Introduction

Ever since BPH started appearing in epidemic proportions first in IRRI farm and later in almost all tropical countries during early nineteen seventies, the program on developing varieties resistant to the pest has been initiated. During the early phases, the major emphasis was on identifying sources of resistance from germplasm at IRRI and also in almost all countries where rice is grown. As the saying goes “Necessity is the mother of invention” That created a forceful necessity to develop methods to screen out the bulk of susceptible germplasm and identify the sources on which breeding programs can be based. Several promising donors like Mudgo, ASD 7, Rathu Heenati, Ptb33, Babawee, ARC10550, Swarnalata, T12, Chin Saba, Balamawee were identified. Some of them were involved in breeding program at IRRI (Athwal et al., 1971). That resulted with the development and release of IR26 with Bph1 gene which was later found to be highly susceptible in Hyderabad India and later in the entire south Asian countries or Indian Sub-Continent. Within few years, IR26 was observed to be susceptible even in Philippines. That created awareness among the scientists on tremendous capacity of BPH to overcome the host plant resistance and rendering them susceptible within few generations. Development of more virulent biotypes was also proved to be true with the help of greenhouse experiments first at IRRI and later in many other countries. The realization that BPH present in Indian subcontinent is more virulent than BPH in other Asian countries created awareness to have reaction of newly developed IRRI varieties to possess resistance to south Asian biotype also.

Soon there was more emphasis to identify resistance in wild rices also. Thus, IRRI along with other national programs started identifying sources and genes of resistance to BPH in various wild rices and different accessions in each of wild species of genus Oryza. The wild species of genus Oryza used so far in different countries are Oryza rufipogon (AA genome), O.officinalis (CC genome), Oryza eichingeri (CC genome), O. minuta (BBCC genome), O. latifolia (CCDD genome), O. australiensis (EE genome), O. punctata (BB and BBCC)and O. granulate (GG genome), (Brar and Khush, 1997).

Prahalada et al., (2017) reported that thirty BPH resistance genes have been identified and mapped to six of the 12 chromosomes (2, 3, 4, 6, 11, and 12) of rice. Among those, only 17 genes (BPH1, BPH2, BPH6, BPH9, BPH12, BPH14, BPH15, BPH17, BPH18, BPH19, BPH25, BPH26, BPH27, BPH28, BPH29, BPH30,31 and BPH32) have been fine-mapped, However, only seven genes (BPH14, BPH17, BPH18, BPH26, BPH29, BPH9 and BPH32) have been cloned and characterized (Du et al. 2009; Tamura et al., 2014; Liu et al., 2015; Wang et al., 2015; Ji et al., 2016; Ren et al., 2016; Zhao et al., 2016). But, most of the identified resistance genes are biotype/population specific and do not provide strong resistance to different BPH biotypes/populations.

It will be more appropriate to reveal the progress on host plant resistance to BPH at IRRI as well as in various national programs in different rice growing countries.

1 IRRI

International Rice Research Institute (IRRI) located at Los Banos, in Philippines near the capital city of Manila stood worthy of its name as a truly international in character ever since it was established in 1960. The institute laid strong foundation in research on all aspects of rice cultivation both in generating the genetic material, knowledge generation and updating on all other aspects of rice culture. Regarding the research on BPH also IRRI continued the same trend.

1.1 Early research work and standardization of methodologies

Immediately after BPH started appearing as a pest of dwarf high yielding rice varieties which were first created at IRRI Research Farm, Dr. D.S. Athwal working as plant-breeder and Dr. M.D. Pathak working as entomologist took a serious note of the situation and started looking for varieties which could with-stand the attack of this deadly insect pest. They have also arranged an international symposium in 1978 and published the proceedings during the next year with the title “Brown Planthopper- a Threat to Rice Production in Asia”. They have also standardized the technique to screen many varieties in a short time to eliminate the bulk of the susceptible germ-plasm and identify small number of promising donors for involvement in breeding program. The work was further carried forward by next generation plant breeder Dr. Gurdev S. Khush and entomologist Dr. E.A. Heinrichs. During later period Dr. Darshan S. Brar followed by Dr. Kshirod K. Jena took active interest and carried the mantle forward. Later on, when Dr. Kshirod K. Jena was posted to Korea as Temperate Rice Breeder he has made strenuous efforts in identifying new genes for BPH resistance and incorporating them in rice varieties suitable for Korean situation. Apart from active research they have reviewed the ongoing global work from time to time and updated the available information (Brar and Khush, 1997; Jena and Mackill, 2008; Brar et al., 2009; Jena and Kim, 2010). From Entomology side after Dr. E.A. Heinrichs, Dr R.C. Saxena, Dr M. B. Cohen and Dr Z.R. Khan also contributed a lot and published several papers.

From the beginning IRRI’s emphasis was on exploiting cultivated varieties and wild rices for BPH resistance and transferring resistance genes to locally suitable varieties through biotechnological tools.

BPH-resistant variety IR26 with the Bph1 gene for resistance was released in the Philippines in 1973 and in Indonesia and Vietnam in 1974. It was widely planted in those countries. A biotype appeared in 1977 that could damage IR26; it was designated as biotype 2. After the breakdown of resistance in IR26; the varieties IR36 and IR42 bph2 with gene were released (Khush, 1977). They were widely adopted in the Philippines, Indonesia, and Vietnam but were found to be susceptible to South Asian biotype (biotype 4). IR42 became susceptible in North Sumatra Province of Indonesia in 1982. These varieties were resistant until 1989-90. IR56 with the Bph3 gene was released in 1982 in the Philippines. Several other varieties (IR60, IR62, IR68, IR72, and IR74) were released and were resistant to biotype 3. Some varieties are resistant on the Indian subcontinent but susceptible in Southeast and East Asia (Brar et al., 2009).

1.2 Attempts to transfer BPH resistance genes from Oryza officinalis and Oryza australiensis

Jena et al., (1992) attempted to transfer BPH resistance genes from wild rice Oryza officinalis to cultivated rice varieties of Oryza sativa. Fifty-two introgression lines (BC2 F8) from crosses between two Oryza sativa parents and five accessions of O. officinalis were analyzed for the introgression of O. officinalis chromosome segments. DNA from the parents and introgression lines was analyzed with 177 Restriction fragment length polymorphism (RFLP) markers located at approximately 10 cM intervals over the rice chromosomes. Most probe/enzyme combinations detected RFLPs between the parents. Of the 174 informative markers, 28 identified putative O. officinalis introgressed chromosome segments in 1 or more of the introgression lines. Introgressed segments were found on chromosomes 11 of the 12. In most cases of introgression, O. sativa RFLP alleles were replaced by O. officinalis alleles. Introgressed segments were very small in size and similar in plants derived from early and late generations.

In another study by Ishii et al., (1993), they carried out RFLP analysis to tag the alien genes for BPH resistance and earliness introgressed from wild species Oryza australiensis into cultivated rice, O. sativa L. One introgression line (IR65482-4-136-2-2), resistant to biotypes 1, 2, and 3 of BPH and early in flowering, was selected from BC F4 of the cross between O. sativa (IR31917-45-3-2) and O. australiensis (accession 100882). Recurrent parent, O. australiensis, and introgression line were surveyed for RFLP using probes of chromosomes 10 and 12. Two probes, RG457 and CD098, detected introgression from O. australiensis. Cosegregation between introgressed characters and molecular markers was studied in F2, derived from the cross between the introgression line and recurrent parent. The gene for BPH resistance is linked with RG457 of chromosome 12 at a distance of 3.68±1.29 Centimorgan (cM), and the gene for earliness is linked with CD098 of chromosome 10 at a distance of 9.96 ±3.28 cM. Such close linkage is useful in marker-based selection while transferring BPH resistance from introgression line into other elite breeding lines (a centimorgan (cM) or map unit is a unit for measuring genetic linkage). It is defined as the distance between chromosome positions for which the expected average number of intervening chromosomal crossovers in a single generation is 0.01. It is often used to infer distance along a chromosome.)

Huang et al., (1997) have developed an RFLP framework map with 146 RFLP markers based on a doubled haploid population derived from a cross between an indica variety IR64 and a japonica variety Azucena. The population carries 50.2% of IR64 loci and 49.8% of Azucena loci, indicating an equal amount of genetic materials from each parent has been transmitted to the progenies through another culture. However, some markers showed segregation distortion. These distorted marker loci are located on 10 chromosomal segments. Using this map, they were able to place 8 isozymes, 14 RAPDs, 12 cloned genes, 1 gene for BPH resistance onto rice chromosomes. The major gene for BPH resistance was mapped on chromosome 12 near RG463 and isozyme Sdh-1. In another study, Lang et al., (1999) have done STS marker analysis of the introgression lines for BPH resistance from O. autraliensis and O. sativa. Two introgression lines (IR65482-4-136, and IR65482-17-511) resistant to BPH biotypes 1, 3 were selected from BC2F4 of the cross between O. sativa (IR31917-45-3-2) and O. australiensis (accession 100882).

1.3 Fine mapping of Bph-10 and Bph18 genes after introgression from Oryza australiensis

Lang and Buu, (2003) have transferred Bph-10 gene from O. australiensis into IR54742 through introgression. They have done further Fine mapping of Bph-10 gene with mapping population derived from a cross of IR31917-45-3-2 / IR54742. Through bulked segregant and linkage analyses, Bph-10 was detected within 4.6 cM region in chromosome 12. Jena et al., (2006) have identified a major resistance gene, Bph18 (t), in an introgression line (IR65482-7-216-1-2) that has inherited the gene from the wild species Oryza australiensis. Genetic analysis revealed the dominant nature of the Bph18 (t) gene and identified it as nonallelic to another gene, Bph10 that was earlier introgressed from O. australiensis. Identification of Bph18 (t) enlarges the BPH resistance gene pool to help develop improved rice cultivars, and the PCR marker (7312.T4A) for the Bph18 (t) gene can be readily applicable for marker-assisted selection (MAS).

1.4 Incorporation of Bph18 gene into japonica cultivars

Suh et al., (2011) based in Korea used the novel resistance gene Bph18 earlier identified by Jena et al., (2006) and incorporated it into an elite japonica cultivar, Junambyeo, which is highly susceptible to BPH. The Bph18 gene was introduced by marker-assisted backcross (MAB) breeding into Junambyeo. The backcrossed progenies were evaluated for desirable agronomic and grain quality traits and the selection of improved breeding lines while simultaneously evaluating for BPH resistance by bioassays in the greenhouse and foreground selection. Of the 26 advanced backcross breeding lines (ABL), four lines showed agronomic traits similar to those of the recurrent parent, with strong resistance to BPH. Molecular genotyping of the four ABL revealed the conversion of genotypes closely resembling the genotype of Junambyeo. The percentage of donor chromosome segments in ABL decreased from 12.3% in the BC2 to 9.4%, 8.4% and 5.3% in BC3, BC4 and BC5 generations, respectively. BPH resistant elite breeding lines with agronomic and grain quality traits similar to those of the recurrent parent were successfully developed by foreground and background analysis in japonica background without linkage drag.

