Abstract
Sheath blight disease (ShB) severely affects rice production; however, the details of defense against ShB remain unclear. To understand the rice defense mechanism against ShB, an RNA sequencing analysis was performed using Rhizoctonia solani inoculated rice leaves after 48 h of inoculation. Among them, 3417 genes were upregulated and 2532 were downregulated when compared with the control group (> twofold or < 1/2). In addition, the differentially expressed genes were classified via Gene Ontology (GO), Kyoto Encyclopedia of Genes and Genomes (KEGG), and MapMan analyses. Fifty-nine GO terms and seven KEGG pathways were significantly enriched. A MapMan analysis demonstrated that the phytohormone and metabolic pathways were significantly altered. Interestingly, the expression levels of 359 transcription factors, including WRKY, MYB, and NAC family members, as well as 239 transporter genes, including ABC, MFS, and SWEET, were significantly changed in response to R. solani AG1-IA inoculation. Additionally, OsWRKY53 and OsAKT1 negatively regulate the defense response in rice against R. solani via gain of function study for OsWRKY53 and loss of function study for OsAKT1, respectively. Furthermore, several differentially expressed genes contain R. solani-responsive cis acting regulatory elements in their promoter regions. Taken together, our analyses provide valuable information for the additional study of the defense mechanisms against ShB, and the candidate genes identified in this study will be useful resource for future breeding to enhance resistance against ShB.
Similar content being viewed by others
References
Alvarez ME, Pennell RI, Meijer P-J, Ishikawa A, Dixon RA, Lamb C (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92:773–784
Audenaert K, De Meyer GB, Hofte MM (2002) Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid-dependent signaling mechanisms. Plant Physiol 128(2):491–501
Bonman JM, Khush GS, Nelson RJ (1992) Breeding rice for resistance to pests. Annu Rev Phytopathol 30:507–528
Cao P, Jung K, Choi D, Hwang D, Zhu J, Ronald PC (2012) The rice oligonucleotide array database: an atlas of rice gene expression. Rice 5(1):17
Chen LQ, Hou BH, Lalonde S, Takanaga H, Hartung ML, Qu XQ, Guo WJ, Kim JG, Underwood W, Chaudhuri B, Chermak D, Antony G, White FF, Somerville SC, Mudgett MB, Frommer WB (2010) Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468(7323):527–532
Chen LQ, Qu XQ, Hou BH, Sosso D, Osorio S, Fernie AR, Frommer WB (2012) Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science 335(6065):207–211
Cole T, Williams BA, Geo P, Ali M, Gordon K, Baren MJ, Van SSL, Wold BJ, Lior P (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28(5):511–515
Damian S, Andrea F, Stefan W, Kristoffer F, Davide H, Jaime HC, Milan S, Alexander R, Alberto S, Tsafou KP (2015) STRING v10: protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res 43:4–47
Dardick C, Chen J, Richter T, Ouyang S, Ronald P (2007) The rice kinase database. A phylogenomic database for the rice kinome. Plant Physiol 143(2):579–586
Fahad S, Nie L, Khan FA, Chen Y, Hussain S, Wu C, Xiong D, Jing W, Saud S, Khan FA, Li Y, Wu W, Khan F, Hassan S, Manan A, Jan A, Huang J (2014) Disease resistance in rice and the role of molecular breeding in protecting rice crops against diseases. Biotechnol Lett 36(7):1407–1420
