Single-feature polymorphism mapping of isogenic rice lines identifies the influence of terpene synthase on brown planthopper feeding preferences
© Kamolsukyunyong et al.; licensee Springer. 2013
Received: 28 February 2013
Accepted: 1 July 2013
Published: 2 August 2013
Bph3, a major brown planthopper (BPH) resistance locus derived from the rice cultivar Rathu Heenati (RH), has been used as a stable donor of traits that improve highly susceptible aromatic rice varieties in Thailand. Map-based cloning was initiated using a set of isogenic lines (ILs) harboring the major Bph3 locus on chromosome 6. IL genomes were scanned with a 57 K Affymetrix Rice GeneChip to identify the gene responsible for Bph3.
Single-feature polymorphism (SFP) mapping was used to localize 84 candidate genes. An expression analysis of 15 selected candidate genes in the aromatic rice cultivar KDML105 (KD) and the ILs under normal conditions revealed two differentially expressed sequences. Following hopper feeding, only one candidate gene, Os04g27430, was differentially expressed. Os04g27430 encodes a putative sesquiterpene synthase (STPS) gene that was induced by BPH feeding in ILs. An antixenosis test in three selected ILs revealed a major role for STPS in insect preference during the first 120 hours of the rice-insect interaction. Functional SNPs in exon 5 that resulted in the deletion of seven amino acids in the susceptible rice line were identified. Moreover, three additional SNPs associated with three transcription binding sites were also identified, which might explain the differential response of Os04g27430 during the anti-feeding test.
Os04g27430 is the second known rice STPS induced by BPH. The gene may involve an antixenosis BPH resistance mechanism. The combination of the STPS and the Bph3 locus was more effective than Bph3 alone in the tested ILs.
KeywordsBrown planthopper Single-feature polymorphism (SFP) Sesquiterpene synthase (STPS) Antixenosis on feeding preference (AFP)
Microarray-based genome mapping identification of additional genes correlated with brown planthopper (BPH) resistance in rice
Qbph4, Bph17, and Bph20(t) were mapped to the intervals RM335 – RM401 and RM8213 – RM5953 and with the linked marker RM5953, respectively. The Qbph4 region encompassed a position from 689,354 to 13,163,724 bp, and Bph17 encompassed 4,360,621 to 9,388,937 bp on pseudomolecule 4 (Os-Nipponbare-Reference-IRGSP-1.0). A total of 36 SFP-containing genes (Os04g03050 – Os04g22280) were located in the Qbph4 region (Figure 1B). Nineteen of these genes (Os04g08800 – Os04g16878) were also specifically associated with the Bph17 region. The Qbph2 and Bph15 genes were mapped in the same region by the RFLP markers C820-R288 and C820-S11182. The region located between 6,902,846 and 9,349,627 bp on pseudomolecule 4 contained eight SFP-containing genes (Os04g13050 – Os04g16878). The linked marker of Bph12(t), RM261, was adjacent to Os04g11780, the resistance protein LR10, with a physical distance of 130.5 kb. Moreover, another NBS-LRR resistance-related protein, Os04g25900, also contained an SFP.
Compared to the expression analysis of BPH-infested RH studied by Wang et al. (2012), three BPH resistance-related genes, two putative resistance proteins, Os04g11780 (LR10) and Os04g14220 (RPM1), and an F-box-containing protein, Os04g11660, were found to contain SFP (Figure 1B and Additional file 2: Table S1) in the present study. In contrast, no candidate BPH resistance gene on chromosome 3, 6, and 10 identified in the study by Wang et al. (2012) was found to contain an SFP in our study. This difference may be due to the different BPH-susceptible rice cultivars, KD and Taichung native 1 (TN1), used for the RH comparison in the two studies.
The SFP-containing genes were classified into various functional groups, as shown in Figure 1C. The largest group contained genes with unknown functions such as expressed proteins, hypothetical proteins, and uncharacterized proteins (Additional file 3: Table S2). Transposons and retrotransposons formed the second largest group. The most significant finding was the identification of 10 genes that encode metabolic enzymes in the third most abundant group, which included three genes encoding terpene synthases (TPS). These enzymes are involved in the biosynthesis of secondary metabolites known as terpenoids, a large group of volatile compounds involved in defense mechanisms against plant herbivores (Schnee et al. 2006 Yuan et al. 2008). The fourth most abundant group included seven R gene-like sequences on chromosomes 3, 4, 8, and 10. These findings suggest that several minor quantitative trait loci (QTLs) may strengthen BPH 3 in terms of stable BPH resistance in RH and ILs. The last three groups contained genes involved in protein phosphorylation processes, transcription factors, and transporters.
Expression analysis of SFP-containing genes
Genomic characterization of Os04g27430
Another STPS gene (Os08g07100) that is reportedly induced by BPH (Cho et al. 2005) was not polymorphic between KD and IL308 at the expression level in the present study (Figure 7A). This gene was induced by BPH feeding in both rice strains. Moreover, the gene was induced by BPH feeding and by the fall army worm (Yuan et al. 2008), suggesting that the gene plays a common role in the response to herbivore attacks on rice plants.
