicle blight
- seedling rot
- grain rot
- Pseudomonas glumae
- Burkholderia glumae
- Burkholderia gladioli
- disease control
- genetic resistance
- chemical control
- cultural practice
Bacterial panicle blight (BPB), caused primarily by
Effective management of BPB is critical to minimizing the damage caused by the disease and maximizing production returns. However, limited options for management of the disease are available currently. No single genes or quantitative trait loci (QTLs) for complete resistance to BPB have been found so far [13, 14]. Only a few rice cultivars with partial resistance are available for commercial use. No chemical control options are available in the USA although oxolinic acid has been used as a major control measure for BPB in Japan for more than two decades . Resistant populations of
In this article, we focus on the review of recent advances on the development of management strategies for BPB, including exclusion, genetic resistance, chemical control, biological control, and cultural practice. In addition, world distribution of the pathogen, characteristic symptoms of BPB, and current understanding of epidemics of BPB are also included. Two review articles covering the pathogenesis of
Since the first description of
|Latin America||1989||B. glumae|||
|The Philippines||1996||[30, 31, 32]|
|Louisiana (USA)||2001||[1, 33]|
|Arkansas (USA)||2009||[1, 9]|
|Texas (USA)||2009||B. glumae||[1, 10]|
|Honduras||2011||Lex Ceamer, personal communication|
BPB of rice can be caused by either
The symptoms of BPB include seedling blight, sheath rot, and panicle blighting [1, 2, 3, 4]. These symptoms can be induced by either
Unlike rice sheath blight and blast, BPB is difficult to be diagnosed based on the symptoms on panicles. Similar symptoms on panicles can be caused by many abiotic and biotic factors including heat, insect damage, and secondary microorganisms [3, 4, 47]. However, BPB has the symptoms that can be distinguished from other causes. BPB occurs sporadically on individual plants or in circular or oval patterns in the field (Figures 2 and 3). In contrast, common panicle blanking, caused by abiotic stress such as from excessive heat, develops in the field more uniformly and does not form apparent foci. There are three important characteristics of BPB that separate it from other panicle disorders: (1) BPB often does not appear to prevent successful pollination although it can affect individual glumes or whole panicles (Figure 4). Thus, seed may be present on the panicle unlike panicle sterility that is caused by heat stress. (2) Infected florets initially have discoloration ranging from light green to light brown on the basal portion of the glumes with a reddish-brown margin separating this area from the rest that becomes straw-colored later (Figures 4 and 5). (3) The rachis or branches of the panicle remain green for a while at the base of each floret, even after the glumes desiccate and turn tan (Figures 4 and 5). Florets at the latest stages of infection usually appear to be gray or black due to the abundant growth of saprophytic fungi on the surface (Figure 5). The disease can cause linear lesions on sheaths with a distinct reddish-brown border and a gray and necrotic center, resulting in sheath rot (Figure 6A) and stem rot (Figure 6B). On the leaves, lesions are circular to oval with a smooth reddish-brown border and a gray or straw-colored center (Figure 6C). If the infected plants are young, this disease can cause seedling blighting (Figure 6D) or seeding rot. The symptoms of seedling rot were first reported in Japan  and frequently occur in young rice plants. However, these symptoms on leaves, sheaths, stems, and seedlings are rarely observed under the field conditions in the Southern USA . This is one of the reasons why no scouting methods have been developed to detect and predict the development of BPB based on the symptoms on leaves and sheaths at the early crop growth stages.