Gao Y, Zhang C, Han X, Wang ZY, Ma L, Yuan P, Wu JN, Zhu XF, Liu JM, Li DP, Hu YB, Xuan YH (2018) Inhibition of OsSWEET11 function in mesophyll cells improves resistance of rice to sheath blight disease. Mol Plant Pathol 19(9):2149–2161
Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227
Hamann T (2012) Plant cell wall integrity maintenance as an essential component of biotic stress response mechanisms. Front Plant Sci 3:77
He Y, Xu J, Wang X, He X, Wang Y, Zhou J, Zhang S, Meng X (2019) The Arabidopsis pleiotropic drug resistance transporters PEN3 and PDR12 mediate camalexin secretion for resistance to Botrytis cinerea. Plant Cell 31(9):2206–2222
Helliwell EE, Wang Q, Yang Y (2013) Transgenic rice with inducible ethylene production exhibits broad-spectrum disease resistance to the fungal pathogens Magnaporthe oryzae and Rhizoctonia solani. Plant Biotechnol J 11(1):33–42
Hwang S, Kim Y, Sohn S, Choi D (2018) Gene expression profiling provides insight into the escape behavior of deepwater rice during submergence. J Plant Biol 61(6):374–382
Jain P, Singh PK, Kapoor R, Khanna A, Solanke AU, Krishnan SG, Singh AK, Sharma V, Sharma TR (2017) Understanding host-pathogen interactions with expression profiling of NILs carrying rice-blast resistance Pi9 gene. Front Plant Sci 8:93
John Lilly J, Subramanian B (2019) Gene network mediated by WRKY13 to regulate resistance against sheath infecting fungi in rice (Oryza sativa L.). Plant Sci 280:269–282
Jung KH, Cao P, Seo YS, Dardick C, Ronald PC (2010) The Rice Kinase Phylogenomics Database: a guide for systematic analysis of the rice kinase super-family. Trends Plant Sci 15(11):595–599
Karmakar S, Datta K, Molla KA, Gayen D, Das K, Sarkar SN, Datta SK (2019) Proteo-metabolomic investigation of transgenic rice unravels metabolic alterations and accumulation of novel proteins potentially involved in defence against Rhizoctonia solani. Sci Rep 9(1):10461
Kim E, Kim Y, Hong W, Lee C, Jeon J, Jung K (2019) Genome-wide analysis of root hair preferred RBOH genes suggests that three RBOH genes are associated with Auxin-mediated root hair development in rice. J Plant Biol 62(3):229–238
Krattinger SG, Kang J, Bräunlich S, Boni R, Chauhan H, Selter LL, Robinson MD, Schmid MW, Wiederhold E, Hensel G, Kumlehn J, Sucher J, Martinoia E, Keller B (2019) Abscisic acid is a substrate of the ABC transporter encoded by the durable wheat disease resistance gene Lr34. New Phytol 223(2):853–866
Lee FN, Rush MC (1983) Rice sheath blight a major rice disease. Plant Dis 67(7):829–832
Li J, Long Y, Qi GN, Li J, Xu ZJ, Wu WH, Wang Y (2014) The Os-AKT1 channel is critical for K+ uptake in rice roots and is modulated by the rice CBL1-CIPK23 complex. Plant Cell 26(8):3387–3402
Li N, Chen J, Yang F, Wei S, Kong L, Ding X, Chu Z (2017a) Identification of two novel Rhizoctonia solani-inducible cis-acting elements in the promoter of the maize gene, GRMZM2G315431. Sci Rep 7:42059
Li N, Lin B, Wang H, Li X, Yang F, Ding X, Yan J, Chu Z (2019) Natural variation in ZmFBL41 confers banded leaf and sheath blight resistance in maize. Nat Genet 51(10):1540–1548
Li N, Wei S, Chen J, Yang F, Kong L, Chen C, Ding X, Chu Z (2018) OsASR2 regulates the expression of a defence-related gene, Os2H16, by targeting the GT-1 cis-element. Plant Biotechnol J 16(3):771–783
