Molecular Breeding of Rice Restorer Lines and Hybrids for Brown Planthopper (BPH) Resistance Using the Bph14 and Bph15 Genes
© The Author(s). 2016
Received: 8 March 2016
Accepted: 24 September 2016
Published: 4 October 2016
The development of hybrid rice is a practical approach for increasing rice production. However, the brown planthopper (BPH), Nilaparvata lugens Stål, causes severe yield loss of rice (Oryza sativa L.) and can threaten food security. Therefore, breeding hybrid rice resistant to BPH is the most effective and economical strategy to maintain high and stable production. Fortunately, numerous BPH resistance genes have been identified, and abundant linkage markers are available for molecular marker-assisted selection (MAS) in breeding programs. Hence, we pyramided two BPH resistance genes, Bph14 and Bph15, into a susceptive CMS restorer line Huahui938 and its derived hybrids using MAS to improve the BPH resistance of hybrid rice.
Three near-isogenic lines (NILs) with pyramided Bph14 and Bph15 were obtained by molecular marker-assisted backcross (MAB) and phenotypic selection. The genomic components of these NILs were detected using the whole-genome SNP (Single nucleotide polymorphism) array, RICE6K, suggesting that the recurrent parent genome (RPG) recovery of the NILs was 87.88, 87.70 and 86.62 %, respectively. BPH bioassays showed that the improved NILs and their derived hybrids carrying homozygous Bph14 and Bph15 were resistant to BPH. However, the hybrids with heterozygous Bph14 and Bph15 remained susceptible to BPH. The developed NILs showed no significant differences in major agronomic traits and rice qualities compared with the recurrent parent. Moreover, the improved hybrids derived from the NILs exhibited better agronomic performance and rice quality compared with the controls under natural field conditions.
This study demonstrates that it is essential to stack Bph14 and Bph15 into both the maternal and paternal parents for developing BPH-resistant hybrid rice varieties. The SNP array with abundant DNA markers is an efficient tool for analyzing the RPG recovery of progenies and can be used to monitor the donor segments in NILs, thus being extremely important for rice molecular breeding.
KeywordsRice Brown Planthopper (BPH) Bph14 and Bph15 MAS Hybrid Rice
Rice (Oryza Sativa L.) is one of the most important food sources for more than half of the world population. It is predicted that an additional 116 million tons of rice will be needed by 2035 to feed the growing population (Seck et al. 2012). However, the brown planthopper (BPH, Nilaparvata lugens Stål), which sucks the phloem sap of the rice leaf sheath and transmits viral diseases such as rice grassy stunt virus (RGSV), rice ragged stunt virus (RRSV) and rice wilted stunt virus (RWSV), often leads to severe yield losses in the agricultural industry (Fujita et al. 2013).
More than 90 % of the world’s rice is grown in Asian countries. China is the largest rice-producing country in the world, although the planting area is less than that in India. The total rice production in 2015 was about 208 million tons in China, which accounted for more than 20 % of the world’s total rice yield. Widely grown hybrid rice is one of the main factors contributing to the increase in rice yield in China since the 1970s. The IRRI estimates that planthoppers cause annual yield losses of 1 to 2 million tons of paddy rice in China (Fujita et al. 2013). The total planting area of rice infested by BPH in China exceeded 25 million hectares between 2005 and 2007 (Qiu et al. 2012). Rapid expansion of the planting area of hybrid rice is probably one of the main causes of the BPH crisis because most of the hybrid rice varieties released in China are susceptible to BPH (Hu et al. 2012). The area planted to hybrid rice has already increased by over 50 % in China, and the planted area of hybrid rice in India and other Asian countries such as Vietnam, Myanmar and Indonesia, has also increased in recent years (Horgan and Crisol 2013). Therefore, it is a very urgent task to develop hybrid rice cultivars with BPH resistance as soon as possible.
