BUI1 coordinates actin cytoskeleton remodeling and ROS homeostasis to confer broad-spectrum disease resistance in rice

Abstract

The cytoskeleton functions as a dynamic intracellular structural scaffold, enabling cells to rapidly respond to biotic and abiotic stresses. During plant innate immunity, the cytoskeleton undergoes significant actin remodeling. Using the rice-Magnaporthe oryzae pathosystem, we demonstrate that pattern-triggered immunity (PTI) induces a rapid and transient actin filament reorganization dependent on the Class II formin protein BENT UPPERMOST INTERNODE1 (BUI1). Disruption of actin filaments using latrunculin B significantly enhances host susceptibility to the blast fungus M. oryzae. Importantly, the bui1 mutant exhibits compromised resistance not only to blast but also to the bacterial blight pathogen Xanthomonas oryzae pv. oryzae and the sheath blight fungus Rhizoctonia solani. We identify that this enhanced susceptibility to multiple pathogens stems from increased ROS scavenging activity in bui1, mediated by upregulation of peroxidase-encoding genes and consequent reduction in H₂O₂ accumulation. Furthermore, genetic analyses reveal that BUI1 acts downstream of the immunity suppressor RESISTANCE OF RICE TO DISEASES1 (ROD1), as the bui1 mutation compromises rod1-mediated broad-spectrum resistance. Our findings establish BUI1 as a key regulator linking cytoskeletal reorganization to receptor-mediated immune signaling and ROS homeostasis during plant-pathogen interactions, providing new insights into the integration of actin dynamics with plant defense mechanisms.

Keywords

BUI1 / Actin cytoskeleton / Susceptibility / ROS / rod1

References

[1] Badet T, Léger O, Barascud M, Voisin D, Sadon P, Vincent R, Le Ru A, Balagué C, Roby D, Raffaele S. Expression polymorphism at the ARPC4 locus links the actin cytoskeleton with quantitative disease resistance to Sclerotinia sclerotiorum in Arabidopsis thaliana. New Phytol, 2019, 222: 480-496

[2] Basu D, Le J, Zakharova T, Mallery EL, Szymanski DB. A SPIKE1 signaling complex controls actin-dependent cell morphogenesis through the heteromeric WAVE and ARP2/3 complexes. Proc Natl Acad Sci U S A, 2008, 105: 4044-4049

[3] Bhandari DD, Brandizzi F. Plant endomembranes and cytoskeleton: moving targets in immunity. Curr Opin Plant Biol, 2020, 58: 8-16

[4] Brieger K, Schiavone S, Miller FJJr, Krause KH. Reactive oxygen species: from health to disease. Swiss Med Wkly, 2012, 142 w13659

[5] Cao Y, Liang Y, Tanaka K, Nguyen CT, Jedrzejczak RP, Joachimiak A, Stacey G. The kinase LYK5 is a major chitin receptor in Arabidopsis and forms a chitin-induced complex with related kinase CERK1. Elife, 2014, 3 e03766

[6] de Jong JC, McCormack BJ, Smirnoff N, Talbot NJ. Glycerol generates turgor in rice blast. Nature, 1997, 389: 244-244

[7] 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

[8] Dodds PN, Rathjen JP. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet, 2010, 11: 539-548

[9] Gao M, He Y, Yin X, Zhong X, Yan B, Wu Y, Chen J, Li X, Zhai K, Huang Y, Gong X, Chang H, Xie S, Liu J, Yue J, Xu J, Zhang G, Deng Y, Wang E, Tharreau D, Wang GL, Yang W, He Z. Ca²⁺ sensor-mediated ROS scavenging suppresses rice immunity and is exploited by a fungal effector. Cell, 2021, 184: 5391-5404.e17

[10] Gourlay CW, Ayscough KR. Identification of an upstream regulatory pathway controlling actin-mediated apoptosis in yeast. J Cell Sci, 2005, 118: 2119-2132

[11] Gourlay CW, Carpp LN, Timpson P, Winder SJ, Ayscough KR. A role for the actin cytoskeleton in cell death and aging in yeast. J Cell Biol, 2004, 164: 803-809

