Identifying mutations in sd1, Pi54 and Pi-ta, and positively selected genes of TN1, the first semidwarf rice in Green Revolution

Botanical Studies - Tập 63 - Trang 1-21 - 2022
Jerome P. Panibe1,2,3, Long Wang4, Yi-Chen Lee3, Chang-Sheng Wang5,6, Wen-Hsiung Li1,3,7
1Institute of Molecular and Cellular Biology, National Tsing Hua University, Hsinchu, Taiwan
2Bioinformatics Program, Taiwan International Graduate Program, Institute of Information Science, Academia Sinica, Taipei, Taiwan
3Biodiversity Research Center, Academia Sinica, Taipei, Taiwan
4State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University, Nanjing, China
5Department of Agronomy, National Chung Hsing University, Taichung, Taiwan
6Advanced Plant Biotechnology Center, National Chung Hsing University, Taichung, Taiwan
7Department of Ecology and Evolution, University of Chicago, Chicago, USA

Tóm tắt

Taichung Native 1 (TN1) is the first semidwarf rice cultivar that initiated the Green Revolution. As TN1 is a direct descendant of the Dee-geo-woo-gen cultivar, the source of the sd1 semidwarf gene, the sd1 gene can be defined through TN1. Also, TN1 is susceptible to the blast disease and is described as being drought-tolerant. However, genes related to these characteristics of TN1 are unknown. Our aim was to identify and characterize TN1 genes related to these traits. Aligning the sd1 of TN1 to Nipponbare sd1, we found a 382-bp deletion including a frameshift mutation. Sanger sequencing validated this deleted region in sd1, and we proposed a model of the sd1 gene that corrects errors in the literature. We also predicted the blast disease resistant (R) genes of TN1. Orthologues of the R genes in Tetep, a well-known resistant cultivar that is commonly used as a donor for breeding new blast resistant cultivars, were then sought in TN1, and if they were present, we looked for mutations. The absence of Pi54, a well-known R gene, in TN1 partially explains why TN1 is more susceptible to blast than Tetep. We also scanned the TN1 genome using the PosiGene software and identified 11 genes deemed to have undergone positive selection. Some of them are associated with drought-resistance and stress response. We have redefined the deletion of the sd1 gene in TN1, a direct descendant of the Dee-geo-woo-gen cultivar, and have corrected some literature errors. Moreover, we have identified blast resistant genes and positively selected genes, including genes that characterize TN1’s blast susceptibility and abiotic stress response. These new findings increase the potential of using TN1 to breed new rice cultivars.

Tài liệu tham khảo

Amador V, Monte E, Garcı́a-Martı́nez J-L, Prat S (2001) Gibberellins signal nuclear import of PHOR1, a photoperiod-responsive protein with homology to Drosophila armadillo. Cell 106:343–354. https://doi.org/10.1016/s0092-8674(01)00445-7 Bailey TL, Gribskov M (1998) Combining evidence using p-values: application to sequence homology searches. Bioinformatics 14:48–54. https://doi.org/10.1093/bioinformatics/14.1.48 Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202–W208. https://doi.org/10.1093/nar/gkp335 Barman SR, Gowda M, Venu RC, Chattoo BB (2004) Identification of a major blast resistance gene in the rice cultivar ‘Tetep.’ Plant Breed 123:300–302. https://doi.org/10.1111/j.1439-0523.2004.00982.x Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170 Bushnell B (2021) BBMap. https://sourceforge.net/projects/bbmap/. Accessed 4 Feb 2021 Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL (2009) BLAST+: architecture and applications. BMC Bioinformatics 10:421. https://doi.org/10.1186/1471-2105-10-421 Chandler RF Jr (1992) An adventure in applied science: a history of the International Rice Research Institute. International Rice Research Institute, Los Baños, pp 51–116 Chen X, Jia Y, Wu BM (2019) Evaluation of rice responses to the blast fungus Magnaporthe oryzae at different growth stages. Plant Dis 103:132–136. https://doi.org/10.1094/PDIS-12-17-1873-RE Cheng X, Wu Y, Guo J, Du B, Chen R, Zhu L, He G (2013) A rice lectin receptor-like kinase that is involved in innate immune responses also contributes to seed germination. Plant J 76:687–698. https://doi.org/10.1111/tpj.12328 Cingolani P, Platts A, Wang LL, Coon M, Nguyen T, Wang L, Land SJ, Lu X, Ruden DM (2012) A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 6:80–92. https://doi.org/10.4161/fly.19695 Coates JC, Laplaze L, Haseloff J (2006) Armadillo-related proteins promote lateral root development in Arabidopsis. Proc Natl Acad Sci USA 103:1621–1626. https://doi.org/10.1073/pnas.0507575103 Dievart A, Perin C, Hirsch J, Bettembourg M, Lanau N, Artus F, Bureau C, Noel N, Droc G, Peyramard M, Pereira S, Courtois B, Morel J-B, Guiderdoni E (2016) The phenome analysis of mutant alleles in leucine-rich repeat receptor-like kinase genes in rice reveals new potential targets for stress tolerant cereals. Plant Sci 242:240–249. https://doi.org/10.1016/j.plantsci.2015.06.019 Eddy SR (1998) Profile hidden Markov models. Bioinformatics 14:755–763. https://doi.org/10.1093/bioinformatics/14.9.755 El-Gebali S, Mistry J, Bateman A, Eddy SR, Luciani A, Potter SC, Qureshi M, Richardson LJ, Salazar GA, Smart A, Sonnhammer ELL, Hirsh L, Paladin L, Piovesan D, Tosatto SCE, Finn RD (2018) The Pfam protein families database in 2019. Nucleic Acids Res 47:D427–D432. https://doi.org/10.1093/nar/gky995 Emms DM, Kelly S (2019) OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol 20:238. https://doi.org/10.1186/s13059-019-1832-y Fukuoka S, Saka N, Mizukami Y, Koga H, Yamanouchi U, Yoshioka Y, Hayashi N, Ebana K, Mizobuchi R, Yano M (2015) Gene pyramiding enhances durable blast disease resistance in rice. Sci Rep 5:7773. https://doi.org/10.1038/srep07773 García-Martinez JL, Gil J (2001) Light regulation of gibberellin biosynthesis and mode of action. J Plant Growth Regul 20:354–368. https://doi.org/10.1007/s003440010033 Garg OK, Singh BP (1971) Physiological significance of ascorbic acid in relation to drought resistance in rice (Oryza sativa L.). Plant Soil 34:219–223 Garg AK, Kim J-K, Owens TG, Ranwala AP, Choi YD, Kochian LV, Wu RJ (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Natl Acad Sci USA 99:15898–15903. https://doi.org/10.1073/pnas.252637799 Gramene (2020) http://www.gramene.org/. Accessed 10 May 2020 Gupta SK, Rai AK, Kanwar SS, Chand D, Singh NK, Sharma TR (2011) The single functional blast resistance gene Pi54 activates a complex defence mechanism in rice. J Exp Bot 63:757–772. https://doi.org/10.1093/jxb/err297 Hammesfahr B, Odronitz F, Mühlhausen S, Waack S, Kollmar M (2013) GenePainter: a fast tool for aligning gene structures of eukaryotic protein families, visualizing the alignments and mapping gene structures onto protein structures. BMC Bioinformatics 14:77. https://doi.org/10.1186/1471-2105-14-77 Hargrove TR, Coffman WR, Cabanilla VL (1979) Genetic interrelationships of improved rice varieties in Asia. International Rice Research Institute, Manila, pp 2–10 International Rice Genome Sequencing Project, Sasaki T (2005) The map-based sequence of the rice genome. Nature 436:793–800. https://doi.org/10.1038/nature03895 International Rice Research Institute (IRRI) (2013) Standard evaluation system for rice, 5th edn. International