1.5 Entomology research at IRRI on genetic stability of BPH resistant varieties

From entomology side also, they have tried to evaluate the genetic stability of BPH resistant rice varieties released in Philippines earlier. Cohen et al., (1997) studied the mechanism and level of BPH resistance in the popular rice cultivar IR64 with BPH collected from Central Luzon, Philippines. In greenhouse experiments, IR64 showed slight to moderate levels of antibiosis, antixenosis, and tolerance relative to the cultivar IR22 which contains no major genes for BPH resistance. IR64 was also more resistant than IR26 in most experiments, despite the fact that both varieties have the same major gene Bph1. This confirms that IR64 contains one or more additional, apparently minor, genes for BPH resistance. Later Cruz et al., (2011) conducted experiments to study how the varieties with the Bph3 gene for resistance to BPH are still effective in much of the Philippines even after 30 years of their release in 1970s and 1980s. They determined the effects of adaptation to one resistant variety, IR62 assumed to possess the Bph3 gene- on (1) resistance against a series of varieties with similar biotypical responses (presumed to contain the same major resistance genes), and (2) a differential variety with the bph4 gene that occurs at the same chromosome position as Bph3. They also examined the effects of high soil nitrogen on the effectiveness of Bph3. Feeding, planthopper biomass, and development times were reduced in a wild BPH population when reared on IR62 compared with the susceptible standard variety TN1. However, nitrogen application increased the susceptibility of IR62. After 13 generations on IR62, BPH had adapted to the plant’s resistance. Virulence of the adapted BPH against the variety ‘Rathu Heenati’ supports the idea that Bph3 is present in IR62. Across similar IR varieties (IR60, IR66, IR68, IR70, IR72, and IR74), feeding, planthopper biomass, and development rates were generally higher for IR62-adapted than for non-adapted BPH. However, contrary to the expectations, many of these varieties were already susceptible to wild BPH. Fitness was also higher for IR62-adapted BPH on the variety ‘Babawee’ indicating a close relation between Bph3 and bph4. Based on these results the authors opined that that the conventional understanding of the genetics behind resistance in IR varieties needs to be readdressed to develop and improve deployment strategies for resistance management.

2 Japan

The major emphasis on rice breeding for BPH in Japan is related to mapping of genes which have already been named or identifying new genes which have not so far been identified elsewhere. The major institutes which have undertaken the work are:

1) Kyushu National Agricultural Experiment Station, Chikugo, Fukuoka 833, Japan

2) Plant Breeding Laboratory, Faculty of Agriculture, Graduate School, Kyushu University; Fukuoka 812–8581, Japan

3) Laboratory of Plant Genetics, Department of Biological and Environmental Science, Faculty of Agriculture, Kobe University, 1-1 Rokkodai-cho, Nada-ku, Kobe 657-8501, Japan

4) Rice Genome Research Program, STAFF-Institute, 446-1 lppaizuka, Kamiyokoba, Tsukuba, Ibaraki 305-0854, Japan

5) National Institute of Agrobiological Resources, 2-1-2 Kannondai, Tsukuba 305-8602, Japan

Several scientists have participated in executing the research work.

2.1 Attempts to characterize Bph1 and bph2 genes in japonica background

Hirabayashi and Ogawa (1995) were first to report on the tagging of a BPH resistance gene Bph-1 in rice. They have carried out RFLP analysis and determined the location of Bph-1 gene on the chromosome 12 and not on chromosome 4 as reported earlier. Bph-1 was linked at the recombination value of 10.7 % with a RFLP marker XNpb 248 on chromosome 12. Continuing the studies on BPH resistance gene Bph1, Sharma et al., (2002) have constructed a linkage map of Bph1. RFLP and Amplified fragment length polymorphism (AFLP) markers were selected by the bulked segregant analysis and used in the mapping study of 262 F2s that were derived from a cross of ‘Tsukushibare’, a susceptible japonica cultivar, and ‘Norin-PL3’, an authentic japonica Bph1-introgression line. Twenty markers were mapped within a 28.9-cM region containing the Bph1 locus on the long arm of rice chromosome 12. Combining the result of segregation analysis of BPH resistance by the mass seedling test and that of the markers, the Bph1 locus was mapped within a 5.8-cM region between two flanking markers. The closest AFLP markers, em5814N and em2802N, was at 2.7 cM proximal to the Bph1 locus.

Murata et al., (1998) made an attempt to clarify the nature and position of bph2 rice gene for resistance to BPH. Previously it was reported bph2 to be recessive and either allelic or closely linked to a dominant BPH resistance gene, Bph1. The bph2 gene was introgressed from an indica resistance donor variety, ‘IR1154-243’, into a japonica breeding line, ‘Norin-PL4’. A segregation analysis of BPH resistance in F2 and F3 progenies from a cross of a japonica susceptible variety, ‘Tsukushibare’, and ‘Norin-PL4’, however, showed that the resistance gene in ‘Norin-PL4’ behaved as a dominant gene. Genotyping of ‘Norin-PL4’ using 99 RFLP markers covering all 12 rice chromosomes showed that ‘Norin-PL4’ possessed a large segment of chromosome 12 introgressed from ‘IR1154- 243’. Six RFLP markers on the introgressed segment co-segregated with BPH resistance and bph2 was mapped at 3.5 cM from the closest RFLP marker, G2140. The position of bph2 on the standard ‘Nipponbare’/‘Kasalath’ map was at a considerable distance (about 30 cM) from that of Bph1 previously mapped using a different population. Further, no susceptible recombinants were obtained in a large number of F3 progeny from crosses between two Bph1 carrier lines and ‘Norin- PL4’. The problem of dominance/recessiveness of bph2 could be ascribed to different environments, different genetic backgrounds, or different BPH biotypes used in the bioassay. To test these possibilities, phenotypes of the heterozygotes must directly be determined using genetically defined BPH biotypes.

In further studies on bph2 gene, Murai et al., (2001) have constructed a high-resolution linkage map as a foundation for map-based cloning of the bph2 locus. An advanced mapping population derived from a cross of ‘Tsukushibare’ (a susceptible japonica cultivar) with ‘Norin-PL4’ (an authentic bph2- introgression line) was used. Segregation analysis by the mass seedling test showed that bph2 behaved as a single dominant gene. Through bulked segregant analysis and linkage analysis, bph2 was located within a 3.2-cM region containing eight AFLP markers. One marker (KAM4) showed complete co-segregation with bph2, and bph2 was mapped within a 1.0-cM region delimited by KAM3 and KAM5, two flanking markers. KAM4 was converted into a PCR-based sequence-tagged-site (STS) marker and its co-segregation with bph2 was validated.

2.2 Characterization and fine mapping of bph4 rice gene in Japonica background

Sri Lankan indica rice cultivar Babawee harbors BPH resistance gene bph4. Kawaguchi et al, (2001) tried to locate bph4 rice gene by crossing Babawee as female parent with two susceptible cultivars IR24 (indica) or Tsukushibare (japonica) as male parents. Segregation of the BPH resistance in the two crosses was studied by directly assaying the F2 phenotypes and by determining the F2 genotypes based on the F3 phenotypes. In both cross combinations, the segregation of the BPH resistance significantly deviated from the ratio expected for the single recessive gene model. With RFLP markers the map position of bph4 could not be determined exactly but the gene was assigned to the distal region of the short arm of rice chromosome 6 based on the bulked segregant analysis and linkage analysis.

2.3 Characterization of bph20 (t) and Bph21 (t) genes in relation to BPH populations collected in different periods in Japan

Myint et al., (2009) studied the demographic parameters of four laboratory strains of BPH collected in Japan between 1966 and 2005. They used near-isogenic lines (NILs) and pyramided line (PYL) of rice carrying bph20 (t) and Bph21(t) genes conferring resistance to BPH. Six traits: adult survivorship, development of female abdomen, nymphal survivorship, nymphal developmental period, adult body weight, and oviposition were examined. Based on the adult survivorship and development of female abdomen, the BPH strains of Hatano-66 (BPH collected from Hatano during 1966) and Chikugo-89 (BPH collected from Chikugo during 1989) were avirulent to bph20 (t)-NIL and Bph21(t)-NIL as well as their PYL carrying both bph20(t) and Bph21(t). On the other hand, the BPH strains of Isahaya–99 (BPH collected from Isahaya in 1999) and Nishigoshi-05(BPH collected from Nishigoshi-in 2005) were virulent to bph20(t)-NIL and Bph21(t)-NIL but still avirulent to their pyramided line (PYL). Four other demographic parameters of the avirulent strains of BPH showed low nymph survivorship, prolonged nymphal developmental period, light body weight of adults and small number of eggs laid on the resistant lines to BPH. These results suggest that a resistance mechanism such as feeding inhibition caused by the two major genes conferring resistance to BPH, similarly affect both on nymphal and adult stages. The PYL with both bph20 (t) and Bph21 (t) had an epistatic effect of resistance to the BPH strains migrated into Japan since 1999.

2.4 Scope for reusing Bph2 rice gene along with Bph25, to ensure durable resistance to BPH

The indica rice cultivar ADR52 carries two BPH resistance genes, Bph26 and Bph25. Map-based cloning of Bph26 revealed that Bph26 encodes a coiled-coil-nucleotide-binding-site- leucine-rich repeat (CC-NBS-LRR) protein. Bph26 mediated sucking inhibition in the phloem sieve element. Bph26 was identical to Bph2 on the basis of DNA sequence analysis and feeding ability of the Bph2-virulent biotype of BPH. Bph2 was widely incorporated in elite rice cultivars and was well-cultivated in many Asian countries as a favourable gene resource in rice breeding against BPH. However, Bph2 was rendered ineffective by a virulent biotype of BPH in rice fields in Asia. They suggest that Bph2 can be reused by combining with other BPH resistance genes, such as Bph25, to ensure durable resistance to BPH (Tamura et al., 2014).

3 China

The main line of research work conducted in various organizations in China is on identification and characterization of new genes from wild rices conferring BPH resistance into cultivated rice. The following are the organizations which had major contribution on this aspect.

Ø  China National Hybrid Rice Research Center, Changsha, 410125, China

Ø  China National Rice Research Institute, Hangzhou, 310006, China

Ø  Chinese Academy of Agricultural Sciences, Beijing, 100081, China;

Ø  Chinese Academy of Sciences, Beijing, 100101, China;

Ø  Guangxi Academy of Agricultural Sciences, Nanning, 530007, China

Ø  Guangxi University, Nanning, 530005, China

Ø  Huazhong Agricultural University, Wuhan, 430070, China

Ø  Hubei Academy of Agricultural Sciences, Wuhan, 430064, China

Ø  Nanjing Agricultural University, Nanjing, 210095, China

Ø  South China Agricultural University, Guangzhou, 510642, China

Ø  Wuhan University, Wuhan, 430072, China

Ø  Zhejiang Agriculture and Forestry University, Hangzhou, 311300, China

3.1 Wild rice Oryza eichingeri contributed BPH resistance genes

Wild rice species is an important source of useful genes for cultivated rice improvement. Some accessions of Oryza eichingeri (2n = 24, CC) from Africa confer strong resistance to BPH and WBPH. Guoqing et al., (2001) used RFLP and performed simple sequence repeats (SSR) analysis on disomic backcross plants between Oryza sativa (2n = 24, AA) and O. eichingeri. The objective was to identify the presence of O. eichingeri segments and further to localize BPH-resistant gene. In the introgression lines, 16 O.eichingeri segments were detected on rice chromosomes 1, 2, 6, or/and 10. The dominant BPH resistant gene, tentatively named Bph13(t), was mapped to chromosome 2, being 6.1 and 5.5 cM away from two microsatellite markers RM240 and RM250, respectively.