[12] Hardham AR, Jones DA, Takemoto D. Cytoskeleton and cell wall function in penetration resistance. Curr Opin Plant Biol, 2007, 10: 342-348

[13] Henty-Ridilla JL, Shimono M, Li J, Chang JH, Day B, Staiger CJ. The plant actin cytoskeleton responds to signals from microbe-associated molecular patterns. PLoS Pathog, 2013, 9 e1003290

[14] Henty-Ridilla JL, Li J, Day B, Staiger CJ. Actin depolymerizing factor4 regulates actin dynamics during innate immune signaling in Arabidopsis. Plant Cell, 2014, 26: 340-352

[15] Huang G, Liang W, Sturrock CJ, Pandey BK, Giri J, Mairhofer S, Wang D, Muller L, Tan H, York LM, Yang J, Song Y, Kim YJ, Qiao Y, Xu J, Kepinski S, Bennett MJ, Zhang D. Rice actin binding protein RMD controls crown root angle in response to external phosphate. Nat Commun, 2018, 9 2346

[16] Jelenska J, Kang Y, Greenberg JT. Plant pathogenic bacteria target the actin microfilament network involved in the trafficking of disease defense components. BioArchitecture, 2014, 4: 149-153

[17] Jones JD, Dangl JL. The plant immune system. Nature, 2006, 444: 323-329

[18] Kang Y, Jelenska J, Cecchini NM, Li Y, Lee MW, Kovar DR, Greenberg JT. HopW1 from Pseudomonas syringae disrupts the actin cytoskeleton to promote virulence in Arabidopsis. PLoS Pathog, 2014, 10 e1004232

[19] Kobayashi Y, Kobayashi I. Depolymerization of the actin cytoskeleton induces defense responses in tobacco plants. J Gen Plant Pathol, 2007, 73: 360-364

[20] Leontovyčová H, Kalachova T, Trdá L, Pospíchalová R, Lamparová L, Dobrev PI, Malínská K, Burketová L, Valentová O, Janda M. Actin depolymerization is able to increase plant resistance against pathogens via activation of salicylic acid signalling pathway. Sci Rep, 2019, 9 10397

[21] Li J, Staiger CJ. Understanding cytoskeletal dynamics during the plant immune response. Annu Rev Phytopathol, 2018, 56: 513-533

[22] Li G, Liang W, Zhang X, Ren H, Hu J, Bennett MJ, Zhang D. Rice actin-binding protein RMD is a key link in the auxin-actin regulatory loop that controls cell growth. Proc Natl Acad Sci U S A, 2014, 111: 10377-10382

[23] Li J, Henty-Ridilla JL, Staiger BH, Day B, Staiger CJ. Capping protein integrates multiple MAMP signalling pathways to modulate actin dynamics during plant innate immunity. Nat Commun, 2015, 6 7206

[24] Lin H, Wang M, Chen Y, Nomura K, Hui S, Gui J, Zhang X, Wu Y, Liu J, Li Q, Deng Y, Li L, Yuan M, Wang S, He SY, He Z. An MKP-MAPK protein phosphorylation cascade controls vascular immunity in plants. Sci Adv, 2022, 8 eabg8723

[25] Lu Y, Zhang Y, Lian N, Li X. Membrane dynamics regulated by cytoskeleton in plant immunity. Int J Mol Sci, 2023, 24 6059

[26] Ma X, Zhang Q, Zhu Q, Liu W, Chen Y, Qiu R, Wang B, Yang Z, Li H, Lin Y, Xie Y, Shen R, Chen S, Wang Z, Chen Y, Guo J, Chen L, Zhao X, Dong Z, Liu YG. A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Mol Plant, 2015, 8: 1274-1284

[27] Morton WM, Ayscough KR, McLaughlin PJ. Latrunculin alters the actin-monomer subunit interface to prevent polymerization. Nat Cell Biol, 2000, 2: 376-378

[28] Nakao LS, Olson MF, Vázquez-Medina JP, Valdivia A. Editorial: reactive oxygen species (ROS) signaling during cytoskeleton dynamics. Front Cell Dev Biol, 2023, 11 1295263