The disease cycle and epidemiology of BPB of rice are not completely understood. Both
The bacterial pathogen invades germinated seeds, inhabits the roots and lower sheaths, and moves up the growing plant as an epiphyte (an organism growing on a plant surface, but not as a parasite) [2, 51, 52]. A recent study, using real-time fluorescence quantitative PCR to monitor the infection process of
High temperatures in combinations with high humidity or frequent rain are essential for the development of BPB epidemics. The outbreaks of BPB are usually triggered by conditions of high temperatures in combination with simultaneously high relative humidity during the heading-flowering stages. In the observations of Yokoyama and Okuhara , the disease developed when minimum daily temperature was ≥23°C and moderate rainfall (<30 mm/day) occurred during heading. Tsushima et al.  found BPB commonly occurred when relative humidity was more than 95% for 24 hours during flowering. Lee et al.  reported that the disease did not develop when the minimum daily temperature was less than 22°C and when relative humidity was below 80% during the heading stage. Nandakumar et al.  found that the optimum temperature for the growth of
The outbreaks of BPB in the Southern USA in the epidemic years appeared to be related to unusual weather conditions. Weather conditions favorable for the development of the disease were high nighttime temperatures and high humidity or frequent rainfall during heading and flowering . For example, in the 2010 epidemic year, abnormally high minimum (night time) temperatures occurred on June 21 through July 10 (Figure 7) when ca. 60% of the Texas rice acreage was near or at heading and flowering. During that period, rainfall was frequent and relative humidity was 95% or above most of the time (Figure 7). The combination of favorable weather conditions, high nighttime temperatures and high humidity, occurring at the most susceptible stages of rice plants promoted the infection and development of BPB. Similar weather patterns were observed in 1995 when a severe epidemic of BPB took place in Texas. There were many days with high maximum temperatures 35°C or above, day temperatures above 32°C from 10 am to 12 pm (the flowering time), and precipitation from the last week of June through the first week of August (Table 2). Heading and flowering occurred on a large percentage of the Texas rice crop during that period. These conditions were associated with severe outbreaks of BPB and significant yield losses in 1995. Figure 8 shows an example of the severity of this disease in 1995 and its association with yield loss for different rice cultivars, with the disease severity levels ranging from 1 to 22% of panicles affected.
|Crop phenology (% heading)||Month||Week||Days||Total precipitation (cm)|
|≥35°C||Mean ≥ 24°C||10 am to noon ≥32°C||Precipitation|
5. Management strategies
Successful disease control generally relies on employing management strategies toward reducing the damage to a manageable and acceptable level. These strategies are exclusion, genetic resistance, chemical control, biological control, and cultural practice. However, for control of the BPB disease at a given geographical area, there are few management options available currently. To effectively manage rice BPB, rice producers must start with the use of pathogen-free seeds as an exclusion measure, plant with partially resistant cultivars, apply with available chemicals or biocontrol agents, and use proper cultural practice. Integrated use of these available management strategies is the key to the effective and sustainable control of the BPB disease.
Since the BPB disease has been reported in more than 18 countries (Table 1) and the disease is not present in all the rice-producing countries and regions, exclusion of the BPB pathogens from a disease-free region is the most effective strategy to prevent BPB of rice. Plant quarantine is an effective measure to achieve this goal. For example, within the USA, the state of California has employed a plant material quarantine procedure to prevent the introduction of the BPB pathogens, other rice pathogens, and weed and insect pests into the state from the southern rice-producing USA. A similar plant quarantine law has been established and enforced in China to prevent the potential importation of the BPB pathogens from foreign countries since 2007 .
BPB is seedborne and infected seeds serve as the primary source of inoculum [1, 2, 48]. Therefore, the use of certified seeds that are free of the BPB pathogens is another effective measure to exclude the disease from a disease-free geographic area. Different molecular detection methods including PCR that have been developed to test rice seed lots [19, 48] can aid in this process. In the USA, the use of pathogen-free seeds is recommended to manage the BPB disease. However, using PCR procedure to ensure the BPB pathogens free in certified seed has not been employed. To reduce the BPB disease, it is recommended that farmers should not use the seeds harvested from the fields that are infected with BPB the previous year.
