Transcriptomic analysis of wheat reveals possible resistance mechanism mediated by Yr10 to stripe rust

Zhongyi Wu, Gaohua Zhang, Ran Zhao, Qi Gao, Jinchen Zhao, Xiaoxu Zhu, Fangyan Wang, Zhensheng Kang, Xiaojing Wang

Stress Biology ›› 2023, Vol. 3 ›› Issue (1) : 44. DOI: 10.1007/s44154-023-00115-z
Original Paper

Transcriptomic analysis of wheat reveals possible resistance mechanism mediated by Yr10 to stripe rust

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Abstract

Stripe rust, caused by Puccinia striiformis f. sp. tritici (Pst), is a catastrophic disease that threatens global wheat yield. Yr10 is a race-specific all-stage disease resistance gene in wheat. However, the resistance mechanism of Yr10 is poorly characterized. Therefore, to elucidate the potential molecular mechanism mediated by Yr10, transcriptomic sequencing was performed at 0, 18, and 48 h post-inoculation (hpi) of compatible wheat Avocet S (AvS) and incompatible near-isogenic line (NIL) AvS +  Yr10 inoculated with Pst race CYR32. Respectively, 227, 208, and 4050 differentially expressed genes (DEGs) were identified at 0, 18, and 48 hpi between incompatible and compatible interaction. The response of Yr10 to stripe rust involved various processes and activities, as indicated by the results of Gene Ontology (GO) enrichment analysis and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis. Specifically, the response included photosynthesis, defense response to fungus, metabolic processes related to salicylic acid (SA) and jasmonic acid (JA), and activities related to reactive oxygen species (ROS). Ten candidate genes were selected for qRT-PCR verification and the results showed that the transcriptomic data was reliable. Through the functional analysis of candidate genes by the virus-induced gene silencing (VIGS) system, it was found that the gene TaHPPD (4-hydroxyphenylpyruvate dioxygenase) negatively regulated the resistance of wheat to stripe rust by affecting SA signaling, pathogenesis-related (PR) gene expression, and ROS clearance. Our study provides insight into Yr10-mediated resistance in wheat.

Keywords

Transcriptome / Yr10 / Virus-induced gene silencing system / (VIGS) system / 4-hydroxyphenylpyruvate dioxygenase / HPPD

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Zhongyi Wu, Gaohua Zhang, Ran Zhao, Qi Gao, Jinchen Zhao, Xiaoxu Zhu, Fangyan Wang, Zhensheng Kang, Xiaojing Wang. Transcriptomic analysis of wheat reveals possible resistance mechanism mediated by Yr10 to stripe rust. Stress Biology, 2023, 3(1): 44 https://doi.org/10.1007/s44154-023-00115-z

