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Hybrid Rice Outperforms Inbred Rice in Resistance to Sheath Blight and Narrow Brown Leaf Spot

    Affiliations
    Authors and Affiliations
    • Jun Shi1 2
    • Xin-Gen Zhou1
    • Zongbu Yan1
    • Rodante E. Tabien1
    • Lloyd T. Wilson1
    • Li Wang1 3
    1. 1Texas A&M AgriLife Research Center, Beaumont, TX 77713, U.S.A.
    2. 2Mianyang Academy of Agricultural Sciences, Mianyang, Sichuan 621023, China
    3. 3Meishan Vocational & Technical College, Meishan, Sichuan 620010, China

    Published Online:https://doi.org/10.1094/PDIS-11-20-2391-RE

    Abstract

    Sheath blight (ShB; caused by Rhizoctonia solani AG1-1A) and narrow brown leaf spot (NBLS; Cercospora janseana) are among the most important diseases affecting rice production in Texas and other southern parts of the United States. Because of the high yield potential, hybrid rice acreage is continually increasing. Understanding the relative levels of resistance to ShB and NBLS in hybrids compared to those of inbreds is important for effective disease management; however, this information remains largely unknown. A comparison of the performance of hybrid rice and inbred rice was performed involving 173 hybrid and 155 inbred genotypes (cultivars and elite breeding lines) over the course of five crop seasons (2016 to 2020) and two locations in Texas. The results showed that genotype, cultivar type (hybrid or inbred), location, and their interactions had significant effects on the severity of ShB and NBLS. The ShB severity in hybrid genotypes was significantly lower than that in inbred genotypes, with an average reduction of 27% in disease severity during the 5-year, two-location evaluation. Most (53%) of the hybrid genotypes were rated moderately resistant, whereas almost all (97%) of the inbred genotypes ranged from very susceptible to moderately susceptible. Similarly, NBLS severity in hybrid genotypes is significantly lower than that in inbred genotypes. All but four hybrid genotypes exhibit immune reactions to NBLS. In contrast, 77% of inbred genotypes exhibit NBLS symptoms, with disease resistance reactions ranging from susceptible to resistant. The results demonstrate that hybrid rice is generally less susceptible to sheath blight and has a higher level of resistance against NBLS compared with inbred rice.

    Rice (Oryza sativa L.) is one of the three major food crops (rice, wheat, and maize) globally, and it is, by far, the most important crop because it feeds more than half of the world’s human population. Rice is also a major crop in the United States, producing 7.5 million metric tons of rice on 1.3 million hectares (Childs et al. 2020). Nearly all the rice produced in the United States is grown in seven states: Arkansas, California, Florida, Louisiana, Mississippi, Missouri, and Texas. However, plant diseases, especially fungal diseases, are among the factors that limit rice production (Singh et al. 2017; Zhou 2010).

    Sheath blight (ShB), caused by Rhizoctonia solani Kühn AG1-1A [teleomorph: Thanatephorus cucumeris (A. B. Frank) Donk], is the second most important disease in rice worldwide and the most important disease affecting rice production in Texas and other southern states (Allen et al. 2020; Groth 2005; Uppala and Zhou 2018). The disease is soilborne and its sclerotia and mycelia in plant debris serve as primary inoculum. The development of ShB starts with the contact of sclerotia with leaf sheath near the waterline, followed by infection that leads to the formation of initial lesions. The lesions expand and coalesce to form larger lesions with irregular outlines and gray–white centers surrounded by dark brown borders. As lesions coalesce on the sheaths, entire leaves may eventually die. The disease spreads vertically through runner hyphae, growing upward along plant leaves and sheaths and horizontally through runner hyphae from tiller to tiller and from plant to plant. Under most conducive conditions, the disease can cause lodging and result in severe damage to the rice crop. ShB can cause up to 44% yield loss and a significant reduction in milling quality (Marchetti and Bollich 1991). It has been estimated that the occurrence of the disease in the three midsouthern states, Arkansas, Louisiana, and Mississippi, can cause yield loss that would otherwise feed 1.7 million people annually (Tsiboe et al. 2017).