Fujita et al. (2013) reviewed the progress in the identification of BPH resistance genes. To date, 29 major BPH resistance genes/loci have been identified from cultivated, landrace and wild species of Oryza (Fujita et al. 2013; Wang et al. 2015). These are located on 8 of the 12 chromosomes in rice, whereas no BPH genes have been identified on chromosomes 1, 5, 7 and 8. Multiple BPH-resistance loci are closely positioned or overlap on the same chromosome regions, and four gene clusters have been designated as A, B, C and D (Fujita et al. 2013). The continuing validation of BPH-resistance loci offers possibilities for rice molecular breeding.
Compared with traditional chemical control, a host plant resistance breeding strategy is a more effective and environmentally friendly method to control BPH damage (Jairin et al. 2010; Sun et al. 2005). Molecular marker-assisted selection (MAS) is a highly efficient approach for plant-breeding scientists to select target genes both rapidly and precisely (Tanksley et al. 1989). It has been certified that pyramiding of resistance genes can provide stronger and more durable resistance for susceptible rice cultivars in contrast to single gene introgression. Myint et al. (2012) found that the BPH resistance level of Bph25 + Bph26-NILs was significantly higher than Bph25-NILs or Bph26-NILs. Qiu et al. (2012) found that the indica rice 9311 and japonica rice Nipponbare lines with pyramided Bph6 and Bph12 had obviously less damage compared to monogenic lines.
Bph14 and Bph15, separately located on chromosome 3 and 4 in B5 (a breeding line derived from O. officinalis), are two widely adopted genes in the BPH-resistance breeding practice (Huang et al. 2001; Li et al. 2006; Xia et al. 2010; Zhu et al. 2013a; Zhu et al. 2013b; Hu et al. 2012; Hu et al. 2015; Cai et al. 2015). Bph14 was the first cloned BPH resistance gene and encodes a coiled-coil, nucleotide-binding and leucine-rich repeat (CC-NB-LRR) protein (Du et al. 2009). Bph15 was previously mapped to a 47-kb region, but the latest research showed that the region containing Bph15 was nearly 580 kb between DNA marker g12140-2 and marker T12 in B5, which originated from the C genome of O. officinalis (Yang et al. 2004; Lv et al. 2014). A previous study found that the BPH-resistance effect of Bph15 was higher than that of Bph14. Moreover, both Bph14 and Bph15 exhibit partial dominance and have a pronounced dosage effect on the resistance to BPH in hybrids (Li et al. 2011; Hu et al. 2012).
Huahui938 is an elite rice restorer line of CMS selected by our laboratory in previous years. We developed several hybrids with high yield, good quality and resistance to blast using Huahui938 as a male parent. However, Huahui938 and its derived hybrids are susceptible to BPH. In the present study, we further improved the BPH-resistance of Huahui938 and its derived hybrids by pyramiding Bph14 and Bph15 using marker-assisted backcross selection (MAB) and whole-genome SNP array analysis, following the effective evaluation of pyramided genes conferring resistance to BPH in the improved NILs and the corresponding hybrids.
Development of NILs with Bph14 and Bph15 Genes Using MAB
Resistance Reaction of the Selected NILs and Hybrids in Response to BPH
The Performance of Agronomic Traits of the NILs and Their Hybrids
The agronomic and rice quality traits of the three selected NILs and their derived hybrids
Traits of grain qualities
The evaluation results of the agronomic and rice quality traits of hybrids derived from the selected NILs showed that most of traits were identical to those of the hybrids derived from the recurrent parent, Huahui938 (Table 1). Among them, the GY of improved hybrid Luohong4A/HB13002-9-7 was not significantly different from that of the control Luohong4A/Huahui938. In addition, all three improved hybrids had better rice quality with a higher HR and significantly lower CK and CD compared with Luohong4A/Huahui938. Furthermore, most of the agronomic traits of the three improved Quan9311A/NILs were identical to the control Quan9311A/Huahui938 except that Quan9311A/ HB13002-30-10 had a higher GW. Additionally, all three hybrids derived from Quan9311A had a better rice quality with a significantly lower chalky grain rate (CK). Compared to Fengliangyou4, a popular and outstanding hybrid variety in agricultural production, the hybrid Luohong4A/HB13002-9-7 showed similar GY but shorter DTH and lower PH. Meanwhile, the hybrid Quan9311A/HB13002-9-7 had a significantly higher GY and lower CK compared with Fengliangyou4 (Table 1). The BPH-resistant NILs and hybrids, which were identical to the recurrent parent and its derived hybrids with respect to the agronomic and rice quality traits, are more strongly desired.