Os04g27430 is likely the STPS that functions as zingiberene synthase, which catalyzes the formation of a number of sesquiterpene products (Iijima et al. 2004). Sesquiterpene volatile compounds are the potential products of this gene and may play a role in BPH resistance mechanisms in RH and ILs.
Allelic variation in TPS genes leading to a volatile compound composition difference has been reported in maize (Köllner et al. 2004). In rice, several rice varieties have been shown to release different volatile blends (Lou et al. 2006); however, the gene(s) that controls these differences has not yet been identified. In our preliminary study, a total of 25 sesquiterpenes were identified by GC-MS in the mixture of volatile compounds emitted by KD and RH rice plants infested by BPH. The major sesquiterpene product that KD emitted at a significantly lower level than RH is E-β-farnesene (data not shown), the common constituent of the aphid alarm pheromone (Bowers et al. 1972 Edwards et al. 1973 Pickett and Griffiths. 1980) and the aphid repellent of wild potato (Gibson and Pickett. 1983). This variation may be due to a defect in the KD allele of Os04g27430 at both the genomic and the protein sequence levels.
Os04g27430 may play a more important role than Bph3 in the antixenosis mechanism
This study clearly demonstrates that the Bph3 critical region and at least 84 other genes have been transferred to ILs. This unexpected finding may be a consequence of the phenotypic selection process used in the breeding program before the implementation of marker-assisted selection. These genes may play a complementary role to BPH 3 in the BPH resistance mechanisms of IL rice plants. In this study, Os04g27430 was identified as a BPH feeding-inducible STPS that may be involved in the BPH resistance mechanism of RH. This gene may contribute in the antixenosis mechanism by interfering with BPH settling.
KD, Khao Dowk Mali 105
Single feature polymorphism
Single nucleotide polymorphism
This work was supported by the National Center for Genetic Engineering and Biotechnology (BIOTEC) (Grant No. P0010270) and the Agriculture Research Development Agency (ARDA) (Grant No P12/2552). WK thanks the Ministry of Science and Technology, Thailand, for financially supporting his Ph.D. studies.
- Bowers WS, Webb RE, Nault LR, Dutky SR: Aphid alarm pheromone: Isolation, identification, synthesis. Science 1972, 177: 1121–1122. 10.1126/science.177.4054.1121View ArticlePubMedGoogle Scholar
- Cheng AX, Xiang CY, Li JX, Yang CQ, Hu WL, Wang LJ, Lou YG, Chen XY: The rice (E)-β-caryophyllene synthase (OsTPS3) accounts for the major inducible volatile sesquiterpenes. Phytochemistry 2007, 68: 1632–1641. 10.1016/j.phytochem.2007.04.008View ArticlePubMedGoogle Scholar
- Cho SK, Jung KW, Jeung JU, Kang KH, Shim KS, You MK, Yoo KS, Ok SH, Shin JS: Analysis of differentially expressed transcripts from planthopper-infested wild rice (Oryza minuta ). Plant Cell Rep 2005, 24: 59–67. 10.1007/s00299-004-0905-9View ArticlePubMedGoogle Scholar
- Edwards LJ, Siddall JB, Dunham LL, Uden P, Kislow CJ: Trans-β-farnesene, alarm pheromone of green peach aphid, Myzus persicae (Sulzer). Nature 1973, 241: 126–127.View ArticleGoogle Scholar
- Gibson RW, Pickett JA: Wild potato repels aphids by release of aphid alarm pheromone. Nature 1983, 302: 608–609. 10.1038/302608a0View ArticleGoogle Scholar
- Huang N, He G, Shu L, Li X, Zhang Q: Identification and mapping of two brown planthopper genes in rice. Theor Appl Genet 2001, 102: 929–934. 10.1007/s001220000455View ArticleGoogle Scholar
- Iijima Y, Davidovich-Rikanati R, Fridman E, Gang DR, Bar E, Lewinsohn E, Pichersky E: The biochemical and molecular basis for the divergent patterns in the biosynthesis of terpenes and phenylpropenes in the peltate glands of three cultivars of basil. Plant Physiol 2004, 136: 3724–3736. 10.1104/pp.104.051318PubMed CentralView ArticlePubMedGoogle Scholar
- Jairin J, Teangdeerith S, Leelagud P, Phengrat K, Vanavichit A, Toojinda T: Physical mapping of Bph3, a brown planthopper resistance locus in rice. Mj Int J Sci Tech 2007, 1: 166–177.Google Scholar
- Jairin J, Teangdeerith S, Leelagud P, Kothcharerk J, Sansen K, Yi M, Vanavichit A, Toojinda T: Development of rice introgression lines with brown planthopper resistance and KDML105 grain quality characteristics through marker-assisted selection. Field Crop Res 2009, 110: 263–271. 10.1016/j.fcr.2008.09.009View ArticleGoogle Scholar
