Exploiting plant immune “switches” for resistance engineering

Bangting Wu , Kaichen Xu , Anum Bashir , Xinyu Han , Qiping Sun , Peng Sun , Guan-Feng Wang , Ricky J. Milne , Meixiang Zhang , Leiyun Yang , Guoyong Xu , Guotian Li

Stress Biology ›› 2026, Vol. 6 ›› Issue (1) : 32

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Stress Biology ›› 2026, Vol. 6 ›› Issue (1) :32 DOI: 10.1007/s44154-026-00306-4
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Exploiting plant immune “switches” for resistance engineering
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Abstract

Plant diseases, caused by various pathogens, pose a serious threat to sustainable agriculture. Plants have evolved a sophisticated immune system to detect and mount effective responses against pathogens. The plant immune system contains numerous programmable immune "switches" that safeguard plants against pathogens while minimizing energy consumption in the absence of pathogens. The cloning of disease-resistance (R) genes, along with the elucidation of the molecular mechanisms regulating these immune "switches", has provided resources and strategies for genetic engineering of novel disease resistance. This review focuses on the resistance engineering through the manipulation of immune “switches”. It begins by summarizing recent advances in plant immunity, then explores the mechanisms behind plant immune "switches", and finally discusses potential strategies for engineering immune genes via these "switches". These strategies include engineering promoters to confer precise spatiotemporal regulation at the transcriptional level; engineering mRNA or its regulatory elements to facilitate specific and stable translation of R proteins at the post-transcriptional and translational levels; and engineering proteins at the post-translational level to broaden the pathogen-recognition spectrum of R proteins. Collectively, these strategies will accelerate the development of disease-resistant crop cultivars, thereby enhancing agricultural productivity and global food security.

Keywords

Immune “switches” / Resistance engineering / Engineering promoters / Engineering mRNA / Engineering proteins

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Bangting Wu, Kaichen Xu, Anum Bashir, Xinyu Han, Qiping Sun, Peng Sun, Guan-Feng Wang, Ricky J. Milne, Meixiang Zhang, Leiyun Yang, Guoyong Xu, Guotian Li. Exploiting plant immune “switches” for resistance engineering. Stress Biology, 2026, 6(1): 32 DOI:10.1007/s44154-026-00306-4

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References

[1]

Abramson J, Adler J, Dunger J, Evans R, Green T, Pritzel A, Ronneberger O, Willmore L, Ballard AJ, Bambrick J, Bodenstein SW, Evans DA, Hung CC, O'Neill M, Reiman D, Tunyasuvunakool K, Wu Z, Žemgulytė A, Arvaniti E, Beattie C, Bertolli O, Bridgland A, Cherepanov A, Congreve M, Cowen-Rivers AI, Cowie A, Figurnov M, Fuchs FB, Gladman H, Jain R, Khan YA, Low CMR, Perlin K, Potapenko A, Savy P, Singh S, Stecula A, Thillaisundaram A, Tong C, Yakneen S, Zhong ED, Zielinski M, Žídek A, Bapst V, Kohli P, Jaderberg M, Hassabis D, Jumper JM. Accurate structure prediction of biomolecular interactions with AlphaFold 3. Nature, 2024, 630: 493-500

[2]

Akimoto K, Katakami H, Kim HJ, Ogawa E, Sano CM, Wada Y, Sano H. Epigenetic inheritance in rice plants. Ann Bot, 2007, 100: 205-217

[3]

Bennett NR, Watson JL, Ragotte RJ, Borst AJ, See DL, Weidle C, Biswas R, Yu Y, Shrock EL, Ault R, Leung PJY, Huang B, Goreshnik I, Tam J, Carr KD, Singer B, Criswell C, Wicky BIM, Vafeados D, Garcia Sanchez M, Kim HM, Vázquez Torres S, Chan S, Sun SM, Spear TT, Sun Y, O’Reilly K, Maris JM, Sgourakis NG, Melnyk RA, Liu CC, Baker D. Atomically accurate de novo design of antibodies with RFdiffusion. Nature, 2025, 649: 183-193

[4]

Bethke G, Thao A, Xiong G, Li B, Soltis NE, Hatsugai N, Hillmer RA, Katagiri F, Kliebenstein DJ, Pauly M, Glazebrook J. Pectin biosynthesis is critical for cell wall integrity and immunity in Arabidopsis thaliana. Plant Cell, 2016, 28: 537-556

[5]

Borowsky AT, Bailey-Serres J. Rewiring gene circuitry for plant improvement. Nat Genet, 2024, 56: 1574-1582

[6]

Cai Q, Qiao L, Wang M, He B, Lin FM, Palmquist J, Huang SD, Jin H. Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes. Science, 2018, 360: 1126-1129

[7]

Campo S, Peris-Peris C, Siré C, Moreno AB, Donaire L, Zytnicki M, Notredame C, Llave C, San Segundo B. Identification of a novel microRNA (miRNA) from rice that targets an alternatively spliced transcript of the Nramp6 (Natural resistance-associated macrophage protein 6) gene involved in pathogen resistance. New Phytol, 2013, 199: 212-227

[8]

Cao L, Karapetyan S, Yoo H, Chen T, Mwimba M, Zhang X, Dong X. H2O2 sulfenylates CHE, linking local infection to the establishment of systemic acquired resistance. Science, 2024, 385: 1211-1217

[9]

Cesari S, Thilliez G, Ribot C, Chalvon V, Michel C, Jauneau A, Rivas S, Alaux L, Kanzaki H, Okuyama Y, Morel JB, Fournier E, Tharreau D, Terauchi R, Kroj T. The rice resistance protein pair RGA4/RGA5 recognizes the Magnaporthe oryzae effectors AVR-Pia and AVR1-CO39 by direct binding. Plant Cell, 2013, 25: 1463-1481

[10]

Chen X, Liu P, Mei L, He X, Chen L, Liu H, Shen S, Ji Z, Zheng X, Zhang Y, Gao Z, Zeng D, Qian Q, Ma B. Xa7, a new executor R gene that confers durable and broad-spectrum resistance to bacterial blight disease in rice. Plant Commun, 2021, 2 100143