References

[1]
Andrews S (2010) FastQC: A quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/
[2]
Bennett S (2004) Solexa Ltd. Pharmacogenomics 5(4):433–438. https://doi.org/10.1517/14622416.5.4.433
[3]
BokoreFE, CuthbertRD, KnoxRE, RandhawaHS, HiebertCW, DePauwRM, SinghAK, SinghA, SharpeAG, N'DiayeA, PozniakCJ, McCartneyC, RuanY, BerraiesS, MeyerB, MunroC, HayA, AmmarK, Huerta-EspinoJ, BhavaniS. Quantitative trait loci for resistance to stripe rust of wheat revealed using global field nurseries and opportunities for stacking resistance genes. Theor Appl Genet, 2017, 130(12):2617-2635
CrossRef Google scholar
[4]
BolgerAM, LohseM, UsadelB. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics (oxford, England), 2014, 30(15):2114-2120
CrossRef Google scholar
[5]
Boller T, He SY (2009) Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science (New York, N.Y.) 324(5928):742–744. https://doi.org/10.1126/science.1171647
[6]
BoltonMD. Primary metabolism and plant defense-fuel for the fire. Molecular Plant-Microbe Interactions: MPMI, 2009, 22(5):487-497
CrossRef Google scholar
[7]
CaoH, BowlingSA, GordonAS, DongXN. Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell, 1994, 6: 1583-1592
CrossRef Google scholar
[8]
ChangQ, LiuJ, WangQ, HanL, LiuJ, LiM, HuangL, YangJ, KangZ. The effect of Puccinia striiformis f. sp. tritici on the levels of water-soluble carbohydrates and the photosynthetic rate in wheat leaves. Physiol Mol Plant Pathol, 2013, 84: 131-137
CrossRef Google scholar
[9]
Chen WQ, Kang ZS, Ma ZH, Xu SC, Jin SL, Jiang YY (2013) Integrated management of wheat stripe rust caused by Puccinia striiformis f. sp. tritici in China. Scientia Agricultura Sinica 46(20):4254–4262. https://doi.org/10.3864/j.issn.0578-1752.2013.20.008
[10]
Chen XM (2005) Epidemiology and control of stripe rust (Puccinia striiformis f. sp. tritici) on wheat. Canadian Journal of Plant Pathology 27(3):314–337. https://doi.org/10.1080/07060660509507230
[11]
Dangl JL, Horvath DM, Staskawicz BJ (2013) Pivoting the plant immune system from dissection to deployment. Science (New York, N.Y.) 341(6147):746–751. https://doi.org/10.1126/science.1236011
[12]
Desmond OJ, Edgar CI, Manners JM, Maclean DJ, Schenk PM, Kazan K (2005) Methyl jasmonate induced gene expression in wheat delays symptom development by the crown rot pathogen Fusarium pseudograminearum. Physiol Mol Plant Pathol 67(3–5):171–179. https://doi.org/10.1016/j.pmpp.2005.12.007
[13]
DinglasanE, PeriyannanS, HickeyLT. Harnessing adult-plant resistance genes to deploy durable disease resistance in crops. Essays Biochem, 2022, 66(5):571-580
CrossRef Google scholar
[14]
DobonA, BuntingDC, Cabrera-QuioLE, UauyC, SaundersDG. The host-pathogen interaction between wheat and yellow rust induces temporally coordinated waves of gene expression. BMC Genomics, 2016, 17: 380
CrossRef Google scholar
[15]
FAOSTAT (2021) Food and Agriculture Organization of the United Nations. Food and Agriculture Data. http://www.fao.org/faostat/en/#data
[16]
FryerMJ. The antioxidant effects of thylakoid vitamin E (α-tocopherol). Plant, Cell Environ, 1992, 15(4):381-392
CrossRef Google scholar
[17]
GesseseM, BarianaH, WongD, HaydenM, BansalU. Molecular mapping of stripe rust resistance gene Yr81 in a common wheat landrace Aus27430. Plant Dis, 2019, 103(6):1166-1171
CrossRef Google scholar
[18]