    Narrow brown leaf spot (NBLS), caused by Cercospora janseana (Racid). O. Const. (synonyms: Cercospora oryzae Miyake, Passalora janseana Racib. U.), is another important disease with worldwide distribution (Hollier 1992). NBLS was first reported in Japan in 1906 (Hollier 1992). In the United States, NBLS was first found in Texas in 1935, and it was commonly present in most rice fields (Tullis 1937). The disease was historically considered a minor disease from the standpoint of production because of its nature of sporadic occurrence (Atkins 1975). However, for the past few decades, NBLS has increased its incidence and severity in the southern United States, especially Texas and Louisiana, because of the humid, warm Gulf Coast climate that is favorable for the development of the disease (Uppala et al. 2019). Severe epidemics of NBLS occurred during years with warm springs and wet summers (Groth 2008; Uppala and Zhou 2019). The disease is more severe in late plantings and in the ratoon (second) crop, which is a common practice following the main crop harvest in Texas and Louisiana to maximize the returns of rice production (Liu and Zhou 2011). The NBLS pathogen is seedborne and survives in infected rice plant residue year after year, serving as the primary inoculum. The disease spreads long distances by windborne spores during a cropping season (Uppala and Zhou 2019). The pathogen attacks leaf, sheath, internode, panicle branch, and glume tissues, causing linear brown lesions. The disease is usually more severe during the late growth stages and can cause premature ripening, yield reduction, and reduced milling quality under conducive conditions. Grain yield losses of up to 40% have been reported (Hollier 1992).

    Fungicides comprise the primary ShB and NBLS management tools in the United States (Uppala and Zhou 2018); however, fungicide use is not always economical or environmentally effective. The use of resistant cultivars, avoidance of excessively high nitrogen fertilizer rates, optimum seeding rates, and good cultural practices are recommended for the management of ShB and NBLS (Groth and Bond 2007; Handiseni et al. 2015; Uppala and Zhou 2019); however, these control measures are not always available or sufficiently effective. Cultivars with acceptable levels of resistance to ShB are unavailable. Although NBLS-resistant cultivars are available, the frequent development of new races of the NBLS pathogen can breakdown cultivar resistance (Estrada et al. 1981; Sah and Rush 1988); unfortunately, the efficacy of available agronomic management practices is often inconsistent.

    The introduction of hybrid rice has provided producers with a profitable alternative to traditional inbred rice production. Hybrid rice is the product of a cross between two genetically distinct rice parents that are selected because of their desirable traits. Because hybrid rice has high yield potential, uses less pesticides (Huang and Yan 2016), and can reduce input costs, farmers have adopted this new technology quickly. Since the release of the first commercial hybrid rice in China in 1976, hybrid rice acreage has increased globally (Shakiba and Scott 2019; Virmani et al. 2003; Yuan 1998). In the United States, the introduction and adoption of hybrid rice have significantly changed rice production since the release of the first hybrid cultivar in 2006 (Childs et al. 2020; Huang and Yan 2016; Shakiba and Scott 2019). The U.S. hybrid rice acreage has significantly increased and is currently more than half of the total rice acreage (Harrell et al. 2018). Because of the scope of the U.S. hybrid rice production, it is crucial to understand the performance of hybrid rice on field resistance against ShB and NBLS, which will help develop practical strategies for effective management of these diseases. However, detailed data regarding the susceptibility or resistance of hybrid and inbred rice to these diseases under field conditions are lacking. Most previous studies focused on the evaluation of a limited number of rice cultivars or genotypes, especially hybrid rice, to ShB, and few studies have evaluated resistance to NBLS or both ShB and NBLS (Groth 2005; Groth and Bond 2007; Mani et al. 2016; Sha et al. 2007; Tang et al. 2007; Wang et al. 2011; Wu et al. 2013). The objectives of this study were to evaluate resistance to ShB and NBLS in large sets of hybrid and inbred rice across 5 years in two testing sites to help gain a better understanding of hybrid and inbred disease resistance and to identify resistant germplasm that can be used to develop new cultivars with improved resistance.

    Materials and Methods

    Inbred and hybrid genotypes evaluated.