[11]

Chen T, Xu G, Mou R, Greene GH, Liu L, Motley J, Dong X. Global translational induction during NLR-mediated immunity in plants is dynamically regulated by CDC123, an ATP-sensitive protein. Cell Host Microbe, 2023, 31: 334-342.e5

[12]

Chen C, Imran M, Feng X, Shen X, Sun Z. Spray-induced gene silencing for crop protection: recent advances and emerging trends. Front Plant Sci, 2025, 16 1527944

[13]

Chen X, Yao X, Yan F, Li S, Wang ZD, Yin FY, Zhou M, Wang Z, Qin L, Zhao B, Lu K, Zhang L, Li X, Mu X, Zhang Y, Lu T, Ma JB, Zhao YK, Lin D, Wang M, Li Q, Qi S, Long J, Bai B, Ma JY, Liu Y, Feng Y, Yang XB, Zhang J, Xu Y, Chen L, Zou S, Ding X, Zhang MX, Yang DL, Cheng Z, Zhou H, Dong H. Alternative splicing of OsNPR3 promoted by the bacterial TAL effectors-targeted splicing regulator OsRBP11 antagonizes OsNPR1 function and enhances disease susceptibility in rice. Mol Plant, 2025, 18: 1505-1525

[14]

Cui Y, Qian H, Yin J, Xu C, Luo P, Zhang X, Yu M, Su B, Li X, Lin J. Single-molecule analysis reveals the phosphorylation of FLS2 governs its spatiotemporal dynamics and immunity. Elife, 2024, 12 RP91072

[15]

De la Concepcion JC, Franceschetti M, MacLean D, Terauchi R, Kamoun S, Banfield MJ. Protein engineering expands the effector recognition profile of a rice NLR immune receptor. Elife, 2019, 8 e47713

[16]

De la Concepcion JC, Vega Benjumea J, Bialas A, Terauchi R, Kamoun S, Banfield MJ. Functional diversification gave rise to allelic specialization in a rice NLR immune receptor pair. Elife, 2021, 10 e71662

[17]

Deng Y, Zhai K, Xie Z, Yang D, Zhu X, Liu J, Wang X, Qin P, Yang Y, Zhang G, Li Q, Zhang J, Wu S, Milazzo J, Mao B, Wang E, Xie H, Tharreau D, He Z. Epigenetic regulation of antagonistic receptors confers rice blast resistance with yield balance. Science, 2017, 355: 962-965

[18]

Dinesh-Kumar SP, Baker BJ. Alternatively spliced N resistance gene transcripts: their possible role in tobacco mosaic virus resistance. Proc Natl Acad Sci U S A, 2000, 97: 1908-1913

[19]

Fan X, Zhao Y, Ji W, Rodamilans B, Simón-Mateo C, García JA, Wu X, Wu X, Cheng X. A pathogen protease-activated molecular decoy for customized resistance in plant. Plant Biotechnol J, 2025, 23: 2403-2405

[20]

Feng Q, Wang H, Yang XM, Hu ZW, Zhou XH, Xiang L, Xiong XY, He XR, Zhu Y, Li GB, Zhao JH, Ji YP, Hu XH, Pu M, Zhou SX, Zhao ZX, Zhang JW, Huang YY, Fan J, Wang WM, Li Y. Osa-miR160a confers broad-spectrum resistance to fungal and bacterial pathogens in rice. New Phytol, 2022, 236: 2216-2232

[21]

Förderer A, Li E, Lawson AW, Deng YN, Sun Y, Logemann E, Zhang X, Wen J, Han Z, Chang J, Chen Y, Schulze-Lefert P, Chai J. A wheat resistosome defines common principles of immune receptor channels. Nature, 2022, 610: 532-539

[22]

Fu ZQ, Dong X. Systemic acquired resistance: turning local infection into global defense. Annu Rev Plant Biol, 2013, 64: 839-863

[23]

García-Murillo L, Valencia-Lozano E, Priego-Ranero NA, Cabrera-Ponce JL, Duarte-Aké FP, Vizuet-de-Rueda JC, Rivera-Toro DM, Herrera-Ubaldo H, de Folter S, Alvarez-Venegas R. CRISPRa-mediated transcriptional activation of the SlPR-1 gene in edited tomato plants. Plant Sci, 2023, 329 111617

[24]

Gauthier MA, Shand K, Hayashi S, Waterhouse PM, Barrero RA, de Felippes FF. MicroRNA-induced gene silencing (MIGS): a tool for multi-gene silencing and targeting viruses in plants. Plant Biotechnol J, 2025,

[25]

Geng X, Jin L, Shimada M, Kim MG, Mackey D. The phytotoxin coronatine is a multifunctional component of the virulence armament of Pseudomonas syringae. Planta, 2014, 240: 1149-1165

[26]

Glasscock CJ, Pecoraro R, McHugh R, Doyle LA, Chen W, Boivin O, Lonnquist B, Na E, Politanska Y, Haddox HK, Cox D, Norn C, Coventry B, Goreshnik I, Vafeados D, Lee GR, Gordan R, Stoddard BL, DiMaio F, Baker D. Computational design of sequence-specific DNA-binding proteins. Nat Struct Mol Biol, 2023, 32: 2252-2261

[27]

Gong Z, Morales-Ruiz T, Ariza RR, Roldán-Arjona T, David L, Zhu JK. ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase. Cell, 2002, 111: 803-814

[28]

Gou M, Huang Q, Qian W, Zhang Z, Jia Z, Hua J. Sumoylation E3 ligase SIZ1 modulates plant immunity partly through the immune receptor gene SNC1 in Arabidopsis. Mol Plant Microbe Interact, 2017, 30: 334-342

[29]

Gu K, Yang B, Tian D, Wu L, Wang D, Sreekala C, Yang F, Chu Z, Wang GL, White FF, Yin Z. R gene expression induced by a type-III effector triggers disease resistance in rice. Nature, 2005, 435: 1122-1125

[30]