GöhreV, JonesAM, SklenářJ, RobatzekS, WeberAP. Molecular crosstalk between PAMP-triggered immunity and photosynthesis. Molecular Plant-Microbe Interactions, 2012, 25(8):1083-1092
CrossRef Google scholar
[19]
Hao Y, Wang T, Wang K, Wang X, Fu Y, Huang L, Kang Z (2016) Transcriptome analysis provides insights into the mechanisms underlying wheat plant resistance to stripe rust at the adult plant stage. PLoS One 11(3): e0150717. https://doi.org/10.1371/journal.pone.0150717
[20]
HolzbergS, BrosioP, GrossC, PogueGP. Barley stripe mosaic virus-induced gene silencing in a monocot plant. Plant J Cell Mol Biol, 2002, 30(3):315-327
CrossRef Google scholar
[21]
International Wheat Genome Sequencing Consortium (IWGSC) (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science (New York, N.Y.) 361(6403). https://doi.org/10.1126/science.aar7191
[22]
Kang Z, Wang X, Zhao J, Tian C, Huang L (2015) Advances in research of pathogenicity and virulence variation of the wheat stripe rust fungus Puccinia striiformis f. sp. tritici. Scientia Agricultura Sinica 48(17):3439-3453. https://www.chinaagrisci.com/CN/10.3864/j.issn.0578-1752.2015.17.011
[23]
KangasjärviS, TikkanenM, DurianG, AroEM. Photosynthetic light reactions-an adjustable hub in basic production and plant immunity signaling. Plant Physiol Biochem, 2014, 81: 128-134
CrossRef Google scholar
[24]
KunkelBN, BrooksDM. Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol, 2002, 5(4):325-331
CrossRef Google scholar
[25]
LambC, DixonRA. The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol, 1997, 48: 251-275
CrossRef Google scholar
[26]
LangmeadB, SalzbergSL. Fast gapped-read alignment with Bowtie 2. Nat Methods, 2012, 9(4):357-359
CrossRef Google scholar
[27]
LillR, FreibertSA. Mechanisms of mitochondrial iron-sulfur protein biogenesis. Annu Rev Biochem, 2020, 89: 471-499
CrossRef Google scholar
[28]
LiuY, KongD, WuHL, LingHQ. Iron in plant-pathogen interactions. J Exp Bot, 2021, 72(6):2114-2124
CrossRef Google scholar
[29]
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCTMethod. Methods (San Diego, Calif.) 25(4):402–408. https://doi.org/10.1006/meth.2001.1262
[30]
LorenzoO, SolanoR. Molecular players regulating the jasmonate signalling network. Curr Opin Plant Biol, 2005, 8(5):532-540
CrossRef Google scholar
[31]
LuY, YaoJ. Chloroplasts at the crossroad of photosynthesis, pathogen infection and plant defense. Int J Mol Sci, 2018, 19(12):3900
CrossRef Google scholar
[32]
MatringeM, KsasB, ReyP, HavauxM. Tocotrienols, the unsaturated forms of vitamin E, can function as antioxidants and lipid protectors in tobacco leaves. Plant Physiol, 2008, 147(2):764-778
CrossRef Google scholar
[33]
McIntoshR, MuJ, HanD, KangZ. Wheat stripe rust resistance gene Yr24/Yr26: a retrospective review. The Crop Journal, 2018, 6: 321-329
CrossRef Google scholar
[34]
MittlerR, ZandalinasSI, FichmanY, Van BreusegemF. Reactive oxygen species signalling in plant stress responses. Nat Rev Mol Cell Biol, 2022, 23(10):663-679
CrossRef Google scholar
[35]
MortazaviA, WilliamsBA, McCueK, SchaefferL, WoldB. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods, 2008, 5(7):621-628
CrossRef Google scholar
[36]
MurLA, SantosaIE, LaarhovenLJ, HoltonNJ, HarrenFJ, SmithAR. Laser photoacoustic detection allows in planta detection of nitric oxide in tobacco following challenge with avirulent and virulent Pseudomonas syringae Pathovars. Plant Physiol, 2005, 138(3):1247-1258