    A total of 155 inbred genotypes and 173 hybrid genotypes were evaluated over 5 years (2016 to 2020) in two locations (Beaumont and Eagle Lake) in Texas. Each genotype was evaluated during at least two repeated field trials across either locations or years. Most genotypes were evaluated for 3 years or more at each location. Sixteen rice cultivars (Cheniere, CL111, CL151, CL153, CL163, CL272, Cocodrie, Della 2, Diamond, Jazzman 2, Presidio, Rex, Rondo, Roy J, Titan, and Wells) were selected and served as the checks, with their ShB resistance ranging from moderate resistance to susceptible and with their NBLS resistance from immune reaction to susceptible. Each of these check cultivars was included for comparisons of resistance for 3 years or more at each location. Among the 155 inbred genotypes, 28 were inbred cultivars (Antonio, AR1111, Cheniere, CL111, CL151, CL153, CL163, CL172, CL272, CL272subB, Cocodrie, Della 2, Diamond, Jazzman 2, Jupiter, Lakast, M206, Meementau, MM-14, Presidio, PVL01sub, Rex, Rondo, Roy J, Taggart, Thad, Titan, and Wells) that were developed by the inbred breeding programs of Arkansas, California, Louisiana, Mississippi, and Texas, and all the remaining were elite inbred lines developed by the Texas inbred breeding program. Among the 173 hybrid genotypes, four were hybrid cultivars (CLGemini214, CLXL745, XL753, and XP760) developed by RiceTec (Alvin, TX), one was a hybrid cultivar (CLH161) from the Louisiana hybrid breeding program, and 168 were hybrids developed by the Texas hybrid breeding program. Selection of these hybrid genotypes during this study represented the current hybrid cultivars and breeding lines available from private and public breeding programs in the United States. Hybrid breeding lines were produced through either the three-line cytoplasmic sterility (CMS) breeding or two-line thermo-sensitive genic breeding. CMS breeding involves the creation of locally adapted cytoplasmic male sterile lines and near-isogenic maintainer lines, with the latter, when crossed with a corresponding CMS line, allowing continued production of CMS seed, as well as a restorer line that is normally from a different genetic group than the CMS line or its maintainer, which is referred to as a wide cross, and genetic distance responsible for the hybrid vigor expressed as increased yield. Thermo-sensitive genic male sterility (TGMS) consists of one parent having a gene that results in flowers being male-sterile when exposed to normally hot summer temperatures, which, when crossed with a restorer line from a different genetic group, referred to as a wide-cross compatible restorer, produces a hybrid. However, when TGMS occurs under low temperature during the late season, such as with a late ratoon crop, the sterility gene is not active, and the flowers self-pollinate, producing the next generation of TGMS seed. The advanced CMS lines are in in the fourth backcross (BC4) generation, whereas the TGMS lines are in the F3 generation. The hybrid breeding lines used in this study were made from 16 sterile lines (107s, 175s, 196s, 212s, 259s, 265s, 277s, 279s, 121A, 327A, 333A,339A, 387A, 405A, 411A, and 435A) by separately crossing with 18 restorer lines (151R, 152R, 153R, 154R, 161R, 162R, 163R, 164R, 171R, 172R, 173R, 181R, 182R, 183R, 190R, 191R, 192R, and 199R). The eight TGMS sterile lines (107s, 175s, 196s, 212s, 259s, 265s, 277s, and 279s) came from F6 to F10, and the eight CMS lines (121A, 327A, 333A,339A, 387A, 405A, 411A, and 435A) came from B4F1 to B8F1 of sterile lines mating with maintainer lines. The restorer lines came from F5 to F8 generations of restorer lines mating with inbred lines.

    Field experiments and weather conditions.