Seed treatment can serve as the last resort to reduce and even eliminate the seedborne BPB pathogen populations and to control subsequent head disease to an accepted level. Rice seeds treated at 65°C of dry heat for 6 days can eradicate the BPB pathogens . Seed treatment with the antibiotic bactericide oxolinic acid (Starner®) has been shown to control the bacterial pathogens in naturally and artificially infected seeds . An antagonistic
5.2 Genetic resistance
Considerable research efforts have been conducted globally to develop resistant cultivars as an effective and sustainable strategy for management of BPB of rice. Unfortunately, no single genes or quantitative trait loci (QTLs) for complete resistance to BPB have been found so far [13, 14]. Only several rice cultivars with partial resistance are available for commercial use. In Japan, BPB resistance breeding research efforts started as early as 1975; three partially resistant cultivars were identified through a field screening of nine cultivars and lines . No resistant cultivars and breeding lines were identified in a study of screening 293 cultivars and lines using greenhouse inoculation at the flowering stage in 1983 [63, 64]. From 1985 through 2013, there were nine reported studies that screened a total of 798 cultivars and breeding lines in the field and greenhouse and identified a total of 28 cultivars and lines showing partial resistance to BPB [13, 65, 66, 67, 68, 69, 70, 71, 72, 73]. Most recently, Mizobuchi et al.  identified two tropical
In the USA, a collaborative research effort has been established for decades in the southern states of Arkansas, Louisiana, Mississippi, Missouri, and Texas through the Uniform Rice Research Nursery (URRN) to evaluate and develop rice cultivars with high yielding potential and resistance to BPB, sheath blight, rice blast, and other diseases. Annually, more than 200 elite breeding lines and cultivars from the southern states’ breeding programs are evaluated in the URRNs inoculated with
In addition to the host resistance research that has been conducted in Japan and the USA, resistant cultivars and lines have also been reported in other countries. In Brazil, three cultivars were found to be resistant to BPB in the field evaluation . In China, one cultivar, named KaohsiugS.7, was reported to show resistance to the disease when rice plants were inoculated with
Host resistance such as rice blast resistance can be broadly classified into complete and partial resistance . The complete resistance is of qualitative character and race specific, which is controlled by major resistance genes (R genes). However, the partial resistance is of quantitative character and non-race specific, which is controlled by several minor genes known as quantitative trait loci (QTLs). Unlike rice blast resistance having both complete and partial resistances, it is apparent that rice BPB resistance has only partial (quantitative) resistance and no complete resistance has been found. Pinson et al.  provided the first analysis of QTLs of rice resistance to BPB, using a population of 300 recombinant inbred lines (RILs) derived from a cross between Lemont and TeQing, susceptible and resistant to BPB, respectively. Lemon was an American rice cultivar, while TeQing was a cultivar from China. Twelve QTLs, namely,
5.3 Chemical control
Oxolinic acid (5-ethyl-5,8-dihydro-8-oxo-[1,3]dioxolo[4,5-g]quinoline-7-carboxylic acid, Starner®) is the first chemistry that has been reported to be highly effective for control of the BPB disease in rice. This antibacterial compound, a quinoline derivative, was first introduced in Japan in 1989 for control of rice seeding rot and grain rot . Combined use of oxolinic acid as seed treatment and foliar sprays at heading has been reported to be the best strategy for effective control of both seeding rot and gain rot diseases . When applied at the heading stage, this bactericide is highly effective to inhibit multiplication of
Copper and copper-containing bactericides have also been reported to be effective for control of BPB in rice [86, 91, 92, 93]. These bacterial products include Kocide® 2000 (53.8% copper hydroxide), Kocide® 3000 (46.1% copper hydroxide), Previsto® (5% copper hydroxide), Badge® SC (15.4% copper hydroxide plus 16.8% copper oxychloride), Badge® X2 (21.5% copper hydroxide plus 23.8% copper oxychloride), and Top Cop® (8.4% tric basic copper sulfate). In the field trials of Louisiana, a single application of Kocide® 2000 or Top Cop® at the boot stage reduced the BPB severity as much as 75%, and grain yield and milling quality were improved . In our multiyear field trials conducted in Texas, single applications of Kocide® 3000, Badge® SC, Badge® X2, or Previsto® at the heading stage significantly reduced BPB severity, with the reductions ranging from 42 to 96% [91, 92, 93]. However, except Previsto® with a relatively lower level of copper-active ingredient, all other copper products produced varying degrees of phytotoxicity on sprayed leaves and panicles and under certain environmental conditions reduced yields [86, 91, 92, 93]. These copper products have been registered as bactericides and fungicides for control of various bacterial and fungal diseases in citrus, tree crops, vegetables, vines, and field crop (soybeans, wheat, oats, and barley) in the USA. Probably due to their potential phytotoxicity and yield reduction, all these copper products have not been registered for management of the BPB disease on rice in the USA.