Halterman DA, Wei F, Wise RP. Powdery mildew-induced Mla mRNAs are alternatively spliced and contain multiple upstream open reading frames. Plant Physiol, 2003, 131: 558-567

[31]

Han X, Li S, Zeng Q, Sun P, Wu D, Wu J, Yu X, Lai Z, Milne RJ, Kang Z. Genetic engineering, including genome editing, for enhancing broad-spectrum disease resistance in crops. Plant Commun, 2025, 6 101195

[32]

Han X, Yang L, Xia F, Sun P, Guo Z, Chen T, Sha G, Lin L, Wang Y, Kong X, Bashir A, Chen G, Li K, Sun Q, Xiao Y, Hsiang T, Xie W, Li Q, Xie K, Li G. Rational design of promoter editing confers multipathogen resistance in rice. Genome Biol, 2025, 26 371

[33]

Hannan Parker A, Wilkinson SW, Ton J. Epigenetics: a catalyst of plant immunity against pathogens. New Phytol, 2022, 233: 66-83

[34]

Homma F, Huang J, van der Hoorn RAL. AlphaFold-Multimer predicts cross-kingdom interactions at the plant-pathogen interface. Nat Commun, 2023, 14 6040

[35]

Hossain MM, Sultana F, Mostafa M, Ferdus H, Rahman M, Rana JA, Islam SS, Adhikary S, Sannal A, Al Emran Hosen M, Nayeema J, Emu NJ, Kundu M, Biswas SK, Farzana L, Al Sabbir MA. Plant disease dynamics in a changing climate: impacts, molecular mechanisms, and climate-informed strategies for sustainable management. Discov Agric, 2024, 2 132

[36]

Hou M, Xu G. Growth-defense trade-off in plants: from hypothesis to principle to paradigm. Cell Host Microbe, 2025, 33: 1222-1226

[37]

Howard AJ, Rim EY, Garrett OD, Shim Y, Notwell JH, Ronald PC. Combining directed evolution with machine learning enables accurate genotype-to-phenotype predictions. bioRxiv, 2025,

[38]

Hu J, Jiang J, Wang N. Control of citrus Huanglongbing via trunk injection of plant defense activators and antibiotics. Phytopathology, 2018, 108: 186-195

[39]

Hu R, Pi Q, Yang M, Song W, Jiang Z, Zhong C, Han H, Han CG, Zhang Y, Li D. Cleavage of Beclin 1 by metacaspase 1 activates antiviral autophagy in plants. Mol Plant, 2025, 19: 48-65

[40]

Huang S, Jia A, Ma S, Sun Y, Chang X, Han Z, Chai J. NLR signaling in plants: from resistosomes to second messengers. Trends Biochem Sci, 2023, 48: 776-787

[41]

Janjusevic R, Abramovitch RB, Martin GB, Stebbins CE. A bacterial inhibitor of host programmed cell death defenses is an E3 ubiquitin ligase. Science, 2006, 311: 222-226

[42]

Jia F, Xiao Y, Feng Y, Yan J, Fan M, Sun Y, Huang S, Li W, Zhao T, Han Z, Hou S, Chai J. N-glycosylation facilitates the activation of a plant cell-surface receptor. Nat Plants, 2024, 10: 2014-2026

[43]

Kadota Y, Sklenar J, Derbyshire P, Stransfeld L, Asai S, Ntoukakis V, Jones JD, Shirasu K, Menke F, Jones A, Zipfel C. Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol Cell, 2014, 54: 43-55

[44]

Kang H, Fan T, Wu J, Zhu Y, Shen WH. Histone modification and chromatin remodeling in plant response to pathogens. Front Plant Sci, 2022, 13 986940

[45]

Kauder F, Gyetvai G, Schmidt K, Stirnweis D, Haehre T, Prenzler K, Maeser A, Klapprodt C, Tiller F, Lübeck J, Stahl DJ. Expression of a modified Avr3a gene under the control of a synthetic pathogen-inducible promoter leads to Phytophthora infestans resistance in potato. Plant Biotechnol J, 2025, 23: 1683-1701

[46]

Khan MA, Herring G, Zhu JY, Oliva M, Fourie E, Johnston B, Zhang Z, Potter J, Pineda L, Pflueger J, Swain T, Pflueger C, Lloyd JPB, Secco D, Small I, Kidd BN, Lister R. CRISPRi-based circuits to control gene expression in plants. Nat Biotechnol, 2025, 43: 416-430

[47]

Kim JG, Stork W, Mudgett MB. Xanthomonas type III effector XopD desumoylates tomato transcription factor SlERF4 to suppress ethylene responses and promote pathogen growth. Cell Host Microbe, 2013, 13: 143-154

[48]

Kim SH, Qi D, Ashfield T, Helm M, Innes RW. Using decoys to expand the recognition specificity of a plant disease resistance protein. Science, 2016, 351: 684-687

[49]

Kimura S, Kaya H, Kawarazaki T, Hiraoka G, Senzaki E, Michikawa M, Kuchitsu K. Protein phosphorylation is a prerequisite for the Ca2+-dependent activation of Arabidopsis NADPH oxidases and may function as a trigger for the positive feedback regulation of Ca2+ and reactive oxygen species. Biochim Biophys Acta, 2012, 1823: 398-405

[50]

Kong Q, Sun T, Qu N, Ma J, Li M, Cheng YT, Zhang Q, Wu D, Zhang Z, Zhang Y. Two redundant receptor-like cytoplasmic kinases function downstream of pattern recognition receptors to regulate activation of SA biosynthesis. Plant Physiol, 2016, 171: 1344-1354

[51]

Kong L, Qiu X, Kang J, Wang Y, Chen H, Huang J, Qiu M, Zhao Y, Kong G, Ma Z, Wang Y, Ye W, Dong S, Ma W, Wang Y. A Phytophthora effector manipulates host histone acetylation and reprograms defense gene expression to promote infection. Curr Biol, 2017, 27: 981-991

[52]

Kourelis J, Marchal C, Posbeyikian A, Harant A, Kamoun S. NLR immune receptor-nanobody fusions confer plant disease resistance. Science, 2023, 379: 934-939

[53]