Rice Research Institute, Manila, pp 2–18 Itoh H, Ueguchi-Tanaka M, Sakamoto T, Kayano T, Tanaka H, Ashikari M, Matsuoka M (2002) Modification of rice plant height by suppressing the height-controlling gene, D18. Rice Breed Sci 52:215–218. https://doi.org/10.1270/jsbbs.52.215 Jia Y, Bryan GT, Farrall L, Valent B (2003) Natural variation at the Pi-ta rice blast resistance locus. Phytopathology 93:1452–1459. https://doi.org/10.1094/PHYTO.2003.93.11.1452 Jia X, Yu L, Tang M, Tian D, Yang S, Zhang X, Traw MB (2020) Pleiotropic changes revealed by in situ recovery of the semi-dwarf gene sd1 in rice. J Plant Physiol 248:153141. https://doi.org/10.1016/j.jplph.2020.153141 Kawahara Y, de la Bastide M, Hamilton JP, Kanamori H, McCombie WR, Ouyang S, Schwartz DC, Tanaka T, Wu J, Zhou S, Childs KL, Davidson RM, Lin H, Quesada-Ocampo L, Vaillancourt B, Sakai H, Lee SS, Kim J, Numa H, Itoh T, Buell CR, Matsumoto T (2013) Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice 6:4. https://doi.org/10.1186/1939-8433-6-4 Kumar PN, Sujatha K, Laha GS, Rao KS, Mishra B, Viraktamath BC, Hari Y, Reddy CS, Balachandran SM, Ram T, Madhav MS, Rani NS, Neeraja CN, Reddy GA, Shaik H, Sundaram RM (2012) Identification and fine-mapping of Xa33, a novel gene for resistance to Xanthomonas oryzae pv. oryzae. Phytopathology 102:222–228. https://doi.org/10.1094/PHYTO-03-11-0075 Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, Antonescu C, Salzberg SL (2004) Versatile and open software for comparing large genomes. Genome Biol 5:R12. https://doi.org/10.1186/gb-2004-5-2-r12 Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. https://doi.org/10.1093/bioinformatics/btm404 Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079. https://doi.org/10.1093/bioinformatics/btp352 Li H (2013) Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. https://arxiv.org/abs/1303.3997. Accessed 7 May 2021 Li Q, Wang J, Ye J, Zheng X, Xiang X, Li C, Fu M, Wang Q, Zhang Z, Wu Y (2017) The maize imprinted gene Floury3 encodes a PLATZ protein required for tRNA and 5S rRNA transcription through interaction with RNA polymerase III. Plant Cell 29:2661–2675. https://doi.org/10.1105/tpc.17.00576 Liu L-W, Hsieh S-H, Lin S-J, Wang Y-M, Lin W-S (2021) Rice blast (Magnaporthe oryzae) occurrence prediction and the key factor sensitivity analysis by machine learning. Agronomy 11:771. https://doi.org/10.3390/agronomy11040771 Luyckx J, Baudouin C (2011) Trehalose: an intriguing disaccharide with potential for medical application in ophthalmology. Clin Ophthalmol 5:577–581. https://doi.org/10.2147/OPTH.S18827 Ma J, Lei C, Xu X, Hao K, Wang J, Cheng Z, Ma X, Ma J, Zhou K, Zhang X, Guo X, Wu F, Lin Q, Wang C, Zhai H, Wang H, Wan J (2015) Pi64, encoding a novel CC-NBS-LRR protein, confers resistance to Leaf and neck blast in rice. Mol Plant Microbe Interact 28:558–568. https://doi.org/10.1094/MPMI-11-14-0367-R Mahesh HB, Shirke MD, Singh S, Rajamani A, Hittalmani S, Wang GL, Gowda M (2016) Indica rice genome assembly, annotation and mining of blast disease resistance genes. BMC Genomics 17:242. https://doi.org/10.1186/s12864-016-2523-7 Mansueto L, Fuentes RR, Borja FN, Detras J, Abriol-Santos JM, Chebotarov D, Sanciangco M, Palis K, Copetti D, Poliakov A, Dubchak I, Solovyev V, Wing RA, Hamilton RS, Mauleon R, McNally KL, Alexandrov N (2017) Rice SNP-seek database update: new SNPs, indels, and queries. Nucleic Acids Res 45:D1075–D1081. https://doi.org/10.1093/nar/gkw1135 Marçais G, Delcher AL, Phillippy AM, Coston R, Salzberg SL, Zimin A (2018) MUMmer4: a fast and versatile genome alignment system. PLoS Comput Biol 14:e1005944. https://doi.org/10.1371/journal.pcbi.1005944 