[29] Niño-Liu DO, Ronald PC, Bogdanove AJ. Xanthomonas oryzae pathovars: model pathogens of a model crop. Mol Plant Pathol, 2006, 7: 303-324

[30] Senapati M, Tiwari A, Sharma N, Chandra P, Bashyal BM, Ellur RK, Bhowmick PK, Bollinedi H, Vinod KK, Singh AK, Krishnan SG. Rhizoctonia solani Kühn pathophysiology: status and prospects of sheath blight disease management in rice. Front Plant Sci, 2022, 13 881116

[31] Shimono M, Lu YJ, Porter K, Kvitko BH, Henty-Ridilla J, Creason A, He SY, Chang JH, Staiger CJ, Day B. The Pseudomonas syringae type III effector HopG1 induces actin remodeling to promote symptom development and susceptibility during infection. Plant Physiol, 2016, 171: 2239-2255

[32] Sinha J, Singh Y, Verma PK. Cytoskeleton remodeling: a central player in plant-fungus interactions. J Exp Bot, 2024, 75: 3269-3286

[33] Sun H, Qiao Z, Chua KP, Tursic A, Liu X, Gao YG, Mu Y, Hou X, Miao Y. Profilin negatively regulates formin-mediated actin assembly to modulate PAMP-triggered plant immunity. Curr Biol, 2018, 28: 1882-1895

[34] Sun G, Qi X, Wilson RA. A feed-forward subnetwork emerging from integrated TOR- and cAMP/PKA-signaling architecture reinforces Magnaporthe oryzae appressorium morphogenesis. Mol Plant Microbe Interact, 2019, 32: 593-607

[35] Sun G, Feng C, Guo J, Zhang A, Xu Y, Wang Y, Day B, Ma Q. The tomato Arp2/3 complex is required for resistance to the powdery mildew fungus Oidium neolycopersici. Plant Cell Environ, 2019, 42: 2664-2680

[36] Takemoto D, Hardham AR. The cytoskeleton as a regulator and target of biotic interactions in plants. Plant Physiol, 2004, 136: 3864-3876

[37] Tang D, Wang G, Zhou JM. Receptor kinases in plant-pathogen interactions: more than pattern recognition. Plant Cell, 2017, 29: 618-637

[38] Wu B, Qi F, Liang Y. Fuels for ROS signaling in plant immunity. Trends Plant Sci, 2023, 28: 1124-1131

[39] Yang W, Ren S, Zhang X, Gao M, Ye S, Qi Y, Zheng Y, Wang J, Zeng L, Li Q, Huang S, He Z. Bent uppermost INTERNODE1 encodes the class II formin FH5 crucial for actin organization and rice development. Plant Cell, 2011, 23: 661-680

[40] Yun BW, Atkinson HA, Gaborit C, Greenland A, Read ND, Pallas JA, Loake GJ. Loss of actin cytoskeletal function and EDS1 activity, in combination, severely compromises non-host resistance in Arabidopsis against wheat powdery mildew. Plant J, 2003, 34: 768-777

[41] Zhang Z, Zhang Y, Tan H, Wang Y, Li G, Liang W, Yuan Z, Hu J, Ren H, Zhang D. Rice morphology determinant encodes the type II formin FH5 and regulates rice morphogenesis. Plant Cell, 2011, 23: 681-700

[42] Zhang N, Luo J, Rossman AY, Aoki T, Chuma I, Crous PW, Dean R, de Vries RP, Donofrio N, Hyde KD, Lebrun MH, Talbot NJ, Tharreau D, Tosa Y, Valent B, Wang Z, Xu JR. Generic names in Magnaporthales. IMA Fungus, 2016, 7: 155-159

[43] Zhang J, Liu Z, Sakamoto S, Mitsuda N, Ren A, Persson S, Zhang D. Ethylene response factor 34 promotes secondary cell wall thickening and strength of rice peduncles. Plant Physiol, 2022, 190: 1806-1820

Funding

National Key Research and Development Program of China(2023YFC2604500)

RIGHTS & PERMISSIONS

The Author(s)