Li Y, Xia Q, Kou H, Wang D, Lin X, Wu Y, Xu C, Xing S, Liu B. Induced Pib expression and resistance to Magnaporthe grisea are compromised by cytosine demethylation at critical promoter regions in rice. J Integr Plant Biol, 2011, 53: 814-823

[54]

Li T, Liu B, Spalding MH, Weeks DP, Yang B. High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat Biotechnol, 2012, 30: 390-392

[55]

Li L, Li M, Yu L, Zhou Z, Liang X, Liu Z, Cai G, Gao L, Zhang X, Wang Y, Chen S, Zhou JM. The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host Microbe, 2014, 15: 329-338

[56]

Li Y, Li TT, He XR, Zhu Y, Feng Q, Yang XM, Zhou XH, Li GB, Ji YP, Zhao JH, Zhao ZX, Pu M, Zhou SX, Zhang JW, Huang YY, Fan J, Wang WM. Blocking Osa-miR1871 enhances rice resistance against Magnaporthe oryzae and yield. Plant Biotechnol J, 2022, 20: 646-659

[57]

Li X, Niu G, Fan Y, Liu W, Wu Q, Yu C, Wang J, Xiao Y, Hou L, Jin D, Chen S, Hu R, Yang Y, Pei Y. Synthetic dual hormone-responsive promoters enable engineering of plants with broad-spectrum resistance. Plant Commun, 2023, 4 100596

[58]

Li C, Wu J, Fu S, Xu Y, Wang Y, Yang X, Lan Y, Lin F, Du L, Zhou T, Zhou X. Development of a transgenic rice line with strong and broad resistance against four devastating rice viruses through expressing a single hairpin RNA construct. Plant Biotechnol J, 2024, 22: 2142-2144

[59]

Li T, Xu H, Teng S, Suo M, Bahitwa R, Xu M, Qian Y, Ramstein GP, Song B, Buckler ES, Wang H. Modeling 0.6 million genes for the rational design of functional cis-regulatory variants and de novo design of cis-regulatory sequences. Proc Natl Acad Sci U S A, 2024, 121 e2319811121

[60]

Li W, Liu W, Xu Z, Zhu C, Han D, Liao J, Li K, Tang X, Xie Q, Yang C, Lai J. Heat-induced SUMOylation differentially affects bacterial effectors in plant cells. Plant Cell, 2024, 36: 2103-2116

[61]

Li G, An L, Yang W, Yang L, Wei T, Shi J, Wang J, Doonan JH, Xie K, Fernie AR, Lagudah ES, Wing RA, Gao C. Integrated biotechnological and AI innovations for crop improvement. Nature, 2025, 643: 925-937

[62]

Li T, Jarquin Bolaños E, Stevens DM, Sha H, Prigozhin DM, Coaker G. Unlocking expanded flagellin perception through rational receptor engineering. Nat Plants, 2025, 11: 1628-1641

[63]

Liang L, Jiang Y, Zhao P, Wang H, Chen X, Lin X, Sun Y, Zhang W, Fang R, Ye J. Cleavage of Bcl-2-associated athanogene by metacaspase determines plant antiviral immunity. Nat Commun, 2025, 16 9102

[64]

Lim YJ, Yoon YJ, Lee H, Choi G, Kim S, Ko J, Kim JH, Kim KT, Lee YH. Nuclear localization sequence of MoHTR1, a Magnaporthe oryzae effector, for transcriptional reprogramming of immunity genes in rice. Nat Commun, 2024, 15 9764

[65]

Lu X, An Y, Lu W, Li J, Xiong Q, Zhu M, He Y, Yang J, Wang Y, Zhang Z, Gong X, Qian Y, Yu W, Shao Y, Zhou H, Chen X, Tang H, Hou Q, Shi H, Yin J, Tang Y, Zhu X, Zhou Y, Song L, Wang L, He M, Li W, Wang J, Chen X. Pathogen-induced H2O2 triggers phosphorylation of the RNA-binding protein RRM2R to suppress intron intention of OsMAPKKK18 for orchestrating immunity and growth in rice. Mol Plant, 2025, 19: 116-133

[66]

Luo M, Zhu S, Dang H, Wen Q, Niu R, Long J, Wang Z, Tong Y, Ning Y, Yuan M, Xu G. Genetically-encoded targeted protein degradation technology to remove endogenous condensation-prone proteins and improve crop performance. Nat Commun, 2025, 16 1159

[67]

Mao Y, Botella JR, Liu Y, Zhu JK. Gene editing in plants: progress and challenges. Natl Sci Rev, 2019, 6: 421-437

[68]

Maximiano MR, de Sousa LJ, Feitosa GC, Lopes MEM, Ortega B, Madeiro RDS, Távora F, Pereira BM, Brilhante de Oliveira Neto O, Ulhôa CJ, Brasileiro ACM, Aragão FJL, Mehta A, Franco OL. Unlocking nature's shield: the promising potential of CRISPRa in amplifying antimicrobial peptide expression in common bean (Phaseolus vulgaris L.). ACS Omega, 2025, 10: 5909-5918

[69]

McLaughlin JE, KueFoka IC, Lawton MA, Di R. CRISPR activation: identifying and using novel genes for plant disease resistance breeding. Frontiers in Genome Editing, 2025, 7 1596600

[70]

Motion GB, Amaro TM, Kulagina N, Huitema E. Nuclear processes associated with plant immunity and pathogen susceptibility. Brief Funct Genomics, 2015, 14: 243-252

[71]

Mou R, Niu R, Yang R, Xu G. Engineering crop performance with upstream open reading frames. Trends Plant Sci, 2025, 30: 311-323

[72]

Ngou BPM, Ahn HK, Ding P, Jones JDG. Mutual potentiation of plant immunity by cell-surface and intracellular receptors. Nature, 2021, 592: 110-115

[73]

Ngou BPM, Wyler M, Schmid MW, Suzuki T, Albert M, Dohmae N, Kadota Y, Shirasu K. Systematic discovery and engineering of synthetic immune receptors in plants. Science, 2025, 389 eadx2508

[74]