    During each of the 5 years (2016 to 2020), a disease nursery was established at two locations in Texas. One was located at the Texas A&M AgriLife Research and Extension Center in Beaumont, and the other was located at the Texas A&M AgriLife Research’s Wintermann Rice Research Station in Eagle Lake. Inbred and hybrid entries were arranged in a randomized complete block design with three replications. Plots consisted of seven 2.74-m-long rows spaced 0.18 m apart at the Beaumont site and six 2.74-m-long rows spaced 0.19 m apart at the Eagle Lake site. Rice was drill-seeded at 90 kg/ha for inbred genotypes and at 45 kg/ha for hybrid genotypes at both test sites. Rice was planted on 12 April 2016, 26 April 2017, 2 May 2018, 2 May 2019, and 23 April 2020, at Beaumont, and on 6 May 2016, 15 April 2017, 19 April 2018, 12 April 2019, and 23 April 2020, at Eagle Lake. Fertilizers, weed and insert control, irrigation, and other agronomical management were performed according to local recommendations.

    Both locations selected represent typical Texas rice production soils and weather conditions. The Beaumont site has a heavy clay soil, whereas the Eagle Lake site has a sandy soil. The Beaumont site has League-type clay soil (3.2% sand, 64.4% silt, 4.3% organic matter; pH 5.5), and the Eagle Lake site has Crowley fine sandy loam soil (59% sand, 2% silt, 12% clay, 0.7% organic matter; pH 5.3). The Beaumont site has much more rainfalls and relatively more humid weather conditions than the Eagle Lake site. At the Beaumont site, the average minimum, maximum, and mean temperatures (in degrees Celsius) during the months of April through August were 21.4/30.8/25.5, 21.0/30.2/25.1, 20.8/31.1/25.5, 21.1/30.7/25.4, and 21.0/30.8/25.4 in 2016, 2017, 2018, 2019, and 2020, respectively. Recorded total precipitation amounts during the months of April through August were 1,034, 1,692, 690, 874, and 625 mm in 2016, 2017, 2018, 2019, and 2020, respectively; the total precipitation over 5 years was 4,915 mm. The average relative humidity rates during the months of April through August were 80.5, 80.0, 77.0, 80.0, and 78.4% in 2016, 2017, 2018, 2019, and 2020, respectively; the average relative humidity rate over 5 years was 79.2%. At the Eagle Lake site, the average minimum, maximum, and mean temperatures (in degrees Celsius) during the months of April through August were 21.6/31.9/26.0, 21.4/32.2/26.0, 21.0/32.7/26.1, 21.4/32.2/26.1, and 21.0/32.0/25.8 in 2016, 2017, 2018, 2019, and 2020, respectively. Recorded total precipitation amounts during the months of April through August were 625, 884, 326, 622, and 475 mm in 2016, 2017, 2018, 2019, and 2020, respectively; the total precipitation over 5 years was 2,930 mm. Average relative humidity rates during the months of April through August were 78.5, 75.8, 73.8, 76.8, and 77.2% in 2016, 2017, 2018, 2019, and 2020, respectively; the average relative humidity rate over 5 years was 76.4%. Temperature and precipitation data were obtained from the National Climatic Data Center for weather stations located at Beaumont and Eagle Lake (Wilson et al. 2021).

    Pathogen inoculation and disease assessment.

    Each plot was divided into three equal-length sections for disease inoculation or infection according to the method developed by Don Groth (personal communication). One-third of each plot was inoculated with R. solani AG1-1A (isolate TX-RS-1) by broadcasting 150 ml per plot of the inoculum at panicle differentiation plus 7 days each year. The middle section was kept as a barrier between the two end sections, and the final one-third was left for natural infection of NBLS. This plot design accommodates more entries while allowing for separate assessment of ShB and NBLS because the spread of ShB is limited in the plots. Isolate TX-RS-1 of R. solani AG1-1A collected from a diseased rice plant in a commercial field (Zhou et al. 2021) was used to inoculate a 1:3 vol/vol mixture of sterilized rice grains and rice hulls in autoclavable plastic bags with an air-exchangeable opening and incubated at room temperature for 2 weeks. Inoculum was air-dried and broken into small particles (diameter, 1 to 5 mm) before being delivered into plots. NBLS developed from naturally occurring inoculum because the experimental areas had been cropped to rice for >30 years.