Monna L, Kitazawa N, Yoshino R, Suzuki J, Masuda H, Maehara Y, Tanji M, Sato M, Nasu S, Minobe Y (2002) Positional cloning of rice semidwarfing gene, sd-1: rice “green revolution Gene” encodes a mutant enzyme involved in gibberellin synthesis. DNA Res 9:11–17. https://doi.org/10.1093/dnares/9.1.11 Nagano H, Onishi K, Ogasawara M, Horiuchi Y, Sano Y (2005) Genealogy of the “Green Revolution” gene in rice. Genes Genet Syst 80:351–356. https://doi.org/10.1266/ggs.80.351 Nugroho C, Raharjo D, Mustaha MA, Asaad M (2021) Assessing disease severity of rice blast under different rates of nitrogen fertilizer and planting system. E3S Web Conf 306:1034 Panibe JP, Wang L, Li J, Li M-Y, Lee Y-C, Wang C-S, Ku MSB, Lu M-YJ, Li W-H (2021) Chromosomal-level genome assembly of the semi-dwarf rice Taichung Native 1, an initiator of Green Revolution. Genomics 113:2656–2674. https://doi.org/10.1016/j.ygeno.2021.06.006 Paul MJ, Gonzalez-Uriarte A, Griffiths CA, Hassani-Pak K (2018) The role of trehalose 6-phosphate in crop yield and resilience. Plant Physiol 177:12–23. https://doi.org/10.1104/pp.17.01634 Pertea G, Pertea M (2020) GFF utilities GffRead and GffCompare. F1000Res 9:304. https://doi.org/10.12688/f1000research.23297.2 R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 7 May 2021 Rai AK, Kumar SP, Gupta SK, Gautam N, Singh NK, Sharma TR (2011) Functional complementation of rice blast resistance gene Pi-kh (Pi54) conferring resistance to diverse strains of Magnaporthe oryzae. J Plant Biochem Biotechnol 20:55–65. https://doi.org/10.1007/s13562-010-0026-1 Ramalingam J, Raveendra C, Savitha P, Vidya V, Chaithra TL, Velprabakaran S, Saraswathi R, Ramanathan A, Arumugam Pillai MP, Arumugachamy S, Vanniarajan C (2020) Gene pyramiding for achieving enhanced resistance to bacterial blight, blast, and sheath blight diseases in rice. Front Plant Sci 11:591457. https://doi.org/10.3389/fpls.2020.591457 Reinecke DM, Wickramarathna AD, Ozga JA, Kurepin LV, Jin AL, Good AG, Pharis RP (2013) Gibberellin 3-oxidase gene expression patterns influence gibberellin biosynthesis, growth, and development in pea. Plant Physiol 163:929–945. https://doi.org/10.1104/pp.113.225987 Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP (2011) Integrative genomics viewer. Nat Biotechnol 29:24–26. https://doi.org/10.1038/nbt.1754 Sabbu S, Pandey MK, Reddy B, Shaik H, Kumar SV, Kousik MBVN, Bhadana VP, Madhav MS, Kota S, SubbaRao LV, Kumaraswamy M, Giri A, Narasu BL, Rani NS, Sundaram RM (2016) Introgression of major bacterial blight and blast resistant genes into Vallabh Basmati 22 an elite Basmati variety. Int J Dev Res 6:8366–8370 Sahm A, Bens M, Platzer M, Szafranski K (2017) PosiGene: automated and easy-to-use pipeline for genome-wide detection of positively selected genes. Nucleic Acids Res 45:e100. https://doi.org/10.1093/nar/gkx179 Sakai H, Lee SS, Tanaka T, Numa H, Kim J, Kawahara Y, Wakimoto H, Yang CC, Iwamoto M, Abe T, Yamada Y, Muto A, Inokuchi H, Ikemura T, Matsumoto T, Sasaki T, Itoh T (2013) Rice annotation project database (RAP-DB): an integrative and interactive database for rice genomics. Plant Cell Physiol 54:e6. https://doi.org/10.1093/pcp/pcs183 Sharma TR, Madhav MS, Singh BK, Shanker P, Jana TK, Dalal V, Pandit A, Singh A, Gaikwad K, Upreti HC, Singh NK (2005) High-resolution mapping, cloning and molecular characterization of the Pi-kh gene of rice, which confers resistance to Magnaporthe grisea. Mol Genet Genomics 274:569–578. https://doi.org/10.1007/s00438-005-0035-2 Sharma M, Singh A, Shankar A, Pandey A, Baranwal V, Kapoor S, Tyagi AK, Pandey GK (2014) Comprehensive expression