Nishimura K, Fukagawa T, Takisawa H, Kakimoto T, Kanemaki M. An auxin-based degron system for the rapid depletion of proteins in nonplant cells. Nat Methods, 2009, 6: 917-922

[75]

Niu R, Luo M, Wen Q, Xiong Y, Dang H, Xu G. Targeted protein and protein-condensate degradation in plant science research and crop breeding. Mol Plant, 2025, 18: 1270-1283

[76]

Nobori T, Monell A, Lee TA, Sakata Y, Shirahama S, Zhou J, Nery JR, Mine A, Ecker JR. A rare PRIMER cell state in plant immunity. Nature, 2025, 638: 197-205

[77]

Nowara D, Gay A, Lacomme C, Shaw J, Ridout C, Douchkov D, Hensel G, Kumlehn J, Schweizer P. HIGS: host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis. Plant Cell, 2010, 22: 3130-3141

[78]

Oliva R, Ji C, Atienza-Grande G, Huguet-Tapia JC, Perez-Quintero A, Li T, Eom JS, Li C, Nguyen H, Liu B, Auguy F, Sciallano C, Luu VT, Dossa GS, Cunnac S, Schmidt SM, Slamet-Loedin IH, Vera Cruz C, Szurek B, Frommer WB, White FF, Yang B. Broad-spectrum resistance to bacterial blight in rice using genome editing. Nat Biotechnol, 2019, 37: 1344-1350

[79]

Orosa B, Yates G, Verma V, Srivastava AK, Srivastava M, Campanaro A, De Vega D, Fernandes A, Zhang C, Lee J, Bennett MJ, Sadanandom A. SUMO conjugation to the pattern recognition receptor FLS2 triggers intracellular signalling in plant innate immunity. Nat Commun, 2018, 9 5185

[80]

Pel MJ, van Dijken AJ, Bardoel BW, Seidl MF, van der Ent S, van Strijp JA, Pieterse CM. Pseudomonas syringae evades host immunity by degrading flagellin monomers with alkaline protease AprA. Mol Plant Microbe Interact, 2014, 27: 603-610

[81]

Peng A, Chen S, Lei T, Xu L, He Y, Wu L, Yao L, Zou X. Engineering canker-resistant plants through CRISPR/Cas9-targeted editing of the susceptibility gene CsLOB1 promoter in citrus. Plant Biotechnol J, 2017, 15: 1509-1519

[82]

Pi Q, Hu R, Yue N, Jiang Z, Wei J, Chen Y, Yang M, Song W, Zhang Y, Wang J, Li D. The MC4-La1 cleavage module restricts plant virus infection by integrating R-motif-mediated defense mRNA translation. Sci Adv, 2025, 11 eadv0819

[83]

Pretorius ZA, Singh RP, Wagoire WW, Payne TS. Detection of virulence to wheat stem rust resistance gene Sr31 in Puccinia graminis. f. sp. tritici in Uganda. Plant Dis, 2000, 84: 203

[84]

Qiu J, Cao X, Shi H, Chen Z, Zhang X, Cao Z, Huang D, Wen H, Chen Y, Kou Y. miR444b.2-HsfA1-AOC1module mediates heat priming-enhanced blast resistance in rice. Proc Natl Acad Sci U S A, 2025, 122 e2505764122

[85]

Qu J, Kang SG, Wang W, Musier-Forsyth K, Jang JC. The Arabidopsis thaliana tandem zinc finger 1 (AtTZF1) protein in RNA binding and decay. Plant J, 2014, 78: 452-467

[86]

Richard MMS, Gratias A, Thareau V, Kim KD, Balzergue S, Joets J, Jackson SA, Geffroy V. Genomic and epigenomic immunity in common bean: the unusual features of NB-LRR gene family. DNA Res, 2018, 25: 161-172

[87]

Roden J, Eardley L, Hotson A, Cao Y, Mudgett MB. Characterization of the Xanthomonas AvrXv4 effector, a SUMO protease translocated into plant cells. Mol Plant Microbe Interact, 2004, 17: 633-643

[88]

Römer P, Jordan T, Lahaye T. Identification and application of a DNA-based marker that is diagnostic for the pepper (Capsicum annuum) bacterial spot resistance gene Bs3. Plant Breed, 2010, 129: 737-740

[89]

Sánchez-Martín J, Widrig V, Herren G, Wicker T, Zbinden H, Gronnier J, Spörri L, Praz CR, Heuberger M, Kolodziej MC, Isaksson J, Steuernagel B, Karafiátová M, Doležel J, Zipfel C, Keller B. Wheat Pm4 resistance to powdery mildew is controlled by alternative splice variants encoding chimeric proteins. Nat Plants, 2021, 7: 327-341

[90]

Sha G, Sun P, Kong X, Han X, Sun Q, Fouillen L, Zhao J, Li Y, Yang L, Wang Y, Gong Q, Zhou Y, Zhou W, Jain R, Gao J, Huang R, Chen X, Zheng L, Zhang W, Qin Z, Zhou Q, Zeng Q, Xie K, Xu J, Chiu TY, Guo L, Mortimer JC, Boutté Y, Li Q, Kang Z, Ronald PC, Li G. Genome editing of a rice CDP-DAG synthase confers multipathogen resistance. Nature, 2023, 618: 1017-1023

[91]

Shao F, Golstein C, Ade J, Stoutemyer M, Dixon JE, Innes RW. Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science, 2003, 301: 1230-1233

[92]

Song T, Ma Z, Shen D, Li Q, Li W, Su L, Ye T, Zhang M, Wang Y, Dou D. An oomycete CRN effector reprograms expression of plant HSP genes by targeting their promoters. PLoS Pathog, 2015, 11 e1005348

[93]

Sun Y, Zhu YX, Balint-Kurti PJ, Wang GF. Fine-tuning immunity: players and regulators for plant NLRs. Trends Plant Sci, 2020, 25: 695-713

[94]

Sun B, Huang J, Kong L, Gao C, Zhao F, Shen J, Wang T, Li K, Wang L, Wang Y, Halterman DA, Dong S. Alternative splicing of a potato disease resistance gene maintains homeostasis between growth and immunity. Plant Cell, 2024, 36: 3729-3750