CrossRef Google scholar
[37]
MurLA, PratsE, PierreS, HallMA, HebelstrupKH. Integrating nitric oxide into salicylic acid and jasmonic acid/ ethylene plant defense pathways. Front Plant Sci, 2013, 4: 215
CrossRef Google scholar
[38]
NdikuryayoF, MoosaviB, YangWC, YangGF. 4-Hydroxyphenylpyruvate dioxygenase inhibitors: from chemical biology to agrochemicals. J Agric Food Chem, 2017, 65(39):8523-8537
CrossRef Google scholar
[39]
PengS, GuoD, GuoY, ZhaoH, MeiJ, HanY, GuanR, WangT, SongT, SunK, LiuY, MaoT, ChangH, XueJ, CaiY, ChenD, WangS. CONSTITUTIVE EXPRESSER OF PATHOGENESIS-RELATED GENES is an RNA-binding protein controlling plant immunity via an RNA processing complex. Plant Cell, 2022, 34(5):1724-1744
CrossRef Google scholar
[40]
RenW, ZhaoL, ZhangL, WangY, CuiL, TangY, SunX, TangK. Molecular cloning and characterization of 4-hydroxyphenylpyruvate dioxygenase gene from Lactuca sativa. J Plant Physiol, 2011, 168(10):1076-1083
CrossRef Google scholar
[41]
RuanJ, ZhouY, ZhouM, YanJ, KhurshidM, WengW, ChengJ, ZhangK. Jasmonic acid signaling pathway in plants. Int J Mol Sci, 2019, 20(10):2479
CrossRef Google scholar
[42]
Segarra G, Jáuregui O, CasanovaE, & Trillas I (2006) Simultaneous quantitative LC-ESI-MS/MS analyses of salicylic acid and jasmonic acid in crude extracts of Cucumis sativus under biotic stress. Phytochemistry 67(4):395–401.https://doi.org/10.1016/j.phytochem.2005.11.017
[43]
ShermanBT, HaoM, QiuJ, JiaoX, BaselerMW, LaneHC, ImamichiT, ChangW. DAVID: a web server for functional enrichment analysis and functional annotation of gene lists (2021 update). Nucleic Acids Res, 2022, 50(W1):W216-W221
CrossRef Google scholar
[44]
SpoelSH, KoornneefA, ClaessensSM, KorzeliusJP, Van PeltJA, MuellerMJ, BuchalaAJ, MétrauxJP, BrownR, KazanK, Van LoonLC, DongX, PieterseCM. NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell, 2003, 15(3):760-770
CrossRef Google scholar
[45]
Verberne MC, Budi Muljono AB, Verpoorte R (1999) Salicylic acid biosynthesis. Biochemistry and Molecular Biology of Plant Hormones, vol 33. Edited by Libbenga K, Hall M, Hooykaas PJJ. London: Elsevier; 1999:295–312. https://doi.org/10.1016/S0167-7306%2808%2960493-7
[46]
VerbonEH, TrapetPL, StringlisIA, KruijsS, BakkerPAHM, PieterseCMJ. Iron and immunity. Annu Rev Phytopathol, 2017, 55: 355-375
CrossRef Google scholar
[47]
WanA, ChenX, HeZ. Wheat stripe rust in China. Crop Pasture Sci, 2007, 58: 605-619
CrossRef Google scholar
[48]
WangC, HuangL, BuchenauerH, HanQ, ZhangH, KangZ. Histochemical studies on the accumulation of reactive oxygen species (O2− and H2O2) in the incompatible and compatible interaction of wheat—Puccinia striiformis f. sp. tritici. Physiol Mol Plant Pathol, 2007, 71: 230-239
CrossRef Google scholar
[49]
WangL, FengZ, WangX, WangX, ZhangX. DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics (oxford, England), 2010, 26(1):136-138
CrossRef Google scholar
[50]
WangX, WangY, LiuP, DingY, MuX, LiuX, WangX, ZhaoM, HuaiB, HuangL, KangZ. TaRar1 is involved in wheat defense against stripe rust pathogen mediated by YrSu. Front Plant Sci, 2017, 8: 156
CrossRef Google scholar
[51]
WangS, LiQP, WangJ, YanY, ZhangGL, YanY, ZhangH, WuJ, ChenF, WangX, KangZ, DubcovskyJ, GouJY. YR36/WKS1-mediated phosphorylation of PsbO, an extrinsic member of photosystem ii, inhibits photosynthesis and confers stripe rust resistance in wheat. Mol Plant, 2019, 12(12):1639-1650