3.2 BPH resistance in B5 line is located in chromosomes 3 and 4

BPH resistant line B5 has derived its resistance genes from the wild rice Oryza officinalis. In a study, Buna et al., (2001) hybridized B5 with highly susceptible cultivar Taichung Native1. A mapping population composed of randomly selected 167 F2 individuals was used for determining the BPH resistance genes by RFLP analysis. Bulked segregant analysis was conducted to identify RFLP markers linked to the BPH resistance genes in B5. The results indicated that the markers linked to BPH resistance are located at two genomic regions on the long arm of chromosome 3 and the short arm of chromosome 4, respectively. The existence of the two loci was further assessed by the quantitative trait locus (QTL) analysis. They located the two loci at a 3.2 cM interval between G1318 and R1925 on chromosome 3 and a 1.2 cM interval between C820 and S11182 on chromosome 4. Further, Huang et al., (2001) also conducted a molecular marker-based genetic analysis of the BPH resistance in ‘B5’. Insect resistance was evaluated using 250 F3 families from a cross between ‘B5’ and ‘Minghui 63’ based on which the resistance of each F2 plant was inferred. Two bulks were made by mixing, respectively, DNA samples from highly resistant plants and highly susceptible plants selected from the F2 population. The bulks were surveyed for RFLPusing probes representing all 12 chromosomes at regular intervals. The survey revealed two genomic regions on chromosome 3 and chromosome 4 respectively that contained genes for BPH resistance. The existence of the two loci was further assessed by QTL analysis, which resolved these two loci to a 14.3-cM interval on chromosome 3 and a 0.4-cM interval on chromosome 4. This supports the earlier results of Buna et al., (2001) regarding the location of BPH resistance genes in B5. Comparison of the chromosomal locations and reactions to BPH biotypes indicated that these two genes are different from at least nine of the ten previously identified BPH resistance genes. Both of the genes had large effects on BPH resistance and the two loci acted essentially independent of each other in determining the resistance. 

3.3 Rice ‘B5’ is a good source of resistance for WBPH also

In studies on Rice ‘B5’ Tan et al., (2004) employed a mapping population composed of 187 recombinant inbred lines (RILs), produced from a cross between ‘B5’ and susceptible variety ‘Minghui63’, to locate the WBPH and BPH resistance genes. A RFLP survey of the bulked extremes from the RIL population identified two genomic regions, one on chromosome 3 and the other on chromosome 4, likely containing the resistance genes to planthoppers. QTL analysis of the RILs further confirmed that two WBPH resistance genes were mapped on the same loci as Qbp1 and Qbp2, using a linkage map with 242 molecular markers distributed on 12 rice chromosomes. Of the two WBPH resistance genes, one designated Wbph7 (t) was located within a 1.1-cM region between R1925 and G1318 on chromosome 3, the other designated Wbph8 (t) was within a 0.3-cM region flanked by R288 and S11182 on chromosome 4. A two-way analysis of variance showed that two loci acted independently with each other in determining WBPH resistance.

3.4 “DV85” is a new source of BPH resistance

Su et al., (2005) studied an indica rice “DV85” showing resistance to biotype 2 of BPH by bulked seedling test. A recombinant inbred line (RIL) population derived from a cross between susceptible rice “Kinmaze” and “DV85” was phenotyped to map genetic factors conferring BPH resistance in “DV85”. Composite interval mapping revealed that one quantitative trait locus (QTL) with a LOD score of 10.1 was detected between XNpb202 and C1172 on chromosome 11. This QTL was designated as Qbph11. Qbph11 explained 68.4% of the phenotypic variance of BPH resistance in this population. The allele from the resistant parent “DV85” at Qbph11 reduced the damage caused by BPH feeding.

3.5 “AS20-1” with “bph19 (t)” gene exhibits BPH resistance

Chen et al., (2006) performed Genetic analysis and fine mapping of a resistance gene against BPH biotype 2 in rice using two F2 populations derived from two crosses between a resistant indica cultivar (cv.), AS20-1, and two susceptible japonica cultivars., Aichi Asahi and Lijiangxintuanheigu. Insect resistance was evaluated using F1 plants and the two F2 populations. The results showed that a single recessive gene, tentatively designated as bph19 (t), conditioned the resistance in AS20-1. A linkage analysis, mainly employing microsatellite markers, was carried out in the two F2 populations through bulked sergeant analysis and recessive class analysis (RCA), in combination with bioinformatics analysis (BIA). The resistance gene locus bph19(t) was fine mapped to a region of about 1.0 cM on the short arm of chromosome 3, flanked by markers RM6308 and RM3134, where one known marker RM1022, and four new markers, b1, b2, b3 and b4, developed in their study were co-segregating with the locus.

3.6 Bph14 encodes a coiled-coil, nucleotide-binding, and leucine-rich repeat (CC-NB-LRR) protein

Du et al., (2009) cloned Bph14, a gene conferring resistance to BPH at seedling and maturity stages of the rice plant, using a map-based cloning approach. They showed that Bph14 encodes a coiled-coil, nucleotide-binding, and leucine-rich repeat (CC-NB-LRR) protein. Sequence comparison indicates that Bph14 carries a unique LRR domain that might function in recognition of the BPH insect invasion and activating the defense response. Bph14 is predominantly expressed in vascular bundles, the site of BPH feeding. Expression of Bph14 activates the salicylic acid signaling pathway and induces callose deposition in phloem cells and trypsin inhibitor production after planthopper infestation, thus reducing the feeding, growth rate, and longevity of the BPH insects.

3.7 BPH biotypes present in different regions of Asia exhibit varying virulence patterns

Li et al., (2010) studied more than 1200 accessions of common wild rice (Oryza rufipogon Griff.) for the resistance to several biotypes of BPH. Thirty resistant accessions were obtained and 6 of them showed broad spectrum resistance to 5 or all of the 6 BPH biotypes, i.e. biotypes 1 and 2, Bangladesh, Mekong (Vietnam), Cuulong (Vietnam) and Pantnagar (India), which are spreading in most rice growing regions in the world. Genetic analysis has turned out that the BPH resistance in these stocks was controlled by two pairs of recessive genes with duplicate interaction against biotypes 2 and Cuulong biotype, but the resistance to the biotype at Pantnagar was controlled by one pair of recessive gene. This indicated different genetic mechanisms of reaction against BPH biotypes in the resistant sources. The two recessive genes existing in the entry 2183 might be newly discovered genes as no BPH resistance gene has been reported in these chromosome regions. They were tentatively designated as bph18 (t) and bph19 (t), respectively. A total of 143 entries of advanced genetic stocks resistant to BPH and 6promising resistance lines or hybrid combinations with high yield or good quality were bred.

3.8 Bph14 and Bph15 genes could improve resistance levels of MH63 variety

BPH resistance genes Bph14 and Bph15 have been introgressed singly or pyramided into rice variety Minghui 63 (MH63) (Li et al., 2011). The antibiosis and antixenosis effects of these rice lines on BPH and the expression of five P450 genes of BPH regulated by these rice lines were investigated. The resistance level of rice lines harboring resistance genes was improved comparedwithMH63. MH63::14 (carrying Bph14) had negative effects on the development of males, honeydew excretion of females, the female ratio and the copulation rate compared with MH63. MH63::14 also exhibited antixenosis action against BPH nymphs, female adults and oviposition. Besides these negative effects, MH63::15 (carrying Bph15) could also retard the development of females, lower the fecundity and shorten the lifespan of females. The antixenosis action of MH63::15 was stronger than that of MH63::14. When Bph14 and Bph15 were pyramided, antibiosis and antixenosis effects were significantly enhanced relative to single-introgression lines. Among the five P450 genes of BPH, expression of three genes was up regulated, one gene was down regulated and one gene was unchanged by resistant hosts.

3.9 Pyramiding Bph12 and Bph 6 resistance genes resulted in stronger antixenotic and antibiotic effects on BPH

The Bph12 gene in the indica rice accession B14 is derived from the wild species Oryza latifolia. Using an F2 population from a cross between the indica cultivar 93-11 and B14, Qiu et al., (2011) mapped Bph12 gene to a 1.9-cM region on chromosome 4, flanked by the markers RM16459 and RM1305. In this population, BPH12 appeared to be partially dominant and explained 73.8% of the phenotypic variance in BPH resistance. A near-isogenic line (NIL) containing the Bph12 locus in the background of the susceptible japonica variety Nipponbare was developed and crossed with a NIL carrying Bph6 to generate a pyramid line (PYL) with both genes. BPH insects showed significant differences in non-preference in comparisons between the lines harboring resistance genes (NILs and PYL) and Nipponbare. BPH growth and development were inhibited and survival rates were lower on the NIL-Bph12 and NIL-Bph6 plants compared to the recurrent parent Nipponbare. PYL-Bph6 - Bph12 exhibited 46.4, 26.8 and 72.1% reductions in population growth rates (PGR) compared to NIL-Bph12, NIL-Bph6 and Nipponbare, respectively. Furthermore, insect survival rates were the lowest on the PYL-Bph6 - Bph12 plants. These results demonstrated that pyramiding different BPH-resistance genes resulted in stronger antixenotic and antibiotic effects on the BPH insects.

3.10 Cloning Bph27 gene to japonica rice Nipponbare improves BPH resistance

Bph27 gene was derived from an accession of Guangxi wild rice, Oryza rufipogon Griff. (Accession no. 2183, hereafter named GX2183), was primarily mapped to a 17-cM region on the long arm of the chromosome 4. Huang et al., (2012) fine mapped Bph27 using two BC1F2 populations derived from introgression lines of GX2183. Insect resistance was evaluated in the BC1F2 populations with 6,010 individual off-springs, and 346 resistance extremes were obtained and employed for fine mapping of Bph27. High-resolution linkage analysis defined the Bph27 locus to an 86.3-kb region in Nipponbare. Regarding the sequence information of rice cultivars, Nipponbare and 93-11, all predicted open reading frames (ORFs) in the fine-mapping region have been annotated as 11 types of proteins, and three ORFs encode disease-related proteins. Moreover, the average BPH numbers showed significant differences in 96-120 h after release in comparisons between the preliminary near-isogenic lines (pre-NILs, lines harboring resistance genes) and BaiR54. BPH growth and development were inhibited and survival rates were lower in the pre-NIL plants compared with the recurrent parent BaiR54.

3.11 Introgression lines from Oryza minuta showed high resistance to BPH and WBPH

Introgression line population is effectively used in mapping quantitative trait loci (QTLs), identifying favorable genes, discovering hidden genetic variation, evaluating the action or interaction of QTLs in multiple conditions and providing the favorable experimental materials for plant breeding and genetic research. Bin G.S. et al., (2013) utilized, an advanced backcross and consecutive selfing strategy to develop introgression lines (ILs), which were derived from an accession of Oryza minuta (accession No. 101133) with BBCC genome, as the donor, and an elite indica cultivar IR24 (O. sativa), as the recipient. Introgression segments from O. minuta were screened using 164 polymorphic simple sequence repeat (SSR) markers in the genome of each IL. Introgressed segments carried by 131 ILs covered the whole O. sativa genome. The average number of homozygous O. minuta segments per introgression line was about 9.99. The average length of introgressed segments was approximately 14.78 cM, and about 79.64% of these segments had sizes less than 20 cM. In the genome of each introgression line, the O. minuta chromosomal segments harbored chromosomal fragments of O. sativaranging from 1.15% to 27.6%, with an overall average of 8.57%. At each locus, the ratio of substitution of O. minuta alleles had a range of 1.5% to 25.2%, with an average of 8.3%. Based on the evaluation of the phenotype of these ILs, a wide range of alterations in morphological and yield-related traits were found. After inoculation, ILs 11 and 7 showed high resistance to BPH and WBPH respectively.