[95]

Tamborski J, Seong K, Liu F, Staskawicz B, Krasileva KV. Altering specificity and autoactivity of plant immune receptors Sr33 and Sr50 via a rational engineering approach. Mol Plant Microbe Interact, 2023, 36: 434-446

[96]

Tan X, Meyers BC, Kozik A, West MA, Morgante M, St Clair DA, Bent AF, Michelmore RW. Global expression analysis of nucleotide binding site-leucine rich repeat-encoding and related genes in Arabidopsis. BMC Plant Biol, 2007, 7 56

[97]

Tang Z, Shi S, Niu R, Zhou Y, Wang Z, Fu R, Mou R, Chen S, Ding P, Xu G. Alleviating protein-condensation-associated damage at the endoplasmic reticulum enhances plant disease tolerance. Cell Host Microbe, 2024, 32: 1552-1565.e8

[98]

Tang Z, Mou R, Xu G. Defense strategies for plant health: disease resistance and tolerance. Plant Cell, 2025, 37 koaf186

[99]

Tang Z, Shi S, Du X, Xu G. Plant defense strategies: the dual armor of disease resistance and tolerance. New Plant Protection, 2025, 2 e70022

[100]

Thomazella DPT, Seong K, Mackelprang R, Dahlbeck D, Geng Y, Gill US, Qi T, Pham J, Giuseppe P, Lee CY, Ortega A, Cho MJ, Hutton SF, Staskawicz B. Loss of function of a DMR6 ortholog in tomato confers broad-spectrum disease resistance. Proc Natl Acad Sci U S A, 2021, 118 e2026152118

[101]

Tian D, Wang J, Zeng X, Gu K, Qiu C, Yang X, Zhou Z, Goh M, Luo Y, Murata-Hori M, White FF, Yin Z. The rice TAL effector-dependent resistance protein XA10 triggers cell death and calcium depletion in the endoplasmic reticulum. Plant Cell, 2014, 26: 497-515

[102]

Tian J, Tang Z, Niu R, Zhou Y, Yang D, Chen D, Luo M, Mou R, Yuan M, Xu G. Engineering disease-resistant plants with alternative translation efficiency by switching uORF types through CRISPR. Sci China Life Sci, 2024, 67: 1715-1726

[103]

Tian J, Liu Y, Chen D, Xu G, Yuan M. Modifying the TL1-BINDING FACTOR upstream open reading frame coordinates plant growth and defense in rice. Plant Physiol, 2025, 197 kiaf047

[104]

Tsuchiya T, Eulgem T. An alternative polyadenylation mechanism coopted to the Arabidopsis RPP7 gene through intronic retrotransposon domestication. Proc Natl Acad Sci U S A, 2013, 110: E3535-E3543

[105]

Uchański T, Masiulis S, Fischer B, Kalichuk V, López-Sánchez U, Zarkadas E, Weckener M, Sente A, Ward P, Wohlkönig A, Zögg T, Remaut H, Naismith JH, Nury H, Vranken W, Aricescu AR, Pardon E, Steyaert J. Megabodies expand the nanobody toolkit for protein structure determination by single-particle cryo-EM. Nat Methods, 2021, 18: 60-68

[106]

Wang C, Zhang X, Fan Y, Gao Y, Zhu Q, Zheng C, Qin T, Li Y, Che J, Zhang M, Yang B, Liu Y, Zhao K. XA23 is an executor R protein and confers broad-spectrum disease resistance in rice. Mol Plant, 2014, 8: 290-302

[107]

Wang Y, Cheng X, Shan Q, Zhang Y, Liu J, Gao C, Qiu JL. Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotechnol, 2014, 32: 947-951

[108]

Wang Q, He G, Hou M, Chen L, Chen S, Xu A, Fu Y. Cell cycle regulation by alternative polyadenylation of CCND1. Sci Rep, 2018, 8: 6824

[109]

Wang J, Hu M, Wang J, Qi J, Han Z, Wang G, Qi Y, Wang HW, Zhou JM, Chai J. Reconstitution and structure of a plant NLR resistosome conferring immunity. Science, 2019, 364 eaav5870

[110]

Wang H, Li Y, Chern M, Zhu Y, Zhang LL, Lu JH, Li XP, Dang WQ, Ma XC, Yang ZR, Yao SZ, Zhao ZX, Fan J, Huang YY, Zhang JW, Pu M, Wang J, He M, Li WT, Chen XW, Wu XJ, Li SG, Li P, Li Y, Ronald PC, Wang WM. Suppression of rice miR168 improves yield, flowering time and immunity. Nat Plants, 2021, 7: 129-136

[111]

Wang J, Zhang X, Greene GH, Xu G, Dong X. PABP/purine-rich motif as an initiation module for cap-independent translation in pattern-triggered immunity. Cell, 2022, 185: 3186-3200.e17

[112]

Wang W, Qin L, Zhang W, Tang L, Zhang C, Dong X, Miao P, Shen M, Du H, Cheng H, Wang K, Zhang X, Su M, Lu H, Li C, Gao Q, Zhang X, Huang Y, Liang C, Zhou J-M, Chen Y-h. WeiTsing, a pericycle-expressed ion channel, safeguards the stele to confer clubroot resistance. Cell, 2023, 186: 2656-2671.e18

[113]

Wang M, Li S, Li H, Song C, Xie W, Zuo S, Zhou X, Zhou C, Ji Z, Zhou H. Genome editing of a dominant resistance gene for broad-spectrum resistance to bacterial diseases in rice without growth penalty. Plant Biotechnol J, 2024, 22: 529-531

[114]

Wang H, Xiang Y, Liu Z, Yin W, Li B, Qian L, Wang X, Lou C. De novo design of insulated cis-regulatory elements based on deep learning-predicted fitness landscape. Nucleic Acids Res, 2025, 53 gkaf611

[115]