BPH has been one of the important factors constraining rice yield. As the area of cultivated hybrid rice varieties gradually expands around the world, their resistance to BPH is attracting increasing attention by rice researchers (Hasan et al. 2015). Numerous BPH resistance genes have been introduced and pyramided into elite rice varieties, which has resulted in strongly improved capacity of rice to endure damage caused by BPH (Myint et al. 2012; Qiu et al. 2012; Wan et al. 2013; Suh et al. 2011). With the adaptation of BPH to resistant varieties and the evolution of a new biotype of BPH (Fujita et al. 2013), different BPH resistance genes still need to be pyramided into multiple elite hybrid rice varieties to overcome these problems. In the present study, through molecular-marker assisted backcross (MAB) breeding, we successfully transferred two BPH-resistance genes, Bph14 and Bph15, into an elite restorer line Huahui938 to obtain three improved lines, which showed enhanced resistance to BPH compared with the controls. When these NILs were crossed with the CMS line with the same BPH resistance genes, the hybrids (homozygous genotype with resistance loci) were resistant against BPH. Some derived hybrids had higher yield and more desirable rice qualities and agronomic performance compared with the controls. Therefore, it is possible to develop hybrid rice with high BPH resistance and excellent agronomic performance in the future and to solve the problem of hybrid rice being susceptible to BPH (Horgan and Crisol 2013).
The effect of BPH resistance genes would be influenced by various genetic backgrounds (Qiu et al. 2012; Jairin et al. 2010). Some previous studies demonstrated that hybrids with heterozygous Bph14 and Bph15 showed moderate resistance to BPH (Hu et al. 2012; Hu et al. 2013). However, our results indicated that the heterozygote of these two genes was susceptible to BPH in some hybrid backgrounds at the seedling stage. In fact, BPH resistance genes with a partial dominant effect would show moderate resistance or would be susceptible to BPH in a heterozygous state under different genetic backgrounds (Liu et al. 2016). Therefore, it is essential to simultaneously stack Bph14 and Bph15 into male and female parents to guarantee hybrids with certain and durable resistance to BPH.
With respect to rice genetic improvement, developing NILs is the optimal approach to obtain modified lines with desired traits. Molecular marker-assisted selection (MAS) is a very powerful tool to accelerate the progress of developing NILs with pyramided resistance genes and to maintain the desirable characteristics of the recurrent parent. Numerous NILs have been developed with enhanced disease resistance, such as blast resistance, sheath blight resistance, and bacterial leaf blight resistance, under different genetic backgrounds (Miah et al. 2015; Khanna et al. 2015; Chen et al. 2014; Suh et al. 2013; Balachiranjeevi et al. 2015).
In previous studies in which NILs were developed, hundreds of RFLP or SSR markers were usually used for recovering and detecting the genetic background. It is time-consuming and low-efficiency work to identify polymorphism markers between the donor and recipient parent (Chen et al. 2000; Suh et al. 2011; Ahmed et al. 2016). However, it is easy to identify sufficient polymorphism SNP markers for background analysis due to the high-density and extensive marker positioning in an SNP array. In a comparative study estimating the similarity between the recurrent parent and the developed NILs, Khanna et al. (2015) found that the percent similarity was overestimated by SSR markers, and the background analysis using an SNP array was almost 300 times more cost effective and provided a more precise estimation due to higher resolution.
In this study, the genetic background of the improved NILs was analyzed using the SNP array RICE6K, which contains 5,102 SNP and InDel markers. We detected 550 SNP markers showing polymorphisms between Huahui938 and B5 in an efficient amount of time. Jiang et al. (2015) examined the genetic background recovery of developed lines using the same RICE6K array and obtained accurate results. Mi et al. (2016) obtained a modified 9311 line carrying stacked genes f5-n and S5-n with an RPG recovery rate higher than 99 % using RICE6K, and a higher density SNP array in the BC5 generation and the agronomic performance of those NILs did not differ from the recurrent parent 9311. Thus, as the cost of genotyping using an SNP array decreases, it will be possible to use this powerful tool to develop NILs in all breeding schemes in the near future.