3.12 Functional markers (FMs) for Bph14 gene are useful in routine genotyping

Functional markers (FMs) designed from polymorphic sites within gene sequences affecting phenotypic variation are highly efficient when used for marker assisted selection (MAS). Bph14 is the first and only cloned insect resistance gene until 2013 in rice. Compared to the sequences of its non-effective alleles there are a number SNP differences. Zhou et al., (2013) adopted the method of allele-specific amplification (ASA) to design a simple, co-dominant, functional marker Bph14P/N for Bph14. Bph14P/N was combined with two specific dominant markers: one, named Bph14P, targets the promoter region of Bph14 and amplifies 566 bp fragments; and the other, Bph14N, targets the LRR region of bph14 and amplifies 345 bp fragments. Specificity and applicability of the functional marker system were verified in two breeding populations and a Chinese mini core collection of Oryza sativa. This simple, low-cost marker system can be used in routine genotyping for Bph14 in breeding populations.

3.13 Molecular mechanism of the resistance gene Bph15

The BPH-resistance gene Bph15 has been proved to be effective in controlling the pest and widely applied in rice breeding programs. Nevertheless, molecular mechanism of the resistance remains unclear. Lv et al., (2014) narrowed down the position of BPH15 on chromosome 4 and investigated the transcriptome of BPH15 rice after BPH attacked. They analyzed 13,000 BC2F2 plants of cross between susceptible rice TN1 and the recombinant inbred line RI93 that carrying the BPH15 gene from original resistant donor B5. Bph15 was mapped to a 0.026 9 cM region on chromosome 4, which is 210-kb in the reference genome of Nipponbare. Sequencing bacterial artificial chromosome (BAC) clones that span the Bph15 region revealed that the physical size of Bph15 region in resistant rice B5 is 580-kb, much bigger than the corresponding region in the reference genome of Nipponbare. There were 87 predicted genes in the Bph15 region in resistant rice. The expression profiles of predicted genes were analyzed. Four jacalin-related lectin proteins genes and one LRR protein gene were found constitutively expressed in resistant parent and considered the candidate genes of Bph15. The transcriptomes of resistant Bph15 introgression line and the susceptible recipient line were analyzed using high-throughput RNA sequencing. In total, 2,914 differentially expressed genes (DEGs) were identified. BPH-responsive transcript profiles were distinct between resistant and susceptible plants and between the early stage (6 h after infestation, HAI) and late stage (48 HAI). The key defense mechanism was related to jasmonate signaling, ethylene signaling, receptor kinase, MAPK cascades, Ca2+ signaling, PR genes, transcription factors, and protein posttranslational modifications.

3.14 Introgression of a dominant BPH resistance gene Bph27(t) to japonica and indica varieties

Liu, (2016) introgressed a dominant BPH resistance gene Bph27(t) into a susceptible commercial japonica variety Ningjing3 (NJ3) and indica variety 93-11 using marker-assisted selection (MAS). Further, Bph27(t) and a durable BPH resistance gene Bph3 were pyramided by intercrossing single-gene introgressed lines through MAS. The introgression of BPH resistance genes significantly improved the BPH resistance and reduced the yield loss caused by BPH.

3.15 A novel BPH resistance gene Bph32 was identified from PTB33 in China

Ren et al., (2016) were successful in cloning a novel BPH resistance gene, LOC_Os06g03240 (MSU LOCUS ID), from the rice variety Ptb33. The gene was designated as Bph32. This gene was cloned in an approximately 190-kb interval flanked by the markers RM19291 and RM8072 on the short arm of chromosome 6 using bioinformatics analysis and a transgenic approach. The evaluation of BPH resistance in transgenic plants confirmed the crucial function of Bph32 in BPH resistance. Bph32 encodes a short consensus repeat (SCR) domain-containing protein that confers an antibiosis resistance to BPH and is localized in the plasma membrane of the cell. This gene is highly expressed in the leaf sheaths, where the BPH first settles and feeds. Bph32 is a stable BPH resistance gene and provides for rice defense against BPH.

4 Korea

The major emphasis of host plant resistance research in Korea was to transfer already available resistance alleles from indica background to japonica varieties. The following are the main institutes involved in research on this aspect.

1)      Kyung Hee University, Yongin 446-701, Korea

2)      Kyungpook National University, Daegu 702-701, Korea

3)      National Institute of Agricultural Biotechnology, Suwon 441-707, Korea

4)      National Institute of Crop Science, Cheolwon 269-814, Korea

5)      National Institute of Crop Science, RDA, Suwon 441-857, Korea

6)      Seoul National University, Seoul 151-921, Korea

7)      Sunchon National University, Sunchon 540-742, Korea

8)      Yeongnam Agricultural Research Institute, Milyang 627-803, Korea

4.1 Characterization of BPH resistance in Samgangbyeo through near-isogenic rice lines (NILs)

Park et al., (2007) generated 132 BC5F5 near-isogenic rice lines (NILs) by five backcrosses of Samgangbyeo, a BPH resistant indica variety carrying the Bph1 locus, with Nagdongbyeo, a BPH susceptible japonica variety. To identify genes that confer BPH resistance representational difference analysis (RDA) was employed to detect transcripts that were exclusively expressed in one of our BPH resistant NIL, SNBC61, during insect feeding. The chromosomal mapping of the RDA clones that were subsequently isolated revealed that they are located in close proximity either to known quantitative trait loci or to an introgressed SSR marker from the BPH resistant donor parent Samgangbyeo. Genomic DNA gel-blot analysis further revealed that loci of all RDA clones in SNBC61 correspond to the alleles of Samgangbyeo. Most of the RDA clones were found to be exclusively expressed in SNBC61 and could be assigned to functional groups involved in plant defense.

4.2 Fine mapping of Bph1 locus to facilitate marker aided selection

Cha et al., (2008) fine mapped the chromosomal region containing the Bph1 locus, which enabled them to perform marker-aided selection (MAS). They used 273 F8 recombinant inbred lines (RILs) derived from a cross between Cheongcheongbyeo, an indica type variety harboring Bph1 from Mudgo, and Hwayeongbyeo, a BPH susceptible japonica variety. By random amplification of polymorphic DNA (RAPD) analysis using 656 random 10-mer primers, three RAPD markers (OPH09, OPA10 and OPA15) linked to Bph1were identified and converted to SCAR (sequence characterized amplified region) markers. These markers were found to be contained in two BAC clones derived from chromosome 12: OPH09 on OSJNBa0011B18, and both OPA10 and OPA15 on OSJNBa0040E10. By sequence analysis of ten additional BAC clones evenly distributed between OSJNBa0011B18 and OSJNBa0040E10, they developed 15 STS markers. Of these, pBPH4and pBPH14 flanked Bph1at distances of 0.2 cM and 0.8 cM, respectively. The STS markers pBPH9, pBPH19 pBPH20 and pBPH21 co-segregated with Bph1. These markers were shown to be very useful for marker-assisted selection (MAS) in breeding populations of 32 F6 RILs from a cross between Andabyeo and IR71190, and 32 F5 RILs from a cross between Andabyeo and Suwon452.

4.3 Molecular marker-based transfer of BPH resistance to japonica variety, ‘Junambyeo’

Rahman et al., (2009) conducted molecular marker-based genetic analysis of BPH resistance using an F2 population derived from a cross between an introgression line, ‘IR71033-121-15’, from Oryza minuta (Accession number 101141) and a susceptible Korean japonica variety, ‘Junambyeo’. Resistance to BPH (biotype 1) was evaluated using 190 F3 families. Two major quantitative trait loci (QTLs) and two significant digenic epistatic interactions between marker intervals were identified for BPH resistance. One QTL was mapped to 193.4-kb region located on the short arm of chromosome 4, and the other QTL was mapped to a 194.0-kb region on the long arm of chromosome 12. The two QTLs additively increased the resistance to BPH. Markers co-segregating with the two resistance QTLs were developed at each locus. Comparing the physical map positions of the two QTLs with previously reported BPH resistance genes, they conclude that these major QTLs are new BPH resistance loci and have been designated as Bph20(t) on chromosome 4 and Bph21(t) on chromosome 12.

5 India

The main program on BPH resistance in India was to identify suitable markers for BPH resistance from Rathu Heenati and three wild rices Oryza officinalis, Oryza glaberrima and Oryza minuta. Main organizations which were involved in this work are:

1.       Tamil Nadu Agricultural University, Coimbatore 641 003, India

2.       Directorate of Rice Research, Rajendra nagar(ICAR- Indian Institute of Rice Research), Hyderabad-500030, India

3.       Dantiwada Agricultural University, Dantiwada, Banaskantha, Gujarat, India

4.       Anand Agricultural University, Anand, Gujarat, India

5.       Punjab Agricultural University, Ludhiana-141004, Punjab, India

5.1 Marker-assisted selection (MAS) for Bph13 (t) gene

Renganayaki et al., (2002) developed Recombinant inbred lines (RILs) from a cross between ‘IR50’ and ‘IR54745-2-21-12-17-6’ which were used to identify random amplified polymorphic DNA (RAPD) markers closely linked to a BPH Biotype-4 resistance gene [Bph13 (t)] derived from Oryza officinalis Wall. Bulked segregant analysis (BSA) using RAPD primers identified 11 polymorphic fragments. Six fragments, AJ09₂₆₀a, AL05₂₂₀a, AK10₆₉₀a, AK10₄₃₀c, AK10₃₈₀d, and AJ01₂₀₀a, were linked in coupling phase to the Bph13 (t) locus. The remaining five fragments, AJ09 ₂₃₀b, AJ09₁₈₀c, AJ09₁₀₀d, AL05₄₀₀b, and AK10₃₄₀e, were linked in repulsion. The most closely linked RAPD marker, AJ09₂₃₀b, was converted to a codominant linked sequence tagged sites (STS) marker. This marker mapped 1.3 cM from the resistance gene and was placed on rice chromosome 3 by means of ‘IR64 x Azucena’ doubled haploid (DH) population. The tightly linked STS marker could be used for marker-assisted selection (MAS).

5.2 BPH resistance gene introgressed from O. glaberrima is new and tentatively designated as Bph 22(t)

The repeated screening over the years at the Indian Institute of Rice Research, Hyderabad, India, recorded consistent resistance in Rathu Heenati (Bph3 & Bph17), Swarnalatha (Bph 6) and ADR 52 (bph20(t) & Bph21(t)). While other donors Mudgo (Bph1), IR 56 (Bph3), Pokkali (Bph9), IR 65482-4-136-2-2 (Bph10), IR 65482-7-216-1-2 (Bph18) showed either susceptible or moderate resistance. Ram et al., (2009) screened two introgression lines (IR 75870-5-8-5-B-1-B and IR 75870-5-8-5-B-2-B) derived from the cross IR64 x O. glaberrima (TOG 5674) and two introgression lines (IR 71033-62- 15 and IR 71033-121-15) derived from the cross IR 31917-45-3-2 x O. minuta (Acc. 101141) generated at IRRI, Philippines. The two introgression lines derived from O. glaberrima and the parent O. glaberrima (TOG 5674) showed resistance reaction over the years in replicated screening, the other two introgression lines (IR 71033-62-15 and IR 71033-121-15) derived from O. minuta also showed resistance reaction in repeated screening, while its recurrent parent IR 31917-45- 3-2 showed susceptible reaction, suggesting that the gene for BPH resistance in both the lines introgressed from O. minuta. The dominant gene for BPH resistance in IR 75870-5-8-5-B-1-B and IR 75870-5-8-5-B-2-B introgressed from O. glaberrima is new and tentatively designated as Bph 22(t).