analysis of rice armadillo gene family during abiotic stress and development. DNA Res 21:267–283. https://doi.org/10.1093/dnares/dst056 Singh A, Singh VK, Singh SP, Pandian RT, Ellur RK, Singh D, Bhowmick PK, Gopala Krishnan S, Nagarajan M, Vinod KK, Singh UD, Prabhu KV, Sharma TR, Mohapatra T, Singh AK (2012) Molecular breeding for the development of multiple disease resistance in Basmati rice. AoB Plants 2012:pls029. https://doi.org/10.1093/aobpla/pls029 Spielmeyer W, Ellis MH, Chandler PM (2002) Semidwarf (sd-1), “green revolution” rice, contains a defective gibberellin 20-oxidase gene. Proc Natl Acad Sci USA 99:9043–9048. https://doi.org/10.1073/pnas.132266399 Stein JC, Yu Y, Copetti D, Zwickl DJ, Zhang L, Zhang C, Chougule K, Gao D, Iwata A, Goicoechea JL, Wei S, Wang J, Liao Y, Wang M, Jacquemin J, Becker C, Kudrna D, Zhang J, Londono CEM, Song X, Lee S, Sanchez P, Zuccolo A, Ammiraju JSS, Talag J, Danowitz A, Rivera LF, Gschwend AR, Noutsos C, Wu CC, Kao S-M, Zeng J-W, Wei F-J, Zhao Q, Feng Q, El Baidouri M, Carpentier M-C, Lasserre E, Cooke R, da Rosa FD, da Maia LC, Dos Santos RS, Nyberg KG, McNally KL, Mauleon R, Alexandrov N, Schmutz J, Flowers D, Fan C, Weigel D, Jena KK, Wicker T, Chen M, Han B, Henry R, Hsing Y-IC, Kurata N, de Oliveira AC, Panaud O, Jackson SA, Machado CA, Sanderson MJ, Long M, Ware D, Wing RA (2018) Genomes of 13 domesticated and wild rice relatives highlight genetic conservation, turnover and innovation across the genus Oryza. Nat Genet 50:285–296. https://doi.org/10.1038/s41588-018-0040-0 Steuernagel B, Jupe F, Witek K, Jones JDG, Wulff BBH (2015) NLR-parser: rapid annotation of plant NLR complements. Bioinformatics 31:1665–1667. https://doi.org/10.1093/bioinformatics/btv005 Stick RV, Williams SJ (2009) Disaccharides, oligosaccharides and polysaccharides. In: Stick RV, Williams SJ (eds) Carbohydrates: the essential molecules of life, 2nd edn. Elsevier, Amsterdam, p 335 Sun X, Wang G-L (2011) Genome-wide identification, characterization and phylogenetic analysis of the rice LRR-kinases. PLoS ONE 6:e16079. https://doi.org/10.1371/journal.pone.0016079 Supek F, Bošnjak M, Škunca N, Šmuc T (2011) REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS ONE 6:e21800. https://doi.org/10.1371/journal.pone.0021800 Takken FLW, Joosten MHAJ (2000) Plant resistance genes: their structure, function and evolution. Eur J Plant Pathol 106:699–713. https://doi.org/10.1023/A:1026571130477 Tanaka T, Nishijima R, Teramoto S, Kitomi Y, Hayashi T, Uga Y, Kawakatsu T (2020) De novo genome assembly of the Indica rice variety IR64 using linked-read sequencing and nanopore sequencing. G3 Bethesda 10:1495–1501. https://doi.org/10.1534/g3.119.400871 Thakur S, Singh PK, Das A, Rathour R, Variar M, Prashanthi SK, Singh AK, Singh UD, Chand D, Singh NK, Sharma TR (2015) Extensive sequence variation in rice blast resistance gene Pi54 makes it broad spectrum in nature. Front Plant Sci 6:345. https://doi.org/10.3389/fpls.2015.00345 SRA Tools (2021) https://github.com/ncbi/sra-tools. Accessed 7 May 2021 Vergara BS, Chang TT (1985) The flowering response of the rice plant to photoperiod: a review of the literature, 4th edn. International Rice Research Institute, Los Baños, pp 5–35 Wang Y, Bouwmeester K (2017) L-type lectin receptor kinases: new forces in plant immunity. PLoS Pathog 13:e1006433. https://doi.org/10.1371/journal.ppat.1006433 Wang X, Jia Y, Shu QY, Wu D (2008) Haplotype diversity at the Pi-ta locus in cultivated rice and its wild relatives. Phytopathology 98:1305–1311. https://doi.org/10.1094/PHYTO-98-12-1305 Wang X, Lee S, Wang J, Ma J, Bianco T, Jia Y (2014) Current