- Köllner T, Schnee C, Gershenzon J, Degenhardt J: The variability of sesquiterpenes emitted from two Zea mays cultivars is controlled by allelic variation of two terpene synthase genes encoding stereoselective multiple product enzymes. Plant Cell 2004, 16: 1115–1131. 10.1105/tpc.019877PubMed CentralView ArticlePubMedGoogle Scholar
- Kumar R, Qiu J, Joshi T, Valliyodan B, Xu D, Nguyen HT: Single feature polymorphism discovery in rice. PLoS One 2007, 2: e284. 10.1371/journal.pone.0000284PubMed CentralView ArticlePubMedGoogle Scholar
- Liu Y, Su C, Jiang L, He J, Wu H, Peng C, Wan J: The distribution and identification of brown planthopper resistance genes in rice. Hereditas 2009, 146: 67–73. 10.1111/j.1601-5223.2009.02088.xView ArticlePubMedGoogle Scholar
- Lou Y, Hua X, Turlings TCJ, Cheng J, Chen X, Ye G: Differences in induced volatile emission among rice varieties result in differential attraction and parasitism of Nilaparvata lugens eggs by the parasitoid Anagrus nilaparvatae in the field. J Chem Ecol 2006, 32: 2375–2387. 10.1007/s10886-006-9151-7View ArticlePubMedGoogle Scholar
- Pickett JA, Griffiths DC: Composition of aphid alarm pheromones. J Chem Ecol 1980, 6: 349–360. 10.1007/BF01402913View ArticleGoogle Scholar
- Prisic S, Xu MM, Wilderman PR, Peters RJ: Rice contains two disparate ent-copalyl diphosphate synthases with distinct metabolic functions. Plant Physiol 2004, 136: 4228–4236. 10.1104/pp.104.050567PubMed CentralView ArticlePubMedGoogle Scholar
- Rahman ML, Jiang W, Chu SH, Qiao Y, Ham TH, Woo MO, Lee J, Khanam MS, Chin JH, Jeung JU, Brar DS, Jena KK, Koh HJ: High-resolution mapping of two rice brown planthopper resistance genes, Bph20(t) and Bph21(t), originating from Oryza minuta. Theor Appl Genet 2009, 119: 1237–1246. 10.1007/s00122-009-1125-zView ArticlePubMedGoogle Scholar
- Sakamoto T, Miura K, Itoh H, Tatsumi T, Ueguchi-Tanaka M, Ishiyama K, Kobayashi M, Agrawal GK, Takeda S, Abe K: An overview of gibberellin metabolism enzyme genes and their related mutants in rice. Plant Physiol 2004, 134: 1642–1653. 10.1104/pp.103.033696PubMed CentralView ArticlePubMedGoogle Scholar
- Schnee C, Köllner TG, Held M, Turlings TCL, Gershenzon J, Degenhardt J: The product of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores. Proc Natl Acad Sci USA 2006, 103: 1129–1134. 10.1073/pnas.0508027103PubMed CentralView ArticlePubMedGoogle Scholar
- Sun L, Su C, Wang C, Zhai H, Wan J: Mapping of a major resistance gene to the brown planthopper in the rice cultivar Rathu Heenati. Breeding Sci 2005, 55: 391–396. 10.1270/jsbbs.55.391View ArticleGoogle Scholar
- Thongjuea S, Ruanjaichon V, Bruskiewich R, Vanavichit A: RiceGeneThresher: a web-based application for mining genes underlying QTL in rice genome. Nucl Acids Res 2009, 37: D996-D1000. 10.1093/nar/gkn638PubMed CentralView ArticlePubMedGoogle Scholar
- Wang Y, Li H, Si Y, Zhang H, Guo H, Miao X: Microarray analysis of broad-spectrum resistance derived from an indica cultivars Rathu heenati. Planta 2012, 235: 829–840. 10.1007/s00425-011-1546-1View ArticlePubMedGoogle Scholar
- Xu M, Hillwig ML, Prisic S, Coates RM, Peters RJ: Functional identification of rice syn-copalyl diphosphate synthase and its role in initiating biosynthesis of diterpenoid phytoalexin/allelopathic natural products. Plant J 2004, 39: 309–318. 10.1111/j.1365-313X.2004.02137.xView ArticlePubMedGoogle Scholar
- Yang HY, Ren X, Weng QM, Zhu LL, He GC: Molecular mapping and genetic analysis of a rice brown planthopper (Nilarparvata lugen Stål) resistance gene. Hereditas 2002, 136: 39–43. 10.1034/j.1601-5223.2002.1360106.xView ArticlePubMedGoogle Scholar
- Yang H, You A, Yang Z, Zhang F, He R, Zu L, He G: High resolution genetic mapping at the Bph15 locus for brown planthopper resistance in rice (Oryza sativa L.). Theor Appl Genet 2004, 110: 182–191. 10.1007/s00122-004-1844-0View ArticlePubMedGoogle Scholar
- Yuan JS, Killner TG, Wiggins G, Grant J, Degenhardt J, Chen F: Molecular and genomic basis of volatile-mediated indirect defense against insect in rice. Plant J 2008, 55: 491–503. 10.1111/j.1365-313X.2008.03524.xView ArticlePubMedGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.