Li T, Liao K, Xu X, Gao Y, Wang Z, Zhu X, Jia B, Xuan Y (2017b) Wheat ammonium transporter (AMT) gene family: diversity and possible role in host-pathogen interaction with stem rust. Front Plant Sci 8:1637
Li Z, Pinson SRM, Marchetti MA, Stansel JW, Park WDJT (1995) Characterization of quantitative trait loci (QTLs) in cultivated rice contributing to field resistance to sheath blight (Rhizoctonia solani). Theor Appl Genet 91(2):382–388
Lievens L, Pollier J, Goossens A, Beyaert R, Staal J (2017) Abscisic acid as pathogen effector and immune regulator. Front Plant Sci 8:587
Lin IW, Sosso D, Chen LQ, Gase K, Kim SG, Kessler D, Klinkenberg PM, Gorder MK, Hou BH, Qu XQ, Carter CJ, Baldwin IT, Frommer WB (2014) Nectar secretion requires sucrose phosphate synthases and the sugar transporter SWEET9. Nature 508(7497):546–549
Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15(12):550
Marchetti MA, Bollich CN (1991) Quantification of the relationship between sheath blight severity and yield loss in rice. Plant Dis 75(8):773–775
Matsumura H, Reich S, Ito A, Saitoh H, Kamoun S, Winter P, Kahl G, Reuter M, Kruger DH, Terauchi R (2003) Gene expression analysis of plant host-pathogen interactions by SuperSAGE. Proc Natl Acad Sci USA 100(26):15718–15723
Mei J, Guo Z, Wang J, Feng Y, Ma G, Zhang C, Qian W, Chen G (2019) Understanding the resistance mechanism in Brassica napus to clubroot caused by Plasmodiophora brassicae. Phytopathology 109(5):810–818
Mine A, Seyfferth C, Kracher B, Berens ML, Becker D, Tsuda K (2018) The defense phytohormone signaling network enables rapid, high-amplitude transcriptional reprogramming during effector-triggered immunity. Plant Cell 30(6):1199–1219
Mirabet V, Das P, Boudaoud A, Hamant O (2011) The role of mechanical forces in plant morphogenesis. Annu Rev Plant Biol 62:365–385
Moon S, Chandran AKN, Kim Y, Gho Y, Hong W, An G, Lee C, Jung K (2019) Rice RHC encoding a putative cellulase is essential for normal root hair elongation. J Plant Biol 62(1):82–91
Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Med 5(7):621–628
Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate npr1 function through redox change. Cell 113:935–944
Noctor G, Reichheld JP, Foyer CH (2018) ROS-related redox regulation and signaling in plants. Semin Cell Dev Biol 80:3–12
Pastor V, Gamir J, Camanes G, Cerezo M, Sanchez-Bel P, Flors V (2014) Disruption of the ammonium transporter AMT11 alters basal defenses generating resistance against Pseudomonas syringae and Plectosphaerella cucumerina. Front Plant Sci 5:231
Peng X, Hu Y, Tang X, Zhou P, Deng X, Wang H, Guo Z (2012) Constitutive expression of rice WRKY30 gene increases the endogenous jasmonic acid accumulation, PR gene expression and resistance to fungal pathogens in rice. Planta 236(5):1485–1498
Peng X, Wang H, Jang JC, Xiao T, He H, Jiang D, Tang X (2016) OsWRKY80-OsWRKY4 module as a positive regulatory circuit in rice resistance against Rhizoctonia solani. Rice (N Y) 9(1):63
Pooja S, Sweta K, Mohanapriya A, Sudandiradoss C, Siva R, Gothandam KM, Babu S (2015) Homotypic clustering of OsMYB4 binding site motifs in promoters of the rice genome and cellular-level implications on sheath blight disease resistance. Gene 561(2):209–218
Rao VS, Srinivas K, Sujini GN (2014) Kumar GN (2014) protein–protein interaction detection: methods and analysis. J Proteomics 4:147648