In the present study, the hybrid combination Luohong4A/HB13002-50-9-7 exhibited BPH resistance, high yield and good rice quality similar to that of Fengliangyou4. We affirm that this hybrid can be used for rice production in the BPH epidemic region in southern China. The yield of Quan9311A/HB13002-50-9-7 was the highest among the tested combinations even though it showed no resistance against BPH at the seedling stage. We believe this can be used as a high yield hybrid for production in areas where BPH does not occur.
In this study, we successfully transferred both Bph14 and Bph15 into the CMS rice restorer line, and three BPH-resistance NILs were obtained. The results showed that when both male and female parents contained the same BPH resistance genes, the hybrids were resistant against BPH. The combination Luohong4A/HB13002-50-9-7 obtained in this study had high yield, BPH resistance, superior rice quality and desirable agronomic performance, showing a remarkable commercial potential for hybrid rice production in BPH epidemic areas.
Rice Materials and Breeding Scheme
DNA Extraction, PCR, Markers and Genotyping
Total genomic DNA was extracted from fresh rice leaves using the modified CTAB method following Dellaporta et al. (1983). PCR reactions were carried out as described by Jiang et al. (2015). PCR reactions were performed using a MyCycler™ thermal cycler (BIO-RAD USA) with 20 μl reaction mixture that contained 20 ng genomic DNA, 10 mM Tris-HCl (pH 9.0), 50 mM KCl, 2.5 mM MgCl2, 2 mM dNTPs, 10 μM each of the forward and reverse primers, and 1 unit of Taq DNA polymerase. The PCR amplification program consisted of one cycle of denaturation at 95 °C for 5 min, followed by 35 cycles at 95 °C for 30 s, 56 °C for 30 s, 72 °C for 45 s, with a final extension at 72 °C for 7 min. The InDel marker 76-2 (primer sequences F: 5′-GCACATACAGAAATGGTGAA-3′, R: 5′-GGCAAGGGACATGTAGTAAC-3′) linked to Bph14 was used to select positive individual plants with respect to the Bph14 locus in each generation (Du et al. 2009). The SSR marker MS5 (primer sequences F: 5′- TTGTGGGTCCTCATCTCCTC-3′, R: 5′-TGACAACTTGTGCAAGATCAAA-3′) linked to Bph15 (Yang et al. 2004) and the InDel marker InD4 (primer sequences F: 5′-AGAATGCTAAAGATGACTGAA-3′, R: 5′-AACGGTATTGTTCTTGTCTAA-3′), which was more tightly linked to Bph15 (Lv et al. 2014), were used to select individual positive plants in each generation. The PCR products were analyzed using 4 % denaturing polyacrylamide gel electrophoresis. In addition, the whole-genome single nucleotide polymorphism (SNP) array RICE6K was used to analyze the genetic background similarity of the selected NILs with respect to the recurrent parent Huahui938. This SNP array was developed based on Infinium technology, which contains 5102 SNP and insertion-deletion (InDel) markers evenly distributed on the 12 chromosomes of rice with an average density of 12 SNPs per 1 Mb (Yu et al. 2014). For each improved line, total DNA was extracted from 20 plants leaves. Genetic background similarity analysis was performed at the Life Science and Technology Center, China National Seed Group Co., LTD (Wuhan, China), according to Infinium HD Assay Ultra Protocol (http://www.illumina.com/).