    Severity of ShB and NBLS was rated in each plot section at approximately 1 week before the maturity of rice genotypes. ShB severity was rated on a scale of 0 to 9 (0 = no symptoms; 9 = most severe symptoms and damage [plants collapsed]) (Table 1) adapted from the rating system described by Groth et al. (1993). NBLS severity was rated on a scale of 0 to 9 (0 = no symptoms; 9 = most severe symptoms and damage [leaves dead]) (Table 2) adapted from the rating system described by Groth et al. (1993). Each rice genotype was ranked for ShB and NBLS resistance using the scale of reactions ranging from immune, resistant, moderately resistant, moderately susceptible, susceptible, to very susceptible, where immune = 0, 0 < resistant < 3.0, 3.0 ≤ moderately resistant <5.0, 5.0 ≤ moderately susceptible <7.0, 7.0 ≤ susceptible < 8.0, and 8.0 ≤ very susceptible < 9.0.

    Table 1. Tabulated sheath blight (ShB) rating system used in this studyz

    Table 2. Tabulated narrow brown leaf spot (NBLS) rating system used in this studyz

    Data analysis.

    Disease severity data were analyzed with PROC GLM in SAS (version 9.4, SAS Institute, Cary, NC). Because of the significance of the year effect, the effects of genotype, cultivar type, location, and their interactions were analyzed by year. Median and mean values were calculated by year, location, and cultivar type. Using the mean disease severity data, the percent reductions in disease severity on hybrid rice compared with that on inbred rice were computed and analyzed. Mean separations were performed using Fisher’s protected least significant difference (LSD) test at P = 0.05.

    Results

    ShB severity between inbred rice and hybrid rice.

    ShB severity was significantly (P ≤ 0.0084) affected by genotype, cultivar type, location, and their interactions during each of 5 years evaluated (Table 3).

    Table 3. Analysis of variance (P value) for the effects of genotype (cultivar or advanced breeding line), cultivar type (inbred or hybrid), location, and their interactions on the severity of sheath blight and narrow brown leaf spot (NBLS) in rice in 2016 through 2020

    At the Beaumont site, ShB severity in hybrid genotypes was generally lower than that in inbred genotypes during each year (Supplementary Fig. S1). ShB severity in 50% of the hybrid genotypes ranged from 3.7 to 4.0 in 2016, 4.3 to 5.3 in 2017, 5.8 to 6.3 in 2018, 4.7 to 6.3 in 2019, and 4.3 to 4.7 in 2020, whereas ShB severity in 50% of the inbred genotypes ranged from 4.3 to 5.0 in 2016, 7.3 to 9.0 in 2017, 6.2 to 8.3 in 2018, 6.7 to 8.3 in 2019, and 4.7 to 6.7 in 2020 (Fig. 1). The median severity levels for hybrid genotypes were 3.7, 4.5, 6.3, 5.0, and 4.3, with the highest severity levels being 4.3, 6.0, 7.0, 7.7, and 5.0, and the lowest severity levels being 3.3, 3.8, 5.3, 4.3, and 4.0 in 2016 to 2020, respectively (Fig. 1). In contrast, the median severity levels for inbred genotypes were 4.7, 8.1, 7.0, 8.0, and 5.0, with the highest severity levels reaching 5.7, 9.0, 9.0, 8.7, and 8.3, and the lowest severity levels reaching 3.7, 5.0, 6.0, 4.7, and 4.3 in 2016 to 2020, respectively. At the Eagle Lake site, similar patterns of differences in ShB severity between inbred rice and hybrid rice were also observed. ShB severity in hybrid genotypes was generally lower than that in inbred genotypes during each year (Supplementary Fig. S1). The median severity levels for hybrid genotypes were 4.0, 4.3, 4.0, 5.2, and 5.7 in 2016 to 2020, respectively, whereas the median severity levels for inbred genotypes were 7.0, 7.5, 5.0, 7.3, and 7.7 in 2016 to 2020, respectively (Fig. 1).

    Fig. 1.

    Fig. 1. Distribution of sheath blight (ShB) severity in inbred and hybrid rice genotypes at Beaumont and Eagle Lake, TX, in 2016 through 2020.