5.3 OPA08-7 is identified as RAPD marker for WBPH resistance

Parihar et al., (2010) attempted to identify RAPD (Random Amplified Polymorphic DNA) marker for WBPH resistant gene by utilizing Gurjari (WBPH resistant), Jaya (WBPH susceptible) and their F2 progeny. The RAPD analysis was done group wise as well as combined for the bulk segregant analysis (BSA). For the BSA, of the total 50 random primers surveyed, a single linked primer, OPA 08, was identified. This primer generated 8-bands, one of which, OPA08-7, was putatively linked to resistant gene as was evident by its presence in almost all the resistant bulks and vice-versa. This band had molecular weight equal to 1,219.38 bp and was found in resistant parent, Gurjari, and in almost all the resistant bulks (the four susceptible bulks revealed absence of the same band) indicating the band OPA08-7 as a marker for WBPH resistance among the screened rice genotypes.

5.4 Maker assisted selection (MAS) for BPH resistance from Rathu Heenati

A Sri Lankan indica rice cultivar Rathu Heenati was found to be resistant to all biotypes of BPH. Kumari et al., (2010) studied a total of 268 F7 RILs of IR50 and Rathu Heenati by phenotyping for their level of resistance against BPH by the standard seed-box screening test (SSST) in the greenhouse. A total of 53 SSR primers mapped on the chromosome 3were used to screen the polymorphism between the parents IR50 and Rathu Heenati, out of which eleven were found to be polymorphic between IR50 and Rathu Heenati. The eleven primers that have shown polymorphism between the IR50 and Rathu Heenati parents were genotyped in a set of five resistant RILs and five susceptible RILs along with the parents for co-segregation analysis. Among the eleven primers, two primers namely RM3180 (18.22 Mb) and RM2453 (20.19 Mb) showed complete co-segregation with resistance. The identification of SSR markers linked with BPH resistance could be used for the maker assisted selection (MAS) program in rice breeding.

5.5 New sources of resistance from O. nivara and O. punctata

Based on the two years screening, seven accessions of O. nivara (AA), one accession of O. officinalis (CC), seven accessions of O. australiensis (EE), five accessions of O. punctata (BB and BBCC) and nine accessions of O. latifolia (CCDD) were confirmed to be resistant to BPH out of 1989 entries screened. So far no BPH resistance genes have been identified and designated from O. nivara and O. punctate. Hence these may act as new sources of resistance (Sarao et al., 2016).

Of late research on host-plant resistance to BPH has been intensified.

5.6 Rice gene bph5 in ARC10550 conferring resistance to BPH was proved to be combined action of three QTLs

A team at IIRR (DRR) Hyderabad led by Dr T. Ram, Head Plant-breeding utilized the cross Taichung Native 1/ARC10550 (population of 255 F2:3families) to map BPH resistance with 106 polymorphic SSR markers (Deen et al., 2017). The inheritance pattern of different traits suggested that the resistance inARC10550 is controlled by quantitative traits instead of a single recessive gene as reported earlier by Khush et al. (1985). The quantitative trait loci (QTLs) for BPH resistance were analyzed for nine phenotypic traits. QTL analysis has revealed that five major loci were associated with resistance, one for damage score (qBphDs6) on chromosome 6, two for nymphal preference at 48 and 72 h (qBphNp(48h)-1and qBphNp(72h)-12) on chromosome 1 and 12 and two for days to wilt (qBphDw(30)-3and qBphDw(30)-8) on chromosome 3 and 8 explaining the phenotypic variance of 24.23, 8.69, 7.66, 4.55 and 10.48% respectively. Thus, this work has thrown a new light on the contribution of different mechanisms of BPH resistance like antixenosis/ nonpreference, antibiosis and tolerance. The two major QTLs, qBphDs6 for damage score and qBphDw8 for days to wilt are important for further investigations and use in breeding program.

5.7 BPH resistance gene in cultivar CR2711–76 from NRRI, Cuttack exhibiting broad-spectrum resistance to Philippines and Indian BPH populations was designated as Bph31

Studies by Prahalada et al., (2017) revealed that the cultivar CR2711–76 developed at the National Rice Research Institute (NRRI), Cuttack, India, possessed stable and broad-spectrum resistance to several BPH populations of the Philippines and BPH of India. Genetic analysis and fine mapping confirmed the presence of a single dominant gene, BPH31, in CR2711–76. The BPH31 gene was located on the long arm of chromosome 3 within an interval of 475 kb between the markers PA26 and RM2334. BPH31 gene in CR2711–76 exhibited three different mechanisms of resistance: antibiosis, antixenosis, and tolerance. The effectiveness of flanking markers was tested in a segregating population and the InDel type markers PA26 and RM2334 showed high co-segregation with the resistance phenotype. Foreground and background analysis by tightly linked markers as well as using the Infinium 6 K SNP chip respectively were applied for transferring the BPH31 gene into an indica variety, Jaya. The improved BPH31-derived Jaya lines showed strong resistance to BPH biotypes of India and the Philippines. The new BPH31 gene can be used in BPH resistance breeding programs on the Indian subcontinent. The tightly linked DNA markers identified in the study have proved their effectiveness and can be utilized in BPH resistance breeding in rice.

5.8 Identification of a new gene Bph33(t) in rice line RP2068-18-3-5

Another team at Hyderabad led by Dr J.S. Bentur used TN1 × RP2068 cross and identified new R gene [Bph33(t)] using advanced generation RILs and through phenotyping at two locations and linkage analysis with 99 polymorphic SSR markers (Bhaskar et al.,2018). QTL analysis identified at least two major QTLs on chromosome 1 influencing seedling damage score in seed box screening, honey dew excretion by adults and nymphal survival. Since no BPH R gene has been reported on chromosome 1so far, this new locus accounting for over 20% of phenotypic variance has been designated as a new gene Bph33(t).

5.9 A new locus Bph34 in Oryza sativa L. X Oryza nivara was identified

A team of scientists led by Dr. D.S.Brar former Head of Plant Breeding at IRRI presently working at Punjab Agricultural University, Ludhiana, identified through high-resolution mapping a novel genetic locus for resistance to BPH, designated as Bph34 on long arm of rice chromosome 4. The locus was mapped using an interspecific F2 population derived from a cross between susceptible indica cultivar PR122 and BPH-resistant wild species, O. nivara acc. IRGC104646. Inheritance studies performed using F2 and F2:3 populations revealed the presence of single dominant gene. Construction of high-density linkage map using 50 K SNP chip (OsSNPnks) followed by QTL mapping identified single major locus at 28.8 LOD score between SNP markers, AX-95952039 and AX-95921548. Bph34 explained 68.3% of total phenotypic variance. Bph34 locus is 91 Kb in size on Nipponbare reference genome-IRGSP-1.0 and contains 11 candidate genes. In addition to associated SNP markers, two SSR markers, RM16994 and RM17007, also co-segregated with the Bph34 which can be used efficiently for markers assisted transfer into elite rice cultivars. 

6 Thailand

Thailand is a major exporter of rice to U.S., Middle-East and some European Countries. High quality Jasmine rice variety which is preferred for export is ‘Khao Dawk Mali 105’ (KDML105). After BPH became a problem in 1970s onwards the major objective of rice breeding program in Thailand was to incorporate BPH resistance to the background of KDML105. Jirapong Jairin and Apichart Vanavichit are the scientists working in Ubon Ratchathani Rice Research Center, Ubon Ratchathani, who contributed substantially in the research related to BPH resistance in Thailand.

6.1 Transferring BPH resistance genes to KDML105 grain quality back ground

First, they have studied the BPH resistance genes in an indica cultivar ‘Abhaya’ using 400 BC4F2 and F3 backcross introgressed lines of KDML105 derived from a cross between Abhaya and KDML105. The BC4F2 plants were used for DNA analysis. Two local BPH populations collected from central and northeastern Thailand were used to evaluate the BPH resistance in the 400 BC4F3. Through bulked segregant analysis, four AFLP fragments were co-segregated with the BPH resistance. Linkage analysis revealed that these fragments were localized on rice chromosomes 6, 10 and 12. These map locations were in the same genomic regions where major BPH resistance genes or quantitative resistance loci are present (Jairin et al., 2005). While continuing the studies on the same subject, Jairin et al., (2009) attempted to combine KDML105 essential grain quality traits with BPH resistance from the donor cultivar, ‘Rathu Heenati’. The linkage drags between Bph3 and Wxa alleles was successfully broken by phenotypic and marker-assisted selections. All introgression lines (ILs) developed in this study showed a broad-spectrum resistance against BPH populations in Thailand and had KDML105 grain quality standards. Finally, this study has revealed that the ILs can be directly developed into BPH resistant varieties or can be used as genetic resources of BPH resistance to improve rice varieties with the Wxb allele in rice breeding programs.

6.2 Localization and fine mapping of the Bph3 gene and the allelic relationship between Bph3 and bph4

In another study, Jairin et al., (2007a) collected 45 BPH populations in Thailand and performed a cluster analysis that revealed the existence of four groups corresponding to the variation of virulence against BPH resistance genes in Rice cultivars Rathu Heenati and PTB33. These two varieties carrying Bph3 gene, showed a broad-spectrum resistance against all BPH populations. They further attempted to identify chromosomal location of Bph3 in the rice genome by performing simple sequence repeat (SSR) analysis to identify and localize the Bph3 gene. For mapping of the Bph3 locus, they developed two backcross populations, BC1F2 and BC3F2, from crosses of PTB33 x RD6 and Rathu Heenati x KDML105, respectively, and evaluated these for BPH resistance. Thirty-six polymorphic SSR markers on chromosomes 4, 6 and 10 were used to survey 15 resistant (R) and 15 susceptible (S) individuals from the backcross populations. One SSR marker, RM190, on chromosome 6 was associated with resistance and susceptibility in both backcross populations. Additional SSR markers surrounding the RM190 locus were also examined to define the location of Bph3. Based on the linkage analysis of 208 BC1F2 and 333 BC3F2 individuals; they were able to map the Bph3 locus between two flanking SSR markers, RM589 and RM588, on the short arm of chromosome 6 within 0.9 and 1.4 cM, respectively. Thus, they confirmed both the location of Bph3 and the allelic relationship between Bph3 and bph4 on chromosome 6. They suggested that these tightly linked SSR markers can facilitate marker-assisted gene pyramiding and provide the basis for map-based cloning of the resistant gene. Further, they have also performed a similar study with IR71033-121-15 × KDML105, and arrived at the same conclusion regarding location of Bph3 gene on the short arm of chromosome 6. The tightly linked markers RM589 and RM586 could explain 28.2% to 59.8%, of the phenotypic variance of the BPH resistance from the BC1F2, and BC3F2 populations Jairin et al., (2007b; 2010) continued their studies to detect the bph4 locus with the help of 15 polymorphic simple sequence repeat (SSR) markers covering genetic distance of 0.0–63.4 cM on chromosome 6. Fifteen BPH resistant (R) and susceptible (S) individuals were used from each of the 95 and 78 F2 populations derived from crosses of TN1/Babawee and Babawee/KDML105, respectively. One SSR marker, RM586, was associated with the R and S from the F2 populations. Additional markers surrounding the RM586 locus were examined to define the location of bph4. From the genetic linkage map and QTL analysis, the bph4 locus was mapped at the same chromosomal region of Bph3 between two flanking markers RM589 and RM586 which could explain 58.8-70.1% of the phenotypic variations and can be used for marker-assisted selection in BPH-resistant breeding programs.