CrossRef Google scholar
[52]
WangX, ZhangH, NyamesortoB, LuoY, MuX, WangF, KangZ, LagudahE, HuangL. A new mode of NPR1 action via an NB-ARC-NPR1 fusion protein negatively regulates the defence response in wheat to stem rust pathogen. New Phytol, 2020, 228(3):959-972
CrossRef Google scholar
[53]
WangN, FanX, HeM, HuZ, TangC, ZhangS, LinD, GanP, WangJ, HuangX, GaoC, KangZ, WangX. Transcriptional repression of TaNOX10 by TaWRKY19 compromises ROS generation and enhances wheat susceptibility to stripe rust. Plant Cell, 2022, 34(5):1784-1803
CrossRef Google scholar
[54]
WangN, TangC, FanX, HeM, GanP, ZhangS, HuZ, WangX, YanT, ShuW, YuL, ZhaoJ, HeJ, LiL, WangJ, HuangX, HuangL, ZhouJM, KangZ, WangX. Inactivation of a wheat protein kinase gene confers broad-spectrum resistance to rust fungi. Cell, 2022, 185(16):2961-2974.e19
CrossRef Google scholar
[55]
WaszczakC, CarmodyM, KangasjärviJ. Reactive oxygen species in plant signaling. Annu Rev Plant Biol, 2018, 69: 209-236
CrossRef Google scholar
[56]
WuF, ChiY, JiangZ, et al.. Hydrogen peroxide sensor HPCA1 is an LRR receptor kinase in Arabidopsis. Nature, 2020, 578(7796):577-581
CrossRef Google scholar
[57]
XuQ, TangC, WangX, SunS, ZhaoJ, KangZ, WangX. An effector protein of the wheat stripe rust fungus targets chloroplasts and suppresses chloroplast function. Nat Commun, 2019, 10(1):5571
CrossRef Google scholar
[58]
XuX, CrowM, RiceBR, LiF, HarrisB, LiuL, Demesa-ArevaloE, LuZ, WangL, FoxN, WangX, DrenkowJ, LuoA, CharSN, YangB, SylvesterAW, GingerasTR, SchmitzRJ, WareD, LipkaAE, JacksonD. Single-cell RNA sequencing of developing maize ears facilitates functional analysis and trait candidate gene discovery. Dev Cell, 2021, 56(4):557-568.e6
CrossRef Google scholar
[59]
YadavIS, SharmaA, KaurS, NaharN, BhardwajSC, SharmaTR, ChhunejaP. Comparative temporal transcriptome profiling of wheat near isogenic line carrying Lr57 under compatible and incompatible interactions. Front Plant Sci, 2016, 7: 1943
CrossRef Google scholar
[60]
Yin S, Gao Z, Wang C, Huang L, Kang Z, Zhang H (2016) Nitric oxide and reactive oxygen species coordinately regulate the germination of Puccinia striiformis f. sp. tritici urediniospores. Frontiers in microbiology 7:178. https://doi.org/10.3389/fmicb.2016.00178
[61]
YoungMD, WakefieldMJ, SmythGK, OshlackA. Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol, 2010, 11(2):R14
CrossRef Google scholar
[62]
Yuan M, Ngou BPM, Ding P, Xin XF (2021) PTI-ETI crosstalk: an integrative view of plant immunity. Current opinion in plant biology 62:102030. https://doi.org/10.1016/j.pbi.2021.102030
[63]
Zeng QD (2016) The BAC library construction and transcriptome analysis of wheat material which carry Yr26 gene. Ph.D. Thesis, Northwest A&F University, China.
[64]
ZhangH, QiuY, YuanC, ChenX, HuangL. Fine-tuning of PR genes in wheat responding to different puccinia rust species. Biology, 2018
CrossRef Google scholar
[65]
Zhu X, Li X, He Q, Guo D, Liu C, Cao J, Wu Z, Kang Z, Wang X (2021) TaMYB29: A novel R2R3-MYB transcription factor involved in wheat defense against stripe rust. Frontiers in plant science 12:783388. https://doi.org/10.3389/fpls.2021.783388
Funding
National Key R&D Program of China(2021YFD1401000); National Natural Science Foundation of China(32172424); 111 Project from the Ministry of Education of China(BP0719026)

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