Richa K, Tiwari IM, Devanna BN, Botella JR, Sharma V, Sharma TR (2017) Novel chitinase gene LOC_Os11g47510 from indica rice Tetep provides enhanced resistance against sheath blight pathogen Rhizoctonia solani in rice. Front Plant Sci 8:596
Richa K, Tiwari IM, Kumari M, Devanna BN, Sonah H, Kumari A, Nagar R, Sharma V, Botella JR, Sharma TR (2016) Functional characterization of novel chitinase genes present in the sheath blight resistance QTL: qSBR11-1 in rice line Tetep. Front Plant Sci 7:244
Romer P, Recht S, Strauss T, Elsaesser J, Schornack S, Boch J, Wang S, Lahaye T (2010) Promoter elements of rice susceptibility genes are bound and activated by specific TAL effectors from the bacterial blight pathogen. Xanthomonas oryzae pv oryzae New Phytol 187(4):1048–1057
Seo Y, Sriariyanun M, Wang L, Pfeiff J, Phetsom J, Lin Y, Jung K, Chou HH, Bogdanove A, Ronald P (2008) A two-genome microarray for the rice pathogens Xanthomonas oryzae pv. oryzae and X. oryzae pv. oryzicola and its use in the discovery of a difference in their regulation of hrp genes. BMC Microbiol 8(1):99
Shi X, Long Y, He F, Zhang C, Wang R, Zhang T, Wu W, Hao Z, Wang Y, Wang GL, Ning Y (2018) The fungal pathogen Magnaporthe oryzae suppresses innate immunity by modulating a host potassium channel. PLoS Pathog 14(1):e1006878
Singh P, Mazumdar P, Harikrishna JA, Babu S (2019) Sheath blight of rice: a review and identification of priorities for future research. Planta 250(5):1387–1407
Streubel J, Pesce C, Hutin M, Koebnik R, Boch J, Szurek B (2013) Five phylogenetically close rice SWEET genes confer TAL effector-mediated susceptibility to Xanthomonas oryzae pv. oryzae. New Phytol 200(3):808–819
Sun Q, Li TY, Li DD, Wang ZY, Li S, Li DP, Han X, Liu JM, Xuan YH (2019) Overexpression of loose plant architecture 1 increases planting density and resistance to sheath blight disease via activation of PIN-FORMED 1a in rice. Plant Biotechnol J 17(5):855–857
Thimm O, Blasing O, Gibon Y, Nagel A, Meyer S, Kruger P, Selbig J, Muller LA, Rhee SY, Stitt M (2010) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37(6):914–939
Tian X, Li X, Zhou W, Ren Y, Wang Z, Liu Z, Tang J, Tong H, Fang J, Bu Q (2017) Transcription factor OsWRKY53 positively regulates brassinosteroid signaling and plant architecture. Plant Physiol 175(3):1337–1349
Tonnessen BW, Manosalva P, Lang JM, Baraoidan M, Bordeos A, Mauleon R, Oard J, Hulbert S, Leung H, Leach JE (2015) Rice phenylalanine ammonia-lyase gene OsPAL4 is associated with broad spectrum disease resistance. Plant Mol Biol 87(3):273–286
Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25(9):1105–1111
Ulferts S, Delventhal R, Splivallo R, Karlovsky P, Schaffrath U (2015) Abscisic acid negatively interferes with basal defence of barley against Magnaporthe oryzae. BMC Plant Biol 15:7
Venu RC, Jia Y, Gowda M, Jia MH, Jantasuriyarat C, Stahlberg E, Li H, Rhineheart A, Boddhireddy P, Singh P, Rutger N, Kudrna D, Wing R, Nelson JC, Wang GL (2007) RL-SAGE and microarray analysis of the rice transcriptome after Rhizoctonia solani infection. Mol Genet Genomics 278(4):421–431
Wang H, Meng J, Peng X, Tang X, Zhou P, Xiang J, Deng X (2015) Rice WRKY4 acts as a transcriptional activator mediating defense responses toward Rhizoctonia solani, the causing agent of rice sheath blight. Plant Mol Biol 89(1–2):157–171