BPH Bioassay for the Selected NILs and Their Hybrids
The BPH resistance evaluations of the selected NILs and their hybrids were conducted in a net house. Huahui938, Quan9311A, Fengliangyou4 and TN1 were used as susceptible controls, while Luohong4A and the donor parent B5 were used as the BPH resistant controls. The BPH samples used in the test were collected from the field and were continuously reared on TN1 in the laboratory at Huazhong Agricultural University (HZAU), Wuhan, China. The bioassay was performed using a modified seedling bulk test following the SSST (Velusamy et al. 1986; Horgan 2009). Thirty pre-germinated seeds of each entry, including the improved lines and controls with three replications, were evenly sown in 7 × 7 × 8 cm plastic plates. All entries were randomly arranged in a large pool. When the seedlings reached the second leaf stage, they were thinned to 20 plants per plate. At the third-leaf stage, the seedlings were infested with 2nd-3rd-instar BPH nymphs at a rate of 8–10 insects per seedling, and the water was maintained at a depth of approximately 0.5 cm above the root until the evaluation was completed. All seedlings were patted once, 24 h after the infestation, to evenly redistribute the nymphs. When all TN1 plants died, the other plants were examined and the following scores were given: 0 (no damage), 1 (very slight damage), 3 (the first and second leaf of most plants were yellowing), 5 (yellowing, nearly half of the plants had wilted or were dead), 7 (more than half of the plants were dead and the rest were seriously dwarfed) and 9 (all plants were dead) according to the modified criteria based on the Standard Evaluation System for Rice (IRRI 2002). An average resistance score of 0.1–1.9 was designated as highly resistant (HR), 2.0–3.9 as resistant (R), 4.0–5.9 as moderately resistant (MR), 6.0–7.9 as susceptible (S), and 8.0–9.0 as highly susceptible (HS) (IRRI 2002).
Evaluation of Agronomic and Grain Quality Traits
To evaluate the agronomic and rice quality traits, Huahui938, B5, three improved NILs and their derived hybrids from Quan9311A and Luohong4A were planted in a randomized complete block design with three replications at Wuhan, China, in the summer of 2015 under natural field conditions. Each plot consisted of three rows with 10 plants per row at a planting density of 16 cm between plants within a row and 20 cm between rows. The agronomic and rice quality traits were measured according to the standard evaluation system for rice (IRRI 2002). Five mature plants in the middle row were harvested for measurements. The agronomic traits evaluated included number of days to heading (DTH), plant height (PH), panicle length (PL), panicle number (PN), number of grains per panicle (NGP), fertility of the spikelet (FER), grain yield (GY), and 1000-grain weight (GW). The harvested seeds were stored at room temperature for three months at 14 % moisture content. The following grain quality traits were tested: head rice rate (HR), ratio of grain length to width (L/W), chalky grain rate (CK), chalkiness degree (CD), amylose content (AC) and alkali spreading value (ASV).
The background recovery percentage (BRP) was calculated using the following formula: BRP (%) = (R + 1/2H) × 100/P. In this formula, R, H, and P indicate the number of SNP markers homozygous for Huahui938, the number of markers that remained heterozygous, and the total number of polymorphic markers between Huahui938 and B5, respectively. One-way ANVOA and least significant difference (LSD) tests were performed using the SAS statistical software package (version 9.0; SAS Institute, Cary, NC).
Alkali spreading value
Background recovery percentage
Chalky grain rate
Cytoplasmic male sterility
Hexadecyl trimethyl ammonium bromide
Number of days to heading
Fertility of the spikelet
Head rice rate
International Rice Research Institute
Ratio of grain length to width
Least significant difference tests
Molecular marker-assisted backcross
Number of grains per panicle
Polymerase chain reaction
Rice grassy stunt virus
Recurrent parent genome
Rice ragged stunt virus
Rice wilted stunt virus
Standard evaluation system
Single nucleotide polymorphism
Simple sequence repeat
Standard Seedbox Screening Test
Thermo-sensitive genetic male-sterile lines
This research was partially supported by the National High Technology Research and Development Programs of China (863 Programs, “Breeding of New Varieties of Green Super Rice”, Grant No. 2014AA10A604), Wuhan municipal government R & D programs (Grant No. 2014020202010136) and the Bill & Melinda Gates Foundation “Green Super Rice for the Resources-Poor of Africa and Asia”.
HBW carried out the experiments, partial MAS, bioassay of BPH resistance and evaluation of agronomic and rice grain quality traits. STY did partial MAS. TMM conceptualized the study and did phenotype selection. HBW and TMM prepared manuscript together. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
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