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    Ninety-two (53%) of the 173 hybrid genotypes were rated moderately resistant to ShB, with the remaining 47% rated moderately susceptible (Supplementary Table S1). Twenty-two hybrid breeding lines (TH5414, 405A/163, TH5312, TH539, TH551, 435A/163, TH5514, TH559, 333A/153, 339A/153, TH531, TH5314, TH533, TH535, TH5412, TH543, TH549, TH5512, TH553, TH5614, 339A/163, and 196s/163) expressed the lowest levels of ShB severity, with a disease severity rating of <4.0. All commercial hybrid cultivars XL753, CLXL745, XP760, and CLGemini214 were rated moderately resistant or moderately susceptible, with a rating of 5.2 or less. In contrast, 5 (3%) of the 155 inbred genotypes were rated moderately resistant, 86 (55%) were rated moderately susceptible, and 64 (41%) were rated susceptible or very susceptible (Supplementary Table S1). Taggart, Rondo, RU1303116, RU1603144, and RU1603187 were the five inbred cultivars and breeding lines that were rated moderately resistant, with ratings ranging from 4.5 to 4.8.

    The mean ShB severity for hybrids was significantly lower (P ≤ 0.05) than that for inbreds each year at both sites (Table 4). At Beaumont, the percent reductions in disease severity in hybrid rice compared with inbred rice were 19, 38, 19, 25, and 22% in 2016 to 2020, respectively, with a 5-year average reduction of 25%. At Eagle Lake, the percent reductions in disease severity in hybrid rice compared with inbred rice were 36, 40, 22, 25, and 26% in 2016 to 2020, respectively, with a 5-year average reduction of 30%. Across all years and locations, the average ShB severity in hybrid rice was 27% lower than that in inbred rice.

    Table 4. Mean sheath blight severities in inbred and hybrid genotype groups at Beaumont and Eagle Lake, Texas in 2016 through 2020

    NBLS severity between inbred and hybrid rice.

    NBLS severity was significantly (P ≤ 0.0014) affected by genotype, cultivar type, location, and their interactions during each of the 4 years evaluated (Table 3).

    NBLS only developed on four hybrid genotypes (TH5612, TH613, TH633, and TH569) at both Beaumont and Eagle Lake during the 5 years evaluated, with the remaining 169 hybrid genotypes showing an immune response (Fig. 2, Supplementary Fig. S2). In contrast, except for the 2017 evaluation at Eagle Lake, where no significant disease development occurred, NBLS developed in most inbred genotypes, but with large variations in disease severity. Similar patterns of disease severity were observed for inbred genotypes at Beaumont and Eagle Lake (Fig. 2, Supplementary Fig. S2). Thirty-five (23%) inbred genotypes exhibited immune reactions to NBLS, 65 (42%) were rated resistant, and 55 (37%) were rated moderately resistant, moderately susceptible, or susceptible (Supplementary Table S2). At Beaumont, the median severity levels for inbred genotypes were 2.8, 2.2, 6.3, 4.0, and 0 in 2016, 2017, 2018, 2019, and 2020, respectively, whereas at Eagle Lake the median severity levels were 3.3, 0, 3.0, 2.3, and 2.3 in 2016, 2017, 2018, 2019, and 2020, respectively (Fig. 2).

    Fig. 2.

    Fig. 2. Distribution of narrow brown leaf spot (NBLS) severity of inbred and hybrid rice genotypes at Beaumont and Eagle Lake, TX, in 2016 through 2020.

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    On average, except for two cases, NBLS severity in hybrid genotypes were all zero during the 10 year × location evaluations (Table 5). The average severity levels in inbred rice across two locations were 2.7, 1.1, 4.0, 2.9, and 1.3 in 2016, 2017, 2018, 2019, and 2020, respectively. Across all 5 years, the average percent reductions in NBLS severity in hybrid rice compared to inbred rice were 96 and 100% at Beaumont and Eagle Lake, respectively.