Wang J, Shen T, Song M, Fan J, Li Y, Chin TZ, Yu Y, Huang F, Yang X, Li C, Zhou X, Li C, Hong Y, Liu Y. Engineering resistance genes against tomato brown rugose fruit virus. Sci China Life Sci, 2025, 68: 3392-3400

[116]

Wang J, Chen T, Zhang Z, Song M, Shen T, Wang X, Zheng X, Wang Y, Song K, Ge X, Xu K, Qi T, Li F, Hong Y, Liu Y. Remodelling autoactive NLRs for broad-spectrum immunity in plants. Nature, 2025, 645: 737-745

[117]

Wang L, Li H, Ke Y, Zhu P, Li Y, Wang P, Liu H, Li Y, Chen J, Zhou S, Wan L, Dinesh-Kumar SP, Dong S, Huang S. Plug-in strategy for resistance engineering inspired by potato NLRome. Nature, 2025, 649: 396-405

[118]

Wang X, Le BH, Xu Y, Sun P, Qiu M, Zhao Y, Li L, Wang M, Rogers K, Yu Y, Zhang Z, Shou H, Ma W, Chen X. Soybean RNA polymerases IV and V repress defense response genes and plant immunity. Plant Cell, 2026,

[119]

Wasdin PT, Johnson NV, Janke AK, Held S, Marinov TM, Jordaan G, Gillespie RA, Vandenabeele L, Pantouli F, Powers OC, Vukovich MJ, Holt CM, Kim J, Hansman G, Logue J, Chu HY, Andrews SF, Kanekiyo M, Sautto GA, Ross TM, Sheward DJ, McLellan JS, Abu-Shmais AA, Georgiev IS. Generation of antigen-specific paired-chain antibodies using large language models. Cell, 2025, 188: 7206-7221

[120]

Wei LH, Song P, Wang Y, Lu Z, Tang Q, Yu Q, Xiao Y, Zhang X, Duan HC, Jia G. The m6A reader ECT2 controls trichome morphology by affecting mRNA stability in Arabidopsis. Plant Cell, 2018, 30: 968-985

[121]

Wen H-G, Zhao J-H, Zhang B-S, Gao F, Wu X-M, Yan Y-S, Zhang J, Guo H-S. Microbe-induced gene silencing boosts crop protection against soil-borne fungal pathogens. Nat Plants, 2023, 9: 1409-1418

[122]

Wu X, Liu M, Downie B, Liang C, Ji G, Li QQ, Hunt AG. Genome-wide landscape of polyadenylation in Arabidopsis provides evidence for extensive alternative polyadenylation. Proc Natl Acad Sci U S A, 2011, 108: 12533-12538

[123]

Wu Y, Xu W, Zhao G, Lei Z, Li K, Liu J, Huang S, Wang J, Zhong X, Yin X, Wang Y, Zhang H, He Y, Ye Z, Meng Y, Chang X, Lin H, Wang X, Gao Y, Chai J, Parker JE, Deng Y, Zhang Y, Gao M, He Z. A canonical protein complex controls immune homeostasis and multipathogen resistance. Science, 2024, 386: 1405-1412

[124]

Xia S, Han D, Mo Q, Lai J, Yang C. SUMOylation of BAK1 regulates its co-receptor function for specifically activating brassinosteroid response. Plant Commun, 2025, 6 101384

[125]

Xiang Y, Huang W, Tan L, Chen T, He Y, Irving PS, Weeks KM, Zhang QC, Dong X. Pervasive downstream RNA hairpins dynamically dictate start-codon selection. Nature, 2023, 621: 423-430

[126]

Xu G, Sui N, Tang Y, Xie K, Lai Y, Liu Y. One-step, zero-background ligation-independent cloning intron-containing hairpin RNA constructs for RNAi in plants. New Phytol, 2010, 187: 240-250

[127]

Xu G, Greene GH, Yoo H, Liu L, Marqués J, Motley J, Dong X. Global translational reprogramming is a fundamental layer of immune regulation in plants. Nature, 2017, 545: 487-490

[128]

Xu G, Yuan M, Ai C, Liu L, Zhuang E, Karapetyan S, Wang S, Dong X. uORF-mediated translation allows engineered plant disease resistance without fitness costs. Nature, 2017, 545: 491-494

[129]

Xu Z, Xu X, Wang Y, Liu L, Li Y, Yang Y, Liu L, Zou L, Chen G. A varied AvrXa23-like TALE enables the bacterial blight pathogen to avoid being trapped by Xa23 resistance gene in rice. J Adv Res, 2022, 42: 263-272

[130]

Xue C, Qiu F, Wang Y, Li B, Zhao KT, Chen K, Gao C. Tuning plant phenotypes by precise, graded downregulation of gene expression. Nat Biotechnol, 2023, 41: 1758-1764

[131]

Yang C, Wang E, Liu J. CERK1, more than a co-receptor in plant–microbe interactions. New Phytol, 2022, 234: 1606-1613

[132]

Yao D, Arguez MA, He P, Bent AF, Song J. Coordinated regulation of plant immunity by poly (ADP-ribosyl) ation and K63-linked ubiquitination. Mol Plant, 2021, 14: 2088-2103

[133]

Yi H, Richards EJ. A cluster of disease resistance genes in Arabidopsis is coordinately regulated by transcriptional activation and RNA silencing. Plant Cell, 2007, 19: 2929-2939

[134]

Yi G, Mamalis D, Ye M, Carrique L, Fairhead M, Li H, Duerr KL, Zhang P, Sauer DB, von Delft F, Davis BG, Gilbert RJC. Covalently constrained 'Di-Gembodies' enable parallel structure solutions by cryo-EM. Nat Chem Biol, 2025, 22: 69-72

[135]

Yu X, Li B, Jang GJ, Jiang S, Jiang D, Jang JC, Wu SH, Shan L, He P. Orchestration of processing body dynamics and mRNA decay in Arabidopsis immunity. Cell Rep, 2019, 28: 2194-2205.e6

[136]

Yu G, Xian L, Xue H, Yu W, Rufian JS, Sang Y, Morcillo RJL, Wang Y, Macho AP. A bacterial effector protein prevents MAPK-mediated phosphorylation of SGT1 to suppress plant immunity. PLoS Pathog, 2020, 16 e1008933