6.3 Analysis of rice genetics for BPH resistance

Jena and Kim (2010) summarized existing the position of rice genes that confer resistance to BPH as follows: “Of the 21 resistance genes, 18 genes have been localized on specific region of six rice chromosomes using molecular genetic analysis and genomics tools. Some of these resistance genes are clustered together such as Bph1, bph2, Bph9, Bph10, Bph18, and Bph21 on the long arm of chromosome 12; Bph12, Bph15, Bph17 and Bph20 on the short arm of chromosome 4; bph11 and Bph14 on the long arm of chromosome 3 and Bph13(t) and bph19 on the short arm of chromosome 3. Six genes (Bph11, bph11, Bph12, bph12, Bph13 and Bph13) originated from wild Oryza species have either duplicate chromosome locations or wrong nomenclature”.

During the latter period some more, genes have been added to the existing list of genes and some modifications have also been suggested. Ram et al., (2009) identified a new gene from O. glaberrima and tentatively designated as Bph 22(t). Bph23 and Bph24 have been identified from Oryza minuta and Oryza rufipogon to be resistant to South East Asian BPH biotype (Cheng et al., 2013). Tamura et al., (2014) identified two BPH resistance genes, Bph26 and Bph25 from the indica rice cultivar ADR52. Map-based cloning of Bph26 revealed that Bph26 encodes a coiled-coil-nucleotide-binding-site- leucine-rich repeat (CC-NBS-LRR) protein. Bph26 mediated sucking inhibition in the phloem sieve element. Bph26 was identical to Bph2. Bph27 gene derived from an accession of Guangxi wild rice, Oryza rufipogon (Accession no. 2183) was primarily mapped to a 17-cM region on the long arm of the chromosome 4 (Huang et al., 2012). The resistance gene in DV85 has been named as Bph28 (t) (Wu et al., 2014) The resistance gene in RBPH54 derived from O. rufipogon (Wang et al., 2015) has been named as bph29. Hu et al., (2016) reviewed and summarized the whole information available on BPH resistance. Thus, up to the year 2016, 29 major BPH resistance genes have been identified from Indica cultivars and wild rice species, and more than ten genes have been fine mapped to chromosome regions of less than 200 kb. Four genes (Bph14, Bph26, Bph17 and bph29) have been cloned. Several BPH resistant introgression lines (ILs), near-isogenic lines (NILs) and pyramided lines (PYLs) carrying single or multiple resistance genes were developed by marker assisted backcross breeding (MABC). Later on, Bph31, Bph32, Bph33, Bph34 have been added as already described (Prahalada et al., 2017; Ren et al., 2016; Bhaskar et al., 2018; Kishor et al., 2018 respectively).

But the major difficulty in numbering and naming of BPH resistance genes is the existence of different biotypes and characterization of those biotypes. As the position stands today there is broad agreement that three geographically isolated biotypes 1) South-Asian Biotype existing in Indian Sub-continent consisting of India, Sri Lanka, Pakistan and Bangladesh 2) East Asian Biotype existing in China, Japan and Korea 3) South-East Asian Biotype occurring in Thailand, Myanmar, Vietnam, Philippines, Indonesia and Malaysia and northern parts of Australia. Among the total 34 genes so far characterized the reaction of all the genes to all the biotypes is not available. Further existence of QTLs; along with some major genes render the variety moderately resistant and thus confusing the whole situation. The physiological capability of BPH to overcome the resistance barrier imposed by varieties is also complicating the situation. Therefore, the best approach can be to sort out the allelic relationships in the “Six genes (Bph11, bph11, Bph12, bph12, Bph13 and Bph13) originating from wild Oryza species and having either duplicate chromosome locations or wrong nomenclature” as suggested by Jena and Kim (2010). Further there can be an International Committee preferably under the auspices of IRRI to sort out the differences in naming and stream lining the whole information. Any further naming of BPH genes that will be identified in future should be done by that particular committee only. Otherwise the whole issue leads to confusion if everyone starts naming and numbering in his or her own way.

7 Summary and Conclusions                                                          

v  The major theme of genetics and breeding of rice for BPH resistance has been to identify suitable donors from germplasm and catalog the genes and transfer the same to the background of locally adapted varieties. 

v  The genetic sources in the beginning were Oryza sativa cultivars while during later periods the emphasis was to utilize wild rices of genus Oryza.

v  The program was originally initiated at IRRI and later all national programs took active part in collaboration with IRRI and also on their own.

v  The wild species of genus Oryza used so far in different countries are Oryza rufipogon (AA genome), O. officinalis (CC genome), Oryza eichingeri (CC genome), O. minuta (BBCC genome), O. latifolia (CCDD genome), O. australiensis (EE genome), O. punctata (BB and BBCC) and O. granulate (GG genome).

v  At IRRI several varieties with BPH resistance like IR42, IR56, IR60, IR62, IR68, IR72, and IR74 were released for general cultivation first in Philippines and later in other countries. 

v  BPH resistance genes Bph10 and Bph18 from Oryza australiensis were successfully transferred to elite Indica and Japonica varieties with the help of RFLP markers. 

v  Entomology research at IRRI has focused on genetic stability of BPH resistant varieties released from IRRI.

v  In Japan the major emphasis was to characterize Bph1 and bph2 genes and transfer the same to japonica background of “Tsukushibare”.

v  Characterization and fine mapping of bph4 rice gene in Japonica background has also been undertaken.

v  New genes bph20 (t) and Bph21 (t) have been characterized in relation to BPH populations collected in different periods in Japan.

v  Bph26 and Bph25 genes have been characterized. Bph26 was found to be identical to Bph2 on the basis of DNA sequence analysis. Therefore reutilization of Bph2 gene along with Bph25 has been suggested.

v  In China Oryza eichingeri with CC genome is hybridized with O.sativa and a new gene, tentatively named Bph13 (t) was mapped to chromosome 2.

v  In BPH resistant line B5, resistant genes have been located in chromosomes 3 and 4. Rice ‘B5’ was found to be a good source of resistance for WBPH also.

v  “DV85” an Indica variety has been detected as new source of BPH resistance and attempts were made to transfer the gene to japonica back ground. In another Indica variety “AS20-1” BPH resistance gene was tentatively named as “bph19 (t)”.

v  In China, Bph14 has been observed to encode a coiled-coil, nucleotide-binding, and leucine-rich repeat (CC-NB-LRR) protein.

v  Chinese scientists have observed that BPH biotypes present in different regions of Asia exhibit varying virulence patterns.

v  Resistance genes from wild rice Oryza rufipogon Griff have been tentatively designated as bph18 (t) and bph19 (t).

v  Bph14 and Bph15 genes when pyramided could improve resistance levels of MH63variety.

v  Pyramiding Bph12 and Bph 6 resistance genes resulted in stronger antixenotic and antibiotic effects on BPH. Cloning Bph27 gene to japonica rice Nipponbare improved BPH resistance. Introgression lines from Oryza minutashowed high resistance to both BPH and WBPH.

v  In China, Functional markers (FMs) for Bph14 gene are useful in routine genotyping. Molecular characterization of Bph15 region revealed 87 predicted genes in resistant rice.

v  In China, Bph23 and Bph24 have been identified from Oryza minuta and Oryza rufipogon to be resistant South East Asian BPH biotype. Dominant BPH resistance gene Bph27(t) has been introgressed to japonica and indica varieties.

v  A novel BPH resistance gene Bph32 was identified from PTB33 in China. This gene was cloned in an approximately 190-kb interval flanked by the markers RM19291 and RM8072 on the short arm of chromosome 6 using bioinformatics analysis and a transgenic approach.

v  In Korea, scientists characterized BPH resistance in Samgangbyeo through near-isogenic rice lines (NILs). They have fine mapped Bph1 locus to facilitate marker aided selection. Scientists in Korea have also executed Molecular marker-based transfer of BPH resistance to japonica variety, ‘Junambyeo’.

v  In India, Recombinant inbred lines (RILs) from a cross between ‘IR50’ and ‘IR54745-2-21-12-17-6’ which were used to identify random amplified polymorphic DNA (RAPD) markers closely linked to a BPH Biotype-4 resistance gene Bph13 (t) derived from Oryza officinalis.

v  Indian scientists introgressed BPH resistance gene from O. glaberrima which is new and tentatively designated as Bph 22(t). OPA08-7 is identified as RAPD marker for WBPH resistance.

v  In India, maker assisted selection (MAS) was employed for transfer of BPH resistance from Rathu Heenati to IR50.

v  In Punjab India, seven accessions of O. nivara (AA) and five accessions of O. punctata (BB and BBCC) have been identified as new sources of resistance to BPH.

v  Rice gene bph5 in ARC10550 conferring resistance to BPH was proved to be combined action of three QTLs. The cross Taichung Native 1/ARC10550 (population of 255 F2:3families) was utilized to map BPH resistance with 106 polymorphic SSR markers.

v  In India, BPH resistance gene in cultivar CR2711–76 from NRRI, Cuttack exhibiting broad-spectrum resistance to Philippines and Indian BPH populations was designated as Bph31.

v  At Hyderabad, India, TN1 × RP2068 cross was used to identify new R gene Bph33(t) using advanced generation RILs and through phenotyping at two locations and linkage analysis with 99 polymorphic SSR markers.

v  A new locus Bph34 in Oryza sativa L. X Oryza nivara was identified at PAU, Ludhiana under the supervision of Dr. D.S. Brar.

v  In Thailand, BPH resistance genes have been successfully transferred to back ground of KDML105 the high quality Jasmine rice variety which is preferred for export. Localization and fine mapping of the Bph3 gene and the allelic relationship between Bph3 and bph4 has been resolved.

v  Apart from 21 genes reported by Jena and Kim (2010) some additional genes like Bph 22(t) from O. glaberrima, Bph23 from Oryza minuta and Bph24 from Oryza rufipogon were identified to be resistant to South East Asian BPH biotype. Bph25 and Bph26 from the indica rice cultivar ADR52; Bph27 gene derived from Oryza rufipogon have also been added. Further Bph26 was found to be identical to Bph2 identified earlier. The resistance gene in DV85 has been named as Bph28 (t). The resistance gene in RBPH54 derived from O. rufipogon has been named as bph29. Later on Bph31, Bph32, Bph33, Bph34 have been added. Thus there is need to continue research on location of new genes and ways of their utilization. 

v  Now the genome of rice plant and genome of BPH have been sequenced, with more and more molecular and biochemical techniques available, it should be possible to assign molecular roles of these genes to broaden our understanding and better utilization in evolving resistant varieties for BPH.

v  There can be an International Committee preferably under the auspices of IRRI to sort out the differences in naming and stream lining the whole information. Any further naming of BPH genes that will be identified in future can be done by that particular committee only. Otherwise the whole issue may become confusing if everyone starts naming and numbering BPH resistance genes in his or her own way.