    Table 5. Mean narrow brown leaf spot (NBLS) severity in inbred and hybrid genotype groups at Beaumont and Eagle Lake, Texas in 2016 through 2020

    Discussion

    ShB and NBLS are two important diseases affecting rice plant growth, grain yield, and milling quality. Examining and understanding the performances of hybrid rice and inbred rice on field resistance against both diseases will help with the development of effective management strategies for controlling both diseases. The current research involved 173 hybrid and 155 inbred genotypes over 5 years in two locations in Texas environments. The results showed significant differences in resistance to ShB by hybrid and inbred rice genotypes, and that hybrid rice is generally less susceptible. Such patterns were consistently observed across years and locations. Consistently lower median and mean levels of ShB severity were observed in hybrids across all years and locations evaluated. Fifty-three percent of 173 hybrid genotypes were rated as moderately resistant, whereas only 3% of 155 inbred genotypes were rated moderately resistant. The results of the current study support the conclusions of previous research indicating that there are no rice germplasms with highly resistant or immune reactions and that all rice cultivars are susceptible to ShB (Molla et al. 2020; Singh et al. 2002; Willocquet et al. 2012; Zhou et al. 2017, 2019).

    The potential mechanisms involved in enhanced ShB resistance in hybrids are not fully understood. Most previous studies have focused on research to understand the mechanisms associated with the higher yielding potential of hybrids compared to that of inbreds. This improvement is contributed by a relatively higher leaf area index, longer leaf area duration, higher dry matter accumulation before heading, and higher photosynthetic capability at the grain filling stage in hybrid rice compared with those of inbred rice (Dutta et al. 2002; Haque et al. 2015; Horie et al. 2003; Katsura et al. 2007). These traits of hybrids have not been translated to enhanced resistance against ShB in inbreds. In the literature, however, it has been reported that plant height has a role in enhancing ShB resistance in inbred rice. Marchetti (1983) and Sharma et al. (1995) reported that taller inbred rice is more resistant to the infection of ShB. Willocquet et al. (2012) performed a study involving a large set of inbred genotypes and reported that, of all plant traits (plant height, tiller width, number of green leaves, and leaf length), plant height is the most consistent and strongest morphological predictor of ShB severity in a negative relationship. The preliminary results of our study that evaluated the impact of plant height of 19 commercially available hybrid and inbred cultivars on ShB severity also indicate a negative correlation between rice plant height and ShB severity (Zhou, unpublished data). All the hybrid cultivars were taller and had a significant lower level of ShB severity compared with most inbred cultivars evaluated during this preliminary study. It would take more time for the runner hyphae of the fungus to spread vertically from the initial infection site near the water surface to the upper canopy and cause yield loss in taller hybrid rice than shorter inbred rice. However, the confounding effect of all hybrids being taller prevents the ability to determine if plant height or some other factor of hybrids is responsible for the increased level of tolerance found in hybrids. Plant morphological traits are among the most important factors that determine resistance against the infection and spread of ShB (Tang et al. 2007; Willocquet et al. 2012; Wu et al. 2014). ShB resistance is quantitative and controlled by multiple genes (Pinson et al. 2005; Zuo et al. 2014). Quantitative trait loci associated with partial ShB resistance have been observed in inbreds (Molla et al. 2020). The correlation between plant height and ShB resistance has also been confirmed by previous quantitative trait loci studies (Eizenga et al. 2013; Fu et al. 2011; Nelson et al. 2012; Pinson et al. 2005; Sato et al. 2004). Improved ShB resistance in the hybrid genotypes observed during this study could have resulted from their sterile lines, restorer lines, or the interaction of parents with partial ShB resistance traits. However, further research is needed to understand these potential mechanisms associated with enhanced ShB resistance in hybrids. Resistance in rice is an outcome of genotype and environment interactions (Persaud et al. 2019; Zeng et al. 2017).

    Increasing the understanding of the differences in ShB resistance between hybrid rice and inbred rice is important for improving disease management. Commercially available hybrid cultivars in the southern United States have been considered more resistant to ShB and other diseases than inbred cultivars, thereby leading to a significant reduction in rice acreage treated with fungicides. However, to what extent hybrids are more resistant than inbreds remains largely unknown. The current research provides the first insight into the extent to which ShB resistance in hybrids is greater than that in inbreds. The results of this study can help develop more effective and profitable ShB management strategies when making a fungicide application decision. Currently, the use of fungicides is the primary method of controlling ShB disease (Groth 2005; Uppala and Zhou 2018). This is because no cultivars, regardless of cultivar type (hybrid or inbred), with acceptable levels of resistance are available (Mew et al. 2004; Molla et al. 2020; Prasad and Eizenga 2008; Willocquet et al. 2012). Fungicide applications are warranted when planted cultivars are susceptible, disease pressure is high, infection occurs at early stages, and weather conditions are conducive (Groth and Bond 2007; Uppala and Zhou 2018). The integrated use of cultivar resistance and fungicides is the best approach to managing ShB to maximize production returns. The resistant cultivars and breeding lines, including Taggart, Rondo, RU1303116, RU1603144, and RU1603187, identified during this study could provide sources of resistance to developing new cultivars with improved ShB resistance.