[137]

Yuan M, Ngou BPM, Ding P, Xin XF. PTI-ETI crosstalk: an integrative view of plant immunity. Curr Opin Plant Biol, 2021, 62 102030

[138]

Zavaliev R, Mohan R, Chen T, Dong X. Formation of NPR1 condensates promotes cell survival during the plant immune response. Cell, 2020, 182: 1093-1108.e18

[139]

Zhai J, Jeong DH, De Paoli E, Park S, Rosen BD, Li Y, González AJ, Yan Z, Kitto SL, Grusak MA, Jackson SA, Stacey G, Cook DR, Green PJ, Sherrier DJ, Meyers BC. MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. Genes Dev, 2011, 25: 2540-2553

[140]

Zhang XC, Gassmann W. Alternative splicing and mRNA levels of the disease resistance gene RPS4 are induced during defense responses. Plant Physiol, 2007, 145: 1577-1587

[141]

Zhang Y, Zeng L. Crosstalk between ubiquitination and other post-translational protein modifications in plant immunity. Plant Commun, 2020, 1 100041

[142]

Zhang H, Zhu JK. Epigenetic gene regulation in plants and its potential applications in crop improvement. Nat Rev Mol Cell Biol, 2025, 26: 51-67

[143]

Zhang J, Shao F, Li Y, Cui H, Chen L, Li H, Zou Y, Long C, Lan L, Chai J, Chen S, Tang X, Zhou J-M. A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host Microbe, 2007, 1: 175-185

[144]

Zhang X, Liu Y, Yuan G, Wang S, Wang D, Zhu T, Wu X, Ma M, Guo L, Guo H, Bhadauria V, Liu J, Peng YL. The synthetic NLR RGA5(HMA5) requires multiple interfaces within and outside the integrated domain for effector recognition. Nat Commun, 2024, 15 1104

[145]

Zhang C, Wu Y, Liu J, Song B, Yu Z, Li JF, Yang C, Lai J. SUMOylation controls peptide processing to generate damage-associated molecular patterns in Arabidopsis. Dev Cell, 2025, 60: 696-705.e4

[146]

Zhang S, Liu S, Lai HF, Bender KW, Kim G, Caflisch A, Zipfel C. Reverse engineering of the pattern recognition receptor FLS2 reveals key design principles of broader recognition spectra against evading flg22 epitopes. Nat Plants, 2025, 11: 1642-1657

[147]

Zhang S, Wang L, Jiang H, Sun G, Xia Y, Wu J, Chen X, Wang L, Liu T, Ouyang H, Chen X, Wang Y, Wang Y. A conserved Phytophthora apoplastic trypsin-like serine protease targets the receptor-like kinase BAK1 to dampen plant immunity. Nat Plants, 2025, 11: 1401-1415

[148]

Zhang X, Luo Z, Marand AP, Yan H, Jang H, Bang S, Mendieta JP, Minow MAA, Schmitz RJ. A spatially resolved multi-omic single-cell atlas of soybean development. Cell, 2025, 188: 550-567.e19

[149]

Zhang F, Zheng J, Xie X, Tang M, Li H, Zuo L, Zheng L, Liu H, Huang J, Mei Z, Chen XL (2026) Endophyte-engineered plant immunity: A post-GMO strategy for programmable crop defense. Mol Plant. https://doi.org/10.1016/j.molp.2026.01.015

[150]

Zhao H-Y, Yang X-Y, Lei H, Xi X-X, Lu S-M, Zhang J-J, Xin M, Zhang S-Q. Discovery of potent small molecule PROTACs targeting mutant EGFR. Eur J Med Chem, 2020, 208 112781

[151]

Zheng Z, Appiano M, Pavan S, Bracuto V, Ricciardi L, Visser RG, Wolters AM, Bai Y. Genome-wide study of the tomato SlMLO gene family and its functional characterization in response to the powdery mildew fungus Oidium neolycopersici. Front Plant Sci, 2016, 7 380

[152]

Zhong S, Li H, Bodi Z, Button J, Vespa L, Herzog M, Fray RG. MTA is an Arabidopsis messenger RNA adenosine methylase and interacts with a homolog of a sex-specific splicing factor. Plant Cell, 2008, 20: 1278-1288

[153]

Zhong C, Li W, Zhang X, Zhang D, Wen Z, Song W, Jiang Z, Gao Z, Guo H, Bi G, Liu Z, Li D, Dinesh-Kumar SP, Zhang Y. A cell wall-associated kinase phosphorylates NLR immune receptor to negatively regulate resistosome formation. Nat Plants, 2025, 11: 561-579

[154]

Zhou JM, Zhang Y. Plant immunity: danger perception and signaling. Cell, 2020, 181(5): 978-989

[155]

Zhou Y, Niu R, Tang Z, Mou R, Wang Z, Zhu S, Yang H, Ding P, Xu G. Plant HEM1 specifies a condensation domain to control immune gene translation. Nat Plants, 2023, 9: 289-301

[156]

Zhu H, Qin X, Wei L, Jiang D, Zhang Q, Wang W, Liang R, Zhang R, Zhang K, Liu G, Zhao KT, Chen K, Qiu JL, Gao C. Engineered geminivirus replicons enable rapid in planta directed evolution. Science, 2025, 390 eady2167

[157]

Zhu W, Cao S, Huang M, Li P, Ke J, Xu A, Lin Y, Xie J, Cheng J, Fu Y, Jiang D, Yu X, Li B. Differential phosphorylation of receptor kinase SlLYK4 mediates immune responses to bacterial and fungal pathogens in tomato. Sci Adv, 2025, 11 eadu2840

[158]

Zlotorynski E. Mechanism of pathogen-induced cap-independent translation in plants. Nat Rev Mol Cell Biol, 2022, 23: 641

Funding

National Natural Science Foundation of China(32525050)

National Key R&D Program of China(2022YFA1304402)

Key R&D Program of Hubei Province(2023BBB171)

Fundamental Research Funds for the Central Universities(AML2023A05)

Gates Foundation(INV-004428)

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