Acknowledgements

The author is grateful to his friends and colleagues in the Divisions of Entomology, Plant-breeding And Biotechnology of Indian Institute of Rice Research, Hyderabad, India for encouragement. The author is also thankful to all the authors of original research papers whose information is utilized for writing of this article.

References

Athwal D.S., Pathak M.D., Bacalangco E.H., and Pura C.D., 1971, Genetics of resistance to brown planthopper and green leafhoppers in Oryza sativa L. Crop Science, 11: 747-750
https://doi.org/10.2135/cropsci1971.0011183X001100050043x

Bhaskar S. N., Divya D., Sahu N., Sundaram R., Preetinder S.S., Kuldeep Singh, Jhansi Lakshmi V., Bentur J.S., 2018, A new gene Bph33(t) conferring resistance to brown planthopper (BPH), Nilaparvata lugens (Stål) in rice line RP2068-18-3-5, Euphytica 214(3), DOI: 10.1007/s10681-018-2131-5
https://doi.org/10.1007/s10681-018-2131-5

Bin G. S., Yu W., Qiong L. X., Qiang L. K., Kuan H. F., Hong C. C., and Qing G. G., 2013, Development and Identification of Introgression Lines from Cross of Oryza sativa and Oryza minuta, Rice Science, 20(2): 95-102
https://doi.org/10.1016/S1672-6308(13)60111-0

Brar D.S. and Khush G.S., 1997, Alien introgression in rice, Plant Molecular Biology, 35: 35-47
https://doi.org/10.1007/978-94-011-5794-0_4
PMid:9291958

Brar, D.S., Virk P.S., Jena K.K. and Khush G.S., 2009, Breeding for resistance to planthoppers in rice, In Heong K.L., Hardy B. (editors), 2009, Planthoppers: new threats to the sustainability of intensive rice production systems in Asia, Los Baños (Philippines), International Rice Research Institute, pp.460

Buna W., Zhen H., Lihui S., Xiang R., Xianghua L., and Guangcun H., 2001, Mapping of two new brown planthopper resistance genes from wild rice, Chinese Science Bulletin, 46(1): 1092-1095
https://doi.org/10.1007/BF02900685

Cha Y.S., Ji H., Yun D.W., Ahn B.O., Lee M.C., Suh S.C., Lee C.S., Ahn E.K., Jeon Y.H., Jin I.D., Sohn J.K., Koh H.J., and Eun M.Y., 2008, Fine Mapping of the Rice Bph1 Gene, which Confers Resistance to the Brown Planthopper (Nilaparvata lugens Stal), and Development of STS Markers for Marker-assisted Selection, Molecules and Cells, 26: 146-151

Chen J.W., Wang L., Pang X.F., and Pan Q.H., 2006, Genetic analysis and fine mapping of a rice brown planthopper (Nilaparvata lugens Stal) resistance gene bph19 (t), Molecular Genetics and Genomics, 275: 321-329
https://doi.org/10.1007/s00438-005-0088-2
PMid:16395578

Cheng X., Zhu L. and He G., 2013, Towards Understanding of Molecular Interactions between Rice and the Brown Planthopper, Molecular Plant, 6(3): 621-634
https://doi.org/10.1093/mp/sst030
PMid:23396040

Cohen M.B., Alam S.N., Medina E.B., and Bernal C.C., 1997, Brown planthopper, Nilaparvata lugens, resistance in rice cultivar IR64: mechanism and role in successful N. lugensmanagement in Central Luzon, Philippines, Entomologia Experimentalis et Applicata, 85: 221-229
https://doi.org/10.1046/j.1570-7458.1997.00252.x

Cruz A.P., Arida A., Heong K.L., and Horgan F.G., 2011, Aspects of brown planthopper adaptation to resistant rice varieties with the Bph3 gene, Entomologia Experimentalis et Applicata, 141: 245-257
https://doi.org/10.1111/j.1570-7458.2011.01193.x

Deen R., Ramesh K., Padmavathi G., Viraktamath B.C. and Ram T., 2017, Mapping of brown planthopper [Nilaparvata lugens (Stal)] resistance gene (bph5) in rice (Oryza sativa L.), Euphytica 213: 35
https://doi.org/10.1007/s10681-016-1786-z

Du B., Zhang W., Liu B., Hu J., Wei Z., Shi Z., He R., Zhu L., Chen R., Han B., and He G., 2009, Identification and characterization of Bph14, a gene conferring resistance to brown planthopper in rice, Proceedings of the National Academy of Sciences of the United States, 106(52): 22163-22168
https://doi.org/10.1073/pnas.0912139106
PMid:20018701 PMCid:PMC2793316

Guoqing L., Huihuang Y., Qiang F., Qian Q., Zhitao Z., Wenxue Z., and Lihuang Z., 2001, Mapping of a new gene for brown planthopper resistance in cultivated rice introgressed from Oryza eichingeri, Chinese Science Bulletin, 46(17): 1459-1462
https://doi.org/10.1007/BF03187031

Hirabayashi H., and Ogawa T., 1995, RFLP Mapping of Bph-1 (Brown Planthopper Resistance Gene) in Rice, Breeding Science, 45: 369-371
https://doi.org/10.1270/jsbbs1951.45.369

Hu J., Xiao C., and He Y., 2016, Recent progress on the genetics and molecular breeding of brown planthopper resistance in rice, Rice, 9(30): 1-12
https://doi.org/10.1186/s12284-016-0099-0
PMid:27300326 PMCid:PMC4908088

Huang D., Qiu Y., Zhang Y., Huang F., Meng J., Wei S., Li R., and Chen B., 2012, Fine mapping and characterization of BPH27, a brown planthopper resistance gene from wild rice (Oryza rufipogon Griff.), Theoretical and Applied Genetics, DOI 10.1007/s00122-012-1975-7
https://doi.org/10.1007/s00122-012-1975-7
PMid:23001338 

Huang N., Parco A., Mew T., Magpantay G., McCouch S., Guiderdoni E., Xu J., Subudhi P., Angeles E.R., and Khush G.S., 1997, RFLP mapping of isozymes, RAPD and QTLs for grain shape, brown planthopper resistance in a doubled haploid rice population, Molecular Breeding, 3: 105-113
https://doi.org/10.1023/A:1009683603862

Huang Z., He G., Shu L., Li X., and Zhang Q., 2001, Identification and mapping of two brown planthopper resistance genes in rice, Theoretical and Applied Genetics, 102: 929-934
https://doi.org/10.1007/s001220000455

Ishii T., Brar D.S., Multandi S., and Khush G.S., 1993, Molecular tagging of genes for brown planthopper resistance and earliness introgressed from Oryza australiensis into cultivated rice, O. sativa, Genome, 37: 217-221
https://doi.org/10.1139/g94-030
PMid:18470071

Jairin J., Phengrat K., Teangdeerith S., Vanavichit A., Toojinda T., 2007a, Mapping of a broad-spectrum brown planthopper resistance gene, Bph3, on rice chromosome 6, Molecular Breeding, 19: 35-44
https://doi.org/10.1007/s11032-006-9040-3

Jairin J., Sansen K., Wongboon W., and Kothcharerk J., 2010, Detection of a brown planthopper resistance gene bph4 at the same chromosomal position of Bph3 using two different genetic backgrounds of rice, Breeding Science, 60: 71-75
https://doi.org/10.1270/jsbbs.60.71

Jairin J., Teangdeerith S., Leelagud P., Kothcharerk J., Sansen K., Yi M., Vanavichit A., Toojinda T., 2009, Development of rice introgression lines with brown planthopper resistance and KDML105 grain quality characteristics through marker-assisted selection, Field Crops Research, 110: 263-271
https://doi.org/10.1016/j.fcr.2008.09.009

Jairin J., Teangdeerith S., Leelagud P., Phengrat K., Vanavichit A., and Toojinda T., 2007b, Detection of brown planthopper resistance genes from different rice mapping populations in the same genomic location, ScienceAsia, 33: 347-352
https://doi.org/10.2306/scienceasia1513-1874.1998.33.347

Jairin J., Toojinda T., Tragoonrung S., Tayapat S., and Vanavichit A., 2005, Multiple genes determining brown planthopper (Nilaparvata lugens Stal) Resistance in Backcross Introgressed Lines of Thai Jasmine Rice 'KDML105', Science Asia 31: 129-135
https://doi.org/10.2306/scienceasia1513-1874.2005.31.129

Jena K. K. and Mackill D. J., 2008, Molecular markers and their use in marker-assisted selection in rice, Crop Science, 48: 1266-1276
https://doi.org/10.2135/cropsci2008.02.0082

Jena K. K., and Kim S. M., 2010, Current status of brown planthopper (BPH) resistance and genetics, Rice, 3: 161-171
https://doi.org/10.1007/s12284-010-9050-y

Jena K. K., Jeung J. U., Lee J. H., Choi H. C., and Brar D. S., 2006, High-resolution mapping of a new brown planthopper (BPH) resistance gene, Bph18(t), and marker-assisted selection for BPH resistance in rice (Oryza sativa L.), Theoretical and Applied Genetics, 112: 288-297
https://doi.org/10.1007/s00122-005-0127-8
PMid:16240104 

Jena K.K., Khush G.S., and Kochert G., 1992, RFLP analysis of rice (Oryza sativa L.) introgression lines, Theoretical and Applied Genetics, 84: 608-616
https://doi.org/10.1007/BF00224159
PMid:24201348

Ji H., Kim S.R., Kim Y.H., Suh J.P., Park H.M., Sreenivasulu N., Misra G., Kim S.M., Hechanova S.L., Kim H., Lee G.S., Yoon U.H., Kim T.H., Lim H., Suh S.C., Yang J., An J., Jena K.K., 2016, Map-based cloning and characterization of the Bph18 gene from wild rice conferring resistance to brown planthopper (BPH) insect pest, Sci Rep, 6: 34376
https://doi.org/10.1038/srep36688
PMid:27834403 PMCid:PMC5105200

Kawaguchi M., Murata K., Ishii T., Takumi S., Mori N., and Nakamura C., 2001, Assignment of a brown planthopper (Nilaparvata lugens Stal) resistance gene bph4 to the rice Chromosome 6, Breeding Science, 51: 13-18
https://doi.org/10.1270/jsbbs.51.13

Khush G.S., 1971, Rice breeding for disease and insect resistance at IRRI, Oryza, 8: 111-119

Khush G.S., 1977, Breeding for resistance in rice. New York Academy of Sciences, 287: 296-308
https://doi.org/10.1111/j.1749-6632.1977.tb34248.x

Kishor K., Preetinder S. S., Bhatia D., Neelam K., Amanpreet Kaur, Mangat G. S., Brar D. S. and Kuldeep Singh, 2018 High-resolution genetic mapping of a novel brown planthopper resistance locus, Bph34 in Oryza sativa L. X Oryza nivara (Sharma & Shastry) derived interspecific F2 population, Theoretical and Applied Genetics 131(5): 1163-1171
https://doi.org/10.1007/s00122-018-3069-7
PMid:29476225 

Kumari S., Sheba J. M., Marappan M., Ponnuswamy S., Seetharaman S., Pothi N., Subbarayalu M., Muthurajan R., and Natesan S., 2010, Screening of IR50 X Rathu Heenati F7 RILs and Identification of SSR Markers Linked to Brown Planthopper (Nilaparvata lugens Stal) Resistance in Rice (Oryza sativa L.), Molecular Biotechnology, 46:63-71 DOI 10.1007/s12033-010-9279-0
https://doi.org/10.1007/s12033-010-9279-0
PMid:20396978