    NBLS pressure during our 5-year, two-location field study was relatively lower than the ShB pressure. This is partly because NBLS develops from naturally occurring inoculum, whereas ShB develops from artificial inoculum. However, significant differences in NBLS among genotypes, especially between the hybrid genotype group and inbred genotype group, were consistently observed. All but four hybrid genotypes exhibited immune reactions to NBLS; however, even these four had a disease severity rating of <2 on a scale of 0 to 9, indicating a high level of resistance. In contrast, 77% of the inbred genotypes exhibited NBLS symptoms, with disease reactions ranging from resistant to susceptible. The results of this evaluation demonstrate the superior performance of hybrid genotypes compared to that of inbred genotypes for NBLS resistance. In addition, within the inbred genotype group, 35 (23%) of the genotypes showed immune reactions and 65 (42%) were rated as resistant, which is in sharp contrast to the results for ShB indicating that no immune or highly resistant genotypes are present. These differences suggest that NBLS resistance in rice might be controlled by major genes. Research aimed at identifying NBLS resistance associated with quantitative trait loci and major genes has been initiated at the Louisiana State University AgCenter (Addison et al. 2020).

    NBLS can cause significant grain yield and quality loss in susceptible cultivars, especially in late plantings and in the ratoon crop, under wet and warm weather conditions in Texas and Louisiana (Mani et al. 2016; Uppala and Zhou 2019). The results of the current study have implications for disease management. Planting with hybrid cultivars and highly resistant inbred cultivars identified during the current study is the most effective management approach. Planting with a susceptible cultivar may require an application of fungicide for NBLS control when conducive conditions are present. An application of azoxystrobin plus difenoconazole (Amistar Top), the only fungicide labeled for use on the ratoon crop in the United States, may also be warranted for NBLS control in the ratoon crop. The main crop heading stage is the best time to apply fungicide to control NBLS in both main and ratoon crops (Uppala and Zhou 2019). Mani et. al (2016) reported that propiconazole fungicide is recommended for controlling NBLS on moderately resistant cultivars if they are planted late.

    In conclusion, hybrid rice has better resistance against ShB and NBLS than inbred rice. Hybrid rice exhibited an average of 27% greater resistance to ShB than inbred rice. Almost all hybrids showed immune reactions to NBLS, whereas most inbreds exhibited various disease reactions to NBLS. The highly resistant cultivars and elite breeding lines identified during the current study can serve as sources of resistance genes that can be used for developing new cultivars with improved resistance to ShB, NBLS, or both. The findings of this research could also provide the basis for developing host resistance management practices for the effective control of one or both diseases. Additionally, other management practices such as brassica cover cropping, biocontrol agent, and dose-reduced fungicide (Handiseni et al. 2015, 2016, 2017; Zhou et al. 2021) can be incorporated in the current rice production systems for integrated control of ShB, which is the most yield-limiting disease in rice in the southern United States.

    Acknowledgments

    We greatly thank Dr. Guangjie Liu, Jason Samford, and Jack Vawter for their technical assistance and field plot management during this study. We also thank student intern Linda W. Zhou for her assistance with disease assessment. We also appreciate the U.S. Uniform Regional Rice Nursery (URRN) cooperative research team for providing rice cultivars used for this research.

    The author(s) declare no conflict of interest.

    Literature Cited

    The author(s) declare no conflict of interest.

    Funding: The hybrid line development was supported with generous funding from the Texas Rice Research Foundation Jack B. Wendt Endowed Chair in Rice Research. This research was also supported by the China Scholarship Council through the provision of financial support to visiting scholars participating in this study.