Wilson RA, Talbot NJ (2009) Under pressure: investigating the biology of plant infection by Magnaporthe oryzae. Nat Rev Microbiol 7(3):185–195
Xue X, Cao ZX, Zhang XT, Wang Y, Zhang YF, Chen ZX, Pan XB, Zuo SM (2016) Overexpression of OsOSM1 enhances resistance to rice sheath blight. Plant Dis 100(8):1634–1642
Yang B, Sugio A, White FF (2006) Os8N3 is a host disease-susceptibility gene for bacterial blight of rice. Proc Natl Acad Sci USA 103(27):10503–10508
Yang F, Ding X, Chen J, Shen Y, Kong L, Li N, Chu Z (2017) Functional analysis of the GRMZM2G174449 promoter to identify Rhizoctonia solani-inducible cis-elements in maize. BMC Plant Biol 17(1):233
Yang J, Luo D, Yang B, Frommer WB, Eom JS (2018) SWEET11 and 15 as key players in seed filling in rice. New Phytol 218(2):604–615
Yuan P, Zhang C, Wang ZY, Zhu XF, Xuan YH (2018) RAVL1 activates brassinosteroids and ethylene signaling to modulate response to sheath blight disease in rice. Phytopathology 108(9):1104–1113
Yu G, Wang L, Han Y, He Q (2012) clusterProfiler: an R package for comparing biological themes among gene clusters. Omics 16(5):284–287
Zhang J, Chen L, Fu C, Wang L, Liu H, Cheng Y, Li S, Deng Q, Wang S, Zhu J, Liang Y, Li P, Zheng A (2017a) Comparative transcriptome analyses of gene expression changes triggered by Rhizoctonia solani AG1 IA infection in resistant and susceptible rice varieties. Front Plant Sci 8:1422
Zhang Y, Wang X, Rong W, Yang J, Li Z, Wu L, Zhang G, Ma Z (2017b) Histochemical analyses reveal that stronger intrinsic defenses in gossypium barbadense than in G hirsutum are associated with resistance to Verticillium dahliae. Mol Plant Microbe Int 30(12):984–996
Zhang Y, Zhao J, Li Y, Yuan Z, He H, Yang H, Qu H, Ma C, Qu S (2016) Transcriptome analysis highlights defense and signaling pathways mediated by rice pi21 gene with partial resistance to Magnaporthe oryzae. Front Plant Sci 7:1834
Zheng A, Lin R, Zhang D, Qin P, Xu L, Ai P, Ding L, Wang Y, Chen Y, Liu Y, Sun Z, Feng H, Liang X, Fu R, Tang C, Li Q, Zhang J, Xie Z, Deng Q, Li S, Wang S, Zhu J, Wang L, Liu H, Li P (2013) The evolution and pathogenic mechanisms of the rice sheath blight pathogen. Nat Commun 4:1424
Zhu T, Song F, Zheng Z (2006) Molecular characterization of the rice pathogenesis-related protein, OsPR-4b, and its antifungal activity against Rhizoctonia solani. J Phytopathol 154(6):378–384
Acknowledgments
We are immensely grateful to Prof. Bu Qingyun for providing Longjing11, Oswrky53, and OsWRKY53 OE seeds. We also greatly appreciate Prof. Wang Guo-Liang for providing Osakt1 seeds. This research was funded by THE EARMARKED FUND FOR THE CHINA AGRICULTURE RESEARCH SYSTEM, CARS-01 to S.H.W., SUPPORT PLAN FOR YONG AND MIDDLE-AGED SCIENTIFIC AND TECHNOLOGICAL INNOVATION TALENTS IN SHENYANG, RC190489 to Y.H.X. and a grant from THE NEXT-GENERATION BIOGREEN 21 PROGRAM, PJ01325901 to K.H.J.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflicts of interest
The authors declare no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Peng Yuan, D., Xu, X.F., Hong, WJ. et al. Transcriptome analysis of rice leaves in response to Rhizoctonia solani infection and reveals a novel regulatory mechanism. Plant Biotechnol Rep 14, 559–573 (2020). https://doi.org/10.1007/s11816-020-00630-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11816-020-00630-9