Lang N.T., Brar D., Khush G.S., Huang N. and Buu B.C., 1999, Development of STS markers to indentify brown planthopper resistance in a segregating population, omonrice,7: 27-38

Lang N.T., and Buu B.C., 2003, Genetic and physical maps of gene Bph-10 controlling brown plant hopper resistance in rice (Oryza sativa L.), Omonrice, 11: 35-41

Li J., Chen Q., Wang L., Liu J., Shang K., and Hua H., 2011, Biological effects of rice harbouring Bph14 and Bph15 on brown planthopper, Nilaparvata lugens, Pest Management Science, 67: 528-534

https://doi.org/10.1002/ps.2089
PMid:21254325

Li R., Li L., Wei S., Wei Y., Chen Y., Bai D., Yang L., Huang F., Lu W., Zhang X., Li X., Yang X., Wei Y., 2010, The Evaluation and Utilization of New Genes for Brown Planthopper Resistance in Common Wild Rice (Oryza rufipogon Griff.), Molecular Entomology, 1(1): 1-7

Liu Y., Chen L., Liu Y., Dai H., He J., Kang H., Pan G., Huang J., Qiu Z., Wang Q., Hu J., Liu L., Chen Y., Cheng X., Jiang L., and Wan J., 2016, Marker assisted pyramiding of two brown planthopper resistance genes, Bph3 and Bph27 (t), into elite rice Cultivars, Rice, 9: 27

https://doi.org/10.1186/s12284-016-0096-3
PMid:27246014 PMCid:PMC4887400

Liu Y.Q., Wu H., Chen H., Liu Y.L., He J., Kang H.Y., Sun Z.G., Pan G., Wang Q., Hu J.L., Zhou F., Zhou K.N., Zheng X.M., Ren Y.L., Chen L.M., Wang Y.H., Zhao Z.G., Lin Q.B., Wu F.Q., Zhang X., Guo X.P., Cheng X.N., Jiang L., Wu C.Y., Wang H.Y., Wan J.M. , 2015, A gene cluster encoding lectin receptor kinases confers broad spectrum and durable insect resistance in rice. Nat Biotechnol., 33: 301-305

https://doi.org/10.1038/nbt.3069
PMid:25485617 

Lv W., Du B., Shangguan X., Zhao Y., Pan Y., Zhu L., He Y. and He G., 2014, BAC and RNA sequencing reveal the brown planthopper resistance gene BPH15 in a recombination cold spot that mediates a unique defense mechanism, BMC Genomics, 15: 674

https://doi.org/10.1186/1471-2164-15-674
PMid:25109872 PMCid:PMC4148935

Murai H., Hashimoto Z., Sharma P.N., Shimizu T., Murata K., Takumi S., Mori N., Kawasaki S., and Nakamura C., 2001, Construction of a high-resolution linkage map of a rice brown planthopper (Nilaparvata lugens Stål) resistance gene bph2, Theoretical and Applied Genetics, 103: 526-532

https://doi.org/10.1007/s001220100598

Murata K., Fujiwara M., Kaneda C., Takumi S., Mori N., and Nakamura C.,1998, RFLP mapping of a brown planthopper (Nilaparvata lugens Stål) resistance gene bph2 of indica rice introgressed into a japonica breeding line ‘Norin-PL4’, Genes & Genetic Systems, 73: 359-364 

https://doi.org/10.1266/ggs.73.359

Myint K.K.M., Matsumura M., Takagi M., and Yasui H., 2009, Demographic Parameters of Long–term Laboratory Strains of the Brown Planthopper, Nilaparvata lugens Stål, (Homoptera: Delphacidae) on Resistance Genes, bph20 (t) and Bph21 (t) in Rice, Journal- Faculty of Agriculture Kyushu University, 54 (1): 159–164

Parihar A., Pathak A. R. and Parihar P., 2010, Identification of RAPD marker for the White Backed Plant Hopper (WBPH) resistant gene in rice, African Journal of Biotechnology, 9(10): 1423-1426

https://doi.org/10.5897/AJB09.1741

Park D.S., Lee S.K., Lee J.H., Song M.Y., Song S.Y., Kwak D.Y., Yeo U.S., Jeon N. S., Park S.K., Yi G., Song Y. C., Nam M.H., Ku Y.C., Jeon J.S., 2007, The identification of candidate rice genes that confer resistance to the brown planthopper (Nilaparvata lugens) through representational difference analysis, Theoretical and Applied Genetics, 115: 537-547

https://doi.org/10.1007/s00122-007-0587-0
PMid:17585380

Pathak M.D., Cheng C.H., and Furtono M.E., 1969, Resistance to Nephotettix cincticeps and Nilaparvata lugens in varieties of rice, Nature, 223: 502-504

https://doi.org/10.1038/223502a0

Prahalada G.D., Shivakumar N., Lohithaswa H.C., Sidde Gowda D.K., Ramkumar G., Sung R.K., Ramachandra C., Shailaja H., Mohapatra T. and Jena K.K., 2017, Identification and fine mapping of a new gene, BPH31 conferring resistance to brown planthopper biotype 4 of India to improve rice, Oryza sativa L., Rice, 10: 41

https://doi.org/10.1186/s12284-017-0178-x
PMid:28861736 PMCid:PMC5578944

Qiu Y., Guo J., Jing S., Zhu L., He G., 2011, Development and characterization of japonica rice lines carrying the brown planthopper-resistance genes BPH12 and BPH6, Theoretical and Applied Genetics, DOI 10.1007/s00122-011-1722-5

https://doi.org/10.1007/s00122-011-1722-5
PMid:22038433

Rahman M. L., Jiang W., Chu S. H., Qiao Y., Ham T. H., Woo M. O., Lee J., Khanam M. S., Chin J. H., Jeung J. U., Brar D. S., Jena K. K., Koh H. J., 2009, High-resolution mapping of two rice brown planthopper resistance genes, Bph20 (t) and Bph21(t), originating from Oryza minuta, Theoretical and Applied Genetics

https://doi.org/10.1007/s00122-009-1125-z
PMid:19669727

Ram T., Deen R., Gautam S.K., Ramesh K., Rao Y.K., and Brar D.S., 2009, Identification of new genes for Brown Planthopper resistance in rice introgressed from O. glaberrima and O. minuta, Rice Genetics Newsletter, 25: 67- 68

Ren J, Gao F, Wu X, Zeng L, Lv J, Su X, Luo H, Ren G., 2016, BPH32, a novel gene encoding an unknown SCR domain-containing protein, confers resistance against the brown planthopper in rice, Sci Rep., 6: 37645

https://doi.org/10.1038/srep37645
PMid:27876888 PMCid:PMC5120289

Ren X., Weng Q., Zhu L., and He G., 2004, Dynamic mapping of quantitative trait loci for brown planthopper resistance in rice, Cereal Research Communications, 32(1): 31-38 

Renganayaki K., Fritz A. K., Sadasivam S., Pammi S., Harrington S. E., McCouch S. R., Mohan Kumar S., and Reddy A. S., 2002., Mapping and Progress toward Map-Based Cloning of Brown Planthopper Biotype-4 Resistance Gene Introgressed from Oryza officinalis into Cultivated Rice, O. sativa, Crop Science. 42: 2112-2117

https://doi.org/10.2135/cropsci2002.2112

Sarao P. S., Sahi G. K., Neelam K., Mangat G. S., Patra B.C., and Singh K., 2016, Donors for Resistance to Brown Planthopper Nilaparvata lugens (Stål) from Wild Rice Species, Rice Science, 23(4): 219-224

https://doi.org/10.1016/j.rsci.2016.06.005

Sharma P.N., Ketipearachchi Y., Murata K., Torii A., Takumi S., Mori N., and Nakamura C., 2002, RFLP/AFLP mapping of a brown planthopper (Nilaparvata lugens Stål) resistance gene Bph1 in rice, Euphytica 129: 109-117

https://doi.org/10.1023/A:1021514829783

Su C. C., Wan J., Zhai H. Q., WangC. M., Sun L. H., Yasui H., and Yoshimura A., 2005, A new locus for resistance to brown planthopper identified in the indica rice variety DV85, Plant Breeding,124: 93-95

https://doi.org/10.1111/j.1439-0523.2004.01011.x

Su C.C., Cheng X.N., Zhai H.Q., Wan J.M., 2002, Detection and analysis of QTL for resistance to the brown planthopper, Nilaparvata lugens (Stal), in rice (Oryza sativa L.), using backcross inbred lines, Acta Genetica Sinica, 29(4):332-338

Suh J. P., Yang S. J., Jeung J. U., Pamplona A., Kim J. J., Lee J. H., Hong H. C., Yang C. I., Kim Y. G., Jena K. K., 2011, Development of elite breeding lines conferring Bph18 gene-derived resistance to brown planthopper (BPH) by marker-assisted selection and genome-wide background analysis in japonica rice (Oryza sativa L.), Field Crops Research, 120: 215-222

https://doi.org/10.1016/j.fcr.2010.10.004

Tamura, Y. Hattori M., Yoshioka H., Yoshioka M., Takahashi A., Wu J., Sentoku N., and Yasui H., 2014, Map-based Cloning and Characterization of a Brown Planthopper Resistance Gene BPH26 from Oryza sativa L. ssp. indica Cultivar ADR52, Scientific Reports, 4: 5872

https://doi.org/10.1038/srep05872
PMid:25076167 PMCid:PMC5376202

Tan G.X., Weng Q.M., Ren X., Huang Z., Zhu L.L., and He G.C., 2004, Two whitebacked planthopper resistance genes in rice share the same loci with those for brown planthopper resistance, Heredity, 92: 212-217

https://doi.org/10.1038/sj.hdy.6800398
PMid:14666132 

Wang Y., Cao L.M., Zhang Y.X. et al ,2015, Map-based cloning and characterization of BPH29, a B3 domain-containing recessive gene conferring brown planthopper resistance in rice, Journal of Experimental Botany, 66: 6035-6045

https://doi.org/10.1093/jxb/erv318
PMid:26136269 PMCid:PMC4566989

Wu H., Liu Y.Q., He J. et al, 2014, Fine mapping of brown planthopper (Nilaparvata lugens Stål) resistance gene Bph28(t) in rice (Oryza sativa L.), Molecular Breeding 33: 909-918

https://doi.org/10.1007/s11032-013-0005-z

Zhao Y., Huang J., Wang Z., Jing S., Wang Y., Ouyang Y., Cai B., Xin X.F., Liu X., Zhang C., Pan Y., Ma R., Li Q., Jiang W., Zeng Y., Shangguan X., Wang H., Du B., Zhu L., Xu X., Feng Y.Q., He S.Y., Chen R., Zhang Q., He G., 2016, Allelic diversity in an NLR gene BPH9 enables rice to combat planthopper variation. PNAS 113(45): 12850-12855

https://doi.org/10.1073/pnas.1614862113
PMid:27791169 PMCid:PMC5111712

Zhou L., Chen Z., Lang X., Du B., Liu K., Yang G., Hu G., Li S., He G., and You A., 2013, Development and validation of a PCR-based functional marker system for the brown planthopper resistance gene Bph14 in rice, Breeding Science 63: 347-352

https://doi.org/10.1270/jsbbs.63.347
PMid:24273431 PMCid:PMC3770563