advances on genetic resistance to rice blast disease. In: Yan W, Bao J (eds) Rice—germplasm, genetics and improvement. IntechOpen, London. https://doi.org/10.5772/56824 Wang J, Ji C, Li Q, Zhou Y, Wu Y (2018a) Genome-wide analysis of the plant-specific PLATZ proteins in maize and identification of their general role in interaction with RNA polymerase III complex. BMC Plant Biol 18:221. https://doi.org/10.1186/s12870-018-1443-x Wang W, Mauleon R, Hu Z, Chebotarov D, Tai S, Wu Z, Li M, Zheng T, Fuentes RR, Zhang F, Mansueto L, Copetti D, Sanciangco M, Palis KC, Xu J, Sun C, Fu B, Zhang H, Gao Y, Zhao X, Shen F, Cui X, Yu H, Li Z, Chen M, Detras J, Zhou Y, Zhang X, Zhao Y, Kudrna D, Wang C, Li R, Jia B, Lu J, He X, Dong Z, Xu J, Li Y, Wang M, Shi J, Li J, Zhang D, Lee S, Hu W, Poliakov A, Dubchak I, Ulat VJ, Borja FN, Mendoza JR, Ali J, Li J, Gao Q, Niu Y, Yue Z, Naredo MEB, Talag J, Wang X, Li J, Fang X, Yin Y, Glaszmann J-C, Zhang J, Li J, Hamilton RS, Wing RA, Ruan J, Zhang G, Wei C, Alexandrov N, McNally KL, Li Z, Leung H (2018b) Genomic variation in 3,010 diverse accessions of Asian cultivated rice. Nature 557:43–49. https://doi.org/10.1038/s41586-018-0063-9 Wang A, Hou Q, Si L, Huang X, Luo J, Lu D, Zhu J, Shangguan Y, Miao J, Xie Y, Wang Y, Zhao Q, Feng Q, Zhou C, Li Y, Fan D, Lu Y, Tian Q, Wang Z, Han B (2019a) The PLATZ transcription factor GL6 affects grain length and number in rice. Plant Physiol 180:2077–2090. https://doi.org/10.1104/pp.18.01574 Wang L, Zhao L, Zhang X, Zhang Q, Jia Y, Wang G, Li S, Tian D, Li W-H, Yang S (2019b) Large-scale identification and functional analysis of NLR genes in blast resistance in the Tetep rice genome sequence. Proc Natl Acad Sci USA 116:18479–18487. https://doi.org/10.1073/pnas.1910229116 Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ (2009) Jalview version 2–a multiple sequence alignment editor and analysis workbench. Bioinformatics 25:1189–1191. https://doi.org/10.1093/bioinformatics/btp033 Wu B, Hu W, Ayaad M, Liu H, Xing Y (2017) Intragenic recombination between two non-functional semi-dwarf 1 alleles produced a functional SD1 allele in a tall recombinant inbred line in rice. PLoS ONE 12:e0190116. https://doi.org/10.1371/journal.pone.0190116 Yoshida S (1981) Fundamental of rice crop science. International Rice Research Institute, Los Baños, p 215 Zarbafi SS, Ham JH (2019) An overview of rice QTLs associated with disease resistance to three major rice diseases: blast, sheath blight, and bacterial panicle blight. Agronomy 9:177. https://doi.org/10.3390/agronomy9040177 Zeng L-R, Qu S, Bordeos A, Yang C, Baraoidan M, Yan H, Xie Q, Nahm BH, Leung H, Wang G-L (2004) Spotted leaf11, a negative regulator of plant cell death and defense, encodes a U-Box/Armadillo repeat protein endowed with E3 ubiquitin ligase activity. Plant Cell 16:2795–2808. https://doi.org/10.1105/tpc.104.025171 Zhang X, Yang S, Wang J, Jia Y, Huang J, Tan S, Zhong Y, Wang L, Gu L, Chen JQ, Pan Q, Bergelson J, Tian D (2015) A genome-wide survey reveals abundant rice blast R genes in resistant cultivars. Plant J 84:20–28. https://doi.org/10.1111/tpj.12955 Zhang J, Chen LL, Xing F, Kudrna DA, Yao W, Copetti D, Mu T, Li W, Song J-M, Xie W, Lee S, Talag J, Shao L, An Y, Zhang C-L, Ouyang Y, Sun S, Jiao W-B, Lv F, Du B, Luo M, Maldonado CE, Goicoechea JL, Xiong L, Wu C, Xing Y, Zhou D-X, Yu S, Zhao Y, Wang G, Yu Y, Luo Y, Zhou Z-W, Hurtado BE, Danowitz A, Wing RA, Zhang Q (2016) Extensive sequence divergence between the reference genomes of two elite indica rice varieties Zhenshan 97 and Minghui 63. Proc Natl Acad Sci USA 113:E5163–E5171. https://doi.org/10.1073/pnas.1611012113