In addition to oxolinic acid and copper-based bactericides, other bactericides such as kasugamycin, probenazole, and pyroquilon are used for management of rice seedling rot and grain rot in Japan  and Honduras (Lex Ceamer, personal communication).
5.4 Biological control
Several studies have been conducted to develop biological control methods as a strategy for management of BPB of rice. In Japan, Tsushima and Torigoe  conducted the first research on the use of bacterial antagonists for control of BPB under field conditions. An antagonistic
In addition to bacterial biocontrol agents, bacteriophages (also known as phages) have been demonstrated to be effective for management of rice seedling rot in Japan. Adachi et al.  found that two bacteriophages were able to lyse
5.5 Cultural practice
Few studies have been conducted to understand and develop cultural practices that could reduce the incidence and severity of BPB in rice. High levels of nitrogen fertility tend to increase the susceptibility of rice plants to the BPB disease. Avoiding excessive nitrogen rates can help reduce the damage caused by BPB. In an Arkansas study evaluating the effects of nitrogen on BPB severity, it was demonstrated that the severity of BPB at the high nitrogen rate (247 kg/ha) was 1.6 times higher than at the low rate (168 kg/ha) applied during a cropping season . Under the Southern US rice production systems, early planting or use of early maturing rice cultivars to avoid the hottest times of the growing season is another effective approach to reduce the damage caused by the disease. In addition, avoiding excessive seeding rates is also helpful in reducing the incidence and severity of the disease.
6. Conclusion and prospects
BPB has been reported in more than 18 countries and has become a global rice disease. Currently, BPB is one of the major diseases in rice in many countries, including Japan, the USA, and Latin America. The disease is highly destructive, which can cause almost complete losses in yield and milling quality under the most favorable conditions. The outbreaks of BPB are triggered by conditions of high temperatures. With predicted global warming, the disease is likely to be more prevalent on a global scale and to cause more damage in epidemic regions in the future [20, 74]. The global land and ocean surface temperature has been increased by as much as 0.85°C over the period of 1880–2012 based on the 2014 IPCC report . Under the 1°C warming scenario, it is estimated that the increased damage caused by this disease in the Southern USA would result in a $103 million USD annual decrease in consumer surplus and a loss of rice production equivalent to feeding 1.9 million people (Aaron Shew, personal communication).
Effective management of this bacterial disease is challenging. Unlike most of other rice diseases, The BPB disease often develops after the heading stage, and typically no symptoms and signs can be observed before heading. Therefore, no scouting methods are currently available to detect and predict the development of the disease. No standardized seed treatment methods have been developed and commercialized specifically to eradicate or reduce the pathogen populations in rice seeds. No chemical control agents are labeled for management of the BPB disease in most countries, including the USA. The efficacy and increasing use of oxolinic acid have been affected by the development of oxolinic acid resistance in the populations of
Therefore, effective and sustainable control of the BPB disease largely depends on integrated use of available management options. Plant quarantine is the first defense to exclude the BPB pathogens from disease-free countries and regions. The use of pathogen-free seed or certified seed is another effective measure to control this disease. Planting with cultivars having a resistant level as high as possible is always an effective recommendation to reduce the damage caused by the disease. A limited number of rice cultivars, including hybrids, with partial resistance to BPB are available for commercial use in many countries. Since no source of complete resistance has been discovered so far, more research is needed to look for new sources of resistance through screening a greater number of germplasm lines, including those from other countries and the wild species of